Fertilizer Use and Plant Health
Fertilizer Use
and Plant Health
Pro'ceedings of the 12th Colloquium of the International Potash Institute held in
Izmir/Turkey 1976
Publisher: International Potash Institute, CH-3048 Worblaufen-Bern/Switzerland
Phone 031/58 53 73 Telex 33 430
Printed by 'Der Bund' AG, Bern/Switzerland
Contents
Opening and Welcome
Page
P. Chaudet
Opening and Welcome
11
Korkut Ozal
Welcome address
14
Necati Akgiin
Welcome address
16
Yamik Tani
Agriculture in Turkey
17-
K.Mengel
Frame and aim of the Colloquium
25
Session 1
Fertilizer Use and Plant Health:
Physiological aspects
Z.Kiraly
Plant disease resistance as influenced by
biochemical effects of nutrients in fertilizers
33
Rice diseases and physiological disorders
related to potassium deficiency
47
The effect of potassium on catabolism of rot
infected apple fruit callus
61
The effect of nitrogen fertilizers on growth
of cereals and the impact on diseases
69
M./smunadji
F.A.Schulz
M.M.EI-Fouly
A.Aydeniz, F.Hatipoglu
and M.Aktas
The effect of 'N-serve' on the health of
barley, maize and vetch
77
G. Trolldenier and E.Zehler
Relationships between plant nutrition and
rice diseases
K.Mengel
85
Report of the Co-ordinator of the 1st Ses95
sion
5
Session 2
Fertilizer Use and Plant Health: Fungi
Y.Henis
Effect of mineral nutrients on soil-borne
pathogens and host resistance
101
J.M.Lemaire and B.Jouan
Fertilizers and root diseases of cereals
J.F.Jenkyn
Nitrogen and leaf diseases of spring barley 119
K. Temiz
Interaction of fertilizers with Septoria leaf
129
blotch of wheat
K. Van Nerum and G.Scheys
The nutrient status of the soil and the appearance of symptoms of microbial disease 133
u. Kafka/i, M. L. Giskin
and H.Yogev
Effects of nitrogen source and irrigation
frequency on the susceptibility of potato to
late blight (Phytophthora infestans)
141
W.Kriiger
The influence of fertilizers on fungal diseases
of maize
145
M. Ollagnier and J.-L. Renard
The influence of potassium on the resistance
of oil palms to Fusarium
157
L.Dimitri
Influence of nutrition and fertilizer use on
the resistance of forest plants to fungus
167
diseases
I. Kovanci and C. Colakoglu
The effect of varying K level on yield components and susceptibility of young wheat
plants to attack by Puccinia striijormis West. 177
G. W.Cooke
Contribution to the discussion on the effects
of fertilizers on the infection -of the roots of
crops by fungi
183
P. Martin-Prevel
Contribution to the discussion on fungi
H. Laudelout
Report of the Co-ordinator of the 2nd Session
189
Session 3
Fertilizer Use and Plant Health:
Bacteria and Virus
C.Martin
Nutrition and virus diseases of plants
A.Schepers and A.B.R.Beemster
Effect of fertilizers on the susceptibility to
virus infection of the potato, with special
201
reference to mature-plant resistance
6
113
187
193
M.Babovic and Dj. B.Jelenic
Influence of soil fertility on virus disease in
lucerne
211
C. L. Parkas
Can the protoplasm system be applied in
studies on the role of mineral nutrients in
plant diseases?
217
P. Crossmann
Outlines of host-parasite interactions in
bacterial diseases in relation to plant nutri. tion
221
J.Ponchet
Etiology and physiology of bacterial diseases 225
C.Drouineau
Report of the Co-ordinator of the 3rd Session
229
Session 4
Fertilizer Use and Plant Health: Pests
P.C. W.Jones
Pests, resistance and fertilizers.
P. Chaboussou
Cultural factors and the resistance of citrus
plants to scale insects and mites
259
H. Bogenschutz and E. Konig
Relationships between fertilization and tree
resistance to forest insect pests
281
M.P.Ritter
The interaction between nutrients and host
resistance to nema:todes with reference to
mediterranean crops
291
B.A.Oteifa and A. Y.Elgindi
Potassium nutrition of cotton, Cossypium
barbadense, in relation to nematode infection
by Meloidogyne incognita and Rotylenchulus
reniformis
301
L.Brader
Fertilizers in regard to plant resistance to
pests; their role in FAO's Integrated Pest
Control Programme
307
S. Perrenoud
Contribution to the discussion: The effect
of K on insect and mite development
317
H.Baule
Contributions to the discussion on fertilizer
interaction with pests and diseases in forest
trees
318
P. Martin-Privel
Contribution to the discussion on nematodes and insects
324
J.Baier
Contribution to the discussion: The effect
of fertilizers on the health of farm crops in
Czechoslovakia - some research results
326
D. Schr'oeder
Report of the Co-ordinator of the 4th Session
327
P.Chaudet
Closing address
233
329
7
Chairman of the Colloquium
Prof. Dr. V. Tay!ji, Head, Department of Agroecology and Plant Breeding, Faculty of Agriculture, Aegean University, Izmir/Turkey
Opening and Welcome
P. Chaudet, Former President of the Swiss Confederation, President of the International Potash
Institute, Rivaz/Switzerland
Your Excellency, Ladies and Gentlemen,
It is an honour, and a great pleasure, for me in performing my duty of opening this
Colloquium in Izmir to welcome among us the Minister of Agriculture of Turkey,
the Governor of Izmir, the Rector of the Aegean University. of Izmir-Bornova, the
Mayor of Izmir, the Director of Agricultural Research in Turkey, the Dean of the
Faculty of Agriculture, the Dean of the Faculty of Natural Science, Professor Taysi,
President of the Twelfth Colloquium of the International Potash Institute, Members
of the Scientific Board and, finally, all the participants in this meeting.
The presence of so many eminent personalities, and especially that of the Minister of
Agriculture, testifies to the friendship we have been shown in the country chosen for
our deliberations and the interest shown by the political, administrative and scientific
authorities of Turkey must ensure success for an undertaking upon which much of
our future activity depends.
The general theme which has been chosen for the Izmir Colloquium is 'Fertilizer Use
and Plant Health'. The principal problem which we shall discuss is one which concerns
us all deeply: 'How can the resistance of cultivated crops to pests and disease be .
improved by means of appropriate fertilization?'
The choice of this theme ~as not dictated by the current v~gue for the natural life
and 'natural' nutrition, but simply because the Scientific Board of LP. I. considered
that it was important, as much from the scientific as from the practical point of view.
The high losses which limit crop production through the ravages of pest and disease
and the high cost of plant protection chemicals compel us to examine any measures·
which· may improve the resistance of plants to disease.
Once again the International Potash Institute has resolved to deal with a theme for
the future; one which has not up to now attracted all the attention that it deserves. It
has not been at all easy to complete the scientific programme for this colloquium; we
encountered several difficulties during the course of preparation. We may mention
the following:
- There has up to the present been little cooperation between the disciplines concerned,
plant nutrition and plant pathology.
11
- Many of the available results have not yet been collected together and sufficiently
digested to assess their significance.
- Finally, generally speaking, while better nutrition normally enhances the plant's
resistance, cases of negative effects have been reported. There are further involved
differences in the action of the three major nutrients.
Study of these problems is made the more difficult by the extreme complexity of the
processes involved, by the large number of external factors which come into play and,
not least, by the multitude of diseases and pests and their behaviour. It is hardly
surprising that the complex interactions involved frequently result in contradictory
findings in the matter of the effects of fertilizers. This complexity makes difficult the
planning of really adequate experiments.
It is thus hardly surprising that we have met with greater than usual difficulty in making
contact with authoritative speakers. We are more than usually grateful to those
workers who have come forward to present and discuss the results of their labours in
this field.
The International Potash Institute has put forward the theme of this colloquium in
the hope that we shall be successful in exchanging views on experimental work done
up to now on the influence of fertilizers on plant health. But it remains an important
aim which we should aim to achieve - and I address particularly all the specialists
present here - to suggest ways in which research may be intensified and how cooperation between the two fields of plant nutrition and plant pathology may be improved.
Perhaps we may be able to discuss at the end of our deliberations means by which the
exchange of information can be improved.
The importance of mineral fertilizers in crop production is not nowadays in dispute.
Once more, among otp.er things, one of the main aims of our meeting is to highlight
the most efficient means of using fertilizers to improve the productivity and quality of
our agricultural crops.
The President and the Scientific Board of the International Potash Institute express
the hope that study of the topic 'Fertilier Use and Plant Health' will be regarded as
an important contribution by all who are interested in bringing new ideas into
scientific research and in improving the exchange of results and opinions between
specialists in different countries.
I cannot end this introduction to our work without acknowledging how much we all
appreciate the opportunity to discuss a problem of such importance in a country which
has made such efforts in developing its agriculture. Turkish agriculture is still characterised in some areas by semi nomadic life in mountainous regions and a pastoral
summer life on the slopes of the valleys and hills of the plateau. On the plateau, as we
know, increase in cereal production was first achieved by expanding the cultivated
area. The development of sugar beet cultivation in rotation with wheat and with the
use of fertilizers has resulted in a cultural system more stable than the monoculture of
cereals and this holds great promise for the future. Turkey is also well known for tree
crops, traditional in the Mediterranean - olives, figs and, naturally, vines.
These brief remarks illustrate the diversity of Turkish agriculture and the diversity of
the problems with which it is faced. We find ourselves in a country in which there is
12
an active programme of agricultural research; the results of this will open up almost
unlimited prospects for the future. Our choice of venue could hardly be more propitious, from a technical point of view it has much to offer, but without doubt we shall
profit also from the scenic beauty with which we are surrounded which will contribute
to our enjoyment and raise our spirits. We have only one regret; that we are unable
to express ourselves in the language of our hosts. We ask your forgiveness well
knowing that this will be answered by your friendly understanding:
I declare the 12th Colloquium of the International Potash Institute open!
13
Welcome Address
Prof. Dr. Korkut {hal, Minister of Food, Agriculture and Animal Husbandry, Ankara/Turkey
Mr. Chairman, Distinguished Guests and Participants, Ladies and Gentlemen:
On behalf of the Turkish Government and on my own behalf I would like to welcome
the participants of the 12th Colloquium of the International Potash Institute.
This industrially orientated world of ours has again realised with bitter experience
the vital importance of agriculture for the future of humanity.
Ecological, pedological and physiological conditions which have for long controlled
the success of agriculture are now being gradually brought under control by man with
the aim of assuring optimum returns from agriculture. The ever-growing use of the
products of industry and of industrial methods has been indispensible for the success
of agriculture. We now talk of the industrialisation of agriculture.
The use of chemical fertilizers on an ever growing scale has itself had a revolutionary
impact on world agriculture. Human ingenuity is now directed towards discovering
new aspects of fertilizer use. Research workers all over the world are trying to understand the effects of fertilizer use on plant health and to describe these effects scientifically. I am sure that as our knowledge of the complexity of fertilizer effects grows new
possibilities for developing healthier and better crops will be opened up. I sometimes
think of the scientists of our contemporary world as the explorers and pioneers of the
future of our civilisation and developers of modern technology. But, I wish with all my
heart that scientists would be as practical, and as quick, as possible in producing
working solutions to our pressing problems. As a Turkish proverb goes: 'The
scientist can split a thin hair into forty pieces but cannot show the way to the village'.
Therefore, as a scientist converted to politics, I say:
Our world would be quite different if scientists were as practical and pragmatic as
politicians and politicians as broad-minded and cooperative as scientists.
Colloquia such as this serve various purposes of benefit and service. A common pool
is created in which scientific and technological exchanges can take place. They provide
ample opportunity to establish and maintain personal acquaintances. They are valuable
reunions of research families.
Before closing I would like to give some highlights of Turkish Agriculture. Turkey
adopted an agricultural policy to provide subsidies in supplying farmers with agricultural inputs. Last year the average subsidy in fertilizer amounted to 30%. As a
14
result, our consumption of fertilizer in the last 13 years has gone up from 425 000 tons
in 1963 to 4.5 million tons in 1976 despite the crisis of 1973-1974. During the spring of
1976 the consumption ofN was 80% more than during 1975. We believe that by 1980
our fertilizer consumption will reach 9 million tons and will be met basically by
indigenous production.
I have studied the preprints of the papers to be presented. I would like to congratulate
the authors on their fine work. I am sure that discussions during the sessions will
augment their value.
I believe that this Colloquium will, through the valuable contributions of its participants, render great help in our efforts to make in this world a prosperous and happy
livelihood for all of its inhabitants.
I welcome you all to Izmir, a city of historical significance and natural beauties. Here
I am sure you will all be most welcome and I hope you will feel more than at home here.
Finally, I would like to congratulate the Organizers of the Colloquium for their fine
work.
Thank you, Mr. Chairman.
15
Welcome Address
Prof. Dr. Necali Akgiin, Rector of the Ege-University, Bornova-Izmir/Turkey
Ladies and Gentlemen,
It is a great pleasure and honour for me to welcome you on behalf of the Ege University.
As a physician I am convinced of the importance of taking care of human health. Now,
I have also learned to evaluate the importance of taking care of plant health.
This Fertilizer Use and Plant Health Colloquium will be a good occasion, I am sure,
not only to discuss the matter deeply, but also to stimulate interdisciplinary cooperation
on an international level.
Our City of Izmir is proud not only of being clean, quiet and beautiful but also of
having friendly and hospitable people.
I hope that the participants will enjoy their stay in our country and I wish the best for
a successful Colloquium.
16
Agriculture in Turkey
Prof. Dr. Vamik Tay{i, Director, Department of Agroecology and Plant Breeding, Ege University,
Bornova, Izmir/Turkey; Chairman of the 12th IPI-Colloquium
The potential yield of crops is in general reduced, not only by adverse climaticfactors
but also by pests and disease. It is estimated that in Turkey, these losses amount to
one third of the possible yield on the average. This means that our country loses every
year two to three million tonnes wheat (a year's requirement for more than ten million
people), 1.5 to 2 million tonnes sugar beet, several hundred thousand tonnes of cotton
and sunflower seed and millions of tonnes of miscellaneous food crops.
Stephen Wilhelm [I}, discussing biological balance in natural soils, pointed out that
2400 years ago the great Heraclitus of Ephesus, the 'weeping philosopher', in his
famous dictum 'All things flow', taught us that Nature is ever changing. This fluidity
is characteristic of all ecological conditions. Thus we can only tallc of stages in ecological
development, not of fixed states. We cannot say that biological balance is a permanent
state. In nature, the growth of the plant is controlled by dynamic ecological factors. We
strive, through' husbandry measures, such as cultivation technique, manuring and
irrigation, to influence ecological development in order to achieve our aims. We cim
also make such methods serve us in reducing the ravages of disease. From, ancient
times, proper nutrition has been regarded as a sound basis for health. Thus, manures '
and fertilisers not only have direct effects in improving the energetic efficiency of
crops by improving their use of solar energy but also have beneficial effects on the
vegetation by improving its resistance to disease.
Biological problems are not easily soluble in a country like Turkey. Ecological conditions vary greatly from one area to another and it is difficult to find over-all.solutions
to many problems. The direct application of hypothetical ideas, or experience gained
in other countries, has, in many cases, been unsuccessful. All advice must take account
of local conditions.
Turkey consists of two peninsulas, the European Eastern Thrace and the Asiatic
Anatolia. These peninsulas and the many islands have a coastline amounting to
4450 miles. The total land surface, excluding lakes is 780576 km2 , 23 623 in Europe,
the remainder in Asia Minor. The land surface of Turkey is very much folded with a
steep mountain chain in the North on the Black Sea, the Taurus mountains on the
Mediterranean coast, the east Anatolian plateau etc. Thus, climate and ecology are
extremely variable. About 80% of the country lies above 500 m a.s.!. and the area of
land with a slope of 0-1 % is only about 12% of the total.
17
The climate is as variable as the physical geography. Crudely speaking, Turkey has a
Mediterranean climate, but with a monsoonal tendency. Summer rainfall is very low
on account of the feeble cyclonic activity of the air masses and this tendency is
strengthened through the development of a high pressure area in the Mediterranean.
In constrast, in the winter, the tropical and continental air masses cause instability
with heavy rainfall. Within the general climatic conditions, great orographic variability
causes extreme variation in local climate giving both particularly favourable and
particularly unfavourable conditions for agriculture. Practically all climatic conditions
from the subtropical, or even semi tropical, to the continental-boreal can be found
within the country. Table 1 illustrates this extreme variability.
Table 1.
Extremes of climate in Turkey, 1931-1970
Place
Years of
observation
Iskenderum (3 m a.s.l.)
Kars (1775 m a.s.l.)
.
.
Mean annual temperature QC
20.2
4.2
31
35
Ceylanpinar (398 m a.s.l.)
.
Maximal temperature QC
47.6
14
Lowest temperature QC
-43.2
Karakoese (1638 m a.s.l.)
.
Adana (20 m a.s.l.)
Kars (1775 m a.s.l.)
.
.
Sunny days
195.9
46.5
42
38
Kars (1775 m a.s.l.)
Anamur (3 m a.s.l.)
.
.
Days frost
180.9
0.4
38
23
Kars (1775 m a.s.l.)
Antakya (100 m a.s.l.)
.
.
108.6
38
31
Rize (4 m a.s.l.)
Anamur (3 m a.s.l.)
.
.
Overcast days
153.2
39.9
40
23
Rize (4 m a.s.l.)
Igdir (858 m a.s.l.)
.
.
Mean annual rainfall: mm
2357.0 (4045 in 1935)
251.6 ( 169 in 1949)
40
22
24
Q
Days with temperature 2: 20 C
o
Source: Meteorological Bulletins - Ministry of Agriculture.
The great mountain chains and their orientation, the sea inlets etc. shape the general
climate of the country but they determine agricultural conditions in general outline
only. A thorough classification into agricultural regions is not easily carried out as
sufficiently detailed climatic and agro-eco)ogical data are lacking. Attempts have
18
been made by several Turkish authors using different systems. Classification has been
attempted not only on climatic and agricultural grounds but also on social or cultural
bases. Classification on the climatic basis can only be rather elementary.
Agricultural development in Turkey depends mainly on demographic problems. Total
population according to the census of 1975 was 40063000: in 1927 the figure was
estimated at 13.6 million so that, in the space of 48 years, the population has tripled.
From 1927 to 1950 the annual increase in population was 300000 but this has now
increased to 1 million per annum. The present rate of population increase is about
2.6%. Ayerage population density in 1975 was 51 per km2 (Table 2). The eastern and
Table 2. Population growth in Turkey
Year
Population
(millions)
Period
Annual increase
'000
1927
1940
1950
1960
1965
1970
1975
13.65
17.82
20.95
27.78
31.39
35.60
40.06
1923-1927
1927-1940
1940-1950
1950-1960
1960-1965
1965-1970
1970-1975
300
321
313
683
722
842
892
Mean growth rate for 1973-1975: 2.6%/annum.
western parts of the Black Sea coast with the E. Marmara region, the Aegean and
Hatay provinces are more thickly populated, while the mountainous area of E. Anatolia, which is difficult of access is very sparsely inhabited. The Western and Southern
parts of the Central Plateau carry from 30-35 people per square kilometre. These
remarks however do not give a complete picture of agricultural demography. In 1955,71.5% of the total population lived in villages and small country towns but the picture
has changed somewhat in recent years. Today about 60% live in towns and villages
with less than 10 000 inhabitants. In spite of the relative decrease in the rural popula-
Table 3. Area, population and population density by regions
Region
N. and Central Anatolia
Aegean region
Marmara
Mediterranean
N.E. Anatolia
S.E. Anatolia
Black Sea
E. Central Anatolia
S. Central Anato1ia
.
.
.
.
.
.
.
.
.
Area of land
km 2
PopUlation '000
1960
1965
1970
118906
98845
44242
81069
74338
109319
68945
80818
98328
4008
4344
4027
2888
1767
2096
3783
2411
2431
4543
4826
4637
3356
1950
2444
4226
2683
2726
5150
5299
5587
3930
2137
2918
4596
2929
3059
Inhabitants
per km2
43
54
126
48
29
27
66
36
31
Source: Landerkurzberichte (Turkey), Statistics Office, Wiesbaden.
19
Table 4. Population in cities and country districts ('000)
Cities. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Country Districts
1960
1965
1970
7 200
20 555
9343
22048
12735
22 870
Source: Uinderkurzberichte (Turkey), Statistics Office, Wiesbaden.
tion through industrialisation and the flight from the land from 76.5% in 1935 to
71.5% in 1955 and about 64% in 1970, the absolute number is still rising (1935=
12.345 million, 1955= 17.26 million, 1970= 22.87 million (Tables 3 and 4).
Conditions in Turkey are better described in terms of the agricultural population per
unit area of utilisable agricultural land. At first sight, it may be surprising that figures
derived in this way differ so greatly from straightforward population density figures.
Arithmetical figures show that the eastern part of E. Anatolia is very thinly populated
but, on the basis of the area of utilisable agricultural land, population density there
is the highest (over 400 per km2 agricultural land). Everything naturally depends upon
the agricultural possibilities in the area (Table 5).
Table 5. Classification of Turkish agricultural holdings by size and area
Size of holding
1963
ha
Number
1970
Area
Number Area
'000
%
'000 ha
%
less than I , ...................
1- 3 ......................
3- 5 ......................
5- 10 · .....................
10- 20 · .....................
20- 50 · . . . . . . . . . . . . . . . . . . . . .
50-100 · ........... - .......
100-250 · .....................
250-500 · . . . . . . . . . . . . . . . . . . . . .
500 and over ..................
774
844
514
562
292
100
25.0
27.2
16.6
18.1
9.4
3.2
0.4
0.1
0.03
0.01
432
1614
2033
3995
3973
2842
755
370
314
406
2.6
9.6
12.1
23.9
23.7
17.0
4.5
2.2
1.9
2.4
Total .........................
3101
_,
11
3
1
0.5
100
16743
100
%
%
75.1
29.6
14.7
7.1
2.6
0.4
23.2
21.8
14.3
5.7
0.1
5.4
100
100
Source: Uinderkurzberichte (Turkey), Statistics Office, Wiesbaden.
The average Turkish farm is small in size; over 85% of farms are of 10 ha or less.
Improved production on such small enterprises can only be achieved through the
rational use of fertilisers. Up to 1950 fertiliser use remained very low, but relatively
rapid progress has been made since then (Table 6).
20
Of course, if we compare our fertiliser use with that in other countries at varying
levels of development it is seen to be relatively low (Table 7).
Table 6. Use of commercial fertilisers
tonnes N, PzOs and KzO
N
1951
.
1952
:.
1953
.
1954
.
'" .............•.......
1955
1956
'"
.
1957
.
1958
.
1959
.
1960
.
1961 ...............................•........
1962
.
1963
.
1964
.
1965
.
1966
.
1967
.
1968
.
1969
.
1970
.
1971
.
1972
.
1973
.
1974
.
4169
5656
9727
4426
11023
9213
10132
9711
24861
9681
29416
37881
39075
54893
73319
98319
142016
193067
245 168
243067
286764
374369
430252
382 773
3826
5727
5291
6876
14347
4401
5728
4103
9863
10185
13 095
17776
37074
45689
75340
92 857
144217
200 170
213 775
175850
194727
197758
279931
217 687
106
3358
2563
10280
647
6146
15
5238
10500
4500
5500
6000
7500
10500
12000
11500
13250
• 20 150
19700
16750
Table 7. Fertiliser usage in several countries (kg/ha)
N
W. Germany
England
France
,
.
.
.
~~rt:::::::'::::::::::::::::
Greece
Jugoslavia
Spain
Rumania
USSR
Turkey
Pakistan
Persia
.
.
.
.
.
.
.
.
139.9
128.7
·79.8
122.7
50.4
56.7
40.7
32.3
41.0
22.3
19.7
11.7
6.4
Total
115.7 _
70.8
101.1
16.7
46.3
34.1
21.4
22.6
17.1
10.5
12.9
1.8
4.0
152.6
68.7
78.7
0.7
20.2
5.0
19.8
12.7
2.1
12.1
1.4
0.1
408.2
268.2
259.6
140.1
116.9
95.8
81.9
67.6
60.2
44.9
34.0
13.6
10.4
)
(
Source: Annual Fertiliser Review 1972.
21
Statistics for fertiliser show great variability between the different regions according
to climate and agricultural possibilities (Table 8).
Table 8. Fertiliser use in various regions of Turkey, 1974
tonnes
N
Region
Aegean
Marmara
Mediterranean
Black Sea
N.E. Anatolia
,
S.E. Anatolia
N. Central Anatolia
E. Central Anatolia
S. Central Anatolia
'
.
.
.
.
.
.
.
.
.
75340
70971
104456
54395
3900
6485
29930
16468
20935
34754
39515
63358
8462
I 319
6958
32876
9755
21214
5255
5005
5496
385
175
238
172
Home fertiliser production covers only part of our needs (26% of nitrogen use and
54% of phosphate). Our fertiliser requirements will increase rapidly.
Improvements in irrigation and in fertiliser use are absolutely necessary if we are to
achieve the increased agricultural production which is needed in Turkey today. We
should strive to use technology and new biological methods to make agriculture as far
as possible less dependent on the environment and thereby raise yields, quality and
productivity. Only through careful scientific research and testing of measures under
local conditions can any realistic programme of improvement be realised. Methods
developed abroad must first be tested under and adapted to local conditions so that
local natural and social conditions receive full expression. The prob]ems which have
to be solved in the agricultural field alone are very numerous and complicated. Research
under our local conditions on many problems of fertiliser use, irrigation and agricultural ecology has hardly yet begun.
Aid programmes have been carried out with different aims by national and international agencies from many countries. At the same time, universities and other
teaching institutes have been individually concerned with agricultural problems, but
their efforts have seldom been sufficiently coordinated. All research aims will be the
more easily and rapidly achieved by harnessing the human spirit in cooperative effort.
Such a way of working will influence the development of spiritual and intellectual
qualities in the different countries of the world. Such an undertaking will make
possible the attainment of scientific developments and will be an insurance for the
future.
Bibliography
Wi/helm, St.: Analysis of biological balance in natural soil, Ecology of Soil-Borne Plant Pathogens
509-517 (An International Symposium 1963). University of California Press (1970).
Sadasivan, T. S.: Effect of mineral nutrients on soil microorganisms and plant disease. Ibid.
Aka/in, H. T.: Probleme der Neuordnung des Boden-, Wasser- und Forstrechtes in der Ttirkischen
Republik unter Berticksichtigung der landwirtschaftlichen Entwicklung. Freiburg, Breisgau
(1966).
22
Baade, F.: Agricultural problems of Turkey, Pakistan and India. In: Towards a strategy for development cooperation. Proceedings of a conference on Asian development, Rotterdam (1967).
Bodur, S.: Agrargeographische und wirtschaftliche Verhaltnisse der ttirkischen Landwirtschaft,
Giessen (1963).
Kolars, l.F.: Types of rural development. In: Four studies on the economic development of Turkey.
London (1967).
Toysi, V.: Die sozialen Auswirkungen der gegenwartigen ttirkischen Agrarpolitik, 'Von der Agrarzur Industriegesellschaft'. Beitrag XVIII, Verlag Hoppenstedt und Co., Darmstadt.
23
Introductory Paper:
Frame and Aim of the Colloquium
Prof. Dr. K.Mengel, Head, Institute of Plant Nutrition, Justus Liebig University, Giessen/Federal
Republic of Germany
Summary
Production losses due to the infestation of crop plant by pests and various microorganisms can
be considerable, and thus the problem merits attention.
The partially artificial environment of crop plant and the frequent growing the same crop in monoculture favour the attack of various pests and diseases:
.
The plant cell has to compete with very different organisms (animals, higher plants, microorganisms
and viruses), some of them of extreme smallness and of extreme harmfulness. Thus, plant protection
is very complex and heterogeneous.
Therefore the field of the 12th IPI-Colloquium had to be restricted to the dealing with the most
important diseases caused by bacteria, fungi and viruses and attacks caused by insects and nematodes.
As hardly data are available related to mycoplasm like organisms as well as rickettsialike bacteria,
which only recently were found as germs for various plant diseases, the author gives some information
about the most important features of these organisms and the damage caused by them.
Due to virulence and biological adaptability of vari.ous microorganisms the application of fungicides,
bactericides, insecticides or similar chemicals does not always yield a satisfactory success. Therefore,
it is important to look for other approaches which are helpful in limiting and alleviating the damage
caused by biotic diseases.
Breeding for resistance against biotic diseases.is an important measure in improving plant health.
But the author also emphasises, that the efficiency of breeding is limited due to the vitality and
adaptibility of pathogens.
Since also fertilizer use is involved in the question of plant health, the very topic of the Colloquium
.is the study of the relationships between plant nutrition and fertilizer use on one hand and the
resistance and susceptibility of crops on the other hand.
With the intensification of plant production associated with fertilizer use, new varieties and new
rotations the problem has become more severe. But the simple use of organic manure instead of
mineral fertilizer, propagated by the 'biologischer Landbau' is lacking a serious basis, as the
'biologischer Landbau' could not prevent the fungal attack and the yields were generally lower
than those of plots receiving mineral fertilizers.
As the relationships between the plant nutrition and the resistance and susceptibility are very
complex, the Colloquium is thought as a forum where agronomists, biochemists, plant pathologists
and plant physiologists present their research data, observations and experiences relevant to the
topic by explaining the ideas and data in words and terms so that a general understanding is guaranteed, in order to disclose and clarify causal relationships between plant nutrition and plant health.
The Colloquium is divided into four sessions which are devoted to fungi diseases, diseases caused
by bacteriae and viruses as well as pests. The Scientific Board of the International Potash Institute
believes that the key for a better understanding and interpreting of the vast range of experimental
data and observations available can be found on the level of molecular biology. A particular session
devoted to the discussion and the coordinators' reports should help to develop and establish general
lines and conclusions.
25
Resume
Les pertes de production dues a l'attaque des plantes cultivese par les ravageurs et divers microorganismes peuvent atteindre des proportions considerables. Le probleme merite done d'etre etudie
de plus pres.
Le milieu partiellement artificiel dans lequel se developpent les plantes cultivees ainsi que la succession frequente de la meme culture en monoculture favorisent l'attaque par les ravageurs et les
maladies.
La cellule vegetale se trouve en competition avec des organismes de nature tres differente (animaux,
plantes superieures, microorganismes et virus), quelques uns etant de taille tres reduite mais etant
d'un danger extreme. Ainsi done, le probleme de la protection des plantes est tres complexe et tres
heterogene.
Le l2e Colloque J.I.P. a done dfr etre limite aux maladies les plus importantes provoquees peu des
bacteries, des champignons et des virus ainsi qu'aux attaques par les nematodes et les insectes. Etant
donne que seulement tres peu de donnees relatives aux organismes du type mycoplasma ne sont
disponibles, comme par exemple sur les bacteries du genre rickettsia - qui, tres recemment seulement,
ont ete reconnues comme etant les germes de plusieurs maladies des vegetaux - l'auteur presente
quelques informations sur ces organismes et les degiits qu'ils peuvent provoquer.
En raison de la virulence et de la capacite d'adaptation de nombreux microorganismes, les traitements
aux fongicides, bactericides, insecticides ou d'autres produits chimiques ne donnent pas toujours les
resultats escomptes. II est done important d'elaborer d'autres mesures pour limiter et diminuer les
degilts dus aux maladies biotiques. L'une de ces mesures est constituee par la selection tenant compte
des facteurs de resistance envers les maladies biotiques. Mais I'auteur releve que l'efficacite des
mesures de selection est souvent limitee en raison de la vitalite et de la capacite d'adaptation des
pathogenes.
Puisqu'il est reconnu que la fertilisation joue un role dans I'etat de sante des plantes, le theme
principal de ce Colloque est I'etude des relations entre, d'une part, la nutrition des plantes et les
mesures de fertilisation, et, d'autre part, la resistance et la sensibilite des plantes cultivees.
Avec l'intensification de la production vegetale, associee al'emploi des engrais, aux varietes nouvelles
et aux nouveaux systemes d'assolement, le probleme est devenu plus important. Mais le seul
emploi d'engrais organiques propage par les adeptes de l'«agriculture biologique» n'est pas base sur
des principes serieux, puisque l'«agriculture biologique» n'est pas parvenue a eviter les attaques
fongiques et que les rendements sont generalement inferieurs a ceux obtenus avec des cultures ayant
re.;u des engrais mineraux.
Etant donne que les relations entre la nutrition des plantes, d'une part, et la resistance et la sensibilite
des plantes d'autre part, sont tres complexes, le 12e Colloquium J.I.P. a ete constitue en forum
permettant aux agronomes, aux biochimistes, ainsi qu'aux specialistes de la pathologie et de la
physiologie vegetales de presenter Jeurs donnees scientifiques, observations et experiences relatives
au sujet general et d 'expliquer leurs idees a ce sujet permettant ainsi de mieux degager et de clarifier
les relations causatives entre la nutrition et la sante des plantes.
Le Colloque est subdivise en quatre seances de travail consacrees aux maladies fongiques, aux maladies bacteriennes, aux maladies provoquees par les virus et aux ravageurs, respectivement. Le Conseil
Scientifique de l'Institut International de la Potasse est d'avis que la biologie moleculaire pourrait
fournir la clef a une meilleure comprehension et interpretation de la vaste gamme de donnees et
d'observations disponibles. Une seance speciale est consacree ala discussion et a la presentation des
rapports de MM. les coordinateurs des seances de travail, dans le but de developper et d'etablir des
conclusions generales.
Agronomists and experts of plant nutrition tend to stress the importance of growth
and crop production. The aspect, that the economic yield is a kind of a net production
resulting from the total production potential and production losses, is often overlooked
by them. Production losses due to the infestation of crop plants by pests and various
microorganisms can be considerable, and thus the problem merits attention.
Compared with a natural vegetation crop plants are living in a more artificial environment and thus are exposed to various competitors and attacks. In addition growing
the same crops or similar crops for years in monoculture results in conditions, which
favour the attack of various pests and diseases.
26
The organisms from which crop plants may suffer or with which crop plants have to
compete are of very different nature, as these may belong to animals, to higher plants,
to microorganisms including such extreme groups like mycoplasma-like organisms
and viruses. Even in such simple parameters as the cell volume the various organisms
show considerable differences as is indicated in Table 1. It illustrates that a plant cell
may be fill1ed with about some hundred or thousand bacteria cells and that a virus is
extremely tiny in comparison with an eucaryotic cell. Nevertheless these tiny particles
like viruses, which stand on the threshold between living and unliving nature may be
extremely harmful.
Due to this broad range of organisms potentially affecting plant growth, plant protection against these various organisms is very complex and heterogenous. All diseases
caused by animals, bacteria, fungi and viruses are of biotic nature. In the frame of
this colloquium abiotic diseases, such as mineral deficiencies, e. g. 'reclamation disease',
which is caused by a lack of eu, are not included. The preparation committee felt that
Table 1. Mean cell volume of various organisms
volume in [Lm 3
Eucaryotic cell
Blue-green algae
Bacteriae
Rickettsiae
Virion *)
.
.
.
.
.
5-15x 103
5-50
1-5
1-3 x 10- 2
1 x 10- 2-1
X
10- 5
*) A virion is no biological cell in the strict sense of the word. The virion consists of nucleic
acid and a protein coat.
only dealing with the most important diseases caused by bacteria, fungi and viruses
and attacks caused by animals in particular by insects and nematodes, would be a
field broad and heterogenous enough for this colloquium. Also mycoplasma and
mycoplasma-like organisms as well as rickettsia-like bacteria, which only recently
were found as germs for various plant diseases, will not be treated in detail during
this colloquium, as it is believed that hardly data are available which relate this kind
of diseases to plant nutrition. Doi et al. [1967] were the first who discovered that
mycoplasma-like organisms may also be harmful to higher plants. Mycoplasmae are
single cell organisms of pleomorphic shape. They lack a cell wall and for this reason
they are resistant against those antibiotica which attack the cell wall. They possess
DNS and ribosomes and thus have in contrast to viruses an own metabolism. The
vectors of the mycoplasma-like organisms are mainly phloem sucking insects e. g.
aphids. In the last years quite a number of diseases have been found which are caused
by mycoplasma-like organisms (Petzold and Marwitz [1973]).
Often the plants infected show characteristic deformations known as 'rice yellow
dwarf', 'corn stunt', 'little leaf disease of citrus' and 'witches broom'. Rickettsia-like
bacteria differ from the mycoplasma-like organisms as they possess a simple cell wall.
They can infect various crops (Hopkins and Mollenhauer [1973]). A review article
about mycoplasmae and rickettsiae and the disorders they cause in plants and insects
has been published by Davis and Whitcomb [1971].
Man has been confronted with crop diseases and pest attacks since he is growing
crops. Several measures and approaches are known to protect crops or to alleviate the
27
degree of damage caused. Nowadays a broad range of chemicals has been developed
with which the various diseases and attacks can be met. In many cases, however, the
application of fungicides, bactericides, insecticides or similar chemicals do not yield a
satisfactory success, due to the virulence and biological adaptability of various microorganisms. Thus it is important to search not only for new chemicals, but to look
also for other approaches which are helpful in limiting and alleviating the attacks and
biotic diseases.
It is a well known fact that the resistance of plants against diseases is to some extent
genetically fixed. Thus even considerable differences with regard to resistance against
diseases or attacks may exist between cultivars of the same species. A famous example
of this kind is the resistance of grape-rootstocks against the vine-louse (Phylloxera
vasfafrix) which in the last century was a deadly threat to European vine growing.
Due to the introduction of vine-louse resistant rootstocks this threat came under
control and the European vine growing was saved.
This example shows that plant breeding has a substantial impact on the resistance of
crop against pests and in particular against diseases, and breeding of resistant varieties
is one measure in the fight against pests and diseases. Thus in many breeding programs
resistance against diseases is a major issue. On the other hand breeding may also result
in an increased susceptibility against a particular disease. This e. g. was the case in
breeding high yielding rice varieties; some of which were extremely susceptible against
the 'tungro disease' which is a virus infection.
Breeding new varieties of crop plants is a wearisome process and often the adaptability
of microorganisms to new cultivars is faster. Therefore breeding for resistance is only
one measure beside others to meet the diseases and attacks. Another measure of also
limited impact is plant nutrition. Thus also fertilizer use is involved in the question of
plant health. The relationships between plant nutrition and fertilizer use on one hand
and the resistance and susceptibility of crops against biotic diseases and pests on the
other hand is the very topic of this colloquium.
There exists a tendency to blame mineral fertilizer application for an increased susceptibility of crops against diseases and attacks. This view, in Central Europe mainly
hold by people propagating the 'biologisch-dynamischer Landbau' (biological dynamic
husbandry) is too simple and not serious enough to treat the problem. There is no
doubt, that with the intensification of plant production associated with fertilizer use,
new varieties and new rotations the problem has become more severe, but there is also
no question that by the simple use of farm yard manure and other organic materials
instead of mineral fertilizers the problem can not be overcome. Table 2 shows yield
data of field experiments in which the technique of the 'biologisch-dynamischer
Landbau' was tested in comparison with conventional production techniques. In the
Table 2. Grain yields of winter wheat obtained with different production techniques (Abele [1973 J)
Production techniques
1969
1970
1971
1972
grain yield, tlha
Cereals + sugar beet rotation. . . . . . . . . . . . . . . . . .
Monoculture, straw + mineral fertilizer
Monoculture, straw + organic fertilizer (biological
dynamic husbandry)
28
5.03
4.62
4.99
3.59
5.17
3.64
5.14
4.52
3.56
3.95
3.18
4.63
latter mineral fertilizers were used, whereas the 'biologisch-dynamischer Landbau'
only applies organic materials, especially farm yard manure. It can be seen that in
each year highest grain yields were obtained where the wheat was grown in rotation
with sugar beets. In the monoculture treatments in average higher yields were harvested
on the plots with mineral fertilizer application compared with the plots which received
farm yard manure. Abele [1973] states that the lower grain yields obtained in the
monoculture were mainly caused by the infestation with Cercosporella. This example
clearly shows that the 'biologisch-dynamischer Landbau' could not prevent the fungal
attack and it also shows that the mineral fertilizer treatment was slightly superior in
comparison with the farm yard application for wheat grown in monoculture.
It is no question that plant resistance and susceptibility against diseases and pests to
some extent is influenced by plant nutrition (Fuchs and Grossmann [1972], Grossmann
[1970], Trolldenier [1969]), but the relationships are very complex as plant crops and
in particular the organisms which attack them, differ widely and as various properties
and factors can be responsible for the phenomenon which we call resistance or susceptibility. The Scientific Board of the International Potash Institute thought it worthwhile to treat this problem of 'fertilizer use and plant health' in a col1oquium like this,
well conscious of its difficulties due to the heterogenity of the matter. This col1oquium
is thought as a forum where agronomists, biochemists, plant pathologists and plant
physiologists should present their research data, observations and experiences relevant to the topic. Thus we see in this meeting a kind of an experiment where we bring
together experts from different scientific branches. Nevertheless the Scientific Board
of the International Potash Institute holds the view that bringing together scientists of
various branches nowadays can be more useful than meetings of highly specialized
experts.
Due to the fact that each specialized scientific branch tends to speak its own language,
we should try in this colloquium to explain our ideas and data in simple words and
terms so that a general understanding is guaranteed. Understanding each other is a
preposition of the ambitious result we are aiming for, namely to disclose and clarify
causal relationships between plant nutrition and plant health.
The col1oquium is divided in sessions, which are devoted to fungi diseases, diseases
caused by bacteriae and viruses as well as pests. The first session is thought to cover
the physiological and biochemical aspects and interactions between the host plant and
the infecting organisms. The Scienitfic Board of the International Potash Institute
believes that the key for a better understanding and interpreting the vast amount of
experimental data and observations available can be found on the level of molecular
biology. Thus it would be highly appreciated, if this aspect is treated in the col1oquium
thoroughly. To achieve this aim it is not only of importance that papers are presented,
we also emphasize the importance to discuss them seriously. For this reason one session
is devoted to the discussion which together with the coordinators' reports should help
us to develop and establish general lines and conclusions.
I hope that also the location wil1 be helpful in rendering this col1oquium in a successful
one. As you al1 know Izmir, this wonderful charming city characterized by an unique
urbanity, located on the threshold between orient and accident, has been a place of
meetings and contacts since old times. The Latin proverb says: 'Ex oriente lux', which
means from the orient comes the light. So we hopefully believe that we will be enlighted
in our approach to clarify the complex relationships between fertilizer use and plant
health.
29
Bibliography
Abele, U.: VergleiGhende Untersuchungen zum konventionellen und biologisch-dynamischen
Pflanzenbau unter besonderer Berlicksichtigung von Saatzeit und Entitiiten. Dissertation im
Fachbereich 'Angewandte Biologie' der Justus-Liebig-Universitiit Giessen, 1973.
Davis, R.E. and Whitcomb, R.F.: Mycoplasmas, rickettsiae, and chlamydiae: Possible relation to
yellows diseases and other disorders of plants and insects. Ann. Rev. of Phytopathology 9,
119-154 (1971).
Doi, J., Teranaka, M., Yora K. and Asuyama, H.: Mycoplasma or PLT group-like microorganisms
found in the phloem elements of plants infected with mulberry dwarf, potato witches' broom,
aster yellows, or Paulownia witchess broom. Ann. Phytopath. Soc. Jap. 33, 259-266 (1967).
Fuchs, W.H. and Grossmann, F.: Erniihrung und Resisteni von Kulturpflanzen gegenliber Krankheitserregern und Schiidlingen. S. 1007-1107. In: H.Linser, Handbuch der Pflanzenerniihrung
und Dlingung 1/2, Springer-Verlag Wien, New York, 1972.
Grossmann, F.: Einfluss der Erniihrung der Pflanzen auf den Befall durch Krankheitserreger und
Schiidlinge. Landw. Forsch. 25/1. Sonderh. 79-91 (1970).
Hopkins, D.L. and Mollenhauer, H.H.: Rickettsia-like bacterium associated with Pierce's disease of
grapes. Science 179, 298-300 (1973).
Petzold, H. and Marwitz, R.: Mykoplasmen und rickettsien-iihnliche Bakterien als Erreger von
Pflanzenkrankheiten. Mitt. BBA f. Landw. u. Forsten, Berlin-Dahlem, H. 151, p. 159-171 (1973).
Trolldenier, G.: Getreidekrankheiten und Pflanzenerniihrung. Potash Review (Berne), Subject 23,
34th suite (1969).
30
1st Session
Co-ordinator:
Fertilizer Use and Plant
Health: Physiological Aspects
Prof. Dr. K.Mengel, Head Institute of Plant
Nutrition, Justus Liebig University, Giessenj
Federal Republic of Germany
Plant Disease Resistance as Influenced by Biochemical
Effects of Nutrients in Fertilizers
Prof. Z. Kiraly, D. Sc., Research Institute for Plant Protection, Budapest/Hungary
Summary
Nitrogen affects diseases caused by obligate and facultative parasites differently.. The effect of
nitrogen on protein. metabolism, photosynthesis, phenol metabolism, on the reducing capacity of
tissues and on nitrate reductase is discussed. Potassium is treated in relation to phenol metabolism, "wound healing and frost injury. The action of phosphorus is evident mainly in virus infections.
Calcium promotes the resistance of pectic substances and cell walls to enzymatic degradation. The
role of calcium in disease resistance is conspicuous in the restriction of lesion size caused by different
facultative parasites and non-parasitic agents. On the other hand, calcium stimulates some macerating enzymes. Thus, it exerts a dual effect in cell wall metabolism.
Resume
L'azote affecte de differentes manieres les maladies provoquees par des parasites obligatoires ou
facultatifs. L'auteur discute les effets de ('azote sur le metabolisme des proteines, la photosynthese,
le metabolisme des phenols, la capacite rMuctrice des tissus et la reductase des nitrates. Le potassium
est discute en relation avec le metabolisme des phenols, la guerison de blessures et les degats dus au
gel. L'action du phosphore apparait avant tout dans les cas d'infections vi reuses. Le calcium favorise
la resistance des substances pectiq ues et des parois cellulaires envers la degradati on enzymatique.
Le role du calcium se manifeste dans la reduction de la grandeur des lesions provoquees par divers
parasites facultatifs et par des agents non parasitaires. D'autre part, le calcium stimule certaines
enzymes de maceration. Ainsi donc, il exerce un effet double dans le cadre du metabolisme des parois
cellulaires.
Experts in crop production long ago reached the conclusion that high nitrogen
increases susceptibility to many diseases, while potash increases resistance, and the
influence of phosphorus is variable. The vast amount of work that has been done on the
mode of action of nitrogen, potash and phosphorus acting on infectious disease has
resulted in little more than guesses, at least from a physiological point of view. Still,
the contention that it is difficult at present to detect any clear pattern in the metabolic
effect of nutrients on disease, seems to be a pessimistic simplification.
Nitrogen and diseases caused by obligate parasites
The evidence regarding increased susceptibility of host plants to obligate parasites
(rusts, mildews, club root, etc.) in consequence of high nitrogenous fertilization, seems
to be conclusive although the form of nitrogen available to ,the plant may also have
significance (Huber and Watson [1 la]). It is of interest that leaves of wheat that had
33
passed their normal susceptible stage and had become resistant ('adult plant resistance')
to powdery mildew became susceptible again when supplied more nitrogen (Last [15]).
Regarding susceptibility and resistance I would like to stress a very important point.
We have to differentiate between plant resistance to infection and resistance to multiplication of the pathogen in the host tissues. The first form is usually determined on
the basis of the number of infection sites, the latter by different infection types or host
reaction types. Experiments with the stem rust disease of wheat (Puccinia graminis
f. sp. trifici) clearly indicated that infection type of the host was never changed by
nitrogen treatments, however the number of infection sites (uredo-pustules per unit
leaf area) usually increased with increasing nitrogen. This was shown by Daly [6] and
recently by Mashaal [16] in my laboratory. In other words, the resistant infection
types of wheat, namely the hypersensitive flecks or the fully 'immune' reaction (0; and
o reaction types, respectively) are little, if at all, altered by nutritional treatment. On
the other hand, resistance determined on the basis of the density of uredo-pustules
(no. of infection sites) is greatly influenced by high nitrogen treatments. Figure 1 shows
240
220
l;'t
200
zH
180
~
C\l
160
140
El
0
;
120
0
"
;j
100
p
8
80
~
60
UJ
40
20
21
630
1050
p.p.m. OF NITROGEN
Fig. I. Number of pustules of Puccinia graminis f. sp. tritici per I cm 2 leaf area of Little Club grown
in sand culture and treated with modified Hoagland solutions. The standard Hoagland solution
served as control containing 284 ppm of nitrogen.
• = The difference is highly significant (P = 0.01).
the effect of high nitrogen in Hoagland solution on the number of uredo-pustules of
Puccinia gra'minis on leaves of a susceptible cultivar.
Pustule numbers were calculated per cm2 surface of the two terminal leaves and were
expressed as per cent of the control value. The suboptimal nitrogen supply significantly
decreased the number of pustules as compared to the control (36.9% as compared to
the 100% of control). In other words, the two terminal leaves of Little Club wheat
34
under nitrogen stress were more resistant to rust than the leaves on control plants
which received adequate nitrogen (284 ppm) in the Hoagland solution. Plants grown
at 630 ppm nitrogen in the nutrient solution were significantly more susceptible
(174.5%). The increase in susceptibility was even higher at the highest nitrogen level
(1050 ppm): 226.6% of the control. All of the differences were highly significant
(P=0.0l).
Resistance and susceptibility based on the reduction or increase in number of infection
sites, respectively, are of prime importance from a practical point of view. It seems
more important than the phenomenon of resistance based on infection types. Today
plant breeders are more and more involved in breeding new cultivars expressing the
so-called horizontal resistance and tolerance. Both of these forms of resistance are
expressed on the basis of the incidence of attack, in other words, on the basis of the
number of rust pustules on the leaf.
Proteins in relation to disease susceptibility
What about the biochemical effect (s) of nitrogen on the host plant and on plant
disease resistance and susceptibility? As a very important feature, the protein composition of leaves from plants treated with different levels of nitrogen was investigated
with the technique of polyacrylamide gel electrophoresis. The separated protein bands
were stained with amido-black. Most of the protein bands were more intensive in
protein extracts of leaves treated with nutrient solutions containing 630 or 1050 ppm
nitrogen. However, the profile of the electropherograms was not changed in consequence of treatments with nitrogen. Thus, qualitative changes did not occur as a
result of N treatments.
As early as 1934 Gassner and Franke [8] suggested that improved nitrogen nutrition
increases susceptibility of cereals by increasing the formation of several specific
.proteins. However, neither' the methods of Gassner and Franke nor the current methods
of protein chemistry seem to be suitable for the verification of this hypothesis. At any
rate the polyacrylamide gel electrophoresis applied in our experiments was not able to
demonstrate any changes in specific proteins following low or high nitrogen treatments.
Phenolics as influenced by nitrogenous fertilizers
It was shown by us many years ago that the application of nitrogenous fertilizers in
large amounts tends to decrease the total phenol level in wheat leaf tissues (Table 1).
Table 1. Effect of high nitrogen fertilization with NH 4N0 3 on the content of phenolics in leaves of
wheat cultivars (Kirti/y [12l)
Wheat cultivar
R23 Hungarian
Red Coat
Chinese P61-110.5b-4
Total phenolics mg/IOO g dry wt.
Seedling stage
.fIeading stage"
.
.
.
Control
N
Control
N
114
85
180
165
186
105
93
114
"The flag leaf and the next leaf below the flag leaf was used for determination of the phenol content.
35
The same phenomenon is apparent also in rice (Wakimoto and Yoshii [24]). In rice
plants that were enriched with nitrogen fertilizer the key enzymes of phenol biosynthesis (phenylalanine ammonia-lyase and tyrosine ammonia-lyase) were decreased
(Matsuyama and Dimond [l6a}).
As is known, phenol compounds in the host may contribute to the general (performed)
resistance of the host plant. The relationship of nitrogen metabolism to phenol
synthesis has been stressed by Szweykowska [23]. It was pointed out by this author
that there exist competing pathways of aromatic biosynthesis and nitrogen metabolism.
The nitrogen supply affects not only the amount ofphenolics but also their toxicity. As
shown by Kirkham [14] an increase of the ratio of soluble N/phenolics in a medium
lowers the toxicity of polyphenols to fungal pathogens. This observation might have
an in vivo significance as well.
Nitrogen supply affecting virus infection and multiplication
Many years ago Bawden and Kassanis [4] investigated the effects of various levels of
nitrogen on virus establishment in Nicotiana tabacum and N. glutinosa. High levels of
nitrogen increased TMV infection, but did not alter aphid transmission of potato
virus Y. Generally speaking, the most favourable nutritional conditions were the most
favourable for susceptibility to TMV infection. High nitrogen levels increased both
plant growth and susceptibility to virus infection. Similarly, high nitrogen levels led
to increased virus multiplication as evidenced by increases in purified virus obtained
from the plant (Wheathers and Pound [27]).
A more profound investigation was carried out by Zaitlin and Jagendorj [32]. They
investigated the enzymatic processes of photosynthesis as affected by nitrogenous
fertilization and TMV infection. When the nitrogen supply to tobacco plants was suboptimal the Hill reaction rate
2NADP++2H zO
-~
2NADPH+2H++Oz
was reduced and also the photosynthetic phosphorylation
2NADP++2HP+2ADP+2H3PO.
-~
2NADPH+2H++2ATP+2HzO+O z
was impaired. The chlorophyll content was also reduced. On the other hand, when
virus-infected plants received high nitrogen fertilization, symptoms were suppressed,
the chlorophyll was retained, the Hill reaction rate was unaltered and the virus content
of leaves was four times that of leaves with suboptimal nitrogen supply (Table 2).
Table 2. Effect of nitrogenous fertilization on chlorophyll content, Hill reaction rate, and virus
multiplication of tobacco leaves (Zaitlin and Jagendorj [32})
Treatment
Uninfected, plus nitrogen
Uninfected, nitrogen withheld
TMV-infected, plus nitrogen
TMV-infected, nitrogen withheld
.
.
.
.
*flmoles Fe(CN)6 reduced/mg chlorophyll/hr.
36
Mg chlorophyll/g
fresh wt.
Hill reaction
rate*
Mgvirus/g
fresh wt.
0.79
0.57
0.68
0.35
297
197
269
120
6.3
1.4
This observation may lead to the conclusion that the high nitrogen supports virus
multiplication but reduces disease severity, or at least the severity of the symptoms. It
would seem that virus infection exerts its damage mostly on those plants that were
supplied with nitrogen below the optimal level.
Nitrogen and diseases caused by facultative parasites
The aboye-mentioned increased susceptibility of host plants to many pathogens due to
high nitrogen supply does not seem to have general significance. It is characteristic
only for obligate parasites, like rusts, mildews, club-root caused by Plasmodiophora
brassicae, viruses, etc. I would like to stress that facultative parasites, particularly the
ones that cause necrotic leaf spots, behave differently. High rates of nitrogen usually
increase resistance to facultative parasites in the fresh green, young plant tissues
(Griimmer [9a]). Thus diseases caused by obligate and facultative parasites exhibit
quite opposite reactions to high nitrogenous fertilization.
It was shown recently by Aranka Gilly in my laboratory that the young, dark green
leaves of tomato are always more resistant to Alternaria solani than mature or
somewhat senescent leaves. Juvenility and greening of tomato leaves due to the
removal of terminal buds or flowers was also associated with a high degree of resistance
to facultative parasites causing necrotic leaf spots. Similarly, we were able to dt<monstrate that necrotic symptoms caused by two facultative parasites (A. solani and
X. vesicatoria) were significantly suppressed in tomato plants in pure sand cultures
supplied with high rates of nitrogen. Both the number of visible infection sites and the
size of necrotic spots were significantly reduced (Table 3).
It is noteworthy that leaf spots caused by Alternaria solani in tobacco were suppressed
in leaves that were treated with kinetin, which is a juvenility plant hormone-like
compound. Necrotic leaf spots caused by viruses were inhibited by different cytokinin
hormones that induce leaf juvenility (Kiraly, El Hammady and Pozsar [13]). The
effect of cytokinins on necrotic leaf spots and on tissue juvenility resembles that of
intensive nitrogen treatments. In this respect the recognition of Sargent and King [20a]
as well as Peterson and Miller [I8a] seems vitally important: the application of reduced
nitrogen salts to plants can promote accumulation of cytokinins. Evaluating the early
Table 3. Suppression of necrotic leaf spots caused ty Alternaria solani and XantllOmonas vesicatoria
in tomato leaves by high rates of nitrogen
Alternaria solani
Control
,. , ., ,
Hoagland, 70 ppm N ,
285 ppm N standard
420 ppm N
630 ppm N
Xanthomonas vesicatoria
Control
','
Hoagland, 70 ppm N
285 ppm N standard
420 ppm N
630 ppm N
Lesion, no,/IOO cm'
Diameter of
lesions in [lm
.
.
.
.
.
410
757
352
162
166
2200
2350
1710
1370
1000
.
.
.
.
.
1954
3054
2245
768
362
408
480
420
260
280
37
literature on the effects of nutrients on diseases caused by facultative parasites one can
see a similar pattern with Fusarium diseases (Walker and Hooker [26}). The rate of
cabbage yellows disease (Fusarium oxysporum f. sp. conglutinans) development declined
as the concentration of a balanced nutrient in pure sand cultures increased. Other
formae speciales of F. oxysporum similarly decreased as the concentration of N0 3nitrogen increased. These were in contrast to Plasmodiophora brassicae, an obligate
parasite, that increased with high nitrogen supplies (Walker [25}). To visualize the
situation I have tried to summarize the most important results in Table 4.
Table 4. A comparison of high and low nitrogen treatment on diseases caused by obligate and
facultative parasites'
Obligate parasites
Puccinia graminis'
.
.
Erysiphe graminis'
Plasmodiophora brassicae'
.
2
Tobacco mosaic virus • • . • • . . • . • . . . . . . . . . . . • • . . • . . . •
Facultative parasites
.
Xanthomonas vesicatoria'
.
Alternaria solani'
.
Fusarium oxysporum' f. sp. lycopersici
.
f. sp. conglutinans
.
f. sp. vasinfectum
.
f. sp. pisi
.
,+
+
2
LowN
HighN
+
+
+
+
+++
+++
+++
+++
+++
+++
+++
+++
+++
+++
+
+
+
+
+
+
means disease severity
means virus multiplication.
Possible biochemical effects of nitrogen treatments and the action on facultative
parasites
At present it is not known with certainty whether the pathogen or the action of its
toxin or perhaps only the necrotic symptom is suppressed in the resistant tissues of
plants supplied with ample nitrogen. From the results obtained with the so-called
necrotic hosts of viruses (Opel [i8), Kiraly, El Hammady and Pozsar [i3}) it seems
very probable that tissue necroses are inhibited in the vigorous and young plant organs
treated with high nitrogen amounts. If so, facultative parasites, which are in fact semisaprophytes, cannot grow in the absence of dead cells or tissues of plants heavily fertilized with nitrogen. In this respect phenol synthesis, accumulation and oxidation may
have significance. Suppressed phenol synthesis and particularly suppressed phenol
oxidation may lead to the suppression of tissue necrosis. The enzymatic or nonenzymatic 'reducing power' of tissues contributes importantly to the inhibition of the
accumulation of phenol oxidation products. Thus, the high reducing ability can keep
phenolics in a reduced state and can inhibit both phenol oxidation and the necrotic
symptoms (Kiraly [i2}). The effect of nitrogen fertilization on ascorbic acid content
and on enzymatic reducing capacity can be seen in Table 5 and Figures 2 and 3. A
higher level of reducing compound (ascorbic acid) was found in nitrogen fertilized
plants than in the controls. In addition, one can detect stimulated enzymatic reducing
capacity in the leaves of fertilized wheat plants. It is seen in Figure 2 that the activity
of NADPH-dependent glutathione reductase and reduced glutathione-dependent
dehydroascorbic acid reductase (Table 5) increased as a consequence of fertilization
with NH 4N0 3 • The soluble NADPH-oxidase was also stimulated in extracts of the
nitrogen-treated leaves (Figure 3).
38
A
o
ACTIVITY OF NADPH-DEPENDENT
<I
GLUTATHIONE REDUCTASE
0,400
0,300
0,200
0,100
5
2
7
9
HlNUTES
Fig.2. Activity of glutathione reductase in Red Coat wheat leaves. K=control. N=treated with
NH 4 N0 3 • Each cuvette contained 0.5 flM NADPH, 13 flM oxidized glutathione, 0.1 m1 2 x 10-2 M
KCN, enzyme corresponding to 100 mg leaf tissue, phosphate buffer pH 7.5. Total volume: 3.0 ml
(Kirtily [12]).
.
Q
o
NADPH OXIDASE
<I
0,500
0,400
0,300
0,200
4
6
8
10
MINUTES
Fig.3. Activity of NADPH·oxidase enzyme in nitrogen-treated (N) and control (K) leaves of Red
Coat wheat. Each cuvette contained 0.5 flM NADPH, enzyme corresponding to 100 mg leaf tissue,
phosphate buffer pH 7.5. Total volume: 3.0 ml (Kirtily [12J).
39
It is known that several host plants contain preformed resistance factors active against
the attacking or penetrating facultative parasites. One of these factors is tomatine, a
steroidal alkaloid in tomato leaves (Arneson and Durbin [2]). Recently we have found
that young resistant tomato leaves contain several times more tomatine than the
mature and susceptible older leaves. It remains to be seen whether or not nitrogenous
fertilization increases tomatine content in the green parts of tomato plants and how the
facultative parasites attacking this host are able to detoxify the increased amount of
steroid.
We have no idea about the protein alterations in nitrogen-treated plants and about
the significance of proteins in resistance to facultative parasites (Grummer [9a]). Since
there are few facts to go upon, I must rely at present on thought. An approach would
perhaps be the detection of changes in nitrate reductase enzyme following nitrogen
fertilization. As is known, this enzyme has a key role in amino acid biosynthesis.
NADPH z
FAD
NADP
FADH z
)(
)(
The early observation of Schroeder and Walker [21] would lend support to this
approach. They have found that the severity of Fusarium wilt of pea depends on
temperature as well as on nitrate supply. The host was more susceptible at 27°C than
at 21°C. The different response may be related to nitrate reductase activity, because
this enzyme is temperature-sensitive and is an adaptive enzyme that is formed only
when nitrate is available to the plant. Furthermore, nitrate reductase is considered to
be a NADH or NADPH-linked enzyme. As was shown above, pyridine nucleotides
are increased in some plant tissues as a consequence of nitrogenous fertilization.
The action of potassium on infectious disease
It is a general belief among plant physiologists and pathologists that potassium
fertilization reduces the intensity of several infectious diseases, and this occurs with
diseases caused by obligate as well as by facultative parasites. The action of potassium
on plant metabolism is manifold. There is a large group of enzymes that is activated
by K+ more or less specifically. Protein synthesis and many other syntheses (sugars,
Table 5. Effect of fertilization with NH 4 N0 3 on the content of ascorbic acid and on the activity of
dehydroascorbic acid reductase in leaves of winter wheat cultivars (Kirtily [12J)
Ascorbic acid
mg/g dry wt.
Cultivars
Red Coat. . . . . . . . . . . . . . . . . .
Chinese P61-1I0.5b-4 . .... ..
Activity of
dehydroascorbic acid
reductase"
Control
N
Control
N
5.3
6.0
7.5
7.7
5.0
5.2
6.8
7.1
" Ascorbic acid production after 20 minutes by the action of reductase enzyme on glutathione and
dehydroascorbic acid, mg ascorbic acid/g fresh weight.
40
t'
cellulose, cell wall, vitamins, etc.) are promoted by the availability of potassium in large
quantities. It is a well established fact that a reduced supply of potassium leads to
disturbed nitrogen and carbohydrate metabolism of plants (Hewitt [11]). As a rule
non-protein nitrogen compounds and soluble carbohydrates accumulate. Inadequate
potassium supply favours the accumulation of phenols (Mulder [17], Reddy and
Sridhar [19]), sugars and amino acids in leaves of rice. At low potassium levels the
accumulated amino-N contributes to a rapid breakdown of phenols, as was mentioned
in an earlier paragraph. Thereby, the susceptibility of K-deficient rice to bacterial
blight disease (Xanthomonas oryzae) is increased, as was found by Reddy and Sridhar
[ 19].
S.F.Mashaal in my laboratory showed recently that Little Club wheat produced
smaller and fewer rust (Puccinia graminis f. sp. tritici) pustules in sand culture when
generously supplied with potassium. Dr. Aranka Gilly measured the diameter of
necrotic spots in tomato leaves caused by infection with Alternaria solani. In all
experiments of this type modified Hoagland solutions were used, only one of the elements (N or K) investigated being changed at a time, enabling comparison to be made
between disease severity in plants supplied with high, low or normal levels of nitrogen
or potassium. As is seen in Table 6, at low potassium levels the necrotic spots were
larger. In other words, ample potassium increases resistance to Alternaria solani.
Basically similar results were attained by Walker and Hooker [26] with cabbage
yellows (Fusarium oxysporum f. sp. conglutinans).
Toble 6. Suppression by high potassium of necrotic leaf spots caused by Alternaria solani on tomato
leaves
Diameter oflesions in [lm
Hoagland,
8 ppm
78 ppm
237.5 ppm
400.0 ppm
K
.............
K
K standard. . . . . . . . . . . .
K ..... . . . . . . . . . . . . . . .
2000
2170
1380
1028
Potassium and wound healing
Some experimental results indicate that wound healing is also influenced by potassium
nutrition. Allington and Laird [1] found that the potassium level influenced the
duration of infectible sites on leaves of Nicotiana glutinosa which is a 'necrotic' host of
tobacco mosaic virus (TMV). N. glutinosa plants grown on a reduced supply of
potassium produced more infection sites (necroses) than those receiving ample
potassium. Low potassium encouraged infection sites to remain receptive to TMV for
a longer period after wounding. Presumably, wound healing was delayed by insufficient
potassium nutrition.
Recently it was concluded from Hungarian field experiments that potassium fertilization reduced the susceptibility of grape cultivars to infection by Botrytis cinerea.
Infection by this fungus is predisposed by heavy wounding of grape tissues short before
harvest. Ample potassium nutrition supposedly reduces wound injury or stimulates
wound healing and this leads to reduced susceptibility to infection by this fungus.
41
High potassium supply and resistance to frost injury
I would like to call the attention to the idea that high potassium nutrition can increase
frost resistance of plants. At low temperatures during the hardening period in the fall
and winter, the cell sap concentration of plants commonly increases due to sugar
accumulation. It is also a general phenomenon that high potassium nutrition stimulates sugar synthesis and accumulation in plant tissues. There is a reversed correlation
between cell sap concentration and ice formation in the plant when frozen during
winter. Therefore, the higher the sugar accumulation and cell sap concentration the
higher is the resistance to frost injury in some plants. Preliminary investigations in the
Research Institute for Plant Protection, Budapest, have shown that in tissues of apricot
trees infected with Pseudomonas syringae, the causal agent of the apoplexy disease, the
sugar level was rapidly reduced during winter. Thus, infected woody tissues were more
sensitive to frost injury than the uninfected ones. In fact, it has long been known that
cankers on some stone fruit trees and the die-back syndrome (apoplexy) are basically
similar to frost injury phenomena. Summarizing, infection lowers the sugar level in
tissues and, therefore, the plant becomes more sensitive to freezing injuries. It seems
logical to suppose that ample potassium nutrition will suppress frost injury (cankers)
by counteracting the loss in sugar, and will increase resistance of fruit trees to apoplexy
and of other plants to frost injury. There are preliminary results in Hungary to support
the validity of this idea.
A comparison of the action of high and low potassium supply on infectious diseases
and frost injury is seen in Table 7.
. Table 7. A comparison of high and low potassium treatment on infectious diseases and frost injury
Puccinia graminis'
Alternaria solani'
Fusarium oxysporum'
Xanthomonas oryzae'
Tobacco m'osaic virus2
Frost injury'
.
.
.
.
.
.
LowK
HighK
++++
++++
++++
++++
++++
++++
+
+
+
+
+
+
, + means disease severity.
2 + means susceptibility to infection.
Phosphorus and plant diseases
In spite the fact that phosphorus is involved in the formation of a series of bio-organic
compounds and in metabolic processes vitally important to the plant (e.g. phospholipids in membrane formation, nucleic acids in regulation and protein biosynthesis,
P-containing coenzymes, adenylic acid and phosphorylation in energetic and other
processes), its action on disease resistance is variable and seems to be not very conspicuous.
The effect of phosphorus on virus infection and biosynthesis was investigated more
thoroughly because the synthesis of this obligate parasite is perhaps the most closely
42
associated with the metabolic processes influenced by high or Iow levels of phosphorus.
Yarwood [30] has postulated that phosphate greatly enhances the infection process
but the mechanism remained unknown. The balance between nitrogen and phosphorus is sometimes important (Bawden and Kassanis [4]). In the case of TMV
higher amounts of nitrogen can increase susceptibility of the plant to infection only if
adequate available phosphorus is present. Susceptibility is reduced by high nitrogen if
phosphorus is Iow.
The multiplication of viruses is also influenced by this element. Increasing phosphorus
increased the amount of cucumber mosaic virus in spinach (Cheo, Pound and Weathers
[5]). The virus biosynthesis was increased at phosphorus levels high enough to cause
stunting of plant growth.
Calcium and cell walls resistant to enzymatic degradation
One of the largest question marks in plant pathophysiology today is the role of the cell
wall and of cell wall degrading enzymes in disease resistance. Certainly their role, if
any, would be restricted first of all to facultative parasites causing soft and dry rots
(necroses) and to some viruses. The action of these enzymes is characterized by some
degradation of cell walls and separation of cells from one another (maceration). As
regards resistance of plant cell walls to degradation by pathogens, calcium is the
element which has been investigated most intensively.
It is known that chains of pectic acid, the principal binding agent between cells, are
partially cross-linked with Ca++ and Mg++. Calcium pectate forms the binding between
cells resistant to enzymatic degradation by pathogens. In fact Ca++ forms rather rigid
linkages between pectic chains. Indeed certain viruses render infected tissues much
stiffer than normal, and it has been shown (Zaitlin and Coltrin [31]) that the walls of
virus-infected cells contained calcium pectate rather than pectic acid. A' specific
pectin-degrading enzyme was not able to separate TMV-infected cells of tobacco, but
upon addition of a chelating agent (EDTA), which removed Ca++, the host cells
separated according to expectation.Weintraub and Ragetli [28] demonstrated also
with local lesion hosts of TMV that infection affects the binding between the cells by
increasing the amount of calcium associated with the middle lamella. It is of interest
that lesions of apple skin, the so-called Jonathan spot lesions, accumulate four times
as much Ca++ and Mg++ as adjacent normal tissues. Calcium-fertilizer spray applications reduce the rate of Jonathan spot disease (Richmond [20], Schumacher and
Fankhauser [22]). A similar mechanism explains the action of a synthetic auxin,
naphthaleneacetic acid, on resistance of tomato to Fusariuin wilt. This resistance was
dependent upon the presence of Ca++ and the treated plants had less water-soluble
pectin than the untreated ones. Auxin caused demethoxyJation of the pectins and gave
the opportunity for the formation of more bridges by calcium (Edgington, Corden and
Dimond [7]). One may suppose that the type of pectic substance is determined by the
calcium content and this determines the resistance of tomato to Fusarium oxysporum
f. sp. lycopersici. Calcium is implicated in the resistance to several other .diseases
(Wood [29], Goodman, Kiraly and Zaitlin [9]). Table 8 gives a summary of the most
important cases.
Rhizoctonia-infected bean hypocotyls exhibit an extremely interesting case of resistant
pectic substances. Bateman [3] demonstrated the presence of a dialyzable factor in
host tissues, which inhibited maceration by enzymes found in the infected tissues. This
43
Table 8. A comparison of high and .Iow calcium treatment on infectious diseases and non-parasitic
skin spots·
Erwinia phytophthora
Rhizoctonia solani
Sclerotium ro/fsii
Botrytis cinerea
Fusarium oxysporum
Jonathan spot (non-parasitic)
Bitter pit (non-parasitic)
• The
+
.
.
.
.
.
.
.
Low Ca
High Ca
++++
++++
++++
++++
++++
++++
++++
+
+
+
++
+
++
++
mark means disease severity.
inhibitor turned out to be Ca++ which rendered pectic acid resistant to hydrolysis by
polygalacturonase of Rhizoctonia in bean tissues surrounding lesions. By this mechanism the pathogen was confined to a lesion of limited size in the hypocotyl. Calcium
and other ions accumulated only in the late stage of disease, therefore both the enzyme
and the fungus were inhibited only after the lesion increased to a certain size.
Contrary to the above-mentioned effect of calcium, it must be born in mind that some
pectolytic enzymes may be activated by this element. This effect of calcium is not
easily demonstrated because of the nullifying effect of calcium in increasing the
strength of host cell walls. Still, Hancock and Miller [10] have shown that the Ca++
mobilized in lesions caused by Colletotrichum tri/olii in alfalfa supports fungus growth
in host tissues by stimulating the macerating action of another pectolytic enzyme, the
polygalacturonic acid transeliminase. All these results draw attention to different
pectic enzyme systems associated with various parasites and perhaps a dual role for
Ca++ in cell wall metabolism in the host-parasite relationship. This would be the
reason for the experience that the influence of this element on disease resistance is not
unequivocal. Calcium sometimes increases host resistance, however in some other
cases it renders the pathogen more virulent, thereby increasing the severity of disease
symptoms.
In this survey I have tried to summarise the main trends in the action of the most
important elements on plant resistance. Certainly, what is now needed is patient and
perhaps slow but profound experimentation on a biochemical level. This should
produce less equivocal explanations which would be an inprovement on guesswork.
44
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45
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(1960).
46
Rice Diseases and Physiological Disorders
Related to Potassium Deficiency
M.lsmunadji, Head, Plant Nutrition Subdivision, Plant Physiology Division, Central Research
Institute for Agriculture, BogorjIndonesia
Summary
Modern high yielding rice varieties require generous use of nitrogen fertilizer and the use of nitrogen
in unbalanced fertilizers could result in increased disease incidence. The role of potassium in ameliorating the undesirable effects of nitrogen is discussed with reference to effects on physiology of the
rice plant which may affect disease resistance and with particular reference to brown leaf spot
(Cochliobolus miyabeanus), stem rot (Helminthosporium sigmoideum), bacterial leaf blight (Xanthomonas oryzae), sheath blight (Thanetophorus cucumeris), narrow brown leaf spot (Spherulina
oryzina) and blast (Piricularia oryzae Cav.). An experiment in Jakenan, Central Java is described
in which potassium increased yield in a spectacular manner and reduced damage by stem rot from
70% to under 5%.
A general discussion of the role of potassium in various physiological disorders - 'akiochi', 'akagare',
'amyit-po',. 'aogare', 'pansuk' and bronzing diseases in India and Sri Lanka. Experiments investigating
the effecf of potassium on bronzing disease ('mentek') in Cihea, Indonesia are described. A:pplication
of potassium fertilizer resulted in reduced uptake of Fe 2 + from reducing soils, with consequent
reduction in bronzing and increase .in grain yield by up to 100%.
Resume
Les varietes de riz it haut rendement necessitent des apports importants d'engrais azotes. L'application d'azote par I'intermediaire de formules d'engrais non-equilibrees peut dans certains cas favoriser
I'apparition de maladies. On discute le role du potassium en vue de la reduction des effets indesirables
de l'azote en se referant aux effets sur la physiologie de la plante de riz qui peuvent affecter la
resistance contre les maladies, en particulier contre la maladie des taches brunes des feuilles
(Cochliobolus miyabeanus), la pourriture des tiges (Helminthosporium sigmoideum), le charbon des
feuilles (Xanthomonas oryzae), le charbon des gaines (Thanetophorus cucumeris), la maladie des
petites taches brunes (Spherulina oryzina), la brOlure (Piricularia oryzae Cav.). L'auteur decrit un
essai effectue it Jakenan (Java central) dans lequelle potassium a augmente les rendements de fa<;on
spectaculaire en reduisant en meme temps de 70% it moins de 5% les degiits occasionnes par la
pourriture des tiges.
Ces considerations sont suivies d'une discussion generale du role du potassium dans divers troubles
physiologiques apparaissant chez le riz en Inde et en Sri Lanka: «akiochi», «akagare», «amyitpo»,
«aogare», «pansuk» et le «bronzage». On decrit des essais ayant pour but d'examiner !'effet du
potassium sur la maladie du «bronzage» (<<mentek») it CiheajIndonesie. L'application d'engrais
potassiques a provoque une reduction de l'absorption de Fe 2 + dans des sols reducteurs avec diminution consecutive du «bronzage» et augmentation jusqu'it 100% des rendements en grains.
47
I. Introduction
The chemical control of rice diseases has not so far been successful in the tropics. This
is in contrast to the situation in pest control where great advances have been made in
recent years which enable practical control of pests without adverse effects on the
environment.
For disease control to be effective the timing of spraying is extremely important and
chemicals sprayed on the foliage are washed off by frequent showers during the main
rice growing season. The year round cultivation of rice in the tropics also results in
rapid and frequent build-up of pathogenic organisms. To give effective protection
frequent preventive fungicidal sprays must be applied. Costs for such measures are
often prohibitive.
The most promising approach is the use of resistant varieties in combination with
sound management practices. Plant breedt:rs have been successful in producing a
number of varieties with a wide spectrum of relative disease resistance, but the great
variability of pathogenic organisms leads to frequent breakdown in resistance.
To produce high yield, liberal application of nitrogen fertilizer is a must. High nitrogen
levels in the plants - a prerequisite for high yield - is usually related to decreased
disease resistance, especially when potash is deficient.
Little attention has so far been paid to potassium nutrition of rice in the tropics because
high-yielding varieties able to utilise high levels of nitrogen have only recently been
introduced. As the area under high yielding rice increases and with the continued
application of nitrogen, nitrogen-potassium imbalance is likely to increase and this
may lead to increased disease and losses in production.
Though there are many observations and reports which link nutrition with disease,
knowledge about causal relationships is still limited. Because it is a problem on the
borderline between two disciplines - plant physiology and pathology - comprehensive
research has, so far, been limited.
There are also great methodological difficulties involved. If, for example, tests plants
are grown under conditions of potassium deficiency the final result will be composed
of pre-infectional change in the resistance of the plant to the pathogen and a postinfectional effect on the course of the disease in the plant. The change of just one
nutritional factor may cause a complex of changes in the plant, some of which may
favour, whereas others may inhibit infection and spread of the disease.
Nutritional factors change the growing period, the plant type, the cell structure and
the chemical composition of the cell content. Different varieties may respond differently
to the same nutritional environment and the same is true for the pathogens. The above
factors account for some of the conflicting reports we find in the literature. As a
general rule, however, we know that heavy nitrogen applications tend to increase
disease incidence and that in many cases application of potassium helps to counter
this negative effect of nitrogen.
Resistance or susceptibility to disease consists of two major components. Resistance
to infection, which is largely mechanical, depends among other things, on the thickness
of the cuticle and epidermis, the incrustation of silica on the leaf surface, the thickness
of cell walls and the opening of the stomata. Resistance to the spread of disease in the
plant is affected largely by the chemical cOplposition of the cell content, the thickness
and degree of lignification of cell walls and the number and shape of vascular bundles.
48
2. Effects of potassium on morphological and histological characteristics of rice
plants
2.1. Silicification of epidermal cells
The degree of silification of epidermal cells of leaf blades appears to be closely related
to fungus disease resistance. Noguchi and Sugawara [l966] found that potassium
increased the silica content of plants and thereby decreased susceptibility to blast
disease (Tables 1 and 2).
Table 1. Effect of potassium on the number of silicified cells per mm z blade area (Variety: Norin 29,
Toyama soil)
Treatment
Long cells
Short cells
Stomata
Motor cells
0
NP
NPK
NPK z
16
10
18
17
24
18
27
30
5
3
7
8
39
33
46
50
Table 2. Effect of potassium on the silica content (% dry matter)
Treatment
Leaves
Stem
Ear
Root
NP
NPK
NPK z
14.1
18.0
17.8
4.7
5.9
6.1
3.4
3.9
4.1
3.0
3.9
4.1
Okamoto [1958} on the other hand, found that addition of potassium to a-soil low in
both silica and potassium resulted in decreased silica content ofthe plants and increased
susceptibility to blast disease.
2.2 Effect of potassium on the histological structure of rice plants
Although the hardness of the culm is to a large extend affected by varieta:I characteristics, nutrition too has a pronounced influence. Where potassium is deficient
relative to nitrogen, its .addition results· in a pronounced hardening of the tissues
(Table 3).
Table 3. Effect of potassium on the hardness, thickness and ligni~ content of the culm of paddy rice
(Noguchi and Sugawara [1966])
.
Treatment
Hardness of the culm*
Internode No.
NP
NPK
NPK 2
3.0
6.0
6.5
2
3
4
2.2
4.0
4.6
1.5
1.4
2.5
2.6
3.0
4.0
Thickness of the culm (mm) Lignin content
(% dry matter) .
2
0.84
0.86
0.92
0.49
0.55
0.59
4
0.37
0.40
0.42
0.29
0.39
0.37
26.9
27.5
29.3
Variety: Sinriki, Niigata soil.
* Force required to crush 1 cm of the main cuIm in kg.
49
Potassium favourably influenced the lignification of sclerenchym directly under the
epidermis and in the cells surrounding vascular bundles. Potassium has been shown to
be essential to increase the mechanical strength of rice plants and thus enable them
better to withstand infection by pathogenic organisms. Potassium is also involved in
the opening and closure of stomata and this in turn could have an influence on the
penetration of bacteria such as bacterial leaf blight.
2.3. Effect of potassium on the cell contents
Once a pathogenic organism penetrates the outer, largely mechanical, defence line
of a plant, its growth (and damage to the host plant) will largely depend on the availability of a nutritional medium in the cells that suits the organism's specific needs. In
plants deficient in potassium, soluble sugars, amides and amino acids accumulate at
the expense of higher molecular weight compounds, such as lignin, starch and proteins
(Tables 4 and 5). Most pathogenic organisms prefer low molecular weight substances
as nutritional medium to the insoluble or less soluble compounds found in plants with
an adequate supply of potassium.
Table 4. Effect of potassium on total carbohydrates and total sugar content of rice plants at heading
stage. Variety: Norin 29
Treatment
NP
NPK
NPK z
Leaves
T.e.
T.S.
T.S./T.e. %
Sheaths (% dry matter)
T.e.
T.S.
T.S.jT.e:%
22.5
23.2
23.3
2.76
1.59
1.61
12.3
6.9
6.9
23.2
24.3
24.5
2.43
1.79
1.52
10.5
7.4
6.2
T.e.: Total carbohydrates.
T.S.: Total sugars.
Table 5. Effect of potassium on total and soluble nitrogen in rice plants. Variety: Norin 29 at YPI
stage (Noguchi and Sugawara)
Treatment
NP
NPK
NPK z
Blades
Tot.N%
Sol.N %
Sheaths
Sol.N/Tot.N % Tot.N%
Sol.N%
SoI.N/Tot.N %
3.10
2.81
2.76
0.71
0.58
0.42
22.9
20.6
15.2
0.45
0.21
0.18
45.9
34.4
31.6
0.98
0.61
0.57
In K deficient plants monoamino carboxylic acids, amino dicarboxylic acids and their
amides increase. Valine, alanine, aspartic acid, glutamic acid, glutamine, arginine
and putrescine were found in significantly higher concentrations in K-deficient plants
than in healthy plants. There was no proline in healthy plants, but it was present in
K-deficient ones.
It can be assumed that in general a deficiency of potassium, especially if combined with
an excess of N, decreases the mechanical resistance of plants to pathogenic organisms
and provides a better nutritional medium for pathogens once they have entered the
plant.
50
3. Potassium nutrition in relation to some major rice diseases
The occurrence or severity of parasitic rice diseases is usually increased by excessive
nitrogen and a deficiency of potash, but the degree to which potash effectively decreases
disease damage varies greatly with the type of causal organism and with plant variety.
3.1. Brown leaf spot (sesame leaf spot disease)
Brown spot disease is caused by the fungus Cochliobolus miyabeanus (Ito et Kuribayashi) Drechsler ex Dastur. In older literature it is also referred to as Ophiobolus
miyabeanus or Helminthosporium oryzae Breda de Haan. This disease has been reported
from nearly all rice growing countries. It is said to have contributed significantly to the
catastrophic Bengal famine in 1942, causing yield losses of 50 to 90% (Ou [1973)).
Among all rice diseases, brown leaf spot appears to be most closely related to nutritional problems in general and to potassium deficiency in particular. Nutritional
imbalances due to shortage or excess of nitrogen, a shortage of silica, manganese, zinc
or magnesium and/or an excess of phosphorus will favour the outbreak of the disease.
Among the nutritional factors potassium deficiency has the strongest influence.
K deficiency is considered a predisposing factor for this disease. During world war II
when potash supply was short in Japan, brown leaf spot was the most difficult disease
to control. Potassium seems to affect all phases of the disease (Uexkull [1966)).
Akai [1962) cultivated rice plants under condition of normal nutrient supply, and
shortage and excess of nitrogen and potassium and measured the effect of the treatments on the germination of conidia from Cochliobolus miyabeanus arid on the size of
diseased spots. The results are summarized in Table 6.
Table 6. Effect of changing supply of Nand K on germination of Cochliobolus miyabeanus conidia
and on the size of large size diseased spots produced by the fungus
No. of spores measured
No. of germinating spores
Germination %
Large size diseased spots %
Control
Excessive
K
Deficient
K
Excessive Deficient
N
N
1041
390
37.7
39.7
980
248
25.3
26.3
1015
518
51.0
66.8
912
678
73.3
37.7
1002
906
90.4
51.7
Spores originating from K-deficient plants appear to be more virulent. A good
potassium supply reduced the germination rate of conidiospores. In plants well
supplied with K the disease usually remains localized close to the place of infection,
indicating that the spread of mycelia from the infection hyphae is restricted (small
spots).
Brown leaf spot is also very common in Indonesia. It is often seen on problem soils
such as poor podzols, tidal swamp areas, calcareous and peaty soils. Although the
relationship between the nutritional status of these soils and brown leaf spot incidence
has not so far been intensively studied, it appears that such problem soils are often low
in potassium.
Brown leaf spot can be identified by the appearance of oval brown spots with a grey
or whitish centre. Typical spots are often evenly distributed over the leaf surface and
are of the shape and size of sesame seeds (sesame spot disease). Correction of nutri-'
tional imbalances, especially application of potassium, is the most effective means to
combat the disease.
51
3.2. Stem rot
Two closely related fungi cause stem rot. Helminthosporium sigmoideum Cav., also
referred to as Lepthosphaeria salvinii Catt = Magnaporthe salvinii (Catt) Krause and
Webster, and Helminthosporium sigmoideum Cav. var. irregulare Cralley et Tullis.
Heavy losses due to this disease have been reported from India, Japan, the Philippines
and Indonesia. High levels of nitrogen (and phosphorus) and a poor supply of potassium favour the outbreak of this disease. It is most frequently found on illdrained
soils where uptake of potassium is often a problem.
Stem rot usually starts on the outer leaf sheaths near the water line, where numerous
small blackish irregular spots (lesions) appear. At a later stage the stem becomes
infected, starts to rot and collapses causing lodging of the plant.
The relation between outbreak of stem rot and the nitrogen and potassium supply is
shown in Table 7.
Table 7. The effect of different levels of Nand K on stem rot incidence (Yoshi et al. [1949J)
Levels of
N
K
0
0
1
I
2
2
0
2
0
2
0
2
Degree of
damage
1.8
0.5
38.5
7.5
73.1
20.9
The role of potassium in reducing stem rot incidence has been clearly demonstrated
in a planosol area low in potassium in Jakenan, Central Java. Responses to potassium
fertilizer were dramatic and grain yields were doubled. The low yield in the absence
of potassium was not only due to nutrient shortage but also to the heavy incidence of
stem rot as has been confirmed by a recent experiment in the area during the 1974-1975
wet season. C4-63 (green base) was the variety used and the nil-potassium plots
yielded very poorly and were severely affected by stem rot. In 1975-1976 the experiment
was repeated with careful recording of the severity of stem rot on individual plots,
using a modified formula of Yoshi et al. [1949]. The results are detailed in Table 8.
Varieties vary greatly in their resistance to stem rot. Selection of resistant varieties
combined with a balanced nitrogen and potassium supply appears therefore the most
promising way to combat this disease.
3.3. Bacterial leaf blight (Kresek disease - severe form in Indonesia)
Bacterial leaf blight is caused by Xanthomonas oryzae (Uyeda et Ishiyama) Dowson,
which is very widespread in tropical Asia. In some states of India yield losses as high
as 60% have been reported (Ou [1973]). High temperatures, high rates of nitrogen
and excess silica and magnesium favour disease incidence. Potassium and phosphorus
on the other hand, help to reduce damage.
With the steady increase of nitrogen rates in tropical Asia, damage caused by bacterial
leaf blight is expected to increase, especially where nitrogen is not balanced with
adequate P and K. Recent trials in India (Padhi and Mishra [1972]) have shown that
increasing the rate of nitrogen from 0 to 180 kg N/ha increased the infection of leaves
52
Table 8. Grain yield and stem rot incidence of rice (cv. C4-63 gb) as affected by fertilizer treatment.
Jakenan )975-1976 wet season
Treatment
Degree of damage
Yield index
0- 0- 0
0-60- 60
120- 0- 60
120-60- 0
120-60- 30
120-60- 60
120-60- 90
120-60-120
47.0
0.3
7.2
69.2
23.2
4.4
2.3
1.8
100
104
163
66
146
187
202
173
of Taichung Native 1 at harvest by bacterial leaf blight from 38:3% to 88.6%. Addition
of 20 kg/ha Kp as top dressing in addition to a basal dressing of 60 kg/ha KzO
reduced the percentage of leaf blight affected leaves at all N levels by over 20%. In
another trial Davadath and Padmanabhan [1970J observed that potassium not only
decreased the number of leaves affected by bacterial leaf blight, but also decreased the
lengths of lesions of infected leaves (Table 9).
Table 9. Effect of different rates of nitrogen and potassium on the length of lesions of bacterial leaf
blight infected rice leaves (Variety: Taichung Native 1)
K-rate
kg K 2 0/ha
Nitrogen rate, kg N/ha
60
120
180
60
120
180
11.4
10.1
9.1
12.7
11.7
10.3
16.3
14.4
6.8
Figures denote length of lesions in cm.
Varieties differ greatly in their resistance to bacterial leaf blight. The many strains of
bacterium oryzae differ in ability to infect rice plants.
As chemical control is not yet possible, selection of resistant varieties combined with
balanced nutrition is the only way to keep damage from this disease at reasonable
levels.
3.4. Sheath blight
Sheath blight is caused by a fungus called Thanatephorus cucumeris. It is also referred
to as Hypochlls sasakii, Corticium sasakii and Pelliclllaria filamentosa. In traditional
rice culture damage from this disease was limited. High rates of nitrogen, close spacing
and heavy tiJIering - conditions found in high yield rice culture - are expected to
increase incidence and damage from this disease. Adequate potassium and phosphorus
appear to reduce disease incidence, but judging from the limited observations available,
the effect of potassium appears less pronounced than in the case of other diseases.
Varieties highly resistant to this disease have not yet been found. Recently an observation was made on the effect of potassium supply on sheath blight incidence in Cihea,
West Java. The area was grumusol and low in K (!smunadji [1973 J). Plants without K
yielded very poorly. K treated plants tended to be less severely affected by disease. The
yield and severity of sheath blight infestation due to the treatments are shown in
Table 10.
53
Table 10. Effect of potassium on sheath blight infestation of B9c-Md-3-3 CCRIA rice selection) in
Cihea
Treatment
Disease
infestation, %
Yield index
120- 0- 0
120-60- 0
120-60- 60
120-60-120
58.8
67.6
55.0
48.0
100
134
168
190
Sheath blight is, however, one of the few diseases where chemical control has worked
quite well. Organic arsenic compounds and antibiotics appear most promising at this
time.
3.5. Narrow brown leaf spot
Narrow brown leaf spot is caused by the fungus Spherulina oryzina Hara, also referred
to as Cercospora oryzae Miyake. The disease is widespread in South East Asia and
other countries on susceptible varieties. Narrow leaf spot appears to be less severe on
fertile soil. The effect of fertilization on the outbreak of narrow leaf spot on rice is
presented in Table 11.
Table 11. Effect of fertilizers on the outbreak of narrow leaf spot of rice (Yoshida [1948])
Treatment
No. of disease spots
per leaf
No. of disease spots
per leaf sheath
0-0-0
10.0
7.0
12.0
7.0
4.5
1.8
10.0
8.5
12.0
9.0
5.0
3.0
o
-P-K
N -P-O
N-P-K
Nz-P-K
Nz-Pz-K z
Many varieties are somewhat resistant to this disease.
3.6. Blast
Blast is caused by the fungus Piricularia oryzae Cav. This disease is very widespread
and causes heavy damage, especially in the wet season crop. Several hundred different
races of variable pathogenicity of the fungus have been identified. High temperature,
high humidity, close spacing and heavy rates of nitrogen provide an optimum environment for the outbreak of the disease. Plants with a high silica content show a higher
degree of resistance. Application of silica fertilizer has proved to be highly effective in
lowering blast damage in Japan and in Korea.
A great number of experiments from different countries have shown that application
of potassium reduced infection. However, there are also reports indicating increased
disease susceptibility as result of potassium application. On soils low in silica the
addition of potassium tends to reduce the silica content of the leaves, thereby lowering
mechanical resistance to infection. In the case of blast, there appears to be no clear cut
relationship between potassium and the occurrence of the disease. But application of
potash to a deficient soil will usually produce healthier plants. Summarizing the effect of
K on blast disease, Kozaka [1965] wrote:
54
'In Japan potassium deficiency occurs particularly on fields subjected to heavy nitrogen
application or in degraded paddy fields. Sufficient application of potassium, therefore,
is necessary for good growth and high yield. This helps control several diseases,
including blast.'
4. Physiological disorders related to potassium deficiency
Several physiological disorders related to potassium deficiency in lowland rice have
beeen reported in many parts of Asia. In many cases the affected plants showed
rather complex symptoms. This can be well understood, since potassium deficiency
could occur in different soil and climatic conditions, and it was often related to other
nutritional as well as environmental stresses. Moreover potassium deficiency causes a
nutritional imbalance in the rice plant, which could create a dramatic change in the
metabolic activity of the rice plant.
There is ·evidence that potassium plays a role in water metabolism in plants, improves
culm hardness and strength and influences yield. It also influences photosynthesic
activity and respiration (Jackson and Volk [1968]), it affects cabohydrate metabolism
and enzyme activity (Liebhart [1968]). The potassium status of soil and plant is
closely related to crop yield, in quantity as well as quality.
4.1. Diversity of physiological disorders
Akiochi disease, meaning autumn decline, is well known in Japan. Affected plants are
vigorous and healthy early in growth but gradually decline around heading. The yield
is low. Typical symptoms of akiOchi are: early dying of lower leaves, root injury,
occurrence of Helminthosporium leaf spot, low percentage of productive tillers, short
culm and panicle, few grains per panicle, poor grain filling, low grain: straw ratio,
appearance of dark brown spots on the grain and low grain weight (Tanaka and
Yoshida [1970], Baba et al. [1965]).
It has been reported that the disease is closely related to soil type and climate. Affected
plants are low in potassium and silica, but rather high in iron content. About 20% of
the total rice acreage in Japan was once estimated to be affected by akiochi disease.
An Akiochi.like disease was also reported in Korea. Affected plants were low in
potassium, magnesium, manganese and silica. The problem soils were derived from
granite or peat, low in pH and CEC (Tanaka and Yoshida [1970], Park and Tanaka
[1968]).
Akagare, meaning red-withering, is another physiological disease in Japan related to
low potassium. It appears two to three weeks after transplanting. The older leaves
. show reddish brown spots. There are 3 types of akagare disease. Akagare type 1 is
caused by potassium deficiency. First the leaves turn dark green and then small
reddish brown spots appear near the tips of the older leaves, which then die from the
tips. The roots turn light brown, dark reddish brown and sometimes rot. It occurs in
ill drained soils. Akagare type 2 is considered to be due to toxicities of organic acids,
iron and hydrOgen sulphide, associated with· potassium deficiency. First the midribs
of the leaves turn yellow, the reddish brown spots appear around the discolored parts
until the whole leaf becomes reddish brown. Sometimes the yellow discoloration does
not occur. The disease occurs in ill drained soil. Akagare type 3 occurs in lowland
rice soils newly converted from upland: Such soil is usually acid and low in phosphorus.
55
Recent reports have claimed that akagare type 3 is caused by iodine toxicity (Tanaka
and Yoshida [1970], Baba et al. [1965]).
Another disease in Japan is aogare (green withering). Plants suddenly wither 20 days
or more after heading. The disease is aggravated by drainage, typhoon, dry wind and
cool air also. It occurs in well drained sandy soils (Tanaka and Yoshida [1970], Baba
et al. [1965]).
Amyit-po disease in Burma is due to low potassium and high iron. The disease occurs
on alkaline, strongly reducing heavy clay soils. The affected plants appear dark green
at tillering and subsequent growth is retarded. The lower leaves tend to drop off. The
affected plant gives a low yield with poor grain filling (Takahashi [1960b], Tanaka
and Yoshida [1970], Aiyar [1950]).
Pansuk is a physiological disease in Pakistan. Affected plants are reported to be low in
potassium and with unbalanced potassium-nitrogen and iron-manganese ratios.
Affected plants show reddish yellow discoloration of the leaves, starting from the tips.
The disease is associated with stagnant water and can be partly cured by improving
drainage. The condition results in low yield with poor grain filling (Takahashi [1960a],
Tanaka and Yoshida [1970], Kanwar and Sehgal [1966)).
Bronzing diseases have been reported in India and Sri Lanka. In India, affected plants
have low potassium, phosphorus and manganese contents but are high in iron.
Application of lime, potassium, phosphorus and drainage can cure the disease.
Discoloration and brown spots and streaks appear on all aerial parts, including the
leaf sheaths, flag leaf and some grains. The disease occurs in low pH waterlogged
latosol soil. The disease was also observed in soil with about neutral pH and sandy
clay loam in texture. The plants are low in potassium and phosphorus and high in
manganese (Sahli [1968], Tanaka and Yoshida [1970)).
Bronzing disease in Sri Lanka is characterized by the appearance of small brown spots
in the dark green leaves, starting from the tips of lower leaves, later spreading downwards. The tints of the affected leaves vary with variety. In severe cases the brown
discoloration appears even on the uppermost expanded leaves. It is very probably due
to iron toxicity but sometimes claimed to be due to combined high aluminium and low
calcium in the soil. The presence of hydrogen sulphide aggravates the disease incidence.
Potassium fertilizer, followed by phosphate fertilizers and slag, is effective in promoting
growth and yield of rice. However, even the use of balanced NPK fertilizer did not
entirely eliminate the bronzing symptoms. Air drying and liming increase rice production and prevent bronzing. A combination of these with increased use of potassium
fertilizer and slag is recommended as the most effective measure (Inada [1966a and b],
Yamada [1959], Tanaka and Yoshida [1970), Takijima and Kanaganayagam [1970],
Ponnamperuma et al. [1955], Ponnamperuma [1958], Ota and Yamada [1962]).
The cause of mentek disease, known in Indonesia since the end of the nineteenth
century is not yet clearly determined, being variously ascribed to nematode, virus,
strongly reductive conditions in the soil, potassium and phosphorus deficiency, root
rot, too many cloudy days and bad cultural practices.
The term 'mentek' describes symptoms including stunting, leaf discoloration from
yellow through orange or reddish to brown, and rusty spots on the leaves. In many
cases the roots are poorly developed or rotten. Recent findings indicate that mentek
disease in East Java (Ngale) was due to sulphur deficiency (Kiulman [1935/1936,
1936], Vecht [1953], Tanaka and Yoshida [1970], Tanaka et al. [1970], Ismunadji
[1975]).
56
In 1970 a similar disease was reported in Cihea, West Java and was called mentek or
mutut disease. In severe cases almost all the leaves turn brown, a quite characteristic
discoloration suggesting that mentek or mutut should be termed bronzing disease.
Affected plants are low in potassium and high in iron and, sometimes, also high in
manganese (Ismunadji et al. [1973]).
4.2. Bronzing disease in Cihea
4.2.1. Some features of the problem site
Cihea is located in Cianjur, West Java,about 120 km Southeast of Jakarta with an
elevation of about 270 m above sea level. There are two main seasons, the wet season
from November to February and a relatively dry period from May to September.
Average annual rainfall over the period 1961-1970 was 2310 mm. The mean daily
maximum temperature is about 30°C and mean minimum about 23°C. Rice is grown
under irrigation.
The soil of the problem field is grumusol containing the high swelling clay mineral
montmorillonite, the pH 5.68 and it is strongly reductive. Soil samples taken at 22 cm
depth consist of sand 3.8%, silt 42.0% and clay 54.2%. Soil analysis of the problem
field indicates that potassium content is low and manganese content is high (Tanaka
et al. [1970]).
4.2.2. Symptoms of the disease
Early in growth the plants are dark green to blue-green in colour. Tillering is little
reduced. At tillering the lower leaves turn orange or brown, first at the tips and then
spreading down towards the leaf base. The discoloration is often accompanied by
many tiny rusty spots, especially at the leaf tips. The main vein and surrounding tissue
sometimes remain green. Later in growth the discoloration of the lower leaves becomes
more pronounced and, in severe cases, the entire leaf blade 'becomes brown and
subsequent growth is retarded. Eventually the affected leaves dry up and die and in
extreme cases almost all the leaves turn brown. Sometimes, small purplish brown spots
are found on the veins of the leaf and on leaf sheaths, especially of the lower leaves.
The roots of affected plants are poorly developed. Yield is low with the panicles
poorly developed, many empty grains and low 1000 grain weight. The disease occurs
in both wet and dry seasons.
4.2.3. Nutrient status of rice and bronzing disease
The relationship between the nutrient status of rice and the occurrence of bronzing
disease in Cihea has been the subject of a recent report (Ismunadji et al. [1973]). The
disorder seemed to be due to low potassium which induced iron toxicity and, in terms
of visual symptoms, metal 'toxicity seems to be the dominating factor. The soil is
high in manganese and relatively high plant Mn contents are sometimes found. A
consequence of the browning of the leaves is that photosynthetic activity is drastically
reduced due to reduced chlorophyll content, and the balance between photosynthesis
and respiration is disturbed. Accumulation of carbohydrate in the grain is much
reduced and the synthesis of other organic compounds in the plant, both quantitatively
and qualitatively, is disturbed. This explains the reduction in yield due to poor grain
filling and low 1000 grain weight.
There is evidence that under strongly reducing conditions in the soil, potassium
57
uptake by rice is depressed. On flooding of the paddy the redox potential of the soil
reduces with time, reaching a minimum about one month after flooding (Ponnamperuma [1955, 1965]) after which it remains at a constant low level. The consequence
is that the availability of potassium applied as fertilizer in the basal dressing reduces
during the growth of the rice. At the same time the ferrous iron content of the soil
increases due to reduction from the ferric state and this results in excess Fe uptake
at tillering. Strongly reductive conditions are found in the Cihea soil and the situation is
aggravated by the high soluble Mn content of the soil. Plant analysis confirmed that
the plants were low in potassium, high in iron and frequently high in manganese.
4.2.4. The effect ofpotassium fertilizer on bronzing symptoms
It has been shown that the application of potassium fertilizer to a grumusol area in
Cihea could double the yield of rice (!smunadji [1973]). The problem has been further
studied in an experiment carried out during the 1975-1976 wet season at Ciranjang
near Cihea in which the effect of treatment on the severity of bronzing symptoms was
studied. The experiment was sited in an area where bronzing symptoms usually occur.
Iron content of the straw at harvest was used as a criterion, since the symptoms of
bronzing were considered to be mainly due to excessive iron uptake. Table 12 shows
clearly that potassium had a marked effect in reducing the iron content of the straw
and, also, that it increased the grain yield significantly.
Table 12. Effect of potassium on K and Fe contents of rice straw at harvest. cV. JR26. Ciranjang,
1975-1976 wet season
Treatment (kg/ha)
N
P20 S
K 20
0
120
120
120
120
120
120
120
60
60
0
30
60
90
120
150
60
0
60
60
60
60
60
60
%K
ppm Fe
Yield index
1.30
0.93
0.58
0.77
0.96
1.06
1.18
2.02
637
1422
1I05
651
478
792
738
535
lOO
140
1I1
142
136
159
156
154
*) CRJA - P.T. Pupuk Sriwidjaja cooperative research.
A further experiment, conducted concurrently, studied the effect of potassium on
bronzing on a number of varieties of rice. The site chosen was one where bronzing
invariably occurs and five varieties and one selection were tested. Yield data and K and
Fe contents of the straw are detailed in Table 13. Again, potassium had a marked
effect in increasing yield and in reducing Fe content and, thus, severity of the bronzing
symptoms. There was considerable variation in the susceptibility of varieties to
bronzing; IR 22, IR 26 and B9c-Md-3-3 were particularly sensitive, while Perlita 1/1
and IR 34 seemed more tolerant.
The experimental results so far obtained indicate that 'mentek' or bronzing disease in
Cihea is due to excessive iron and manganese uptake from the strongly reducing soils
and that the application of potassium fertilizer has a marked effect in reducing iron
uptake to tolerable levels, thus reducing the severity of the condition and substantially
increasing yield.
58
Table 13. Effect of potassium on bronzing disease of six rice varieties/selection. Cihea, J975-1976
wet season
Variety/selection
Treatment
%K
ppm Fe
Yield .index
Pelita J/I
N
NP
NPK
NPK 2
0.47
0.47
0.66
0.86
43J
564
550
420
lOO
139
157
186
IR20
N
NP
NPK
NPK 2
0.66
0.51
0.93
1.12
464
707
525
485
lOO
86
107
114
IR22
N
NP
NPK
NPK 2
0.62
0.47
0.94
1.18
987
1187
1043
622
lOO
86
134
148
IR26
N
NP
NPK
NPK 2
0.43
0.51
0.75
1.43
1106
779
741
549
lOO
133
176
179
IR34
N
NP
NPK
NPK 2
0.47
0.39
0.77
0.93
477
511
371
453
lOO
161
208
240
B9c-Md-3-3
N
NP
NPK
NPK 2
0.66
0.47
0.69
1.58
1727
1954
1163
.980
lOO
134
168
193
Acknowledgement
The author wishes to express his profound thanks to Dr. H. R. von Uexkull, Regional
Director East and Southeast Asia Program of the Potash Institutes, for his special
attention and valuable support during the preparation of the manuscript, also to
Dr. M.Kosim Kardin and Dr. Sudjadi, Central Research Institute for Agriculture, fOf
identification and scoring of rice diseases in Jakenan and Cihea.
References
1. Aiyar, S.P.: Straw manuring in relation to Amyit-po disease of rice. Proc. Ind. Acad. Sci,
Sect. B 31 (3), 181-192 (1950).
2. Akai, S.: Potash application and occurrence of Helminthosporium (Cochliobolus miyabeanus)
leaf spot on rice. Potash Review, Subj. 23, 27th Suite (1962).
3. Baba, I., Inada, K. and Tajima, K.: Mineral nutrition and the occurrence of physiological
diseases. In: The mineral nutrition of the rice plant, Johns Hopkins Press, Baltimore, p. 173-195,
1965.
4. Devadath, S. and Padmanabhan, S. Y.: Approaches to control of bacterial blight and streak
disease of rice in India. Indian phytopath. Soc. Bull. 6, 5-12 (1970).
5. Inada, K.: Studies on the bronzing disease of rice plant in Ceylon. 1. Effect of yield treatment
on bronzing occurrence and changes in leaf respiration induced by the disease. Trop. Agriculturist 122, 19-29 (1966a).
59
6. Inada, K.: Studies on the bronzing disease of rice plant in Ceylon. 2. Cause of the occurrence
of bronzing. Trop. Agriculturist 122,31-46 (l966b).
7. Ismunadji, M., Hakim, L.N, Zulkarnaini, 1. and Yazawa, F.: Physiological disease of rice in
Cihea. Contr. Centr. Res. Inst. Agric. Bogor 4, 1-10 (1973).
8. Ismunadji, M., Zulkarnaini, 1. and Miyake, M.: Sulphur deficiency in lowland rice in Java.
Contr. Res. lnst. Agric. Bogor 14, 1-17 Cl 975).
9. Jackson, W.A. and Volk, R.J.: Role of potassium in photosynthesis and respiration. In: The
role of potassium in agriculture, ed. by V.J.Kilmer, S.E. Younts and N C.Brady. Amer. Soc.
Agron., Crop Sci Soc. Amer. and Soil Sci Soc. Amer., p. 109-145, 1968.
10. Kanwar, J.S. and Sehgal, J.L.: A note on the chemical composition of leaves from healthy
plant as compared with plants affected by Pansukh disease in rice. Intern. Rice Comm.
Newsletter 15 (4),24-25 (1966).
11. Kozaka, T.: Control of blast by cultivation practices in Japan. In: The rice blast disease. IRRI,
Johns Hopkins Press, Baltimore, Maryland 20, 507 p., 1965.
12. Kuilman, L. W.: The investigation on the mentek disease of rice. Landbouw 11, 77-113 (1935/36).
13. Kui/man, L. W.: Symptoms of mentek disease of the rice plant. Landbouw 12, 225-245 (1936).
14. Liebhart, W. c.: Effect of potassium on carbohydrate metabolism and translocation. In: The
role of potassium in agriculture, ed. by V.J.Ki/mer, S.£. Younts and N C. Brady. Amer. Soc.
Agron., Crop Sci Soc. Amer. and Soil Sci Soc. Amer., p. 147-164, 1968.
15. Noguchi, Y. and Sugawara, T.: Potassium and Japonica rice. Intern. Potash Inst., 102 p., 1966.
16. Okamoto, H.: Relation between rice blast (pyricularia oryzae) and sesame leaf spot (Ophiobolus
miyabeanus) and potassium. Second Japenese Potassium Symposium, Tokyo. Intern. Potash
Inst., p. 76-89,1958.
17. Ou, S. H.: A handbook of rice diseases in the tropics. IRRI, Los Banos, Philippines, 58 p., 1973.
18. Padhi, S. C. and Mishra, A.: Effect of potash top dressing in reducing bacterial leaf blight of
r.ice. Farm Journal 13, 7 (1972).
19. Park, Y.D. and Tanaka, A.: Studies of the rice plant on an Akiochi soil in Korea. Soil Sci
Plant Nutr. 14 (I), 27-34 (1968).
20. Ponnamperuma, F.N.: The chemistry of submerged soils in relation to the growth and yield of
rice. Ph. D. Thesis,·Cornell Univ., 208 p., 1955.
21. Ponnamperuma, F. N.: Lime as a remedy for physiological disease of rice associated with excess
iron. Intern. Rice Comm. Newsletter 7 (I), 10-13 (1958).
22. Ponnamperuma, F.N.: Dynamic aspects of flooded soils and the nutrition of the rice plant. In:
Mineral nutrition of the rice plant. Johns Hopkins Press, Baltimore, p. 295-328 1965.
23. Ponnamperuma, F.N, Bradfield R. and Peech, M.: Physiological disease of rice attributable to
iron toxicity. Nature 175, 265 (1955).
24. Sahu, B. N.: Bronzing disease of rice in Orissa as influenced by soil types and manuring and its
control. J. Ind. Soil Sci 16 (I), 41 (1968).
25. Takahashi, J.: Review of investigations into physiological diseases of rice 1. Intern. Rice Comm.
Newsletter 9 (I), 1-6 (I 960a).
26. Takahashi, J.: Review of investigations into physiological diseases of rice 2. Intern. Rice Comm.
Newsletter 9 (2), 17-24 (I 960b).
27. Takijima, Y. and Kanaganayagam, M.: Nutrient deficiency and physiological disease of lowland
rice in Ceylon. 4. Remedy for bronzing disease of rice. Soil Sci Plant Nutr. 16 (1),17-23 (1970).
28. Tanaka, A., Okajima, H., Shikata, £. and Yamada, Y.: A note on nutrional disorders of the
rice plant .in Java, Indonesia. The Southeast Asian Studies 8 (3), 418-426 (1970).
29. Tanaka, A. and Yoshida, S.: Nutritional disorders of the rice plant in Asia. IRRI Techn. Bull.
10,51 p. (1970).
30. Uexkull, H.R. von: Rice diseases and potassium deficiency. Better Crops 50 (3), 28-35 (1966).
31. Vecht, J. van der: The problem of the mentek disease of rice in Java. Landbouw 25, 45-130
(1953).
.
32. Yamada, N: Some aspects of physiology of bronzing. Intern. Rice Comm. Newsletter 8 (3),
11-16 (1959).
33. Yoshi, H., Koba, S. and Watanabe, B.: On the scale for estimating degree of damage in rice by
stem rot. Annals of the phytopath. Soc. Japan 8 0/4), 19-22 (1949).
34. Yoshida, M.: On Cercospora leaf spot disease of the rice plant. Hiroshima Agriculture 1 (I),
4-11 (1948) (in Japanese).
60
The Effect of Potassium on Catabolism of Rot Infected
Apple Fruit Callus
Dr. F. A. Schulz, Institute of Phytopathology, University of KielfFederal Republic of Germany
Summary
To eliminate the influenc~ of variable ecological factors on the physiological status of the apple fruit,
the effect of potassium nutrition on biochemical alterations during pathogenesis of Pezicula malicorticis was studied in callus culture gro\yn from Cox's Orange apple fruits. Optimum growth of the
callus was obtained with about 40 mM K. The occurrence of pectinolytic and cellulolytic enzymes
was followed by viscosimetric and electrophoretic methods. Increased K concentrations in a liquid
medium had no stimulatory influence on formation of endo-PM G, the key enzyme in pathogenesis of
P. malicorticis. In contrast, in the early phases of pathogenesis there was evident improvement of
formation of this catabolic enzyme in infected callus grown under a regime of 40-120 mM K. The
formation of ~-glucanase was reduced by the same increasing K concentrations in both liquid culture
and rotted callus.
Resume
En vue d'eliminer l'influence de facteurs ecologiques variables sur I'etat physiologique des fruits du
pommier, on a etudie l'effet de l~ nutrition potassique sur les changements biochimiques au cours de
la pathogenese de Pezicula malicorticis. A ces fins on a utilise des cultures de callus provenant de
pommes de la variete Cox Orange. La croissance optimale du callus fut obtenue avec environ
40 mM de K. L'apparition d'enzymes pectinolytiques et cellulolytiques fut etudiee au moyen de
methodes viscosimetriques et electrophoretiques. L'augmentation des concentrations de K dans un
milieu Iiquide n'eut pas d'effet stimulant sur la formation d'endo-PMG, l'enzyme-clef de la pathogenese de P. malicorticis. Par contre, au cours des premieres phases de la pathogenese il y avait
amelioration nette de la formation de cette enzyme catabolique dans les callus infestes qui furent
cultives sous un regime de 40 it 120 mM de K. La formation du ~-glucanase fut rectuite par les memes
conCentrations croissantes de K et ceci aussi bien en culture liquide que dans le callus pourri.
1. Introduction
There are various reports available on the influence of minera:I fertilization on plant
diseases. These are mainly concerned, however, with the effect of ilitrogen and potassium fertilizers on disease development in field crops. The effect of plant nutrition,
particularly of K fertilization, on the occurrence and severity of plant diseases in horticultural plants is almost unknown except for the physiological disorders in pomaceous
fruits (e.g. Bii.nemann and Ladders [2]). At the present time little information is
available on the relationship between the essential macronutrient potassium and the
occurrence of fungal fruit rots of apple and these data are not in complete agreement.
Most information is available on the importance of K for susceptibility to rotting by
Pezicula malicorticis (Jacks.) Nannf. (stat. conid. Cryptosporiopsis malicorticis (Cord!.)
Nannf.), the causal agent of Gloeosporium fruit rot. This fungal parasite is known for its
latent infection. Montgomery and Wilkinson [11] reporting on their long-term field
experiments with apple (cv. Cox's Orange) in England, found considerable increases
in rotting after K application. They observed, however, that the higher susceptibility
following natural contamination decreased after some years experimentation. The host
reaction was not stable. Nyhlen [13] as well as Olsson [14] in Sweden working with
P. alba Guthrie, another fungus of the Gloeosporium fruit rot complex, found no
regularly stimulated disease incidence or rotting following supplementary K fertilization. In some years and on some fruit farms there was a positive correlation between
high K application to apples and rotting and in others there was not.
In older field experiments, Musket! et al. [12] already described the similar contradictionary results that manuring with K in one year lowered resistance and in the following year increased resistance of apples against Cytosporina ludibunda which was used
as a fruit rotting test organism.
In perennial plants the influence of ecological factors is usually very complex so that
results of fruit pathological experiments or observations are- difficult to interpret.
Tissue culture therefore would seem to be an excellent, time saving tool for investigating host-parasite-relationships. This is not only true for obligate parasites (Ingram
[7]). The possibility of growing apple fruit callus and its use for at least some pathophysiological questions has just been studied (Krohn and Schulz [9]). The importance
of extracellular enzymes for pathogenesis of P. malicorticis was extensively studied in
earlier experiments (Schulz [16], Koch and Schulz [8]). The following investigation
was undertaken to elucidate some possible biochemical consequences of K fertilization
for pathogenesis in this disease under defined conditions.
2. Experimental
A slightly modified Nitsch medium was used for callus culture (Krohn and Schulz
[9]). Potassium was applied as KN03. and KHzP04 to give 20 mM K. The additional
K as given as KCl. A mixture of sucrose and sorbitol was used as C source. The pH of
the medium was adjusted to 5.5. The explants were prepared from the fruit tissue of
ripe apples (cv. Cox's Orange). Incubation was in the dark.
P. malicorticis (ATCC 26206) was grown on a liquid glucose-nitrate-medium of Olsson
[14] as the standard; supplementary K was added as KCI or KOH resp. The culture
filtrates were used without any further preparation for enzyme studies. The inoculation
of the callus tissue was done by placing a drop of a spore suspension obtained from a
young plate culture on top of an injured callus. The inoculated fruit callus was incubated at 25°C in the dark. For enzyme analysis the rotted callus was extracted by
various buffers or water followed by 30 min dialysis against distilled water in the cold.
The pectinolytic and cellulolytic enzyme activities of the culture filtrates and of both
healthy and rotted callus extracts was determined viscosimetrically by using apple
pectin and carboxymethylcellulose resp. as the test medium (Schulz [16]). The test
solution consisted of a 1 : 1 mixture of substrate and enzyme preparation. The electrophoretic determination of the qualitative composition of the endo-PMG was made on
PAA-gels stained with methylene-blue (Koch and Schulz [8]).
62
3. Results
3.1. Growth pattern of apple fruit callus
The influence of different K concentrations on the growth of apple fruit callus is shown
in Figures I and 2. The growth pattern is the same for all K concentrations tested.
After a lag phase of 3-4 days the transplants start swelling as a result of cell elongation
in the peripheral area. The first callus formation can be seen after a further 3 days in
the form of small yellow pustules which rapidly enlarge (Figure 3). The healthy callus
remains yellow for about 4 weeks, after which it sometimes shows a light browning.
Normally the callus is soft.
Potassium has a significant influence on caIJus growth. Without any K there is no
growth at all. The optimum growth is obtained with about 40 mM K in the medi.um as
can be seen from both fresh and dry weight per callus. The higher growth not only
depends on cell enlargement but also on cell multiplication. With increasing K
concentration in the medium the callus becomes harder.
600
..-.. 400
01
g
3"
I
I
~
,
..
,,
"6
u
-..
,
,
I
I
I
~
I
,,
I
1
I
.t= 200
I
I
4
."
10
0
0
20
30
days of incuoation
Fig. I. Growth pattern of apple fruit callus (cv. Cox's Orange) under the influence of increasing K
concentration in the medium. - (1) 20 mM K, (2) 35 mM K, (3) 98 mM K, (4) 155 mM K.
63
600
~
01
400
40
g
~
lf)
-..........
:J
0
-'
..'::
Ul
g
\
u
3
~
lf)
.2
20 0
.!2
\
200
~
-'
--,.
:>
C'
'\
u
IS
40
80
120
160
K concentration (mM)
Fig_2. InOuence of increasing K concentration on the fresh and dry weight production of 30 day old
apple fruit callus.
Health) (upper) and Pe:ic/lla lIIalicunicis inoculated (Io\\er) apple fruit callu, (c\. Cox',
Orange).
Callus age:15 da)s. Inoculation after 28 da)s callu,> gro\\th.
Fig.]
64
3.2. Formation of catabolic enzymes
Previous investigations showed the importance of pectin degrading enzymes of
P. malicorticis for disease incidence and rotting.
The present experiments demonstrate the role of K in the formation of endopolymethylgalacturonase (endo-PMG) and ~-glucanase. Under in-vitro conditions, increasing K concentration in the medium appears to have no direct effect on endo-PMG
production as illustrated in Table 1. Without any K there is no growth of the fungus
and no enzyme production. After 14 days incubation, the time for maximum enzyme
formation, no difference can be seen in the degradation of the pectin substrate. Only
the inactivation of the enzyme after 21 days growth seems to proceed somewhat faster
with higher K concentrations. No differences in enzyme formation can be observed
between the anions Cl or OH. In contrast to the endo-PMG there is a significant
reduction in the production of ~-glucanase depending on the K concentration in the
same medium, which can still be seen after 3 weeks growth. The form of potassium,
KCl, KOH or organic form, has no visible influence on the activity of endo-PMG if
tested in increasing concentrations by viscosimetry.
If the hydrolyzing enzymes are extracted from rotted apple callus the picture is different.
Table 2 illustrates that K, at least in the early stages of pathogenesis of P. malicorticis,
has an evident influence on the formation endo-PMG which is the most important
catabolic enzyme responsible for the degradation of the complex pectin. With pro-
Table 1. Influence of K content and age on the formation of endo-polymethylgalacturonase (endoPMG) and ~·glucanase by Pezicula malicorticis.
age
(days)
endo-PMG"
14
22
63.1 d
61.8
20
c
~-glucanaseb
35
98
20
35
98
61.9
.51.3
62.6
46.7
12.3
30.8
5.6
13.3
4.3
10.6 .
b 90 min incubation of a pectin solution at pH 4.5 and 30'C
" the same as above by using carboxymethyIcellulose as the substrate
c mM K in the culture medium
d reI. reduction of viscosity of the test solution under the influence of the pathogen
Table 2. Formation of endo-polymethylgalacturonase. (endo-PMG) and~-glucanase by Pezicula
malicorticis on apple fruit callus grown under various K regimes
age
(days)
endo-PMG"
7
14
21
19.1 d
53.2
61.7
20
c
~-glucanaseb
35
98
20
35
98
48.8
68.3
63.4
37.1
62.9
61.1
65.0
32.7
30.2
68.9
22.6
13.3
69.0
22.4
20.6
" 90 min incubation of a pectin solution at pH 4.5 and 30'C
b the same as above by using carboxymethyIcellulose as the substrate
d mM K added to the culture medium
.
c reI. reduction of viscosity of the test solution containing an aq. extract of the rotted callus tissue
65
gressing disease development the stimulatory effect of K on endo-PMG production is
lost so that after 3 weeks incubation differences between the various K regimes in the
medium are no longer evident. The situation is somewhat different for ~-glucanase
which is initially present in rather large amounts independent of K nutrition. Later, the
cellulase content of the diseased callus is generally reduced and increasingly so at
higher K concentrations in the growth medium.
That the qualitative composition of the endo-PMG from diseased apple fruit callus
depends on the K nutrition of the callus can be seen from Figure 4. It clearly shows in
the intensity and size of the unstained areas that K nutrition actually has a positive
effect on the quality and quantity of the enzyme under these experimental conditions
thus confirming the results of viscosimetry described above. By further separation of
the callus extracts it is found that in the range of 35-95 mM K at least 4 bands are built
up compared to 2 bands at 20 and )55 mM K resp. The dark bands in Figure 4
illustrate the presence of pectinmethylesterase (PME) whose formation is partially
reduced in contrast to the improved production of the chain-splitting endo-PMG.
Fig.4. Formation of isoenzymes of endo-polymethylgalacturonase (endo-PMG) by Pezicula
malicorlicis on apple fruit callus depending on the K nutrition of the callus medium. - From left:
duplicates of each 20, 35,98, 155 mM K-medium. 450 V, 50 mA, 60 min run.
66
4. Discussion
As in annual plants, K may be. supposed to have an effect on predisposition against
fungal diseases in perennial plants and their various parts. However, information is
very scarce and not in full agreement, at least regarding fruit rots. Stimulation as well
as reduction of resistance have been described (Wilkinson and Montgomery [11],
Musket! et at. [I2]). Without further specialization Biinemann and Liidders [2] found
from pot experiments with Cox's Orange that high K availability during spring and
summer increases the 'loss due to fungal rots. Similar increased susceptibility to
Centrospora acerina is also reported for carrots (Roll-Hansen [15]). In other investigations Edney and Perring [3] and Edney [4) sometimes found a positive correlation
between the higli K content of ripe apples from heavily attacked fruit farms and the
high percentage of rotting, while Borecka [1) was unable to confirm this correlation.
These problems require further investigation since it is not clear whether the higher K
. content of the fruits is the cause or, possibly, the effect of the fungus attack.
This variable reaction could be due to the. complex physiological behaviour of fruit
trees in relation to various ecological factors, e. g. plant age, climate and plant nutrition.
The successful growing of apple fruit callus under controlled conditions and simultaneous testing of the effect of K on callus growth has made it possible to eliminate
these influences. At constant Ca and N contents in the medium a positive effect. of
various K regimes on the callus development can be obtained. This agrees with t.hefact
that high K application during the vegetation results in the highest individual fruit
weight and the best total yield (Li1dders and Biinemann [10]).
At the moment there is no ready specific explanation for the increased rotting under
these manurial conditions. It is assumed that the rotting depends on the production of
larger fruits following K fertilization (Olsson [14]). However, we never found a
positive correlation between fruit size and disease incidence of P. malicorticis under
field conditions (Schulz [17]). This could only be obtained after artificial" inoculation at
the same moment. Supposing a high inoculum to exist at a time favourable for infectino
it could actually lead to increased rotting by this pathogen so that the occasional
higher rate of rotting could be explained under certain circumstances. We need to investigate whether this result can be generalised to other fruit rotting fungi.
It is concluded from the results presented here that K nutrition acts indirectly on the
susceptibility of the fruit by altering the carbohydrate and cell wall metabolism. The
regulation of the production of the most important pectinase largely depends on the
carbohydrate concentration in the growth medium (Schulz [17]). Furthermore, if
there is an imbalance between K and Ca because of the additional K manuring, the
structure of the cell wall may differ from normal so that the fungus attack is actually
facilitated.
5. Bibliography
1. Borecka, Halina: Cryptosporiopsis malicorticis (Zeller et Childs) Wollenw. (syn. Gloeosporium
perennans Zeller et Childs) as a pathogen on apple in the storage time. Acta agrobot. 12, 13-66
(1962) (pol.).
2. Biinemann, G. and Liidders, P.: Die Wirkung jahreszeitlich unterschiedlicher Kaliumverfiigbarkeit auf Apfelbaume. VI. Einfluss auf Fruchterkrankungen. Gartenbauwiss. 40, 208-214 (1975).
3. Edney, K. L. and Perring, M. A.: Study of farms with high incidence of Gloeosporium infection.
Rep. E. Mailing Res. Sta. 1972, 157 (1973).
67
4. Edney, K.L.: An investigation of persistent infection of stored apples by Gloeosporium spp. Ann.
appl. BioI. 82, 355-360 (1976).
5. Evans, H.J. and Sorger, G.J.: Role of mineral elements with emphasis on the univalent cations.
Ann. Rev. PI. Phys. 17, 47-76 (1966).
6. Evans, H.J. and Wildes, R.A.: Potassium and its role in enzyme activation. In: Potassium in
biochemistry and physiology. 8th Coil. Intern. Potash Inst., Berne (Switzerland) 13-39 (1971).
7. Ingram, D. S.: Growth of plant parasites in tissue culture. In: Plant tissue and cell culture. Ed.:
Street, H.E., 392-421, Blackwell Sci. Pub!., 1973.
8. Koch, O. and Schulz, F.A.: Einftuss okologischer Parameter auf die Bildung multipler Formen
von Pektinasen durch Pezicula malicorticis in vitro. Phyto. Z. 81, 184-187 (1974).
9. Krohn, P. and Schulz, F.A.: Moglichkeiten des Einsatzes von Kalluskulturen zur Untersuchung
von Fruchtfiiulen. (In preparation).
10. Liidders, P. and Biinemann, G.: Die Wirkungjahreszeitlich unterschiedlicher Kaliumverfilgbarkeit auf Apfelbaume. Ill. Einfluss auf das generative Wachstum. Gartenbauwiss. 39, 69-84 (1974).
I!. Montgomery, H.B. S. and Wilkinson, B. G.: Storage experiments with Cox's Orange Pippin apples
from a manurial trial. J. hort. Sci. 37, 150-158 (1962).
12. Muskett, A.E., Home, A.S. and Colhoun, J.: The effect of manuring upon apple fruits. Ann.
appl. BioI. 25; 50-67 (1938).
13. Nyhlen, A.: Refrigerated storage of some apple varieties 1952-1956. Frukt i ar 60, 91-110 (1959)
(Sweden).
14. Olsson, Karin: A study of the biology of Gloeosporium album and G.perennans on apples. Meddn.
St. Vaxtskyddanst. 13 :104, 189-259 (1966).
15. Roll-Hansen, J.: Fertilizer experiments with carrots on peat soil. Forskn. fors. landbr. 25,
201-218 (1974).
16. Schulz, F.A.: Untersuchungen liber die Bildung pektinolytischer und zellulolytischer Enzyme
durch Gloeosporium perennans. Phyto. Z. 74,97-108 (1972).
J7. Schulz, F. A.: Ein Beitrag zum Problem der Gloeosporium-Faule an Apfel (Pezicula malicorticis
(Jacks.) Nannf.). Habil. Schrift., 269 pp., Kiel (1975).
18. Sharples, R. 0.: The structure and composition of apples in relation to storage quality. Rep. E
Mailing Res. Sta. 1966, 185-189 (1967).
These investigations were gratefully supported by Deutsche Forschungsgemeinschaft,
Bonn-Bad Godesberg, Federal Republic of Germany.
68
The Effect of Nitrogen Fertilizers on Growth of Cereals
and the Impact on Diseases
M. M. El-Fouly, Dr.-agr., Associate Professor, Botany Laboratory, National Research Centre,
Cairo-DokkijEgypt *
Summary
Nitrogen fertilization causes positive changes in growth and yield of cereals, which sometimes could
have negative impacts on the occurence of physiological lodging as well as of the attack with Cercosporella. Through managing N-source and time of application, this could be partially overcome.
Adequate potassium nutrition causes anatomical changes which are opposite to those caused by N
and thus helps in increasing culm stability.
Recently, the use of the growth substance Chlormequat (Cycocel, CCC) in cereal production opened
new possibilities of using \:1igher nitrogen supply, without fearing negative effects on disease attack.
However, CCC treated cereal plants under certain conditions showed higher infection with ear diseases, especially Sepforia. A new package approach is using CCCand a systemic fungicide to overcome drawbacks resulting from growth changes due to high N-supply.
Promotional effects of high N doses on fungal diseases in cereals are especially relevant when the
nutrient supply is unbalanced. This in particular is true for potassium, which favours the formation
of cell wall material. It is supposed that thicker cell walls hamper the penetration of hyphae into the
host cell.
Resume
La fumure azotee provoque des changements dans la croissance et les rendements des cereales, ce qui
peut avoir des consequences negatives concern ant la verse physiologique et I'attaque par
Cercosporella. Par la determination adequate de la source de N et de I'epoque d'application des
engrais azotes, ces effects negatifs peuvent etre partiellement evites. Recemment, I'emploi de
Chlormequat (Cycocel, CCC) - une substance de croissance - dans la production cerealiere a ouvert
des possibilites nouvelles en'vue d'un~ intensification des fumures azotees sans qu'il y ait augmentation simultanee du danger d'attaque par les maladies. Toutefois, dans certaines conditions, les
plantes traitees au CCC montrerent de plus fortes attaques par les maladies des epis, particulierement par Sepforia. Un nouveau «paquet» de mesures de ce genre est constitue par I'utilisation conjointe de CCC et d'un fongicide systemique en vue d'eviter les effets negatifs resultant des changements de la croissance qui apparaissent a la suite d'une forte fumure azotee.
L'effet de fortes-doses de N sur I'intensification des maladies cryptogamiques chez les cereales est
particulierement fort, lorsque I'approvisionnement en elements nutritifs est desequilibre. Ceci est
vrai particulierement en ce qui concerne le potassium qui favorise la formation des materiaux de
structure des parois cellulaires. L'on suppose que des parois cellulaires plus epaisses empechent la
penetration des hyphae dans la cellule-hote.
*
Research Fellow of the Alexander v. Humboldt Foundation, Lehrstuhl fUr Pflanzenernahrung,
TU Munchen-Weihenstephan/FRG.
69
1. Introduction
Detailed reviews on the effect of nitrogen and its different forms on the succeptibiJity
and resistance to diseases were published recently (Bockmann et al. [B), Banning [9},
Fuchs and Grossmanll [l4}, Huber and Watsoll [l6}).
Nitrogen fertilization in modern intensive cereal production is very essential to obtain
highest yields. Bockmann et al. [B} reported about possibilities of reaching grain
yields of eight tons per hectar of winter wheat, summer wheat as well as winter barley
through intensifying nitrogen fertilization persuming that other nutrients are sufficient.
However, high nitrogen supply needed for obtaining high yields causes growth changes,
which sometimes show different negative impacts on disease attack (Fuchs and Grossmann [l4}).
2. Effects of nitrogen
Mulder [24} examined the effects of nitrogen fertilizers on cereal growth and their
relation to the appearance of 'physiological' lodging. Ample nitrogen in form of
calcium ammonium nitrate resulted in longer lower internodes and increased diameter
of the upper internodes, while that of the lower ones did not show any change or
even decreased. In cases, in which plants lodged, culm wall thickness was decreased.
Linser [22} reported that increasing physiological lodging resulting from high Nsupply is apparent, only when the N-dose used increases yield. In case of having any
other limiting factor, increasing N-dose did not show any effect on lodging.
..
Nitrogen induced changes in cereal growth and culm structure also influence the
attack with Cercosporella herpotrichoides causing eye spot disease. According to
Bockmann [5}, excess nitrogen in fOlm of calcium ammonium nitrate in winter wheat
led to decreases in Cercosporella attack in light stands, whereas in close stands the
attack was increased. Also Salt [29} found that those N-doses, applied at different
times, which increased tillering caused more attack with Cercosporella. Different
N-forms had different effects upon the Cercosporella attack in spring wheat, which
could be correlated to growth differences (Au/hammer et al. [3}). Ample N in form
of calcium ammonium nitrate or calcium nitrate increased tillering by 28% compared
to the same amount of N as calcium cyanamid. This increase in tillering was
significantly correlated with increased Cercosporella attack. Other growth changes due
to calcium cyanamid than decreasing tillering, like clo~er ratio of total fresh
weight to dry weight of the lower parts of each tiller, short plants, short basal internodes and large number of adventitious roots could contribute to this positive effect
of this form of N-fertilizers (Bauer [4}). It it also worthy to mention that calcium
cyanamid exerts a direct effect on the growth and metabolism of C. herpotrichoides
(Amberger [I}). However, the possibilities of managing negative effects of high
N-doses through using calcium cyanamid are limited (Bockmann and Knoth [7}).
Changes in growth induced by high N-doses, especially during the stem extension
stage can directly, or indirectly, through changing the micorcJimate, be a contributing
factor to the observed increases in powdery mildew appearance (Obst [25}).
As a matter of fact, it is possible, to some extent, through managing nitrogen fertilization regarding N-source and time of application to control cereal growth and
diminish the adverse effect of high N-supply (Linser [22}).
70
3. Interaction nitrogen/potassium
Getting highest possible Yields from plants fertilized with high N-doses, depends also
upon sufficient supply with other nutrients especially potassium and phosphorous.
Sufficient potassium supply leads to grbwth and anatomical changes, which are, in
general, opposite to those resulting from high N-doses. Potassium increases stem
diameter, culm wall and strengthen the structure of the mechanical tissues (Table 1).
Root growth and compactness are also promoted through potassium. Accordingly,
sufficient and balanced potassium supply increased the resistance of cereal plants to
lodging (Trolldenier [31]).
The effect of N application on fungal diseases is much affected by the supply with other
plant nutrients particularly with potassium and phosphate. This has been shown by
various authors (Hak [I5), Siebold [30}, Trolldenier [32}). The physiological
reasons for the favourable effects of potassium and phosphate are not yet completely
understood. In a review paper Trolldenier [32} suggests that an abundant potassium
supply promotes the formation of thick epidermal cell walls and a well developed
cuticle, both impairing the penetration of hyphae into the host cell. Recent experimental data of Pissarek [26} support this assumption, as it was shown that potassium
especially promoted the development of xylem parenchyma cells and sclerenchymatic
cells.
Table 1. Effects of different nitrogen forms, potassium and CCC on Cercosporella attack,
lodging, growth and anatomical features of cereals
Nitrogen form
Cercosparella attack
Lodging
Plant height
Length of lower intern odes
Diameter of upper internodes
Diameter of lower internodes
Calcium
ammonium
nitrate or
calcium
nitrate
Calcium.
Cynamid
increases
increases
increases
increases
increases
decreases
decreases
increases
decreases
no effect
or decreases
decreases
CuIm wall
Thickness of sclerenchyma cell walls decreases
not affected
Number of vascular bundles
Lignification of vascular bundles
decreases
less sturdy
Root System
Potassium
increases
decreases
decreases
decreases
decreases
generally
no effect
increases
increases
increases
increases
increases
compact and
sturdy
increases
increases
increases
increases
compact
and sturdy
decreases
increases
increases
increases
compact and
sturdy - more
adventitious
roots
CCC
From data from: Au/hammer et al. [3], Bauer [4], Diercks {i2], EI-Fauly and FirgallY [ullpublished],
Koch {i8], Mayr and Presoly [23], Mulder [24], Pissarek and Fillck [27], Trolldellier [3J], Zaher
et al. [33].
71
4. Interaction nitrogenjCCC
Better control of plant growth can be achieved by using plant growth substances.
These substances are becoming a useful tool in plant production and one of them,
ehlormequat (Cycocel or CCe) is playing an increasing role in cereal production
(lung and Scott [17], Linsef· [21}). Treating wheat plants (and other cereals) with
this compound results in different growth modifications, which are in general, opposite
to those induced by high N-Ievels (Table 1). Different cereals species as well as different
cultivars vary in their degree of response to ece. According to these morphological
and anatomical changes in growth, plants treated with eec are more resistant to
lodging than untreated plants. This compound can be used in different parts of Europe
and the Mediterranean region to prevent lodging (Atanasiu and Westphal [2], El-Fouly
and Fawzi [l3], lung and Schott [I 7], Linser [21}). Preventing lodging is mostly
coincident with grain yield increases, which justify the large scale use of eee in
cereal production in many countries.
Moreover, some reports indicate a positive effect of eee on decreasing the attack of
treated plants with C. herpotrichoides and thus plants become resistant to eye spot
Table 2. Cercosporella herpotrichoides attack on different winter wheat cuItivars treated with calcium
cyanamid and CCC (from Diercks [12J)
Cercosporella infection index
Lodging index
(N as calcium ammonium nitrate = 100)
Cultivar
F. Format.
Tenor
WaIthari
,
.
.
N as calcium cyanamid
N as calcium cyanamid
-CCC
+CCC
-CCC
+CCC
89.50
75.27
74.71
77.70
67.20
69.54
96.30
77.50
50.00
0.00
0.00
0.00
Table 3. Effect of nitrogen fertilizers with and without CCC application on Turkish wheat cuItivars
(from Atanasiu and Westphal [2J)
CCC treatment
kg/ha
CuItivar
Grain yield (tons/ha)
kgN/ha
0
50
0
3E
6E
3L
6L
Akbasak
(T. durum)
2.62
1.89
2.13
2.16
2.05
2.97
2.97
2.77
3.13
3.12
2.54
3.10
3.17
3.23
3.13
0
3E
6E
3L
6L
Karakileik
(T. durum)
1.52
1.43
1.21
1.29
1.14
1.57
2.28
2.20
2.26
2.04
1.90
2.44
2.32
2.38
2.63
CuItivar
100
Grain yield (tons/ha)
kgN/ha
0
50
100
220/39
(T. aestivum)
1.69
1.86
1.22
1.45
1.27
1.70
2.10
1,98
1.68
1.67
1.59
1.65
1.82
1.54
1.73
093/44
(T. aestivum)
2.17
1.94
1.80
1.91
2.08
2.37
2.70
2.88
2.64
2.71
2.28
3.14
3.26
3.01
3.22
Lodging: 0-5 all cultivars except 220/39 highly lodged at 100 kg N/ha. CCC prevented lodging in
all treatments.
E: Early treatment (27 days after sowing)
L: Late treatment (64 days after sowing)
72
(Bockmann [6], Diercks [12]). This is mainly due to growth changes induced by this
substance. No direct effect on the fungus could be found. It is interesting to note
that positive effects of eee against C. herpotrichoides attack were apparent, also
when treated plants received N in the fomi of calcium cyanamid (Table 2), which in
turn decreased attack in comparison to calcium ammonium nitrate (Diercks [12]).
Using ece in cereal production, especially wheat, opened new possibilities of increasing N-supply to get maximum possible yields without fearing disease problems
resulting from growth changes caused by high N-doses. In many experiments eee
treatment of wheat plants led to a remarkable shift in the rate of nitrogen fertilizers
needed to obtain maximum yield (Table 3), thus making N-fertilization more beneficial (A tanasiu and Westphal [2], de Vos [JJ]). This was also apparent in rye
(Primost [28]). In cases, in which this shift was not apparent, eee treatment under a
given N-dose led to yield increases through preventing lodging (Table 4). The interaction between eee and N-fertilization should be studied under the aspect of the
effect of increasing N on growth, diseases and yield, when eee treatment is used as a
commOn agronomical practice. Most of the published data are concerned with the
effect of eee under high N-Ievels.
5. Interaction nitrogen/potassium/CCC
In a preliminary experiment in Egypt with wheat cultivar Giza 155 in loamy sand soil,
K-fertilization under unusual high N-supply led to less lodging and higher yield.
Additional treatment with eee was less effective (Table 5). The effect of eee on the
culm stability and flexibility depends also on the potassium nutritional status of cereals.
Thus Koch [18] reported that both K and eee increased the culm diameter and
favoured the formation of rather thick cell walls. Adequate potassium supply is needed
also when eee is applied to cereals, in order to get the possible positive effects of the
latter. Application of eee to potassium deficient cereals led to significant yield
decreases (Table 5), (Kiihn and Linser [l9]).
6. Side effects and use of fungicides
ehanges in growth of cereals caused by eee, which counteract those caused by
high N leading to diminis.h the susceptibility to diseases, have negative impacts on
attack with other diseases. Plants treated with eee showed more"intensive attack
with Septoria nodorum Berk. as well as Fusarium culmorum Link than untreated plants
(Bockmann [6]; Langerjeld [20]). This can be such a severe one that it nullifies the
positive effects due to lodging prevention. The intensive infection of eee treated plants
might be due to one or more of those causes, which result directly or indirectly from its
effect on growth:
1. Short distance between the flag leaf and the ear (in case of Septoria),
2. ehanges in microclimate and retaining more humidity in the field, .
3. Prolongation of ripening time of the treated plants.
Experimental results of Bretschneider-Herrmann and Langelfeld [la] supported that
Septoria is primarily favoured by an increase in air humidity and that both the effects
of nitrogen and eee application probably are more of indirect nature.
These effects could be, however, reduced when eee treatment takes place early in the
73
Table 4. Effect of increasing N-supply with and without CCC-application on lodging and yield
of wheat cultivar G. 155 (El-Fouly and Firgany [unpublished})
Nitrogen
Lodging index
kg/ha
-CCC
+CCC
-CCC
+CCC
100.............................
140..............................
180..............................
2
6
7
I
3
3
12.53
13.59
12.18
13.02
14.52
13.58
Yield kg/plot
Table 5. Effect of K and CCC on lodging and yield of wheat cultivar Giza 155 under heavy
N-dressing (1970-1971) (El-Fouly [unpublished))
Soil: Loamy sand - N 25 kg/ha as organic manure + 150 kg/ha as ammonium sulphate
Grain yield
K ZS0 4
CCC
100 kg/ha
41/ha
lodging
tons/ha
%
+
6
3
I
4.60
5.07
5.13
100
110
112
+
+
season or by applying low doses. Yet, there are many other factors interacting in
determining the minimum cce dose needed under given conditions, to be effective
against possible adverse effects due to high N-doses.
As increased infection with Cercosporella in stands receiving high N supply cannot be
totally overcome through CCC-application, a new approach was tested recently. Its
aim is to combine the different positive effects and develop a package of treatments
giving maximum possible yield. A systemic fungicide was used to control Cercosporella
in combination with cec and high N-doses (Jung and Schott [17]). These combinations led to remarkable yield increases in wheat (Table 7). In the meantime, the fungicidal treatment could be varied to be also effective against Septoria attack.
In this way, it is possible to prevent physiological lodging and Cercosporella attack,
widen the possibilities of using higher N-supply without fearing its negative impacts on
diseases connected with growth changes. In the same time, the drawbacks of eccapplication can be excluded to a great extent.
Table 6. Interaction of CCC effect and potassium supply in pot experiment (70% water capacity with
spring wheat (from Kiihn and Linser [J9))
Grain Yield (g/pot)
Straw Yield (g/pot)
Root wt (g/pot)
Grain/Straw
Stem height (cm)
Powdery mildew attack
74
.
.
.
.
.
.
without Potassium
with Potassium
-CCC
+ CCC
-CCC
+ CCC
23.70
43.70
3.61
0.54
77.3
++
17.30
41.40
3.99
0.42
54.8
+++
49.50
61.90
7.65
0.80
88.0
+
47.50
55.30
8.36
0.86
60.0
++
Table 7. Reactions of winter wheats to treatment with CCC and systemic fungicide for the control
of Cercosporella (grain yield in t/ha; 7 trials of the official Bavariancultivar experiments 1972)
(Fischbeck [1973J) (from Jung and Schott [17J)
Cultivar
syst. Fungicid
without
CCC
Jubilar .........................
Diplomat ................... " .
Caribo .........................
Magnet .......................
Kranich .......................
4.62
4.97
4.98
4.71
5.33
with
+
++
5.04
5.26
5.18
5.33
5.65
5.01
5.30
5.35
5.56
5.67
5.08
5.31
5.36
5.33
6.09
+
++
5.66
5.58
5.59
6.04
5.86
5.56
5.67
5.50
6.42
6.13
7. Acknowledgments
The author wishes to thank Prof. Dr. A.Amberger, Lehrstuhl fiir Pflanzenerniihrung,
TU Mlinchen-Weihenstephan/FRG and Dr. J.Jung, Agricultural Research Station
Limburgerhof, BASF AG, Ludwigshafen/FRG for their interest and suggestions.
Thanks are also to Dr. A. Wunsch, Lehrstuhl flir Pflanzenerniihrung, TU MUnchenWeihenstephan for critically reading the manuscript.
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75
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27. Pissarek, H.P. and Fink, A.: Untersuchungen zur anatomischen-mikroskopischen Diagnose des
latenten Kaliummangels. Landw. Forsch. 27/1, 241-248 (1972).
28. Primost, E.: Der Einfluss des Standortes auf die Wirkung der CCC-Behandlung und Stickstoffdiingung bei Roggen. Z. Acker- und Pflanzenbau 131, 44-56 (1970).
29. Salt,·G.A.: Effects of nitrogen applied of different dates, and of other cultural treatments on
eyespot, lodging and yield of winter wheat. Field Exp. 1952. J. agr. Sci. 46, 407-416 (1955).
30. Siebold, M.: Einfluss der Kalidtingung auf die Stengelfiiule bei Kornermais. Gesunde Pflanzcn
26, 65-68 (1974).
31. Trolldenier, G.: Einfluss der Dtingung auf die Standfestigkeit von Weizen. Kali Briefe Fachgebiet
11, 2. Folge (1965).
32. Trolldenier, G.: Getreidekrankheiten und Pflanzenerniihrung. Kali-Briefe (Bern) Fachgeb. 23.
34 (1969).
33. Zaher, A., Foad, M.K., El-Shaarawi, A. and El-Fouly, M. M.: Morphological and anatomical
modifications in wheat after treatment with chlormequat chloride (CCC). Egypt. J. Botany 16,
125-136 (1973).
76
The Effect of 'N-Serve' on the Health of Barley, Maize
and Vetch
Prof. Dr. A.Aydeniz, F.Hatipoglu and M.Aktas, Department of Radiophysiology'and
Faculty of Agriculture, University of Ankara/Tu~key
~oil
Fertility,
Summary
Barley maize and vetch were grown in pots in the greenhouse at two nitrogen levels (50 and 200
ppm N) and with and without 'N-serve'. 'N-serve' greatly reduced dry matter production by vetch,
harvested after seven weeks growth, had little effect on maize and slightly increased dry matter
production by barley. Yield reduction in vetch was probably due to inhibition of nitrification and a
toxic effect on Rhizobium. There were some effects on plant nutrient contents and Ca content
especially was increased by 'N-serve',
Resume
On a etabli en serre un essai en pots avec l'orge, le ma'is et la vesce. Cet essai comprenait deux doses
d'azote (5'0 et 200 ppm de N) ainsi que des pots avec et sans addition de «N-serve» un inhibiteilr de
la nitrification. «N-serve» a fortement reduit la production de matiere seche par la vesce recoltee
apres sept semaines de croissance; son effet sur le ma'is a etefaible et il a legeremenfaccru la production de matiere seche chez l'orge. La diminution du rendement de la vesce a ete due probablement
a I'inhibition de la nitrification et a un ejfet toxique sur Rhizobium. Jl y avait quelques effets sur les
teneurs en elements nutritifs tandis que la teneur en Ca fut fortement accrue sous I'effet de «N-serve».
1. Introduction
Nitrogen recovery by crops is very variable, e. g. AlIison [1] showed a range from 21
to 79%. Thus much N applied as fertilizer is lost. Poor N recovery may be due to a
small degree to immobilisation or retention of N as ammonia but is mainly due to loss
from known or unknown causes. Three processes appear to be of practical significance
(Prasad et al. [l6]);
1. Leaching, especially on light soils and in areas with heavy precipitation or intensive
irrigation (Johnston et al. [13]), and Levin [l4] described nitrate leaching by the
formula d= ~x 100 where d=depth of leaching,a=amount of leaching water
Pv
(cm) and Pv = field capacity (per cent by volume).
2. Loss by volatilisation as ammonia especially on calcareous soils under both aerobic
and anaerobic conditions. Fenn and Kissel [7, 8] and Fenn [5, 6] found N loss on
77
calcareous soils increased with increasing pH, with increasing potassium and sodium
saturation, increasing temperature and increasing moisture content.
3. Denitrification, varying with soil and other conditions (Burris [3}).
Losses of nitrogen are affected by soil and climatic conditions, rotation, previous crop,
fertilizer use etc. Losses can be reduced by proper placement, timely application and
foliar feeding, the method to be suggested depending on soil and cropping conditions,
type, level and timing of fertilizer application.
According to Goring [9, 10} leaching mainly as nitrate and inhibition or slowing
down of nitrification of applied ammonium or amide N can reduce such losses and
increase the efficiency of applied N.
.
Various chemicals have been investigated for their nitrification inhibiting properties
(Prasad et al. [l6}). The best known of these is 2-chloro-6-(trichloromethyl) pyridine
produced by the Dow Chemical Co. and marketed as 'N-serve'. N-serve has high
bie-logical activity especially with Nitrosomonas species and temporarily inhibits their
activity by blocking a stage in the nitrification process. Bandy and Bremner [2},
Haghes and Velch [l2} have also studied various nitrification inhibitors. Much
research has been done on the application of N-serve with fertilizers e.g. Prasad [15},
Huber et al. [ll}, Sprat! [l8} and Cochran et al. [4}. There are doubts about the
effect of N-serve on Rhizobium.
2. Method
A pot experiment, with an Ankara clay loam soil was conducted in the greenhouse in
spring 1975. Physical and chemical properties of the soil are summarised in Table 1.
Each pot contained 1316 g air dry soil, which was mixed 0-5-20 base fertilizer. Treatments comprised 50 and 200 ppm N as NH 4 N0 3 applied with and without N-serve
at a rate equivalent to 7 kg/ha. The pots were planted with 4 maize seed, 20 vetch seed
or 25 barley seed and kept at 25°C for 7 weeks with moisture at field capacity. At the
end of this period the plants were harvested, dried at 65°C, ground and analysed for
plant nutrient content. All results are derived from the means of three replications.
Table 1. Physical and chemical properties of the soil
Texture
Clay-loam
Sand Silt
Clay
(%)
(%)
(%)
pH
33.77 34.15 32.08 8.2
CaC0 3 C.E.C. Exchangeable cations O.M. Avail(%)
ableP
(meq/ (meq/IOO g)
(%)
100 g)
Ca Mg K
Na
(%)
5.98
30.98
20.504.39 1.47 0.22 1.43
10.2
3. Results and discussion
3.1. The effect of N-serve on yield
The results are summarised in Table 2. The effect of N-serve varied with the type of
plant, decreasing the yield of vetch and maize and increasing that of barley.
78
Table 2. Thc effccl or N-scnc on yield (g clry wcighLlpot)
Vctch
Treatments
No
.1.68
N so - .
N~(H)
4.47
2.57
5.40
N 200 + N-scr\c
1.79
N S,1 + N-sene .
Barley
2.91
5..12
5.0.1
6.84
6.29
2.26
.1.12
.1.45
.1.94
.1.94
3././. V('{ch
N-Serve had a marked en-ect on thc growth of vetch as illustrated in Figures 1-3. Dry
malter yield was reduced by nearly 50% at 50 ppm N and reduced to one third at
200 ppm. The probable reason for the yield reduction was nitrification inhibition and
a toxic effect on Rlti::obilllll as repol"ted by Ri!ey and Barber !7
3./.2. Maize
The effect of N-serve was small, reducing yield from 5.32 to 5.03 at 50 ppm Nand
from 6.84 to 6.29 at the higher level.
3./.3. Bar!ey
There was a positive elTect at the 50 ppm N level (3.12 to 3.45 g) and no eA"ect at the
higher leve I.
: - - - - - - - - - -60----,,..------
Po
Fig. I. The effect or N-scn c on \ ctch.
79
Fif{.2. The eO'ecI or N-,cn e on \ etch alSO ppm N-Ic\ cl.
1"i!{.3. The eO'ccl or N--cnc on \ctch al 200 ppm N-Ic\el.
80
3.2. Effects on plant nutrient contents
3.2.1. Vetch
The results of analysis are given in Table 3. N-Serve decreased the N content slightly
at 50 ppm N from 2.54 to 2.30 and increased it slightly (3.12 to 3.13 g) at 200 ppm.
P content increased slightly from 0.21 to 0.23 at 50 ppm and more strongly (0.19 to
0.26) at 200 ppm N. K content decreased at both levels (4.00 to 3.70 and 4.71 to 3.40
at 50 and 200 ppm N respectively). The effect of N serve was very marked on Ca
content, increasing it from 1.35 to 2.49 and from 1.54 to 2.70 at the lower and higher
N levels. Mg content was similarly increased - 0.44 to 0.51 and 0.36 to 0.63 respectively.
There was no great variation in Zn content, with a slight increase at both levels.
Table 3. The
eff~ct
of N-serve on plant nutrient content of vetch
Treatments
No ....................
Nso ··················· .
Nso+N-serve ...........
N 200 ..................
N zoo + N-serve .........
N
P
Mg
(%)
K
(%)
Ca
(%)
(%)
(%)
Zn
(ppm)
2.053
2.538
2.298
3.115
3.238
0.199
0.214
0.232
0.187
0.263
4.575
4.000
3.700
4.713
3.400
1.462
1.353
2.493
1.535
2.695
0.484
0.445
0.509
0.361
0.626
32.1
27.9
28.8
17.9
19.2
3.2.2. Maize (Table 4)
N-Serve decreased N content slightly from 1.03 to 0.88 at 50 ppm N but increased it
slightly from 1.97 to 2.13 at 200 ppm. P content was slightly increased at the higher
N level- from 0.13 to 0.16. K content was increased from 3.86 to 4.38 at 200 ppm N.
Ca content was very slightly decreased at 50 ppm and increased from 0.68 to 0.74 at
200 ppm N. There was no effect on Mg and Zn.
Table 4. The effect of N-serve on plant nutrient content of maize
Treatments
No··················· .
N so ··················· .
Nso+N-serve ...........
N 200 . . . . . . . . . . . . . . . . . .
N 200 + N-serve .........
P
(%)
K
(%)
Ca
Mg
(%)
(%)
(%)
Zn
(ppm)
0.625
1.027
0.877
1.966
2.129
0.148
0.136
0.140
0.128
0.157
4.037
3.475
3.450
3.862
4.383
0.592
0.531
0.520
0.677
0.737
0.258
0.297
0.295
0.414
0.428
18.5
17.5
16.7
30.9
32.9
N
3.2.3. Barley (Table 5)
N-Serve increased N content from 1.71 to 1.94 at 50 ppm N and from 2.79 to 3.79 at
200 ppm. P content was decreased at both levels - from 0.19 to 0.15 and 0.14 to 0.13 at
lower and higher N levels respectively. K content was decreased at the lower (4.59 to
4.46) and increased at the higher (4.59 to 4.75) N levels. Ca content increased at both
levels: 0.47 to 0.56 and 0.69 to 0.82. Mg content was not affected at 50 ppm N but
increased strongly at 200 ppm from 0.24 to 0.35.
81
Table 5. The effect of N-serve on plant nutrient content of barley
Treatments
N
(%)
P
(%)
K
(%)
Ca
(%)
Mg
(%)
Zn
(ppm)
No··················· .
N oo ...................
N so + N-serve ...........
N 200 ..................
N 200 + N-serve . . . . . . . . .
1.295
1.715
1.942
2.788
3.792
0.210
0.186
0.147
0.141
0.132
4.050
4.587
4.463
4.588
4.750
0.520
0.471
0.556
0.692
0.822
0.200
0.228
0.222
0.245
0.350
23.4
24.6
24.6
36.7
34.6
3.3. Effects on nutrient uptake
3.3.1. Vetch
Due to the yield reduction caused by N-serve nutrient uptakes were greatly reduced:
N by 1.9 times and 2.9 times, P by 1.6 times and 2.1 times, K by 1.9 times and 4.2 times
at the lower and higher N levels respectively. There was no clear effect on Ca uptake
at 50 ppm N but it was reduced 1.7 times at the higher level, Mg uptake was reduced
by about 1.5 times at both levels. Zn uptake was severely reduced at both levels.
3.3.2. Maize
Because the effects of N-serve on yield were only slight the effects on nutrient uptake
were minor. The uptake of most nutrients was slightly decreased at 50 ppm Nand
slightly increased at 200 ppm N.
3.3.3. Barley
Nutrient uptakes were generally increased by N-serve: N from 53.5 to 67.0 mg at
50 ppm N and from 109.8 to 149.4 mg at 200 ppm. P uptake was slightly decreased
at both N levels (5.8 to 5.1 and 5.6 to 5.2 mg at low and high N levels respectively).
K uptake was increased from 143 to 154 mg at 50 ppm N and from 181 to 187 at
200 ppm. Ca uptake rose from 14.7 to 19.2 at 50 ppm N and from 27.3 to 32.4 mg
at 200 ppm. Mg uptake was similarly increased. Zn uptake increased from 0.077 to
0.085 at 50 ppm N and decreased from 0.145 to 0.136 at 200 ppm N.
Acknowledgement
The authors would like to thank the International Potash Institute for arranging this
Colloquium, Dr. Acar Uzgiden of the Dow Chemical Co. for his cooperation and
Mr. Brohi for help of English.
Bibliography
1. Allison, F.E.: Advances in Agronomy. V. 7,213':'250 (1955).
2. Bundy, L. G. and Bremner, J.M.: Inhibition of nitrification in soils. Soil Sci. Soc. Amer. Proc.
37,396-398 (1973).
3. Burris, N.H.: Nitrogen fixation, Radioactive Isotopes in Agriculture. 361-369 (1956).
4. Cochran, V.L., Padendick, R.I. and Woddy, W. M.: Effectiveness of two nitrification inhibitors
for anhydrous ammonia under irrigated and dryland conditions. Agron. J. 65, 649-653 (1970).
82
5. Fenn, L.B.: Ammonia volatilization from surface application of ammonium compounds on
calcareous soils: Ill. Effect of mixing low and high loss ammonium compounds. Soil Sci. Amer.
Proc. 39, 366 (1975).
6. Fenn, L.B.: Ammonia volatilization from surface application of ammonium compounds on
calcareous soils: IV. Effect of calcium carbonate content. Soil Sci. Amer. Proc. 39, 631 (1975).
7. Fenn, L.B. and Kissel, D.E.: Ammonia volatilization from surface application of ammonium
compounds on calcareous soils: I. General theory. Soil Sci. Amer. Proc. Vo!. 37,855 (1973).
8. Fenn, L. B. and Kissel, D.E.: Ammonia volatilization from surface application of ammonium
compounds on calcareous soils: n. Effects of temperature and rate of ammonia nitrogen
application. Soil Sci. Amer. Proc. 38, 606 (1974).
9. Goring, C.A.: Control of nitrification by 2-Chloro-6-(trichloromethyl) pyridine. Soil Sci. 93,
211-218 (1962).
10. Goring, C. A.: Control of nitrification of ammonium fertilizers and urea by 2-Chloro-6-(trichloromethyl) pyridine. Soil Sci. 93,431-439 (1962).
11. Huber, D.M., Murray, G.A. and Crane, J.M.: Inhibition of nitrification as a deterrent to
nitrogen loss. Soil Sci. Soc. Amer. Proc. 33, 975-976 (1969).
12. Hughes, T.D. and Velch, L.F.: 2-Chloro-6-(trichloromethyl) pyridine as a nitrification inhibitor
for anhydrous ammonia applied in different seasons. Agron J. 62, 821-824 (1970).
13. Johnston, W.R., Iftihadich, F. and Daun, R.M.: Tile drainage effluent from systems or irrigated
land. Soil Sci. Soc. Amer. Proc. 29, 287-289 (1965).
14. Levin, L.: Movement of added nitrates through soil columns and undisturbed soil profiles.
Trans. 8th Intern. Congr. of Soil Sci. IV, 1011-1022 (1964).
15. Prasad, R.: Dry matter production and recovery of fertilizer nitrogen by rice as affected by
nitrification retarders N-serve and 'AM'. Plant and Soil 29, 327-330 (1968).
16. Prasad, R., Rajale, G.B. and Lakhdive, RA.: Nitrification retarders and slow release nitrogen
fertilizers, Advances in Agronomy. V. 23, 337-383 (1971).
17. Riley, D. and Barber, S. A.: Toxicity of 2-Chloro-6-(trichloromethyl) pyridine in Soybean (Glycine max. L., Merr) Seedlings. Agron J. 62, 550 (1970).
18. Spraft, E.D.: The effect of ammonium and urea phosphates with and without a nitrification
nhibitor, growth and nutrient uptake of wheat. Soil Sci. Soc. Amer. Proc. 37, 259-263 (1973).
83
j
j
j
j
j
j
j
j
j
j
j
j
Relationships between Plant Nutrition and Rice Diseases
Dr. G. Trolldenier and Dr. E. Zehler, Btintehof Agricultural Research Station, Hannover/FederaJ
Republic of Germany
Summary
A short review is given concerning the causal connections between plant nutrition and rice diseases.
Fertilisation has the greatest effect in moderately susceptible or partially resistant varieties. In
highly resistant and in highly susceptible varieties the nutritional status of the plant has little
influence on the severity of the disease. Resistance to plant diseases may be roughly subdivided into
anatomical and biochemical factors.
The effectiveness of the cuticula and the epidermal cell walls as a barrier is decreased by ample supply
with nitrogen, as synthesis of cell wall materials is reduced. Weaker synthesis of cellulose and lignine
may also be due to potassium deficiency. With poor silicification of epidermal cells, the rice plant
becomes susceptible to fungal diseases. Silicification is reduced with ample nitrogen application, but
improved by high potash doses.
Many pathogenic organisms depend on soluble cell constituents like sugars and amino acids. These
compounds are found at higher levels in plants abundantly supplied with nitrogen and in potassium
deficient plants as well. K deficiency restricts phosphorylation, so that carbohydrates of low molecular weight and soluble nitrogen compounds will accumulate. Some studies indicate higher amounts
of low molecular weight compounds in susceptible varieties than in resistant varieties. Furthermore,
the content of phenolic compounds in the plant, toxic to pathogens, is influenced by plant nutrition.
Increasing nitrogen application reduces the level of phenolic compounds as well as the toxicity of
phenols. The role of potassium needs further elucidation in this respect.
Resume
On don ne un bref apen;u des relations entre la nutrition des plantes et les maladies du riz. La
fertilisation exerce un effet majeur chez les varietes moderement susceptibles ou partiellement
resistantes. Chez les varietes tres resistantes et tres susceptibles J'etat nutritionnel de la plante n'a
que peu d'influence sur le degre de la malad.ie. En premiere approximation, la resistance aux
maladies des plantes peut etre sub-divisee en des facteurs anatomiques et biochimiques.
L'efficacite de la cuticule et des parois cellulaires epidermiques en tant que barriere est diminuee
par un fort apport d'azote, etant donne que la synthese du materiel de la paroi cellulaire est reduite.
Une synthese moindre de cellulose et de lignine peut egalement etre due a une carence en potassium.
Avec une silicification insuffisante des cellules epidermiques, la plante de riz devient susceptible aux
maladies fongiques. L'application de fortes doses d'azote reduit la silicification, qui est amelioree
par l'apport de doses elevees de potasse.
Un grand nombre d'organismes pathogenes dependent des constituants solubles des cellules, tels
que sucres et acides amines. Ces composes se trouvent en concentrations elevees chez les plantes
abondamment pourvues d'azote ainsi que chez les plantes carencees en potassium. La carence en K
restreint la phosphorylation, de sorte que s'accumulent les hydrates de carbone a faible poids
moleculaire et les composes azotes solubles. Quelques etudes indiquent qu'il y a des quantites plus
elevees de composes a poids moleculaire faible chez les varietes suceptibles que chez les varietes
85
resistantes. De plus, la teneur de la plante en composes phenoliques, toxiques pour les agents pathogenes, est influencee par la nutrition. Des doses croissantes d'azote rectuisent la teneur en composes
phenoliques ainsi que la toxicite des phenols. A cet egard on devra elucider de faeon encore plus
detaillee le role du potassium.
Introduction
A recent study of changes in rice farming in Asia revealed that farmers consider
diseases, insects and other pests to be the major constraints to higher rice yields
(Barber and Anden [1975]). A prerequisite for overcoming this problem is improved
knowledge of the intricate interactions existing between plant pathogens and the rice
plant.
As resistance is controlled genetically, plant breeders enhance efforts to develop
varieties resistant to insects and diseases (IRRI [1975]). The degree of disease resistance of such newly bred varieties and the period of time the resistance will hold until
new strains of the pathogen will have developed, are still uncertain. Because of the
great variability of fungi and bacteria resistance can be expected to break down after
some years. Besides, chemical control of diseases has frequently been less successful
in the tropics.
Resistance is modified substantially by environmental factors, such as climate and soil
properties. Thus, ten Have and Kauffman [1972], referring to bacterial leaf blight of
rice, emphazised that for the next few years, and perhaps longer, the only promising
means of reducing the incidence may be careful manipulation of agronomic practices
in the cultivation of high yielding varieties.
The effect of fertilization on the severity of many diseases has been observed for many
years (Trolldenier [1969]). Working on rusts of cereals, Hassebrauk [1930] made a
fundamental observation: The greatest benefits from fertilizers are found with
moderately susceptible or partially resistant varieties. In highly resistant and highly
susceptible varieties the nutritional status of the plant has little influence on the severity
of the disease. In view of the need for higher rice yields, a better understanding of the
causal connections between rice fertilization and disease severity may provide a basis
for modifying agronomic practices and minimizing yield constraints due to pests and
diseases.
Rice resistance and plant nutrition
Undoubtedly, there are many internal factors contributing to host resistance. They may
be roughly subdivided into anatomical and biochemical factors.
1. Anatomical barriers
The strength and the thickness of the cuticula and epidermal cell walls play an important part in allowing or preventing the penetration of fungal hyphae. Recently
Matsuyama [1975] has consolidated earlier findings that ample supply of nitrogen
fertilizers results in a significant decrease of cell wall materials cellulose and lignin
(Tab. 1 and 2), and, consequently, in reduced mechanical resistance to rice blast
disease. It has been shown that weaker synthesis of cell wall constituents may also be
due to potassium deficiency, making rice plants more susceptible to stem rot, Helminthosporium leaf spot and bacterial leaf blight (Matsubayashi et al. [1963]).
86
Table 1. Quantitative alteration of cell wall material (mg/I 00 mg dry wt.) of rice plants amply supplied
with nitrogenous fertilizer (Matsuyama [1975))
Carbohydrate
6th leaf
Control
+N
Pectin
Hemicellulose
(X-cellulose
1.3
36.2
5.8
1.3
25.9
4.8
Total nitrogen
2.7
4.2
Table 2. Quantitative alteration of lignin (fJ-g/IOO mg dry wt.) in rice plants amply supplied with
nitrogenous fertilizer (Matsuyama [1975))
Experiment 1
Experiment 2
Control
+N
1108
1108
475
570
For rice as a typical silica demanding plant, this element is essential for improving
structural strength. With poor silicification of epidermal cells, the rice plant becomes
susceptible to fungal diseases, such as rice blast and Helminthosporium leaf spot. The
resistance of rice plants is, therefore, increased by the application of silica. Many
workers thought that the silicated epidermal layer prevents physical penetration of the
fungus (for references see Du [1972}). For healthy growth the SiOz/N ratio should be
wide (Matsubayashi et al. [1963]). Plants given large amounts of nitrogen are found
to have less silicated epidermal cells and thus lower blast resistance (Du [1972]).
Silicification of cell walls seems to be linked with potassium nutrition. According to
Nogushi and Sugawara [1966]), potassium deficiency reduces the accumulation of
silica in the epidermal cells of the leaf blades, thus increasing the susceptibility to rice
blast. The content of silica in each part of the plant increases parallel with the level of
supplied potassium. The causal connection between potassium and silica nutrition is
still obscure.
The favourable effect of a high silica content is not restricted to plant diseases. Silica
also controls damage caused by stem borers, one of the worst paddy pests (Sasamoto
[1957, 1958), according to Grist [1965]). The moth larvae bore through the rice stems
shortly after hatching. With rice plants high in silica the mandibles of the feeding
larvae become worn out. Therefore the insects prefer plants containing little silica
which is achieved by abundant nitrogen supply.
2. Biochemical factors
Once a pathogen has overcome the anatomical barrier of the epidermis and has not
been 'neutralized' by the gene-for-gene defence system, its growth will be governed by
the suitability of the metabolites in the tissue as source of food. Many pathogenic
organisms depend on soluble cell constituents like sugars and amino acids.
Generally, the level of soluble low molecular cell compounds increases with increasing
nitrogen and decreasing potassium applications. In plants supplied with abundant
nitrogen, amino acids and amides are found in higher concentration. In potassium
87
deficient plants, besides amino acids and amides, sugars accumulate at the expense of
cell constituents of higher molecular weight, such as proteins, cellulose and lignin. This
is due to the fact that with a low potassium level in the plant the activity of decomposing
enzymes, such as amylase, saccharase, glucosidase and protease, is increased. Furthermore, K deficiency restricts phosphorylation, so that carbohydrates of low molecular
weight and soluble nitrogen compounds will accumulate (Mengel [1972]).
Carbohydrates, mineral nutrition and disease resistance
A close relation between carbohydrate metabolism and resistance has been reported for
several plants (Hare [1966]). The effect of potassium on the carbohydrate content in
rice plants has clearly been demonstrated by Nogushi and Sugawara [1966]. While the
amount of total carbohydrates increased due to higher potassium supply, the total
sugar content decreased. The higher content of sugars in potassium deficient plants
indicates a retarded conversion to substances of higher molecular weight.
Interesting observations have recentlybeen made by Reddy and Sridhar [1975] with
respect to bacterial leaf blight. Greater amounts of reducing and nonreducing sugars
were generally found in leaves of the highly susceptible variety T(N)1 than in leaves
of the less susceptible cultivar IR8. With increasing potassium supply the content of
nonreducing (Tab. 3) and reducing sugars decreased. As will be outlined later, amino
acids showed the same relation to potassium nutrition.
The pathogenesis in the highly susceptible variety was not greatly influenced by
fertilizer treatment, while the resistance of the less susceptible cultivar was definitely
increased by higher potassium levels (Fig. 1), which agrees well with the abovementioned findings of Hassebrauk [1930].
Table 3. Changes in nonreducing sugars (Glucose equivalent mg/lOO g oven dry tissue) of healthy and
X. oryzae inoculated highly susceptible and less susceptible rice leaves (Reddy and Sridhar [1975])
Highly susceptible - T(N) I
Inoculated
K
Healthy
level
Age of the plant (days)
(ppm)
38
3
25
75
125
175
(
1558
1491
1081
771
774
Less susceptible - IR8
Healthy
38
(8)
38
1358
1305
1019
664
640
1147
884
784
526
474
Inoculated
38
(8)
1042
817
727
433
406
) days after inoculation
Amino acids, mineral nutrition and disease resistance
The relation between host and pathogen largely depends on the source of nitrogen
which the pathogen will find in the plant.
The growth of Xanthomonas oryzae, the causative organism of bacterial leaf blight,
depends on certain amino acids. Glutamic acid and aspartic acid were found to be
. better nitrogen sources than other amino acids. When analysing the contents of amino
acids in vascular fluids from three susceptible and three resistant varieties, Hsu [1972]
88
125
100
Highly
susceptible T (NI 1
75
E
50
~
"0.
~
25
c
0
.~
~
50
Less susceptible
IR
e
25
0
4
5
Days after inoculation
Fig. J. Influence of different concentrations of potassium on bacterial blight development in two rice
varieties (Reddy and Sridhar [1975]).
generally found higher amounts in susceptible than in resistant varieties. In addition,
leaf or stem extract of the susceptible variety supported better growth of the fungi
in vitro than that of the resistant variety. Nitrogen supply to plants grown in nutrient
solution had a striking effect on disease reaction. While there were just slight symptoms
found in the resistant variety, independent of the nitrogen rate, the plants of the
susceptible variety were severely attacked with increasing N supply and, at high
nitrogen rates, killed 30 days after inoculation. Since Hsu found similar sugar and
amino acid contents in the susceptible variety grown either at 10 or 80 ppm N, different
sugar and amino acid contents could not account for the difference in host reaction.
Higher levels of amino acids in healthy leaves of a variety highly susceptible to
bacterial leaf blight than in leaves of a less susceptible variety were found by Reddy
and Sridhar [1975]. This disagrees, however, with data from Ramakrishnan [1966]
who found in healthy leaves of a variety susceptible to blast less soluble nitrogen than
in a resistant one. In contrast to Hsu [1972], Reddy and Sridhar [1975] observed a
distinct effect of fertilization on sugars and free amino acids. Besides a higher content
of sugars, plants grown at lower potassium levels, also had a higher content of amino
acids than those given higher K rates. In leaves of the highly susceptible variety,
inoculation with Xanthomonas oryzae caused a decrease in amino acids, while. in the
less susceptible cultivar amino acids increased, the highest rate of increase being found
in plants grown at high potassium levels. This finding is again in contradiction with
results from Ramakrishnan [1966] on rice blast. According to this author contents of
89
alcohol soluble, insoluble, and total nitrogen in the infected leaves of a susceptible
variety increased, while nitrogen fractions slightly decreased in the resistant variety.
Close relations between nitrogen metabolism and plant susceptibility have been stated
with brown leaf spot. According to Akai [1962J, the enlargement of Helminthosporium
leaf spots is closely correlated with the content of glutamic and aspartic acid in the
leaves. In plants supplied with abundant potassium the content of these amino acids
and the percentage of large spots were very low, whereas in K deficient plants the
content of amino acids and the percentage of large spots were high. In the same
experiment, only slight differences were found in the content of amino acid- between
treatments with excess nitrogen and N deficiency and it was somewhat surprising to
note that the percentage of large spots was higher with N deficiency than with N surplus.
Results obtained by Noguchi and Sugawara [1966J provide additional evidence of the
effect of potassium on the amount of amino acids and amides in rice plants. In potassium deficient plants ammonia, amides and amino acids accumulate in leaves and stems.
Many experiments have shown the influence of nitrogen fertilization on blast incidence.
Sridhar [1975J, found more amino and total nitrogen in a susceptible than in a resistant
variety. Increasing nitrogen fertilization raised the amino nitrogen content, and even
more markedly the total nitrogen content in the tissue (Tab. 4). During the disease
cycle, both amino and total nitrogen accumulated in the shoots. Since the causative
organism, Pyricularia oryzae, secretes proteolytic enzymes, it can be assumed that some
of the amino acids orginate from the breakdown of host proteins by fungal proteases.
Table 4. Changes in total nitrogen (mg/IOO g dry wt.) of shoots in susceptible and resistant varieties
(Sridhar [1975J)
Resistant plants
Age of the plants (days)
N rate
kg/ha*
Susceptible plants
Age of the plants (days)
15
30
45
60
75
15
30
45
60
75
0
20.4
44.8
67.2
89.5
1880
1880
1880
1880
1880
1160
1230
1290
1430
J490
840
870
890
910
920
790
830
840
860
880
620
660
670
720
740
1530
1530
1530
1530
1530
920
960
J090
J 130
1180
810
820
850
860
890
730
740
790
960
870
610
630
650
670
720
* N application on the J5th day of growth
Phenolic compounds, mineral nutrition and disease resistance
In many host parasite relationships a correlation exists between the degree of resistance
and the phenol level in healthy tissues, probably caused by the toxicity of phenols to
pathogens (Goodman et al. [1967J). Studies by Kiraly [1964J and others conclusively
showed that enhanced susceptibility of heavily N fertilized wheat to stem rust is due
to a reduced phenolic level. Additionally, the toxicity of phenols may be reduced by high
amino nitrogen content, which results in increased susceptibility (Kirkham (1954J,
Flood and Kirkham [1960J).
Sridhar [1972J found in shoots of older plants of a resistant variety an increase in
orthodihydroxyphenols and the same tendency for the total phenol content. He noted
a reduction of orthodihydroxyphenol content in response to nitrogen fertilization,also
enhanced phenolic synthesis due to P. oryzae inoculation, which is in good agreement
90
with the findings of Wakimoto and Yoshii [1958]. A reasonable explanation for the
different behaviour of both cultivars seems to be that the rate of phenol synthesis was
higher in the inoculated resistant variety than in the inoculated susceptible one.
Referring to his yet unpublished results, Samajpati [1972] also suggested a relation
between the incidence of brown leaf spot and the amount of phenolic compounds
formed with different levels of nitrogen, potassium and phosphorus. The author
found a gradual aggravation of disease with increasing nitrogen level and likewise in
the absence of potassium and phosphorus.
A relation between resistance to bacterial leaf blight, potassium nutrition and change
in phenol content has been disclosed in the already mentioned study of Reddy and
Sridhar [1975]. Infected leaves of the highly susceptible variety T(N)l contained less
phenols at all potassium levels than the healthy leaves, while in leaves of the less
susceptible variety IR8 the phenol content increased after infection (Tab. 5). Somewhat difficult to interprete and in certain contradiction to earlier findings (Sridhar
[1972]) is the observation that the phenol content in healthy leaves of the susceptible
T(N)l was higher than in leaves ofthe less susceptible IR8 ( Reddy and SridharI1975]).
Thakur and Ghosal [1976], however, found in healthy plants of a variety susceptible to Fusarium monili/orme (a fungus causing root-rot) lesser amounts of total
phenols than in a resistant variety. After infection the resistant variety showed
substantial increase in total phenols whereas the susceptible variety showed only a
slight increase. Reddy and Shridar [1975] question whether the high phenol content of
potassium deficient plants is due to high amounts of soluble sugars, since synthesis
of phenols is largely influenced by carbohydrate metabolism. On the other hand; toxic
phenols are rapidly broken down by polyphenoloxidase in the presence of high
amino nitrogen content, resulting in reduced toxicity in K deficient plants and consequently increased susceptibility.
Table 5. Changes in total phenols (chlorogenic acid equivalent mg/lOO g oven dry tissue) of healthy
and X. oryzae inoculated highly susceptible and less susceptible rice leaves (Reddy and Sridhar
[1975)}
K
Highly susceptible - T(N)I
Less susceptible - IR8
level
Healthy
Inoculated
Healthy
Inoculated
(ppm)
38
38
(8)
38
38
(8)
3
25
75
125
175
502
459
359
449
425
425
311
234
320
336
344
307
289
309
320
402
430
335
414
440
(
) Days after inoculation
Conclusions
This short survey reveals that further knowledge is required to fully elucidate the causal
connections between plant nutrition and disease resistance of rice. Many fertilizer
experiments have shown a certain antagonism between potassium and nitrogen.
K deficiency and N excess decrease resistance and vice versa. However, deviations from
this rule have been reported under special conditions (Ono [1957]). Generally, it is
91
recommended to balance the unfavourable effect of high nitrogen doses by increasing
the potassium supply as well. Results concerning the effect of other plant nutrients are
often equivocal. Further investigations into the effect offertilization on plant resistance
on the molecular and physiological level of the rice plant pathogen interactions are
needed to minimize yield losses due to diseases. Considerable progress has been made
in recent years in the understanding of the mechanisms of resistance or susceptibility
(e.g. Albersheim and Anderson-Prouty [1975], Hare [1966], Heitefuss [1970]).
According to Shaw [1963], these mechanisms seem to be based on the regulation of
protein synthesis; phenols and phytoalexins may exert an influence on resistance via
protein metabolism. Since besides nitrogen other nutrient elements intervene in extent
and rate of protein synthesis, the nutritional status of the plant as a whole should be
considered when investigating the biochemical processes involved in plant resistance
to rice diseases.
References
I. Albersheim, P. and Anderson-Prouty, Anne J.: Carbohydrates, proteins, cell surfaces, and the
biochemistry of pathogenesis. Ann. Rev. Plant Physiol. 26,31-52 (1975).
2. Akai, S.: Potash application and occurrence of Helminthosporium leaf spot on rice. Potash
Review, Internat. Potash Inst., Berne, Subject 23, 27th suite (1962).
3. Barber, R. and Anden, T.: Factors influencing the use of modern rice technology in the study
areas. In: Changes in rice farming in selected areas of Asia. International Rice Research
Institute, Los Banos, Philippines, p. l7-40, 1975.
4. Flood A.E. and Kirkham, D.S.: The effect of some phenolic compounds on the growth and
sporulation of two Venturia species. In: J. B. Pridham (ed.) Phenolics in plants in health and
disease. Pergamon Press, Oxford, p.81-85, 1960.
5. Goodman, R.N., Kiraly, Z. and Zaitlin, M.: The biochemistry and physiology of infectious plant
disease. Van Nostrand Co. Inc. Princeton, New Jersey, 1967.
6. Grist, D.H.: Rice. Longmans, London, 4th Edition, 1965.
7. Hare, R. c.: Physiology of resistance of fungal diseases in plants. Botanical Rev. 32, 95-137
(1966).
8. Hassebrauk, K.: Ober die Abhangigkeit der Rostinfektion von der Mineralsalzernahrung der
Getreidepflanze. Angew. Botanik 12, 23-35 (1930).
9. Have, H. ten and KauJJman, H.E.: Effect of nitrogen and spacing on bacterial leaf light of rice.
Indian Farming. Jan. (1972).
10. Heitefuss, R.: Wirt-Parasit-Interaktionen. Ber. Dtsch. Bot. Ges. 83, 203-219 (1970).
11. Hsu, S.: Nutritional aspect of host-pathogen relationship in bacterial leaf blight of rice. J. Agric.
Forestry (Taiwan) 21, 1-20 (1972).
12. International Rice Research Institute: Research highlights for 1974, Los Banos, Laguna, Philippines, 1975.
13. Kiraly, Z.: Effect of nitrogen fertilization on phenol metabolism and stem rust susceptibility of
wheat. Phytopathol. Z. 51, 252-261 (1964).
14. Kirkham, D.S.: Significance of the ratio between the water soluble aromatic and nitrogen
constituents of apple and pear in the host parasite relationship of Venturia sp. Nature, 173,
690-691 (1954).
15. Matsubayashi, M., 1to, R., Takase, T., Nomoto, T. and Yamade, N.: Theory and practice of
growing rice. Fuji Publishing Co. Ltd., Tokyo, 1963.
16. Matsuyama, N.: The effect of ample nitrogen fertilizer on cell wall materials and its significance
to rice blast disease. Ann. Phytopathol. Soc. Japan 41, 56-61 (1975).
l7. Mengel, K.: Ernahrung und Stoffwechsel der Pftanze. Gustav Fischer Verlag Stuttgart, 4. Aufl.
1972.
18. Nogushi, J. and Sugawara, T.: Potassium and Japonica rice. International Potash Institute,
Berne, 1966.
92
19. Ono, K.: The relation between rice diseases and potassium. International Potash Institute,
Berne. 1st Jap. Potassium Symp., Tokyo, p.71-87, 1957.
20. Du, S.A.: Rice diseases. Commonwealth Mycological Institute, Kew, Surrey, England, 1972.
21. Ramakrishnan, L.: Studies in the host-parasite relat'ions of blast disease of rice. l. Changes in
N-metabolism. Phytopath. Z. 55, 297-308 (1966).
22. Reddy, P. Ranga and Sridhar, R.: Influence of potassium nutrition and bacterial blight disease
on phenol, soluble carbohydrates and amino. acid contents in rice leaves. Acta Phytopathol.
Acad. Scient. Hungaricae la, 55-62 (1975).
23. Samajpati, N.: Effect of different fertilizer levels on the 'brown spot disease' development in rice
plant. Indian Agric. 16, 317-322 (1972).
24. Shaw, M.: The physiology and host parasite relations of the rusts. Ann. Rev. Phytopath. 1,
259-294 (1963).
.
25. Sridhar, R.: Phenolic compounds and the rice blast disease as influenced by nitrogen fertilization. Riso, 21, 25-31 (1972).
26. Sridhar, R.: The influence of nitrogen fertilization and the blast disease development on the
nitrogen metabolism of rice plants. Riso 24, 37-43 (1975).
27. Thakur, K. S. S. and Ghosal, M.: Study of phenolic contents of resistant and susceptible
varieties of rice in relation to foot-rot disease. Riso 25, 87-91 (1976).
28. Trolldenier, G.: Cereal diseases and plant nutrition. Potash Review, Internat. Potash Inst.
Berne, Subject 23, 34th suite (1969).
29. Wakimoto, S. and Yoshii, H.: Relation between polyphenols contained in plants and phytopathogenic fungi. 1. Polyphenols contained in rice plants. Ann. Phytopathol. Soc. Japan, 23,
79-84 (1958).
93
.j
j
j
j
j
j
j
j
j
Report of the Co-ordinator of the 1st Session
Prof. Dr. K.Mengel, Head, Institute of Plant Nutrition, Justus Liebig University, Giessen/Federal
Republic of Germany
The 1st session was devoted to the biochemical and physiological aspects of 'Fertilizer
Use and Plant Health'. The papers presented in this session showed that four points
seem to be of particular relevance:
1. Infection, dissolution of cell wall material, permeability and stability of the plasmamembrane.
2. Synthesis and building blocks of the cell wall and cuticula.
3. Synthesis of soluble cytoplasmatic constituents.
4. Regrowth and regeneration of infested tissue.
Infection by fungi and many bacteria starts with the dissolution of the cell wall
material. This dissolution is achieved by certain hydrolases excreted by the pathogens.
Dr. Kiraly emphasized that in many cases Ca++ inhibits these hydrolases, e.g. polygalacturonase. On the other hand pectolytic enzymes of the lyase type (transeliminase)
may rather be stimulated than hampered by Ca 2 +. This example shows that observations seemingly contradictory on the surface can be explained by the different
biochemical processes involved.
Dr. Schulz presented data which showed that K+ in tissue culture may exert to some
extent a stimulating effect on the endopolymethylgalacturonase. In this context the
question arises whether, under field conditions, the concentrations of inorganic ions
in the apoplast (free space) of the upper plant parts are dependent on the nutrition of
the plant to a major degree. It can be supposed that this is not the case, and that often
the intracelluar spaces, from which bacterial attack frequently starts, are filled with air
rather than with water. Plant nutrition, however, is brought into play, as soon as the
stability and permeability of the plasmamembrane is affected by the pathogen. It is
assumed that in this case water and solutes are released into the free space. The solutes
(inorganic ions, sugars, amino acids, phenolic compounds) reflect the physiological
and nutritional status of the cell. The solutes probably have an essential influence on
growth and multiplication of the pathogen.
In all cases where the pathogens do not penetrate through wounds into the cell, the
dissolution of the cell wall and sometimes also of the cuticula is a prerequisite for
infection. Thus the thickness of the cuticula and ceIl wall as weIl as the constituents,
by which both are built up, are of substantial importance for the resistance of plant
cells against infection. Dr. ]smunadji pointed out that K+ favours the synthesis of cell
wall material and in particular has a promoting effect on the incrustation of Si into the
95
epidermal cell layer of rice plants. This finding was supported by data presented by
Dr. Trolldenier showing that rice plants which had received an ample N and a suboptimal K supply, showed reduced contents of hemicellulose and lignin in the cell wall.
Both speakers, Dr. Ismunadij and Dr. Trolldenier, emphasized that the improved
resistance of rice due to an ample K supply may result from the thicker cell walls, their
higher content of lignin and the improved Si incrustation in the epidermal cells. The
favourable effect of K+ on the development of the cell wall was also stressed by the
paper of Prof. EI-Fouly. He pointed out that the K effect was enhanced by the application of chlorcholine chloride. As this compound is related to the gibberellic acid
metabolism the assumption is justified that alterations in the cell wall synthesis caused
by the application of chlorcholine chloride result from a change in the phytohormonal
pattern of the cell or tissue.
The finding that too high a N supply favours the synthesis of proteins at the expense of
cell wall material can be explained by the competition for photosynthates and energy
by both metabolic pathways, namely by the protein synthesis and by the synthesis of
cell wall material. Potassium favours the synthesis of photosynthates and the conversion of light energy into chemical energy which results in a more balanced metabolism under the conditions of high N supply. This shows that the N/K ratio in the
nutrient supply has an impact on the resistance or susceptibility of plants against fungal
or bacterial diseases.
There exists a general agreement that especially the soluble organic compounds in the
plant cells have a direct influence on the development and multiplication of the
pathogen. In this respect especially sugars, amino acids, and phenolic compounds are
of major interest. The concentrations of these compounds in the cell depend to some
extent on plant nutrition. It is a well known fact that the N supply and the form in
which N is applied have a direct effect on the content of soluble amino acids in the
tissue. This questions is related to the paper presented by Dr. Aydeniz who reported
about the effect of 'N-Serve' on the growth of some crops.
Up to now it is not yet clear whether the amino acids serving as food for the pathogens
play the most important part in decreasing resistance against the pathogen. Dr. Kiraly
stressed the fact that a higher N supply reduces the amount and the toxicity of phenolic
compounds and thus results in a higher susceptibility against the pathogen. Nitrogen
also affects the key enzymes responsible for the synthesis of phenolic compounds. The
question whether soluble sugars have a major influence on the growth of the pathogen
or may even trigger metabolic pathways relevant for resistance or susceptibility
remains to be clarified. Also further research is needed to find out which type of
soluble compounds in the cytoplasma influenced by plant nutrition is the most
important in affecting resistance or susceptibility.
Studies in which resistant cultivars are compared with susceptible ones may be helpful
in finding out which compound or which process is the most important in controlling
susceptibility or resistance.
Dr. Trolldenier presented such an example. It should be born in mind, however, that
very tiny quantities of these hypothetical compounds may be responsible for the
phenomenon described as resistance or susceptibility and that the detection and
determination of these tiny amounts is difficult.
As the relationships between plant nutrition and plant health are numerous, the
tendency to simplify and generalize is inherent and also justified. The general assumption, however, that an abundant N supply decreases the resistance against diseases is
96
too great a simplification. Dr. Kiraly presented data which demonstrated that in cases
where plants are attacked by facultative pathogens, ample N nutrition may well
increase the resistance. It is supposed that an abundant N supply favours processes
involved in regrowth and regeneration. Regeneration is associated with protein
formation on which the N supply has a direct influence and also an indirect one. The
latter is due to the effect of N on the synthesis of cytokinins which control protein
synthesis. Whether the toxins released by the pathogen interfere with the host proteins
remains to be elucidated and the question of regrowth and regeneration of infested
tissue requires further investigation.
97
2nd Session
Co-ordinator:
Fertilizer Use and Plant
Health: Fungi
Prof. Dr. H.Laudelout, Departement Science du
Sol, Universite de Louvain, Louvain-la-Neuve/
Belgium; member of the Scientific Board of the
International Potash Institute
Effect of Mineral Nutrients on Soil-Borne Pathogens
and Host Resistance
Prof. Y. Henis, Department of Plant Pathology and Microbiology, Faculty of Agriculture,
The Hebrew Dniversity of Jerusalem, Rehovot/lsrael
Summary
Commonly used fertilizers affect plant growth not only directly, as plant nutrients, but indirectly
as well, through their effect on disease incidence and severity. They may affect the pathogen's growth,
its aggressiveness, the aritagonistic soil microflora, or host's resistance. Cases of disease increase
and decrease following fertilizer application are discussed, and analyzed. It is recommended that
fertilizing practice, in particular the form of nitrogen used, and the balance between fertilizer
components, should be considered according totheir possible effect on disease incidence and severity.
Resume
Les engrais habituellement utilises n'exercent leur influence sur la croissance non seulement en leur
qualite d'elements nutritifs (action directe), mais ils agissent egalement sur l'incidence et la severite
des maladies des vegetaux (action indirecte). Ils peuvent affecter le developpement des agents
pathogenes et l'agressivite deceux-ci, la microflore antagoniste du sol ou la resistance des planteshotes. L'auteur discute et examine des cas se referant it l'intensification ou it la reduction de l'attaque
par les maladies it la suite de l'application d'engrais. Il recommande de ne pas perdre de vue, lors
de l'etablissement des plans de fertilisation, les effets possibles des engrais sur l'incidence et la
severite des maladies et de tenir compte tout particulierement de la forme d'azote utilisee ainsi que
de l'equilibre des differents elements nutritifs dans les engrais appliques.
1. Introduction
The primary purpose in applying fertilizers to soil is to enhance plant growth and to
obtain maximum yield. Mineral plant nutrients, however, may exert secondary, often
unpredicted, effects on crop yield through their effect on the growth, survival and
virulence of soil-borne plant pathogens and/or host tolerance to disease. The various
possible interactions between mineral nutrients (applied as fertilizers), soil conditions
and the organisms involved in disease, are summarized in Figure 1. Because of the
complexity of the soil ecosystem, there are still many gaps in our understanding of
the mechanisms involved. These have recently been summarized in a number of books
and reviews (Chapman [8), Baker. and Cook [4}, Garrett [l6}, Papavizas [48},
Henis and Chet [24}, Henis and Katan [25}, Smiley [66}) and will be discussed here
only briefly. The main purpose of this contribution is to present some recently collected
101
Fig. I. Interactions between host, pathogen, fertilizer, soil microflora and environment. The effect of
the pathogen on the host is emphasized. whereas interactions of relatively minor importance are
indicated by a broken line.
data concerning the effects of commonly used fertilizers on pathogen behaviour in
the soil, host resistance, disease incidence and disease severity.
2. Nitrogen
Nitrogen fertilizers, usually applied as potassium, ammonium or calcium nitrate,
ammonium sulphate, ammonia or urea (which is included here because of its rapid
decomposition to NH3 and CO 2 in the soil) have continued to receive much attention
regarding their effect on plant pathogens.
It is generally believed that disease incidence and severity caused by root infecting
fungi increase under the influence of nitrogen fertilizers (Garrett [15]). However, cases
of decrease have also been reported. Table 1 cites some cases of increase, and some
cases of decrease in disease severity following application of nitrogen feltilizers.
2.1. Direct vs. indirect effects
N-fertilizers may affect disease severity either indirectly, due to their effect on the
antagonistic soil microflora or on host tolerance, or by affecting directly the pathogen's
growth or virulence. For example, ammonia is highly toxic to Sclerotium rol/sU,
Fusarium roseum f. sp. cerealis and F. solani f. sp. pisi (Smiley et al. [63, 64], Lahover
and Avizohar Hershenzon [33] and Henis and Chet [23]), whereas nitrite, which may
accumulate in soil during nitrification of ammonia, is toxic to Pythium (Grover and
Sidhu [18]) and Phytophthora (Zentmyer and Bingham [77]).
The decrease in wilt disease caused by F. oxysporlim f. cubense in banana following
urea application has been shown by Sequeira [58] to result from inhibition of the
pathogen by nitrite formed from the applied urea during its decomposition in soil.
102
2.2. Effects of NO-3 and NH+.-N
According to Huber et al. [29J, root diseases differ in their response to specific forms
of nitrogen fertilizers. The diseases caused by Fusarium, Rhizoctonia and Aphanomyces
are increased in severity by NH 4 +-N and decreased by N0 3 --N. Verticillium wilt of
potato (V. albo-atrum) is reduced by NH 4 +-N (Huber and Watson [28J), whereas
take-all disease, caused by Gaeumanomyces graminis (Ophiobolus graminis) is reduced
with NH 4 +-Nand was unchanged or made more severe by N0 3 - - N ( Huber et al. [27J).
Suppression of fusarium diseases by N0 3 --N was reported in beans (Maurer and
Baker [41)), cotton (Mostapha and Moawad [44J) and chrysanthemum (Woltz and
Engelhard [75J). On the other hand, fusarium diseases of carnation and sorghum are
favored by N0 3--N, whereas reports on Fusarium wilt of tomato are contradictory
(Table 1). Generally, most Fusarium wilts seem to be aggravated by both NH4+-N
and N0 3--N.
The bean root rot organism, Fusarium solani f. sp. phaseoli, survives in soil as thickwalled chlamydospores. Papavizas et al. [50, 52J studied· the effect of some N sources
Table 1. Examples of effects of some mineral nutrients on soil-borne plant diseases.
Nutrient
Pathogen
Host
Disease
References
Increase ( +)
Decrease (-)
N0 3 -
Fusarium oxysporum
f. sp. lycopersici
Tomato
+
N0 3 -
F. oxysporum f. sp.
lycopersici
Tomato
N0 3 -
F. roseum
Carnation
N0 3 -
Phytophthora parasitica
var. nicotianae
Tobacco
Walker and Foster [70}
Woltz,and Jones [76}
+
+
Dortworth and Tammen [i2}
Apple [3}
KN0 3
F. solani f. sp. phaseoli
Bean
Maurer and Baker [41}
Ca(N0 3)2
Sclerotium rol/sii
Tomato
Mohr and Watkins [43}
NH.+
Ophiobolus graminis
Wheat
NH.+
O. graminis
Wheat
NH.+
O. graminis
Wheat
NH.+
F. oxysporum f. sp.
lycopersici
Tomato
+
Woltz and Jones [76}
Sorghum
+
Erinle and Edmunds [13}
Cotton
+
Ramney [55}
Eggplant
+
Sivaprakasam
and Rajagopalan [61}
NaN0 3
NH.N0 3
} F. monili/orme
(NH.)SO.
Ca(N0 3)2 } Verticillium albo-atrum
KN0 3
Urea
Verticillium wilt
3
NH
(NH.)zSO. } S. rolfsii
Ca(N0 3)2
Garret! [14}
+-
Huber [26}
Smiley and Cook [65}
Sugarbeet -
Leach and Davey [36)
103
on propagule numbers of this fungus in the soil. Addition of N0 3 --N along with an
effective carbon sources such as glucose, doubled or tripled the number of propagules
over that obtained with the C source alone. When glucose was added to infected soil
with NH 4 +-N the population of F. solani was increased 58 fold, as a result of germination, growth and formation of new chlamydospores.
Other pathogens reported to be favored by N-fertilizers include Verticillium albo-atrum
in cotton (Ramney [55]), V. dahliae in eggplant (Sivaprakasam and Rajagopalan [62])
and Phytophthora parasitica in tobacco (Apple [3]). Decrease in disease severity
following N-fertilizers, has been reported for blast disease caused by Piricularia
oryzae (Matsuyama and Dimond [40], Veeraju and Prasad [68]), Helminthosporium
turcicum in maize (Singh and Sharma [60]), Sclerotium rolfsii in sugar b":et (Leach
and Davey [36]), and in tomato (Mohr and Watkins [43]).
2.3. Effect of various N-forms on the same disease
In some cases, one form of nitrogen increased disease severity, wheres another
decreased it. Thus, increase in disease severity by ammonium and decrease of the
same disease by nitrate have been reported with F. solani f. sp. phaseoli in bean
(Weinke [74] vs. Maurer and Baker [41]), F. oxysporum f. sp. Iycopersici in tomato
(Woltz and Jones [76]) and F. oxysporum f. Iini in cotton (Hughes [30]). Rhizoctonia
solani, which causes damping off in many plants,'is also favoured by NH 4 + and decreased following application of N0 3 - to the soil (Papavizas [51]). An exception to
this rule seems to be G, graminis in wheat, which has been reported to be favored by
N0 3 - and suppressed by NH4 + applications (Smiely and Cook [65]). According to
Hughes [30] the same fertilizer favored Fusarium disease in cotton and decreased crop
yield in a susceptible cotton variety, but suppressed disease and increased crop yield
in a Fusarium-tolerant cotton variety.
2.4. Effect of 'balanced' N-nutrition
Upsetting the NPK balance of mineral fertilizers usually enhances disease development
and severity (Abdel-Raheem and Bird [1], Capetti [7], Hughes [30], Sidorova and
Makhmudov [59], Ragab and EI-Labban [54]). In the case of Fusarium disease the
decrease in severity under balanced nutrition is probably due to a faster rate of root
and stem maturation (Chi and Hanson [9]). Warren and Kommedahl [72] found that
Fusarium seedling blight in wheat averaged 1-2% when NPK fertilizer and wheat
residues were present as compared to 11-14% when both were absent. In a long-term
study (run over 10 years) on the effect of fertilization on pathogen activity, Curl and
Rodriguez Kabana [10] examined the effect of NPK, lime and minor elements on
soil microbial activity, on the behavior of Rhizoctonia solani and F. oxysporum f. sp.
vasinfectum and on crop yield. All plots were under a 3-year rotation consisting of
cotton, corn, wheat and soybean. Most plots carried a winter legume (vetch and
crimson clover) in the rotation. It was found that populations of bacteria were generally
higher in plots that received more complete fertilization than in poorly fertilized ones.
The high fertilization plots also supported high yields. It is thus possible that in addition to the effect on the host, balanced fertilization affects the pathogen through the
enhancement of the activity of the soil microflora.
104
2.5. N-fertilizers and organic amendments
The effect of fertilizers on plant disease is greatly influenced by organic amendments.
Thus, Fusarium root rot of bean was suppressed by a high C : N ratio. Adding nitrogen
nullified this effect (Maier [38], Maurer and Baker [4], Snyder et al. [67]). Papavizas
[47] who studied the effect of 23 organic and inorganic amendments on Thieloviopsis
basicola, which causes black rot ofmany plants in the southern region ofihe United States, found that the pathogen was favored by various forms of inorganic N, resulting in
severe root rot of bean. On the other hand, inoculum density and disease severity were
reduced by incorporation of dry plant materials such as alfalfa hay and corn stover.
The polyvorous pathogen Macrophoniina phaseolum is suppressed by low C: N and
favored by high C: N ratio in organic amendments, the decrease being correlated
with the increase in microbial activity in the soil (Dhingra and Sinclair [11]).
2.6. pH effect and N-fertilizers
Smiley [66] extensively reviewed the literature concerning the importance to root
infection of forms of nitrogen and the pH in the root zone. His survey supports the
hypothesis that the form-of-N-effect on diseases caused by soil-borne plant pathogens
is often also a pH effect, with NH 4 +-N acting to reduce the rhizosphere pH and with
NOr-N acting to increase it, following their uptake by host's roots, inducing pH
differences up to 2.5 units. Thus, suppression by ammonia-N and low pH was reported
for Phymatotrichum omnivorum in cotton,Th. basicola in tobacco, O. graminis in
cereals and turf, V. dahliae and V. albo-atrum in tomato, eggplant, cotton and potato,
and S. scabies in potato. On the other hand, suppression by N0 3 - and/or high pH
was reported for S. rolfsii on sugar beet and tomato, F. 'solani f. phaseoli in bean,
F. roseum f. cerealis 'Culmorum' in wheat, F. oxysporum f. sp. lycopersici in tomato,
F. oxysporum f. vasinfectum in cotton, and F. oxysporum f. chrysanthemum inchrysanthemum.
The author suggests that manipulati'on of the rhizosphere pH could be an important
means for complementing multigenic resistance which is quite sensitive to environmental conditions (i. e. F. roseum). In contrast, this system would be of little use for
favoring monogenic resistance to vascular pathogens (F. oxysporum, Verticillium),
since this form of resistance is relatively insensitive to the environment.
2.7. N-fertilizers and inoculum quality
A hitherto little studied aspect of mineral nutrients on soil-borne plant pathogenic
fungi is their effect on inoculum quality. A pioneer ,,:"ork in this respect was done by
Weinhold et al. [73], who showed that the virulence of Rhizoctonia solani to bean
seedlings was greatly influenced by the exogenous nutrition supplied to the pathogen
in the growth medium.
Zilberstein, Chet and Henis (unpublished) examined the effect of nitrate concentration
on the germinability of microscJerotia of Verticillium dahfiae, which had been produced
on a Czapek agar medium containing various concentrations of nitrate. They found
that germinability was affected by N0 3--N concentration of both production and
germination media. Highest germinability was observed with MS produced on Czapek
medium containing 0.2% N0 3--N and germinated on a medium of the same compo105
sltlOn. Increasing N-concentration of production or germination medium, or both,
adversely affected germinability (Table 2).
Tablc 2. Effect of nitrate concentration in growth and germination media on the germinability of
the microsclerotia of Vcrticillium dahliac".
N0 3 --N in
growth medium
%
N0 3 --N in germination medium (%)
0
0.2
0.5
2
4
Germinability of MS""
0.2
0.5
1
2
%
AGT
%
AGT
%
AGT
%
AGT
%
AGT
%
AGT
39
37
26
20
17
15
14
10
73
43
37
29
99
19
18
14
50
30
33
20
34
18
17
14
33
17
17
17
16
14
27
21
IS
10
17
16
12
8
13
11
12
10
9
7
13
9
16
10
" Microsclerotia collected after 14 days of incubation at 28°C.
"" Percent of germinating microsclerotia (MS) and average number of germinating tubes (AGT)
emerging from each microsclerotium (10 MS per observation) after incubating for 48 h at 28°C.
3. Potassium
As early as in 1946, Walker and Forster [70} reported that Fusarium wilt of tomato
was favored by high nitrogen and low potassium. Sadasivan [57} found that a mixture
of NPK only slightly affected the index of Fusarium wilt of cotton. However, treatment
with nitrogen alone resulted in an increase, whereas P and especially K, markedly
decreased the wilt index. The percentage of the microflora antagonistic to Fusarium
vasin/ectum was high with P and K treatments and low with N treatments. An increase
in Fusarium wilt of carnation by high N and low K was observed by Gasiorkiewicz [17}.
Similarly, Wade [69} reported a decrease of root rot of peas caused by Aphanomyces
euteiches following addition of KCl to a K-deficient soil. This pathogen was also
suppressed by side dressing~ of amino compounds, especially when combined with
KCl (Papavizas and Davey [49}). Another disease reported to be reduced by potassium, is Verticillium wilt of eggplant (Sivaprakasam and Rajagopalan [6J}). On the
other hand, RolI-Hansen [56} has reported an increase in post-harvest rot of carrots
caused by Centro!ipora following fertilization with potassium. Aggravation of potato
scab caused by Streptomyces scabies was also reported by McNew [42}. According to
Chapman [8}, the CalK ratio may be important in club root of cabbage caused by
Plasmodiophora brassicae, high Ca and low K lessening disease severity.
4. Calcium
Hallock and Garren [19} found that gypsum (CaS0 4 ·H20) application at a rate of
680 kg/ha to peanut, significantly reduced pod rot caused by Pythium myriotylum
and R. solani. On the other hand, decreased Ca in pods was associated with treatments
of both MgS04 and K 2 S0 4 , the critical concentration of Ca++ in pods required for
106
tolerance being ca. 0.2% (Hallock [20]). According to Halterlein and Lambeth [21],
Ca++ + Mg++ had a direct effect on blossom end-rot incidence in Lycopersicum
esculentum. The formation of lesions in bean stems by R. solani was suppressed by
Ca++. This was attributed to the formation of calcium pectate which is less available
to the lytic enzyme polygalacturonase than pectic acid (Bateman [5]). Calcium has
been also shown by Bateman and Beer [6] to decrease southern blight caused by
S. rolfsii by neutralizing the oxalic acid produced by the pathogen which presullmbly
plays an important role in disease development. Jonesand Woltz [31] used hydrated
lime + ground limestone as an amendment to increllse the pH of the soil solution to
9.0, thus reducing the incidence and severity of Fusarium wilt of tomato caused by
F. oxysporum f. sp. lycopersici race 2. Addition of micronutrients reversed disease
control, indicating that control was achieved as a result of decrease in micronutrient
availability. Recently, calcium has been shown by Alien and Nandra [2] to increase
sporulation of 10 Phytophthora isolates from agave.
5. Sulphur
Fertilizing with sulphur powder fulfils three purposes: it serves as a source of S04-(after oxidation by soil microorganisms) to the plant; it may directly affect pathogens
and its oxidation in soil usually results in a decrease in soil pH. It has been used
extensively as a soil amendment to suppress common scab of potato (Walker [71])
caused by Streptomyces scabies.
6. Phosphorus
Phosphorus is a nutrient for plants and micro-organisms second in importance only to
nitrogen. An interesting aspect of this element is its favorable effect on the symbiotic
association between plants and some soil fungi (Lamb and Richards [34, 35]). According to Newhook and Podger [45] little leaf disease of exotic conifers caused by
Phytophthora cinnamomi is essentially a reflection of nutrient deficiencies, since it is
corrected by single applications of fertilizers. The critical element, however, is not
always the same, being phosphorus in New Zealand and nitrogen in the United States.
In New Zealand, phosphate application initiates a sequence of interactions, resulting in
increased mycorrhizal development. The complexity of the interactions between the
organism involved in disease and fertilizers is.emphasized by the fact that phosphate
application does not always provide protection. An interesting indirect effect on disease
following mycorrhiza development was also demonstrated by Marx [39], who.showed
that some mycorrhizal fungi produced antibiotic substances which presumably inhibited the pathogen.
7. Other minerals
Both plants and microorganisms require trace elements for growth. Some trace elements, such as Cu and Zn, are highly toxic to microorganisms at rates which are well
above the nutritional requirements and exhibit selective toxicity towards pathogens.
107
The literature regarding the effects of trace elements on wilt diseases has been extensively reviewed (Sadasivan [57)). Suppression of the production of fungal toxins and
of cellulolytic and pectic enzymes involved in pathogenesis may explain their role in
reducing wilt diseases. However, contradictory reports concerning the increase of
wilt diseases by trace elements (Hart [22], Jones and Woltz [32]) make it impossible
to draw general conclusions regarding their effect on disease.
Lewis [37) extensively studied the effect of 11 cations, applied as mineral salts, on root
rot of peas caused by Aphanomyces euteiches. In greenhouse experiments, Al+++,
Ca++, Cu++, and Zn++ significantly reduced disease at concentration rates of
50-100 [Lg/g soil. The cations were effective in combination with various anions, mainly
chlorides, nitrates, phosphates, sulphates and carbonates, and their effectivity was not
altered by the addition of a complete fertilizer (20 :20: 20). The effect of Al+++, Cu++,
and Zn++ (but not Ca++) on disease reduction lasted throughout 3 successive pea
plantings. Hadar, Chet and Henis [unpublished] studied the effect cif these cations on
Rhizoctonia disease of beans. In contrast to A. euteiches, disease severity in the greenhouse was significantly increased following their application to soil at the rates of
50-100 [Lg/g soil (Table 3).
Recently, Orellana et al. [46] reported that soluble aluminium at a rate of 8 [Lg/g
decreased Verticillium albo-atrum on sunflower at pH 4.7 or less. Addition of CaC0 3 •
however, increased disease severity. An interesting observation was recently made
by Primavesi et al. [53] who reported a correlation between blast disease of rice
by Pyricularia oryzae and low soil content of microelements, especially Cu++, in
Brazilian soils. Addition of 3 kg CuS0 4/ha with irrigation water to plants which had
been treated with NPK, gave the highest yield. Disease was completely controlled in
soil containing 18 ppm Mn++ and 2 ppm Cu++.
Table 3. Effect of some mineral elements on severity of damping off disease of beans (Phaseolus
vulgaris) caused by Rhizoctonia solani·.
Element
0
Mn
Zn
Mg
Concentration
in soil, [lg/g
0
lOO
lOO
100
Infection
index"
Diseased
plants (%)
0.74
0.88
1.32
1.0
29
36
78
38
• Inoculum concentration I [lg/g soil of propagules of 490-590 [l size prepared from 7-day-old
cultures which had been grown on Potato Dextrose Agar.
•• Infection index rating from zero - no disease, to 5 - stem completely gird led with R. solani, after
incubation of 21 days in the greenhouse. Average of 5 replications.
8. Conclusions
The information available on the effect of mineral nutrients on soil-borne pathogenic
fungi and their hosts allows only few generalizations to be made, because of the great
differences existing in the nutritional requirements of the organisms involved, as well
as in their micro- and macro-environments. Yet, in some cases (e. g. increase in severity
of Fusarium diseases due to excessive nitrogen; decrease in disease severity by balanced
108
fertilization; control of Aphanomycesroot rot by trace elements) the available information seems to be fairly consistent. Our ability to predict side effects of mineral nutrients
on plants, and to employ them for controlling soil-borne pathogens, depends on a
better understanding of the mechanisms involved, a closer coordination between
workers and a better system of collecting data and analyzing new observations on the
effect of mineral nutrients on diseases all over the world.
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112
Fertilizers and Root Diseases of Cereals
J. M. Lemaire and B. Jouan, INRA, Plant Pathology Laboratory, Rennes/France
Summary
It is difficult to generalise about the influence of manuring on foot and root diseases of cereals. The
approximate picture seems to be that potassium has no effect, phosphorus a slight beneficial effect;
the effect of nitrogen is open to discussion but seems to be more often unfavourable especially when
applied early in the season. Nitrogen can have opposing effects at all stages of the life cycle of the
parasite and of the relationship between host and parasite. For example its effect is beneficial with
regard to the conservation of inoculum because it reduces the time taken by plant residues to rot
down but, at the same time, application of nitrogen to the straw makes the parasite better able to
survive so long as crop residues are present. On balance, then, is its influence positive or negative?
The answer to this question probably varies according to locality, climate and cultural technique.
In the case of soil born disease we are very much concerned with the interactions between host,
parasite and the environment and it is rare that a factor affects the whole in the same direction.
There is much interest in the effects of fertilisers and amendments on soil biology and we are only
now at the beginning of research in this field.
Resume
11 parait difficile de degager une ou plusieurs idees simples sur I'influence de la fumure sur les maladies du pied des cereales.
En premiere approximation, la potasse n'aurait pas d'incidence, l'acide phosphorique un effet
legerement benefique, J:azote un effet discutable mais plutot dHavorable surtout si les applications
sont precoces. L'azote est susceptible d'agir dans des sens opposes a presque tous les niveaux du
cycle du parasite et de son interaction avec la pIante hote. A titre d'exemple, on peut rappeler qu'au
niveau de la conservation de I'inoculum de pietin-echaudage, son action est benefique puisqu'il
contribue a reduire le temps de degradation des residus de culture et par la Iimiter la duree de conservation de I'inoculum, mais en meme temps les applications d'azote sur la paille donnerait au
parasite UI; meilleur pouvoir pour se conserver tant que les residus de culture existent. Le bilan est-il
positif ou negatif? La reponse doit vraisemblablement varier avec le lieu, le climat, les techniques
culturales.
Pour les maladies d'origine tellurique, I'interaction plante-parasite-milieu est tellement forte qu'it
est rare qu'un facteur agisse toujours dans le meme sens. Toutefois, it semble que les consequences
des fumures et des amendements sur les biocenoses du sol presentent le plus d'interet et que nous
n'en sommes qu'au debut des recherches dans ce domaine.
1. Introduction
Cereal diseases can be divided into two major groups according to the way in which
they spread. Those which are not dispersed by spores, or only to a limited extent, pass
113
through a major part of their life cycle in the soil and are generally responsible for the
group of root diseases which become increasingly serious in intensive cereal glowing.
We shall discuss among these, those which are seen on the roots and the stem bases,
exemplified by take-all, eyespot and, to some degree, brown foot rots.
H is obvious that any measures which tend to modify physico-chemical conditions
in the soil will have major effects on the development of this type of disease. The use
of fertilisers lime or manures could therefore influence disease development in three
ways:
- by influencing the parasite directly or indirectly particularly as regards its survival
in the soil
- by influencing the resistance of the host plant
- by effects on the biotic environment of both fungus and plant.
These aspects will be discussed in two sections, the first concerned with general aspects
of disease and fertilisers, the second with modifications to the microbiological environment caused by manures and fertilisers.
2. The biology of disease organisms and the influence of manuring
Take-all of cereals, caused by Gaeumannomyces graminis is a serious disease which
reduces yield and quality of harvest; the inoculum is carried over on susceptible
grasses and on crop residues and regrowth. The carry-over is fairly short-lived on
light textured, chalky and alkaline soils because plant residues break down rapidly
and, in this case, the use of nitrogen fertiliser or green manure has little practical
effect on survival of the parasite. On loamy or acid soils the disease can remain
active for several years and, in this case, any operation which tends to accelerate the
break down of plant residues and roots will diminish the capacity of the parasite to
survive. Much the same applies in the cases of eyespot (Cercosporella herpotrichoides)
and foot rots caused by Fusarium roseum var. culmorum.
Spreading nitrogenous fertiliser on the straw after harvest thus indirectly tends to
lessen the incidence of the diseases, though several authors (Garret [5], Chambers
[2], Deacon [4] and West and Thrower [22]) have shown that nitrogen applied to
the straw directly promotes the survival of G. graminis by restoring its saprophytic
potential. The same does not apparently apply in the case of C. herpotrichoides. In
practice it is difficult to achieve the proper balance and we think, like Scott [i6] and
Shipton [17], that the post-harvest treatment of straw is of little practical importance.
In fact the spreading of N fertiliser on the straw would only be of advantage in oceanic
climates (water being essential for rotting down of the straw) and on soils of pH
below 6.
In the case of Fusarium roseum Smiley et al. [i8] stated that F. roseum f. sp. cerealis
culmorum was markedly reduced following application of liquid ammonia but this
had no practical effect on the following crop as the number of affected shoots was
higher on the plots receiving N than on the controls.
Eyespot (Rhizoctonia solani) affects a wide variety of hosts and has for this reason
been much studied though losses due to this disease are seldom very severe in cereals.
Das and Western [3] showed that the growth of this fungus in sterile soil was increased
by balanced fertiliser, by low rates of potassium and by very high rates of phosphorus;
114
its growth was decreased by high rates of nitrogen and by very high rates of potassium.
However, here again, the effects on the fungus were not reflected in the effects on the
crop. The disease was more severe at high rates of nitrogen while phosphorus and
potassium had no effect. The conditions which favour the establishment and multiplication of the fungus in the soil seem to be the opposite of those which increase its
virulence.
The examples which we have mentioned show that the effect of fertiliser on the parasite itself should not alone be taken into consideration and that fertilisers ar~ likely
to have a more important effect on the interaction between host and parasite. Fertilisers have important effects on the physiology of the plant. Potassium generally has
little effect on cereal disease on our soils, however, Ponchet and Coppenet [15]
reported that potash seemed to increase the disease when phosphorus was deficient.
The general view seems to be that phosphate tends to reduce disease while nitrogen
tends to increase it. Vanterpoo! [21] showed that cereal rots due to pythium were
more serious on soils high in N and low in P. Cassini [1] showed that imbalance
between Nand K in the fertiliser could be the cause of loss due to Fusarium roseum.
In practice, balanced manuring tends to reduce the incidence of disease through its
beneficial effect on the plant. Thus high losses from take-all and eyespot are common
on soils low in nitrogen;
We have had the opportunity to observe the development of take-all and eyespot in
an experiment at the INRA station at Lusignan/France; the principal aim· of this
experiment was to measure on test crops of maize and wheat the effect of three years
under lucerne on N supply from the soiL The four treatments detailed in Table 1 were
replicated 6 times.
.
'.
Table 1. Effect of 3 year lucerne ley and rate of N applied to test crops on the incidence oftake-all
and eyespot
Treatment
I. 3 years maize ..........
2. 3 years maize ..........
3. 3 years maize ..........
4. 3 years lucerne .........
Test crop and N rate (kg/ha)
% plants severely
affected by disease
Year 4 maize
Take-all
50
100
150
0
Year 5 wheat
50
100
150
0
Eyespot
%
sig
%
sig
25
16
23
43
b
a
b
c
49
62
60
67
a
b"
b
b
Wheat on treatment 4, deficient in nitrogen, was the most severely affected by take-all
Moderate rates of nitrogen increased resistance but at very high rates the balance is
again in favour of the disease.
However, the effect of N fertiliser needs to be described in greater detail as it depends
on the form of nitrogen and the time of application. Some authors have reported a
reduction in take-all following application of ammoniacal (Garret [6]) or a mixture
of nitrate and ammoniacal (Hornby et al. [9]) forms. On the other hand it is recognised that, at equivalent rates of application, early nitrogen favours take-all much
more than late (Ponchet and Coppenet [15], H uber [8] and Sterter [20]). In fact,
apart from effects on the environment, nitrogen application has two opposing effects;
115
it favours the plant by promoting the development of new crown roots but makes
the roots less resistant to infection - Weste and Throner [22]. These opposing effects
explain some of the contradictory results which are observed in practice.
We have noticed, with M. Coppenet (unpublished results) that some trace-elements
are also important in connection with take-all. Thus, four copper sulphate sprays
applied to correct copper deficiency on a barley crop, improved its health, the percentage of plants killed by take-all being reduced from 16.2 to 5.4. Further we have shown
in both field and pot experiments that take-all in wheat was reduced by manganese
deficiency.
3. The influence of fertilisers and other measures on soil micro-biology and its
consequences for the development of root disease
It is well known that take-all can be serious on both alkaline and acid soils. A large
change in pH following excessive lime application can cause particularly severe
take-all attack (Ponchet and Coppenet [15]). The disease is often particularly virulent
shortly after the reclamation of acid or alkaline soils (Lemaire and Jouan [23]). In
the two examples cited, the severe take-all attack is connected with a severe modification of the microbial equilibrium which favours the establishment and proliferation
of the parasite. Application of nitrogen can equally modify soil microbiology either
by changing the pH of the root environment (Smiley and Cook [19]) or by favouring
the groups concerned in the nitrogen cycle (ammoniators, nitrifiers, proteolytics,
denitrifiers). This is perhaps why the use of 2-chloro-6-trichloromethyl pyrimidine
(N-serve 24), which slows down nitrification, can work against the increase in take-all
which would follow the application of ammoniacal N.
The influence of green manures is mainly through the microflora; Huber and Watson
[7] showed that nitrification is high with a green manure like lucerne, less with wheat
and very weak with barley. On our part, we have shown that leguminous green manures
have a more favourable effect on the cellulolytic bacteria and the whole bacterial
flora than do green manures based on crucifers or grasses. Soya is the most promising
of the leguminous (unpublished work).
Mineral fertilisers and adjustment of pH have indirect effects on disease by their
effects on antagonistic organisms. Thus, Kaufman and Williams [11] showed that
Penicillium funiculosum which is antagonistic to Fusarium roseum and Rhizoctonia
solani is promoted by P and K fertilisers. Nitrogen has a similar beneficial effect on
soils cropped with wheat, but the converse applies with maize.
It seems to us that it is mainly through their action on the microflora that various
treatments affect the health of wheat. The very numerous microbiological analyses
that we have conducted show that the take-all fungus is affected by different groups
of micro-organisms. Ammonifying, nitrifying and denitrifying bacteria stimulates
fructification while proteolytic and amylolytic bacteria seem to be unfavourable to
the parasite (Lemaire et al. [12]. As it is not possible successfully to establish
organisms in the soil without 'biological preparation' we have tried to stimulate the
antagonistic microflora already present in the soil by incorporating the appropriate
nutrient substrates ( Jouan and Lemaire [10]). Several types of protein (gelatine, soya
flour, lucerne flour, etc.) have exhibited an unfavourable influence on G. graminis
in a number of situations. Plant health at harvest was improved (less take-all and
116
eyespot) and grain quality was bettered (higher specific weight, higher N content and
baking quality). We have also found that soya flour reduces loss due to Rhizoctonia.
The nutrient substrates act by stimulating a specific microflora vigorously but over
a short period. The efficacy of the treatment varies with temperature, humidity and
soil type. In pot culture at 20 0 e the activity of proteolytic organisms reaches a maximum 15 days after incorporation, their number being from 1000 to 10 000 times
those found in the control. A week later their antagonistic effect becomes evident in a
reduction in the level of the disease organism. The mycelium breaks up, no more
perithecia are produced and activity is reduced by 80-100%.
These experimental results have, unhappily, no immediate practical application on a
field scale in the light of the protein shortage and because not all soils respond to
treatment in the same way. However, the' results may be followed up by the use of
industrial "or agricultural byproducts.
4. Bibliography
1. Cassini, R., Cassini, KemIe and Pauvert, P.: La lutte integree dans les rotations cerealieres.
Bull. Techn. d'Inf. 297, 201-210 (1975).
2. Chambers, S. c.: Some factors affecting the survival of cereal root pathogen Ophiobolus graminis in wheat straw. Aust. J. Exper. Agric. Anim. Husb. I, 90-93 (1971).
3. Das, A. C. and Western, J. H.: The effect of inorganic manures, moisture and inoculum on the
incidence of root disease caused by Rhizoctonia solani Kuhn in cultivated soil. Ann. appl.
BioI. 47, 37--48 (1959).
"
,
4. Deacon, J. W.: Behaviour of Cercosporella herpotrichoi'des and Ophiobolus graminis on buried
wheat plant tissue. Soil Biology and Biochemistry 5, 339-353 (1973).
5. Garett, S. D.: Soil conditions and the take-all disease of wheat. Ann. Appl. BioI. 23, 667-669
(1936).
6. Garett, S. D.: Soil conditions and the take-all disease of wheat. VI. The effect of plant nutrition
upon disease resistance. Ann. Appl. BioI. 28,14-18 (1941).
7. Huber, D. M. and Watson, .R. D.: Effect of organic amendment on soil-borne plant pathogens.
Phytopathology 60, 22-26 (1970).
8. Huber, D. M.: Spring versus fall nitrogen fertilisation and take-all of spring wheat. Phytopathology 62, 434--436 (1972).
9. Hornby, D. and Goring, C.A.I.: Effects of ammonium and nitrate nutrition on take-all disease
of wheat in pots. Ann. Appl. BioI. 70,225-231 (1972).
10. Jouan, B. and Lemaire, J. M.: Modifications des biocenoses du sol. I. Etude preliminaire de
. I'incorporation de substrats nutritifs au sol et ses consequences pour l'evolution d'agents
phytopathogenes d'origine tellurique. Ann. Phytopath. 6, 297-308 (1974).
11. Kaufmann, D. D. and Williams, L. E.: Influence of soil reaction and mineral fertilisation on
numbers and types of funge antagonistic to four soil-borne plant pathogens. Phytopathology
55, 570-574 (1965).
12. Lemaire, J. M., Ponchet, J. and Jouan, B.: Contribution a l'e1ude des facteurs physiques et
microbiologiquesqui indulsent la fructification de l'Ophiobolus graminis SACC = Linocarpon
cariceti B. et BR. Ann. Epiphyties 17, 61-73 (1966).
13. Lemaire, J. M. and Jouan, B.: Modifications microbiologiques entrainees par Ia mise en culture
de sols nouvellement defriches. Incidence sur I'installation de l'Ophiobolus graminis SACC
(Linocarpon cariceti B. et BR.) et du Streptomyces scabies (Thaxt) Waksman et Henrici. Ann.
Epiphyties 17, 313-333 (1966).
"
14. Ponchet, J. and Coppenet, M.: Influence de la fumure minerale sur le developpement du pietinechaudage: Linocarpon cariceti B. et BR. Ann. des Epiphyties 13, 277-283 (1961).
15. Ponchet, J. and Coppenet, M.: Influence de divers facteurs culturaux sur le developpement
du pietin-echaudage: Linocarpon cariceti B. et BR. Ann. des Epiphyties 13, 285-291 (1962).
16. Scott, P. R.: Effects of nitrogen and glucose on saprophytic survival of Ophiobolus graminis
in burried straw. Ann. Appl. BioI. 63, 27-36 (1969).
117
17. Shipton, P.J.: Influence of stubble treatment and autumn application of nitrogen to stubbles
on the subsequent incidence of lake-all and eyespot. I'lant. Path. 21,147-155 (1972).
18. Smiley, R. W., Cook, R.J. and Papen Dick, R. J.: Fusarium foot rot of wheat and peas as
influenced by soil applications of anhydrous ammonia and ammonia azide solutions. Phytopathology 62, 86-91 (1972).
19. Smiley, R. W. and Cook, R.J.: Relationship between take-all of wheat and rhizosphere pH in
soils fertilized with ammonium vs nitrate-nitrogen Phytopathology 63, 882-290 (1973)
20 Stetter, S.: N.P. of K. G0ds kings indflydelse pa fodsygeangred ved kontinuerIig korndyrkning.
(Influence of artificial fertilizers on Ophiobolus graminis and Cercosporella herpotrichotdes in
continuous cereal growing). Tidsskr. f. PlanteavI. 75, 274-277 (1971).
21. Vanterpool, T. C.: Studies on browning root-rot of cereals. Ill. Phosphorus nitrogen relations
on infested fields. Canad. J. Res. 13, 220 (1935).
22. Weste, Gretna and Thrower, L. B.: The effect of added nitrate on the growth of Ophiobolus
graminis. Plant and Soil 35, 161-172 (971).
118
Nitrogen and Leaf Diseases of Spring Barley
J. F. Jenkyn, B. Se., Ph. D., Plant Patholc gy Department, Rothamsted Experimental Station.
Harpenden, Hertfordshire/Great Britain
'
Summary
,
Susceptibility of cereals to leaf pathogens is often increased by nitrogen fertilizers. These diseases
may, therefore, limit the increases in yield potentially obtainable from extta nitrogen. Damage may
be increased further if nitrogen is applied late, so the optimum time to apply the fertilizer can depend
on whether or not fungicides or resistant varieties are used.
Resume
La sensibilite des cereales aux pathogenes des feuilles est souvent accrue par les engrais azotes. Ainsi
done, ces maladies peuvent diminuer les rendements qu'on pourrait obtenir potentiellement par des
doses supplementaires d'azote. Il y a augmentation des degiHs en cas d'application tardive de I'azote.
Ainsi done I'epoque optimale de I'application de ces engrais depend du fait si I'on' a utilise ou non
des fongicides ou des varietes resistantes.
1. Introduction
Susceptibility to pathogens can be modified by changes in crop nutrition. On cereals,
the incidence of Erysiphe graminis (powdery mildew), for example, is affected by all
three major nutrients, nitrogen, phosphorus and potassium (Glynne [9j, Last [l8}).
Of these, nitrogen is of particular interest for although it usually increases susceptibility
it is often used in large amounts. In England and Wales, average use of nitrogen on
spring barley in 1974 was estimated to be 73 kg/ha; the corresponding estimates for
phosphorus (P 205) and potassium (K20) were 39 kg/ha of each (Church [5}).
It remains uncertain why much nitrogen increases suceptibility to diseases, but
evidence is accumulating, mainly from experiments with wheat (Hebert et al. [lO),
Dilz and Schepers [7}, Ellen and Spiertz [8}) , that the increases in yield obtained by
applying extra nitrogen ('response') may be limited by leaf pathogens. Fungicides
, effective against many of the leaf pathogens of cereals are increasing both in availability
and use, so it is important to understand their interactions with nitrogen so that both
the fungicides and the increasingly costly fertilizer can be used most efficiently.
This paper considers some of the effects of nitrogen and fungicides on leaf diseases
and yield of spring barley.
119
2. Effects of nitrogen on the susceptibility of barley to leaf pathogens
2.1. Disease incidence
The amount of leaf affected by pathogens on spring barley is usually increased when
nitrogen fertilizer is applied (see, for example, Last [i8) and Tables 1 and 2). Occasional exceptions,as reported for mildew in 1970 by Jenkyn and Moffatt [14} (Table 1),
are difficult to explain but may, perhaps, be due to unusual weather conditions affecting
uptake.
These increases in susceptibility probably occur with all susceptible varieties, but not
always equally. Jenkyn [ll} found that with no nitrogen fertilizer Deba Abed was
less affected by leaf blotch (Rhynchosporium secalis) than Cambrinus but with 132 kg
N/ha Deba Abed had more disease than Cambrinus (Table 2). If such interactions are
common, they may explain some of the variability in results when varieties are compared at a number of sites.
Table 1. Effects of nitrogen fertilizer on incidence of mildew on spring barley at Rothamsted in 1970
and 1971 (from Jenkyn and Moffatt [I4}).
% leaf area affected by mildew
(3rd youngest leaf at G. S.· 10.5-11.1)
Nitrogen
(kg/ha)
1970 (5 varieties)
38
75
113
S.E
.
.
.
.
6.2
4.9
4.2
±0.30
1971 (6 varieties)
17.0
21.6
25.7
± 0.69
• Growth Stage (Large [I5})
Table 2. Effects of nitrogen fertilizer on incidence of leaf blotch (Rhynchosporium secalis) on spring
barley in 1967 (from Jenkyn [ll}).
Nitrogen
(kg/ha)
% leaf area affected by leaf blotch
(flag leaf at G. S. 1004-11.1)
Variety
0
66. . . . . . . . . . . . . . . . . . . . . . . . .
132.
..
.
.............
..
.. . . ..
Proctor
Cambrinus
Deba Abed
0.4
1.3
4.5
1504
21.3
30.5
3.6
20.5
57.3
'------v~----~
S.E.±2.75
2.2. Pathogen growth
At present there are few data to explain the large effects which nitrogen fertilizers
often have on the incidence of foliar diseases on cereals. Nitrogen, by increasing
growth, gives a denser crop and therefore a more humid environment, which may be
important, especially for those pathogens requiring free water for infection. However,
120
Last [17] considered this physical effect to be of little importance for powdery mildew
on wheat.' This view is supported by data obtained by Bainbridge [1] using well
spaced barley plants (Table 3). Nitrogen had no effect on spore germination or
appressoria formation but increased the numbers of successful infections, colony
growth rate and spore production. Colony growth and sporulation seemed most
affected by an increase in nitrogen from 50 to 100 mg/kg soil whereas infection was
most affected by increases above 100 mg/kg soil.
In contrast to observations made on crops, barley seedlings inoculated with Rhynchosporium secalis in glasshouse experiments developed more lesions where given no
nitrogen than where nitrogen was applied (Table 4) (Jenkyn and Griffiths [13]).
Doubling nitrogen from c. 7.5 to c. 15.0 g/m2 of soil surface area had a similar but,
smaller effect. These results suggest that the increases in leaf blotch commonly
observed in field crops given much nitrogen are due to increases in pathogen growth
or sporulation, or that the proportion of spores which infect is influenced by increased
humidity within the crop.
Table 3. Effects of nitrogen on growth of mildew on spring barley in a pot experiment (from
Bainbridge [1]).
Nitrogen (mg/kg soil)
Germination (% of spores after 24 h) ...........
Appressoria (% of spores after 24 h) ...........
Infections (% of appressoria after 72 h) ..........
Length of colonies after 96 h (mm) ..............
Log No. spores in 6 h/mm 2 of pustule ...........
50
lOO
200
400
S.E.
66.5
59.7
3.7
0.47
2.97
69.1
59.4
4.8
0.83
3.24
68.1
60.2
8.5
1.05
3.33
67.4
59.3
16.8
1.10
3.39
± 1.46
±2.60
±°1.02
±0.05
±0.03
Table 4. Effect of nitrogen fertilizer on infection by Rhynchosporium secalis of seedling leaves of
barley grown in boxes (from Jenkyn and Griffiths [13]).
2nd leaf
Nitrogen
(g/m 2 of soil surface
area - approx.)
Numbers of lesions
Cambrinus
Proctor
Mean
0
7.5
15.0
6.4
4.9
4.4
1.5
1.0
1.0
3.9
2.9
2.7
v"
S.E.± 1.46
3rd leaf
0
7.5
15.0
4.8
3.3
3.0
S.E.±0.28
2.4
1:6
1.4
'--...----.S.E.±0.76
3.6
2.4
2.2
S.E.±0.29
3. Yield response of spring barley to nitrogen applied at different rates and times
In experiments on winter wheat using sulphur dust to control mildew, Hebert et al. [10]
demonstrated that mildew may affect both the response to nitrogen and the optimum
121
time to apply it. Only two amounts were tested though and responses could not be
fully explored. More recently Dilz and Schepers [7] have demonstrated the importance
of using a growth regulator to control lodging and fungicides to control diseases on
wheat crops given much nitrogen if maximum yields are to be obtained.
Effects of nitrogen and ethirimol (applied as a seed dressing to control powdery mildew)
on yields of spring barley were investigated by Jenkyn and Moffatt [14]. Yields were
often most increased by ethirimol where most nitrogen was given but these experiments
only tested nitrogen at three rates. However, Boyd et al. [3] as well as Needham and
Boyd [21] have described experiments which tested up to nine amounts of nitrogen
and have compared results from sites differing in incidence of leaf diseases. For most
experiments yield responses to nitrogen were best represented by two intersecting
straight lines but at sites affected by leaf diseases, smooth curves fitted the results
better than straight lines.
Recent experiments at Rothamsted and at Saxmundham (near the East coast of
England) have examined further the effects of diseases on the response of spring barley
to different amounts of nitrogen, applied at different times, in experiments using
fungicides to control the pathogens.
3.1. Effects of brown rust (Puccinia hordei) - Saxmundham 1973 and 1974
In 1973 and 1974 we tested the effects of the fungicide benodanil, to control brown
rust, on three varieties given three amounts of nitrogen at two times (Widdowson et al.
[26]). In both experiments, the fungicide increased yields more as more nitrogen was
given and more where nitrogen was applied as a top dressing in May, at growth
stage (G.S.) 4 (Large [15]), than where it was applied to the seed-bed in March
(Table 5). Controlling brown rust also increased the amount of nitrogen removed in
the barley grain. In 1973, yields of untreated susceptible varieties (Mazurka and Midas)
were more where nitrogen was applied to the seed-bed than where it was applied late
Table 5. Effects of the fungicide benodanil on grain yield (t/ha at 85% dry matter) of spring barley
(average of 3 varieties) given three amounts of nitrogen at two times (from Widdowson et al. [26J).
1973
Benodanil (B)
Nitrogen (kg/ha)
50
100
150. . . . . . . . . .. .. . . ..
.
...
Time of nitrogen
All in March
'l', in March; 'l', in May
All in May
.
.
.
S.E.!
S.E.2
.
.
1974
B
increase
4.23
5.06
5.25
4.36
5.49
5.65
+0.13
+0.43
+0.40
4.92
4.99
4.63
4.99
5.13
5.39
+0.07
+0.14
+0.76
~
±0.09l
±0.105
S. E.! for horizontal comparisons
S.E.2 for vertical and diagonal comparisons
122
B
increase
3.76
4.78
5.01
3.90
4.93
5.35
+0.14
+0.15
+0.34
4.96
4.66
3.93
4.91
4.89
4.39
-0.05
+0.23
+0.46
-..-'
±0.104
±0.095
as a top dressing, but yields of the resistant variety, Julia, and of susceptible varieties
sprayed with the fungicide, were most where all nitrogen was applied as atop dressing
(Figure 1). By contrast, seed-bed nitrogen in 1974 increased yields more than May
nitrogen, whether or not brown rust was controlled, presumably because there was
little rain after the top dressing was applied.
6
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/V
/V/
/1/
/1/
/V
/1/
/V
/1//
/1//
VVV
VI/v
VVI/
VVI/
v/V
v/V
+ //1/
wlUJ //1/
/I/V
Julia
1/71/
[7;
I//V
1/ /V
I//V
V/V
V/V
VV
I/V
I/v
VV/
1/ /1/
~~
V /1/
1/ /V
1/ /V
V/V
V/V
V 1/
V /
VV
VV/
vI/
vV/
/
v//
1/
1/
//
...J
...
UJw
v/
v//
v
...Jv ~
1//
·Mazurka
...
/
v
I//V"
V/v
V v
vVv
Midas
Fig. 1. Grain yield in 1973, of three barley varieties given nitrogen at sowing (E), in May (L) or half
at each time (E+ L), without (open histograms) or with benodanil sprays (from Widdowson et al.
[26J ).
3.2. Effects of mildew (Erysiphe graminis) and brown rust (Puccinia hordei) - Rothamsted 1975
In the Saxmundham experiments, fungicides to control mildew (ethirimol as a seed
dressing plus tridemorph sprays) were applied to all plots but an experiment at
Rothamsted in 1975 tested foliar sprays to control rust (benodanil) and mildew
(tridemorph) separately as factors. Their effects were tested on spring barley (cv.
Zephyr) given six amounts of nitrogen at two times.
The experiment was sown late (23 April) because the spring was very wet but there was
then little rain between mid-May and early September, so that yields were much
smaller than usual.
Nitrogen applied as a top Clressing, on 22 May (before the start of tillering), increased
yields much less than nitrogen applied to the seed-bed (Table 6). Brown rust did not
become prevalent until very late in the season but mildew was severe from the seedling
stages, so that tridemorph sprays (on 6 June, 24 June and 21 July) increased yields
much more than a benodanil spray on 24 June. As at Saxmundham in 1973 and 1974,
benodanil increased yields most where nitrogen was applied late (presumably because
123
Table 6. Effects of the fungicides tridemorph (T) and benodanil (B) on grain yield (t/ha at 85% dry
matter) of spring barley (cv. Zephyr) given nitrogen at two times (Rothamsted, 1975).
Time of nitrogen
Response to
All in April .............
Y. in April; % in May ...
All in May ...... - ......
3.06
3.11
2.57
T
B
TB
T
B
TB
3.83
3.50
3.25
3.27
3.23
2.97
3.78
3.58
3.54
0.77
0.39
0.68
0.21
0.12
0.40
0.72
0.47
0.97
S.E.
±0.100
late nitr9gen favoured rust more than did early nitrogen). By contrast, increases with
tridemorph were the same whether the nitrogen was applied early or late, but less
where nitrogen was applied as a split dressing (Table 6).
Increasing the amount of nitrogen applied to the seed-bed increased yields but
response was much greater where tridemorph was used to control mildew (Figure 2).
The fungicide did not seem to affect the amount of nitrogen needed to obtain maximum
yield.
Averaged over all fungicide treatments there was no detectable response to increasing
amounts of nitrogen applied late (Figure 3). However, response to late nitrogen was
apparently limited by both pathogens. Each fungicide, applied separately, increased
yield but it was only on those plots sprayed with both fungicides that a response to
increasing amounts applied late was obtained (Figure 3) (0.71 ± 0.349 t/ha by increasing
nitrogen from 25 to 90 kg/ha).
4·6
'0
.<:
-.
~
E
4·2
.
.,.;
~
..... 3-8
d>
~
.,..,
3-4
<:
.~
C>
3·0
2·6
0
20
40
60
Nitrogfn
80
100
120
140
(kg /ha)
Fig.2. Yields of spring barley given different amounts of nitrogen to the seed-bed, with (0) and
without (e) tridemorph sprays to control mildew.
124
---
4·4
co
-J:
~
...E
o-!
on
co
4·0
3·6
;:;
...
32
';;'
...
c
~
C>
2·8
2·4
0
20
40
60
Nitrogen
80
100
120
140
(kg / ha)
Fig.3. Average yields over all fungicide treatments, of spring barley given different amounts of
nitrogen as a top dressing (e) and yields of those plots sprayed with both tridemorph and
benodanil (0), to control mildew and brown rust respectively.
4. Utilization of fertilizer nitrogen
In studying the interactions between nitrogen and leaf diseases we should also consider
how pathogens may affect, either directly or indirectly, the uptake and metabolism of
nitrogen by the host.
In maize, uptake of nitrate can be stimulated by. a host-specific toxin produced by
Helminthosporium carb'onum (Yoder and Scheffer [28j). Powdery mildew can have a
direct effect on the assimilation and metabolism of nitrogen in barley leaves, causing
accumulation of ammonium (but not nitrate or nitrite) ions and evolution of ammonia
gas in the first four days after infection (Sadler and Scott [24 j ).
Uptake of nitrate by mildew-infected cereals may be affected by changes in transpiration (Priehradny [23 j, Martin et al. [20 j), and by smallet root systems (Last [19 j,
Paulech [22 j) which may be unable to fully exploit nitrogen leached down the soil
profile by rain. Utilization may also be affected by accelerated leaf senescence. o( Last
[l9j, Large and Doling [l6j, Brooks [4j, Simkin and Wheeler [25j, Jenkyn [l2j).
Accumulation of nitrate in crop plants, especially in the stem tissue, often occurs
because uptake exceeds assimilation (Darwinkel [6 j). In glasshouse experiments at
Rothamsted, nitrate concentrations in the sap of barley plants with and without
mildew were estimated using the method described by Williams [27j. In the first
experiment, spring barley seed (cv. Zephyr), either untreated or dressed with ethirimol
to control mildew, was sown in a soil-less compost. As expected, nitrate concentrations
were initially large in all plants (Table 7). In those treated with ethirimol, nitrate
concentrations deClined rapidly after G. S. 6-7 (early stem extension) but in untreated
plants (which had severe mildew) concentrations remained high.
In a second experiment, untreated and ethirimol-dressed spring barley seed (cv. Zephyr)
was sown in loam and given different amounts of nitrogen (Table 8). Unfortunately,
125
Table 7. Nitrate concentrations (ppm) in sap from stem bases of barley plants grown from untreated
seed or seed dressed with ethirimol fungicide to control powdery mildew.
Seed dressing
Growth stage
None.............................
Ethirimol .. . . . . . . . . . . . . . . . . . . . . . ..
5
6-7
10.1-10.2
10.4-11.1
11.2
750
625
875
350
700
125
387
59
185
I
Table 8. Nitrate concentrations (ppm) in sap from stem bases of barley plants grown from untreated
seed or seed dressed with ethirimol fungicide and given different amounts of nitrogen fertilizer.
Seed dressing
None
Ethirimol
S.E.
Nitrogen/pot· Growth stage
(g)
2--4
8-9
0.00
0.25
0.50
0.75
I
708
736
708
0
630
931
972
0.00
0.25
0.50
0.75
736
861
861
0
0
219
667
23
150
±37.3
±76.5
±64.3
I
10.1-10.2
1
I
553
778
0
I
11.1-11.2
0
0
475
753
0
0
0
0
±113.9
• Each pot contained 1.1 kg soil
mildew in this experiment was unusually severe, but the extent to which nitrate
accumulated in the stem bases clearly depended both on the amount of nitrogen
supplied and on mildew control. Accumulation of nitrate in plants given much nitrogen
and with severe mildew suggests that the capacity to utilize nitrogen is affected more
than its uptake. However, root size is probably not critical in the restricted confines of
a pot and further observations on field crops are necessary.
Diseases may also affect the efficiency with which nitrogen is used after it has been
incorporated in organic compounds. In healthy plants, organic nitrogen compounds
are translocated from old leaves, as they senesce, to younger leaves and eventually to
the ear. Experiments at Rothamsted show that in senescing leaves infected with
powdery mildew, the content of IX-amino nitrogen remains high (M.E.Finney, pers.
comm.), suggesting that such recycling is decreased.
5. Conclusions
It is clear that the symptoms caused by leaf pathogens are usually increased by
fertilizer nitrogen. Pathogens may also, either directly or indirectly, affect root growth,
transpiration and photosynthetic capacity, and thus the ability of the plant to absorb,
translocate and metabolize nitrogen compounds. At present we do not know how
these interactions affect the nitrogen requirements of plants. Under otherwise similar
126
conditions a diseased plant will produce less dry matter than a healthy plant and may
have a decreased capacity to utilize nitrogen, but it may be necessary to apply more
nitrogen to a diseased crop to compensate for a smaller root system and for diversion
of some nitrogen to the pathogen.
Without accurate weather forecasts it is difficult to predict the best time to apply
nitrogen to spring barley. Nevertheless, delayed application of all or part of the nitrogen
may decrease leaching losses and, on some soils and in some seasons, increase yields
(Bowerman and Harris [2]). However, recent experiments (Widdowson et al. [26]),
show that there is then an increased risk of damage by leaf diseases so that their
control by fungicides is therefore more important.
.
In the past, experiments investigating response of cereals to different amounts of
nitrogen have largely ignored pathogens but, now that the means to control them are
available, these interactions are deservedly beginning to receive more attention. If the
ways in which pathogens alter the plants response to nitrogen can be better understood,
it might be possible to improve recommendations for nitrogen use, relating it to choice
of variety, intended use of fungicides and other factors likely to affect disease incidence.
6. Bibliography
I. Bainbridge, A.: Effect of nitrogen nutrition of the host on barley powdery mildew. PL Path. 23,
pp. 160-161 (1974).
2. Bowerman, P. and Harris, P.B.: The rate and time of application of nitrogen on continuous
.
spring barley. Expl Husb. 27, pp.45-49 (1974).
3. Boyd, D.A., Yuen, Lowsing T.K. and Needham, P.: Nitrogen requirement of cereals. 1. Response
curves. J. agric. Sci. 87, pp. 149-162 (1976).
4. Brooks, D.H.: Observations on the effects of mildew, Erysiphe graminis, on growth of spring
and winter barley. Ann. appL BioL 70, pp. 149-156 (1972).
5. Church, B.M.: Use of fertilisers in England & Wales, 1974. Rep. Rothamsted Exp. Stn. for
1974, Pt. 2, pp. 195-199 (1975).
6. Darwinkel, A.: Aspects of assimilation and accumulation of.nitrate in some cultivated plants.
Agric. Res. Rep. 843, pp. 1-64 (1975).
7. Dilz, K. and Schepers, J.H.: Stikstofbemesting van granen. 24. Effekt van ziektebestrijding op
de stikstofreaktie van winter- eri zomertarwe met en zonder toepassing van chloormequat.
Stikstof, No. 71, pp.452-458 (1972).
8. El/en, J. and Spiertz, J.H.J.: The influence of nitrogen and benlate on leaf-area duration, grain
growth and pattern ofN-, P- and K-uptake of winter wheat (Triticum aestivum). Z. Acker- und
Pflanzenbau 141, pp.231-239 (1975).
.
9. Glynne, M.D.: Effect of potash on powdery mildew in wheat. PL Path. 8, pp.15-16 (1959).
10. Hebert, T. T., Rankin,W.H. and Middleton, G.K.: Interaction of nitrogen fertilization and
powdery mildew on yield of wheat. Phytopathology 38, pp. 569-570 (1948).
11. Jenkyn, J.F.: Studies on the resistance of barley to Rhynchosporium secalis (Oud.) Davis. Ph. D.
Thesis, University of Wales, 1969.
12. Jenkyn, J.F.: Effects of mildew (Erysiphe graminis) on green leaf area of Zephyr spring barley
.
1973. Ann. appL Bio1. 82, PP. 485-488 (1976).
13. Jenkyn, J.F. and Griffiths, E.: Some effects of nutrition on Rhynchosporium secalis. Trans. Br.
mycol. Soc. 66, pp. 329-332 (1976).
14. Jenkyn, J.F. and Moffatt, J.R.: The effect of ethirimol seed dressings on yield of spring bariey
grown with different amounts of nitrogen fertilizer 1969-71. PL Path. 24, pp. 16-21 (1975).
15. Large, E. c.: Growth stages in cereals. Illustration of the Feekes scale. PL Path. 3, pp. 128-129
(1954).
16. Large, E. C. and Doling, D.A.: The measurement of cereal mildew and its effect on yield. PL
Path. 11, pp.47-57 (1962).
17. Last, F. T.: Some effects of temperature and nitrogen supply on wheat powdery mildew. Ann.
appL BioL 40, pp. 312-322 (1953).
127
18. Lasl, F. T.: Effects of nutrition on the incidence of barley powdery mildew. PI. Path. 11, pp. 133
135 (1962).
19. Last, F. T.: Analysis of the effects of Erysiphe graminis DC. on the growth of barley. Ann. Bot.
26, pp. 279-289 (1962).
20. Martin, T.J., Stuckey, R.E., Safir, G.R. and ElIingboe, A.H.: Reduction of transpiration from
wheat caused by germinating conidia of Erysiphe graminis f. sp. tritid. Physiol. PI. Path. 7,
pp. 71-77 (1975).
21. Needham, P. and Boyd, D.A.: Nitrogen requirement of cereals. 2. Multilevel nitrogen tests with
spring barley in south western England. J. agric. Sci. 87, pp. 163-170 (1976).
22. Paulech, c.: Einfluss des Getreidemehltaupilzes Erysiphe graminis DC. auf die Trockensubstanzmenge und auf das Wachstum der vegetativen Pflanzenorgane. Biologia, Bratislava 24,
pp. 709-719 (1969). (Abst. in Rev. PI. Path. 49, 1619).
23. Priehradny, S.: Anderungen der Fiihigkeit der Gerste beim Befall mit dem echten Getreidemehltaupilz Erysiphe graminis f. sp. hordei Marchal Wasser zu binden. Biologia, Bratislava 24,
pp. 509-523 (1969). (Abst. in Rev. PI. Path. 49, I 15).
24. Sadler, R. and Scott, K.J.: Nitrogen assimilation and metabolism in barley leaves infected with
the powdery mildew fungus. Physiol. PI. Path. 4, pp. 235-247 (1974).
25. Simkin, M.B. and Wheeler, B.E.J.: Effects of dual infections of Puccinia hordei and Erysiphe
graminis on barley, cv. Zephyr. Ann. appl. BioI. 78, pp. 237-250 (1974).
26. Widdowson, F. V., Jenkyn, J.F. and Penny, A.: Results from two barley experiments at
Saxmundham, Suffolk, measuring effects of the fungicide benodanil on three varieties, given
three amounts of nitrogen at two times 1973-1974. J. agric. Sci. 86, pp.271-280 (1976).
27. Williams, R.J.B.: The rapid determination of nitrate in crops, soils, drainage and rainwater
by a simple field method using diphenylamine or diphenylbenzidine with glass fibre paper.
Chemy Ind. 1969, pp. 1735-1736 (1969).
28. Yoder, O. C. and Scheffer, R.P.: Effects of Helminthosporium carbonum toxin on nitrate uptake
and reduction by corn tissues. PI. Physiol. 52, pp. 513-51 7 (1973).
128
Interaction of Fertilizers with Septoria Leaf Blotch
of Wheat
Dr. K. Temiz, Regional Agricultural Research Institute, Menemen-Jzmir/Turkey
Summary
Siete Cerros 66 wheat was grown in the greenhouse, inoculated with Septoria trifid and treated with
3 rates of nitrogen, 3 rates of potassium and 2 rates of phosphorus. The effects of tbe fertilizers on
the development of the disease was studied.
The percentage of plants infected was increased by increasing N fertilizer but was un-affected by P
and K. The intensity of the disease was reduced by P and K and by the moderate rate of N. More
and larger pycnidia were formed in the presence of P and at the high K level.
Resume
On a cultive en serre du ble de la variete Siete Cerros 66 qu'on a inocule avec Septoria tritid et au·
quel on donnait 3 doses d'azote, 3 doses de potassium et 2 doses de phosphore. On a etudie les effets
de ces engrais sur le developpement de la maladie.
Le taux de plantes infestees fut accru par des doses croissantes de N, mais il resta, inchange sous
l'action de P et de K. L'intensite de la maladie fut reduite par P et K ainsi que par la faibledose de
N. En presence de P et de la dose la plus elevee de K il y avait formation de pycnidies plus nombreuses et plus grandes.
1. Introduction
Until recently the wheat diseases of importance in Turkey were covered smuts
(Tilletia spp.), rusts (Puccinia spp.), loose smut (Ustilago tritici), foot rot (Cercosporella herpotrichoides), take-all (Gaeumannomycesgraminis) and wheat gall nematode (Anguina tritici) [2]. The important diseases other than rusts were kept under
control b¥ seed treatment [2, 3]. There was danger of rust epidemics from time to
time.
However, the situation changed with the introduction of the Mexican wheat varieties
and within two years a new disease was seen on the high yielding Mexican wheats.
This was Leaf Blotch caused by Septoria tritici. It caused serious damage particularly
in the rainy coastal region. The damage was seen generally as elongated or oval spots
on the leaves which first became yellow and then necrotic. The pycnidia, the imperfect
stage of the pathogen, are formed on these spots. They are dark brown to begin with,
then black and spherical. pycnidia on the stubble provide the source of infection for
the next crop, making control difficult [4].
129
Although the disease was not known in Turkey until the introduction of the Mexican
varieties it was known in neighbouring countries [l). It is difficult to know why it
was not known earlier because local wheat varieties are susceptible to varying degrees.
The disease was observed to cause a 30% decrease in yield by Penjamo under artificially
created epidemic conditions for two years around Sake [6, 7].
Why was not the disease observed earlier? Before the introduction of the Mexican
varieties no fertilizers were used on wheat but farmers were asked to use fertilizer
when the Mexican seed was distributed. When they saw the results they started to use
fertilizer on local varieties also and it seems that fertilizer, while stimulating growth
and increasing yield potential, may have made the plants more susceptible to infection.
It therefore seemed advisable to study the relationship between fertilizers and the
disease.
2. Materials and Methods
2.1. Layout and treatments
Wheat was grown in Mitscherlich pots each containing 7 kg soil. The experiment,
established in the greenhouse at the Aegean Regional Agricultural Research Institute,
comprised the 18 treatment combinations of 3 levels of nitrogen, 3 of potassium and
2 levels of phosphorus repeated four times in an overall random arrangement. On the
basis of soil analysis carried out at Ege University, Faculty of Agriculture, Department
of Plant Nutrition, the following rates were recommended per 7 kg soil: 0, 4.5 and 9 g
ammonium sulphate (20% N); 0,2 and 4 g potassium sulphate (50% K 2 0) and 0 and
3.7 g triple supers (43% P 2 0 S)' Phosphorus and potassium were applied at sowing and
nitrogen in three equal portions at sowing, 25 and 36 days later.
2.2. Inoculation
The inoculum was obtained by soaking infected leaves in water for about an hour
and rubbing by hand to speed up the transfer of spores from the pycnidia to the water.
After sieving off the leaves, the inoculum was sprayed on the leaves of the experimental
plants three times at intervals of a few days, commencing ten days after the final
application of N. The pots were covered with polythene and the humidity kept high
for 48 hours after each spraying. The pots were carried outdoors in hot weather to
prevent thermotherapy.
2.3. Observations
Observations commenced a week after inoculation and were completed when the
infection reached the third leaf from the soil level. The following observations were
made:
- Level of disease attack. Height above the base to which leaves were attached, 1 - 1st
leaf, 2 - 2nd leaf, 3 - 3rd leaf.
- Number ofplants infected. Infected plants as percentage of total.
130
- Disease intensity on leaves. Leaves (3rd and below) scored ftom 0-10, 10 signifying
whole leaf area infected.
- Pycnidia type. 0 - no pycnidia on lesions, 1 - pycnidia just visible size 50-100 fL,
2 - pycnidia obvious, 100-150 fL, spherical shape, dark brown or black.
- Lesion type. A - yellow or dried, generally covering '/3 to 'h leaf surface, no pycnidia,
margins diffuse. B - Yellow or dry, 1-5 x 5-15 mm area, no pycnidia, margins clear.
C - Varying sizes, pycnidia present, oval form. P - 1-1.5 x 5-15 mm area, pycnidia
present, broken streak type.
3. Results and conclusions
The infection reached the third leaf from the ground under all treatments. The numerical
data for per cent plants infected and for estimates of disease intensity were subjected
to statistical analysis, those for pycnidia and lesion type, being more descriptive, were
not suitable for computation but it was possible to obtain a general picture of fertilizer
effects.
3.1. Percentage plants infected
Increasing the rate of nitrogen applied increased the number ofplants infected (Table 1).
Phosphorus and potassium had no effect.
Table 1. Effect of nitrogen on number of plants infected
Treatment
Mean %
infected
no······
nl
n2
.
························, .
•• ..••••••••••••.•••.•..•
s. e. of mean
" ..
77.3
87.9
95.5
0.79
3.2. Disease intensity on leaves
The intensity of attack was reduced by increasing,potassium and by the application
of phosphorus. The disease intensity was reduced. by the moderate rate of N (n l compared with no) but increased again at the high rate (n z). There was no interaction
between the fertilizers, the lowest disease intensity being given by the combination
nlPlk z. Mean scores for the main treatments are given in Table 2.
Table 2. Effect of treatments on disease intensity
Treatment
Mean"
score
Treatment
Mean
score
no ........
n l ........
n2 . . . . . . . .
s.e.ofmean
5.00
3.04
3.96
0.160
k o ...... · ..
kl ········ .
k2 ········ .
4.71
4.17
3.13
0.160
. Treatment
Po····· ....
PI········ .
Mean
score
4.39
3.61
0.130
131
3.3. Picnidia
The spherical, dar k brown or black, typical pycnidia were of normal size (l00-150 fJ.)
when high rates of N, P and K were used in combination. In the absence of nitrogen
the pycnidia were either very small or non-existent. However, the lesions were larger
and the tissue around the infection point was more affected although the pycnidia
were few or nonexistent in the absence of N fertilizer.
3.4. Lesion type
A type lesions predominated in the absence of N with B, C or D types when N was
applied alone or in combination with PK or K. There was a tendency for C and D
types to predominate at the high level of K. There was a higher proportion of D type
lesions when the high rate of N was used with P and high K. When high rates of
balanced fertilizer (like n 2pk 2) were used the lesions were streaky, when unbalanced
complete fertilizer was used they were oval, while when the fertilizer combination
included no nitrogen they were large and spreading.
Some interesting results have been obtained but more research is needed to explain
the phenomena.
Bibliography
I. Eyal, Z.: Effect of Septoria leaf blotch on the yield of spring wheat in Israel. Plant Disease
Reporter 56 (IT) (1972).
2. Iren, S.: The major wheat diseases, weeds and their control in Turkey, CENTO Council for
Scientific Education and Research. pp. 83-93, 1973.
3. Ozkan, M.: Bugdaym hastahklardan korunmasl. Ttirklye Blhmsel ve Teknik Ara~tIrma Kurumu,
Tarim ve Oramnclhk Ara~tirma Gurubu yayim, sayi 8, 200-211 (1970).
4. Shearer, B.!. et al.: The Common Septoria Diseases of Wheat. Botanical Review 37 (2),231-262
(1971).
5. Svec, L. V. and Crittenden, H, W.: Effect of potassium on the incidence of Diaporthe sojae in
soybean. Agronomy Journal 66 (5), 696-697 (1974).
6. Temiz, K.: Effect of Septoria leaf blotch on the yield of spring wheat in Turkey. Annual Report
of 1973. Aegean Regional Agricultural Research Institute, Menemen-Izmir.
7. Temiz, K.: Effect of Septoria leaf blotch on the yield of spring wheat in Turkey. An'nual Report
of 1974. Aegean Regional Agricultural Research Institute, Izmir.
132
The Nutrient Status of the Soil and
the Appearance of Symptonis of Microbial Disease
Dr. Ir. K. Van Nerum and Prof. Dr. G. Scheys, Catholic University of Louvain, Faculty of Agricultural Science. Louvain/Belgium
Summary
A study was made of the relationship between plant behaviour and soil physical and chemical
conditions. This embraced field investigations and experiments under controlled conditions.
With asparagus; soil texture, drainage and soil Ca content influenced degeneration of the crop.
Experiments in nutrient solution showed, among other things,' that symptoms of Fusarium attack
and the quality of shoots was determined by the Ca content of the medium.
With chicory it was shown that Pseudomonas and Verticillium were more severe when soil physical
and chemical conditions were unfavourable. The parasite was frequently found in the affected
tissues.
It seems that infection by Fusarium, Pseudomonas and Verticillium is secondary and that amelioration
of soil physical and chemical conditions is an effective means of reducing attack.
Resume
On a effectue une etude sur les relations entre le comportement de la plante et les conditions physiques et chimiques du sol. ElIe comprenait des essais en plein champ et des essais en conditions controlees.
Dans le cas de I'asperge, la texture du sol, le drainage et la teneur en Ca du sol avaient une influence
sur la degeneration de la culture. Parmi d'autres choses, les essais en solution de culture montrerent
que les symptomes de la Fusariose et laqualite des pousses sont determines par la teneur en Ca du
milieu.
Dans le cas de la chicoree on a pu constater que I'incidence de Pseudomonas et de Verticillium a ete
plus severe lorsque les conditions physiques et chimiques du sol furent defavorables. On retrouva le
parasite frequemment dans les tissus affectes.
J1 semble que les attaques par Pseudomonas, Fusarium et Verticillium constituent des phenomenes
d'importance secondaire et que I'amelioration des conditions physiques et chimiques du sol soit un
moyen efficace pour reduire les attaques.
1. Introduction
Thanks to the Soil Cartographic Centre of Belgium detailed pedological maps are
available. These maps have been established on the basis of pedological characteristics
(Tavernier, Marechal and Amerijckx [7]).
Several years ago, teams were set up to study crop behaviour on the. different cartographic units with reference to the nutrient status of the soils. These studies made it
possible to establish tables of the nutrient status of the soils and their suitability for
133
cultivation (Studiecentrum voor Tuinbouwgronden [5}). Actual nutrient deficiency is
rare in Belgian soils but nutrient disequilibrium, caused through the uncontrolled use
of fertilisers, does occur, particularly on the lighter soils. The resulting problems are
not very well known.
2. Method of investigation
2.1. Study of the suitability of the soil and nutrition in the field
The required information on soil suitability was obtained in collaboration with the
growers. A plan for each crop was established in a preliminary investigation. It was
necessary to decide, among other things, which characteristics were important, when
and why they were important. The physical description of the soils comprised the
following determinations:
-
Textural class, or mechanical composition of the soil
Drainage class based on the degree of gleying in the profile
Profile development
Horizons with texture differing from the plough layer
Relief and micro-relief
Nutrient conditions were characterised by chemical analysis of one or several samples
of surface and subsoil. The extractant used was ammonium lactate and cations were
determined by atomic absorption photometry, phosphorus colorimetrically.
2.2. Plant studies in pot culture
Following these field soil investigations problems of nutrition were studied in pot
culture in a controlled environment. These experiments made possible a deeper understanding of the behaviour of the plant in different nutrient environments. Special
techniques were used. There were two plastic receptacles for each treatment and these
were connected by a flexible hose. The receptacle containing the plant and substrate
was placed on the bench while the other, containing the nutrient solution, could be
raised above the level of the fixed receptacle in such a way that its contents flowed into
the substrate, while lowering the solution container allowed surplus solution to drain
back into the reservoir. The level of the solution was restored before each irrigation
using de-ionised water. In the early stages these operations were done by hand, later
on the whole operation was completely mechanised.
This equipment allowed us to work throughout the season with the same nutrient
solution, whose composition was restored from time to time by careful adjustment to
give similar nutrient conditions to those encountered by the plant in the field.
3. Asparagus growing
Belgium produces only blanched asparagus. The crop is grown on sands, loamy sands
and sandy loams and the area cultivated is declining. Rots occur on the stems and roots
and after several years the field becomes valueless. The affected parts of the plant
contain the mycelium and spores of F.oxysporum and F. culmorum (Van Assche and
Kempenaers [8}).
134
3.1. Results of soil investigations
The complete results have been published by Van Nerum and Palasthy [I2}. They will
only be summarised here under the relevant headings. The statistical analysis summarised in Table 1 shows that productivity and the degree of degeneration are both
influenced by the same pedological factors. Factor analysis (Harman [2}) of the 11
variants recorded in the field during the enquiry is shown in Table 2. This method
Table 1. F values for variance due tp characters investigated in the field survey on asparagus
Source of variation
Texture
Degree of gleying .. ,
Texture x gleying
year
Texture x year
Gleying x year
2nd order interaction
Error
Total variance
Sum of
No. of
diameters shoots
.
.
.
.
.
.
.
.
.
15.17**
80.70**
9.1 1**
23.28**
0.48
4.10**
1.46
12.59**
64.24**
6.92**
8.07**
0.74
3.91 **
1.82
No. of
shoots
5mm
No. of
dead
shoots
4.22*
2.09
0.27
31.93**
1.38
1.23
1.47
4.37*
3.88*
1.94
27.05**
3.04*
0.36
1.40
D.F.
2
2
4
3
6
6
12
1202
1237
F value
for
p=0.05
2.99
2.99
2.37
2.60
2.09
2.09
1.75
* significant p = 0.05
** significant p=O.OI
Table 2. Factor analysis - 11 variants, 1240 observations. Examination of principal components
Factor loading Poor
principal
conditions
component
(-2S)
Variable
1. Texture .........•...........
2; Drainage
.
3. Sum of stem diameters
.
4. Number of shoots
.
5. Number of shoots <5 mm
.
6. pH (HP)
7.
8.
9.
10.
I J.
.
pH {KCn .•.................
P
.
K
;
.
Mg
.
Ca
.
0.351
0.435 •
0.545
0.539
0.191
0.798
0.810
0.309
0.542
0.483
0.736
19.2
18.5
349.7
36.6
15.3
4.4
3.5
15.9
8.9
2.7
7.8
Mean
20.2
21.2
612.9
60.7
19.4
5.4
4.6
22.8
18.7
6.0
36.1
Good
conditions
(2S)
21.3
23.9
929.4
89.1
24.0
6.5
5.7
31.0
32.3
10.8
85.5
allows, among other things, the simultaneous investigation of several variables with
the aim of finding the nutrient levels required for crop improvement. This optimal
nutrition for asparagus is calculated in Table 2 by projecting the coordinates for each
variable to + 2S and -2S. The simultaneous improvement of the nutrition variants
has a considerable influence on the sum of stem diameter per unit area. In order that
nutrition can have a favourable effect, attention must be paid to certain physical
conditions (drainage and texture). It is clear that not only do the amounts of nutrients
require adjustment but equally the balance between these elements should be altered.
The optimum is quite high compared with other crops studied. For intensive cropping,
as in horticulture, research should aim to investigate the whole complex of factors
involved rather than trying to solve the problem in a piecemeal fashion.
135
3.2. Results of nutrition experiments in pot culture
3.2.1. Experiment with major element excess and deficiency
This experiment was conducted with plants which had been grown normally in the
field for one year before planting in the pots. It showed up the loss in yield of asparagus
due to deficiencies in Ca and Mg. Ca deficiency, characterised by necrosis and death of
the young growths, becomes evident in the month of August. The symptoms are seen
on the newly formed tissues. Mg deficiency is seen at the same time of year in yellowing
and shedding of leaflets, the symptoms appearing on the older tissues. The shoot loses
its turgidity, shrinks and dies. Excesses of N, K and P are very harmful, the plants
eventually decaying. On the contrary, excess of Mg or Ca has a favourable influence on
the number and diameter of shoots. Macroscopic examination of buds shows the very
unfavourable influence of Ca and Mg deficiency and of excess of P. The symptoms of
Ca and Mg deficiency look very much like an attack of Fusarium (van Maris [10],
Van Assche and Kempenaers [8]).
3.2.2. Systematic experiments (Homes [3])
The plants were established in pure sand free of nutrients and transplanted into pots in
pure sand mixed with perlite and containing the desired levels of nutrients. The effect
of Ca and Mg in promoting root and shoot growth was remarkable. Excess of P and
of K checked development of both root and shoot. The optimum concentration was
about 800 meq. per pot. The calculation of the optimum interaction did not result in
realistic figures.
3.2.3. Factorial experiment (4 factors, 3 levels)
This experiment was planned to clarify the roles ofP and K in asparagus nutrition. The
impression was that P and K played only a secondary role. The results showed that P
and K were both important and essential for asparagus but that they should not be
abused.
.
3.2.4. Randomised block experiment (2 blocks, 6 treatments, 7 replications) to investigate
rate and form of nitrogen fertiliser
This experiment showed that for optimum results N should be applied as '13 NH+4
and 2/ 3 N0 3-. Divergence from this ratio results in accumulation of either ammonium
or nitrate.
3.2.5. Superimposed orthogonal Latin Square experiment (l0 elements, 11 rates)
(Dugue and Girault [1])
The results were analysed by factor analysis. This showed inter alia that the plant can
elaborate a given quantity of organic matter under several different nutrient composition conditions. To explain this phenomenon it seemed to us that two mechanisms
were involved, namely substitution and accumulation. By substitution one understands
the possibility of replacing one element with another (Mg, Ca, Na, K). By accumulation
we mean that the plant can accumulate elements in excess without benefit to the plant
(K, P, N, Na). These two phenomena are not however unlimited, that is to say once a
certain level has been exceeded the plant will suffer and may die.
Factor analysis, allowing the examination of a large number of variants, shows that
when nutrient ratios are optimal the plants' mineral uptake is lower. The plants in
136
question have thus elaborated the maximum of organic matter with a mIlllmum
absorption of mineral nutrients. The mechanisms of accumulation are not well known.
Because of accumulation of certain elements, the plant can suffer from deficiency in
others even when analysis fails to reveal· an absolute deficiency. It seems that one
element can be fixed or immobilised by excess of another (P-Ca).
Table 3 allows comparison of the analysis of plants originating from the field with
those from experiments. Bad conditions are shown in coiumns -28, good in columns
headed 28.
Table 3. Analysis of plants from the field compared with plants from superimposed Latin square
experiment. meq/l00 g D.M.
Element
Ca ..................
Mg ..................
Na . . . . . . . . . . . . . . . . .
K ..................
P ...................
Mn .................
N ..................
1967 survey
-2S
OS
2S
59.6 67.7 76.2
10.6 15.4 21.2
64.5 46.2 32.1
53.0 54.7 56.4
17.4 17.7 17.6
17.0 10.8
6.5
223.5 210.2
236
1965 survey
-2S
OS
2S
43.7 53.5 64.4
11.6 12.2 12.8
74.8 45.2 25.9
61.4 64.3 67.3
25.5 21.5 21.5
14.7
9.5
5.8
239.0 251.2 263.3
Pot experiment
-2S
OS
2S
39.2 40.8 42.4
26.5 36.7 48.4
8.6 19.2
3.1
138.9 57.0 18.1
43.7 28.7 17.6
15.7 15.9 16.0
234.1 171.2 118.1
3.2.6. Infection experiments
Asparagus was sown in a mixture of white sand and perlite which was watered with a
solution of optimal nutrient composition as found in the previous experiment (3.2.5.).
Two plastic containers (60 x 30 cm) each contained 200 plants. When the plants
attained a height of 10 cm they were sprayed with an emulsion of fusarium spores
which had been raised in Petri dishes. No symptoms of Fusarium attack were found up
to the time the experiment was terminated two months later.
3.3. Conclusion
It is hypothesised that in the nutrient conditions found in Belgian soils deficiencies of
calcium and magnesium are factors which limit asparagus production. Further, inappropriate physical conditions for asparagus culture can be the cause of poor yields
and phenomena attributed to Fusarium attack. The deficiency symptoms caused by
lack of these elements are similar to the symptoms of Fusarium.
4. Chicory (Witloof Chicory)
Chicory culture was originally typical of Belgium, though now, 25000 ha are grown
in France, 10 000 in Belgium and 3000 in the Netherlands. Yields in practice vary
between 12 and 18 tons/ha. The crop is grown in two stages: the growing of the roots
in the open field and the production of the marketable chicory by forcing in beds.
Chicory culture has to contend with several serious problems, notably:
Verticilliose: attack by Verticillium dahliae
Leaf rot Caused by Pseudomonas marginalis
Sclerotinia sclerotiorum causing rot, particularly in the forcing bed.
Yield variation in forcing beds
137
The degree of infection by Verticillium and by Pseudomonas can be measured by
counting the plants showing the symptoms. However, differences in productivity
cannot always be ascribed to the two diseases mentioned nor to differences in productivity of roots in the field. The differences are often due to abnormal behaviour of the
root which grows in unbalanced relation to the aerial parts.
In the field survey root production was estimated as the sum of root diameter per are
and plant health by counting the plants showing symptoms of rot.
4.1. Results of analysis of data from field survey (Van Nerum and Palasthy [11 J)
To investigate the relationship between rot and the physical and chemical characteristics of the soil data from fields showing degrees of infection varying between 10 and
100% were subjected to factor analysis, the results of which are given in Table 4. This
analysis showed that there were two things which influenced the appearance of rot
symptoms:
- soil series and nutrition, the latter being largely dependant upon series.
- drainage and the thickness of the humified layer, rich in phosphorus and sodium.
Table 4. Factor analysis of data from 1050 fields showing rot at 10%-100%
Characteristics
Factor loading Factor loading Factors
principal
secondary
transformed
components
components
by rotating axes
Texture
Drainage
Depth of humified layer
.
.
.
.
.
.
.
.
.
0.539
0.461
-0.072
0.665
0.316
0.339
0.596
0.752
0.446
0.423
-0.196
-0.304
-0.374
0.085
-0.343
-0.106
0.190
0.040
-0.391
0.226
0.200
0.065
-0.330
0.370
-0.065
0.140
0.540
0.560
0.135
0.450
pH (H 2 0)
.
P mg/IOO g soil
,
K mg/IOO g soil.
Mg mg/100 g soil
Ca mg/IOO g soil
Na mg/IOO g soil.
Diameter at collar
Diameter at collar (adjusted for number of
plants)
Number of plants
Rot index
.
.
.
0.222
0.310
-0.337
0.638
-0.1 93
0.625
0.050
-0.510
-0.380
Hypothetical interpretation of these results
The cause of susceptibility to wilt is insufficiency of calcium in parts of the plant
where it is needed, among other things, for cell wall building. The first column of
Table 4 shows that on heavy soils well supplied with nutrients rot is not serious. The
second column shows that on moist light textured soils with a shallow humified layer,
though well supplied with P and Na and with moderate applications of Ca and Mg, the
crop is more susceptible.
Drainage influences the equilibrium between mono-valent and di-valent ions, the
equilibrium being displaced in favour of the mono-valent by humidity, i.e. effect of
drainage (Donnan equilibrium). On the other hand P fixes Ca, a phenomenon which
is all the more important when there is little available Ca. Na is also antagonistic to Ca.
The third column shows the important influence on the phenomenon of an absolute
deficiency of Ca and Mg. This third column is obtained by rotating the axes between the
two first spectra in such a way as to maximise the variance of the rot.
138
4.2. Results of experiments in pot culture
4.2.1. Systematic experiments (Van Nerum and Palasthy [13])
These experiments showed that nutrition influenced leaf shape as well as the weight of
roots and foliage. The high K treatment showed rotting Of the young leaves, that is to
say of the leaf tips, indicating possible Ca deficiency (K-Ca antagonism).
4.2.2. Factorial experiment in superimposed Latin Squares (6 elements, 7 rates)
(Van Eylen [9])
Table 5 gives mean analytical data for plants showing severe symptoms ofrot compared
with healthy plants. As always, the method of estimating severity of attack is debatable.
In this case, scores were awarded in the range 0-10, a score over 7 being taken as severe
attack; rot free plants were those with a score of O. In the field enquiry disease attack
was measured by counting all affected plants but in this experiment we were more
interested in the severity of attack. The results were examined by regression analysis.
Table 5. Mineral content of plants grown in pot culture (superimposed Latin square experiment,
7 elements, 7 rates) meq/IOO g D.M.
Plants with severe rot symptoms
Element
Ca
Mg
.
.
K
.
P
N
.
..
Leaves
Roots
35
4.4
9.6
18
29
11
92
46
56
94
Plants free from rot
Leaves
68
41
32
6
173
Roots
12
6
1.4
6.3
85
These experiments showed that the treatments affected not only the degree of rotting
but also the appearance of the foliage, the proportion between erect and drooping
leaves and individual leaf shape. The rots, particularly that of the leaf tip, were typical
of those due to lack of Ca (table 5). The Ca deficiency could have been caused either by
too little Ca applied in the treatment or by antagonistic effects of other elements,
notably P, K or Mg.
4.2.3. Factorial experiments in forcing beds (7 elements, 7 rates)
(Stuyckens [6])
The experiments in forcing beds were carried out in order to study the incidence of
abnormalities of commercial importance. The previous experiments had shown that
the appearance and behaviour of the plant was influenced by the composition of the
nutrient solution and exactly the same phenomena were observed in the experiments in
forcing beds. We have been able to solve the problem of obtaining yield and quality in
water culture comparable to that obtained by traditional methods of forcing. The
composition of the nutrient solution used, when forcing in water culture or on artificial
media, is of paramount importance.
4.3. Conclusion
The following hypothesis is suggested. Under Belgian conditions, nutrient imbalance,
coupled with physical soil conditions which are not well suited to chicory culture, can
cause symptoms of rot which resemble attacks by Verticillium and Pseudomonas.
139
Nutrient balance influences not only production (amount of organic matter elaborated)
but also the whole behaviour and appearance of the plant. The latter phenomenon is
most important in the case of chicory.
5. General conclusions
We have also studied strawberry (Van Nerum, Palasthy and Lamberts [11)), and
research on other crops is in progress. The investigations described in this paper and
those still in progress allow us to advance some general conclusions.
It seems to us that in the past plant nutrition has been much too exclusively concerned
just with effects on yield and production and too little with the behaviour of the plant
under study. It seems to us that the method of factor analysis which allows the
simultaneous study of a whole range of variants in different media can, in one way or
another, be very useful.
We have been able to show that certain symptoms known to be due to microbial
diseases can also be caused by nutrient imbalance. Defective nutrition can render the
plant more susceptible to microbial attack. We have been able to verify, in the course
of our experiments, that unbalanced nutrient solutions not adapted to the crops under
study can cause various abnormalities in growth and can weaken the plants. We think
that such plants are liable to be infected by parasites and perhaps also by saprophytes.
We think that what is to be regarded as the optimum in nutrition should not be based
as in the past on one single palameter, but rather on the whole behaviour of the plant
including its susceptibility to possible disease.
6. References
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
140
Dugue, P. and Girault, M.: Analyse de variance et plans d'experience, Dunod, Paris (1959).
Harman, H.: Modern factor analyses. The University of Chicago Press (1967).
Homes, M.: Alimentation equilibree des vegetaux, Wetteren (1961).
Peeters, G.: Factor analysis, computer program, Rekencentrum, K.U.L., Heverlee (1967).
Studiecentrum vo?r Tuinbouwgronden: Studie van de bodemge~chiktheidvoor asperges, Tweejaarlijkse verslagen LW.O.N.L. (1965-1967-1969).
Stuyckens, F.: Onderzoek van nieuwe trektechnieken voor witloof, Eindverhandeling. Faculteit
der Landbouwwetenschappen K.U.L. (1971).
Tavernier, R., Marechal, R. and Amerijckx, J.: Bodemkartering en bodemklassificatie in Belgie,
Gent.
Van Assche, C. and Kempenaers, A.: La fusariose chez les asperges. Verslag van het Intern.
Tuinbouwcongres, blz. 362-366 (1962).
Van Eylen, A.: Bemestingsonderzoek in vitro voor witloofwortelteelt. Faculteit der Landbouwwetenschappen, K.U.L. (1971).
Van Maris, P.J.H.: Fusskrankheiten bei Spargel. Report of the third meeting 5th-7th sept. of
the Intern. Working Group for Asparagus breeding, p. 3-8 (1961).
Van Nerum, K., Palasthy, A. and Lamberts, D.: Studie van de bodemgeschiktheid voor de
aardbeiteelt. Agricultura 14, No.4, p.492-430 (1966).
Van Nerum, K. and Palasthy, A.: Studie van de bodemgeschiktheid voor de aspergeteelt. These
de doctorat. Faculteit der Landbouwwetenschappen K.U.L. (1970).
Van Nerum, K. and Palasthy, A.: La chicoree de Bruxelles, aptitude des sots et problemes de
nutrition, Section horticole d'eucarpia, Symposium International Gembloux, p.217-226 (1970).
Effects of Nitrogen Source and Irrigation Frequency on
the Susceptibility of Potato to Late Blight
(Phytophthora infestans)
U.Kafkafi*, M.L.Giskin* and H. Yogev**
Summary
Potatoes (var. Up-to-Date), grown on a clay soil, were fertilized with four different sources of
nitrogen: ammonium sulphate, potassium nitrate, urea plus potassium sulphate, and a mixture of
urea, potassium nitrate and potassium sulphate. Plants in the urea plus potassium sulphate treatment
contained the lowest percentage of dry matter, the highest percentage of Nand P, and were affected
least by Phytophthora. The crop with the largest interval betweenirrigations (4 days) was the least
affected by the disease.
.
Resume
Des pommes de terre (var. Up-to-Date) cultivees sur un sol argileux furent fertilisees avec de l'azote
provenant de quatre sources differentes: sulfate d'ammonium; nitrate de potassium; uree + suI fate
de potassium; melange uree - nitrate de potassium - sulfate de potassium.
Les plantes du traitement uree + sulfate de potassium contenaient le pourcentage le plus faiblede
matiere seche, le pourcentage le plus eleve de N et de P et eUes furent les moins attaquees par
Phytophthora. Parmi les modes d'irrigation examin6s (4 jours) les plantes ayant ete soumises il. !'irrigation avec le plus grand intervaUe ont presente la plus faible attaque par la maladie.
1. Introduction
The internal metabolism of nitrogen has the main effect on plant growth. Kirkby and
Mengel [1967] demonstrated in a nutrient solution experiment that nitrate nutrition
favors dry matter production while ammonium-uptake reduces carbohydrate accumulation, with urea playing an intermediate role.
Since carbohydrate production is the main reason for growing potatoes, it was decided
to measure the effect of various sources of nitrogen on the carbohydrate production of
potatoes grown under field conditions.
'
2. Materials and Methods
A complete factorial experiment compnstng three irrigation frequencies and four
nitrogen sources was initiated. Potato (var. Up-to-Date) was seeded on May 6 and the
* Div. of Soil Chemistry and Plant Nutrition, ARO, The Volcani
** Extension Service, Ministry of Agriculture, Zefat/lsrael.
Center, Bet Dagan/lsrael.
141
field received a basic treatment of 50 m 3/ha of farmyard manure, 500 kg/ha of superphosphate (18% PzOs), and 500 kg/ha of potassium chloride. After emergence, six
equal top dressings of the nitrogen fertilizers were given every 2 weeks. The total
amount of N applied was 240 kg/ha and that of K was 660 kg/ha.
The three irrigation treatments tested were: sprinkler irrigation, given when the
tensiometer reading was 40 cbar at 30-cm depth; sprinkler irrigation once every 4 days;
and sprinkler irrigation once every 2 days. The four nitrogen sources tested were:
ammonium sulphate, potassium nitrate, urea plus potassium sulphate, and a combination of urea, potassium nitrate and potassium sulphate.
Three plant samples were taken during the season for determination of the dry
matter yield and percentage, and the nitrogen, phosphorus and potassium contents.
Six soil samples were taken in the course of the season and the content of N-N0 3 was
determined in the upper 40 cm layer. Phytophthora disease incidence was estimated
twice, each time by two observers who rated each plot according to one of five degrees
disease attack:
1.
2.
3.
4.
5.
no attack (full green color to leaves)
a few disease spots in the plot
many disease spots in the plot
plants partly destroyed
plants totally destroyed.
3. Results and Discussions
The effect of the different fertilizers on the dry matter production of tops and tubers at
three different dates, averaged for all irrigation treatments, is shown in Table 1. The
effect on the percent dry matter is shown in Table 2. The urea plus potassium sulphate
treatment produced the highest top yield and the lowest tuber yield until mid-August.
It led to lowest dry matter percentage of all nitrogen fertilizers used; the second lowest
was in the urea plus potassium nitrate treatment.
The concentration of nitrogen, phosphorus and potassium in the tops of the potato
plants are shown in Table 3. The urea plus potassium sulphate treatment produced the
highest concentration of Nand P in the plant, with no effect on the potassium content.
This effect of the top dressing suggests that urea enters the plant as urea probably
through the leaves, and hydrolyses there to ammonia or ammonium.
Table 1. Dry matter yield kg/ha (averages of all irrigation treatments)
Date
18. VI
Nitrogen fertilizer
Top
(NH.).SO•.................
KN0 3 . . . . . . . . . • . . . . . . . . . . .
CO(NH.)•..................
CO(NH.).+KN0 3 • · · · · · · · · .
1500
1900
2080
1980
S.E
142
.
63""
23. VII
Tubers
19. VIII
Top
Tubers
Top
Tubers
4410
4860
5390
5520
4920
5740
3710
4650
3200
3710
3690
4050
9400
8730
6220
9070
350 n.s. 450"
460n.s. 730""
Table 2. Percent dry matter in potato (averages of all irrigation treatments)
Date
23. VII
18. VI
Nitrogen fertilizer
Top
(NH.),S04 ... . . . . . . . . . . . . . .
KN0 3 . . . • • . . . • . . . . . . . . . . . .
CO(NH 2).. . . . . . . . . . . . . . . . . .
CO(NH 2). + KN0 3 . . . . . . . . . .
9.2
9.2
9.4
8.8
S.E. . . . . . . . . . . . . . . . . . . . . . . .
0.3 n.s.
Tubers
19. VIII
Top
Tubers
Top
Tubers
12.2
12.5
10.2
11.6
19.5
19.7
16.2
17.5
12.3
11.9
11.2
12.4
20.3
19.4
17.5
19.2
0.40**
0.45**
0.67
0.49
Table 3. Nutrient content of potato plants
Nitrogen fertilizer
.
18.VI
23. VII
19. VIII
%N
(NH4),S04
.
KN04 ········································
CO(NH.),
.
.
CO(NH 2)2+ KN0 3
4.02
4.08
4.59
4.40
5.38
4.92
6.57
5.63
3.82
3.56
4.43
3.83
S.E.'
0.15n.s.
0.34*
0.29 n.s.
.
%P
(NH.).S04
..
KN0 3 • . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
CO(NH 2),··················· '
.
CO(NH2),+KN0 3 • • • • • • • • • • • · • • · • • · • · • • • • • • • ••
0.44
0.39
0.38
0.40
0.43
0.38
0.46
0.40
0.31
0.27
0.32
0.29
S.E
0.01**
0.01**
n.s.
.
%K
(NH 4),S04 .. ,
.
KN0 3 • • • • • · • · • • • • • • • • · • • • • • • • • • • • • • • • • • · • • · • •
CO(NH2)2···································· .
CO(NH 2). + KN03
.
4.2
4.0
4.1
4.1
3.9
3.9
4.3
4.1
2.8
2.9
3.1
2.9
S.E
n.s.
n.s.
n.s.
,
.
It is known (Van Tuil, de Wit) that the cation anion balance favors phosphate (anion)
uptake when the ammonium ion enters the plant.
The conclusion that urea penetrated through the leaves is supported by the data of
N0 3-N found in the soil during the growing season, as shown in Table 4. There was no
effect of the fertilizer source on the amount of nitrate nitrogen in the upper 40 cm layer,
where the level of nitrate in the soil was ample to satisfy the crop's demands.
The estimations of Phytophthora attack are summarized in Table 5. The lower (average)
infection at each rating date was found in the irrigation treatment with the longest
interval (4 days) between irrigations. Testing the effect of nitrogen source on each
irrigation frequency showed that plants in the urea plus potassium sulphate treatment
were the least infected.
It is unlikely that the potassium sulphate added to the urea had any effect on the
Phytophthora attack as the potassium content in the plants was the same (Table 5) in all
143
Table 4. Amount of N-N0 3 (kg/ha) in the upper 40-cm soil layer (averages of all irrigation treatments)
Date
Nitrogen fertilizer
3.VI
18.VI
2.VII
23. VII
19. VIII
15.IX
(NH"hSO" . . . . . . . . . . . . . . . . . . . .. .
KN0 3 . • • • • • . • . • • . • . . • . . • . • • . • . •
CO(NH 2)2' ......................
CO(NH 2)2 + KN0 3 • • • • • • • • • • • . • . •
161
186
174
175
157
185
169
204
134
120
167
121
96
76
104
93
320
178
143
146
135
191
222
191
S.E.............................
n.S.
n.s.
n.s.
n.S.
n.s.
n.S.
Table 5. The effect of fertilizer source and irrigation frequency on the incidence of Phytophthora
attack in potato plots (rating* are averages of 5 replications).
A
B
C
Average
19.VIII9.IX
19.VIII9.IX
19.VIII9.IX
19.VIII9.IX
(NH")2S0" ...... , ...........
KN0 3 • • • • . • • • . • • • • • • . . . • . . .
CO(NH2)2 + K 2SO" ...........
CO(NH 2)2 + KN0 3 + K 2SO" ...
Average .................. -.
4.0
3.4
3.0
3.2
3.4
4.1
4.4
3.1
3.9
3.9
3.2
4.2
2.8
3.2
3.3
3.4
3.8
3.0
3.4
3.4
4.1
4.5
3.5
4.3
4.1
3.5
3.8
2.9
3.3
4.0
4.3
3.4
4.0
SR ........................
0.21 *
0.25*
0.22 * N.S.
0.23 *
0.24"
0.23 "
0.25 "
Fertilizer
3.9
3.9
3.6
3.7
3.8
" 1 = all plants green, 2 = several infection spots in the plot, 3 = many infection spots in the plot,
4 = tops partly destroyed, and 5 = plants totally destroyed.
A = Irrigation at 40 centibar at 30 cm depth
B = Irrigation every 4 days
C = Irrigation every 2 days
the treatments and sulphate was given to three treatments, without having any apparent
effect. It therefore appears that of all the fertilizers tested the urea alone was responsible
for significantly decreasing the late blight attack.
It is not yet possible to determine what caused the specific effect of urea in decreasing
the disease damage: it may have been the specific effect of urea, or the physiological
status of the plant resulting from urea absorption through the leaves, which is reflected
in higher water, nitrogen, and phosphorus in the plant.
4. References
1. Kirkby, E.A. and Mengel, K.: Ionic balance in different tissues of the tomato plant in relation to
nitrate, urea or ammonium nutrition. PI. Physiol. 42, 6-14 (1967).
2. Van Tuil, H.D. W.: Organic salts in Plants in Relation to Nutrition and Growth. Center for Agricultural Publications and Documentation. Wageningen. Agricultural Research Report No.657,
1965.
3. De Wit, C. T., Dijkshoorn, W. and Noggle, J. c.: Ionic balance and growth of plants. Versl.
Landbouwk. Onderz. 69.15 (1963).
144
The Influence of Fertilizers on Fungal Diseases of Maize
Dr. W.Kriiger, Biologische Bundesanstalt, Institut fUr Getreide-, Olfrucht- und Futterpflanzenkrankheiten, 2305 Heikendorf-Kitzeberg/Federal Repu,blic of Germany
Summary
The use of fungicides on maize has been limited by the biology of the parasites and economic
factors. Emphasis in disease control has therefore, been on breeding and field husbandry including
the use of fertilizers. Fertilizers had only slight influence on leaf blights. Nitrogen and phosphate
increased and potassium and calcium slightly decreased the incidence of blight caused by Drechslera
turcica. Similar results were observed with Ustilago maydis and Sphacelotheca reiliana, but with
.
reference to U. maydis they were contradictory.
More reports are available concerning stalk rot of maize. Generally the disease caused by Fusarium
species (F. graminearum, F. moniliforme, F. oxysporum, 1". culmorum) was increased by N-fertilization
and decreased by potassium. If however, Diplodia zeae was the causal agent, nitrogen decreased and
phosphate (in various forms) increased the disease. The effect of rate of fertilizer was very variable,
higher rates not always producing effects in proportion to those obtained at medium or lower rates.
The effect of fertilizers was influenced by the degree of susceptibility of the cultivars and to some
extent by field husbandry measures. Only two sets of data were available on the effect of fertilizers
on ear rot of maize. As with stalk rot, the effect depended on the fungi causing the disease.
Complications and interactions of fertilizers with the physiological metabolism and the physical
properties of the stalks are discussed with reference to stalk rot.
Resume
L'usage de fongicides sur ma1s est limite par la biologie des parasites en question et par des facteurs
d'ordre economique. Dans le domaine de la hitte contre les maladies l'accent a donc ete mis sur la
selection et sur les pratiques de culture y compris les mesures de fertilisation. Les engrais n'ont que
peu d'influence sur la maladie du charbon. L'azote et les phosphates ont augmente legerement
l'incidence du charbon provoquee par Drechslera turcica, tandis que le potassium et le calcium ont
eu un certain effet depressif sur cette maladie. D'es resultats semblables ont ete obtenus avec Ustilago
maydis et Sphacelotheca reiliana, mais avec U. maydis les resultats furent contradictoires.
Un plus grand nombre de donnees est disponible en ce qui concerne la pourriture de la tige du ma1s.
Generalement cettemaladie - provoquee par une espece de Fusarium (F. graminearum, F. moniliforme,
F. oxysporum, F. culmorum) - s'est intensifiee sous l'effet de la fumure azotee et a ete diminuee par
le potassium. Cependant, lorsque Diploidia est l'agent initiateur, l'azote a reduit et les phosphates
(sous diverses formes) ont augmente I'intensite de la maladie. L'effet des doses d'engrais fut tres
variable, les doses elevees ne produisant pas toujours des resultats proportionnellement plus nets
par rapport aux doses moyennes ou faibles.
.
Les effets des engrais ont ete influences par le degre de sensibilite des varietes et - dans une certaine
mesure - par les pratiques culturales. L'on ne disposa que de deux se.ries de donnees relatives il
l'action des engrais sur la pourriture de l'epis du mais. Comme pour la pourriture des tiges,.l'effet
dependait du cryptogame provoquant la maladie.
L'auteur discute egalement les complications et les interactions des engrais avec le metabolisme
physiologique et les proprietes physiques des tiges en se referant il la pourriture des tiges.
145
1. Introduction
It has been known for several decades that fertilizers not only increase the yield of
crops but also affect disease incidence and they must therefore, be considered for
inclusion among prophylactic measures within the framework of field husbandry.
Though certain chemicals have proved to be effective in controlling certain diseases,
their use has, up to now, been limited because of difficulties caused by mode of
infection, the height of the plants and economic considerations. Hence, the emphasis
in seeking control has been on husbandry improvements. There has been considerable
success in breeding more resistant and disease-tolerant hybrids but other husbandry
methods, such as time of planting, spacing, ploughing and fertilization must be
considered. This paper reviews and discusses the effects of fertilizers on the various
diseases.
2. Effect of fertilizers on diseases of maize of various plant parts
2.1. Leaf diseases
Many leaf diseases have been reported on maize of which only a few are really
troublesome on a large scale. From the economic point of view those caused by
Drechslera maydis (Nisikado) Subram. & Jain (syn. Helminthosporium maydis Nisikado) and Drechslera turcica (Pass.) Subram. & Jain (syn. Helminthosporium turciclim
Pass.) are the most important. Research has accordingly concentrated on these fungi.
In Table 1 the influence of the fertilizers is shown (Hooker, Johnson, Shurtle./f and
Pardee [17]). The data reveal that nitrogen and phosphate influenced the disease
only slightly. Negligible differences were seen between the effect of the two rates
applied (about 85 and 170 kg/ha N). The effects of potassium and calcium were more
pronounced and there were striking differences between the two rates of potassium.
The effect of calcium was most evident in plots without potassium. However, Royand
M isra [40] noticed no effects of potassium so that the effect of K + may probably
depend also on soil potassium status as will be discussed later.
Table 1. Leaf blight ratings of US 13-1 corn as influenced by various applications ofK, N, limestone,
and phosphate at Brownstown, Ill., in 1961 (Hooker, Johnson, Shurtleff and Pardee [17J)
kg/ha K
Lime
No phosphate
kg/ha N
Rock phosphate
kg/ha N
Superphosphate
kg/ha N
0
85
170
0
85
170
0
85
170
4.2*
1.2
3.2
1.5
4.0
2.8
4.2
1.2
4.5
2.8
42
2.2
4.8
0.8
4.8
2.0
4.2
1.8
0
yes
no
86,5
yes
no
1.8
. 0.8
1.8
1.0
2.8
1.5
1.2
1.5
2.2
1.5
2.8
1.8
3.2
1.2
3.0
2.0
2.8
1.5
173,0
yes
no
1.5
1.0
2.0
0.8
2.0
1.5
1.0
1.2
2.5
1.0
2.2
. 0.8
1.5
0.8
3.2
1.0
2.2
1.2
* The
leaf blight ratings are the average of 2 observations and range from 0.5 (slight infection)
to 5.0 (severe infection).
146
An increase of leaf blotch following N-fertilization was reported by Ray and Misra
[40] and Vidhyasekaran and Kandasamy [48]. The opposite effect was observed by
Singh and Sharma [42] and Karlen [19]. N- fertilizer affected the proportions of the
various substances containing nitrogen in the plants and there may be a relationship
between the amount of NOr, NO z-, NHr and organically bound nitrogen and
the growth of the fungi in the plants. This could be governed by enzyme-effects
(exopalygalaeturonase, peetintranseliminase).
2.2. Boil smut [Ustilago maydis(DC.)] Cda.
As early as about 1900 manure was said to increase the infection of maize by U. maydis.
The reason was the statement by Brefeld [9] that spore germination was stimulated
by nutrient solutions and manure, but there were no exact experiments up to that time.
Volk [49] obtained different infections in greenhouse experiments when variable
fertilization was applied. Whilst balanced fertilization with NPK and nitrogen and
both low and high amounts of potassium increased infection, phosphate and normal
rates of potassium decreased smut. In the field the results were even more variable.
According to Piemeisel [37], Fleisehmann [13], Vohl [50], Shkodenko [43] and
Miihle and Frauenstein [32] the incidence of the disease increased with N, NPK and
when the soil as 'well' supplied with nutrients. Only phosphate as sole fertilizer
reduced smut infection in some instances. The results of Miihle and Frauenstein [32]
are given in Table 2.
The infection was increased by manure and N-fertilizer and was reduced when potassium was supplied in addition. Lime and phosphate had no influence.
Smaller effects were found by Waiter [51] in 4-years field experiments and also by
Predko [39] and Mirie'[29].
.
Table 2. Boil smut on maize
Number of smut galls (Sum of 4 replications) as affected by fertilizers (Milhle and Frauenstein [32])
(abbreviated, omitting plant parts)
Treatment
Without manure With manure
Without lime
Without lime
With manure
With lime
Without manure
With lime
Unfertilized 1963 ....
1964 ....
Sum ..............
27
10
37
44
47
91
50
44
94
23
26
49
64
39
103
95
95
190
82
73
155
58
46
104
62
27
89
72
84
156
71
82
153
41
30
71
58
24
82
64
46
110
60
72
132
40
32
72
34
15
49
44
61
105
55
53
108
38
14
52
NP
Sum
NPK
1963 ....
1964 ....
..............
1963 ....
1964....
Sum
..............
NK
1963 ....
1964 ....
Sum
PK
Sum
..............
1963 ....
1964 ....
..............
147
A direct, but limited effect on the pathogen may be expected by the use of calcium
cyanamide (CaCN2) applied at rates of 500 kg/ha and more (Dietrich [11 J).
2.3. Cob and tassel smut [Sphacelotheca reiliana (Kiihn) Clinton]
Experiments on the influence of fertilizers on this fungus are scarce. Baier and Knlger
[4 J reported that the infection increased not only after N and NPK but also after PKfertilization and 'Kraal manure'. Podharsky [38J only recommended the use of higher
rates of phosphate.
2.4. Root and stalk rot of maize
The influence of fertilizers on the complex of root and stalk rot of maize, well known
throughout the world, has been much more thoroughly investigated. Root rot, usually
incorporated into the complex, should be analysed separately, because both diseases
may develop independently and sometimes even in a contrary manner (Kruger and
Weiler [25J). Furthermore, the pathogens involved in both diseases should be taken
into consideration. They are primarily species of the genus Fusarium (F. graminearum
Schwabe, F. moniliforme Sheld., F. culmorum (Smith) Sacc. and F. oxysporum) and
Diplodia zeae (Schw.) Lev. In certain regions Rhizoctonia bataticola (Taub.) Butler,
Colletotrichum graminicola (Ces.) Wilson and Phaeocytostroma ambiguum (Mont.)
Petr. are of importance.
Stalk lodging is not only a consequence of fungal attacks but also a characteristic of
cultivars. Physical peculiarities of the stalks may be influenced by fertilizers and play,
therefore, a part in the standing power of the stalks.
My discussion does not extend to changes in plant composition and alterations in
the physiological behaviour of plants which may be caused by the various nutrient
elements as this would be beyond the scope of this paper.
2.4.1. The effect of nitrogen on stalk rot of maize
Early reports on the effect of fertilizers did not mention that the breaking of the stalks
was due to diseases. It may, however, be assumed that the high percentage of lodging
was caused by fungi in the first instance and only secondly by inherently weak
stalks. - Stalk rot generally increased with increased nitrogen supply (Wittels and
Seatz [53J, Krantzand Chandler [22J, Otto and Everett [33J, Parker and Burrows [36J,
Thayer and Williams [47J, Munson [31J, Hinkle and Garrett [16J, Kriiger, Grobler
and DuPlooy [24J, Abney [2J, Kriiger [23J. Even after artificial inoculation with
Gibberella zeae (Schw.) Petch (syn. F. graminearum), D. zeae and Pythium spp. stalk
breakage, internal rotting and premature dying increased when nitrogen exceeded K 20
application (Foley and Wernham [14J). The results were not uniform, however.
Whilst some of the experiments showed quite an increase of stalk rot with increasing
nitrogen, some others (Krantz and Chandler [22J, Abney [2J, Kriiger et al. [24J,
Kruger [23J, Hinkle and Garrett [16J, Parker and Burrows [26J, Otto and Everett [33J
and Josephson [18J showed only slightly more stalk rot or an increase only up to
a certain level (60 to 80 kg/ha N) or an interaction with other fertilizers or organic
amendments. Four main interactions have to be taken into consideration:
- with other fertilizers,
- with hybrid cultivars,
148
- with organisms causing stalk rot,
- with various other factors.
Before discussing these interactions the effect of potassium should be elucidated.
Furthermore, it should be mentioned that one nitrogen-fertilizer (calcium cyanamide)
decreased the occurrence of stalk rot (Stein [43]). This effect would be expected to
be caused more by killing of the fungus in the soil than by changing the physiological
state of the plants.
2.4.2. The effect ofpotassium on stalk rot of maize
Potassium seems to be the fertilizer which most interacts with and reduces stalk rot
(Liebhardt and Murdoch [26], Anonymous [1], Boswell and Parks [8], Younts and
Musgrave [55J, Siebold [41], Wittels and Seatz [53]). The effect seems to be limited
to a certain level of application due probably to the natural occurrence of potassium
in the soil. That may be concluded from experiments in South Africa where stalk rot
was practically unaffected by KCl-fertilization (150 kg/ha KzO) in a soil fairly rich
in potassium (Kriiger et al. [24], Kriiger [23]). Younts and Musgrave [55J obser·ved
no real effect when applying only about 40 kg/ha KzO but a large effect when 240 kg/ha
were supplied. Similar results were obtained by Siebold [41] and Burkart, Zscheischler
and Diez [9b], who described exceptional K+ fixation in a clay soil of the Danube
valley in Bavaria. Up to 600 kg/ha KzO was necessary to increase yield economically
and decrease stalk rot to a level of about 12% in contrast to 45% in plots without
potassium. Other results showed a reduction of disease at lower rates only (75 kg/ha
KzO) but no further reduction with higher amounts {Boswell and Parks [8], Josephson
[18J. After artificial inoculation with G. zeae, D. zeae and pythium spp. the same
trend could be found. The extent of rotting inside the stalks and the stalk breakage
were reduced by potassium when nitrogen was low (Foley and Wernham [14]).
Contrary results were noticed by Martens and Amy [28] with D. zeae inoculations.
There is the indication that at least in some instances the effect of the K-fertilizers on
stalk rot waS due to the cr- and not solely to K+ as was concluded by Younts and
Musgrave [55] who used K ZS0 4 and KP0 3 for comparison. That effect of Cl- was,
however, partially questioned by Martens and Amy [28].
2.4.3. Interaction oj nitrogen with other fertilizers
The interaction of nitrogen with potassium was demonstrated by Thayer' and
Williams [47], Munson [31], andOtto and Everett [33]. In some experiments the
effect of potassium was more pronounced at lower and medium nitrogen rates (Thayer
and Williams [47], Thayer [46]) and Otto and Everett [33]. On the other hand
v. Burkesroda [9a] found that it was more so at higher amounts (Figure I). In experiments in Germany potassium (40% KCI) was applied at 240 kg/ha KzO in addition to
various amounts of slurry (60-150-250 m'/ha) and for comparison with mineral
fertilization (N: 150, PzOs: 120, KzO: 200 kg/ha). Stalk rot was reduced in all four
seasons as can be seen from Table 3. There was the indication that the effect was
more pronounced in seasons when a moderate percentage of plants was infected
than in those when only slight (1975) or severe (1974) infection was present. The
effect of slurry was not well defined. In some years no differences were visible, in
others an increase of stalk rot was noticed, mainly with higher amounts of the
manure (1971,1973 and 1974).
149
"0
~
-g
o~
_
.........
,
... '
....
50 1---+--+--+-+--f-:=-~~'-+'--t--+----1I---++--+--t---;
....
-_..
-~
\
40 r-+--+-t---+---+-t+--+--+-t--+---+-+-+--+---l
30 1--+---+-+--+--I--+-~-+--+----4-+--+l--+-~
- --- -,- _.
20 1---H\r--t-I---t---I--+--\iI---I--=t-...-t--..:=:::j:---+--+---I
\~ -
~
10 I---+---+~-+--+-_+--+---+~+--+---;I---+---+-+-+-~
....... 1 - 1 - - - .
_'"
\
.... ~- I--I--_\~
Figure 1. Lodging of maize plants decreases with rising potash applications (N : K interactions).
Nitrogen-potash experiment with Rhodesian double hybrid 13, fourth season. Marodzi-Toitagura
Intensive Conservation Area (v. Burkersroda [9a]) --- drawn by the author.
NI = 40 lb N per acre
Nz = 80 Ib N per acre
N 3 = 120 lb N per acre
K I = 30 Ib KzO per acre
K z = 60 lb KzO per acre
K 3 = 120 Ib KzO per acre
P = 60 lb PzOs per acre
Table 3. Influence of potassium and slurry on stalk rot of maize (Krilger and Hoffmann [unpublished
results])
Fertilizer
kg/ha
Infected maize stalks in %*
KzO
1971
1972
1973
1974
1975
Mineral fertilizers
0
240
16.7
15.3
9.0
22.0
14.7
38.8
30.5
5.5
3.1
50 m 3/ha slurry
0
240
8.9
18.4
6.6
30.5
18.0
39.0
32.8
6.8
4.9
150 m 3/ha slurry
0
240
13.3
13.2
9.0
36.1
25.4
52.0
45.5
1.8
1.5
250 m 3 /ha slurry
0
240
18.5
13.5
9.3
58.5
27.9
53.3
51.5
4.4
1.8
2.4
5.0
8.1
8.5
2.1
LSD, p<0.05
* Stalk rot was determined by pressing the lower portion of the stem by thumb and forefinger. Stalks
yielding to pressure were counted as infected.
150
2.4.4. Interaction offertilizers with hybrid cultivars
In spite of breeding for resistance stalk rot is still an important factor in maize production. The reduction of stalk rot by potassium was seen in the moderately resistant
cultivars. In highly resistant (Boswell and Parks [8)) and highly susceptible (Dtto
and Everett [33)) hybrids the differences vanished. That is quite understandable as
the susceptible 'cultivars get the disease in any case unless really powerful control
measures are used and the resistant ones are not infected even under moderate stress
or unbalanced fertilizer conditions.
2.4.5. Interaction offertilizers with stalk rot inciting organisms
Unfortunately some of the publications do not detail the organisms -responsible for
the stalk rot. F. moniliforme and G. zeae (syn. F. graminearum) or Fusarium spp. were
stated to be pathogens in experiments by Dlto and Everett [33), Thayer [46), Parker
and Burrows [36) and Thayer and Williams [37). Fusarium spp. are also assumed to
be present in experiments by Siebold [41] as concluded by the author who made a
survey of maize diseases (1969-1973) in Germany (Kriiger [unpublished data)):
However, in the USA, in S. Africa and other countries, other fungi (D. zeae, R. bataticola) cause stalk rot. In S. Africa two Fusarium species and D. zeae were present
every year but which organism dominat.ed depended upon the weather conditions.
The effect of the fertilizers· on stalk rot varied according to the dominating fungi.
Stalk rot caused by Fusarium spp. was generally reduced by the sole application of
phosphate whilst that caused by D. zeae increased (Table 4). Nitrogen (+ PzOs) on
the other hand reduced Diplodia-stalk rot and increased Fusarium-infestation (Kriiger
et al. [24), Kriiger [23)). Kraal manure and compost had about the same effect as
the mineral N -fertilizers. Similar results were obtained in South Africa by Mallett [27).
Broken stalks (as a criterion of stalk rot) were fewer in N-fertilized (0-200-400 kg/ha N)
plots where D. zeae was present as known by the author. Phosphate had no effect.
Stalk rot increased also with increasing plant population (11000--33000 plants/ha),
the increase being about the same, independent of the fungi (D. zeae or Fusarium spp.)
causing the disease. The application of nitrogen (40 and 100 kg/ha N) had no pronounced effect on the ratio of stalk rot (Kriiger [23)).
Table 4. Effect of fertilizers on the incidence of stalk rot (Krilger et al. [24], shortened, only the
mean values of various experiments are given)
Treatment
0 .............
P ............
N+P . ........
N+P+K .....
N+P+K+Ca
1959/60*
1962/63**
1961/62*
Stalk
rot
Arcsin
V%
Yield
in***
bags/
morgen
Stalk
rot
Arcsin
V%
Yield
in
bags/
morgen
Stalk
rot
Arcsin
Diplodia
pycnidia
Arcsin
'\1%
'\1%
Yield
in
bags/
morgen
11.5
25.9
13.0
8.4
18.1
15.3
19.1
25;9
21.4
26.6
20.1
33.2
19.1
15.8
23.1
17.7
20.9
30.1
24.2
27.6
19.6
27.7
34.4
29.1
30.8
17.7
34.9
17.7
30.2
32.6
15.9
16.1
21.8
18.1
20.1
* caused mainly by D. zeae
** caused mainly by F. moniliforme and D. zeae
*** 1 bag/morgen= 100 kg/ha
151
2.4.6. Interaction offertilizers with other factors
There was an increase in stalk rot when crop residues were ploughed down in contrast
to being left on the surface. Nitrogen (120 kg/ha N) as subtreatment caused more
stalk rot irrespective of the main treatment (Parker and Burrows [36]). The N-effect
on the Diplodia-stalk rot was not changed substantially in experiments were a) crop
residues were doubled, b) maize stalks were removed and c) stalks were ploughed
down in normal quantities (Kriiger [23]). - Application of 240 kg/ha KzO (as KCl)
in the row resulted in slightly more stalk rot in contrast to broadcasting the fertilizer
(Younts and Musgrave [55]).
2.5. Effect of fertilizers on root rot
Effects on root rot have been little investigated. In field experiments, Kriiger [23]
reported a slight increase of root rot of fully grown plants when they were top dressed
with 25 and 50 kg/ha N. The causal fungi were mainly F. moniliforme and F. oxysporum.
Maize in the seedling stage and grown in solutions was not affected by N, P and K at
various rates when F. moniliforme and F. moniliforme vaT. subglutinans were the
pathogens (Edwards [12]). Similar results were obtained in gravel culture with N, P
and K at three rates in factorial combinations when G. roseum f cereals (probably
syn. F. graminearum) was injected into the solution and the roots scored two weeks
later (Thayer and Williams [47]).
2.6. Effect of fertilizers on cob rot of maize
There have been few experiments. K6hler [21] reported that cob rot was reduced by
phosphate when P content in the soil was low and when Fusarium (F. moniliforme?)
was involved but not when D. zeae or G. zeae were the pathogens. Similar results
were obtained by Kerr [20] in Rhodesia where nitrogen was applied to soil high in
phosphate. In this case the ear infection caused by D. zeae decreased with increasing
N-fertilizer.
2.7. Some explanations of the effect of fertilizers
It is quite difficult to understand the effect of fertilizers. Depending on the scientific background of researchers the mode of action is either explained by effects on
morphological characters of the stalks or by effects on chemical composition. A direct
effect on the fungi may on the other hand not ·be completely excluded. - The rind
thickness, length and diameter of stalks and the corresponding mechanical strength
required to crush the stalks were used as criteria and were changed by fertilization,
mainly by nitrogen (Foley [15], Sleper and RUssel [44]), but the breaking strength
was not altered ( Abney and Foley [3]). The stalks were consequently weaker per unit
cross-sectional area. Potassium increased stalk size and a greater load was required to
break them. That effect lasted, however, only up to frost, when all stalks were severely
lotted. Quite contrasting were the findings of Zuber and Loesch [56] when analysing
the stalks of hybrids susceptible and resistant to stalk rot. They found that the ash
and potassium content was higher in susceptible hybrids. The contrary would have
been expected. No reason can be offered for that fact.
152
Another characteristic is the chemical composition of the stalks (BeMiller, Tegtmeier
and Pappelis [6]), including soluble sugars in the pith (Craig and Hooker [l0],
Mortimore and Ward [30]) which may play a part in susceptibility (Whitney and
Mortimore [52], BeMiller and Pappelis [5], Younts and Musgrave [55]). The sugar
content seems, however, to be closely connected with the pith condition, based on
ceIl death pattern, and which may finalIy play a dominant role (Craig and Hooker [10],
Pappelis, Mum/ord, Abney and Pappelis [35], Wysong and Hooker [54]). Nitrogen
and phosphate increased and potassium and limestone decreased the rate of cell
mortality (Martens and Arny [28], Pappelis and Boone [34]). The increase of dead
ceIls may, however, not be the sole reason for infection by all parasites. As was shown
above (Kriiger et al. [24], Kriiger [23] and Kerr [20]) the fungi causing stalk rot.
may react differently. Recent investigations (BeMiller, Johnson and Pappelis [7])
have shown that along with the ceIl death pattern other constituents (K, Si, P, Fe,
Co, Sr, Cu, Mo, Ba, Mg, N and crude fiber and other solubie substances) changed as
weIl during the period after silking. That is the time when infection usually occurs.
3. Discussion
From these somewhat contradictory and limitec,l results it may be concluded that
fertilizers do have some influence on maize diseases. Real control is limited to a (ew
cases in deficient soils. We should therefore, aim at the balanced use of fertilizers
combined with other measures of good husbandry in order to reduce'disease in high
yielding crops. Nitrogen usuaIly increased the incidence whilst potassium, probably
preferably in the form of KC!, phosphate and calcium may have decreased it. It
would, however, be unrealistic to demand a reduction in nitrogen usage as the
consequent yield reduction would be too serious. Excessive applications should in
any case be avoided.
The reaction of organisms should not be negleCted as was shown with D. zeae and
Fusarium spp. which were influenced differently by nitrogen and phosphate. Special
attention should be paid to the fertility state of the Soil in order to determine whether
any reaction of the plants may be expected when 'normal' quantities of the fertilizers
are applied. Furthermore, the uptake of fertilizers by the plants and the effect on
growth is influenced by soil moisture, soil type, temperature, humidity, rainfall and
evaporation. Thus, it may be expected that these factors affect infection and/or spread
of the fungi in the plants as well. In future experiments these environmental conditions
should not be neglected in order that the variability in the results obtained can be
explained. Fertilizers might be expected to produce an effect by changing the physiological state and consequently the resistance to a fungal attack. Conclusions should
be drawn carefully when stalk rot is assessed after artifical inoculations in the internodes, because that reaction does not always correspond to the degree of naturally
occurring stalk rot.
153
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25. Kriiger, W. und Weiler, N.: Uber die Anfalligkeit der Maishybriden gegen Wurzelfiiule. Z.
Acker- und Pflanzenbau 141,205-210 (J975).
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Agron. J. 57, 325-328 (1965).
154
27. Malleft, J.B.: Influence of plant population density and fertilizer treatment on maize grain
yields and related plant characteristics in the Bergville district. S. Afr. J. agric. Sci. 7, 55-62
(1964).
28. Martens, J. W. and Amy, D. e.: Effects of potassium and chloride ion on root necrosis, stalk
rot, and pith condition in corn (Zea mays L.). Agron. J. 59, 499-502 (1967).
29. Miric, Mirjana: Effect of irrigation, fertilization and sowing density on the appearance of
U. maydis in some maize hybrids. Zast. Bilja, 20, 261-267 (1969). Abstract: Rev. appl. MycoI.
49, 426 (1970); Russ.
30. Mortimore, e.G. and Ward, G.M.: Root and stalk rot of corn in southwestern Ontario. Ill.
Sugar levels as a measure of plant vigor and resistance. Can. J. Plant Sci. 44, 451-457 (1964).
31. Munson, R.D.: Influence of nutrient balance and other factors on corn maturity. Comm. Fert.
& Food Chem. 104, 24-25 (1962).
32. Miihle, E. und Frauenstein, Kiite: Der Einfluss der Dtingung auf das Auftreten des Beulenbrandes
an Kornermais. Nachrichtenbl. Pflanzenschutzd. DDR 20,15-18 (1966).
33. OftO, H.J. and Evereft, H.L.: Influence of nitrogen and potassium fertilization on the incidence
of stalk rot of corn. Agron. J. 48, 301-305 (1956).
34. Pappelis, A.J. and Boone, L. V.: Effects of soil fertility on cell death in corn stalk tissue. Phytopathology 56, 850-852 (1966).
35. Pappelis, A.J., Mumford, Pauline M., Abney, T.S. and Pappelis, G.A.: Classification of corn
inbreds using pith cell death patterns and the prediction of stalk rot response. Cereal Res.
Communications 3, 227-232 (1975).
36. Parker, D. T. and Burrows, W. e.: Root and stalk rot in corn as affected by fertilizer and tillage
treatment. Agron. J. 51, 414-417 (1959).
37. Piemeisel, F.J.: Factors affecting the parasitism of Ustilago zeae. Phytopathology 7, 294-307
(1917).
38. Podhradsky, J.: Diseases of maize in Hungary and some remarks on theircontroI. Novenytermeles 9,321-334 (1960) (ung.) Abstract: Rev. appI. Mycol. 40, 423 (1961).
39. Predko, I. G.: The effect of previous crops and fertilizers on blister smut of maize. Zshchita
Rastenii No. 10, 54 (1972). Abstract: Rev. Plant Path. 52, 446 (1973).
40. Roy, R.K. and Misra, A.P.: The influence of soil fertility on the severity of leaf blight of maize
(Helminthosporium turcicum Pass.). Indian Phytopath. 19, 359-363 (1966). Abstract: Rev. appl.
MycoI. 47, 91 (1968).
41. Siebold, M.: Einfluss der Kalidtingung auf die Stengelfaule bei Kornermais. Gesunde Pflanze
26, 65-68 (1974).
42. Singh, B.M. and Sharma, Y.R.: Effect of nitrogen fertilization on the incidence of Helminthosporium turcicum in maize. Indian Phytopath. 26, 474-478 (1973). Abstract: Rev. Plant Path.
54, 335 (1975).
43. Shkodenko, V.I.: Influence of mineral fertilizers on infection of maize by blister smut. Zakhyst
Roslyn 52-56 (1969). Abstract: Rev. Plant Path. 49, 28 (1970), Russ.
44. Sleper, D.A. and Russel, W.A.: Interrelationships among several stalk characteristics in maize
and their significance in resistance to natural stalk breakage. Iowa State J. ScL 45, 197-209 (1970).
45. Stein, E.: Untersuchungen tiber Auftreten und Bekampfung der Maisstengelfaule. Gesunde
Pflanze 25, 44-47 (1973).
46. Thayer, P.L.: Some factors affecting Gibberella stalk- and root-rot of corn. Diss. Abstr. 19,
653-654 (1958). Abstract: Rev. appI. Mycol. 38,513 (1959).
47. Thayer, P. and Williams, L.E.: Effect of nitrogen, phosphorus,and potassium conCentrations
on the development of Gibberella stalk- and root rot of corn. Phytopathology 50, 212-214{1960).
48. Vidhyasekaran, P. and Kandasamy, D.: Effect of soil fertility on the physiology of corn plants
in relation to Helminthosporiose disease incidence. Phytopath. Z. 72, 11-20 (1971).
49. Volk, A.: Beitrage zur Kenntnis der Wechselbeziehungen zwischen Kulturpflanzen, ihren
Parasiten und der Umwelt. 4. Mitt. Einfltisse des Bodens, der Luft und des Lichtes auf die
Empfindlichkeit der Pflanzen fUr Krankheiten. Phytopath. Z. 3, 1-81 (1931).
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51. Waiter, J.M.: Factors affecting the development of corn smut, Ustilago zeae (Beckm.) Unger.
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155
53. Wittels, H. and Seatz, L.F.: Effect of potash fertilization on yield, stalk breakage and mineral
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Diplodia stalk rot in corn hybrids. Phytopathology 56,26-35 (1966).
55. Younts, S.E. and Musgrave, R.B.: Chemical composition, nutrient absorption, and stalk rot
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.
156
The Influence of Potassium
on the Resistance of Oil Palms to Fusarium
M.Ollagnier' and J.-L. Renard'
Summary
The application of increasing rates of potassium chloride greatly reduced the development of wilt
caused by Fusarium oxysporum f. sp. elaeidis in oil palms in the Ivory Coast. The very strong effect
on a susceptible cross was equally marked in a resistant one. The leaf potassium level which is
most favourable for resistance is the same as that required for optimum production.
Resume
L'application de doses croissantes de chlorure de potassium fllduit fortement la progression de la
maladie du deperissement due 11 Fusarium oxysporum f.sp. elaeidis sur palmier a huile en Cote
d'Ivoire.
'
L'effet tres important sur un croisement sensible est encore tres net sur un croisement resistant.
Le niveau optimum de nutrition potassique de la feuille vis-a-vis de la fusariose est sensiblement le
meme Que le niveau optimum vis-it-vis de la production.
1. Introduction
Prendergast [11] reported in 1957 that potassium fertilizer applied as 1 to 2 kg sulphate of potash per tree reduced damage caused by Fusarium on oil palms at Cowan
Estate, Nigeria. The same author [12] showed that in the pre-nursery and nursery
nitrogen reduced the incidence of the disease on young plants following inoculation
but that in the same conditions potassium played no part.
We have obtained identical results on plants inoculated with Fusarium oxysporum
f. sp. elaeidis in the nursery receiving nutrient solutions containing variable amounts of
potassium. However, a fertilizer experiment carried out in the Ivory Coast (DA Cp.. 13
at Dabou on savannah soil in an area strongly infected with Fusarium) showed that
potassium did affect the predisposition of the oil palm to attack by the disease. Similar
results were obtained earlier in the People's Republic of Benin (Dahomey).
Director of Research, IRHO, Paris.
'Director, Plant Pathology Department, IRHO, Ivory Coast.
1
157
2. Description of the experiment
A 4 x 2 x 2 x 2 factorial experiment with confounding was laid down in 1964 at Dabou
on a savannah soil with oil palms planted in the same year. Potassium was applied at
four levels, the other elements (Mg, Band Mn) each at two levels. The plots each
comprised four rows of 13 trees all of which received the fertilizer treatment, the two
central rows only being recorded.
The levels of potassium applied, the only treatments which interest us here, are given
in Table 1.
Since maximum production was not achieved at the K 3 level, treatment K 1 the yield
of which was the same as that of Kz, was modified in 1973 to receive 4Y> kg per .tree
from that date.
Two breeding lines were planted in equal numbers in each plot viz:
- Da 835 (D3D x P2054P) susceptible
- Da 810 (Ll5TT x D1OD) resistant.
Table 1. Schedule of KCI applications (kg KCl per tree and per annum)
K,
K2
K3
.
.
.
.
.
.
0.100
0.200
0.300
0.400
0.500
0.500
0.250
0.500
0.750
1.000
1.250
1.250
0.500
0.750
1.250
1.500
1.500
1.500
0.500
1.000
1.500
2.000
2.500
3.000
.
.
0.500
0.750
1.250
4.500
1.500
1.500
3.000
3.000
Dates
1964 (Planting)
1965
1966
1967
1968
1969
,
1970 to 1972
From 1973
3. Results
3.1. General development of Fusarium
The first cases of palms infected with Fusarium were noticed during 1968. At that stage
an average of 2% of the palms was affected and at eleven years from planting 22%
were infected (Figure 1). There was a large difference between the susceptible and
resistant lines. Disease development on the susceptible line was very rapid, reaching
37.9% infected at 11 years while, at the same age, only 7.8% of the resistant plants
were diseased.
3.2. Influence of potassium on the development of Fusarium
The influence of potassium chloride on the number of diseased plants first became
really apparent in 1971, the percentage of diseased plants being the same on all treatments in 1968 and 1969. From 1971 the evolution of the disease was most rapid in the
Ko treatment; differences between the treatments K" Kz and K 3 became more marked
in 1973, 1974 and 1975. The level of disease in treatment K 1 was roughly the mean for
158
50
K1i
//KO
40
//
~
2
a:
/
Susceptible
Cross
DA 835
K2
// / ;/
30
~._.
"
K3
'f
,/ ,f/'"
-cl:
/
/
III
~
....
:'/
u..
/I
/
j;';
I
20
/
, __I
/
fr //
,
10
///
,t/ /
,7.1
KO
/
Resistant
Cross
/
LM 810
K1
./
o
DATES
Fig.I. Development of Fusarium attack at various K levels' on susceptible and resistant crosses.
the whole experiment. High potassium dressings did not prevent the appearance of the
disease but slowed down its progress; the spread of disease from one tree to another
was reduced; it appeared as though the main effect of potassium fertilizer was to
prevent growth of the Fusarium, the number of initial infection sites being independent
of the fertilizers applied (Figure 1).
While there was a very marked effect of potassium on the susceptible cross it was
equally large ori the resistant one.
The results showed a very neat pattern of significance, the variance ratio (linear effect
of potassium/error variance) moving from 0.52 (insignificant) in 1971 to 6.21 * (significant at p= 0.05) in 1973, 6.98* in 1974 and 10.3* in 1975.
These very clear results showing a relationship between increasing rates of potassium and increasing resistance to Fusarium confirm those obtained by IRHO in
the Peoples Republic of Benin (Dahomey). That experiment was begun in 1948 on a
stand of old palms all planted in 1929/30 and comprised four treatments measuring the
effects of K, NP and their interaction. There was a marked favourable effect of potassium (Table 2).
159
Table 2. Benin Republic (Pobe Station)
Upper figures: Effect of potassium on % trees affected by Fusarium (1964)
Middle figures: Mean yield-kg. bunches/tree (1959-1964)
Lower figures: Leaf K contents (J 964)
N-P
(-)
K
12.5 %
77.0
0.801
6.2 %
66.0
0.869
(-)
50.0
60.0
0.501
28.1
45.0
0.389
3.3. Leaf analysis and Fusarium
The relationship between potassium application and the development of Fusarium is
reflected in a similar relationship between damage caused by the disease and leafpotassium content (Figure 2). During 1968/69 there was no connection between the occurrence of palms affected by Fusarium and leaf potassium, but, starting in 1971, and
even more clearly from 1973, significant differences between leaf K content and the
percentage of diseased palms appeared. Disease attack was markedly reduced when leaf
K content exceeded 0.8% K and above this value the disease made only slow progress.
This effect of potassium only became apparent nine years after the first application of
fertilizer.
t.KO
Kl
°loF
~
.. K2
30
• K3
19756
1974 A.....
~
25
::J
a:4:
Vl
::J
....
.......
............
............
.........
20
.........
l.L
~
15
1971 A.....
..
~
.... ....
i
.... ....
-- -- ......... .......
....
.
\
~~
,\
"'.....
'6
..
0
........ ~,
,~.
-..•
10
1969 A----_ -- -------il.,.•
5
1968 A-._._._.
./.A "'i
-.-._~~
0,400 0.500 0.600 0,700 0.800 0,900 1.000 LEAF K %
Fig.2. Effect of leaf K on Fusarium attack.
160
3.4. The effect on production
Yields of the legitimate palms (i. e. excluding supplies planted to replace vacancies in
the original stand, which were of different parentage) were separately recorded for
healthy and diseased palms. The potential production per hectare was calculated from
the yield of the healthy palms and this is compared in Table 3 with the actual yield
recorded from the whole plot listing under each treatment the percentage yield loss due
to the combined effect of fertilization and disease. Losses in potential production were
closely connected with potassium nutrition (Figure 3) and were also related, to the
severity of attack by Fusarium (Figure 4). There w'!-s a highly significant correlation
(r = 0.982) between percentage of diseased palms and loss in potential yield for the
seasons 1972/73, 1973/74 and 1974/75 and the relationship can be expressed in the
equation y = 0.786x-0.18. The regression line is steeper for seven year old palms
(season 1971/72) than for the older palms.
The potential yield which depends on potassium fertilization alone is only really
affected at the lowest rates. The yield reduction is due mainly, therefore, to the effect of
Fusarium wilt, which is very marked in treatment Ko. It can be concluded that the
direct effect on yield of average potassium fertilization can be masked by losses through
wilt.
Regular application of potassium fertilizer to keep the leaf K level above 0.9%
benefited the health of the plantation; at ten years after planting the loss in potential
production in palms which received heavy potassium applications was orily one half of
that in palms which received no potassium. In any case potassium had a large direct
effect in increasing yield by increasing both mean bunch weight and number of bunches
produced. For the two last seasons, the potential yield of bearing trees under treatment
6
KO
" Kl
• K2
• K3
toZ
w 25
u
Cl:
W
0-
1Il
1Il
20
9
0
..J
w
>'
15
..J
« 10
i=
z
w
b0-
S
0,400 0,500 0,600 0.700 0.800
O.~OO
1.000 LEAF K %
Fig.3. Yield loss related to K nutrition.
161
......
0\
N
Table 3. Yield per hectare under various treatments (kg bunches(ha)
1972-1973
1973-1974
1974-1975
Treat- Yield
Potential Loss( % Loss
ment original yield
ha
in
yield
trees
Potential Loss( % Loss
Yield
original yield
in
ha
yield
trees
Potential Loss( % Loss
Yield
original yield
ha
in
yield
trees
Yield
Potential Loss( % Loss
ha
in
original yield
yield
trees
Ko
K,
Kz
K3
7477
10648
11513
13683
10403
15848
15118
16531
Seasons
1971-1972
--
Ko
K,
Kz
K3
11898
15910
14908
16893
15272
18567·
16662
18990
3374
2657
1754
2097
22.1
14.3
10.5
11.0
9173
12331
12905
15026
1696
1683
1392
1343
18.5
13.6
10.8
8.9
13 385
19068
16820
18315
2982
3220
1702
1784
22.3
16.9
10.1
9.7
10610
14005
14329
15600
13859
17704
16410
18029
3249
3699
2081
2429
23.4
20.9
12.7
13.5
K content
% Fusarium
K content
% Fusarium
K content
% Fusarium
K content
% Fusarium
0.481
0.730
0.812
0.946
15.1
11.5
10.5
9.1
0.433
0.748
0.811
0.943
24.7
16.5
13.7
11.4
0.503
0.783
0.798
0.931
26.9
21.9
14.7
11.4
0.533
0.810
0.784
0.921
30.1
25.0
16.8
14.8
Table 4. DA ES D83 Development of Fusarium from end 1971 to August 1975 (comparison of extension and replanting)
Line
LM 1706
LM 1544
LM 1598
LM 1691
LM 1551
LM 1599
LM 1732
LM 1720
LM 1719
LM 1686
-Fusarium
1971
1973
1974
1975
Index
113
81
112
65
123
100
80
40
55
67
Leaf % potassium
......
0\
w
Extension
Replanting
No. of trees
recorded
% Fusarium
101
105
104
54
106
107
101
107
98
118
3.0
2.9
1.0
3.7
7.5
0.9
0.0
1.9
1.0
0.8
Oct. 1971
May 1973
5.0
5.7
1.9
5.3
10.4
0.9
0.0
0.0
2.0
0.0
July 1974 August 1975
5.0
8.6
4.0
13.0
19.8
0.9
0.0
0.0
2.0
0.0
4.9
10.5
4.8
16.6
27.3
3.7
0.0
0.0
2.0
0.0
2.2
No. of trees
recorded
103
108
108
54
107
108
54
108
108
. 108
% Fusarium
Oct. 1971
15.2
9.3
0.9
7.4
16.0
2.8
1.9
0.0
0.0
0.9
May 1973
July 1974 August 1975
11.5
12.1
4.6
7.4
29.0
3.7
5.5
0.0
0.0
0.0
12.3
19.4
10.1
14.8
34.5
4.6
1.8
0.0
0.0
0.0
14.3
22.2
10.1
20.3
41.1
7.4
5.5
1.8
0.0
0.0
5.3
3.0
7.7
5.2
10.0
6.5
1.19
1.18
12.3
0.89
0.89
f:,
'I. Yield
loss
KO
K1
• K2
• K3
'I
25
1971
f
i
/
20
i
/
I
/
15
/
I
~
11
I
1
......".1
1
10
15
20
25
30
'I, F
FigA. Effect of percentage Fusarium attack on loss in potential yield.
K 3 was about 18 tonne/ha (Table 3) while the corresponding figure for treatment Ko
was only 13.5 tonne.
3.5. The effect of previous cropping
Evidence on the effect of previous cropping is available from an experiment (DA
ES.83) comparing the behaviour of ten breeding lines:
Extension (planted on land cleared from savanna) 12.3 % palms infected with Fusarium.
Replanting (planted on land previously carrying oil palm) 6.5% palms infected.
In the case of the most susceptible lines disease was, in some cases, only half as severe
in the replanting as in the extension planting (Table 4). Since the soil of an old plantation carries a good reserve of F.oxysporum (Renard [13]) one would have expected
more severe losses in the replanted area than in the extension. However, leaf analysis
seems to offer an explanation of the results as leaf K was always higher (mean value
1.2) in the replanting than in the extension (0.9). In the light of the results obtained in
experiment DA CP 13 described above it seems reasonable to think that the better
performance in resistance to Fusarium by replanted palms was at least partly caused by
the higher potassium content.
164
3.6. Other forms of Fusarium
The disease with which we have been concerned above is characterized by wilting of
the palm leading sooner or later to its death and is due to Fusarium oxysporum
entering the plant via the root and penetrating the stem to a varying height. The
pathogenicity of this fungus has been abundantly demonstrated using an inoculation
technique in the nursery to measure resistance by various progenies ( Renardetal. [ 14]).
There are two other diseases of adult palms which are associated with different
Fusarium organisms:
The disease known as Boyomi (Heim [8]), in which Fusarium bulbigenum var.
tracheiphilum is found in the rachis and causes its desiccation, accompanies severe
magnesium deficiency. A fertilizer experiment carried out in the Congo showed that
application of magnesium sulphate considerably reduced this disease (33% trees
affected in the nil magnesium treatment compared with 7% for those receiving Mg).
In this case it was not possible to test the pathogenicity of Fusarium experimentally.
Applying potassium to the soil (though leaf K content was adequate) had an adverse
effect (23% trees affected with potassium, 17% without) due probably to an antagonistic effect on magnesium uptake which was, in this case, the limiting fae.tor.
Crown disease, which affects young palms, is due to a single recessive gene (de
Berchoux et al. [3]) and is associated with Fusarium solani var. minus. Without doubt
the dominant factor is in this case genetic and, up to now, no connection with nutrition
has been demonstrated.
4. Discussion
Potassium has been shown to have beneficial effects in a wide.range of fungal diseases.
Akdogan [2] drew attention to this,in the case of ink disease of chestnuts. It has been
well demonstrated in the case of stalk rot of maize caused by Fusarium moniliforme
(Abney et at. [1]) or ofrice caused by Leptosphaeria salvinii, Chien [5]. It has also
been found with leaf disease such as mildew in the vine (Hoffman et al. [9]) or apple
scab (Le/ter et al. [10]) and in diseases affecting the inflorescence like ergot in
sorghum which is caused by Sphacelia sorghi (Chinnadurai [6]).
Some authors have noted opposite effects of potassium. Thus potassium fertilizer
increased foot rot of grasses (Stetter [16]) and favoured Cercospora in coffee
(Fernandez [7]). Stored carrots were more susceptible to Centrospora acerina when
they had received generous potassium dressings during growth (Roll-Hansen [15]).
However, such examples are comparatively rare.
The effect of potassium on disease resistance probably results fIOm its involvement in
metabolic processes within the plant. Through its direct effect on water economy,
. potassium deficiency leads to the accumulation of soluble glucides' and enhanced
activity of hydrolases which allows 'free amino-acids and ammonia to accumulate, all
of which substances promote the development of parasites (Chaboussou [4]).
5. Conclusion
Several conclusions can be drawn from the observations made on Fusarium attack on
oil palm on a Tertiary Sand in the savanna zone:
165
At high rates of potassium (Kz and K 3) fewer trees were attacked by Fusarium than at
low rates (Ko and K 1).
Potassium fertilizer can reduce the severity of attack by the disease but heavy dressings,
even when applied right from the time of planting, do not reduce the number of initial
infections. Potassium has a long-term effect which becomes marked at seven years
from planting.
Leaf analysis, which enables us to measure the uptake of potassium, shows that a level
of 0.9% K is equally 'critical' both for yield and resistance to Fusarium.
Fusarium is a most important disease in certain parts of Africa and the generous use of
potassium fertilizer is without any doubt a very important complement to the progress
which has been made by plant breeders in improving resistance to the disease.
References
1. Abney, T. S. and Foley, D. c.: Influence of nutrition on Stalk rot development ofZea Mays. Phytopathology 61, 1125-1129 (1971).
2. Akdogan, S.: Kestane miirekkep hastaligi. (Phytophthora cambivora Petri) mticadelesi tizerinde
arastirmalar. Researches on the control of ink disease (P. cambivora) of Chestnut Bitki Koruma
Btilt. 10, 121-130 (1970).
3. de Berchoux, C. and Gascon, J.-P.: L'arcure defoJiee du palmier it huile, Oleagineux, 713-715
(1963).
4. Chaboussou, F.: Le role du potassium et de l'equilibre cationique dans la resistance de la pI ante
aux parasites et aux maladies. Le Document technique de la SCPA 16, 1-26 (1973).
5. Chien, C. C. and Chu, C.L.: Studies on the effect of fertilizers to rice disease. Jnl. Taiwan Agric.
Res. 19, 62-71 (1970).
6. Chinnadurai, G.: The role of fertilizers on the incidence of sugary disease of Sorghum. Trop.
Agric. Trin. 48, 51-53 (1971).
7. Fernandez, Borrero, O. and Lopez-Duque, S.: Fertilizaci6n de plantulas de cafe y su relaci6n con
la incidencia de la mancha de hierro (Cercospora coffeicola Berk-y Cooke). Cenicafe, Centro
Nacn - Invest. Cafe, Chinchina Caldas, Colombia, Tropical Abstracts 28, W 2117 (1971).
8. Heim, R.: Introduction it l'etude au Boyomi, Rev. de Mycologie XIV, suppl. col. n° 2, 41-49
(1949).
.
9. Hoffmann, M. and Samish, R. M.: Free amino-acid content in fruit tree organs as indicator of
the nutritional status with respect to potassium. 6th Int. Coil. on Plant anal. and ferti. ProblemContribution Volcani Institute of Agr. Res. Bet Dagan, Israel 1970,1735 E., 189-206 (1969).
10. Lefter, G. and Pascu, I.: Influenta factorilor climaticici technici ampra sensibilisatii la rapan a
soiului golden delicious. Protectia cultur, horti viticole 6, 95-100 (1970).
11. Prendergast, A. G.: Observations on the epidemiology of vascular wilt disease of the oil palm
(Elaeis guineensis, Jacq.), J. W. Afric. Inst. for Oil Palm Res. 2, 147-175 (1957).
12. Prendergast, A. G.: A method of testing oil palm progenies at the nursery stage for resistance to
vascular wilt disease caused by Fusarium oxysporum, Schl. J. W. Afric. Inst. for Oil Palm Res. 4,
156-175 (1963).
13. Renard, J.-L.: Incidence de la culture du palmier it huile sur les populations des Fusarium dans
les sols de savane en basse Cote d'Ivoire. Revue de Mycologie 32, 3,211-227.
14. Renard, J.-L., Gascon, J.-P. and Bachy, A.: Recherches sur la fusariose du palmier it huile,
Oleagineux, 581-591 (1972).
15. Roll-Hansen, J.: Fertilizer experiments with carrots on peat soil. Forskning og Forsk i Landbruket. Sta. Exp. Stn. Kvithamar, Norway 25,201-218 (1974).
16. Stetter, S.: Effect of N, P and K fertilizers on foot rot diseases in continuous cereal growing.
Tidsskr. PI. Av. 1, 75,274-277 (1971).
166
Influence of Nutrition and Fertilizer Use
on the Resistance of Forest Plants to Fungus Diseases
Dr. L. Dimitri, Forstdirektor, Hessische Forstliche Versuchsanstalt, In·stitut fUr Forstproduktion;
Hann. Miinden/Federal Republic of Germany
Summary
Several examples of the influence of nutrition and fertilizer use on the resistance of forest plants to
fungus diseases are presented. Results of research work undertaken on a broad international scale
demonstrate that plant production is more profitable when fertility is naturally high or when so.il
fertility is improved by the use of fertilizers; this is particularly true for long living species like forest
trees. The well planned and careful use of fertilizers increases growth and also, in many cases,
improves ecological resistance frequently eliminating or at least reducing the cost of technical or
chemical control. Inappropriate use of fertilizers, however, may not only lead to financial loss but
also increase o.ur trees' susceptibility to infection.
.
The influence of nutrition on leaf diseases is exemplified by reference to Marssonina, Melampsora
and Pollacia spp. on poplar, Microsphaera alphitoides on oak and Lophodermium pinastri on Pinus
silvestris. The influence on stem diseases is discussed with reference to damage caused by Fomes
annosus on Norway spruce. Important connections between soil conditions, fertilizer use and the
protective influence of mycorrhiza are also discussed.
The influence of specific macro- and micro-nutrients on host resistance to pathogens can only be
assessed by working with genetically uniform material under comparable conditions and ~ith defined pathogens. Broad interdisciplinary co-operation is essential for such research, since very complex biological, pathological, genetic and biochemical problems have to be dealt with.
Resume
L'auteur presente plusieurs exemples de l'influence de la nutrition et de l'application des engrais sur
la resistance des plantes forestieres envers les maladies cryptogamiques. Les resultats de recherches
effectuees a l'echelle internationale montrent que la production vegetale est abondante lorsque la
fertilite naturelle du sol est elevee ou lorsqu'elle est amelioree par l'application d'engrais. L'emploi
judicieux des engrais intensifie la croissance et, dans beaucoup de cas, ameliore la resistance ecologique, permettant ainsi de rectuire les coUts ·de la lutte technique ou chimique contre les parasites.
Cependant !'emploi inadequat des engrais ne peut pas seulement conduire a des pertes financieres,
mais egalement augmenter la sensibilite aux infections des arbres forestiers.
L'influence des elements nutritifs principaux et secondaires sur la resistance de I'hote envers les
pathogenes ne peut etre determinee que si I'on travaille avec du materiel, qui - sous conditions
egales - est genetiquement uniforme et avec des pathogenes bien definis. Pour un tel travail de
recherche une large cooperation interdisciplinaire est essentielle, puisque des problemes tres com~
plexes de nature biologique, pathologique et biochimique sont impliques.
L'influence de la nutrition sur les maladies des feuilles est decrite en se basant sur Marssonina,
Melampsora et Pollacia spp. chez le peuplier, Micrasphaera alphitaides chez le chene et Laphadermium pinastri chez Pinus silvestris. L'influence sur les maladies des tiges est discutee en se rHerant
aux degats provoques par Fomes annasus chez le pin de Norvege. On discute egalement des relations
importantes entres les conditions de sol, la fertilisation et I'effet protecteur des mycorrhizes.
]67
1. Introduction
The quantitative and qualitative performance of plants is determined both by genetic
factors and by the environment. These factors are equally relevant for the development
of diseases and they may modify both host reaction and behaviour of the pathogen.
It is not easy to investigate these factors, since they influence two living organisms host and pathogen -, but not always in the same direction.
It is necessary to distinguish clearly between (1.) resistance caused by genetic codes
and (2.) the apparent resistance which is modified by the environment (so called
'ecological resistance', BjOrkman [6]), although it is not always possible to distinguish these two factors under field conditions.
The influence of specific macro- or micro-nutrients is of varying importance not only
for growth but also in resistance of plants to pathogens and adverse environmental
factors: the content of one nutrient - e. g. potassium - may increase significantly
resistance of the plants against one disease but reduce it against another one.
Sites naturally well supplied with nutrients or where nutrition has been improved may
show varying influence not only on tree species (interspecific influence) but also on
different provenances or clones within one species (intra-specific influence). From the
numerous cases of inter-relationship some problems referring to nutrition and
resistance of forest trees against fungus diseases will be selected for discussion.
Both, the parasitic and the saprophytic relationship between pathogen and host are
characterised by the exchange of chemical substances. For biotrophic and necrotrophic
parasites (Giiumann [20]) the host plant may have a potential for defence by mobilising biochemical resistance factors within the living cell. Whether and to what extent
the host plant can utilize these possibilities depends to a considerable extent on its
nutritional state. It is not only the absolute amounts of nutrients but also the relationship between the individual nutrients which is important for both saprophytes and
parasites.
During their long production period forest trees are often exposed to extreme stress by
biotic and abiotic factors. It is therefore necessary to investigate in this context all
forms of resistance, such as infection resistance; resistance against spreading; active
and passive resistance; apparent and phased resistance. It is equally important to
expand measures which might increase resistance and to diminish all those which
might reduce it.
Improvement of nutrient supply does not have only a direct influence on the plant
but the growth and resistance of trees is also influenced by its favouring the activity of
micro-organism and mycorrhizal fungi.
There is a considerable international literature on the various aspects of this complex
problem. Because of the limited space available the discussion is confined to some consideration of the influence of nutrition on the organs of assimilation on stem and root
rot and of its importance for development of mycorrhiza.
2. Nutrition and disease resistance of plant organs
2.1. Foliation
Morphological structure and chemical composition of the superficial cell layers or the
cells of leaves and needles may play an important role in infection resistance. For
instance, species specific waxes of the cuticle may influence significantly the infection
by fungi, because the waxes contain components which may favour or stop growth of
168
-
the mycelium (Schutt [45, 46]). So far we have, however, insufficient information
on the influence of ecological factors on the amount and composition of these waxes.
More information is available on the relation between nutrient content of the soil and
that of the organs of assimilation on the one hand and the nutrient content of leaves
or needles and their resistance 'against pathogens on the other hand.
These ·aspects have been most thoroughly investigated for poplars among the broadleaved trees and for pine, Douglas fir and others among the conifers.
Van der Meiden [35] showed that the severity of attack by Melampsora diminished as
the K content of poplar leaves increased.
'
'
Content of K
in % of
dry weight leaf
0,9
1,0
1,3
Melampsora attack
on leaves
heavy
medium
weak
The same relationship could be demonstrated by Kolster and van der Meiden [28]. for
Marssonina attack of poplar leaves. Gargave and Pinon observed only a weak attack on
the leaves of the quick growing poplar clone I 214 by Marsonina [19] if nutrition was
well balanced and sufficient.
Lack of one anion (N0 3 , H zP0 4, S04) caused severe damage. Leaves insufficiently
supplied with Ca or Mn showed not only chlorotic discoloration but were also more
susceptible to attack by this parasite.
Suzuki [55] and Suzuki and Chiba [56] investigated the behaviour of clones of several
poplar hybrids in solution culture comparing well balanced complete nutrient solution
with solutions deficient in N, P or K. They showed that there is distinct differentiation
between the influence of specific nutrients on the resistance of poplar leaves against
'Melampsora larici-populina. Plants of the same clone showed a higher resistance
against this rust fungus if they had been grown in a solution short of Nand P. The
reduced sugar content of the leaves due to shortage of these elements is considered to
be an important factor of this type of resistance. The seasonal pattern of resist.ance
also shows a good correlation with the content of glucose and sucrose of the leaves.
However, there was a remarkable reduction in resistance against infection by plants of
the same clone, if K was in short supply. A distinct reduction of the attack by Microsphaera alphitoides was found for leaves with increased K contc::nt foilowing application
of potassium fertilizers (Penningsfeld [38]).
When investigating the resistance of specific clones and sibs of poplars of the section
Leuce against Pollacia radiosa Weisgerber [58] could distinguish two distinctly different
groups:
- group a: clones or sibs showing the same reaction at all test sites (i.e. they are either
resistant or not)
- group b: performance of resistance of the clones or sibs varies considerably according to sites
After seven years of observation it can be assumed that for plants of group 'a' genetic
control of resistance is so strong that it cannot be modified by site influences; For
plants of group 'b' such strong fixation does not apparently exist. The results of such
research give most valuable hints for resistance breeding.
The needle cast caused by Lophodermium pinastri can be considered as the most im169
partant disease of the widespread pine species, in particular of Pinus silvestris. Due to
the great economic importance and the remarkable damage caused to this species by
this fungus intensive research has been undertaken to measure the genetically fixed
resistance, to improve growing conditions by soil improvement and to reduce losses
by using fungicides. SchUtt [44] was able to show that there were considerable
differences with respect to growth in height, intensity of attack and the inter-relation
between these two factors for 20 provenances of Scots Pine planted on ten test sites in
the Federal Republic of Germany and West Berlin.
Rack [40] found no increase in resistance against infection and spreading in a trial on
nutrient shortage subsequent to fertilization, but damage by needle cast was less in the
fertilized plots due to increased growth. A clear relationship between nutritional state
and attack by Lophodermium was found by Zottl and Jung [61]: The relative attack
for Scotch pine plants on plots fertilized with N, P, K and Mg was only half of that of
plants on plots without fertilization. But trace nutrients may also have some influence.
lyer, Schulte and Randall [25) suppose that this might be the reason for the better
resistance against needle cast of Pinus banksiana compared with that of Pinus resinosa
because the needles of 2-year old plants of the first species had twice the Mn and Al
content than those of the second species.
2.2. Stem damage
The bole of a tree represents the major part of its volume and value. It is, therefore, the
objective of fertilization to increase this part of volume and value. Damage of the bole
caused by external wounds and/or stem rot developing from root rot reduce the
financial return and diminish stand stability. Genetic control and ecological resistance
are of great importance in this context. The ecological resistance of host plants against
the cosmopolitan pathogen Fomes annosus has been subject to comprehensive investigations, while so far little is known about the genetic resistance of host plants. Emphasis
of worldwide research has been laid on this optional biotrophic parasite because:
1. Many tree species - in particular the economically important conifers of the
Northern hemisphere - are attacked.
2. As well as the financial losses caused by this pathogen stand stability is severely
endangered.
The results of detailed research work undertaken in Southern (Rohmeder [42]) and
Northern Oermany (Zycha and Kata [62)) are summarized by Laatsch [32] as
follows:
a) lateral root systems and periodical drying up of the soil,
b) surface soils with high content of carbonat in the surface layers or additional lateral
supply of water rich in bicarbonats,
c) soils rich in nitrogen (afforestation of agricultural lands, basalt weathering loams)
and
d) the combination of the above mentioned characteristics causes a reduction of the
resistance of Norway spruce against this pathogen, because damage is highest
where these conditions occur. Rishbeth [41] on the other hand explains the higher
infection of pine on calcareous soils by the absence of Trichoderma viride, a fungus
which exerts a strongly antagonistic influence on Fomes annosus.
Based on detailed investigations Seibt j 48] found no direct increase in infection by
Fomes annosus after normal fertilization.
170
/
I'
Site improvement of Norway spruce stands with lime fertilizer and partial tillage:"- both
measures which contribute to the mobilisation, of the nutrients stored in the raw humusdid not increase damage by Fomes annosus of almost 29000 trees (Kramer [29, 30})
within 10 years of observation. However, spreading of the fungus within the trees was
apparently promoted by the increased and irregular growtJ.1 following site improvement.
Rohmeder [42} and Pechman et al. [37} had already stressed that different factors are
concerned in the infection of trees and the spreading of the fungus within the tree.
Normally infection rises with increasing pH-value ( Holmsgaard et al. [22), Evers [ 13}).
Infection by Fomes annosus decreases with increasing content of K, Mn a1)d Mg of the
uppermost soil layer.
The significantly higher infection of Norway spruce by Fomes annosus on sites with
high supply of carbonate and nitrogen may be only partially attributed to the direct
influence of these nutrients. It is apparently far more significant that on these sites the
supply of K, Mn, Fe (Laatsch et al. [33), Baule [5]) as well as P and other important
nutrients is hampered (Jung and Riehle [26}).
It has been proved several times that the content of macro- and micro nutrients in the
wood has an important influence on disintegration of the wood and spreading of the
fungus as well as on the growth of Fomes annosus in living trees. Disintegration of
wood of Norway spruce rich in Mn is quicker than that with a low content of Mn
(Courtois and Braun [9}). Pobegailo et al. [39} also showed that there is a relationship
between trace elements - in particular Mn content of the soil and that of pine needles
and the intensity of infection.
Fomes annosus infection was remarkably reduced by application of a high rate of sulphur dust on the heavily infested stands of Pinus elliottii and Pinus taeda in Mississippi.
The treatment also resulted in a long lasting reduction of the pH-value and promoted
the activity of soil microorganisms. Application of the same amount (2000 Ib/acre) of
NH4NO r fertilizer at the same time did not show any significant results (Froelich and
Nicholson [l6}).
The investigations referred to so far have been undertaken on different sites with
different populations. Dimitri [11} investigated resistance to spread of the fungus in
various clones of Norway spruce on a comparable site and Aquinagalde and Cerny [1}
determined the chemical characteristics of the wood of these clones. These investigations show that for clones with a limited infection and higher phenotypic resistance the
wood contains less N but significantly more substances soluble in petroleum ether than
that of clones which are infected more severely.
Norway spruce provenances have been planted in -a provenance trial on six different
locations with three replications of 100 trees per plot each. At the age of 16 years
30 trees per plot were inoculated both during and outside the vegetation period with
the same very active strain of Fomes annosus. Success of infection as well as average
spreading of the mycelium in the trees (i. e. the phenotypic infection and spreading
resistance) was much lower for trees of the same provenance growing on sites of group I
than for those growing on sites of group H. The pH-values and some other characteristic data for nutrients of these two site groups are listed below:
pH
Site group I
Site group H
4.1
4.1
N
%
0.06
0.16
C
%
0.7
2.2
C:N·
11
13
Ca
mg
4.3
7.1
PzOs
mg
3.7
5.3
KzO
mg
3.0
2.7
Mg
mg
3.0
6.7
171
The adverse reaction, i. e. the influence of a severe Fomes annosus infection on the
nutritional status of older Norway spruce trees has also been investigated. Sinner and
Rehfuess [51] showed that rotten trees with partially damaged root system, sapwood,
cambium and phloem had significantly lighter needles with lower content of K and N
but higher content of P than, their healthy neighbouring trees. A considerable modification of the physiological status of trees after attack by Armillaria mellea (Singh and
Bhure [50]) has also been observed. The needles of the infested trees showed reduced
content of most of the macro-nutrients (N, P, K, Mg and Na) and an increase of Ca
and the three micro-nutrients Mn, Fe and Zn.
The most important stem disease of Pinus elliottii and P. taeda is fusiform rust which
is caused by Cronartium fusiforme. Infection increased for P. elliottii if before or during
the first three years after planting discing (N-mineralisation) was undertaken. Infection
was even higher if during the second vegetation period this operation was accompanied
by application of NPK (Dinus and Schmitling [J 2]). For several years seedlings of
P. elliottii were artificially inoculated with basidio-spores of C. fusiforme (Schmidt
et al. [43]).
The results of these investigations underline the hypothesis that increased rust infection
is probably combined with too intensive stimulation of growth of the host plant.
Higher P content promoted rust infection more than growth. However, the comprehensive fertilization trials with Nand P undertaken by Hollis et al. [23] in the
Southern United States showed no reliable relationships between fertilization, growth
and fusiform rust within an observation period of five years. They suggest, therefore,
that fertilization can improve tree growth without necessarily increasing rust incidence.
The results of research undertaken by Breuel [8] indicate that improvement of the
upper soil layers by tillage and NPKCaMg fertilization significantly reduce bark
necrosis of poplars of section Aigeiros Duby caused by Dothichiza populea.
2.3. Root damage and the importance of mycorrhiza
The composition of the flora of micro- and macro-mycetes as well as the occurrence of
mycorrhizal fungi differs considerably between the various site groups (Haas [21]
and literature cited).
The occurrence of viable spores of Fomes annosus in the litter, humous upper soil and
deeper soil layers (shell-lime stone, sandstone weathering soils) is in all cases sufficient
for a primary (though varying) infection (Siepmann [49]). However, conditions for
survival of the spores differ very much with the soil type (Kuhlman [31]). According
to the research carried out by Zycha and Kliefoth [63] germination, and thus suryival
of spores is strongly influenced by soil physical and chemical properties: in some soils
spores perish because they germinate quickly, whereas in other soils they remain
virulent for long periods and germinate only when a potential infection site discharges
substances which favour germination.
Occurrence and importance of fungi which live symbioticaJly with more highly
developed plants (mycorrhiza) and so influence growth and resistance is judged
differently in the literature. In general fertilization is supposed to have a positive effect
on development of mycorrhiza (Linnemann [35], Weissen and Manil [59]). Application of P-fertilizers seems to give better results than that of N-fertilizers (Koberg [27],
Skimer and Bowen [52]). After evaluating occurrence of mycorrhiza in ten tree species
in eleven forest types of Czechoslovakia Sobotka [53] came to the conclusion that the
172
intensity of mycorrhiza does not depend directly on the content of N, P or K or on
pH-value or biological activity in the soil. On sites with good a supply of water and
nutrients trees are apparently less disposed for and dependent on mycorrhiza than they
are on poorer sites. Liming caused a remarkable change in the composition of basidiomycetes and a strong reduction of mycorrhiza. However, this did not lead to
decreasing increment of Norway spruce trees (Fiedler and Hunger [14J).
The importance of mycorrhizal fungi for infection resistance seems to be clear and
significant for young trees. Stack and Sinclair [54J proved that the mycorrhiza fungus
Luccaria laccata considerably reduced the infection of Douglas· fir seedlings by
Fusarium oxyosporum:
- infestation without L. laccata
- infestation with L. laccata
53%
15%
It is equally important that the protective influence of L. laccata had already begun
before development of mycorrhiza. According to the research work of Hiippel [24J
Boletus bovinus does not provide complete protection of seedlings of Norway spruce
and Scotch pine against Fomes annosus, but may in many cases prevent entrance of the
pathogen. According to Azevedo [4J older and healthy stands of Pinus pinaster are
characterized by abundance of various mycorrhiza fungi, whereas in stands with
damage by Fomes annosus only few of these fungi were found. This protective influence is not a direct result of mycorrhiza - as Meyer [6J and others assume - because
(1.) the infection of older trees with Fomes annosus does not occur at the thin points of
the roots but in other regions (Dimitri [10 J) and (2.) highly aggressive parasites - e. g.
Armillaria me/lea can infect the host through the mycelial strands of the mycorrhiza
fungi (Gandray [18 J). The often demonstrated strongly proved strong antagonistic
influence of the mycelium of the mycorrhiza fungi living in the soil seems to be far
more important in this context.
Given soil conditions or their improvement by fertilization do not only influence the
desired species composition and antagonistic effect of the microorganisms of the soil,
but also signifies a considerable promotion of the resistance of the host plant. If healthy
roots can be infected through undamaged or only slightiy damaged bark, the chemical
composition of the periderm and the inner bark and phloem must have great importance for infection resistance. Starting from this hypothesis Laatsch et al. [33J assumed
that (1.) the value and quantitative ratio of specific components and (2.) the production
of inhibitory substances in the bark must depend on the nutritional state of the tree.
Production and enrichment of these irihibitory substances produced from carbohydrates in the secondary metabolism (polyhydroxyphenols and their glycosides) is
probably small if HP, N, K or Mn are short and N is very abundant.
This hypothesis is supported by Wenzel and Diaz-Palacio [60J in so far as with
disturbed waterbalance (1.) smaller needles of Norway spruce, (2.) lower content of. K
combined with higher content of Ca and Mg, (3.) falling concentration of inhibitory
substances in the phloem and (4.) reduction of the fungistatic effect of the phloem flow
have been observed. It is supposed that during periods of insufficient water supply
infection of Norway spruce with Fomes annosus is easier as a result of reduced concentration of fungicidal substances in the phloem. The latest results of research work
undertaken by Alcubilla and Rehfliess [2J showed that the nutritional state of Norway
spruce sample trees can be characterized by determination of the macro-nutrient
content (N, P, K, Ca and Mg) of phloem samples taken at the butt of a tree. Detailed
173
phloem analysis may serve not only as a diagnostic method for the nutrient state but
also provide important parameters for assessing the disposition of Norway spruce
against infections.
Fertilization of a 26-year old Douglas fir stand attacked by Poria weirii with urea
[CO(NH2)2]' NH 4N0 3 , Ca(N0 3h and NaN0 3 did not result in a reduction of the
spreading of the infestation or in reduced mortality (Wallis and Reynolds [57]).
3. Conclusions
As in human or veterinary medicine insufficient or over-abundant nutrition of forest
plants often leads to disease. Arbitrary fertilizer dressings often applied without prior
soil or needle analysis, may have more negative than positive results. But there is
impressive evidence that stand improvement and fertilizer applications according to
site, tree species and stand age contribute to increasing the ecological resistance.
Examples may be taken from reference literature, such as Baule and Fricker [6],
Schwerdt/eger [47], Fiedler, Nebe, Hoffmann [15] and others.
If we wish to draw conclusions from the observations so far available on the relation
between the nutrient status of forest sites and the reaction of tree species to various
pathogens it must always be remembered that we are dealing here with a very complex
subject. No clear and valid deductions can be derived from such results with respect to
the genetically determined 'species related' resistance, nor to the modification of
disease resistance by the environment. The reason is that we still know too little about
the influence of site conditions and fertilizers on the morphological, physiological and
biochemical properties of trees and how they affect the various pathogens which attack
various organs of the tree.
These uncertainties may explain the fact that identical fertilizer treatment of the same
tree species may have very different results on different sites.
Clear elucidation of these interactions can only be obtained by well planned experiments using genetically uniform host material and clearly defined pathogens executed
under comparable environmental conditions. There is a need for intensified research on
forest trees and this should involve the maximum interdisciplinary and international
co-operation.
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174
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175
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44. Schiitt, P.: Der Schilttebefall der Kiefer in Abhiingigkeit von Herkunft und Anbauort. Forstwiss.
CbI. 83, Jg. H. 5/6, 140-163 (1964).
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(1971).
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Stammholz. Forstwiss. CbI. 83, 101-118 (1964).
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176
The Effect of Varying K Level on Yield Components
and Susceptibility of Young Wheat Plants to Attack by
Puccinia striiformis West
J. Kovanci and H.C;olakoglu, Plant Nutrition Department, Faculty of Agriculture, Aegean University,
Izmir/Turkey
Summary
Preliminary results are given from an experiment investigating the effect of varying·potassium.level
(0.2 to 1.2 mM K/l) on two wheat cultivars grown in water culture. At the beginning of the generative
phase of growth, increasing K increased growth (dry matter production of both shoot and root),
reduced the transpiration coefficient, increased plant height and reduced susceptibility to disease
attack.
Resume
Les auteurs donnent les n\sultats preliminaires d'un essai qui avait pour but d'etudier I'effet de
niveaux variables de potassium sur deux varietes de ble cultivees en solution nutritive. Au debut de
la phase generatrice de la croissance, les niveaux croissants de K augmenterent la croissance. (production de matiere seche dans les pousses et les racines) diminuerent le coefficient de transpiration
augmentere·nt la taille des plantes et diminuerent la sensibilite aux attaques par les maladies.
1. Introduction
Potassium is a major plant nutrient and, when applied with other elements in balanced
fertilizer, increases the yield of crops significantly. Balanced nutrition prevents physiological disorders and improves resistance to disease. Several investigators have reported
that potassium plays an important role in carbohydrate metabolism and indirectly
affects the thickness of the cell wall, reducing infection by both obligate and facultative
parasites, e.g. Glynne [5], Last [11], Mengel [14], Trolldenier [21], Pissarek and
Fink [17], Mengel and Haeder [15] and Smiley et al. [18]. High disease damage to
wheat has been reported in the Aegean region (Karaca [8] and Kaat [9]). The purpose
of the experiment here described was to find out the effect of potassium nutrition on
the occurrence and severity of Stripe Rust (Puccinia striijormis West) on wheat grown
in solution culture.
177
2. Material and Methods
Two wheat cultivars, both highly susceptible to stripe rust were selected: a Mexican
wheat (Super-X) and a local cultivar (Cumhuriyet-75). The plants were established in
quartz sand and, after two weeks, transplanted to water culture supplying three levels
of potassium: K 1 0.2 mM, Kz, 0.4 mM and K 3 , 1.2 mM K/l, as KCI. Plastic pots,
capacity 17.1 litre were used, each containing] 9 plants (0.9 liter per plant). The pots
were aerated twice daily and pH and K concentration were controlled weekly, being
kept approximately constant throughout the growing period. A few days after the
completion of tillering the plants were inoculated with stripe rust by the pulverization
method. Further details of the procedure are summarised below:
Macronutrients (10-3 MfI): 2 Ca(N0 3)z, 2 NH 4N0 3 , 0.5 NaH 3P0 4 , 3 CaCl z, 2 MgS0 4 ,
and 0.2, 0.4, 1.2 KCI.
Micronutrients: (10-6 M/I): 20 Fe (chelate), 14 MnS0 4 ]0 H 3B03 , ].4 CuS0 4 ,
].5 ZnS04 , 0.3 NH4 molybdate and 0.2 Co(N0 3)z'
Sowing date 6.2.76, Transplanted 22.2.76, Inoculated 24.3.76 (after tillering). First
harvest 20.4.76 (beginning of generative phase, ]st replication only harvested). Second
and third harvests will be taken at the milk ripe and fully ripe stages respectively. There
were 6 replications.
At harvest, the fresh weight of tops was recorded and dry weights (dried at 105 degrees
C.) of tops and roots were separately recorded. K, Ca and Na were determined in the
digests by flame photometer, Mg by atomic absorption and total N by Kjeldahl.
Water consumption was also measured. Disease severity, or susceptibility of the plants
to fungus, were recorded according to the Cobb scale (Lecberg [12]).
3. Results and Discussion
3.1 Influence of Potassium on yield components and water consumption
Increasing the potassium concentration in the nutrient solution increased all the
components of yield (Table ]).
Table 1. Yield components and water consumption of wheat.
Water
cons.
ml/pot
Trans.
coefft.
77
85
8500
10800
11200
341
302
286
58
66
71
9600
10 lOO
10500
443
377
302
K-Conc.
mM/I
Top
fresh w.
g/pot
dry w.
g/pot
Root
dryw.
g/pot
Top/Root
dryw.
g/pot
Number Plant
hight
of till/
pot
cm
Cum-75
0.2
0.4
1.2
166
232
300
23.9
34.6
36.7
1.0 I
1.16
2.44
24.91
35.76
39.14
38
41
47
Sup-x
0.2
0.4
1.2
140
160
234
21.2
26.0
32.0
0.48
0.77
2.76
21.68
26.77
34.76
32
36
44
Cultivars
• average of 5 plants/pot
]78
72·
Similar results showing a marked effect of potassium on growth in water culture have
been obtained with oats and barley by Mengel and Forster [16], Mengel and Haeder
[15] and Baier and Smetankova [3] and with other species by Asher and Ozanne [2]
in sand culture, Mac/eod [13], Forster and Mengel [4], Steineck [2] and Wiechens
[23] in water culture, pot and field experiments.
Water consumption was increased by increasing K but the transpiration coefficient
was decreased due to the increase in dry matter yield, thus a high K level improved the
efficiency of water utilization. Several investigations - Kilhn and Linser [10], Ho!ner
[6], Amberger [1], Humble and Hsiao [7] - have shown that under normal growth
conditions K plays an important role in t/1e regulation of osmotic pressure in the plant
and that its higher concentration in the guard cells is responsible for the opening and
closing of the stomata (Trolldenier [22]).
3.2 The effect of potassium level on K uptake, K content and its relation to disease
resistance in wheat
Increasing the K levels from 0.2 to 1.2 mM/l in nutrient solution, increased the
K-uptake from 329 to 1385 mg/pot for Cumhuriyet-75 and from 272 to 1238 mg/pot
for Supper-x and K-content was also increased in both cultivars (from 1.18% to
3A3% for Cumhuriyet-75 and from 1.22% to 3.54% for Super-x. It is obvious from
Table 2 and Figure 1 that especially the highest K level has increased the K-uptake and
due to that, K-content was also positively increased in both cultivars.
Fig.i. Effect of different potassium levels on yield and K-uptake of wheat.
1'00
1300
/
/
1200
40
11 00
.-
"0
.e'"
.
."/
"0
~
...................
.-/'
0-
/
./."/
o
~
>0
/
-/'
• 32
o
/,/'
.'/
.',/
36
.'./
28
•/
".
."/
24
/
--
--
900 1)
o
800 ;..
2
700
,/
600
./
//
/
/
......
500
Dry W.
o-----t
." ., K-Uplake
,-"i
1000 '"
E
/
Cumhuriyet- 75
:/ /
~
.
a.
::>
~
-;;
400 ~
300
1/
I
_ _ ---4
Dry W.
0-'''''
K-Uptake
200
SUptr- x
100
20
t'
o
0.2
0.4
0.6
0.8
1.0
1.2
K -Concentration (m Val/Il
179
Table 2. Effect of different K concentrations on K-uptake, K-content and susceptihility to fungus.
K-conc.
mM/l
K-uptake mg/pot
Top
Root
Top+ Root
%KD.M.
Top
Root
Degree of suscep.
to fungus
Cumhur.-75
0.2
0.4
1.2
283
557
1258
47
56
127
329
613
1385
1.18
1.61
3.43
4.62
4.81
5.27
70-S
50-S
4Q-S
Super-x
0.2
0.4
1.2
259
529
1133
13
24
105
272
552
1238
1.22
2.03
3.54
2.83
3.15
3.54
90-S
7Q-S
50-S
Cultivars
Fig. 2. Relationship between K content and fungus effect on wheat.
100
3.6
90
3.0
80
2.
70.
Q.
e 2.2
60 i"
.
~
0:
E
8
--.--.
~ 1.8
"
'" "
"
~
so ~
'"
,
.............
40
K '/,
cumhuriftt - 75
5 U set p.
K '/,
5Uptr_X
sUSCtp.
I.()
0.2
0..4
0..6 .
0.8
K_concrntrQtion(m val/l)
(100:indicQtts
the
30
1.0
highest susctpt ibility
12
to
disease)
It is clear from the first results obtained in this investigation that, at the onset of the
generative stage of development in the wheat plant, increasing potassium has decreased
the severity of fungal attack. It is suggested that this may have been due to an increase
in cell wall thickness brought about by improved potassium supply which would
decrease the penetration by the fungus. This is suggested by other workers' results
(Trolldenier [21], Smiley et al. [i8) and Fink [17}).
180
References
1. Amberger, A.: Funktionen des Kalis in der Pflanze. Kalibriefe 10, Fachgeb.2, I.Folge 1-6
(1968).
2. Asher, C.J. and Ozanne, P.G.: Growth and potassium content of plants in solution cultures
maintained at constant potassium concentrations. Soil Sci. 103, 155-161 (1967).
3. Baier, J. and Smetimkova, M.: Potassium and yield components. Potassium research and agricultural production. 10th Colloquium of the IPI. 131-140 (1974).
4. Forster, H. and Mengel, K: Einflilsse der Kaliumernahrung auf die Ertragsbildung verschiedener Sommerweizensorten (Triticum aestivum L.). Z. Acker und Pflanzenbau 139, 146-156
(1974).
5. Glynne, M.D.: Effect of potash on powdery mildew in wheat. PI. Path. 8,15-16 (1959).
6. Ho/ner, W.: Influence of potassium on water economy. Potassium in biochemistry and physiology. 8th Colloquium of the IPI. 125-129 (1976).
7. Humble, G.D. and Hsiao, T. c.: Specific requirement of potassium for light-activated opening
of stomata in epidermal strips. Plant PhysioI. 44, 230-234 (1969).
8. Kaat, H.: Yurdumuzda hastalik, zarar.li ve yabanci otlarm killtilr bitkilerinde olusturdugu zarar
dereceleri ilzennde Incelemeler. (1975) (unpublished).
9. Karaca, f.: Sistematik bitkihastaliklan. Cilt 2, 1-180, E. O. matbaasi-Izmir.
10. Kiihn, H. and Linser, H.: Beziehungen zwischen Kaliumernahrung, Wasserversorgung und
Chlorcholinchlorid (CCC)-Wirkung bei Sommerweizen. Kalibtiefe 8, Fachgeb.2, I.Folge, 1-10
(1966).
11. Last, F. T.: Effects of nutrition on the incidence of barley powdery mildew. PI. Path. 11, 133-135
(1962).
12. Lecberg, E. L.: Methodology for disease measurement related to assessment oflosses, Background
papers prepared for FAO symposium on crop losses, Rome, 11-43 (1967).
13. Mac/eod, L. B.: Effects of N, P and K and their interactions on the yield and kernel weight of _
badey in hydroponic culture. Agron. Journal 61, 26-29 (1969).
14. Mengel, K: Ernahrung und Stoffwechsel der Pflanze. VEB Gustav Fischer Verlag Jena, 1-322
(1961).
15. Mengel, K and Haeder, H.E.: Photosynthese und Assimilattransport bei Weizen wahrend der
Kornausbildung bei unterschiedlicher Kaliumernahrung. Z. Acker und Pflanzenbau 140,
206-213 (1974).
16. Mengel, K and Forster, H.: Der Einfluss der K-Konzentration der Nahrlosung auf die Ertrags·
bildung, die Qualitat und den K-Aufnahmeverlauf bei Hafer. Plant and Soil 35, 65-75 (1970.
17. Pissarek, H.P. and Fink, A.: Untersuchungen zur anatomisch'-mikroskopischen Diagnose des
latenten Kaliummangels. Landw. Forsch. 27/1,241-248 (1972).
18. Smiley,R. W., Cook, R.J. and Papendick, R.f.: Fusarium root rot of wheat and peas as influenced by soil applications of anhydrous ammonia and ammonia-potassium azide solution.
Phytopathology 62, 86-91 (1972).
19. Stanchev, L., Lebenson, R. and Bobochevska, D.: Agtochemie 1-421 (1971), Plowdiv.
20. Steineck, 0.: The relation between potassium and nitrogen in the production of plant material
Potassium research and agricultural production. 10th Colloquium oOPI 159-166 (1974).
21. Trolldenier, G.: Getreidekrankheiten und Pflanzenernahrung. Kalibriefe, Fachgebiet 11,
2.Folge.
22. Trolldenier, G.: Recent aspects of the influence of potassium on stomatal opening and closing.
Potassium in biochemistry arid physiology. 8th Colloquium of the IPI, 130-133 (1971).
23. Wiechens, B.: Die Bedeutungder K-Dynamik der Keuperboden flir die Ertragsbildung. (1975).
Dissertation.
181
Contribution to the Discussion on the Effects of Fertilizers on the Infection
of the Roots of Crops by Fungi
Dr. G. W. Cooke, e.B.E., F.R.I.e., F.R.S., Chief Scientific Officer, Agricultural Research Council,
London/United Kingdom; member of the Scientific Board of JP!
Most practical advances in agriculture in developed countries are now made as a
result of multidisciplinary work involving specialists in different disciplines. This
meeting is important because it has brought together specialists in crop nutrition and
those concerned with pests and diseases of crops. Increased yields are often the result
of interactions between two or more factors which affect the growth of crops. It is
important to know how the interactions between fertilizers and factors causing plant
disease arise. We must ask whether larger yields are simply the result of the greater
capacity of a well-fertilized plant to grow, or whether the fertilizers have an effect on
the level of infection. Evidence on these questions has been provided by the long
term experiments at Rothamsted.
It has been observed for many years that soil-borne diseases, and pests (such as wheat
bulb fly), had their most serious effects on yields of cereals on plots where too little
fertilizer was applied. Special experiments were started to investigate the problem and
detailed investigations were also made by plant pathologists on the crops grown on
the 'classical' Experiments-Broadbalk Wheat (started 1843) and Hoosfield Barley
(started 1852). The results given below are mainly the result of work initiated by my
colleagues Mr. D. B. Slope (plant pathologist) and Dr. G. E. G. Mattingly (soil chemist),
but other Rothamsted workers have also contributed; important references are given
at the end of this note.
.
Effect of fertilizers on infection of cereals by
take-all fungus in the Rothamsted experiments
Effect of phosphate
The effect of phosphate fertilizer was investigated in an experiment which began in
1967/68 where. barley was grown and treated with several amounts of phosphate
Table 1. Yields of barley and rating for infection by take-all as affected by phosphate fertilizer.
(West Barnfield Experiment, Rothamsted)
P applied
each year
kg P/ha
o
16
64
Take-all
rating
Yield of grain
t/ha
1968
1971
1968
1971
3
1
1
122
70
40
3.8
4.4
4.1
3.7
4.9
5.6
Soluble soil P
(in 0.1 MNaHC0 3 )
mg/kg
6
10
34
183
(the work was begun by Messrs Slope and Maffingly). Some results are given in
Table 1 for yields and infection of the roots by take-all fungus (Gaeumannomyces
graminis). There was practically no take-all in the early years but the crop was seriously
infected by 1971. Yields were raised by phosphate fertilizer in all years but take-all
infection was diminished.
Winter-wheat was sown after six consecutive barley crops had been grown on this
experiment. It was seriously infected by take-all but the infection diminished with
increasing levels of phosphate, and yields increased. Some results from this wheat
crop are in Table 2.
Table 2. The effects of phosphate fertilizer on infection by take-all fungus in wheat grown after
6 barley crops on West Barnfield at Rothamsted
P applied
each year
kg P/ha
Percent of plants
infected by
take-all
73
16
69
58
o
64
Yield of
grain
t/ha
5.1
6.0
6.5
Further evidence on the effect of phosphate on take-all was provided by wheat grown
after barley in a long-term Rotation Experiment on phosphate made on Sawyers field
at Rothamsted. Some results are in Table 3.
Table 3. The effect of amount of phosphate fertilizer applied each year on infection by take-all of
wheat grown after barley in the Rotation experiment on Sawyers field
P applied
each year
kg P/ha
o
12
25
Percent of
plants infected
by take-all
90
14
15
Yield of
grain
tlha
4.8
7.5
7.0
Soil P soluble
in 0.1 MNaHC0 3
mg/kg
8
12
18
The results of this experiment on Sawyers field (Table 3) show well how infection by
the fungus is greatly lessened by increasing soluble soil phosphate as a result of
repeated dressings of P-fertilizer.
Effect of potassium
No large effects of potassium fertilizers on infection by take-all have been recorded.
Sometimes small interaction effects have been observed in the classical experiments at
Rothamsted. An example is in Table 4 which shows recent results with wheat on
Broadbalk.
Table 4. Effects of P and K fertilizers applied each year on the infection of wheat by take-all on
Broadbalk
All plots received a dressing of N fertilizer
Annual fertilizer
Percent of plants infected
with take-all
Nitrogen only
78
22
N+P
10
N+P+K
There was a large effect of P on infection and a further improvement when K was
applied as well as P.
184
Effect of nitrogen
Sometimes nitrogen fertilizers have a dramatic effect on infection by take-all fungus.
The example in Table 5 is from an examination of the roots of barley growing on the
Hoosfield Classical experiment at Rothamsted.
Table 5. Effects of nitrogen fertilizer on infection of barley by take-all fungus on Hoosfield at
Rothamsted
N applied each year
kg N/ha
o
48
96
144
Percent of plants infected
with take-all on plots having
PK fertilizer
53
26
4
3
Conclusions
The important conclusions from this work on long-term experiments at Rothamsted is
that phosphate fertilizer not only increases yields of cereal crops infected with take-all
fungus but it can also have very large effects on the amount of infection. In some experiments the wheat and barley grown continuously is severely infected when no P, or
small dressings only, are applied; with larger dressings of phosphate repeated each
year the roots of the plants have much less disease. A few examinations of infected
crops suggest that nitrogen may have similar large effects on level of infection.
Improvements in root health caused by potassium fertilizers are much less frequent
than gains from N arid P; where effects of K are recorded they are smaller and usually
occur only where P fertilizer is also applied. The long-term experiments at Rothamsted
provide· convincing evidence that root disease in cereals is diminished by phosphate
fertilizer. The work emphasises the practically important point that where wheat and
barley are grown continuously soil phosphate must be maintained at 'satisfactory'
levels to minimise the effects of soil-borne root diseases. .
The work done does not show how infection is diminished by increasing phosphate
in the soil. Understanding of the nature of the effects will probably have to wait for
developments in the biochemistry of the mechanism of fungal infections which will
be related to changes in the concentrations of ions in the cell contents which are
caused by fertilizers.
References
Rothamsted Experimental Station: Proceedings of Subject Day on Plant Diseases (1976).
Slope D.B., Broom E., Mattingly G.E.G. and Bolton J.: Effects of P and K fertilizers on root rots of
barley. Rep. Rothamsted Exp. Stn. for 1971, Part r, pp. 143-145 (1972).
Slope D.B., Broom E. and Mattingly G.E.G.: Effects of P and K fertilizers on root rots of barley.
Rep. Rothamsted Exp. Stn. for 1973, Part r, pp. 131-134 (1974).
Slope D.B, Prew R.D., Gutteridge R.T., and Mattingly, G.E.G.: Take-all and other root rots.
Rep. Rothamsted Exp. Stn. for 1974, Part r, pp. 223-227 (1975).
185
Contribution to the Discussion on Fungi
P. Martin-Prevel, Director of Research, Plant Physiology Department, Institut de Recherches sur les
Fruits et Agrumes (IRFA-GERDAT), Montpellier/France
At the risk of adding to the confusion resulting from so many contradictory results I
would lik~ to quote four observations on tropical plants.
(1) It seemed in yesterday's discussion that some of us could not 'see the wood for
the trees'. It may well be necessary to understand the effects of mineral elements
on amino-acids etc. but the lack of such complete understanding should not
prevent us from measuring global effects on growth and development of the plant.
These are essentially dynamic phenomena while the examination of metabolic
effects often results in a static view of things; and their measurement is very
simple. M. Lemaire was one of the few speakers who mentioned effects on the
development of plant organs. Here is another example from M. Muller of I.F.c.c.
(GERDAT/France) concerning coffee rust (Hemileia vastatrix) in Cameroun:
with a plentiful nitrogen supply, even if the disease is severe, the tree recovers
better, because the leaves are more numerous and larger.
(2) The utilisation of nutrients absorbed by the plant is important in these processes
and Dr. Jenkyn alluded to this. In Ivory Coast, P.Frossard inoculated bananas
with anthracnose in an experiment comparing different forms of nitrogen fertilizer
laid down by J. Gode/roy and J. Guillemot of f.R.F.A. (GERDATjFrance). He
showed that plants receiving urea were more susceptible to this disease of the fruit
than those receiving no nitrogen but less susceptible than those receiving nitrogen
as sulphate of ammonia. The leaves of the latter were inferior in growth to those
receiving urea and contained higher levels of nitrogen, as J. Marchal and I found:
thus they contained a higher proportion of unelaborated N in various forms which
unfortunately we were unable to investigate.
(3) In the case of Phytophthora of pineapples in Ivory Coast, P. Frossard and
J.J. Lacoeuilhe of I.R.F.A. obtained the following results with liming:
pH
:::; 4.5
4.9
5.7
::> 6.8
Plants killed by fungus
0%
6%
31%
36%
187
One might at first postulate an indirect effect of pH through influencing other soil
characteristics or nutrition. However, the treatment used to force flower initiation
involves introducing acetylene into the heart of the leaf rosette, the source being
calcium carbide. One of the effects of this treatment is to increase strongly the
penetration of Phytophthora into the leaves and this is definitely the effect of
calcium. Thus the effect referred to above is a direct effect of calcium.
(4) One region of Cameroun is particularly known for the severity of rice blast
(Piricularia oryzae) and this was generally thought to be due to climate. However,
Delassus and Seguy of f.R.A.T. (G.E.R.D.A.T./France) brought volcanic soil by
lorry from another area free from Piricularia and were able to grow healthy rice.
It should be noted that the fungus attacks the leaves, not the roots. Up to now,
numerous fertilizer experiments have not been able to show the cause of this
induced resistance and We should be very glad if anyone here could offer some
explanation.
188
Report of the Co-ordinator of the ·2nd Session
Prof. Dr. H.Laudelout, Departement Science du Sol,
Universite de Louvain, Louvain-la-Neuve/Belgium; member of the Scientific Board of IPI
During this session the complexity of the relationships between mineral fertilization
and the resistance of cultivated plants to fungal diseases has been thoroughly analyzed
despite the complexity of the subject. A number of examples has demonstrated the
foIIowing relationships: change in the mineral environment of the plant modifies its
physiology and, consequently, its resistance; at the same time, in the case of root
disease, the pathogenicity of the parasite is also changed. Again, changes in the metabolism of the soil caused by change in ionic environment have consequences such as:
increase in the biomass which in turn reacts back upon the ionic environment, enhanced
competition by one species or a group of species and a reduction in pathogen population or in sources of infection. The causes of these changes can be the results of quite
simple mechanisms like the toxicity of nitrite produced during the oxidation of
ammonia or of antibiotic processes. It is encouraging to find that such suggested
relationships are little by little being based less on pure speculation and more on
concrete observation. During the discussion some exceIIent examples of the relationship between mineral nutrition and disease incidence were given from observations
made at Rothamsted. The real problem is how to generalise from these results in such
a way that we can suggest appropriate practical measures. To do this we need suffi. ciently precise knowledge of the mechanisms involved in the effects of the factor
studied. This research into mechanisms can lead to fundamental considerations as
shown by one example from the discussion: the effect of liming or of potassium
fertilization on the resistance of a plant to two parasites will be conditioned by the
enzyme mechanisms involved in ceII wall attack.
It is clear that, as precise results are accumulated on the effects of various agronomic
techniques, the choice of the economically most favourable combination of treatments
will become more and more the business of the specialist: One of the communications
at this meeting gave an interesting example: given that the effect of nitrogen on
susceptibility of barley to disease varies according to variety, how do we choose the
best combination of variety, rate of nitrogen, time of application and fungicide treatment?
A good example of the fact that the combination of genetic improvement and the use
of fertilizers can lead to results of great practical importance was given by the experiments of IRHO in Ivory Coast. Using a resistant variety with appropriate potassium fertilization reduced the effects of fusarium wilt of oil palm almost to zero.
189
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3rd Session
Co-ordinator:
Fertilizer Use and Plant
Health: Bacteria and Virus
G. Drouineali, Conseiller scientifique, Institut
National de la Recherche Agronomique (lNRA),
Paris/France; member of the Scientific Board
of the International Potash Institute
Nutrition and Virus Diseases of Plants
CMartin, Head, Department of Plant Physiology, I.N.R.A., Dijon/France
Summary
The influence of mineral nutrition on virus diseases of plants has been relatively little studied. A
possible explanation of this state of affairs is that because these typical obligate parasites are almost
exclusively nucleo-proteic in nature, the great majority of workers have directed their studies to
examination of the relationships and competition between viruses on the one hand and the nucleic
acids and normal proteins of the host on the other. Virus biosynthesis depends upon substances
already synthesised by the healthy host cell using the enzymes of the host so that the important part
played by mineral nutrients in these normal processes becomes secondary in the study of the viral
infection in the true sense.
However, we shall see at the end of this study that plant health has an important influence on
appropriate fertilizer recommendations.
The following are discussed:
- The influence of nutrition on virus symptoms
- The influence of nutrition on the infective potential of viral particles and on the susceptibility to
virus of the host
- The influence of nutrition on virus multiplication
- The role of certain mineral elements in meristem culture, a valuable technique for the multipli.cation of virus free plants.
Resume
Le role de la nutrition minerale sur les maladies a virus des plantes a ete relativement peu etudie.
On peut peut-etre trouver une explication a cet etat de fait en rappelant que la nature presque toujours exclusivement nucleoproteique de ces parasites typiquement obligatoires, a conduit la grande
majorite des chercheurs a orienter leurs travaux vers l'etude des relations et de la competition entre
virus d'une part et acides nucleiques et proteines normales de l'hote d'autre part. La biosynthese
du virus se faisant aux depens de materiaux deja syntMtises par la cellule saine et grace il des enzymes
de l'hote, le role important des elements mineraux dans ces mecanismes normaux devenait secondaire
dans l'etude de l'infection virale proprement dite.
Cette etude revele la grande importance·de l'etat sanitaire de la plante pour l'elaboration des recommendations en matiere de fertilisation des vegetaux cultives.
Les points suivants sont abordes:
- .I'influence de la nutrition mr l'expression des symptomes du virus.
- .I'influence de la nutrition sur le pouvoir infectieux des particules virales et sur la sensibilite des
plantes aux virus.
- .I'influence de la nutrition sur la multiplication du virus.
- le role de certains elements mineraux sur la culture de meristemes, l'une des rares techniques de
guerison des plantes malades d'un virus.
193
1. Influence of nutrition on virus symptoms
The growth of plants is so dependent upon soil conditions that one may postulate,
without fear of contradiction, that these must have an important influence on virus
diseases (defining a diseased plant as one which shows symptoms); thus a number of
observations have been made which relate the severity of certain diseases to soil type
and nutritional status of the host plant.
The precise significance of such observations remains equivocal, however, because few
really searching experiments have been carried out and it is difficult to know whether
soil conditions have affected the appearance of symptoms or whether they have
actually affected the development of the pathogen itself. Host nutrition can modify the
plant's reaction to infection and its susceptibility to infection; but it also has effects in
the field by creating conditions more or less favourable to the vectors of the virus.
Brierly and Stuart [3], for example, found that by increasing the nitrogen dressing in
relation to other nutrients the susceptibility of onion to the virus yellow dwarf was
increased as was also the severity of the symptoms. Direct comparison of plants
showing symptoms at high and low levels of nitrogen suggested that nitrogen had a
greater effect than that of merely increasing susceptibility to infection; at low N levels
some of the infected plants exhibited no symptoms and were thus recorded as being
healthy. On the other hand susceptibility to infection may well not have been affected
by the nutritional conditions as much as the activity of the vectors; it must be true that
the larger the plant the greater the chances of its becoming infected and further, once
it is infected it is an abundant source of infection for other plants. The interaction of
these and other factors merits more study than it has received up to now.
Before studying the variables which play a part in the plant's reaction to virus it is
necessary to consider the importance of the physiological state of the plant at the time
it becomes infected. Almost invariably, the more active the growth of the plant when
it is infected the more severe the symptoms and the more they are widespread. Leaves
which have ceased growing at the time of infection generally show no symptoms even
though they contain the virus. Thus, strains of virus X which cause severe ringspot
symptoms on all the leaves when young tobacco plants are inoculated produce only
isolated lesions immediately around the point of inoculation on older, less actively
growing, plants. We have ourselves demonstrated the importance of the physiological
state, which is itself dependant upon external factors including nutrition, in the hostvirus relationship (Martin [8)),. this is perhaps not the proper time to quote this
work as Schepers and Beemster [12] will deal with their work in this field with potato
in a paper which follows.
To return to the effect of nutrition on the expression of symptoms it has just been
noted that nitrogen exacerbates the symptoms of yellow dwarf in onion. In contrast,
the opposite is found with sugar beet yellows and with leaf-roll in potatoes. Certain
varieties of beet show no symptoms when they receive abundant nitrogen even though
100% of the plants may be infected; thus, infected commercial crops showing no
obvious sign of disease are very dangerous sources of contamination of crops grown
for seed since virus infection can reduce the seed yield by 60 or 70 per cent. This is why
it is necessary to isolate seed crops even though, as in the majority of cases, the virus is
not transmissible in the seed.
Leaf roll in potato is another serious virus disease of the yellow type against which
there is available no method of combatting losses from disease other than rigorous
194
control of the health of planting material destined for seed production. This control of
foundation stocks should take full account of the nutritional status of the lines under
test; it is necessary to avoid excessive supplies of nitrogen in relation to phosphorus
and potassium. In this particular case, I think, detailed study of the nutrition of samples of plants destined for seed production could greatly reduce the fallibility of the
method.
2. Influence of nutrition on the infection potential of virus particles and on the
susceptibility of plants to virus
Before discussing the influence of nutrition on th~ susceptibility of plants to virus we
should first examine the infective power of virus .particles produced from plants of
differing nutrient status. Several ideas have been advanced in this area. Thus, in 1941
Spencer [13] stated that the infectivity per unit weight of tobacco mosaic virus varied
according to the nutrition of the host and the period for' which it had been infected. At.
first he reported that the total virus content of leaves deficient in nitrogen remained
constant for 16 days, while its virulence decreased by a half; on the other hand in
leaves well supplied with nitrogen the content of virus increased by five times over the
same period without any loss in virulence. In a later paper published in 1942 Spencer
[ 14] concluded that both concentration of virus and its virulence increased during the
twenty days following infection of the leaves and that the virus reached higher concentrations in leaves well nourished with nitrogen than in those which were N deficient
and thought that limiting the supply of N inhibited the development of virulence per
unit weight of virus rather than limiting multiplication of the virus.
Such experiments are the daily bread of the pseudo-scientific 'muck and mystery'
school. Bawden, the celebrated British virologist, with his customary genius, demonstrated point by point that these findings were fallacious.
It should be emphasised that in all experiments on inoculated leaves the interpretation
of quantitative differences is always difficult because we cannot say to what extent the
final result, expressed as quantity of virus per unit weight of leaf, is affected by the
number of points of entry and the possibilities for virus multiplication around these
points.
Bawden and Kassanis [1] showed that there was no evidence of any significant difference in virulence between virus preparations originating from plants which received
varying supplies of nitrogen, phosphorus and/or potassium. A preparation of tobacco
mosaic virus extracted from a plant is always heterogeneous and can be separated into
f~actions of different particle size and varying virulence. The richer a fraction in
particles over 300 m[L long, the greater its virulence per unit weight of virus. Varying N,
P or K supply does not cause variation in the proportion of virulent particles in the
populations extracted. Differences in infectivity per unit weight between virus extracted
from variously nourished plants are always very slight and without relation to nutrition
of the plant.
Spencer's concll1sions about virulence were based upon a number of fallacies. He did
not demonstrate: 1. that his method of isolating the virus ensured the extraction of all
the virus in the samples; 2. that the method used isolated virus and nothing else and
195
3. that the said method was not itself responsible for aggregation of the virus or at
least for a comparable degree of aggregation in the different samples. It is known that
the virulence of a virus preparation is inversely proportional to the degree of aggregation.
As Spencer [13, 14] gives no information in his publications on the percentage of
virus recovered or about the homogeneity of the final products, he had insufficient
grounds to justify his conclusions. For example, to mention the most important aspect
of his experimental method: the virus was isolated by a preliminary centrifugation at
66 000 g of previously frozen juice followed by a second, lower speed, centrifuging of
solutions obtained by re-suspending the material resulting from the first extraction.
Apparently, according to Spencer the supernatant liquid from the second, low speed
centrifugation only contained virus and the yield of the latter increased with the level
of N determined by micro Kjeldahl. It is a feature of Spencer's results that the preparations, made by this method, which had the lowest virulence were those in which
the yield of virus was the least. Thus, in the absence of strict criteria as to the purity of
the virus preparations, the differences observed could be explained simply by the
presence of a protein or nitrogenous compound as an impurity at a constant level in all
the preparations. The effects of this would be proportionally smaller as the quantity of
virus increased.
Turning to the effects of nutrition on the susceptibility of plants to virus, it would be
most surprising, because nutrition has such large effects on the growth and behaviour
of plants, if it had no effect at all upon their susceptibility.
Spencer [ 14], ever the same, states that the number of local lesions caused by tobacco
mosaic in Nicotiana glutinosa and Phaseolus vulgaris (a good means for estimating the
sensitivity of plants to virus) increased with increasing nitrogen as this exceeded the
level required for optimum growth. In tobacco, particularly, phosphorus also increased
susceptibility; low potassium favoured susceptibility which diminished as K was
increased to levels appropriate for normal development of the plant.
Bawden and Kassanis [1] repeated this work. They showed that potassium had a small
but definite effect on the resistance of tobacco to mosaic; nitrogen and phosphorus
had a more definite effect. Virus susceptibility of the plants only increases to the extent
that addition of supplementary nitrogen results in increased growth. The magnitude of
the effects largely depends, however, on the way in which the results are expressed. If
the number of lesions per leaf is taken as the criterion large differences are recorded as
the size of the leaves is increased by nitrogen and phosphorus, but, if the comparison
is made on the basis of number of lesions per unit surface area of leaf, the differences,
though still present, are less marked. For example, on the per leaf basis phosphorus,
increases the number of lesions by 500%; but if the comparison is made per unit area,
the difference falls to 50%.
These results of Bawden and Kassanis have been regularly confirmed by other workers
faced with the same problem. Thus Foster [6] showed that the number of infection
sites on a plant inoculated with cucumber mosaic varied according to the nutrition of
the plant. Plants well supplied with N were more susceptible than those which were
deficient. Further, high phosphorus with low potassium, high calcium. and high magnesium increased susceptibility to virus while, conversely, low phosphorus with high
potassium for example, reduced susceptibility to the same virus.
196
3. Influence of nutrition on virus multiplication
Here again it was Bawden and Kassanis [1] who produced the first sound results
which have, for the most part, been confirmed by subsequent work with other hostvirus systems. As pointed out by Bawden, who at the time did not have access to growth
chambers, the plant's reaction varies with external conditions (temperature, light,
humidity) and thus with the time of year when the experiments are made; thus
nutrition can influence the multiplication of virus according as to whether the experiments are carried out in June or November. If experiments are made in summer, plants
respond rapidly in growth to nitrogen and in these conditions nitrogen will also
increase the production of virus, quite different from winter, when the application of
nitrogen could reduce growth of the plants. Table 1 gives the results of one of Bawden
and Kassanis' experiments carried out with the system tobacco - TMV. The plants
were grown on a peat/sand mixture receiving varying nutrient solutions. The virus in
the juice from ground leaves was purified by various precipitation methods and
weighed.
Table 1. After Bawden and Kassanis [i]
Elements added
Relative weight of plants
(NPK= lOO)
Nil.
N
P
K
NP
NK
PK
NPK
12.6
5.6
30.8
11.2
72.8
16.8
39.2
lOO
Virus content of juice
Concentration
mg/ml juice
2.3
2.1
4.3
2.4
5.0
1.8
3.0
4.4
Total virus
content
13
4
54
II
125
13
43
170
In this experiment, nitrogen only increased the level of virus when the plants received
adequate phosphorus and when they responded in growth.
The effect on total weight of virus is much greater than that' on virus concentration in
the juice; this is because nutrition modifies the growth of the plant and, generally,
conditions which increase plant size also increase the content in virus. It should be
noted however that potassium reduces the concentration of virus without a corresponding effect on growth of the plant. Cheo, Pound and Weathers [5] in 1952 confirmed
almost all Bawden and Kassanis' results using a different biological system-spinach and
cucumber virus 1. In this case spinach achieved maximum growth at 630 ppm N; at
higher levels the plants were stunted. Virus concentration in leaf juice corresponded
closely with growth of the plants. In the case of phosphorus the response in growth
appeared to vary with season. Generally, phosphorus increased plant growth with the
optimum level at 93 ppm P; there was slight stunting at 547 ppm - much less than that
caused by excessN. P levels high enough to cause stunting of the plants did not affect
virus in the same way and the highest virus levels were recorded at the highest P levels.
The only result of Bawden and Kassanis which was not confirmed by this work was
that concerning the effect of potassium, where Cheo et al. found that in the case of
spinach and cucumber mosaic the level of potassium giving maximum growth also
resulted in the highest concentrations of virus.
197
Tomaru [15J also working with cucumber mosaic, found that the concentration of
Virus varied in a cyclical manner whatever the N level in the nutrient solution. The
maxima of these concentrations were higher and were reached more quickly at higher
N levels, but, in all cases declined thereafter.
There are a few reports on the role of trace elements in virus multiplication: zinc,
iron, molybdenum, boron, but they add little to the understanding of the relationship
between virus and host nutrition.
We should now further discuss the roles of nitrogen and potassium in host-virus
relationships. Kiraly [7J yesterday mentioned the results of Zaitlin and Jagendorf [16J
who gave a plausible explanation of the role of nitrogen in virus infected plants via the
Hill reaction and photosynthetic phosphorylation. I do not wish to discuss further this
particular point but I should like to dwell a little on the hypothetical roles of Nand K
in the metabolism of phenolic compounds as these are often said to be implicated in
resistance mechanisms. It is said that nitrogen reduces the phenol content and, as a
result, in general increases the susceptibility o( plants to disease and, particularly to
virus; potassium has the opposite effect. In the first place, to talk, in 1976, of total
phenols has no more biochemical or biological significance than to talk of total nucleic
acids; thus illumination has a much greater influence on the total phenol content of
plants than does N or K supply but the reactions of such plants towards virus are quite
different. It is said that a generous supply of N lessens the activity of the enzyme
phenyl-alanine ammonia lyase (PAL) which plays a key role in the synthesis of phenols
and that in this lies the explanation for the greater susceptibility of plants well supplied
with nitrogen. Well, the activity of PAL can be totally suppressed by treatment with an
auxin like compound, 4-amino-3-5-6 trichloropicolinic acid, without in any way
modifying the susceptibility of tobacco to TMV. On the other hand by critical analysis
of the numerous phenolic compounds contained in the plant it can be shown that
certain molecules containing a phenolic residue seem to play a determinant part in the
sensitivity of plants to virus and in the capacity of the latter to multiply the pathogen:
this concerns some phenol-amines (Martin- Tanguy et at. [9J) but as yet little is known
of the part played by mineral elements in their biosynthesis. Much remains to be done
in this field.
4. The role of potassium in meristem culture and in cell differentiation
Morel and Martin [lOJ pointed out in 1952 that meristem culture is a most valuable
technique for eradicating virus from plants. Its use has been greatly extended in recent
years and it has been used for the treatment of many cultivated plants and has resulted
in the introduction of efficient methods of in vitro multiplication which are beginning
to be used in commercial practice. In principle all plants can be freed of virus by
meristem culture and subsequently multiplied in vitro provided the correct medium,
and in particular the correct nutrient solution, can be found, and with due attention to
other growth factors.
The importance of potassium in the development of meristems, of potato at least, was
discovered through an experimental error. During an experiment designed to study the
effects of temperature on the development of the apex one series of meristems was
accidentally placed on a culture medium with five times the normal potassium content:
to the surprise of the authors, Morel et al. [11 J all these developed into very green and
198
vigorous plantlets though, using the medium standard at that time it was usual for
yields to be only from 50 to 60% of viable but lank plantlets. This was the more
surprising because the normal medium had proved quite adequate for the growth of
adult plants and it was not at first realised why it should be deficient in certain elements
for meristem culture. This led to study of the effects of mineral composition of the
- medium on the growth of meristems.
In a first experiment the basic medium was compared with media enriched with
potassium chloride at 5, 10 and 15 mM per litre. After three months the mean lengths
of the ex-plants under the various treatments were as follows: at the lowest K concentration- 1 mm, at 10 mM KCI- between 5 and 10 mm and at 15 mM KCI- also
from 5 to 10 mm. At the highest. concentration there was greater multiplication of explants. Thus the need for a high concentration of K ions for the development of the
apex was neatly demonstrated.
This was followed by various experiments concerning the effects of varying K, N0 3
and NH4 • I will not be so fastidious as to describe these in detail but will pass straight
to Morel's conclusions:
- The K ion had a uniform effect on all ex-plants.
- N0 3 and NH4 ions only allowed the elongation of a limited number of explants.
Though these explants were not calibrated, and are difficult to measure it seems. that
there is a limiting size above which they cannot grow in the absence of high K concentration and that the ions N0 3 and NH 4 only affect those which have passed this
threshold.
The function of potassium in embryogenesis has recently been studied by Brown et al.
[4] growing a suspension of carrot tissue in vitro. They showed that the K+ concentration which allowed maximum growth of un-differentiated cells in suspension
(l mM) is much lower than that required for maximum embryogenesis (20 mM).
Neither Na+ nor NH 4 + could replace K+. However, these effects are difficult to explain
because, though potassium is concerned in many metabolic processes, its exact
function is often still ill defined. Possibly the intact whole plant achieves this high K
concentration in the apex through mechanisms in the roots and vascular system. The
detached apex is apparently incapable of absorbing enough potassium from a medium
containing sufficient to cater for the m;~ds of the complete plant and it is therefore
necessary to force the K ion to penetrate the cell by raising the K concentration of the
external medium considerably.
An analogous situation in in vitro growth of tumour tissue was described by Braun and
Wood [2]. Tumour tissues of Vinca rosea developed vigorously in vitro on White's
medium containing no growth substances. Normal tissues require 7 different factors:
auxin, inositol, cytokinin, glutamine, asparagine, cytidilic acid, and guanilic acid. If
the concentrations ofKCI, NaN0 3 and NaH zP0 4 are considerably increased the authors
state that normal tissues become capable of development without glutamine, asparagine, cytidilic and guanilic acids. BraWl and Wood think that these mineral ions are
needed· for the synthesis of growth substances. The cell wall permeability of tumour
tissue is modified so that it allows the diffusion of sufficient of these elements into the
external medium to allow this synthesis to take place, while the healthy cell wall does
not. It is therefore necessary either to supply these growth regulators or to' force the
mineral ions to penetrate to the active sites by raising their concentrations in the
medium.
199
It seems therefore that it is at the level of cell wall permeability that we should search
for the specific role of the potassium ion.
In conclusion it is necessary to mention some of the consequences for the fertilization
of commercial crops of our ability to produce virus free plants. As you well know there
is in Europe a vast programme for the production of virus free root stocks and scions
of fruit trees. The use of such planting material in orchards without changing the
fertilizer programme, which was devised to meet the needs of unhealthy trees, can
result in serious loss as the grower is now dealing with extremely vigorous plants
which are difficult to bring to fruiting. Such observations confirm the results discussed
above: virus diverts for its own use substances produced in the plant by mineral
nutrition and photosynthesis and it may well be that the virus free tree's needs for
mineral nutrients in particular are reduced. The eradication of virus from cultivated
plants and their maintenance in a healthy condition could certainly prove to be a useful
means of achieving economy, particularly in energy.
References
1. Bawden, F. C and Kassanis, B.: Some effects of host nutrition on the susceptibility of plants to
infection by certain viruses. Ann. appL BioI. 37, 46-57 (1950).
2. Braun, A. and Wood, A.: On the activation of certain essential biosynthetic systems in cells of
Vinca rosea. Proc. nat. Acad. Sci. USA 48,1776-1782 (1962).
3. Brierley, P. and Stuart, N. V.: Influence of nitrogen nutrition on susceptibility of onions to
yellow dwarf virus. Phytopathology 36, 297-301 (1946).
4. Brown, S., Wetherell, D.F. and Dougall, D.K.: The potassium requirement for growth and
embryogenesis in wild carrot suspension cultures. Physiol. Plant. 37,73-79 (1976).
5. Cheo, P. C, Pound, G. S. and Weathers, L. G.: The relation of host nutrition to the concentration
of Cucumber virus I in spinach. Phytopathology 42,337-381 (1952).
6. Foster, R.E.: Host nutrition affects virus infection. Phytopathology 67, 98 (1957).
7. Kiraly, Z.: Plant disease resistance as influenced by biochemical effects of nutrients in fertilizers.
12th. Colloquium of the Intern. Potash Institute, Izmir-Turkey (1976).
8. Martin, C: Contribution a l'etude du phenomene d'hypersensibilite au virus de la Mosaique du
Tabac. Bull. Soc. Fran~. Physiol. Veg. 12, 345-354 (1966).
9. Martin-Tanguy, J., Martin, C, Gallet, M. and Vernoy, R.: Sur de puissants inhibiteurs naturels
de multiplication du virus de la Mosaique du Tabac. C. R. Acad. Sci. Paris, seance du 24 Avril
1976,4 p. (1976).
.
10. Morel, G. and Martin, C: Guerison de Dahlias atteints d'une maladie a virus. C. R. Acad. Sci.
Paris, 235, 1324-1325 (1952).
11. Morel, G., Martin, C and Muller, J.F.: La guerison des pommes de terre atteintes de maladies
a virus. Ann. Physiol. Veg. 10, 113-139 (1968).
12. Schepers, A. and Beemster, A. B. R.: Effect of fertilizers on the susceptibility to virus infection of
the potato, with special reference to natural plant resistance. 12th Colloquium of the Internal.
Potash Institute. Izmir-Turkey (1976).
13. Spencer, E. L.: Inhibition of increase and activity of tobacco mosaic virus under nitrogen deficient
conditions. Plant Physiol. 16,227-239 (1941).
14. Spencer, E. L.: Specific biological activity of tobacco mosaic virus as influenced by age of lesions
and nitrogen supply. Plant Physiol. 17, 210-222 (1942).
IS. Tomaru, K.: Changes in virus concentration of tobacco plants at different periods of time after
inoculation with cucumber mosaic virus. Bull. Hatano tobacco Experim. Sta. 58, 33-38 (1967).
16. Zaitlin, M. and Jagendorj, A. T.: Photosynthetic phosphorylation and Hill reaction activities of
chloroplasts isolated from plants infected with tobacco mosaic virus. Virology 12, 477-486 (1960).
200
Effect of Fertilizers on the Susceptibility to Virus
Infection of the Potato,
with Special Reference to Mature-Plant Resistance
A.Schepers, Ing., Research Station for Arable Farming, Lelystad/The Netherlands, and A.B.R.
Beemster, Dr. Ir., Institute of Phytopathological Research, Wageningen/The NetherlandS
Summary
From experiments on the relation between plant morphology and mature-plant resistance to potato
virus yN in potatoes it is concluded that mature-plant resistance develops gradually in the crop.
There is evidence that the rate of mature-plant resistance reaches a sufficiently high level when
development of new leaves on the main stems has ceased and yellowing of lower leaves has started.
A number of experiments studied the effect of fertilization on the development of mature-plant
resistance in the potato crop. In a greenhouse experiment potato plants were inoculated with potato
virus X. Results indicated that application of extra nitrogen delayed the development of potato
plants, thus keeping them longer in a stage where virus can easily multiply and move from the
inoculated leaves to the tubers.
Applying extra phosphorus had a slight effect in the opposite direction, the plants reaching the stage
of mature-plant resistance somewhat sooner than did the control plants.
Similar studies with potato virus yN were made in a number of field experiments and the results
showed that the effect of high nitrogen application was slightly unfavourable in that the plants
showed a slightly higher percentage of infected tubers than those in the plots with lower nitrogen
doses. The same holds for phosphorus, but to a smaller extent. Potassium did not affect mature-plant
resistance at all.
The general conclusion is that fertilization is not a major factor in mature-plant resistance, changes
in the general pattern of mature-plant resistance probably occur only when excessive amounts of
nitrogen and phosphorus, which are not used in practice, are given.
Les auteurs donnent un aper~u de la litterature relative au probleme de la sensibilite aux virus des
plantes de pomme de terre. Les resultats experimentaux sont souvent contradictoires.
Les auteurs ont effectue des essais ayant pour but d'etudier les relations entre la morphologie des
plantes d'une part, et la resistance des plantes mures envers le virus yN de la pomme de terre,
d'autre part. Les resultats obtenus montrent que la resistance des. plantes mures se developpe
graduellement dans une culture. Il y a evidence que le taux de resistance des plantes mures atteint un
niveau suffisamment eleve lorsque le developpemeilt de feuilles nouvelles sur les tiges principales a
cesse et que commence le jaunissement des feuilles infe.rieures. D'autres travaux seront necessaires,
afin de pouvoir arriver a des conclusions definitives.
L'on a etudie au moyen d'un certain nombre d'essais, les effets de la fertilisation sur le developpement de la resistance des plantes mures de pomme de terre. Dans le cadre d'un essai en serre on a
inocule des plantes de pomme de terre avec le virus X de la pomme de terre. Les resultats ont montre
que des applications supplementaires d'azote ont retarde le developpement des plantes de pomme de
terre, c. a. d. qu'elles furent maintenues plus longtemps a un stade durant lequel les virus se multiplient aisement et que migrent facilement des feuilles inoculees aux tubercules. Des doses supplementaires de phosphore eurent un effet oppose puisque sous leur influence le stade de la resistance de la
plante mure fut atteint un peu plus tot que chez les ·plantes temoin.
20.1
Le meme probleme fut etudie dans le cadre de plusieurs essais en plein champs qui porterent sur les
virus yN de la pomme de terre.
L'effet de doses elevees d'azote fut faiblement dHavorable, puisque le pourcentage de tubercules infestes fut plus eleve que dans les parcelles ayant re<;u des doses d'azote plus faibles. I1 en fut de
meme - quoique dans une moindre mesure - en ce qui concerne le phosphore. Le potassium n'avait
aucun effet sur la resistance de la plante mOre.
En conclusion, l'on peut dire que la fertilisation ne constitue pas un facteur majeur dans le contexte
du probleme de la resistance de la plante mOre. Probablement, des changements concernant la
resistance de la plante mOre ne surviennent que lorsqu'on applique des doses extremement elevees
d'azote et de phosphore, ce qui n'est que tres rarement le cas dans la pratique agricole.
i. Introduction
One of the factors affecting tube! yield of potatoes is fertilization. In the practice of
seed potato growing fertilizers not only affect yield, but also the yielding capacity of the
seed produced. Much work has been done studying the effect of fertilization on the
next year's crop, from which it has become clear that two principal entirely different
factors are involved, viz. one causing physiological changes and the other being a
matter of virus infection.
1.1. Application of increasing amounts of nitrogen was found to result in earlier
sprouting of the seed tubers and often in more rapid juvenile development of the
progeny plants (Kottmeyer [26]; Kriiger [27]; Wiinscher [45]; Hofferbert and zu
Putlitz [20]; Pfeffer [30]). In some cases phosphorus had a similar effect (Hofferbert
and zu Putlitz [20]; Brandt and Sessous [8]). High amounts of chloride may also
affect growth of the plOgeny crop positively (Arenz [I]; Wiinscher [45]).
Other workers failed to find any effect of fertilizers on the productivity of the seed
(Volkart [41]; Fischnich [9]; Reichard [34]; Schepers et al. [36]). The latter observed
that seed obtained from fields with high N dressings showed a tendency to produce
fewer main stems.
.
1.2. Much work has been done to study the effects of fertilization of the seed potato
crop on aphid development. Aphids are known to be efficient transmittors ofanumber
of important potato viruses, the infection of the tubers by the latter determining in large
measure the quality of seed potatoes. Whether or not viruses will be transmitted and
will reach the seed tubers depends infer alia on the development of the aphids and on
the susceptibility of the plants.
Increased rate of development of aphids has been observed with increasing nitrogen
rates (Janssen [22]; Kriiger [27]; Wiinscher [45]; Stricker [39]; Proeseler [32]). The
same was found for the application of chloride (Wiinscher [45]; Klapp [25]; Proeseler
[32]). Aphid development was also favoured by potassium deficiency (Janssen [22];
Klapp [24]). High amounts of phosphorus had an inhibiting effect on aphid development (Wiinscher [45]; Gericke [12]; Kriiger [28]; Brandf and Sessous [8]).
In The Netherlands, Harrewijn [13, 14, 15, 16, 17] recently investigated the effects of
host plant nutrition on aphid development (Myzus persicae) and confirmed that
increasing nitrogen dressings favoured the development of the aphid population. At
very high N rates, higher than used in practice, development of the population was
inhibited. Reproduction rate was also reduced if nitrogen was given as manure.
:;:02
High doses of potassium given as a split application, giving a potassium content in
June of 4.5% or more in the dry matter of the foliage, decreased aphid population
considerably.
Phosphorus favoured aphid development and so did magnesium. Aphid reproduction
rate decreased at high K/Mg ratios.
.
Calcium had no significant effect on aphid development.
In water culture experiments wing formation in Myzus persicae was directly favoured
by ample availability of NOs and P04-ions and by low K/Mg ratios. Moreover, wing
formation was shown to depend on:
- population density (influenced by mineral nutrition),
- composition of the nutrient medium (pH, amino acids, the pattern of the latter a. o.
being influenced by the K/Mg ratio in the medium),
- specific substances in the nutrient medium which affect aphid physiology (e~g. ratio
tyrosine/tryptophan),
- availability of certain micro-elements (e.g. eu, Li), and
- plant age.
1.3. Fertilizers have very variable effects on the rate of virus infection. Nitrogen
deficiency leads to a Iow rate of virus infection of the seed (Janssen [23]; Wiinscher
[45]), excess of nitrogen usually leads to a more severe virus infection of the progeny
(Klapp [24]; Wiinscher [45]; Hiller [19]; Arenz [2]; Stricker [39]; P/effer and
Goerlitz [29]). These results might have been influenced by the length of the growth
period, which is shortened by Iow and prolonged by high nitrogen applications.
In this connection it is also worth mentioning that excess of nitrogen may cause a masking of virus symptoms in potato plants (Arenz [2]; Arenz and Hunnius [3]; Wenzl
and Reichard [43]), which may lead to a less healthy progeny, because the virusinfected plants cannot all be eliminated by roguing.
With phosphorus fertilization both favourable (Wiinscher [45]; P/effer and Goerlitz
[31]; Ippel and Nelitel [21]) and unfavourable effects (Hawkins et al. [18]; Ross
et al. [35]) on the virus infection of the progeny have been found.
Some investigations show a high rate of virus infection of the progeny when chloridecompounds are applied (Ross et al. [35]; Arenz [1]; Klapp [25]; P/effer and Goerlitz
[31]). It is assumed (Toman [40]; Wiinscher [45]) that this Cl-effect can be ascribed
to the late maturation of the crop. Cl could also have a masking effect on virus
symptoms.
Other workers found no effect of fertilization on the virus infection of the progeny
(Gabriel [10,11]; Walsh [42]; Birecki et at. [7]).
2. Seed potato growing in The Netherlands and fertilization
Since the work of Janssen [23] little attention has peen given to the effect of fertilization of seed potato crops on virus infection in the Netherlands. Provided that excess
of nitrogen is avoided the subject is considered to be of minor importance. The development of aphid vectors of viruses is a main .factor in seed potato growing. By daily
catching aphids in yellow traps (Moericke [29]) it is possible to obtain information on
the date of appearance and the numbers of the most important aphid species during
the season. Based upon these data the General Netherlands Inspection Service/or Seeds
203
of Field Crops and of Seed Potatoes (N.A .K.) fixes dates on which the foliage of the
potato crop must be destroyed (mechanically or chemically) or pulled.
As mentioned earlier high rates of nitrogen are not normally applied, because tuber
initiation and tuber growth are delayed, resulting in lower yields at the date of haulm
killing. Cultural practices are directed towards obtaining an early crop by pregermination of the seed, early planting and a rather high plant density, all factors promoting optimal growth in the early stages.
3. Mature-plant resistance to viruses in potatoes
As was pointed out earlier, growing of high quality seed potatoes in The Netherlands
can only be successful when the haulms are destroyed before the virus is translocated
from the leaves to the tubers. Work on translocation of virus in potato plants
(Beemster [4, 5, 6]) has shown that transport of virus from leaves to tubers is very
rapid in young plants; with increasing age of the plants, however, speed of virus
transport decreases and when plants have reached a certain stage no more virus will
reach the tubers. This phenomenon, called mature-plant resistance, holds for the most
important potato viruses and can be of help in producing high quality seed potatoes.
Among the many interesting questions related to the phenomenon of mature-plant
resistance there are two of great importance for the farmer: 1. how to recognize in the
field the stage of development of the plants in which mature-plant resistance has
reached a sufficiently high level and 2. how can crop growth be affected in such a way
that mature-plant resistance develops quickly in a potato crop. In the following the
results of some experiments related to both questions will be presented.
3.1. Determining the stage of growth by which mature-plant resistance develops
As daily tuber production around the date of haulm killing may exceed 500 kg/ha, it is
very important for the farmer to fix such a date accurately. As was mentioned earlier
the farmer tries to make use of mature-plant resistance by early planting and pregermination, but till now there are no means of determining the degree of mature-plant
resistance, present in a crop at a given time. Therefore, a number of experiments have
been carried out in The Netherlands to study the question as to whether certain
morphological characteristics of potato plants correlate with the presence of a sufficient degree of mature-plant resistance. (Reestman and Schepers [33],. Schepers and
Reestman [38]), some of the results will be briefly mentioned in the following.
In the experiments different build-ups of the potato crop (variety Bintje) were realized
by applying two plant densities: 20000 and 60000 plants per ha. In 1974 groups of
plants were inoculated with potato virus yN (PVyN) at ten days' intervals, starting on
June 11, the last inoculation being performed on July 31. Sap from PVyN-infected
potato plants (diluted 1 :10 and mixed with carborundum, 350 mesh) was used as
inoculum and sprayed on the crop with a paint spraying gun (Wiersema [44]), at a
pressure of 4-5 atm. Care.was taken to hit all parts of the plants. Samples of 150 tubers
each of five replications were collected at the date of inoculation, and two and four
weeks later. The rate of tuber infection by PVyN was established by planting the
tubers and testing the plants for the presence of virus.
204
Observations on morphological characteristics of the plants were made periodically
(the dates of inoculation), by counting the number of leaves per main stem, the number
of lateral branches and by watching the degree of yellowing or dropping of leaves of
the main stems.
In Figure 1 the results of the experiment are shown. It is clear that the pattern of
PVyKinfection was almost identical for both plant densities. It has to be noted that in
Figure 1 the lines X and Y give percentages of tuber infection obtained 2 weeks and 4
weeks after inoculation, respectively, plotted against inoculation dates. Thus the lines
X and Y give an indication of how mature-plant resistance developed during the
season, in relation to the date of inoculation. The first two inoculations (on June 11
and 20) resulted in almost complete infection of the tubers; the inoculation on July 1
resulted in a lower percentage of tuber infection, particularly when considering the
results obtained 2 weeks after inoculation, indicating that mature-plant resistance had
Number of leaves
per main stem
30
60000 pI.jha
20000 pl.jha
O/oPVyN
100
25
_3
2
20
Cc
"''''
:<:3
~
.0>,
...
15
80
0
eu=
L..l1>
60
100
10
80
5
40
40
60
20
20
10/6
- - - - - Number of leaves per main stem
I = Number. of leaves ~ '/2 cm to the 1st flower
2 = Number of leaves ~ Yz cm to the 2nd flower
3 = Number of leaves ~ Yz cm to the 3rd flower
4 = Total number of leaves
........................... Percentage of sprouted axil-buds of the 10 lowest leaves on the main stem.
= total
II = ~ 5 cm.
I
-------- Percentage of the lowest 10 leaves on the main stem which had yellowed or had
dropped,
_._._._.-.-.- Percentage of infected tubers
x = two weeks after inoculation .
y = four weeks after inoculation
z = natural infection
Fig.I. Some morphological characteristiCs of potato plants and the infection of tubers by potato
virus yN' 2 and 4 week~ after inoculation. Left: 20000 pl.jha; right: 60000 pI.jha.
205
become noticeable. The inoculations performed later did not result in any appreciable
amount of tuber infection. Although virus transport from leaves to tubers continued
during this period (see the results of the inoculation on July 1), it seems that an initial
infection at this time did not result in a significant infection of the tubers. The data on
plant morphology show that the time of appearance of a noticeable rate of matureplant resistance (as expressed in the rate of tuber infection) was more or less related to
the time at which formation of new leaves had almost ceased and when the lower leaves
had started yellowing (or dropping).
Tuber infection of the plants from the plots which were not inoculated artificially
continued till the end of August as can be concluded from line Z. Apparently, virus
brought into the plants earlier than July 10 was still multiplied and translocated
during the period when initial infections no longer gave rise to tuber infection.
3.2. Effect of fertilization on mature-plant resistance
In a preliminary experiment, carried out under greenhouse conditions the effect of
excessive doses of nitrogen and phosphorus on mature-plant resistance to potato virus
X (PVX) was studied. In this experiment single-stemmed potato plants, grown in pots
(10 liters) with normal fertilization were inoculated manually with PVX, 44, 58 and
72 days after planting. In the same way groups of plants which had received an extra
amount of 3 g calcium ammonium nitrate per pot every two weeks (starting 2 weeks
after planting), and a third group having received 3 g superphosphate at the same intervals were treated. One, 2 and 3 weeks after inoculation the tubers of 5 plants of each
group were harvested, whereas at the time of plant maturity another 5 plants of each
treatment were harvested. The harvested tubers were planted the next season and the
plants growing from them' tested for the presence of PVX, using Gomphrena globosa
as a test plant. The percentages of tuber infection, found in each of the treatments are
given in Table 1.
Table 1. The percentages of virus infection of tubers of potato plants grown at different nutritional
conditions after inoculation with potato virus X
Age of plants at the
time of inoculation
(days after planting)
Period between inoculation and harvest
I week
2 weeks
3 weeks
at the time of
plant maturity
44
0
3
0
0
4
7
30
26
7
38
50
24
72
38
80
39
100
100
80
100
100
97
44
58
72
0
3
0
29
0
0
27
21
3
58
31
0
72
55
79
81
98
58
72
44
58
206
normal
fertilization
extra
nitrogen
extra
phosphorus
extra nitrogen
& phosphorus
Without going into detail it can be concluded that both in plants with normal fertilization and in those with extra phosphorus mature-plant resistance was apparent
already at the first inoculation (44 days after planting), because tuber infection did not
reach the 100% level, even at the last date of harvesting (about 10 weeks after inoculation). Mature-plant resistance generally became increasingly pronounced the older the
plants were at the time of inoculation, as'is clearly shown by the percentages of tuber
infection given in Table 1. It is also clear that the extra nitrogen doses affected the plants
in such a way that mature-plant resistance developed only very slowly, negatively influencing the health of the seed. There is some evidence that in the experiment described the application of extra phosphorus had a favourable effect because the group
of plants inoculated 72 days after planting and having received the extra phosphorus,
showed the lowest pelcentage of virus infection.
To obtain information on the effects of fertilization oh virus infection under field
conditions a series of experiments were carried out in the years 1961, 1962, 1963 and
1966 (Schepers et al. [37]). In these experiments potato plots of the variety Bintje
with varied N, P and K fertilization were mechanically inoculated with PVyN. The
inoculations were performed on single-stemmed plants of which the youngest fullgrown leaf was inoculated with sap from virus-infected potato plants using carborundum as an abrasive. The inoculations were carried out periodically on the dates
given in Table 2. Tubers were harvested four weeks after each inoculation and planted
the next season. From the results of testing the plants or watching them for symptoms
the percentages of tuber infection, given in Table 2, were obtained. In Table 2 the
results of the 1966 experiment are not presented because no infected tubers were found
in the progeny. In 1963 only one - moderate - K-rate was given.
In 1961 and in 1962 the first inoculation was performed when tuber formation had
already started; in 1963 tubers were not present at the time of the first inoculation. The
results of the 1961 and 1962 experiments show a fairly high degree of mature-plant
resistance present in the crop at an early stage of growth, viz. at the beginning of the
tuber formation period. Two weeks later mature-plant resistance had become almost
complete.
Table 2. The percentage of tuber infection of potato plants grown with vaded N, P and K fertilization
four weeks after inoculation with potato virus yN
1961
1962
1963
27/6 6/7 20/7
14/6 28/6 12/7 27/7
6/6 13/6 20/6 27/6 18/7
lowN
low P, low K , .......
low P, high K .......
high P, low K .......
high P, high K .......
I3
18
14
7
0
0
0
2
0
0
0
2
27
18
39
38
I
4
5
3
3
2
3
2
0
I
0
0
high N
low P, low K ........
low P, high K .......
high P, low K .......
high P, high K .......
14
24
34
24
0
3
0
2
3
0
4
3
35
41
46
43
15
7
4
0
8
7
3
6
6
2
5
10
Date of inoculation
65
27
29
32
3
56
41
28
23
6
43
24
23
33
0
57
27
29
51
207
In 1963, mature-plant resistance, although present, was not very significant in the very
early stage of growth. After tuber formation had set in, the percentage of infected
tubers remained at the same, moderate, level for some weeks. A high degree of matureplant resistance was present in the crop on July 18. In that year no inoculation was
carried out between June 27 and July 18.
The high nitrogen level seems to have somewhat delayed the appearance of matureplant resistance.
The effect of phosphorus was variable. The infection of the tubers tended to increase
with increasing amounts of phosphorus. In literature the opposite has often been
reported (Wiinscher [45); Arenz and Hunnius [3}; Pfeffer and Goerlitz [31}; Proeseler
[30} ), as was also the case in the greenhouse experiment described before.
The favourable effect of both nitrogen and phosphorus on virus synthesis could
theoretically be explained because both elements are required for the synthesis of
nucleoproteins (viruses).
The potassium rate is apparently of little importance with respect to the development
of mature-plant resistance.
In our field experiments the effects of fertilizers on virus infection of the tubers were
not statistically significant. It can be stated that with normal doses of nitrogen,
phosphorus and potassium sufficient to obtain optimal yields at the time of haulm
destruction, there is no need to fear unfavo,urable effects of fertilization on the rate of
virus infection of seed tubers under Dutch conditions.
References
1. Arenz, B.: Pflanzenernahrung und Kartoffelbau. Landwirtschaftliches Jahrbuch ftir Bayern 27,
(5/6), 51-63 (1950).
2. Arenz, B.: Die Ausbreitung der Viruskrankheiten (Blattroll- und Strichelkrankheit) der Kartoffel in Abhiingigkeit von Sorte und Umweltbedingungen. Bayerisches Landwirtschaftliches
Jahrbuch 33, (6), 657-674 (1956).
3. Arenz, B. and Hunnius, W.: Grundlagen und Technik des Pflanzkartoffelbaus. Bayerischen Landwirtschaftverlag GmbH, MUnchen, 1959.
4. Beemster, A.B.R.: Een vergelijking tussen het transport van X-virus en twee verschillende
stammen van Y-virus. T. PI. ziekten 67, 278-279 (1961).
5. Beemster, A.B.R.: Het transport van Y-virus in aardappelplanten na besmetting door bladluizen. Med. Landbouwhogeschool en de Opzoekingsstations van de Staat te Gent, 1786-1796,
(1965).
6. Beemster, A.B.R.: Virus translocation in potato plants and mature-plant resistance. In:
J. A. de Bokx (Ed.): Viruses of Potatoes and Seed Potato Production. Pudoc, Wageningen,
144-151, (1972).
7. Birecki, M. and Kazimierz Kubicki: Influence ofvernalization and additional fertilizing applied
over a many year period on the productional value of seed potatoes. (Polish with Eng. summ.)
Rocziniki Nauk Rolniczych. Tom 8i-A-i, 29-46 (1960).
8. Brandt, J. and Sessous, D.: Bedeutung der PhosphorsiiuredUngung ftir Leistung und Gesundheit der Kartoffel. Phosphorsaure i3, (5), 293-311 (1953).
9. Fischnich, 0.: Bericht iiber die Tiitigkeit der Forschungsanstalt ftir Landwirtschaft, Braunschweig-VOlkenrode, 30-32 (1957).
10. Gabriel, W.: Influence of increasing phosphorus doses on the value of the seed potato tubers
(Polish with Eng. summ.). Biuletyn Institutu Ziemniaka 7, 57-67 (1971).
11. Gabriel, W.: Influence of phosphorus fertilization on the yield and quality of seed potatoes after
early haulm removal (Polish with Eng. surnm.). Biuletyn Institutu Ziemniaka 9, 45-55 (1972).
12. Gericke, S.: Wirkung und Wirtschaftlichkeit der PhosphorsauredUngung irn Kartoffelbau.
Tellus Verlag, Essen, (1954).
208
13. Harrewijn, P.: Reproduction of the aphid Myzus persicae related to the mineral nutrition of
potato plants. Ent. expo & appli. 13, 307-319 (1970).
14. Harrewijn, P.: Wing production by the aphid Myzus persicae related to nutritional factors in
potato plants and artificial diets. In: J. G. Rodriguez (Ed.): Insect and mite nutrition. North
Holland, Amsterdam, 575-588, (1972).
15. Harrewijn, P.: Functional significance of indole alkylamines linked to nutritional factors in
wing development of the aphid Myzus persicae. Ent. expo & appl. 16, 499-513 (1973).
16. Harrewijn, P.: Invloed van de fysiologische toestand van de waardplant op het populatieverloop
van zuigende insecten, met name bladluizen .. Jaarverslag Inst. v. Plantenziektekundig Onderzoek
(1975).
17. Harrewijn, P.: De invloed van bemesting op bladluispopulaties in aardappelen. In press (1976).
18. Hawkins, A., Terman, G.H. and Simpson, G. W.: Effect of rate of fertilizer application on spread
of leafroll and mosaic. Bull. 449 Maine Agr. Exp. Sta., 301 (1947).
19. H;ller~ W.: Okologische Versuche zur Untersuchung der Einwirkung von Dlingung und Wuchsstoffen aufErtrag und Viruskrankheiten bei Kartoffeln. Boden und Pflanze 41,5-10 (1955).
20. Hofferbert, W. and zu Putlitz, G.: Kann man durch mineralische Dlingung den Nachbauwert
der Kartoffeln beeinflussen? Kartoffelbau 7, (6), 112-115 (1956).
21. Ippel, H. and Neutel, H.: Doeltreffende fosfaatbemesting sleutel tot het ideale aardappelgewas.
Meded. NAK 19, (10/11), 121-122 (1963).
22. Janssen, J.J.: De invloed van kalibemesting op het voorkomen van bladluizen bij aardappels.
Landbouwk. Tijdschr. 40 (483), 1-7 (1928).
23. Janssen, J.J.: Invloed der.bemestingop de gezondheid van de aardappel. T. PI. ziekten 35,
119-151 (1929).
24. Klapp, E.: Zusammenhang diingungs- und bodenbedingter Standortunterschiede mit Pfirsichblattlausbesatz und Nachbauwert der Kartoffel. Z. flir Acker- und Pflanzenbau 93, 347-359
(1951).
25. Klapp, E.: Kalium-Mangel und Y-Virus. Diskussionsbeitrag Kalium symposium. Int. Potash
Inst. Bern, 193 (1956).
26. Kottmeyer, F.: Ertrag und Pflanzgutwert unter Beriicksichtigung des Einflusses von N-DiingemitteI und verschiedener Bodenarten. Kiihn-Archiv 15,25-196. Diss. Halle, 1927.
27. Kriiger, F.H.: Uber den Einfluss einseitiger Dlingung auf den Kartoffelbau. Z. Acker- und
Pflanzenbau 93, 359-385 (1951).
28. Kriiger, F.H.: Wirkung der Phosphatdiingung auf Wachstum und Virusbefall der Kartoffel.
Phosphorsiiure 13, 285-292 (1953).
29. Moericke, V.: Eine Farbfalle zur Kontrolle des Fluges von Bla ttliiusen insbesondere der Pfirsichblattlaus Myzodes persicae. Nachr. bl. Dt. PfI. Schutz. Braunschweig 3, 23-24 (1951).
30. Pfeffer, c.: Uber den Einfluss der Diingung auf den Pflanzgutwert von Kartoffeln. Eur. Pot.
J. 2, 238-250 (1959).
31. Pfeffer, C. and Goerlitz, H.: Uber den Einfluss der Mineraldiingung und einiger Spurelemente
auf die Wanderungsgeschwindigkeit der Viren und den Virusbefall von Pflanzkartoffeln.
Albrecht Thaer Archiv 5, 216-235 (1961).
32. Proeseler, G.: Beziehungen zwischen Kartoffelbau und Diingung. Dt. Landw.14, 170-172 (1963).
33. Reestman, A.J. and Schepers, A.: Toepassing'van morfologische gewasanalyse bij het toprolonderzoek van aardappelen. Jaarverslag van het Proefstation voor de Akkerbouw Wageningen,
61-64 (1971).
34. Reichard, T.: Der Einfluss der Stickstoff- und Chlorkaliumdiingung auf den.Pflanzgutwert von
Kartoffeln. Bodenkultur 14, 303-312 (1964).
35. Ross, A.F., Chucka, J.A. and Hawkfns, A.: The effect of fertilizer practice induding the use of
minor elements on stem-end browning, net necrosis and spread of leafroll virus in the Green
Mountain variety of potato. Maine Agric. Exp. Sta. Bull. 447, 9.7-142 (1947).
36. Schepers, A., Hoogland, R.F. and Krijthe, N.: Influence ofNPK-applicationto seed-potato crops
on the productivity on the progeny. Eur. Pot. J. 12,251-263 (1969).
37. Schepers, A., Beemster, A.B.R. and Reestman, A.J.: Ouderdomsresistentie tegen virusziekten bij
pootaardappelen. Jaarverslag Proefstation voor de Akkerbouw·Lelystad-Wageningen, 65-67
(1972).
38. Schepers, A. and Reestman, A.J.: Mature-plant resistance against PVyN in relation to some
morphological characteristics. Abst. of Conference Papers, 6th Triennal Conference EAPR,
Wageningen, 100-102 (1975).
39. Stricker, H.: Untersuchungen liber die Beeinflussung des Pflanzgutwertes der Kartoffel durch
die mineralische Dlingung in einer Abbaulage. Dt. Landwirtsch. 9, 113-188 (1958).
209
40. Toman, W.A.: Einfluss der Erniihrung und Umwelt auf den Virusbefall der Kartoffe1n und die
Leistungsfiihigkeit des Nachbaues. Boden und Pflanze 41, 10-12 (1955).
41. Volkart, A.: Der Einfluss steigender Stickstoffgaben auf den Saatgutwert der Kartoffeln. Landwirtsch. Jahrb. d. Schweiz 62, 83-95 (1948).
42. Walsh, T.: Discussion and Communication, 3rd Session Potassium Symposium. Int. Potash Inst.'
Bern, 191 (1956).
43. Wenzl, H. und Reichard, T.: Zur Frage der Maskierung der Blattroll-Symptome durch Dtingung. Pflanzenschutz-Berichte XXVII, 51-65 (1961).
44. Wiersema, H. T.: Breeding for resistance. In: I.A. de Bokx (Ed.) Viruses of Potatoes and Seedpotato Production. Pudoc, Wageningen, 174-187, (1972).
45. Wiinscher, CH.: Uber den Einfluss der Diingung auf Leistung und Gesundheit der Kartoffel.
Z. Acker- und Pflanzenbau 94, 377-421 (1952).
210
Influence of Soil Fertility on Virus Disease in Lucerne
Prof. Dr. M. Babovic and Prof. Dr. Dj. B. Jelenic*, Faculty of Agricultural Sciences, University of
Belgrade/Yugoslavia
Summary
The effect of virus infection on growth and yield of ten lucerne cultivars was examined in field trials
on chernozem (Zrenjanin) and smonitsa (Zajecar) enabling some study of the influence of soil
fertility on progress ,of the disease..
Lucerne mosaic virus and cucumber mosaic virus decreased yield by up to 42% and growth by up to
28%. Soil fertility influenced both growth and yield and severity of virus attack. At the first harvest,
viurs affected yield little. Later, infection was more severe on chernozem. The relatively higher
fertility of this soil, particularly high Nand P content, prolonged the period of active growth
enabling the virus to develop more vigorously and promoting the migration of aphids, thus accelerating spreading of the disease.
Resume
On a examine l'effet de l'infection par des virus sur la croissance et le rendement de dix varietes de
luzerne dans des essais en plein champ sur chernozem (Zrenjanin) et smonitsa (Zajecar), permettant
l'etude de !'influence de la fertilite du sol sur le developpement de la maladie.
Le virus de la mosaique de la luzerne et le virus de la mosaique du concombre ont diminue le rendement jusqu'a 42% et la croissance jusqu'a 28%. La fertilite du sol a influence la croissance, le rendement, ainsi que la gravite de l'attaque par les virus. Pour la premiere coupe, les virus ont peu affecte
le rendement. Ulterieurement, l'infection a ete plus importante sur chernozem. La fertilite relativement plus elevee de ce sol, particulierement des teneurs en N et P elevees, ont prolonge la periode de
croissance active, permettant au virus de se developper plus vigoureusement et favorisant la migra
tion des pucerons, accelerant ainsi la propagation de la maladie.
Introduction
Lucerne is one of the principal forage crops in Yugoslavia. It is susceptible to a number
of diseases and lucerne mosaic virus is found almost everywhere. There are many data
on its harmful effects ( Henson and Diachun [8]; Froscheiser [6]). The disease is the more
serious because the virus is transmitted in the seed (Belli [4]; Froscheiser [5, 7];
Babovic [2]; Tosic and Pesic [10]). There are various aphid vectors. Lucerne mosaic
virus with cucumber mosaic virus is a serious limitation to lucerne production.
Our investigations, carried out in 1972-1975, aimed to find out how soil fertility
. influenced the yield of virus infected lucerne and how it influenced the severity of
symptoms and spreading of the disease.
* Member
of the Scientific Board of IPI
211
Experimental
Ten cultivars of Yugoslavian and American origin were used: They are listed in Tables
1 and 2. The first four listed are from Yugoslavia, the remainder from the USA. The
experiments were laid down in March 1972 with four replications on chernozem
(Zrenjanin) and two on smonitsa (Zajecar). Seed was spaced at 300 x 500 mm with
200-210 plants per cultivar. Observations on plant growth and virus symptoms were
made at monthly intervals. Virus was tested on Phaseolus vulgaris cvs. Topcrop and
Pinto, Nicotiana glutinosa and Chenopodium amaranticolor Coste and Reyn. Diseased
plants were individually marked and spread of virus in their immediate vicinity was
monitored. Aphid migration was also monitored. Soil analysis was carried out by
standard methods.
Results
Virus symptoms were first noted one year after sowing, the symptoms comprising leaf
chlorosis, curling and twisting, mosaic like spots and dwarfing of shoots. It was confirmed that the symptoms were caused by lucerne mosaic virus and cucumber mosaic
virus. The disease was found on all cultivars on chernozem with a varying degree of
severity (12% on Ranger F. C. to 28% on Banatska) in the first year after planting. On
smonitsa, the most severe infection, on Banatska, was only 6%. During vigorous early
growth the symptoms abated, and the diseased plants were difficult to distinguish from
the healthy both in appearance and in productivity. Later on the symptoms became
more evident and diseased plants suffered reductions of 3-5 % in growth and about 9%
in yield. The number of diseased plants increased over the same period but the spread
was not confined to plants near to the sources of infection. During the third year from
planting (1974) infection increased by 2-14% on all cultivars on chernozem, the spread
taking place in the immediate neighbourhood of the already infected plants. In 1975 the
infection spread more slowly in concentric circles, the number of plants infected
increasing by 1-9%.
The disease spread more slowly on smonitsa, where, at the end of three years the
percentage infection was only 6-9%. The spread of the virus on chernozem is illustrated in Table 1.
Table 1. Spread of lucerne alfalfa virus on chernozem
Cultivar
NS. Banat 2 SM lJ
NS. VZ. SM. III
Banatska
Krusevac I
Ecotipo marchigano
Arnimbostord
Narragansett, F. e. 39,529
Vernal F. C. 39,527
Ranger F.e. 39,529
Ranger, MSB F. e. 38,921
212
Number
of plants
138
152
176
167
170
182
179
162
179
167
% infected
% increase
1973
1974
1975
20
24
28
22
26
23
16
22
12
22
13
6
11
13
13
10
14
2
6
2
4
5
in infecti 0 n
I
0
4
7
9
5
8
9
The effect of infection on growth and yield of the cultivars under test on chernozem
are listed in Table 2.
Though the experiments were sited at some distance from other lucerne fields, aphids
were recorded on the experiments at the end of the first season. They were recorded in
each of the three following years but their numbers were relatively low due to cold
rainy weather in May, June and the first half of July in these years reducing the
population and limiting migration.
Table 2. Influence of virus on growth and yield
Cultivar
Growth and yield decrease in percent per year in relation to
healthy plants
1973
NS. Banat 2 SM II
NS. VZ. SM. III
Banatska
Krusevac 1
Ecotipo marchigano
Arnimbostord
. Narragansett, F. e. 39,529
Vernal F. C. 39,527
Ranger F.e. 39,529
Ranger MSB F.C. 38,921
1974
growth
yield
7
3
0
0
7
5
0
5
9
8
18
0
37
2
4
23
10
26
17
9
growth
2
3
4
9
5
10
4
6
8
5
1975
yield
growth
yield
13
7
0
25
26
9
17
13
11
0
2
6'
27
0
0
3
3
2
2
0
20
15
0
0
42
0
46
2
0
20
The general pedological and agrochemical properties of the soils chernozem and
smonitsa are characterised by great differences in ecological conditions.
Chernozem: On the basis of paleobotanical investigation (Soo), it can be conCluded
that Pannonian calcareus shernozem (Zrenjanin-Vojvodina) was formed in the Boreal
Post-Glacial period, i.e. about 10 000 years ago; this represents the predominant type
of chernozem in Yugoslavia. The chief characteristics of Pannonian calcareous
chernozem are: a) dark brown colour; b) carbonates beginning from the surface;
c) medium or considerable thickness; d) exellent structure ; e) medium humus content.
A description of a chernozem profile in Zrenjanin region:
A = 0-30 cm. Plough layer, dark brown in colour, loamy In texture carbonate
beginning from the surface, small, crumbly structure.
A
30-50. Undisturbed part of the cumulative humus horizon. Loam, dark in
colour, carbonate, with an excellent grainy structure and many passages of
earthworms with caprolites. Pseudomicellium from 50 cm downwards.
AC = 50-90 cm. Transitional horizon: gradual transition from humus horizon to
loess. As regards texture, heavy loam of indeterminate structure. Many
passages of earthworms can be seen.
Cl = 90-120 cm. Loess with many ,holes ('krotovinas') and numerous passages of
earthworms. Some infiltration of humus is observable.
Cz = 120--'200 cm. Loess without fossils.
Chemical properties: Humus content 4---6%, calcium carbonate up to 10-11%
beginning from the surface. In the lower part of the transitional horizon the CaC03
213
content rises to 30%. Soil reaction - pH: A horizon - 8,3 (in H 2 0), 7.20 (in nKCI);
AChorizon - 8.80 (in HP), 7.50 (in nKCI); Cl horizon - 8.90-9.20 (in HP), 7.60-7.80
(in nKCI).
Nitrogen total content: A horizon - 0.24%, AC horizon - 0.12%, Cl horizon - 0.05%.
Available phosphorus and potassium content in mg/lOO g of soil: P20S in A horizon
24.2-31.8, in AC horizon 3.4-7.4, in Cl horizon 2.6-3.2; K 20 in A horizon 27.2-31.8,
in AC horizon 7.8-10.2, in Cl horizon 5.6-7.4 mg/lOO g of soil. Biological activity is
high except during ,the dry period in summer. Fertility very high.
Smonitsa: These soils are most widespread in the eastern part of Yugoslavia (in Serbia
and Macedonia). Chief properties of smonitsa soi1are connected with the pedological
characteristics as reliCt hydrogenic soils of the tertiary period. Smonitsa in Zajecar
region have a profile of the Al-AC-C type. The depth of the humus horizon is
70-100 cm. It is dark gray to black in colour, and at times coarsly lumpy and prismatic
in structure. As regards their mechanical composition, they most frequenthy belong to
medium and light clays, but heavy clays, containing over 80% of physical clay
(particles under 0.01 mm) are not infrequent. Only traces of skeletal matter are found
in this soil type. With rare exceptions, this soil is characterised by very poor physical
properties. They are very difficult to cultivate.
The reaction ranges from slightly acid to slightly alkaline, as a rule over pH 6.5. The
content of the humus in the plough layer is 4-7%. In spite of their poor physical
properties and some lack of readily available P20 S (1.90-3.11 mg P20 sj100 g of soil),
and available potassium 3.7-11.2 mg K 20/lOO g of soil smonitsa soils are used exclusively for field crops.
Discussion
The results showed that both lucerne mosaic virus and cucumber mosaic virus spread
very irregularly on both soils. The spread was relatively fast on chernozem where, at
the end of the third year in some var;eties (Ecotipo marchigano and Banatska) up to
40% of plants were affected. In contrast, spread on smonitsa was very slow and the'
highest degree of infection found, on Banatska, was only 9%. Thus spread was much
greater on the more fertile soil. The chernozem is a fertile agricultural soil on which
growth was prolonged, thus increasing the possibility or virus multiplication and
increasing the migration of aphids. On chernozem, virus had a large effect on growth
and yield, though in the year of planting symptoms were masked. The spread of virus
and consequent effects on yield were very much less on smonitsa. This indicates clearly
the influence of soil fertility. Similar results were obtained by Kreitlow et al. [9];
Henson and Diachun [8]; Babovic (l) and Froscheiser [6].
It seems that the higher N content of the soil has a special influence on the appearance
and expansion of virus infection and also on productivity of lucerne. However, one
should not overlook the possible effects of other important factors as the two experimental soils were situated in different climatic regions.
214
References
1. Babovic, M.: Uticaj virusa zutog mozaika pasulja na porast, bokorenje i formiranje cvasti crvene
deteline. Prvi kongres mikrobiologa Jugoslavije, 710-713 (1969).
2. Babovic, M.: Uporedna proucavanja prenosenja virusa mozaika lucerke. semenom nekih
americkih i jugoslovenskih populacija lucerke. Arhiv za polj. nauke 103,73-79 (1975).
3. Babovic, M.: Stepen prenoslijvosti virusa mozaika lucerke semenom lucerke. Mikrobiologija u
stampi (1975).
4. Belli, G.: Rilievi od esperienze sulla transmissione per seme del virus del mosaico dell'erba
medica e dimostrazione della sua esclusione in cloni di vite virosati. Ann. Fac. Agr. di Milano,
la, 33 (1962).
5. Froscheiser, F. 1.: Prevalence of alfalfa mosaic virus in alfalfa in M innesota. Plant Dis. Rept. 48,
506 (1964).
6. Froscheiser, F.l.: Variable influence of alfalfa mosaic virus strains on growth and survival of
alfalfa and on mechanical and aphid transmission. Phytopathology 59, 857-862 (1969).
7. Froscheiser, F.l.: Alfalfa mosaic virus transmission to seed through alfalfa gametes and longevity
in alfalfa seed. Phytopathology 64, 102 (1974)..
8. Henson, L. and Diachun, S.: Effect of a strain of alfalfa mosaic virus on the yield of clonaly
propagated Atlantic alfalfa. Phytopathology 47, 15 (1957).
9. Kreitlow, K. W., Hunt, O.J. and Wilkins, L.B.: The effect of virus infection on yield and
chemical composition of Ladino clover. Phytopathology 47, 390-394 (1957).
10. Tosic, M. and Pdic, Z.: Investigation of alfalfa mosaic virus transmission through alfalfa seed.
Phytopat. Z. 83, 320-327 (1975).
215
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
Can the Protoplast System Be Applied in Studies on the
Role of Mineral Nutrients in Plant Diseases?
Prof. Dr. G. L. Farkas, Institute of Plant Physiology, Biological Research Center, Szeged/Hungary
Summary
It has been pointed out that the contradictory results obtained on the role of mineral· nutrients in
plant diseases and disease resistance are due to the lack of a reproducible experimental system. It is
suggested that some basic problems of the effect of the supply of mineral nutrients on the primary
reactions of virus replication could be studied by using the protoplast system. Attention has been
drawn to the fact the results obtained should be extrapolated very cautiously to entire plants.
Resume
On souligne)e fait que les resultats contradictoires obtenus quant au role des elements mineraux
chez les maladies des plantes et la resistance vis-a.-vis des maladies sont dus a. l'absence d'un dispositif
experimental reproductible. 11 est suggere que quelques problemes de base de l'effet de l'apport
d'elements mineraux sur les reactions primaires de la multiplication du virus pourraient etre etudies
en utilisant le systeme des protoplastes. L'attention est attiree sur le fait que les resultats obtenus
devraient etre extrapoles tres prudemment a. la plante entiere.
Investigations, at the biochemical level, on the role of mineral nutrients in plant
diseases and disease resistance have been hampered by the lack of reproducible experimental systems. This explains the high number of contradictory data summarized
among others by Kiraly [4] and Martin [5] in the present volume. To obtain reliable
results at the biochemical level the biological process to be studied (a) should be rapid,
(b) should occur in a system from which sufficient amount of material can be obtained
for detailed analytical work, and (c) should take place synchronously in a high number
of cells. Clearly, points (a) and (c) do not apply to most entire-plant host-parasite
systems, and partly this explains the contradictory results on the role of phenolics,
amino acids, enzymes etc. in plant diseases as affected by mineral nutrition.
In plant virology the successful use of virus-infected protoplasts as a new technique for
studying the biochemical aspects of virus replication raised hopes which have at least
partially been fulfilled [8, 9]. In a suspension of protoplasts (plant cells from which
the cell walls have been removed by pectolytic and cellulolytic enzymes) the individual
'cells' can be infected simultaneously with viruses and virus replication takes place
rapidly and synchronously in them [8,9].
217
Since the present-day techniques make the isolation of sufficiently large amount of
protoplasts possible the requirements listed above (a--c) are fulfilled by this system.
This has been proved by the successful application of plant protoplasts at least in some
areas such as the primary events of virus replication [1,8,9], selection of virus-free
material [3] etc. Therefore, the question arises whether or not the protoplast/virus
system could be used for studying the role of mineral nutrition in disease development
in plants. The aim of the present discussion is to entertain this idea.
One should be cautious in making predictions. Still, it seems very likely that the effect
of the level of various of mineral nutrients (ratios of various nutrients) on well defined
steps of virus replication could certainly be studied with a much better reliability in
protoplasts than in an entire plant system. On the other hand, we should be aware that
the effect of nutrients on the whole plant is complex since the nutrients affect the disease
situations often through a chain of reactions associated with growth and developlpent.
Therefore, one should not be over optimistic: the protoplast system can be used and
should be used only in studies on primary effects of macro and micro elements on virus
replication in context of cell/virus relationships. These effects may not necessarily be
the same as those exerted on the final outcome of a disease situation in an entire plant
system but at least they can be expected to be reproducible and they can be used to try
to distinguish primary effects from secondary ones.
i am not aware of any work on protoplast and cell cultures which has been done with
this purpose in mind. As a matter of fact, the media which are used for maintaining the
protoplast cultures are empirical in nature [8] and systemic studies on the effect of
changes in the composition of the culture medium (mineral nutrients) on the protoplasts and on the virus multiplication occurring in them are warranted. In spite of the
fact that the urgent need for this kind of work had been pointed out [8], no effort has
been made to establish the optimal ratios and/or to clarify the exact role of macroand micro elements in healthy and/or virus-infected protoplast cultures.
There is, however, good evidence that the plant cell culture technique can be applied
successfully to solve problems related with mineral nutrition. By using selective
pressure in liquid cell culture (high salt medium) salt tolerant cell lines have been
obtained [2, 6]. These selected lines respond differently to high levels of NaCI as
compared to the original ones. This result suggests that if entire plants differring in
their properties to respond to certain level of the nutrients can be regenerated, they
may perhaps be used in the future to separate the effect of a particular nutrient on
plant development and disease development per se.
References
1. Aoki, S. and Takebe, I.: Replication of tobacco mosaic virus RNA in tobacco mesophyll protoplasts inoculated in vitro. Virology 65, 343-354 (1975).
2. Dix, P.J. and Street, H.E.: Sodium chloride-resistant cultured cell lines from Nicotiana sylvestris
and Capsicum annuum. Plant Sci. Letters 5,231-237 (1975).
3. Farkas, C.L.: Protoplasts: a new tool in plant virus research. In: 'Cell Genetics in Higher Plants',
ed. by D. Dudits, C.L. Farkas and P. Maliga. Proceedings of a UNDP/UNESCO/ICRO Training
Course, Szeged, Hungary, 1976. Publishing House of the Hungarian Academy of Sciences,
pp. 207-21 8.
4. Kiraly, 2.: Plant disease resistance as influenced by biochemical effects of nutrients in fertilizers.
12th Colloquium of the Internat. Potash Inst., Izmir-Turkey (1976).
5. Martin, c.: Nutrition and virus diseases of plants. 12th Colloquium of the Internat. Potash Inst.,
Izmir-Turkey (1976).
218
6. Nabors, M. W., Daniels, A., Nadolny, L. and Brown, c.: Sodium chloride tolerant lines of tobacco
cells. Plant Sci. Letters, 4, 155-159 (1975).
7. Sakai, F. and Takebe, I.: Protein synthesis in tobacco mesophyll protoplasts induced by tobacco
mosaic virus infection. Virology, 62, 426-433 (1974).
8. Takebe, I.: The use of protoplasts in plant virology. Ann. Rev. Phytopathol. 13,105-125 (1975).
9. Zaitlin, M. and Beachy, R.N.: The use of protop lasts and separated cells .in plant virus research.
Adv. Virus Res. 19, 1-35 (1974).
i
f
219
Bacterial Diseases and Plant Nutrition
Dr. Ride, Angers/France, who was to have spoken on this subject found it impossible
to attend the Colloquium and to fill the gap, Prof. F. Grossmann and Dr. J. Ponchet
agreed to share in improvising a contribution, the latter dealing with general considerations, the former with the relationships between plant nutrition and pathogenesis in
main types of bacterial diseases.
Outlines of Host-Parasite Interactions in Bacterial
Diseases in Relation to Plant Nutrition
Prof. F. Grossmann, Institute of Phytomedicine, Hohenheim University, Stuttgart/Federal Republic
of Germany
Summary
An attempt has been made, using several types of bacterial diseases, to elucidate the influence of
mineral nutrients for hoH on pathogenesis. Certainly the picture has been oversimplified. As this
Colloquium has shown with other groups of pathogens, too, the relationships between nutrition and
disease development are extremely complex and it is thus very difficult to give precise advice as to
how, under practical conditions, disease incidence might be limited through fertilizer treatment.
Resume
En prenant comme exemple quelques types de maladies bacteriennes des vegetaux, on a essaye de
montrer l'jnfluence des elements nutritifs mineraux sur la pathogenese. Sans doute, ce schema est-il
considerablement simplifie. Comme ce Colloque l'a egalement montre pour d'autres groupes d'agents
pathogenes, les relations entre l'approvisionnement en elements nutritifs et le developpement de la
maladie sont extremement complexes, et il est tres difficile de formuler des recommandations permettant de limiter avec une certaine silrete l'attaque par les maladies dans la pratique a l'aide de la
fumure.
Unfortunately, the main paper dealing with 'Bacterial Diseases and the Nutrition of
Plants' has been withdrawn. Therefore the author will attempt a short survey of the
interrelationships between plant nutrition and host-parasite interactions in bacterial
diseases of plants. For this purpose bacterial diseases of plants may be rougWy
classified into four main types:1.
2.
3.
4.
Leaf spot diseases
Soft rots
Vascular diseases
Tumor-inducing diseases
Withil). these classes the individual diseases are generally similar in appearance and
pathogenesis. Nevertheless the boundaries between the groups are not sharply defined;
for example leaf spot and vascular diseases merge into one another.
221
1. Leaf spot diseases
Numerous diseases belong to this group, mainly caused by species of Pseudomonas and
Xanthomonas. Wildfire in tobacco and halo blight of beans may be quoted as examples.
The causal agents enter the plant in most cases through the stomata and in this connection the structure of the stomata and, particularly, their opening mechanism is
important. The pathogens can only enter when the stomata are open. There has for a
long time been evidence that the closing of the stomata is delayed in potassium deficiency and thereby the danger of infection is increased (Volk [1931]). The same holds
true for nitrogen excess (Volk and Tiemann [1927]; Poskuta and Indeka [1968],
Matthee and Daines [1969]).
Following penetration, the bacteria spread and multiply in the intercellular spaces and
this is favoured by water-soaking of the tissues. Leaves of potassium deficient plants
are more susceptible to water soaking and thus favour the development of the disease
(Allington and Johnson [1942], Mattheeand Daines [1969]). Liability to water soaking
depends to a great deal on the stability and permeability of the cell membranes. The
same applies to nutrient supply to the bacteria in the intercellular spaces, an adequate
nutrient supply being essential for their multiplication. Calcium has a stabilising effect
on the cell membranes. Accordingly, there are findings which show that increasing
calcium supply increases resistance to various bacterial leaf spot diseases ( Sacco [1946],
Dimond et al. [1952]).
In many cases, toxins elaborated by the causal agents of leaf spot diseases play an
important part. This holds true, for example, for tobacco wildfire and halo blight of
beans mentioned above. One could well imagine that toxin production would be
affected by nutritional conditions in the plant though there is, so far, little concrete
evidence on this point.
Summarising results available in the literature on bacterial leaf spot diseases, it seems
that as a general rule resistance is lowered by potassium deficiency and nitrogen excess
(cf. Fuchs and Grossmann [1972]). During this Colloquium 1smunadji drew attention
to such a connection in the case of bacterial leaf blight of rice (Xanthomonas oryzae).
However there seem to be exceptions; Kiraty pointed out yesterday that high nitrogen
dressings reduced attack of tomatoes by Xanthomonas vesicatoria. But, in this connection, it should be mentioned that earlier work by Nayudu and Walker [1960] has
shown that the improved resistance may not be ascribed to increased nitrogen supply as
such but rather to the increase in osmotic pressure in the nutrient solution which is one
consequence of the increased N supply.
On the other hand, under field conditions a number of microclimatic factors are
important and these also can be influenced by fertilization.
2. Soft rots
Typical diseases of this kind ·are wet rot and blackleg in potatoes caused by Erwinia
spp. Soft rots are found in many other crops, too.
The causal organisms enter the tissues through wounds and thus the intensity and
speed of wound healing are of great importance. The formation of wound cork is
accelerated by high potassium supply and at the same time symptoms of soft rot in
Brassicae are reduced (Leltchs [1959]). In agreement with this, Kirttly showed in his
222
paper that potassium deficiency delayed wound healing. Thomson et al. [1975] reported
that high nitrogen resulted in more growth cracks in sugar beet which in turn led to an
increase in rot caused by Erwinia sp.
Regarding the spread of infection in the plant, the middle lamella between the cells is
dissolved by pectolytic enzymes, such as polygalacturonase, secreted by the bacteria,
As a result, the structure of the tissues is destroyed leading to the appearance of soft
rot symptoms. The breakdown of the middle lamella is inhibited by high calcium
content in the pectins. Thus, resistance to bacterial soft rot is improved by high
calcium supply as, for example, has been established in the cases of Erwinia attack on
shoots of tomato and tobacco (Stapp and Hartwich [1957]) as well as on bean plants
(Platero and Tejerina [1976]). Kivilaan and Scheffer [1958] obtained similar results
for bacterial stem rot in Pelargonium.
3. Vascular diseases
These diseases are of widespread importance, especially in warm countries. For
example, slime disease caused by Pseudomonas solanacearum is responsible for serious
losses in tobacco, potato and many other crops. Corynebacterium spp. also cause
various diseases of this type. Because of the predominant symptoms these are often
called bacterial wilts.
The causal agents enter the plants partly through the aerial parts but mainly from the
soil via the roots, entry being facilitated by wounding. Regarding wound healing, the
same considerations apply as in the case of the soft rots.
The disease develops in the plant initially by spreading of the bacteria through the
xylem vessels. Sufficient water and mineral nutrients'are available in the vessels for the
development of the bacteria, but supplies of carbohydrate and nitrogenous compounds
may be the main controlling factors. Several vascular bacteria are favoured by high
nutrient supply to the host, e.g. Corynebacterium michiganense in tomato (Walker and
Kendrick [1948]), while others like Pseudomonas solanacearum (Gallegly and Walker
[ 1949) ) behave in the reverse direction. This may be because the first group of parasites
requires a source of organic nitrogen (Wei et al. [1952]) and, therefore, their nutrition
depends on anabolic processes in the host while the second group can live on inorganic
nitrogen and in this case there is, possibly, direct competition between parasites and
hosts for available nitrogen within the vessels in which the bacteria may take the upper
hand.
Typical attacks result in the formation of slime in the vessels whose contents become
viscous. This hinders the transport of water and nutrients. So far, no concrete data
seem to exist on the influence of host nutrition on slime formation.
In the later stages of the disease the bacteria migrate out of the -vessels and destroy the
neighbouring tissues. At this stage conditions are similar to those in the soft rots and
calcium improves resistance. Ponchet has told me that in recent work by Messiaen et al.
promising results against Pseudomonas solanacearum in tomato have been obtained by
calcium fertilization.
223
4. Tumor-inducing diseases
A good example of this type of disease is crown gall caused by Agrobacterium tumefaciens. Despite many investigations, the pathogenesis of this disease is still not fully
understood. Thus, sporadic examples of nutrient effects can hardly be interpreted.
Sulphur or sulphate is said to reduce tumor formation in castor plants (Verona [45 j).
According to Hussin and Deep [1965 j, the development of tumors in sweet cherries
and tomatoes is prevented by boron deficiency; this might be explained by interference with the carbohydrate transport.
References
I. Allington, W B. and Johnson, J.: The relation of potassium to watersoaking of tobacco. Phytopathology 32, I (1942).
2. Dimond, A.E., Stoddard, E.M. and Chapman, R.A.: Chemotherapeutic investigations on the
common bacterial blight of beans. Phytopathology 42,72-76 (1952).
3. Fuchs, W.H. und Grossmann, F.: Ernahrung und Resistenz von Kulturpflanzen gegeniiber
Krankheitserregern und Schadlingen. In: H.Linser (Herausg.), Handbuch der Pflanzenernahrung und Diingung, Bd.I, 1007-1107. Springer-Verlag, Wien und New York, 1972.
4. Gallegly, M.E., Jr., and Walker, J. C: Plant nutrition in relation to disease development. V.
Bacterial wilt of tomato. Amer. J. Bot. 36, 613 - 623 (1949).
5. Hussin, H. and Deep, I. W.: Effect of mineral nutrition on development of crown gall on Bonny
Best tomato and Mazzard cherry. Phytopathology 55, 575-578 (1965).
6. Xivi/aan, A. and Scheffer, R.P.: Factors affecting development of bacterial stem rot of Pelargonium. Phytopathology 48, 185-191 (1958).
7. Leuchs, F.: Ober Beziehungen zwischen Faulniserscheinungen, Wundheilung und Kaliversorgung an Rosenkoh!. Z. Pfl.-Krankh. Pfl.-Path., Pfl.-Schutz 66, 499-508 (1959).
8. Matthee, F.N. and Daines, R.H.: The influence of nutrition on susceptibility peach foliage to
water congestion and infection by Xanthomonas pruni. Phytopathology 59, 285-287 (1969).
8. Nayudu, M. V. and Walker, J. C: Bacterial spot of tomato as influence by temperature and by
age and nutrition of the host. Phytopathology 50, 360-364 (1960).
10. Platero, M. and Tejerina, G.: Calcium nutrition in Phaseolus vulgaris in relation to its resistance
to Erwinia carotovora. Phytopath. Z. 85, 314-319 (1976).
11. Poskuta, J. and 1ndeka, L.: The movement of stomata of maize leaves as influenced by the age,
nitrogen nutrition and growth regulators. Bull. Acad. Poloz. Sci. 16, 779-782 (1968).
12. Sacco, P.: Mineral absorption and resistance to wildfire in tobacco. Pub!. Pa. State Coll. 901
(1946); Rev. app!. Myco!. 29, 232 (1950).
13. Stapp, C and Hartwich, W.: Zur Frage der Resistenzverschiedenheiten pflanzlicher Wirte
gegeniiber pathogenen Bakterien und ihre Ursachen. Ill. Faktoren von Virulenzeinfluss auf
Erwinia phytophthora. Zb!. Bakt., Abt. H, 110, 449-470 (1957).
14. Thomson, S. V., Hills, FJ. and Schroth, M.N.: Cultural procedures to reduce bacterial vascular
necrosis and rot of sugarbeet. Proc. Amer. Phytopath. Soc. 2, 119 (1975).
15. Verona, 0.: Azione repressiva sullo sviluppo dei tumori dovuti a Bact. tumefaciens dallo zolfo
somministrato al terreno. Ann. Fac. agr. R. Univ. Pisa, N.S., 6, 7pp. (1945); Rev. app!. Myco!. 26,
237 (1947).
J 6. Volk, A.: Einfliisse des Bodens, der Luft und des Lichtes auf die Empfanglichkeit der Pflanzen
flir Krankheiten. Phytopath. Z. 3, 1-88 (1931).
17. Volk, A. und Tiemann, E.: Zur Anatomie verschieden ernahrter Pflanzen. Forsch. Geb. Pflanzenkrankh. Immunitat im Pflanzenreich, 3. Heft, 45-79 (1927).
18. Walker, J. C. and Kendrick, J. B., Jr.: Plant nutrition in relation to disease development.
IV. Bacterial canker of tomato. Amer. J. Bot. 35, 186-192 (1948).
19. Wei, CT., Walker, J.G. and Scheffer, R.P.: Plant nutrition in relation to disease development.
VII. Cucurbit wilts. Amer. J. Bot. 39, 245 - 249 (1952).
224
Etiology and Physiology of Bacterial Diseases
Dr. J.Ponchet, Head, Department of Plant Pathology, INRA, Antibes/France
Summary
The knowledge of the several characteristic features of plant infection by pathogenic ,bacteria is
essential to the understanding of host - parasite relationship and their interactions with nutrition.
The development of bacterial infection is closely linked with host physiology and it may be supposed
therefore; that nutrient balance would play an essential part in the infection process.
The author distinguishes a latent, epiphytic phase. The infection actually takes place only if the
concentration of the nearly always founded pathogenic bacteria on the plants organs is raised above
a threshold level and if the host is receptive. Following inoculation the tissues lose electrolytes, more
potassium than calcium, phosphorus, nitrogen or magnesium. The host metabolism mobilises its
resources to oppose the invasion. Frost damage which facilitates the infection of fruits can be
lessened by a generous potassium supply. The author discusses the question: how can the means
used by the plant to resist infection be improved by adequate nutrition?
Much more research, in which physiologists and bacteriologists should collaborate, is needed about
the internal mechanisms involved in the host-parasite interaction for better determination of the
nutritional needs of crops.
Resume
La connaissance des caracteristiques de l'infection des plantes par des bacteries pathogenessemble
etre essentielle pour la comprehension des relations entre plante-hote et parasite et de leurs interactions avec la nutrition. Le developpement de I'infection bacterienne est etroitement lie ala physiologie de la pJante-hote. Ainsi on peut supposer que le bilan des elements nutritifs peut jouerun role
e,sentiel dans le processus d'infection.
.
L'auteur distingue une phase epiphytique. Reellement l'infection a lieu seulement si sur les organes
de la plante la concentration des bacteries pathogenes, qui s'y trouvent presque toujours, depasse
une certaine valeur seuil et si la plante-hote est receptive. A la suite de I'infection, les tissues perdent
des electrolytes, plus de potassium que de calcium, phosphore, azote ou magnesium. Le metabolisme
de la plante-hote mobilise des ressources pour resister al'invasion. Les degiHs dus au gel, qui facilitent
I'infection peuvent etre reduits par des doses abondantes de potassium. L'auteur discute le theme
suivant: Comment les moyens utilises par la plante pour resister a I'infection peuvent-ils etre
ameliores par une bonne nutrition?
Beaucoup plus de recherches, auxquelles devraient collaborer les physiologistes et les bacteriologistes;
sur les mecanismes intervenant dans les interactions entre plante-hote et parasite sont donc necessaires afin de mieux determiner les besoins nutritifs des cultures.
The infection of plants by pathogenic bacteria has several characteristic features and a
knowledge of these is essential to the understanding of host-parasite relationships and
their interactions with nutrition. Pathogenic bacteria are few in number compared
with saprophytes whose important function, particularly in the soil, must not be
overlooked. The latter include bacteria wrnch fix atmospheric nitrogen for the plant
(Rhizobium spp.) or which make possible the nitrogen cycle in the soil. The form of
nitrogen available in the soil depends upon the species predominating and on the
composition of the medium and this can influence the physiology of the host plant and
thus its susceptibility (Huber [1970J). It is known that nitrites which accumulate when
the nitrifying flora has been destroyed by steam sterilisation of the soil are poisonous
to the plant.
225
Few pathogenic bacteria live in the soil; they are carried in the air or in water, on the
seed and on crop residues.
The development of bacterial infection is closely linked with host physiology and it
may be supposed, therefore, that nutrient balance would play an essential part in the
infective process.
1. Latent epiphytic phase
Pathogenic bacteria are often found on the organs of apparently quite healthy plants.
Cameron [1971] cites several examples: Pseudomonas syringae, Erwinia amylovora,
Agrobacterilim tumefaciens. In the case of Pseudomonas mors prunorum f sp. persicae
for example, Gardan [1970] and Luisetti [1973] have shown that peach leaves carry
the parasite outside periods of infection (10 3 or 104 bacteria per leaf). The bacteria
multiply on the surface and can attain 106 per leaf or per flower under favourable
conditions. The higher the concentration is raised above a threshold level the more
necroses will be apparent and the more rapidly will they spread. Leaf exudates and
environmental conditions affect multiplication, but infection does not actually take
place unless the host is receptive.
2. Host susceptibility
Infection sites comprise stomata or natural wounds (petiole scars after leaf fall) or
wounds caused by frost, abrasions, cultural operations etc.
We know little of metabolic changes caused by wounds and even less about their
possible role in the process of infection (Cameron [1971]). Frost damage, which
facilitates the infection of pears or apricots by Pseudomonas syringae can be lessened by
a generous potassium supply which raises the tissue sugar content thus reducing their
sensitivity to low temperature, as mentioned by Kiraly (see chapter 1 of these proceedings).
That the development of susceptibility can result from nutrient disequilibrium has been
shown by Lemattre [1973] in the cases of Saintpaulia and Pelargonium.
Sensitivity to latent infection can be increased by variation in environmental factors
such as humidity, which affects turgidity, or temperature (Nayudu [1960]) or lighting
conditions (Cook [1971]). Several authors have concluded that ageing has an effect,
plant tissues generally becoming more resistant with increasing age.
3. Nutrition and the defence mechanism of the plant
Most of the factors which condition the result of a bacterial infection are related to the
physiology of the host and its variations; it is probable that they depend very much
upon nutrition.
As Cameron [1971] says, mineral nutrients have little effect upon the susceptibility of
plants unless they are deficient or present in excess. Grossmann will give below
several examples of such interactions, but it is impossible to deduce any generalised
conclusion.
226
We have to ask ourselves what are the means used by the plant to resist infection and
how can they be improved by good nutrition. The primary defence barriers are mechanical (closed stomata, cuticle) but it is not easy to see how nutrition can be concerned in
the'penetration phase, except perhaps by accelerating wound healing. Having entered
the plant, the bacteria may find obstacles to their multiplication in the tissues in the
form of induced substances. As has been well defined by Klement [1971] induced
resistance comprises premunity, protective reaction triggered by filtrates from dead
bacteria and hypersensitivity caused by incompatibility between parasite and host
showing itself in rapid destruction (8-10 h) of the cells surrounding the site of infection
which completely prevents further penetration by the infecting agent. The hypersensitive reaction is induced by one or more proteins of high molecular weight
elaborated by the bacterial cell (Sequiera [l971]). Following inoculation the tissues
lose electrolytes, more potassium than calcium, phosphorus, nitrogen or magnesium
(Cook [1971]). Clearly, host metabolism is actively concerned and it mobilises its
resources to oppose the invasion; thus further detailed study of these reactions is
needed to find means of improving host resistance. The bactericidal substances
produced by the cells may be phenols or quinones but little work has been devoted to
their identification and we know very little about these matters and the way in which
they may be involved in the improvement of yield through cultural measures or
through fertilisation.
Much more research, in which physiologists and bacteriologists should collaborate,
is needed, as the more is known about the internal mechanisms involved in the hostparasite interaction the more we are likely to be able to use this knowledge in better
defining the nutritional needs of cultivated crops.
References
.1. Cameron, H. R.: Relationship of host metabolism to bacterial infection. Proc. 3rd intern. Conf.
on Plant Pathogenic Bacteria, Wageningen, 59-61 (1971).
2. Cook, A. A.: Alteration of hypersensitivity in plants to bacterial infection. Proc. 3rd intern. Conf.
on Plant Pathogenic Bacteria, Wageningen, 171-178 (1971).
3. Gardan, L., Prunier, J.P. and Luisetti, J.: Recherche et etude des variations de Pseudonomas mors
prunorumf sp. persicae. Influence de la dose d'inocu1um. Ann. PhytopathoJ. 5, 4, 347-353 (1972).
4. Huber, D. M. and Wafson, R.D.: Effect of organic amendment on 'soil-borne plant pathogens.
Phytopathology 60, 22-26 (1970).
5. Klemenf, Z.: Development of hypersensitivity reaction induced by plant pathogenic bacteria.
Proc. 3rd intern. Conf. Plant Pathogenic Bacteria, Wageningen 157-164(1971).
6. Lemattre, M.: Evolution des maladies bacteriennes en cultures f1orales. Horticulture fran~aise,
11-25 (1973).
7. Luisefti, J., Gardan, L. and Prunier, J.P.: Etude du pouvoir pathogime de Pseudomonas mors
, prunorumf sp. persicae. Influence de la dose d'inoculum. Ann. Phytopathol. 5, 4, 347-353 (1973).
8. Nayudu, M. V. and Walker, J. c.: Bacterial spot of tomato as influenced by temperature and age
and nutrition of the host. Phytopathology 50, 360-364 (1960).
9. Sequiera, L.: Prevention of hypersensitive reaction.' Proc. 3rd intern. Conf. Plant. Pathogenic
Bacteria, Wageningen (1971).
227
Report of the Co-ordinator of the 3rd Session
G.Drouineau, Conseiller scientifique, Institut National de la Recherche agronomique(INRA),
Paris/France; member of the Scientific Board of JPI
The first part of this session was devoted to the relationships between the mineral
nutrition of plants and virus diseases.
Following a survey of the ideas involved in modern molecular biology by Professor
Mengel, Dr. Martin dealt with the whole problem of the interaction virus: mineral
nutrition underlining the biochemical aspects of these interactions as they affected
growth and development.
We can distinguish different ways in which the relation between virus and the physiology and nutrition of the plant may be of importance. The expression of symptoms is,
one thing, susceptibility to virus is another. We need to know the conditions which
favour virus multiplication which depend upon the metabolism of the cell, which in
turn is totally dependent upon nutrition.
.
We cannot make progress in the study of the physiological relationships of virus
without research into cell biochemistry and Dr. Martin has particularly studied the
phenomenon of hyper-sensitivity. It seems now that the number of local lesions
increases with N supply to the plant but, in this sense, susceptibility is only increased
to the extent that nitrogen increases growth. Nand P are concerned in the multiplication of virus. Virus control is based on phytosanitary selection and fertilizer use is
important in this context.
Meristem culture makes it possible to obtain virus free stocks and the development of
this technique involves research into the composition of culture media which varies
according to the species we are trying to multiply. It has been found that the potassium
concentration required for meristem culture is ten times as high as that needed for
growing entire plants or plant organs in artificial media.
The paper of A. Schepers and A. B. R. Beemster dealt with virus in potatoes., The
resistance of the plant determines to what extent the tubers, which wiII be used for seed,
become infected. Plant resistance increases with maturity and Nand P have opposing
effects on this. Potassium has little influence on the resistance of mature plants.
M.Babovic and Professor D.J.Jelenic dealt with lucerne virus in Jugoslavia as it is
affected by soil type and with the effects on yield. On two soils - chernozem and
smonitsa - the progress of infection is very different, rapid in the first case, slow in the
second. This interesting example of the effect of ecological conditions is ascribed by
them to the influence of nitrogen.
We can conclude from that part of the session dealing with virus that fertilization can
229
modify sensitivity to virus and the reproduction of virus particles in the cells and
tissues of cultivated plants. This comes about through effects on the metabolism of the
host. Virus is a typical obligate parasite with imperfect metabolism. Its biosynthesis is
absolutely dependent upon the nucleotides and amino acids of the host. Thus it is
necessary to understand the mechanisms involved and the part played by nutrient
elements in the fundamental processes of plant metabolism. This understanding is
needed in order that we may thoroughly test the various hypotheses which have been
advanced to explain the phenomena of susceptibility and resistance. In this area, the
ideas advanced by Dr. Farkas on the possibilities of using protoplast culture are
particularly interesting.
The second part of the session was devoted to a brief review of the relation between
mineral nutrition and bacterial diseases of plants by Professor Grossmann and Dr.
Ponchet. No other papers were contributed. Bacteria are facultative parasites, infection
by which depends on several predisposing factors:
- Physiological state of the host
- Presence of wounds in host tissue
- Nutrient status of the host.
In general, infection is a function of multiplication of bacteria on or around the
infection sites. The notion of inoculum threshold is very important, bacteria remaining
latent if the threshold is not attained or if the potential infection sites are not receptive.
Four types of bacteria have been distinguished: leaf blotch, soft rot, tracheo-bacteria
and tumours. Wounds (potential infection sites) can be caused accidentally (cuts, frost
damage, insect damage) or naturally (scars after leaf fall).
It has been demonstrated that calcium supply influences susceptibility to pectinolytic
bacteria by increasing resistance to enzymes that attack plant membranes (polygalacturonases) but the effects vary according to the enzyme systems concerned.
Nitrogen generally increases susceptibility to bacteria, while phosphorus has no definite effect. Potassium increases resistance, particularly to Xanthomonas and Pseudomonas. An increase in the sugar content of the cells reduces the effect of frost damage
which is the main cause of Pseudomonas attack in fruit trees.
There are no precise data on the effect of fertilization on the development of disease
caused by mycoplasma.
230
4th Session
Co-ordinator:
Fertilizer Use and Plant
Health: Pests
Prof. Dr. D.Schroeder, Institute of Plant Nutrition and Soil Science, Christian-AlbrechtUniversity, Kiel/Federal Republic of Germany;
member of the Scientific Board of the International Potash Institute
Pests, Resistance and Fertilizers
F. G. W. Jones, M.A., Sc. D. (Cantab.), F.r. BioI., Rothamsted Experimental Station, Harpenden,
Herts./England
Summary
The relationship between crop plants and pests is dynamic and each pest-crop situation has unique
features. Pests include nematodes, slugs, arthropods, birds and mammals. Little work has been
done on the influence of fertilizers on plants attacked by slugs, birds and mammals. Resistance to
pests by plants includes escape, tolerance, non-preference, antibiosis and hypersensitivity. Host
finding, oviposition, feeding and real resistance (the last three categories) are mediated principally
by secondary plant products' and also by physical characters. The feeding of large pests is coarse and
not very selective. That by smaller pests is more discreet. Some pests burrow into plants and others
develop intimate relationships which include the induction of tissue changes essential to survival.
Such relationships can be upset by single gene changes in the host but resistance based on polygenes
is likely to te more permanent.
Literature citations of the effects of N, P and K on pest numbers indicate that the usual response
to N is an increase, probably because N increases the food supply. Leaf feeding pests in forests
behave unusually: nitrogen application decreases their numbers markedly. The effects of P and K
vary and lead to increases, decreases or no apparent change, in equal proportions. Detailed studies,
mostly in the laboratory, have given very conflicting results possibly because many are unnatural.
In the field different ways of counting can produce opposed results. The evidence that organic
fertilizers decrease pest numbers and increase plant resistance is equivocal.
Experiments at Rothamsted provide no evidence that fertilizers increase plant resistance. However,
in Park Grass plots nitrogen applications decreased the numbers of all soil arthropods. In Barnfield the numbers of cyst-nematodes attacking mangolds is correlated better with yields than with
manurial treatments. Organic manures (dung and castor meal) have effects which seem to match
their content of N, P and K only. Other experiments underline the importance of nitrogen fertilizer
in increasing the yield of crops under attack.
The effect of pests above or below ground is to decrease the size of the root system and limit the
volume of soil an attacked plant can exploit for minerals, nitrogen and water. There is no evidence
that, in most pest-crop situations, fertilizers have more than a marginal effect in a plant's real
resistance to pests (non-preference, antibiosis or hypersensitivity). They operate more through mechanisms of escape and tolerance.
Resume
Les relations entre les plantes cultivees et les ravageurs sont dynamiques et toute situation ravageur/
plante cultivee est caractetisee par des faits uniques. Parmi les ravageurs on compte les nematodes,
limaces, arthropodes, oiseaux et mammiferes. On n'a effectue que peu d'etudes sur l'influence des
engrais sur les plantes attaquees par les limaces, les oiseaux et les mammiferes. La resistance des
plantes aux ravageurs peut etre subdivisee en les categories suivantes: echappement, tolerance, nonpreference, antibiose et hypersensibilite. La recherche de I'h6te, l'oviposition, la nutrition et la resistance reelle sont conditionnees principalement par des produits vegetaux secondaires et, egalement,
par des caracteristiques physiques.
.233
Les grands ravageurs s'alimentent de fac;on grossiere et pas tres selective; la nutrition des ravageurs
plus petits est plus discrete. Certains ravageurs se creusent it I'interieur des plantes tandis que d'autres developpent des rapports intimes qui comprennent egalement I'induction d'alteration des tissus
qui sont essentielles it la survie. De tels rapports peuvent etre renverses par des changements de
genes individuels chez l'hote, mais la resistance basee sur des polygenes peut etre consideree
comme plus permanente.
Selon la litterature sur les effets de N, Pet K sur le nombre de ravageurs, la reponse it Nest habituellement constituee par un accroissement, probablement parce que N intensifie I'alimentation. Les
ravageurs des feuilles d 'essences forestieres se comportent contrairement: I'apport de N provoque
une diminution de leur nombre. Les effets de P et K varient et provoquent des accroissements, des
diminutions ou pas du tout de changements apparents, et cela en proportions egales. Des etudes
detaillees, effectuees pour la plupart au laboratoire, ont donne des resultats tres contradictoires,
probablement parce qu'un grand nombre d'entre elles sont effectuees en conditions non naturelles.
En plein champ, les differentes methodes de comptage peuvent produire des resultats contradictoires.
La preuve que les engrais organiques reduisent le nombre des ravageurs et augmentent la resistance
des plantes est equivoque.
Les essais effectues it Rothamsted n'ont pas fourni I'evidence que les engrais augmentent la resistance des plantes. Cependant, sur des parcelles de gazon 1'apport d'azote a provoque une reduction
des tous les types d'arthropodes du sol. A Barnfield le nombre de cystonematodes attaquant les
betteraves est en meilleure correlation avec les rendements que ne le sont les traitements fertilisants.
Les engrais organiques (fumier et farine de chataignes) ont des effets qui semblent dus uniquement
itleurs teneurs en N, Pet K. D'autres essais soulignent I'importance des engrais azotes en vue d'accroitre les rendements de cultures attaquees par des ravageurs.
L'effet de l'attaque aerienne ou souterraine des ravageurs est de reduire le volume du systeme
racinaire des plantes et de limiter le volume de sol qu'une pIante peut exploiter en vue d'absorber
des elements minhaux, de l'azote et de I'eau. JI n'existe pas de preuves - et ceci se rapporte it la
majorite des situations ravageurs/plante cultivee - que les engrais auraient des effets plus que marginaux sur la resistance reelle des plantes envers les ravageurs (non-preference, antibiose ou hypersensibilite). lls exercent leur action plutot en influenc;ant des mecanismes d'echappement et de
tolerance.
1. Introduction
The relationships between crop plants and the pests that attack them and decrease
yield or adversely affect quality, are complex, dynamic and quantitatively very variable.
The factors controlling the relationship are of two types; those that are relatively
constant for any specific pest-crop situation and those that are variable. Constant
factors include the growth pattern of the crop, the nature of the injury inflicted and its
characteristic distribution pattern on and between plants. Variable factors include time
of attack in relation to plant growth, the intensity of injuries caused, the duration of
the attack and environmental factors affecting plant growth (Bardner and Fletcher
[6]). To these must be added the population density of the pest attacking and the rate
at which it feeds and multiplies. The farmer has under his control previous cropping,
which determines the number of non-migratory pests in situ before a crop is planted,
the planting date, seed rate, fertilizer application, certain cultural practices and,
nowadays, a range of pesticides to quell an attack should it get out of hand. The factors
he cannot control are variations in the time of attack by immigrant pests, the weather
and the inherent characteristics of the soil.
To provide a background to the ways in which fertilizers may influence the pest-crop
situation in favour of the crop, some salient features of pests, the effects of their feeding
on crop plants and the ways in which the plants resist attack are considered. Evidence
of the influence of nutrients on pest numbers and on the performance of the crop under
234
attack is reyiewed and some examples given of results from published and unpublished
work, and from substantial experiments at Rothamsted.
Pests are animals harmful to crops: they include species of nematodes, slugs, arthropods, (wood-lice, centipedes, symphyla, mites, insects), birds and mammals (Jones and
Jones [50]). Nematodes, slugs and arthropods other than adult insects are relatively
immobile whereas mammals and especially winged insects and birds are highly mobile
and able to find host plants over considerable distances. Work on the influence of
fertilizers is confined to insects, mites and nematodes; little has been done in relation to
slugs, birds or mammal pests.
2. Characteristics of pests
The ways in which pests differ from fungal, bacterial and viral pathogens, the results
of their co-evolution with their host plants and the origins of resistance to attack are
summarised in Table 1. Table 2 lists types of feeding and their effects.
The possession of digestive and excretory systems and the manner of feeding make
possible the acceptance of diets that vary widely in the proportions of the basic food
requirements (proteins, polypeptides, amino acids, carbohydrates) they contain. These
therefore play only a minor role in resistance, which is related mainly to secondary
plant substances that provide accessory compounds the pest has ceased to manufacture,
and triggers for its sensory system that interlock the life cycle of the pest with that of
its host plant. The production of substances toxic in various ways and the ability or
inability of the pest to deal with these is also an important component of some kinds of
resistance. Each pest, regardless of the group to which it belongs, has an individual life
style in such matters as adaptation to climate, number of generations a year, mechanisms for synchronising its life cycle with that of its host, method of surviving adverse
periods, maximum potential for increase and so on. Some pests are 'exploiters, multiplying rapidly to great numbers on the occasions when an abundant food supply presents itself, and surviving in small numbers between these events. Others multiply less
rapidly but maintain their populations with greater persistence and smaller fluctuations
from year to year. Mobile species invade their host crops each year and immobile ones
are present in the soil at planting as a residue from the previous crops.
The hypothetical pest archetype was an animal able to feed on any plant, since all are
able to supply water and the other basic food requirements if eaten in bulk. This
archetype discarded what it did not need, synthesised all the accessory substances it
required and detoxified any poisons it encountered. Such an archetype probably did
not and could not exist. Its great battery of physiological and biochemical mechanisms
would require a formidable genetic code to produce and manage. The pests from which
we suffer today are.the products of a long period of co-evolution with their respective
hosts resulting in many kinds of relationship and varying degrees of host specificity
(Beck [9]; Ehrlich and Raven [24]).
3. Types of resistance
Resistance in a plant host is of several types (Painter [77], [78]; Fowden, Jenkins and
Parrott [32]). Sometimes attack is avoided in whole or in part because the periods
of activity of the pest are not properly synchronised with the vulnerable stages of the
235
host. This is termed escape: examples are in Table 3 and Figure 1. Sometimes attack is
tolerated (tolerance) because the host is able to replace lost parts or lost neighbours by
compensatory growth (Figure 2), or by failing to react to virulent toxins which, in
susceptible plants, cause necrotic lesions (hypersensitivity). Some hosts are less heavily
attacked or avoided because of a deficiency in the train of stimuli that leads to feeding
or oviposition, or because they contain substances that deter or repel. This is usually
referred to as non-preference. Antibiosis occurs when the quality of food is inappropriate, nutrients are in the wrong proportions, the food is unpalatable, sticky hairs or
other morphological impediments are present, there is an excess of fibre or harmful
toxins that interfere with growth and reproduction.
Table 1 A Characteristics of pests that distinguish them from fungal, bacterial and viral pathogens
Larger size
Limiting membranes impervious to food substances
Feeding via the mouth only
Possession of a digestive system
Possession of an excretory system
Possession of a sensory system and behaviour patterns
B Effects oJ co-evolution with their host plants
Specialisations
- method of feeding
- host finding
- physiological
- ability to detoxify poisons
- need for accessory substances
- need for sensory triggers
C Origins oJ resistance in host plants
Physical
Mechanical
Chemical/Biochemical
Table 2
- microclimatic, morphological
- fibres, Si0 2
- toxins, non-production of key substances,
production of deterrents and repellents
Types of feeding and their effects
Mechanisms
Position
Effects
Biting
Rasping
Piercing and sucking
- superficial
- deep
Exposed
Concealed
- below ground
- within buds
- within mines
Mechanical
Nutritional
Causing tissue changes
- galls
- transfer cell systems
- dissolution of middle lamellae
Note: This table is to read downwards only.
236
Table 3. Escape from attack: the relation between frit fly attack and sowing date of spring oats in
the U.K. (Petherbridge [79})
Sowing date
Percentage of tillers attacked
o
February 1st
20th
.
.
Mamhl~
.
.
.
.
20
.
32
15th
23~
31st
April 14th
trace
trace
trace
10
Note: plants cease to be attractive for egg laying after the first leaf expands.
60
,...
Early carrots
0
'0
Late carrots
Q;
0.
0-
c
40
t"
'E"
'"
:;;
;:::
20
0'
Q;
J:>
E
"
Z
.0 Feb
Mar
Apl
May June July
Auq
Sept
Oct
N.ov
Fig. 1. Manipulation of carrot plantings to obtain partial escape from carrot fly attack. 'Early
sowings are well developed when first generation flies migrate into the field. Late sowings avoid the
first generation and suffer only the second which must migrate. Main crop carrots are attacked by
the first generation and more heavily by the second which is produced in the field. After Petherbridge and Wright [80}.
.
Of these kinds of resistance, non-preference is the most advantageous in that it reduces
the amount of feeding or prevents it altogether and so the host suffers little or no
damage and large populations of the pest do not develop. Escape is a precarious type
of resistance. Its successful exploitation depends on the skill of the farmer and the
vagaries of the weather. Tolerance allows large populations to breed which endanger
susceptible cultivars. Antibiosis, like non-preference, is a matter of degree, when weak
the crop may be fed upon and yield lost but usually the pest's reproductive capacity is
diminished and control by pesticide or other means is facilitated.
237
e _ _• ___
100
.---------.~
.
None
Pro;x:;.rtion
[
I
1
V4
Y2
+'4
All
of leaf Slrfoce destroyed. 4- to B- leaf stage
A
o
N;I
1'4
h
Proportion of plcnt population deslrOfed.
¥.!
singling
All
stage
B
Fig. 2. A. Compensation in sugar beet after defoliation in the seedling stage.
B. Compensation in sugar beet after loss of seedlings in the singling stage. 0-0, yield expected
without compensation. e-e, yield obtained, losses regular. ---, Anticipated effect of irregular
losses caused by pests. After Jones et al. [49].
4. Host finding, feeding and oviposition
In the sequence of events that begins with host finding and ends with feeding or with
egg laying, the pest receives a number of stimuli from the host in a definite sequence.
First, volatile substances may be perceived at great dilution that initiate searching
(excitants). Reactions to the same or different odours may direct the animal to its
host, where arrestants ensure that it stays, incitants initiate biting or piercing and
sucking and feeding stimulants prolong feeding until appetite is satisfied. A similar
sequence ends in oviposition. Deterrents and repellents may be produced that interfere
with host finding, feeding or oviposition. In feeding and egg laying, physical stimuli
also play a part and may include appreciation of shape and form, surface texture,
hairiness and resistance to biting or piercing (by mouth parts or ovipositor). Gross
physical differences e. g. in the shape and distribution of plant organs, may also affect
the issue. For a review of all these factors see Hedin, Maxwell and Jenkins [37].
It is conceivable that in a relatively simple but highly adapted pest, one volatile
chemical might mediate all stages up to the initiation offeeding or oviposition. In most
pests, however, a galaxy of stimuli, chemical and physical, olfactory and gustatory
seem to be needed. These enable a pest with catholic tastes to find one or other of many
hosts, or a more specialised pest with a few related hosts in one plant family to find
them amongst many others. Moreover, whether the pest feeds on many or a few hosts,
the stimuli direct it to a particular part of its host, for few feed on all parts. Since the
stimuli must have a measure of specificity, they are drawn from secondary plant components, e. g. terpenoids, acetogens, alkaloids and phenylpropanes (Klun [55]),
which the host and its allies have acquired during evolution and to which the pest has
become conditioned during its co-evolution. (Ehrlich and Raven [24]).
238
5. Types of crop
Crops fall into two groups: those raised from seed and those raised from tubers,
transplants, runners, bulbs, etc. Some crops (e. g. brassicas, tobacco,leeks, celery, and
onion [sets]) are all sown in seed beds and are transplanted later and therefore fall into
both groups. Most seeds, especially small ones, are vulnerable when first sown. Large
seeds, tubers, transplants and bulbs are less vulnerable because they represent more
plant material and so, in establishing root and shoot systems, are better able to replace
roots or buds that are destroyed. An example of the great range of pests* a crop may
experience is in Table 4 and the type of damage they cause is illustrated in Figure 3.
For crops raised from seed, the most critical stage is during and just after germination.
If the main shoot is severed, the plant may die. The progressive resistance acquired
with growth is illustrated for winter wheat and the wheat bulb fly in Table 5. This is
because, after a certain stage tillering produces extra stems that can replace any lost
(Jessup [44]). However, some plants produce a great excess of flowers e.g. cotton; coconut palm, and so are easily able to replace those-destroyed (McKinlay and Geering
[68]; McKinlay [67]).
Table 4. Pests of beet and its allies (Janes and Janes [50})
A. Seedling pests
Group 1
Wireworms
Chafer grubs
Millipedes
Root ectoparasitic
nematodes
Feed below ground only
Group 2
Field mice
Cutworms
Leatherjackets
Feed above or below ground according to circumstances
Group 3
Small birds
Beet carrion beetle
Mangold flea beetle
Sand weevil
Feed above ground only
Group 4
Mangold fly larva
Mines the leaves
Group 5
Stem nematodes
Invades growing points, petioles and leaves
B. Pests of the mature crop
Group 6
Bean aphid
Peach-potato aphid
Capsids
Beet leaf bug
Sucks sap, aphids spread virus diseases
Group 7
Woodpigeon
Tortoise beetles
Silver Y moth larva
Consumes leaves
Group 8
Beet cyst-nematode
Stem nematode
Invades and destroys rootlets
Causes crown canker in autumn
• For Latin names of pests see lanes and Janes [50}, Singh [86} and Metcalfe et al. [69}
239
Normal
Carrion
,
beetle
/
Wireworm
Mangold fly
Millipede
Chafer grub.
Pigmy beetle
Caterplllan.
Earwigs
L
Fig. 3. Illustration of the types of injury caused by a range of sugar beet pests. After Jones and
Jones [50}.
The density of the stand characteristic of a crop is also important when pests which
destroy seedlings are present, e.g. wireworms, cutworms, leatherjackets. For example,
with wire-worms at five million per hectare, there are on average two per plant for
wheat at two and a half million seedlings per hectare, and eighty per plant for sugar
beet with sixty-two thousand five hundred plants per hectare. The greater resistance of
wheat to these kinds of pests is partly a reflection of these facts and of the crop's ability
to tiller i.e. to produce subsidiary side shoots which take over if the central shoot is
destroyed. Control of wireworms and leatherjackets, pests in Britain before organochlorine pesticides were available was based largely on avoidance of fields with large
population counts (Stapley [87}).
240
Table 5. Effects of wheat bulb fly on winter wheat plants in different stages of growth (M. G. Jones
[unpublished)}
Stage
Shoots
Attack
% killed
Earing
main
main
main
main
90
70
7
delayed in survivors
Yield lost
Leaves
1
2
3
4
shoot
shoot
shoot
shoot
none
delayed
all
much
some
some
}
2
5
main shoot
tiller
both
none
none
none
delayed
unaffected
delayed
little
none
little
3
6
main shoot
tiller
both
none
none
none
delayed
unaffected
delayed
slight
none
little
6. Types of feeding
The larger animal pests, birds, mammals, slugs, large adult and larval insects, feed
coarsely consuming great amounts of plant material (Figure 3). The damage they do is
mostly mechanical from the destruction of parts, skeletonisation of leaves or severance
of growing points. Some insect larvae burrow into plant tissues and feed in concealment
causing tunnels, mines and blisters. Nematodes, mites and aphids and their allies
extract sap by piercing and sucking. Those species that feed briefly and move frequently
to new feeding sites may inject toxins with impunity but pests' that feed at one site for
long periods must inject saliva that is non-toxic or the feeding site is destroyed. Some
pests in this last group (aphids, gall midges, endoparasitic nematodes) induce tissue
changes in the host which are essential for survival (lones and Northcote [51,52}).
Whereas resistance based on escape, tolerance, non-preference and antib{osis is
usually mediated by many genes (polygenic), that based on an intimate relationship
between host and parasite is often monogenic, the products ofa single gene in the host
being sufficient to upset the relationship and prevent development and reproduction
(Gallun [35): lones [48}; Sidhu [85}). Non-preference based on the lack of a single
key substance or antibiosis due to the presence of a specific toxin could also be
controlled by one gene. Resistance based on polygenes is often only partial but is
usually long-lasting, whereas that based on single genes tends to be total but precarious.
7. Effects of feeding on host
The effect of a pest on its host is essentially a matter of the numbers feeding i. e. the
population density, and the type of damage that it does versus the amount of host
tissue available and the rate at which it is replaced by growth. The food supply, i.e. the
amount of suitable plant tissue available, determines how dense a pest population may
become but there are other factors e. g. space, enemies, competitors and disease which
prevent pests from reaching their full potential. Hence, numbers are not always related
directly to the food supply or to the intensity and frequency of cropping. Nevertheless,
241
a certain frequency and intensity is essential for the development of large resident pest
populations or to provide the substrate to be exploited by immigrant pests, and any
factor which improves growth and yield tends to increase pest"numbers.
In relation to crop nutrition and the effect of fertilizers on pests and on resistance to
them, anything that limits the growth of the root system is important because it
reduces the volume of soil that can be exploited for water and nutrients. Above-ground
injury reduces photosynthetic capacity and deprives the root system of assimilates
mainly sucrose, some amino acids and various accessory substances, but the demand
for water, nitrate and cations is reduced. The net effect is a slowing of root extension
and a smaller root system (Dunning and Iwanicki [21)).
When a pest attacks the root system directly, large parts may be pruned away. The most
serious damage is severance of the tap root just beneath soil level: this kills or cripples
the plant. Smaller and less powerful pests which prune only a fraction of the root
system cause less injury, for most plants have more than they require, the excess
coming into play only when the soil is deficient or only marginally stocked with
particular nutrients or in times of water stress. Consequently, relatively large portions
of the root system can often be removed without serious consequences to growth and
yield. Small pests with specialised feeding habits e. g. root browsers, feeders on the
nodules of legumes, root miners, root aphids and root ectoparasitic and endoparasitic
nematodes cause damage of a different kind (Tables 6, 7). Nematodes slow root
extension, induce branching and shunt nutrients to the exterior through their bodies.
Like aphids above ground, those that feed long in one place are sinks of nutrients
Table 6. Effect of Herodera rostochiensis on the potato plant, summarised from Trudgil/ et al. [91, 92,
93J and Evans et al. [29J
Roots
Smaller, more branched
Search smaller soil volume
Take up water and nutrients less efficiently
Water and nutrients shunted to exterior by female nematodes
Haulms
Fewer, shorter stems
Same number of smaller leaves per stem
Total N, P, K, Mg, Ca, Na
depressed
Concentrations:
unchanged
depressed, especially K
increased
increased
N
P,K, Mg
Ca, Na
Dry matter
Water usage
less efficient
Table 7. Comparison of the mean chemical composition of nine susceptible potato varieties grown
on land infested and uninfested with potato cyst-nematodes in a dry year (Evans [unpublishedJ)
Infested
Uninfested
242
Eggs/g soil at
planting
Yield of tubers,
t/ha
% in dry matter
K
Ca
Mg
P
N
101
0
5.8
29.4
3.44
4.15
2.10
1.58
0.40
0.37
0.18
0.31
5.05
5.45
K/Ca
1.64
2.62
additional to growing points with which they compete. The chemical composition of
the material so shunted is largely unknown. It contains sugars and nitrogenous
products, some of them excretory, and possibly also cations which otherwise would
have found their way in the sap stream to the overground parts of the plant. Work in
pots suggests that the mechanical damage caused by root-invading larvae is more
important than that from their feeding (Seinhorst and den Ouden [84]). Apart from
the effects on the size and form of the root system and the loss of the nutrients so
side tracked, heavy attacks may also debilitate root systems and lay them open to
secondary pathogens which cause further damage. Sometimes ability to support above
ground growth is so impaired that the plants fall over in wind or are otherwise easily
uprooted (e. g. blackhead toppling disease of banana caused by the burrowing nematode). The overground symptoms of this kind. of attack are stunted chlorotic plants
with a tendency to wilt in bright sunshine and to senesce early. Senescence is probably
related to increases in abscissic acid induced by water stress (Hiron and Wright [42]).
8. Effects of pest numbers on their multiplication and on the yields of host crops
Figure 4 contains typical curves showing the relationship between pest input and output for a crop season, i. e. the population density at planting and after harvest, or for
some other period, and also for the kind of relationship that exists between pest
numbers and yield. A crop grown in soil well supplied with a balanced mixture of
essential mineral nutrient grows better and is therefore able to support greater numbers
of the pest and is on the whole better able to withstand attack, giving larger maximum
and minimum yields. Pest numbers do not invariably increase. Small numbers, if not
unduly checked by enemies and competitors (in which case the species concerned would
not be serious pests) multiply at the maximum rate that circumstances permit. Larger
numbers compete with each other for fqod and sometimes for space or suitable niches.
As a result the multiplication rate decreases and may become less than unity at very
large population densities. Competition of this type would produce a relatively flattopped curve (L e. one derived from the logistic curve). Large numbers have another
effect; they diminish the food supply and sometimes also degrade its quality. Hence
multiplication usually falls off more steeply than it would if competition were the only
factor operating. The equilibrium point (E) is where the food supplied by the host
under attack and the numbers of the pest are in balance. Whether numbers increase
when additional fertilizers are given to the soil in which the host plant is growing
depends on the density of the pest initially. Most often numbers are below the equilibrium point and so the usual response is an increase; o.ccasionally, however, when
numbers are great initially, a decrease follows. Exceptionally, fertilizers appear to
decrease numbers regardless of initial density.
9. Effects of crop nutrition on pests
Experiments in pots, sand or water culture, although necessary to test ideas and
establish principles, are difficult to translate into field practice. This is especially so
when the pots or culture vessels are small. Then the roots are confined to a limited
volume, sometimes as small as 120 m1 (e. g. Curtis [16J), the nutrients are readily
243
Y 2 ! - - - - -___
mox
Y1
mox
-0
Cl)
>-
Y2
min
YI
min
p.
El
PI
I
XI
/
Pf
/
/
/
I
I
/
I
/
I
PI
Pi
Fig. 4. Upper curves, relationship between yield and log initial population density (Pi+), left without
fertilizer, right with NPK. Lower curves, population input (Pi) and population output (Pf+ I), related to
the yields in the upper curves. x I, line indicating neither increase nor decrease. ·-·-·-·Iogistic
curve, food supply undamaged. - - curve for an obligate bisexual species. - - - - initial curve for
a parthenogenetic species. E', logistic equilibrium. E, observed equilibrium.
available and the concentration ranges from severe deficiency to large excess. When
superphosphate or ammonium sulphate are added to sand or soil cultures, difficulties
are experienced in maintaining the pH at or near neutrality. In culture solutions also,
it is difficult to maintain a standard pH and often this is not attempted (e. g. Otei/a
[74]). In pots, the healthy plants in controls grow rapidly and may exhaust the supply
of nutrients, particularly nitrogen, so leading to earlier senescence than that of attacked
plants; a result contrary to usual field experience. In field trials with usual fertilizer
rates, effects on pests are mostly monitored incidentally when infestations happen to
occur. Rarely are trials undertaken with the sole intention of testing the effects of
fertilizers on the pests themselves.
The reported effects of nutrients in some recent laboratory tests and field trials are
summarised in Table 8. These tend to confirm that applications of nitrogen usually
244
result in an increase in pest numbers. Increases are mostly related to young or rapidly
growing test plants or field crops. In maturing crops, late in the year long after the
nitrogen was applied, its effects wear off, (e.g. aphids on the ears of cereal crops
Table 9). The spectacular decreases innumbers of sawfly and lepidopterous caterpillars
that feed on needles or leaves of forest trees after applications of nitrogen, is contrary
to the general experience with field crops. The reasons for this difference are uncertain:
Explanations advanced include changes in the concentration of nutrients in leaf tissue,
the production of greater amounts of resin or the creation of undergrowth conditions
favourable for the development of parasites and other enemies (Stark [88]; Foster
[30]). Decrease in the numbers of the mites infesting the leaves of rye-grass (Table 10)
with increasing applications of nitrogen and potassium is apparently due to a change
in growth habit of the host crop, from a compact habit to one with longer stems and a
sma))er ratio of leaf to stem. In pots in the laboratory, Gibson [unpublished] found that
nitrogen rates had no effect On numbers.
Much laboratory work has been done on mites and aphids but results are conflicting
(Table 11 ), possibly because the suitability of the host changes with age: this is we))
documented for aphids (Kennedy et al. [54]), and also because the healthy host plant
tends to maintain the concentration of its constituents within circumscribed limits,
except when grown in media grossly deficient or grossly overloaded with particular
nutrients. This is achieved partly by regulating uptake and partly by changes in plant
size. Further, the pest may thrive we)) on a range of diets, so that its growth and
reproduction depend rather more on quantity of food available than on quality, at
Table 8. Number of citations of effects of N, P, and K on plants susceptible to a range of insect,
mite and nematode pests
Source
K
P
N
*+
0
+
0
+
0
Tandon [89] ..........
Anon [3] . . . . . . . . . . . .
Other sources ** .......
15
13
12
5
2
4
0
3
5
2
1
3
4
0
4
1
3
0
0
3
4
2
2
3
3
2
2
Totals ...............
40
11
8
6
4
3
7
7
7
* + Numbers increased, 0 unaffected, - decreased
* * mostly experiments with plants in sand or other c,ultures.
Table 9. Infestation of barley ears with aphids, Sitobion avenae and Metopolophium dirhodum in the
field (Bardner and Fletcher [unpublished])
Nos of'aphids per 20 ears
N as nitrochalk, kg/ha
15 July
25 July
Mean
,
,,
,
,
38
75
113
Mean
,.,.""
, ..
429
216
426
463
257
187
439
220
,."",...........
323
342
325
330
245
Table 10. Effect of Nand K on numbers of mites on rye-grass, in field plots (Plumb in Anon [2J)
Kg N/ha+
Kg K/ha
Mites/5 tillers
Yield t/ha dry matter
Untreated
Treated with acaricide
.
.
.
37.5
24
75
150
48
96
226
19
7.7
8.5
11.3
12.4
12.9
14.0
+ As 25:0:16, N: Pz0 5 :K zO
Table 11. Some observations on the effects of nutrients in laboratory and field on mites and other
pests
Author
Species
Rodriguez [82J
Two-spotted mite
Rodriguez and Rodriguez [83J
Two-spotted mite
Le Roux [58J
Host
Numbers doubled when concentration of major nutrients
doubled
Tomato
. Two-spotted mite
Henneberry [38J
Two-spotted mite
Henneberry and Shriver [39 J
Two-spotted mite
Rajarathnan and Law [8I]
Red spider
Vrie [98J
Fruit tree red .
spider
Barker and Tauber [7J
Pea aphid
Taylor et al. [90J
Pea aphid
Comment
Nitrogen increased concentration of B-complex vitamins
Mites increased with Nand K
and sometimes with P
Lima bean
Oil palm
Mites increased with N, decreased with P and total carbohydrate
Mites increased with N
Most on plants without boron
Mites increased with N but so
did predatory mite
Pea
Deficiencies of N, P, K, Ca,
Mg reduced fecundity
High and Iow N levels without effect
Barker and Tauber [8J
Pea aphid
Fecundity decreased by N
Maltais and Auclair [61J
Auclair et al. [5 J
Pea aphid
Varieties most susceptible contained more N and less sugar,
also contained more free and
total amino acids
Michael [70J
Peach aphid
Tobacco
Decreased by N, increased
byK
Wooldridge and Harrison [IOI]
Peach aphid
Brussels
sprout
Growth and numbers
creased by Nand K
Emden [27J
Peach aphid
Brussels
sprout
Increased with N, decreased
with K. High N/K ratio favours aphids
Yolk et al. [97J
Peach aphid
Potato
Decreased with K as KCl
otherwise N, K or NK without effect
246
in-
Author
Species
Host
Comment
V61k and Bode [96J
Potato aphids
Potato
N, P, K had little effect
Taylor et al. [90J
Potato aphids
Potato
High or low N levels had
little effect
N decreased numbers per leaf
Arant and Jones [4J
Grain aphid
Oats
Daniels [i7J
Grain aphid
Wheat
Emden [27J
Cabbage aphid
Brussels
sprout
El Tigani [26J
Six species of aphid
Lack of anyone of several
nutrients caused increase, surplus of anyone caused reduction as often as increase
Markkula et al. [63J
Two species of
aphids and one
mite
Mites on cucumber increased
byK.
High N/K ratio increased
number of mites and peach
aphids on several plants. No
effect on pea aphids
Tulisalo and Markkula [94J
Weevil
Pea
Peat, N, P, K without effect
Eden [22J
Weevil
Rice
Few in glasshouse cultures
. supplied with N. More per
linear foot of row but fewer
per g plant in field when N
supplied
Little affected by N
Bowling [lOJ
Weevil
Increased with N, P, K no
effect
Increased with N
Ishi and Hirano [43J
Stem borer
Favoured by N
K and P without effect
Hirano and Ishi [40J,. [41]
Gadd [33J
Shot-hole borer
Tea
Allen and Selman [1 J
White butterfly
Cabbage
Okigbo and Gyrisco [76J
Hessian fly
Wheat
Johnson et al. [45 J
Midges
CunlifJe [15J
Frit fly
Oat
Increased by N; P and K
little effect
N deficiencies slowed growth,
P and K also essential
Increased with N as result of
tillering
Long term N, P, K and dung
no effect
Nand P had no effect on
tiller attack, N reduced attack
on grain
Joyce [53J
Jassid and white fly Cotton
N increased both
McEwen et al. [66J
Root ecto-parasitic nematode
Field bean
N had no consistent effect
Oteifa [75J
Root-knot
nematode
Tomato
K increased egg deposition
Curtis [16J
Beet cyst-nematode
Potato cystnematode
Sugar beet
Decreased by K in small pots
Potato
K fertilizer did not replace
that lost from nematode
attack
Evans [unpublishedJ
247
least until the pest becomes crowded and drastically upsets the physiology of its host.
Results may also vary between laboratory and field, and with the method of assessing
numbers. Thus, Daniels [17J found in laboratory tests that aphid numbers were fewer
in cultures that received nitrogen. In the field, however, there were more aphids per
linear foot row on plots to which nitrogen had been added but fewer per g of plant
tissue.
The effects of phosphorus and potassium (Table 11) are less clear than those of nitrogen.
Both nutrients are required by the host and the pest feeding upon it, but in quantities
smaller than their requirements for nitrogen which is a major constituent of protein.
Plants deficient or replete with essential mineral nutrients may, in addition, contain
atypical concentrations of organic compounds that could increase or decrease the
growth or reproductive capacity of the pest (Maxwell [65J). Potassium has a major
role in the functioning of enzyme systems ( Evans and Wildes [28J) and might conceivably modify the suitability of plants as hosts. Laboratory evidence suggests that in
some crop-pest situations, fertilizers can modify antibiosis and non-preference
(Leuck [59J,. Wiseman et al. [100 J), but whether these effects can be fitted into field
practice when several pests with conflicting requirements are present remains to be seen.
On most occasions, the fertilizers applied seem to have only marginal effects on the
host's inherent susceptibility or resistance to attack. In most situations their effects
appear to operate mainly through improved growth. The idea that deficiencies in trace
elements contribute to 'potato sickness' caused by cyst-nematodes (Ellenby [25J) has
not been substantiated. Again, the better health and growth of crops when these
deficiencies are rectified is mainly responsible for improved 'resistance'. Nevertheless,
there is some evidence that trace elements sometimes diminish pest numbers. For
example, Rajarathnan and Law [81J found that boron decreased the numbers of mites
attacking oil palm seedlings. Also, sandy soils containing appreciable concentrations
of copper appear to decrease numbers of some root ectoparasitic nematodes (Cooper
[13J).
There is much controversy about the role of organic fertilizers in pest control, especially
in the control of plant parasitic nematodes. In many experiments, organic matter
containing unknown amounts of major and minor nutrients are added to impoverished
soils and claims are made as a result of the improved yields obtained. Many such
experiments have been concerned with root-knot nematodes, populations of which are
difficult to assess. The effects of organic materials, if any, stem from the nutrients they
contain, improved soil structure, production of toxic breakdown products or encouragement of competing organisms of which nematode trapping fungi are thought to be
important.
Lin/ord et al. [60 J found there was a dramatic decrease in the numbers of all soil
nematodes after an initial upsurge of saprobic species. Duddington and Duthoit [18J
claimed green manure gave some control of cereal cyst-nematode. Watson [99J
observed that plants grew better and root-knot nematode damage was lessened when
mulches of organic matter were applied. Finely chopped crop residues at 12.5 and
25 tlha reduced injury by root-knot nematodes (Johnson [46J). Many other examples
of benefits from organic matter of a similar nature can be quoted, e.g. Gaines [34J,
van der Laan [56J, Lear [57J, Miller and Edington [71J, Miller et al. [72J, Mankau
and Minteer [64J, Johnson [47J, Hameed [36J, Vlk [95J, Mammen [62J. Although
adding organic matter usually increases yields, it is not always clear that this is the
result of a decrease in the numbers of noxious nematodes. O'Bannon [73J found peat
248
moss actually favoured the invasion of citrus root stocks by the citrus nematode,
otherwise rates of increase and peak numbers were much the same as in controls
without peat. In experiments in microplots organic matter had little effect on the
numbers of cyst-nematode eggs (Table 12) and Markkula et al. [63] found sphagnum
peat had no advantages over mineral soil in the prevention of pest attack; it decreased
the reproduction of some and favoured that of others.
·10. Results from some experiments at Rothamsted
The classical experiments, on plots that have received the same treatments for many
years, and certain other experiments provide invaluable evidence of the influence of
fertilizers, mineral and organic, on pest damage or pest numbers. In Broadbalk where
wheat was grown both continuously and in a fallow cycle, oviposition by wheat bulb
fly into fallow soil in July and August was not affected by different manurial treatments.
However, plots not given potash were more severely damaged by the larvae (Figure 5)
because the plants grew more slowly and some were still in the single"shoot stage when
Grain
K
%decrease
N
yield
% increase
°
2
36 kg jha 3q kg j, IUr-_-,-O_-.------,0r--...-----r---r_r------r--.:..,6
(+) (+) FYM
None
+
+
+
PNa Mg
+
PNa Mg.
+
None
+
P
+
P Na
+
P
+
P Mg
~:~:~:~:::::
Fig. 5. The effects of wheat bulb fly attacks on the percentage increase and decrease in grain yields
of some Broadbalk plots in the year after fallowing. Zero line refers to yields two years after fallowing when many fewer eggs are laid. Means for 1953 to 1966, exc1udingJ963. Amounts of N, P and K
applied in dung (=FYM) as in Table 13. After Johnson et al. [45].
2~9
N
V>
o
Table 12. Effects of organic matter and nematode trapping fungi on numbers of cyst-nematodes, eggs/g soil, in microplots
0
Bran
Fungus
Beet cyst-nematode (Duddington et al. [20])
Initial population
124
133
116
Final population
114
103
144
Bran
+ Fungus
Leaf mould
Leaf mould
+ Fungus
Spent hops
Spent hops
+ Fungus
NS
NS
110
117
Potato cyst-nematode (Duddington et al. [19]); Jones [unpublished]
Final population
529
724
973
(70 eggs/g initially)
Chopped Chopped
cabbage
cabbage
+ fungus
Final population
70
71
76
(10 eggs/g initially)
Significance
557
77
702
75
543
702
Compost
Compost
+ fungus
40
82
NS except
bran + fungus
NS
\
invaded by newly hatched larvae in February (Table 5). Aphelenchid nematodes are
somewhat fewer in dunged plots but plant parasitic species are equally numerous in all
(Table 13). The nitrogenous fertilizers applied to Park Grass have changed the sward
and decreased the number of soil arthropods appreciably (Figure 6). Barnfield grew
sugar beet or mangolds for more than 100 years and, although not found to be infested
with beet cyst-nematode until 1944, the infestation was probably of long standing.
Table 14 gives egg populations in the autumn of 1948, and mangold yields averaged
for the years 1904 to 1940. Generally the soil populations correlate with the yield,
especially for the nitrogen and castor meal treatments. Counts are especially small on
the 'no nitrogen' series and 'no mineral' series being least on plots receiving neither.
Probably numbers are in equilibrium with the available quantity of fine roots and any
correlation with treatments is the result of the nematodes' effects on root development.
Table 13. Nematode populations in Broadbalk plots, log nematodes/litre soil (Corbett et al. [l4})
Aphelenchids .................... ....
All plant parasitic species ..............
All nematodes ........................
Nil
ON
NP
NPK
Dung
3.13
3.66
4.35
3.34
3.87
4.38
3.13
3.87
4.32
3.11
3.87
4.37
2.75
3.86
4.37
* N 96, P 34, K 90 kg/ha. 35 t/ha dung equivalent to N 53, P 31, K 109 kg/ha (Boyd (l1 J) .. applied
for more than 100 years.
20
o
o
o
616
c
N
E
...
3
Q,I
a..
'"
:u 2
oD
E
::l
C
o
48
q6
144
Nitrogen applied kg/ha
Fig. 6. Effects of nitrogen on the arthropod fauna of Park Grass plots. After Edwards and Lofty
[23J.
251
Table 14. Beet cyst-nematode populations, eggs/g soil in 1948 and mangold yields (t/ha) on Barnfield,
sugar beet and/or mangold since 1856 (Fen wick and Reid [unpublished])
Nitrogen series
Numeral series
*0
P
PNaMg PK
PKNaMg Dung
Dung
+ PK
Means
** Castor meal
0.3
(20.8)
0.9
(23.7)
10.1
(48.2)
7.8
(44.1)
7.5
(51.9)
9.9
(57.7)
4.6
(69.7)
5.9
(45.1)
+
0.2
(18.7)
0.9
(22.2)
7.4
(54.0)
5.4
(55.2)
5.4
(66.4)
6.9
(58.3)
4.0
(73.9 )
4.3
(49.8)
(NH.)2S0•
0.2
(14.1)
1.0
(17.1)
3.6
(40.5)
12.1
(36.4)
6.3
(39.0)
2.2
(55.1)
6.5
(75.0)
4.6
(38.5)
NaN0 3
5.5
(26.5)
6.7
(40.3)
10.6
(46.3)
8.9
(42.3)
9.5
(47.7)
4.6
(70.3)
8.6
(73.7)
7.7
(49.6)
°
0.1
(7.5)
2.8
(10.1)
2.0
(9.9)
1.1
(9.4)
5.0
(10.6)
0.9
(43.6)
1.6
(50.0)
1.9
(20.2)
Means
1.3
(17.5)
2.5
(22.6)
6.7
(39.8)
7.1
(22.7)
6.7
(43.1)
4.9
(40.7)
5.1
(67.0)
4.9
(40.7)
Castor meal
(NH.)2S0•
* Minerals: P, K, Na and Mg at 34, 224, 90,22.4 kg/ha respectively; dung, 35 t/ha .
•• Castor meal, (NH.)2S0., and NaN0 3 to supply 96 kg/ha.
Note: 35 t dung is equivalent to 53 kg N, 31 kg P, 109 kg K (Boyd [11]) .. minerals, dung and castor
meal applied to the same plots for more than lOO years.
The view that nematodes cannot flourish where fertilizers are withheld and only
'natural' manures used finds no support. The plot receiving both dung and rapecake has
the fourth largest egg count. In a series of experiments in which dung, N, P and K were
applied to potatoes, by chance one trial was sited on land heavily infested with potato
cyst-nematode. Yields from this trial are compared with three others in Table 15.
Nitrogen applied as ammonium sulphate almost doubled the yield on the infested site
Dung alone was not so outstanding. Potash and phosphate, with which all sites were
already well supplied, increased yield only slightly.
In a series of trials on light land farms, where sugar beet suffered heavy attacks from
root ectoparasitic nematodes, nitrogen greatly increased yield (Table 16) but 249 kg/ha
produced only 80% of the yield from plots fumigated with DD nematicide (dichloropropane/dichloropropene mixture).
11. Conclusions
Pests that attack overground parts of crops have the same ultimate effects as those
that attack below ground: they decrease the size of the root system and diminish the
capacity to extract nutrients and water from the soil.
In most pest-crop situations, nitrogen fertilizers increase the numbers of pests because
they increase the food supply for them. They also increase yields by increasing the
speed with which critical stages are passed, by improving ability to compensate for lost
252
Table 15. Effects of dung and N, P and K fertilizers: yield increases on a site infested with potato
cyst-nematode compared with the mean increases on three uninfested sites (Yates et al. [102j)
Total tubers, t/ha
Dung, t/ha
12.6
25.1
50.2
2.94
5.67
10.72
17.68
-2.26
1.10
16.62
-0.15
0.35
9.04
-2.84
0.15
2.79
5.35
6.96
3.29
3.11
3.09
2.06
1.71
2.56
1.83
1.18
2.96
0
mean yield
*max. yield
28.25
38.67
33.37
37.46
Yield increases
Infested, one site
Dung v 0 ..........
**N v 0 ...........
KvO ..............
PvO .. ...........
15.44
2.88
1.56
Uninfested, three sites
Dung v 0 . . . . . . . . .
NvO .............
KvO .............
PvO .... .........
3.14
3.31
2.16
* From plots receiving 50.2 t/ha dung and N.
** 113 kg N/ha.as ammonium sulphate, 41 kg P/ha as superphosphate and 156 kg K/ha as muriate
of potash.
Note: 12.6 t/ha dung is equivalent to 20 kg N, 12 kg P and 41 kg K/ha (Boyd [l l}).
Table 16. Effect of DD fumigation and nitrogen applied as nitrochalk to sugar beet grown on sandy
soils infested with stubby root nematodes. Mean yields of washed roots, t/ha from j 5 trials over
3 years (Cooke and Draycott [l2j)
N, kg/ha
o
83
166
249
Fumigated. . . . . . . . . . . . . . . . .
35.9
42.7
43.5
44.7
Unfumigated . . . . . . . . . . . . . . .
24.8
31.2
33.5
35.3
se
±1.20
DD injected at 380J/ha by hand.
plants or plant parts and, at least initially; by diluting the intensity of attack per unit of
. plant weight. That is, they help plants to escape from attack and to tolerate attack.
Neither of these are considered to be 'resistance' in the true sense. In a few pest-crop
situations,notably in forests and possibly in grass, nitrogen decreases pest numbers for
reasons which are unclear, but could be from changes in the -ratio of N to other
nutrients, the ratio of amino acids or other nitrogenous compounds to sugars in plant
sap, changes in growth habit or, in soils, from complex effects on the soil ecosystem.
The large effects of nitrogen are to be expected, as it is a major constituent of protein:
also, for crops other than those able to fix nitrogen, cultivated soils are inherently
nitrogen deficient. The general effects ofN are summarized in Figure 7 for attacks other
than those which are catastrophic. When such attacks occur neither N nor any other
fertilizer would have any effect.
253
40
30
infested
20
~
heavily infested
1·0
00·l---'----"'------'-------'
o
I
2
3
4
Nitroqen levels
Fig. 7. The relation between nitrogen levels and yields of crops heavily, lightly and unattacked by
pests.
The effects of P, K and of the minor and trace elements are less clear. The idea that K
is outstandingly important in conferring 'resistance' to pest attack finds little support.
Where any element is grossly deficient, supplying it is likely to improve the growth of
crops and the multiplication of the pests that feed upon them. The effects of P and K in
most well managed agricultural soils are slight compared with those from nitrog·en. The
effects of applications of dung and organic matter on pests are obscure. The claims
made that they suppress pests are probably over-rated and, for soil nematodes in
temperate areas, seem to have little foundation. In classical and other experiments at
Rothamsted, where fertilizers, mineral and organic, have been applied to the same
plots for more than 100 years, or to plots in trials repeated on different sites in several
seasons, organic matter has had little effect other than might be expected from the N,
P and K it contains.
Where it has been studied, resistance seems to be a property within plant cells and of
the whole plant, rather than of substances translocatable from tops to roots or vice
versa. It has long been known to nurserymen that grafting susceptible scions on to
insect-resistant root stocks, and the reverse, does not change the resistance of the
susceptible organ nor weaken materially the resistant one. Grapevines and Phylloxera
are a classic example. Similar considerations may apply to nematode resistance
(Forster [31]).
Undoubtedly the composition of cell sap is affected by the nutrients applied to soil as
N, P and K, and may sometimes enhance or reduce the real resistance of the crop to
particular pests by modifying non-preference or antibiosis (Singh [86]). These effects
are usually small compared to the beneficial effects of balanced applications of N, P
and K that aim to provide optimum crop nutrition in a particular soil where there are
no deficiencies of minor and trace elements. The effects might well operate in different
directions for different pests attacking the same crop.
254
12. Bibliography
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brassicae [L.]) to diets of mineral deficient leaves. Bull. ent. Res. 48, 229-242 (1957).
2. Anon: Rothamsted subject day: I nitrogen. p. 100, Harpenden, Rothamsted Experimental
Station (mimeographed), 1975.
3. Anon: Plant pests in relation to soil and nutritional factors (1956-1974). Annotated bibliography No. SB 1746, Comm. Bur. Soils, Harpenden, England (in press), 1976.
4. Arant, F. S. and Jones, C. M.: Influence of lime and nitrogenous fertilizers on the population
of greenbugs infesting oats. J. econ. Ent. 44, 121-122 (1951).
.
5. Auclair, J. L., Maltais, J. R. and Carlier, J.J.: Factors in resistance of peas to the pea aphid,
Acyrthosiphon pisum (Harr.) 11. Amino acids. Canada Ent. 89, 457-464 (1957).
6. Bardner, R. and Fletcher, K.E:: Insect infestations and their effects.on the growth and yield
of field crops. Bull. ent. Res. 64, 141-160 (1974).
7. Barker, J. S. and Tauber, O. E.: Fecundity of and plant injury by the pea aphid as induced by
nutritional changes in the garden pea. J. econ. Ent. 44, 10ID-I0l2 (1951).
.
8. Barker, J. S. and Tauber, O. E.: Fecundity of pea aphid on garden pea under various combina-'
tions of light, moisture and nutrients. J. econ. Ent. 47, 113-116 (1954).
9. Beck, S. D.: Theoretical aspects of host plant specificity in insects. In Proc. Summer Inst.
Biological control of plant insects and disease. Eds. Maxwell, F. G. and Harris, F.A., University Press of Mississippi, pp. 290-311, 1974.
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826-827 (1963).
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(1959).
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258
Cultural Factors and the Resistance of Citrus Plants
to Scale Insects and Mites
F. Chaboussou, Directeur de Recherches honoraire, Institut National de la Recherche agronomique
(INRA), Charge de Mission, Pont de la Maye/France
Summary
1. Re~earch and observation in Morocco have shown us that swarming of Tetranychus on citrus
is connected with pesticide treatment against coccids and particularly against Californian red scale
( Aonidiella aurantii).
The same process is at work as in other plants, such a disturbance arising not only from destruction
of the natural enemies of the pest but predomimintly from effects of pesticides ~ insecticides particularly - on the physiology and biochemical state of plant tissues. In other words the modification
of the metabolism of the plant caused by plant protection chemicals leads in turn, through nutritional effects, to a raising of the biotic potential of mites.
S,uch an effect of pesticides - fungicides and acaricides are just as much involved as insecticides dim, among other things, react positively on the multiplication of the coccids themselves. Such
revivals in population, independent of effects' on the natural predators have been observed on
Citrus just as they have on deciduous trees following certain insecticide treatments (organo-phosphorus compounds).
2. These results must be brought into the consideration of the whole field of the plant's resistance
to pests, fungal and virus diseases, especially as concerns the physiological mechanisms involved.
This leads us to a consideration of the various factors which can affect the physiology and thus
the resistance of the plant and these are found to be reflected in the level of soluble compounds in
the sap and tissues.
On the question of the resistance of citrus to coccid attack, the work of Steyn done over 25 years
ago, but scarcely noticed till now, led us to study the effects of soil conditions and their amendment
on the biotic potential of two coccid species.
3. Nadir's research on the foliar analysis of citrus confirms in some measure Steyn's results, confirming the bad effects of excess calcium on the susceptibility of citrus to coccid attack.
Following on Nadir's work we have been able to show that liming increases the multiplication of
Lepidosaphes beckii and Saissetia oleae. Conversely application of potassium results in a significant
reduction in the biotic potential of the two coccids. Leaf analysis shows an increase in Ca
level in the leaf through liming and a decrease in calcium and magnesium through application of
potassium (K2S0 4 and KN0 3) .. Thus there seems to be, at least at first sight, and within the limits
of our work, a negative correlation between tlie ratio K/Ca + Mg and the biotic potential of coccids.
4. These encouraging results led to investigations on how to optimise the metabolism of citrus to
achieve at the same time maximum yield and maximum resistance. This raised the problem of
finding out to what extent foliar analysis would prove useful in such research. The early results
obtained and the comparison of our figures with those of Steyn as well as the experience of a practical grower, which should certainly not be disregarded, showed that leaf analysis could be of considerable help.
.
Yield and resistance are by no means incompatible and this appears to reside in the fact that both
these properties in citrus depend upon maximum protein synthesis. In turn the desired metabolic
259
condition implies a minimum content of soluble substances in the plant tissues, a level below that
suitable for coccids.
5. To sum up, the results already obtained seem to show that the search for improvement in the
plant's resistance through its physiology is not just Utopian but quite practical. However, to achieve
the maximum efficacy, efforts to improve conditions for the plant should not only involve the
judicious use of fertilisers to induce the desired cationic balance but also spray applications, the results
of which, though they may be temporary, can be most beneficial. Attention should be paid to the
favourable effects of organic manures due their trace element and growth substance content. These
have hardly been studied up to the present.
Further research should lead, if not to the total suppression of insecticides and acaricides, at least
to a reduction in their use, as the results obtained by certain arboralists have elsewhere shown to
be possible. If control is possible by these means it opens the way to a happy combination of plant
resistance and biological control by the parasites and predators of the pests.
Resume
\. Enquetes et observations conduites au Maroc nous ont montre que les pullulations de Tetranyques sur Citrus etaient liees aux traitements pesticides conduits contre les cochenilles et notamment contre le Pou rouge de Californie: Aonidiella aurantii.
11 s'agit done du meme processus que pour les autres plantes, un tel «desequilibre» provenant non
seulement de la destruction des ennemis naturels, mais aussi et surtout des repercussions des pesticides - insecticides notamment - sur la physiologie et l'etat biochimique des tissus. Autrement dit
la modification du metabolisme de la plante entrainee par les produits phytosanitaires, provoque
a son tour, par effet nutritionnel, l'elevation du potentiel biotique des Acariens.
Une telle incidence des pesticides: fongicides et acaricides etant aussi bien concernes que les insect
ticides, peut d'aiIleurs egalement retentir positivement sur la multiplication des Cochenilles ellesmemes. Des regains de multiplications, independants de toute action sur les ennemis naturels, ont
effectivement ele observes aussi bien sur Citrus que sur arbres a feuilles caduques, ala suite de certains traitements insecticides (esters phosphoriques).
2. Ces resultats mettent done a nouveau en evidence toute l'importance du terrain - au sens physiologique du terme - concernant la resistance de la plante vis-a-vis de ses ravageurs: qu'il s'agisse de
cocheniIles, d'Acariens aussi bien que des maladies cryptogamiques, voire meme des maladies a
virus.
Ce fait nous a ainsi amene a nous preoccuper des differents facteurs susceptibles d'agir sur la physiologie - et done la resistance de la plante. Celle-ci se trouve en effet en liaison avec le niveau des substances solubles dans la seve et les tissus.
Comcernant le probleme de base de la resistance des Citrus vis-a-vis des cochenilles, les travaux de
Steyn (remontant a plus de 25 ans, mais passes inapen;us jusqu'alors) nous ont conduit a etudier les
repercussions de la nature du sol et de certains amendements vis-a-vis du potentiel biotique de deux
especes de cocheniIles.
3. Les recherches de Nadir concernant le diagnostic foliaire des agrumes rejoignent, en quelque sorte,
les resultats de Steyn, confirmant les effets nefastes d'un exces de calcium sur la susceptibilite des
Citrus vis-a-vis des cocheniIles.
Mettant en effet a profit certains essais d'amendements sur mandariniers conduits par Nadir au
Maroc, nous avons pu etablir que les amendements calcaires augmentaient le niveau des populations de Lepidospahes Beckii et de Saissetia oleae. Inversement, les amendements potassiques provoquaient de tres sensibles regressions dans le potentiel biotique de ces deux cocheniIles.
Parallelement, les analyses relatives au diagnostic foliaire montraient une elevation du taux de
calcium dans les feuilles avec les amendements calcaires, et au contraire, une regression de ce meme
element, ainsi que du magnesium, avec les traitements potassiques (SO.K 2 et N0 3K).
Ainsi parait-il exister, en premiere approximation tout au moins et dans les Iimites oil nous avons
opere, une correlation negative entre l'elevation du rapport K/Ca + Mg et le potentiel biotique des
cochenil1es.
4. Ces resultats encourageants conduisent donc a la recherche d'un metabolisme optimum des
Citrus susceptibles d'entrainer a la fois un maximum de rendement et un maximum de restance.
lis soulevent egalement le probleme de savoir dans quelie mesure la methode du diagnostic foliaire
peut nous etre utile dans une telle recherche. Or, d'apres les premiers resultats obtenus, notamment
par la confrontation de nos propres chiffres avec ceux de Steyn, ainsi que ceux d'un arboriculteur
260
du Maroc ayant empiriquement opere, cette eventualite n'est nullement a ecarter: le diagnostic
foliaire pourrait etre d'un secours tres appreciable.
Il s'avere que rendement et resistance ne sont nullement incompatibles, bien au contraire. Et ceci
paraissant tenir au fait que ces qualites des Citrus seraient toutes deux Sous la dependance d'un
maximum de proteosynthese. A son tour, un tel etat du metabolisme implique en effet un minimum
de substances solubles dans les tissus de la plante, et donc un niveau inferieur de susceptibilite
vis-a-vis des cochenilles.
5. En resume: les resultats encourageants deja obtenus paraissent bien montrer que la recherche
d'une stimulation de la resistance de la piante par action sur sa physiologie n'est nullement utopique,
mais presente au contraire un interet certain.
Cependant, afin de presenter le maximum d'efficacite, le conditionnement de la piante devra non
seulement faire appel a la fertilisation du sol par le dosage judicieux des amendements et des fumures
et viser en particulier a l'instauration d'un equilibre cationique adequat, mais aussi aux pulverisations
d'engrais foliaires, leurs repercussions, meme temporaires, pouvant se monirer ben6fiques.
En particulier egalement, l'attention devra etre portee sur les incidences - a priori favorables - des
fumures organiques, dans la mesure oil elles renferment: oligo-elements et substances de croissance (ces repercussions ayant ete peu etudiees jusqu'a present).
Pratiquement,'la stimulation de la resistance des Citrus devra etre etudiee au cours des periodes de
leur cycle evolutif annuel oil ils se montrent davantage sensibles vis-a-vis des cochenilles ou des
acariens.
De tels travaux devraient conduire, sinon a une totale suppression des interventions insecticides et
acaricides, du moins a leur tres sensible reduction, comme le montrent bien d'ailleurs deja, les resultats obtenus par certains arboriculteurs. En particulier, cette forme de lutte permettant d'associer
heureusement resistance et lutte biologique par les parasites et les predateurs.
1. Introduction
The author was originally asked to speak on 'The effect of potassium an pest resistance
in Citrus' but he has asked permission of the organisers of the Colloquium to enlarge
the scope to include the influence of 'cultural factors' in the title. This was done for two
reasons:
The first resides in the fact that no nutrient element - even a major element like
potassium - acts in isolation within the plant. It exercises its influence, in effect, in
conjunction with all the other essential major and trace 'elements. Briefly, as has been
already explained (Chaboussou' [1973)) nutritional equilibrium plays a dominant role
in the plant's physiology and, hence in its potential for resistance to pest attack. We
have the opportunity in the present work to explain once again the nutritional processes involved in this phenomenon.
There is a second reason for considering the health of the plant in the wider context.
The use of fertilisers, so important in itself in influencing the behaviour of the plant, is
only one among a whole range of possible cultural improvements. It is thus important
to consider all these together, and.we cannot repeat this too often, in any consideration
of the susceptibility of plants to pests or to disease. Some of these factors, very often
not recognised, if not actually ignored, are of the first importance: pesticides can have
repercussions on the metabolism of the plant tissues and these can inhibit if not totally
nullify the beneficial effects which fertiliser dressings well adapted to the nutritional
requirements of the plant might be expected to have upon its health.
In other words, and as we hope to show in this paper, these extrinsic factors are just as
much concerned and just as importalit in the biochemistry and metabolism of the
tissues as are the intrinsic genetic factors. This also means, even though the idea may
be somewhat revolutionary, that the study of the effects of the various cultural factors
26J
merits at least as much attention as the numerous studies which have been uniquely
devoted to purely genetic aspects of the problem.
In the first part we shall deal with the influence of certain cultural factors on the biotic
potential of citrus pests, especially scale insects and mites. This will enable us to draw
up a list of the extrinsic factors which may have an influence on resistance by the plant.
The second part will be devoted to study of the mechanisms involved in stock-scion
relationships, pesticide treatment, the soil and fertiliser use. This should lead to precise
description of the relations between host and pest, or to what determines the property
of resistance.
Then, in the third part we shall examine the beneficial results obtainable, thanks to
description of the relations between host and pest, or to what determines the property
of resistance.
.
Finally we shall try to extract some main conclusions which result from the work and
appear to confirm our ideas.
2. Citrus physiology and biotic potential of pests
2.1. Disturbance of biological equilibria by pesticide treatment
The author has several times visited Morocco to study the multiplication of Tetranychus mites on Citrus. Earlier work had already produced evidence of a connection
between the use of insecticides against scale insects (notably against Californian red
scale: Aonidiella aurantii) using synthetic insecticides like DDT or various organophosphorus compounds, and the subsequent build up of so-called secondary pests
such as mites.
Thus, Delucchi [1965] confirmed that in Morocco as in many other regions, the
massive build-up of bud mite followed the use of organo-phosphorus compounds
against scale. This was not confined only to Tetranychus types like T.telarius, T.cinnaharinus or Hemitarsonemus latus but also various other scales such as Chinese scale
(Ceroplastes sinensis), Australian scale (Iceria purchasi) and smooth scale (Coccus
hesperidum). Hart and 1ngle [1970] have demonstrated experimentally that following
treatment of citrus with various insecticides, particularly organo-phosphorus compounds the resulting multiplication of Coccus hesperidum led to other processes than
the eventual destruction of the natural parasites of this scale by the pesticides.
Thus the indirect mechanism of this multiplication which we had already demonstrated
with red spider on the vine (Chahoussou [1969]) has been experimentally confirmed.
Moreover, in 1942 Holloway et al. had also shown that such build up in the population
of sucking insects could equally well follow spraying of the foliage with mineral salts of
copper or zinc which were known to be quite harmless to the natural predators.
In brief, all these facts confirm the idea that the 'abnormal' build-up of pests, again
called biological disequilibrium, can follow the application of pesticides, and indeed
fungicides as well as insecticides, through an indirect process caused by the effects of
these compounds on the physiology of the plant. This becomes biochemically modified
to produce nutritional conditions favouring the biotic potential not just ofmites and aphids
but also ofscale insects.
As we have shown for P.ulmi and E.carpini on the vine, this stimulation via the
nutritional route can soon influence fecundity, longevity, shortening of the life cycle and
distortion of the sex ratio in favour of the females.
262
All this obliges us to consider carefully all the various extrinsic factors which could
affect the physiology of the plant - in this case the Citrus. We shall now examine this
with reference to scale insects.
2.2. Soil conditions and the biotic potential of scales
Steyn [1951] drew attention to the great variation in the virulence of Californian red
scale (Aonidiella aurantii) between different areas in S.Africa. Instead of attributing
these differences to variations in climate, as he might in the circumstances have been
tempted to do, Steyn asked himself whether soil variation in chemical characteristics
might not be the main factor responsible for the variation in scale attack.
To confirm his idea, Steyn carried out a trial with citrus grown in sand culture using
nutrient solutions deficient in various nutrients, notably Ca, P and N. He studied the
development of mites on the leaves of trees treated in this way, using as the criterion the
duration of one generation. Results for analysis of similar leaves (two of the oldest
leaves on 10 month old plants were used) are given in Table 1.
Table 1. Leaf contents of various elements (ppm in D M) in Citrus under various fertiliser treatments
Treatment
N
P
Ca
Mg
K
K/Ca
Control ....................
Deficient in Ca .............
beftcient in P ...............
Deficient in N ..............
24780
21200
25600
15200
1034
973
1000
1 191
53500
39400
52700
46900
4620
3560
4180
3820
14020
29400
13560
15520
0.262
0.746
0.257
0.330
The trees were grown in the nutrient solutions from 11 October 1943 to 11 December
1947, i.e. for 4 years and 2 months. The following results were obtained breeding the
insects on plants aged 2 years 7 months.
At the low level of calcium Steyn noted a significant increase in the duration of the life
cycle (from larva to larva). From the biochemical point of view he noted that the
solution high in K resulted in the lowest Ca content in the leaves. In particular in the
low calcium treatment Ca and Mg in the leaves were both reduced while compared
with the control, the K content was twice as high. This is emphasised in the K/Ca ratio.
As for the scale insects, the low leaf contents of Ca and Mg and the high levels of K
reduced the number of generations passed through in the year.
Among other things the author points out that this behaviour is reflected in field crops
in S.Africa, leaf potassium reachin'g 20 000 ppm in D.M. on soils low in Ca while it is
only from 4000 to 15000 on soils better supplied with Ca and Mg.
We believe that Steyn's work in S.Africa can profitably be compared with Nadir's
research on leaf analysis of citrus in Morocco. The latter was able to show that in most
of the orange groves in Morocco leaf Ca content is abnormally high while, in correlation, P, K and Na are low. This high Ca content which is a handicap to citrus growing
is not just the result of soil conditions but is mainly caused by the composition of the
irrigation water which contains up to 80 mg Call in the form of bicarbonate, amounting
to an application of 800 kg/ha, nearly 4 kg per tree. Thus, so far as concerns certain
regions of Morocco, it is the physiological state of the trees, due mainly to the high Ca
content of the irrigation water, which favours the development of the scale insects. This
explains in'large measure why A.aurantii is so virulent in the Rharb.
263
The alkalinity of the soils and of the irrigation water leads also to trace element
deficiencies, which occur both at too high and too Iow pH. Such deficiencies, particularly of zinc or iron tend to favour the multiplication of scale insects. Thus, workers
at IFAC have been able to confirm that pineapples grown in nutrient solutions
deficient in zinc are affected by abnormal proliferation of the scale Diaspis boisduvali.
Certainly it would seem that one would be entitled to suggest that scale insects, particularly Californian red scale, are particularly noxious pests not only in Morocco but
also in other regions because of unbalanced nutrition arising from the alkalinity of the
soils reflected in excessive calcium levels in the leaves. Steyn has drawn attention to the
importance of the link between soil properties, plant physiology and the plant's
resistance to pests.
However, soil factors are by no means the only ones concerned in affecting the
physiology of the plant. It is in fact quite otherwise. So let us now consider everything
which may be of importance in devising cultural measures which could be effective in
improving resistance.
2.3. Other factors which can influence the physiology of the plant
There are two types of factors which may be concerned:
(a) Intrinsic factors, comprising genetic characters, rootstock and age of the tissues or
of the plant.
(b) Extrinsic factors both climatic and cultural. The latter comprise, soil structure, soil
chemical composition, the use of fertilisers and finally, last but not least, pesticide
treatments.
Among all these, it is assuredly the genetic factors which have received the most attention. In contrast, except for a few practical growers and protagonists of 'biological'
farming, and a very few research workers the extrinsic factors have up to now been for
all practical purposes ignored. However, there have been cases where the influence of
extrinsic factors has outweighed that of genetic make-up. This is why it seems to us
indispensible to emphasise this aspect of the problem which is so often ignored.
3. Cultural factors in the physiology and resistance of the plant
Having chosen the type of fruit he wants to grow and the variety, the grower has to
suffer the consequences of ageing trees and effects of climate. He has no control over
these but he is, on the other hand, master of his cultural methods, though no doubt he
does not always do everything in the way he should. And this is generally because he is
largely ignorant of the effects these may have on physiological conditions and thus on
resistance to both animal pests and diseases.
We shall review successively: influence of rootstock, of pesticide treatment and finally
of fertilisers and cultivation.
3.1. Influence of rootstock
This aspect of culture has, without doubt a far greater influence on the behaviour of the
scion towards pests and diseases than we suspect (see our study of Physiology and
Resistance of the Plant).
264
The susceptibility of the scion to both pests and disease seems to arise from an apparent
slowing down of the process of protein synthesis resulting in increased concentration
in the leaf tissue of soluble substances, particularly free amino-acids. Confining ourselves to citrus, Wallace et al. [1953] showed among otherthings that the rootstock
had effects not only on tree height, yield and quality of the fruit but also on its susceptibility to various diseases. Thus, Tristeza is an excellent example a fruit tree
disease in which the rootstock - scion relationship plays an important part. The most
severe symptoms are seen when an orange is grafted onto bitter orange. There is a
tendency in practice to use resistant rootstocks like orange, Poncirus trifoliata etc.
What then is the determining fador in disturbances induced in the scion by the
rootstock. Whether we are concerned with the vine (Bovay [1959]) Bovay and Isoz
[1964] deciduous fruit trees (Blanc-Aicard and Brossier [1962]) or citrus (Wallace
et -al. [l952-1953] }(Bar-Akiva et al. [1972]) the different authors all reach the conclusion that the rootstock determines cationic equilibrium in the sap, and particularly
the ratio of di-valent to monovalent ions. Thus through mineral nutrition, metabolism
in the scion and, particularly protein synthesis, is dependent on the root system. The
cationic balance is important in controlling the content of nitrogenous substances
(soluble and insoluble) and of various glucides... and thus the susceptibility of the
plant towards what one may justly call its parasites.
3.2. Influence of pesticide treatment
This is an important subject which we have already discussed at length elsewhere
(Chaboussou [1969] a) and which will be only very briefly summarised here.
Whether they be inorganic or organic, fungicides, acaricides insecticides or herbicides
the various plant -protection chemicals may be capable of entering the plant and
disturbing its metabolism. Nevertheless penetration will depend upon a variety of
things: the chemical nature of the pesticide and rate of application but also on the
initial state of the plant, particularly on the osmotic pressure in its cells.
Thus pesticides may enrich the plant in metallic or other elements contained in the
formulation: Cu, Fe, Zn, Mg, Mn, S, P, etc.
Other substances seem to interfere through their molecular structure; thus it appears
for example that some chlorinated compounds, and particuarly DDT, may have
effects comparable with those produced by growth substances.
Such substances react upon the main physiological processes in the plant such- as
respiration, transpiration, photosynthesis and protein synthesis. Nevertheless the_~ame
product does not always have the ~ame effects which depend not only on the nature of
the compound but also on the rate applied, time and frequency of application, and,
finally, on the initial state of the plant. This latter depends in turn on its genetic makeup, ecological conditions, its nutrition and the age of its organs. In any case one can
say that, through their action on the processes of photosynthesis and protein synthesis
pesticides can modify in a more or less marked manner, and over a variable period, the
balance between carbohydrates and nitrogenous compounds. The same applies with
regard to the detailed composition of these categories. Thus certain phosphorus
compounds like parathion and thiometon applied to beans cause an increase in leaf
content of essential amino acids like methionin, valin and tryptophane.
In the case of DDT, when applied at 0.1 % to vines or pears, it has a positive effect on
protein synthesis which in turn affects the yield. Soon after application leaf content of
265
nitrogen and proteins rises while the content of reducing sugars falls. Similar results on
pears have been obtained by Kamal [1960]. It may well be that such an effect on leaf N
content is a major cause of the build-up of scale, particularly Panonychus ulmi (Chaboussou [1969]) after application of DDT. Nevertheless it is known that a substance
like DDT - the use of which is now banned - can cause physiological and biological
reactions in the plant which vary very much according to the initial condition of the
latter, specifically its auxin content. The same sort of thing applies in the case of
phosphorus insecticides and acaricides which can inhibit protein synthesis. In other
words they poison the plant at the same time as they poison the pest. This is evidenced
by the accumulation of free amino-acids and reducing sugars in the plant tissues.
One could imagine that such a process could render the plant more susceptible to
species of the genus Tetranychus whose nutritional needs are met by the high content of
these soluble substances in the plant. A well known case is that of the multiplication of
Eotetranychus orientalis studied by Wa/a et al. [op. cit.] following the use of various
acaricides like amidithion, formothion and demeton which was correlated with increased contents in the leaves of reducing sugars and amines. This phenomenon of the
multiplication of TetranychUs following the use of organophosphorus compounds
seems to be of fairly general occurrence (Dobrovski [1968], Chaboussou [1970]).
Furthermore, analogous effects are found following the use of several fungicides - or
rather 'anticryptogamics' - a preferable term which does not specify their mode of
action. Numerous organic compounds like maneb can result, at least early in growth,
in the promotion of protein synthesis. Treated plants in comparison to untreated show
increased leaf content of insoluble nitrogen compounds and decreased content of
reducing sugars. (Among other things we use the ratio NijRS as a criterion of effects
on the biochemistry of the plant. Ni signifies insoluble N, RS signifies reducing sugars).
As with insecticides, the effect of fungicides varies considerably according to the state
of the plant, particularly age of the leaves.
In practice then, while much depends on the timing and frequency of spray applications,
the reproduction of mites and particularly of yellow spider (Eotetranychus carpini)
seems to be related to a dominance of proteolysis over protein synthesis in the leaf.
This explains why certain oldicides like dinocap and binapacryl having curtailed the
development of Tetranychus by a direct toxic effect later on stimulate it by a trophic
effect (Oilb [1972]).
In addition to their effects on the relation between protein synthesis and proteolysis
these compounds produce significant changes in K, Ca, Mg and P contents. Thus it may
be suggested that, in a general way, leaf analysis could be used as an indicator of
conditions in the plant for the purpose of monitoring the rational use of spray chemicals as well as for indicating fertiliser requirements: yield and resistance always appear
to be linked, always on the condition that the rules of sound fertiliser use are respected.
3.3. Influence of the soil and of fertilisers
We have recently reviewed this subject at length, here we shall simply mention the main
points.
a) Attacks by insects and mites. There have been several investigations of the effects of
fertilisers or nutrient solution composition on the susceptibility of plants to attack by
266
insects or mites. Thus, the multiplication of P. lilmi is dependent on leaf N level which
varies both with season and N fertiliser use. In a general way the multiplication of
Tetranychlis is related to leaf nitrogen content. The same thing applies for both P. lilmi
and T.lirticae. Nevertheless the form of the nitrogen and, notably the nature of the
amino-acids present play a necessary part. On the other hand nitrogen is nO,t the only
nutrient element which influences the reproduction of the mite and the attraction
which the plant has for it. As indicated above compounds which are a source of energy,
like sugars, are also important.
The nitrogen to glucide ratio in conjunction with the cation content is influenced alike
by the type of rootstock, pesticide treatment and manuring. Thus, to cite only one
example, Fritzsche [1961] was able to show with beans that K deficiency caused an
increase soluble carbohydrates in the leaf and, in consequence, the'multiplication of
T.lirticae. We shall see later on how important correct fertiliser use is for improving
pest resistance in citrus.
b) Diseases. Fertilisers have been blamed for increasing susceptibility of plants to
disease, just as they have been blamed for increasing pest attack. Fertilisers like the
rootstock and pesticides also affect the composition of the leaf tissue.
In a general way one can say that nitrogen, or rather excess nitrogen, in soluble form
increases the susceptibility of plants to fungus disease. This is certainly the case for
rusts, oIdium in wheat and vine, apple speckle, mildew and botrytis on vine, sclerotinia
of carrot, etc.
Other nutrients mostly have effects· in the opposite direction to that of nitrogen,
potassium improves the plant's resistance to disease. In this context it is necessary to
emphasise that in the case of certain die-backs of citrus we are still very far from unravelling the various possible causal factors. Thus Shadha et al. [1970] thought that,
in the Punjab, die-back resulted from the interaction of a number of factors among
which they mentioned nutrient deficiencies and bad cultural practices. One may also
ask oneself to what extent the latter factors may be involved in the development of
disease and insect attack - some workers (Primavesi [1972]) are categoric on this
point. So much the more because sometimes simple soil treatment suffices to reduce the
ravages of pests and disease.
3.4. The influence of cultural methods and cultivation
Flanders [ 1970] has published an excellent paper on the complex relations between the
physiological state of the plant, scale insect attack and control of scale by natural
predators. According to him two ecological phenomena are closely correlated: (1) host
plant resistance to the coccid induced physiologically by the environment. (2) Resistance of the scale to the parasitic wasp physiologically induced by the host plant. In the
present context we are mainly concerned with the first point. The author refers particularly to the work of Thiem [1938] on the population dynamics of Lecanililn corni.
This showed that population decline of the scale was related to physiological conditions
in the host plant, a phenomenon which Thiem called 'pheno-immunity'.
L. corni is particularly sensitive to conditions in the host plant; Flanders had evidence
that plants which appeared to be resistant to the scale were physiologically different
from those which were infested. Pheno-immunity to coccids was exhibited in those
conditions which were generally considered to be favourable for growth of the plants.
267
It is otherwise under edaphic conditions unfavourable for growth whether due to
excessive humidity or drought or poor humus content or poor soil structure.
Thiem [1938] found that plants originally heavily infested could be improved. Soils
could be classified as 'infectious' or 'resistant' according to the degree of scale infestation on plants growing on them. But, infectious soils could be made resistant through
improved drainage, manuring and improved cultural practices.
In the case of Saissetia oleae Swaine and Duggan [1928] observed that attacks on
citrus varied not only between districts but also between different orchards and this
variation was traced to the influence of manuring and cultural methods. Cultivation
could have an effect through its effect on water relationships in the soil and from time
to time this appeared to be a determir.ant factor in coccid attack. It was noted that
swarms of Aonidiella aurantii only occurred on enfeebled trees.
Priesner [1938] noticed that E. corni was smaller and laid fewer eggs on resistant trees
than it did on susceptible hosts, and ascribed the decline in infestation simply to
changes in moisture conditions in the sub-soil. On the other hand, resistant soils could
become infectious as a result of degradation in soil structure. Priesner also observed
that trees already attacked by one coccid species could easily become infested with
other species or by insects of other groups. He also noticed that even insects with
damaged mouth parts could distinguish between weak and strong plants.
According to Thiem improvement of soil conditions (stagnant water, drought) were as
important as chemical improvement in promoting phenoimmunity. Trees in Cairo
were subject to attack by various coccids simply because they were planted under
asphalt.
In any case, according to this author, the internal plant processes were related to sap
composition which, in turh, depended mainly on soil physical conditions.
In this connection it is pointed out that aeration and temperature are the two main
factors influencing protein synthesis in the roots. Thus, Labananska et al. [1972] found
that the leaves of citrus growing on poorly areated soil contained less protein amino
acids but more non-protein amino-acids like lysine, arginine, aspartic acid and
proline. The amino-acids, amides and amines represent the major part of soluble
nitrogen compounds in the plant and their role is fundamental since they are the
building blocks for proteins. Plant nutritionists are also showing a growing interest in
the effect of root environment on the plant. Thus on the subject of disease Klotz et al.
have pointed out that good aeration in the rooting zone has a highly beneficial effect in
Phytophthora infestation of citrus. Such a phenomenon is probably related to a decrease
in soluble nitrogen compounds in the plant tissues which seems to be a process generally
concerned in plant resistance.
3.5. Biochemical conditions and plant resistance
All the above - and as we have already shown elsewhere (Chaboussou [1972]) - it
seems that nutritional conditions are offundamental importance in the relation between
the plant and its attacker whether this be insect, mite, fungus or even virus. In particular
sucking arthropods like coccids, jassids, thrips or mites appear to be particularly
sensitive to changes in internal conditions in the plant. This sensitivity appears to be
related to high amino-acid content in the sap (more particularly perhaps that of a nonprotein nature) as well as high reducing sugar content. Such a physiological condition
corresponds with defective protein synthesis caused by the operation of various factors
268
like unsuitable rootstock, defective root aeration, poor sap circulation, various pesticide treatments and finally fertilisers. In a general way this also applies to susceptibility
to disease. Thus Dufrenoy [1936J wrote: 'Every circumstance which is unfavourable to
the formation of new cytoplasm tends to cause the accumulation in the cell vacuole of
useless soluble compounds: sugars and amino-acids; this accumulation of soluble
compounds appears to favour the nutrition of parasitic micro-organisms' and thus to
lessen the resistance of the plant to parasitic diseases.' The same author remarked that
such a disturbance in metabolism could result from unbalanced manuring, particularly
with respect to the NPK ratio. This was the case, as we have seen above, in certain
parts of Morocco. This is why it seems to us essential straight away to attempt to show
the benefits to be expected from correction of the fertiliser treatment. We start with the
fact that in certain areas like the Rharb the trees suffer from an excess of calcium
because of the nature of the soil and irrigation ~ater. (Nadir [op. cif.J).
4. Adjustment of citrus physiology as a means of countering coccid attack
4.1. Regression of coccids on mandarins under the influence of K-fertilisation
We had the opportunity to benefit from the fertiliser experiments conducted by Nadir,
starting in 1965, on a plot of mandarins at Sidi Bouknadel, Morocco. These experiments, which were originally purely agronomic, aimed to show that a massive appli"
cation of potassium to the soil caused an increase in K content of the leaf and simultaneously a reduction in calcium. The four treatments comprised; control, CaC0 3 ,
K ZS0 4 and KN0 3 each applied at 3 kg per tree and per annum. Our plan was to study,
commencing in 1970, the insect fauna on the young trees and, more particularly, the
coccid population. The two main species observed were Lepidosaphes beckii and
Saissefia oleae.
Four series of observations were made annually in mid April, mid July, mid October
on the leaves and mid December on the fruit. These observations' were made on two .
trees out of the total of eight receiving the relevant fertiliser treatment. On each
occasion we examined 50 leaves, 10 twigs and ten fruits at the north, south, east and
west of the canopy, half from the centre and half from the outside of the tree. The counts
were made on the plots with the aid of a magnifying glass. Tables 2 and 3 give the
results of these observations.
Table 2. Development of Lepidosaphes beckii populations on mandarins under various fertiliser
treatments. 1970
Treatment
Control.....
.
K 2 SO.
CaC0 3 • . • . • • • • • • . • • • • • •
KN0 3 • • • • • • • • • • • • • • . • • •
No. of individuals on leaves
No. of individuals on fruit
April
8
129
63
69
July
October
December
28
287
8
280
100
656
97
224
3163
1743
9451
1673
Mme Skitarelic's results - Sidi Bouknadel
269
Table 3. Saissetia oleae populations on mandarins under various fertiliser treatments. 1970
(Mme Skitarelic)
Treatment
Control. .. . . .. .. . .. .. . .. . . .. ... ....
K ZS0 4 ••••••••••••••••••••••••••••
CaCO s
KNO s .............................
Observations on leaves (400)
On fruits (80)
April
July
October
December
19
49
30
25
117
66
81
38
63
51
45
48
194
99
258
82
The results obtained in 1971 for various coccids are shown in Table 4 and confirm
those obtained in 1970.
Table 4. Results of observations in April 1971 - Sidi Bouknadel (Mme Skitarelic)
Treatment
No. of individuals on 400 leaves
L. Beckii
S.oleae
P. ziziphi
L. Beckii
S. oleae
P. ziziphi
Control ........
K ZS0 4 . . . . . . . .
CaCO s ........
KNO s .........
4009
1386
7325
1372
75
54
116
33
132
54
116
33
216
90
765
41
38
33
46
13
104
20
49
No. of individuals on 80 fruit
10000
/ CaC 03
/
/
/
/
/
7000
I
/
/
/
/
/
I
I
/
/
5000
/
/
/
/
/
/
/
3000
/
/
I
2500
I
,
/
/
1500
April
,/ '
I
/
I
500
/
I
///
/
~~?~//"'
July
October
,
Control
/
'
/
K2 S04
"'.:',;.... KN03
........
December
Fig. 1. Lepidosaphes beckii Newman counts on mandarins. Sidi Bouknadel, 1970.
270
?
Figures 1-4 illustrate these results. Figure 1 concerning L. Beckii shows that though
growth of the population for the first 9 months of 1970 was only slight one can nevertheless see that there was a larger population growth under the Caco 3 treatment. On
,the other hand, at harvest time when the insects congregate on the fruit the population
difference had become very great, the Caco3 treatment having three times as high a
population as the control while it was reduced by a half on the treatments with
potassium nitrate or sulphate.
From 1971 the differences were even greater, especially on the leaves and twigs, the
potassium treatments having only one third the population of the control (Figure 2).
The population of Saissetia oleae shows similar behaviour to that of L. beckii. There
are similar reductions, compared with control, in the potash treatments and an increase - less marked it is true but real - under the CaC03 treatment (Figure 4).
These results show clearly that the mode of multiplication of coccids is in effect linked,
as for other insects, with nutritional factors. Put in another way, the population
differences appear to follow differences in composition of the plant and notably of the
sap. One may validly conclude from the results obtained that this differentiation is the
result of the setting up in the plant of a particular cationic balance for each treatment.
From 1968, that is 10 months after beginning the experiment, analysis showed an
increase in K content and a decrease in Ca content of the leaves. Analyses of the leaves
and bark made by Nadir gave the results shown in Tables 5 and 6.
nLeaves
[ Twigs
CO")
0
800
765
u
'"
8000
u
700
600
500
400
300
200
100
Fig. 2. L. beckii counts on variously treated mandarins. Sidi Bouknadel, 30/4/71.
271
Table 5. Leaf analysis of mandarins under various fettiliser treatments - 10 October 1969 % DM
Treatment
N
P
K
Ca
Mg
K
Ca+Mg
K 2 S0 4 ........
CaC0 3 . . . . . . . .
KN03 . . . . . . . . .
Control ........
2.775
2.596
2.827
2.626
0.147
0.128
0.147
0.119
2.427
0.787
2.348
0.739
4.262
5.724
3.633
5.572
0.117
0.298
0.118
0.256
0.554
0.130
0.626
0.126
Table 6. Analysis of mandarin rind - 10 October 1969 % DM
Treatment
N
P
K
Ca
Mg
K
Ca+Mg
K 2 S0 4 ........
CaC0 3 .- ......
KN0 3 . . . . . . . . .
Control ........
1.309
1.262
1.297
1.410
0.102
0.089
0.094
0.099
1.629
0.771
1.374
0.887
0.420
0.633
1.374
0.887
0.052
0.079
0.053
0.062
3.451
1.082
2.511
2.513
Thus the potassium treatments have produced similar results in raising the K content
of the rind as they did in the leaves. At the same time there was a reduction in Ca and
M
o
U
9450
III
U
I
\
.,
\
\
\
\
\
\ g
"\ C
0
3163
\u
\
1743
1673
o
1,5
2
2,5
3
3,4
K/Ca.Mg in rind on 10110/69
Fig. 3. L. beckii counts on mandarins at harvest. 1970 (total of 80 fruit).
272
Mg levels, so that the K/Ca + Mg ratio is effectively altered in the trees manured with
both types of potash fertiliser. Figures 3 and 4 illustrate the relation between the
populations of L.Beckii and S.oleae on the fruits atharvest in 1970 and the K/Ca + Mg
ratio measured in October 1969. One can well believe that after four years oftreatm~pt
leaf analysis would tend to reach values which would alter little from then on. Thus it
appears to have been well demonstrated that the decline in populations of these two
coccids was correlated with an increase in the ratio K/Ca + Mg in the respective organs.
Such a cationic balance establishes in the plant biochemical conditions which are unfavourable for the biotic potenital of these inse'cts. As Steyn has already demonstrated,
the breeding cycle is probably lengthened and further the biochemistry of the citrus
will also affect the fecundity of the pests. Flanders [op. cif.] has shown that this is less
on resistant plants.
.
It is further probable that, correlated with these two aspects of multiplication, this
modification of the physiology of the citrus plant will have effects on the attraction of
the pests by the plants. Thus, as regards the preference of the coccids for different
organs, Delucchi [1965] noticed that in the Rharb in autumn the density of Californian
red scale was always higher on the fruit than on the leaves or branches. This pheno-
258
194
99
82
o
1,5
2
2,5
3
3,4
K/Ca.Mg in rind on 10110/69
Fig. 4. S. oleae counts on mandarins at harvest. 1970 (total of 80 fruit).
273
menon is probably of a chemotrophic nature and one may suppose that an analogous
mechanism is at work in the choice of the coccids for whole plants which differ physiologically. Delacchi has also emphasised that only the populations on the fruits are able
to survive lethal or sub-lethal climatic conditions. This shows the importance of th~
nutrition of the insect in its resistance to destruction by external agents and thus in its
virulence. That this idea is well founded is confirmed by Bri1ning and Obel [1969-1971]
who worked on the effect of various amendments on other species of coccid on a
deciduous tree, the oak.
4.2. Citrus physiology in the practical control of coccids
(a) Leaf analysis, crop yield and coccid resistance
High yield and pest resistance are by no means incompatible. Thus, Calvert and Smith
[1972] drew attention to the disadvantage of too high Ca levels in the soil. Such an
imbalance caused premature fruit drop, the fruit remaining small, thin skinned and
high in sugar. Analysis of the leaves showed that the K level was only from 0.56 to 0.84.
According to Nadir [1974] a good yield requires a K content above 1% and K higher
than N. Calcium appears to restrain the uptake ofK by the roots. We have shown how
by correcting the cationic balance to raise the KjCa + Mg ratio the resistance of
mandarins to coccids is improved and such leaf analysis values are precisely those
which the agronomists think desirable for maximum yield.
Much work has been done on the mineral nutrition of citrus and this has been summarised in a booklet published by the International Potash Institate [1958]. According
to Chapman who is an achnowledged expert in this field the desirable nutrient levels
are those shown in Table 7, which refer to leaves aged from 4 to 10 months taken from
the fruiting branches.
Table 7. Optimum leaf analytical values for Citrus according to Chapman % DM
Element
N
p
K
Ca
Mg
Na
Value.. ... .. ...
2.2-2.7
0.12-0.18
1.00-1.70
3.0-6.0
0.30-0.60
0.1-0.15
The results obtained at Sidi Bouknadel indicate that the leaf levels aimed at for coccid
resistance on Mandarins were precisely those which the agronomist would desire. Thus
the K ZS0 4 treatment compared with control raised K from 0.739 to 2.427, a desirable
increase; reduced Ca from 5.572 to 4.262, a desirable lowering; reduced Mg from
0.256 to 0.117, possibly too low, and raised N from 2.626 to 2.775, a slight change only
and probably due to the form of nitrogen. The ratio KjCa + Mg, which we have used
as an index of resistance to coccid attack varies according to Chapman's figures between 0.12 and 0.51. Table 8 gives values of this ratio determined by Nadir.
Table 8. Values for K/Ca + Mg in leaves and fruit of mandarins
K/Ca + Mg
Control
Leaves
Fruit . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
0.126
0.513
274
0.130
1.082
0.554
3.451
0.626
2.511
If we compare the figures obtained by Steyn [op. cit.] we see that the value for
K/Ca + Mg changed from 0.24 for control, the most seriously attacked by coccids, to
0.67 for the low Ca treatment which, we recall, resulted in good resistance to the pest,
Aonidiella aurantii. One cannot fail to be struck by the agreement between the results.
It seems to be well confirmed that raising this ratio to around 0.5 or 0.6 is favourable
for both resistance and growth. Protein synthesis, yield and pest resistance are all
bound up with optimising physiological conditions in the plant.
We should now like to examine briefly empirical results obtained on a commercial
holding in Morocco.
(b) Cultural practice and coccid resistance
The results obtained in practice on a commercial holding in Morocco* are presented
as a logical follow-up to the preceding section. Fertilisers played a large part.
Insecticide treatment
Like most farmers in the Rharb M. Leonardi* has had to face two problems, which as
we have seen are connected: multiplication of Californian red scale and swarming of
mites. The latter reached such a level that they denuded the trees causing premature
leaf fall. At that time the routine measure against. A. aUrantii was two parathion sprays,
in May and September. As we have seen above this compound is particularly apt to
stimulate the development of mites. Should one therefore use an acaricide which does
not always have the hoped for effect and this for the simple rea30n that, as we have seen
above, after producing an initial set back to the pest numerous acaricides can cause the
multiplication of both mites and scales!
Among other things M. Leonardi had noticed on a plot of clementines signs of zinc
deficiency which is caused by excess lime in the soil, which also promotes the multiplication of coccids. To cure this inconvenience M. Leonardi applied zineb three times.
He also omitted the September parathion spray. These measures resulted in an
immediate and definite decline in mite population. From the second year the spray
applied in May consisted of a mixture of parathion and zineb, and there were three
other zineb treatments between May and September. This has been the routine treatment each year since 1968.
Fertiliser programme
This is characterised by complete omission of phosphorus. Since 1967-1968 the rates
applied per tree were as follows:
in February 2.5 kg ammonium sulphate
3 kg potassium sulphate
0.3 kg copper sulphate (Cu deficiency)
in May-June 2 kg ammonium nitrate
These mineral fertilis~rs are supported by a generous application of dung and four
times yearly spraying of the trees with a formulation containing trace elements and
vitamins.
* This is concerned with the cultural methods used by M. Leonardi, estate agent to H. M. Hassan II
at Sidi Moussa and Sidi Slimane Morocco. We are grateful for his help and for the welcome he
gave us.
275
Results
The proportion of harvested fruit which is marketable which depends very much on
the level of scale contamination* varies from 92-98%. Marbling is virtually nonexistent**.
In the light of the results we obtained at Sidi Bouknadel it seems likely that the excellent results can be ascribed to the improvement in the biochemistry of the leaves
which has taken place since the institution of the improved practices. This is supported
by comparison of leaf analyses made in 1967 and 1969, two years after the modifications were introduced. This is shown in Table 9.
Table 9. Changes in leaf analysis - variety Valencia
Date
8/9/67 ..........
3/9/69 ..........
% ofDM
mg/kg DM
N
P
K
Ca
Mg
Zn
Mn
Cu
B
2.94
2.78
0.20
0.23
1.28
1.40
5.02
3.20
0.38
0.24
19
20
41
11
13
8
237
102
These values are not strictly comparable with those obtained at Sidi Bouknadel by
Nadir on mandarins. In the first place different varieties are involved and, secondly, the
method of leaf sampling probably differed. However, analogous results followed the
application of potash fertilizers in both orchards. Once again we see an increase in K
content correlated with a lowering in Ca and Mg. In only two years the K/Ca + Mg
ratio was shifted from 0.28 to above 0.40. As at Sidi Bouknadel the raising of this ratio
is seen to benefit resistance to coccids. In turn, this thinning out of coccids and the
abandonment of the autumn parathion treatment which this allowed is in large measure
responsible for the decline in mites. We should emphasise that the biochemical changes
which stimulated resistance to pests were induced by the joint action not only of mineral
fertilisers and spraying the foliage but also by the generous applications of farmyard
manure. It is probable that these organic manures, whose effectiveness in pest and
disease resistance have for long been recognised, act through their trace element content
and the growth substances which they contain. It would be worth studying these
effects in greater detail.
We shall now examine to what extent foliar application along with soil application of
fertiliser can be of use in protecting citrus against pest attack.
Spraying with potassium fertiliser
Ca/vert and Smith [1972J pointed out that it is difficult on calcareous soils - not the
case at Sidi Bouknadel - to raise leaf K levels in citrus, except to a very limited extent,
by soil application of potassium fertiliser. These authors noted that leaf K contents of
citrus from 0.5 to 0.8% were by no means rare on calcareous soils. However, maximum
yield on such soils was associated with leaf K levels of I % and more. Therefore the use
ofKN0 3 sprays was considered to correct the K deficiency. This was quite apart from
the fact that such spraying had already been shown to have a beneficial effect on pitting.
* Tolerable contamination level -
3 coccids per fruit.
Marbling and pitting are significantly reduced by potash fertiliser or dusting with KN0 3 (lanes
et al. [1967]).
H
276
According to Ca/vert and Smith [op. cit.] spraying the leaves witn KN03 was more
effective in raising leaf K content than application of the equivalent amount of fertiliser
to the soil. They emphasised also that the correction of K deficiency was of the
greatest importance in citrus, potassium having a greater influence on fruit quality than
any other element. Visual symptoms of this deficiency are rare. The effects of K
deficiency on fruit production, growth and premature leaf fall are felt before the leaf
symptoms are seen.
Spraying with potassium salts is of double interest: first they offer a new method of
influencing cationic balance in the leaf in order to improve its metabolism and the
resistance of the plant, secondly the method is quick and convenient and has a rapid
effect, albeit sometimes temporary. The absorption of KN0 3 can be traced by analysis
before and after application: it is absorbed by both upper and lower leaf surfaces, it is
rapid and takes place in the week following spraying. Nadir's work has shown that
treatment with potassium nitrate causes an 'increase in leaf potassium in the course of
the 15 days following application accompanied by an improvement in the KjCa ratio.
The same author showed that K is first held in the young leaves and only migrates later
to the older leaves. Nadir also showed that the raising of the K level carried over to the
following year, thus, five KN0 3 treatments in 1964 raised K levels and lowered Ca in
1965.
On the other hand, according to Ca/vert [1969] K content is only raised temporarily
and returns to the original level four weeks after spraying. However, as the same author
was able to show evidence of response in fruit quality and yield as a result of spraying
it appeared logical to conclude that K had been translocated and utilised in the
metabolism of the whole tree.
According to Ca/vert and Smith [op. cit.] to avoid scorch and shedding of the older
, leaves and necrosis on the young leaves the safe application rate varies between 4.54
and 9.07 kg KN0 3 in 380 litres water. The lower rate was used without any inconvenience by Ca/vert in three applications made respectively in May July and October.
This was sufficient to maintain K at the desired level during the growth period. Wetting
or solubilising agents like DMSO help the dissolving and penetration of the potassium
nitrate. Sprays containing 1-5 g KN0 3 per litre with addition of DMSO at 5-10 gjl
have been suggested.
Finally it should be said that KN0 3 sprays are quite compatible with trace elements
like zinc, manganese or copper. Even so such trace element applications should only be
used with caution and after preliminary trial. While in Morocco favourable effects of
zinc oxide applied with certain insecticides have been noted, Thompson [1929]
recorded multiplication of coccids and Paratetranychlis citri after using sprays based on
zinc sulphate.
It'seems that the desired adjustments to the plant'smetabolism are sometimes difficult
to achieve and also difficult to determine with exactitude. Figures we have given for
leaf analysis are only an approximation to the ideal desired. However, encouraging
results have already been obtained on the effect of foliar application on certain mites.
We shall conclude this chapter with an example of this kind.
4.3. Reduction of Brevipalpus population by treatment with potassium nitrate
In accordance with our views' on the trophic determination of the multiplication of
some mite species, XXX M. Willinsky in Morocco has shown at Sidi Slimane (Socamri)
277
that KN0 3 sprays reduced the numbers of Brevipalpus. While on 6/10/69 he founds
a mean of 1.33 individuals per fruit on the controls there were never more than
0.44 - three times fewer - on the plots treated with KN0 3 . (This confirms results we
have obtained in the laboratory with T.urticae on vines receiving analogous treatments.) As for the cause of the population reduction it is probably similar to that
involved in reducing the population of L. beckii and S.oleae on trees manured with
potassium. Following the raising of the K level and consequent adjustment of the
cationic balance in the leaf, protein synthesis is intensified with concurrent reduction in
the content of soluble substances: this results in a lowering of the biotic potential of
mites as it does in the case of coccids.
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280
Relationships between Fertilization and Tree Resistance
to Forest Insect Pests
Dr. H.Bogenschiitz and Dr. E.Konig, Forstliche Versuchs- und Forschungsanstalt Baden-Wiirttemberg - Abt. Waldschutz - Stegen-WittentalfFederal Republic of Germany
Summary
Fertilization in forest stands can influence the population dynamics of forest insect pests. Leaf- and
needle-feeding insect populations are reduced after .fertilization with N, P and Ca, and aphids and
spider mites decrease with K treatments. Thesegeneral rules however, as shown by new results, do
not always hold true. Variations in the plants, including influences by site and climate differences,
and variations in the insect pests and their reactions, lead to differing test results.
Fertilization induces physiological, morphological and phenological changes in plants. These
changes, in turn, affect the population dynamics of phytophagous insects. Examples are cited.
The entomological aspect of fertilization represents a step towards stabilization of the nutritional
quality of forest stands, which in turn - together with natural enemies - leads to stabilization of
population densities of forest pests.
Resume
La fertilisation des peuplements forestiers peut avoir une influence sur la dynamique des populations
d'insectes ravageurs des arbres forestiers. Les populations d'insectes se nourrissant d'aiguilles et de
feuilles sont rectuites sous l'effet des fumures azotee, phosphatee et apres des applications de chaux,
tandis que les attaques par les aphides et les acariens sont diminuees sous l'effet de la fertilisation
potassique. Toutefois, il la lumiere de resultats recents, ces regles generales ne sont pas toujours
valables. Des variations qui se presentent chez les plantes, y compris les influences exercees par les
conditions du site et les differences climatiques, ainsi que des changements chez les insectes ravageurs
et les reactions de ceux-ci, conduisent il des resultats qui peuvent differer d'une essai ill'autre.
La fertilisation engendre des changements physiologiques, morphologiques et phenologiques chez
les plantes. De leur cote, ces changements affectent la dynamique des populations phytophages. Les
auteurs en citent des exemples.
L'aspect entomologique de la fertilisation represente un pas en avant vers la stabilisation de la
qualite nutritionelle des peuplements forestiers. De son cote, la qualite nutritionelle conduit - conjointement avec l'action des ennemis naturels - il la stabilisation des densites de population des
insectes ravageurs dans les forets.
Introduction
A tree is resistant to forest insect pests when its probability of successful utilization
as a host is reduced. Strictly speaking this definition only refers to genetically
determined characteristics of the plant. Temporary resistance, however, induced by
environmental conditions - including fertilization - rather should be called pseudoresistance. In the following report resistance will be used in the later sense.
28\
In considering the relationship between fertilization and tree resistance to forest
insect pests, we would like to begin with the following remark: 'The improvement of
the biological condition and fertility of the soil increases the possibility of the forest
reaching its desired economical state' (Wittich [38]). Whereas in the past, wood
production has been the primary economic goal of the forest, recently the social values
of the forest are increasingly recognized. In accordance with this development, the
increase of wood production by supplementation of the soil with plant nutrients, is
receiving much attention (Baule and Fricker [2]).
Today fertilization is viewed as a method through which disturbed ecosystems can
recover a healthy balance (Baule [1]). A forest is considered healthy when it fulfils
the set management goals (wood production, recreation, social values). The attainment
of these goals can be delayed or prevented by outbreaks of phytophagous insects.
Therefore, attention must be given to resistance of each individual tree. In the 1950's
Biittner [5], Merker [l6] and Oldiges [21] were among the first to prove that tree
resistance to insect pests is increased as a result of fertilization. This realization was
more significant at a time when publications were questioning pesticide use. The
exaggerated hope that the use of insecticides could be curtailed by fertilization was
subdued by new results (Thalenhorst [35]). Nevertheless fertilization is a meaningful
tool of integrated pest management (Franz [la], Eichhorn [7]).
The following discussion will be divided into two sections. The first is a short summary
of past investigations on the relationship between fertilization and occurrence of
insect pests. The second part deals with the reasons for these relationships in more
detail.
The effect of fertilization in forest stands
There have been many reports written describing the difference in insect populations
on fertilized and untreated areas. It is not intended to describe these results in detail
here. Summaries have been written on this subject, for example by Baule [1], Merker
[18] and Schindler [24]. Thalenhorst [33] summarized the pertinent literature printed
in German up to 1972. A few new experiments are mentioned below.
It has been shown, that the reaction of leaf-feeding larvae on fertilization differs from
that of sap sucking insects and bark beetles. Therefore these three groups of insects
are dealt with separately.
1. The influence of fertilization on leaf- and needle-consuming larvae of lepidoptera and of
sawflies
Fertilization with nitrogen, phosphorus and calcium caused a decrease in the above
insect populations. Populations increased, however, with applications of potassium
and certain trace elements (Baule and Fricker [2], Thalenhorst [35]). This was
determined by tests with Lymantria monacha L., L. dispar L., Bupalus piniarius L.,
Rhyacionia buoliana Den. u. Schiff., Coleophora laricella Hb., Diprion pini L., Pristiphora abietina Christ, and Brachyderes incanus L. Negative results have also been
reported, as indicated in the following tests: Spruce stands were treated with 200 kg
282
nitrogen per ha. No significant difference in populations of the sawfly-Iarvae of
Pristiphora abietina on fertilized and unfertilized sites could be determined (Schwerdtjeger [30]). Another test with the same species also showed no significant results
(Gussone and Zottl [13 J). In this case sites were treated with 100 kg NJha or with a
complete fertilizer.
Reports of fertilization effects on Rhyacionia buoliana varied. A population decrease
was reported by Merker and Biittner [19], Nej [20], Schindler [24], Schindler and
Baule [25] and Wellenstein [37]; population increase was noted by Eidmann and
Ingestad [9] and BIirzynski [6]. The reasons for these differences may be determined
by examination of the individual sites: On sites unsuited for Pinus sylvestris, living
conditions for insects are also poor. When conditions are improved, for example by
fertilization, the pines offer better conditions for the pest and populations increase. If
by fertilization the tree resistance is increased above the level suitable for insect attack,
then the pest population will decrease accordingly (Eidmann [8]). Merker [18]
concluded that in those tests reporting negative results, the amount of fertilizer was not
sufficient.
These examples illustrate that results can be applied only to certain site conditions
(climate, soil condition). General conclusions cannot be drawn for all sites. This
applies also to potassium application and the resulting increase in insect populations.
Tests in Belgium revealed that the European pine shoot moth popu\ation decreased
after potassium treatment (Nej[20]). In the USA, pure nitrogen fertilizer had no
effect on the density of the same pest; phosphates led to a density decrease; when
potassium was added to the phosphate, the decrease was more evident (Pritchet and
Smith [23]).
Needle-feeding species not mentioned .above were examined by Thalenhorst [35]
and Wellenstein [37]. In nutrient deficiency experiments of Thalenhorst in a spruce
stand, the effect on Eucosma tedella (Cl.) (Tortricidae) and Pristiphora ambigua (Fall.)
(Tenthredinidae) were studied. These results will be discussed in the next section.
Wellenstein found that fertilization of young pines (Pinus sylvestris) with compost
caused a 50% decrease in population density of Brachyderes incanus L. (Cucurlionidae).
2. The effects of fertilization on sap-sucking insects and spider mites
While nitrogen fertilization inhibits the population development of defoliators, it
induces population increase of sap-sucking insects. Treatment with potassium,
however, inhibits population growth of sucking insects. Consequently, the population
increase due to nitrogen fertilization can be partially counteracted by the application
of potassium fertilizer (Baule [1]). Briinning and Uebel found these results of laboratory and field experiments with Eulecanium comi Bche. and E. rujulum Ckll. (Coccidae)
on locust and red oak trees [4]. Merker [18], however, stated as follows: 'No uniform
effects have been observed on our native aphids due to the fertilization of their plant
hosts. On some aphids, such as fir Adelgidae, fertilization has no effect. The effects
on others (e.g. Lachnidae) cannot be generalized; they are sometimes detrimental,
but not always. Some aphids may undergo enormous population increases when their
host trees are fertilized'.
Nitrogen fertilizer also promotes the population growth of mites. Thalenhorst [35]
studied the spruce mite, Oligonychus· ununguis Jac., bark aphids (Lachnidae) and
the spruce gall aphid Sacchiphantes abietis. The results of his soil nutrient deficiency
283
experiments with these insects are shown in Table 1. They are summarized as follows:
a) The population development of Lachnidae and of Oligonychus ununguis is promoted
by NPK or PK; PK fertilization inhibits more than NK fertilization. This agrees
with the above mentioned results.
b) Sacchiphantes abietis shows little reaction to fertilization.
c) Eucosma tedella is inhibited by the combinations NK, NP and NPK, but is promoted by PK fertilization. These results agree with the general rule.
d) The population growth of Pritiphora ambigua is stimulated by all the fertilizers
tested.
Table 1. Influence of fertilization on the abundance of spruce insects (according to Thalenhorst
[35}J
Influence
Oligonychus
ununguis
clearly negative ...
untreated, PK untreated
slightly negative ...
unclear ..........
PK,NK
NP
NP, NPK
Sacchiphantes
abietis
Eucosma
tedella
Pristiphora
ambigua
NK,NP
untreated
PK
NPK
NK
untreated, NP
NK
slightly positive ...
clearly positive ....
Lachnidae
NPK
NPK
NPK
untreated
PK,NK
PK
NP
All these results on the effects of fertilization on defoliating insects or on aphids
cannot be generalized. Further methodical experiments are necessary to reach satisfactory conclusions.
3. The effect of fertilization on bark beetles
This group of insect pests must be dealt with seperately from those already mentioned.
The susceptibility of trees to bark beetle attack depends upon the trees turgidity (osmotic pressure). The addition of 1000 kg of calcium ammonium nitrate per hectare
to endangered conifer stands increased the osmotic pressure to such a point that
attacks by the fir engraver Pityokteines curvidens Germ., 1ps typographus L. and
related species were repelled. It is suspected that the effects last approximately 4-5
years (Merker [18]). This type of fertilization should be repeated on a rotating basis
since the tree's susceptibility is dependent on weather conditions and is therefore
unpredictable (Schindler [24]).
In concluding the first part of this paper, the effects of fertilization on damage due to
browsing (Thalenhorst [34]), wind, snow, salt, pollution, frost and drought (Baule
[ 1]) should be briefly mentioned. Browsing damage increases after fertilization, while
the damaging effects of the others decline.
The causal connections: fertilization - plant - insect damage from an entomological point of view
As a result of fertilization, plants have access to more nutrients and water. The water
capacity of the soil is increased by improving the humus. The resulting changes in the
plant are primarily physiological, but their morphology and phenology are also affected.
284
Figure 1 demonstrates fertilization-induced changes in plants which affect phytophagous insects. The abundance of these insects is variable; population increase is a
function of fertility and immigration, while population decrease depends on mortality
and emigration.
Referring to the subject of this paper, one of the key question is how population dynamics ofphytophagous insects are influenced by fertilization-induced changes in the host.
The entomologist is qualified to answer only this.
Fertilization
Phytophagous insects
Plants
Morphology .
Leaf and needle
structures
--<
Chemical reactions
Physiology
Phenology
~---,.
Fertility
Mortality
I
Water balance
_.- Leafing
Immigration
?~
~
Abundan",
Emigration
Entomophagous insects
Fig. 1. Chain of the effect of fertilization.
1. The effect of physiological
changes
Fertilization mainly affects the plants' metabolism, for example the rati.o of proteins
to carbohydrates in needles and leaves, in favour of proteins (Schwenke [27]).
It has been suggested that the nutritional content of the leaves decreases as a result of
this phenomenon. Several authors, however, have reservations about this hypothesis
(e.g. Eidmann [8], Merker [18]). Recently Lunderstiidt and Hoppe [15] studied the
nutritional value of spruce needles for larvae of the sawfly Gilpinia hercyniae Htg. They
found no evidence that the relationship between carbohydrates and proteins was a
determining factor in decreasing the nutritional value of the leaves.
The actual changes in metabolism of forest trees resulting from fertilization have not
yet been determined. However, there is no doubt that any change in the nutritional
value of the host plants influences the fertility and thus the abundance of phytophagous
insects (Schwerdtfeger [28, 29]).
Secondary metabolites such as phenoles, waxes and terpenes play a predominant role
in plant resistance. For example, the volatile fraction of conifer oleoresin, mainly
monoterpenes, produced by trees, especially when available water has decreased,
may act as primary attractants to bark beetles (summary by Postner (27]). Also,
285
attack by the European pine shoot moth is dependent on the content ofcertain essential
oils of pines (Smeljanez [3 J}) .
Many researchers examining tree susceptibility to insect pest attack assume that
fertilization increases water content. Eidmann [8], however, stated that trees exposed
to a high nitrogen level reacted by reducing root expansion; therefore the total water
absorption capacity was decreased rather than increased.
Nevertheless it is certain that the turgidity of conifers, which have been invaded but
only slightly damaged, rises as a result of irrigation but also of fertilizer treatment.
Bark beetle larvae present in the tree before treatment react to such a change by
consuming water, swelling and consequently dying (Merker [18]).
The resin system of conifers is a defense mechanism often activated upon attack by
phytophagous insects. The physical characters of resin, especially the exudation,
are also dependent upon the water content of the plant tissues. Contact with resin
may result in the death or dispersal of the attacking pest. [Results from bark beetles
( Merker [27]), the American white-pine weevil, Pissodes strobi (Peck) (van Buijtenen
and Santamour [36]) the European pine shoot moth (SchrOder [26], compare to the
negative results of Sme!janez and Matowich [32])].
2. The effect of morphological changes
Changes in metabolism influence plant growth and therefore plant form and structure.
Thalenhorst [35] studied the effects of fertilization on the needle structure of spruce.
He found that needle density, length, and thickness, as well as the width of the stomatic
stripes, varied greatly among individual trees.
Although all changes resulting from any of the tested exogenous factors -site, weather,
or fertilization - were within the range of individual variation, the changes in needle
structure due to fertilization were marked (Table 2). In some cases Thalenhorst was
able to identify the function of the host tree's resistance mechanisms. For example,
Eucosma tedella chose shoots with needles of high density and thickness for egg laying
purposes. These needle characteristics are reduced by nitrogen fertilization. Thus
fertilization indirectly influences the instinctive orientation mechanism of this insect
which is responsible for the infestation of individual trees. Fiihrer [11] showed
that the hardness of the stomatic stripe, the preferred entrance area of these larvae,
varied amoung individual trees and from species to species. It is possible that these
mechanical differences are due to site characteristics. If so, fertilization could indirectly
influence this type of morphological change, which can act as a mortality factor.This
possibility, however, must stilI be investigated (compare to the experiments of Huang
[ 14] on the relationships between morphological characteristics of spruce needles
and the egg laying behaviour of Gilpinia hercyniae).
3. The effect of phenological changes
The phenology of plants is also affected by fertilization, which can in this way influence
the population dynamics of pest insects. Thalenhorst [35] showed that on spruce
286
Table 2. Relationship between fertilization and the needle characteristics of spruce (according to
Thalenhorst [35])
untreated, PK
NK,NP
NPK
.
.
.
Needle
density
Needle
length
Needle
thickness
Stomatic
stripes
high
medium
low
low
medium
high
high
low
medium
narrow
} wider
treated with nitrogen fertilizer buds opened earlier than on untreated trees. The females
of Pristiphora abietina lay their eggs in spruce buds, where the' scales have already
fallen off, but the needles are still compactly bundled together. Since fertilization
affects the timing of this stage, the females are forced to disperse to' trees with late
development. This change in the timing of bud burst, which gives spruce a temporary
resistance to attack, can also be induced by weather conditions. Such a change in
phenology can lead to the mortality of less mobile insects or larval stages. The connection between the phenological pattern of bud burst shown by young spruce trees
and attack by Sacchiphantes abietis should be mentioned here. The resistance of
certain spruces to the development of spruce galls depends in part on faulty.timing
between budburst and the development of the aphids (Bischoff, Ewert und Thalenhorst [3}). See Schwerdtfeger [28} for the relationships between the development
patterns of plants and trophic responses of insects.
Concluding remark
The presentation thus far clearly demonstrates that our knowledge of the effects of
fertilization on the populations of various insect pests is rather sketchy. It is obvious
that much research must still be done involving the concerted efforts of botanists
(physiologists, anatomists), entomologists and soil scientists to resolve this problem.
In conclusion we would like to mention the effects on the survival of predators and
parasites, when the abundance of phytophagous insects, which they depend upon,
are changed. Recently Fiihrer [I2} pointed to the risk of outbreak among pest species,
naturally held in check by predators and parasites, when their abundance falls below
a minimum density level. However, this risk need not be taken into account when
dealing with control methods using fertilizer, since fertilization rarely, if ever, causes
a population reduction of more than 50%. In this light, the limited ability offertilization
to reduce pest populations attains a positive significance.
In the search to decrease the susceptibility of forest stands to catastrophic pest
outbreaks, the problem of stabilizing the nutritional quality of the soil is of greater
importance than that of individual tree resistance. The solution to this problem can
be greatly facilitated by fertilization techniques.
Acknowledgement
The authors are indebted to Ms. C. Harring, Forstzoologisches Institut der UniversiHit
FreiburgJFRG, for translating the manuscript.
287
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minerale. XIV. IUFRO-Kongress. Referate V, 650-658 (1967).
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334-482. Verlag Paul Parey, Hamburg ,Berlin 1974.
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Am. Proc. 36, 660-663 (1972).
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289
The Interaction between Nutrients and Host Resistance
.to Nematodes with Reference to Mediterranean Crops
M. P. Ritter, Directeur de la Station de Recherches sur les Nematodes, INRA, Antibes/France
Summary
Generally speaking, root nematodes affect the mineral nutrition of the plant in a selective manner;
in particular, they reduce the absorption of potassium. The mineral nutrition of the host likewise
influences the development of the nematodes which parasitise it and certain physiological characteristics of their progeny.
For any element the effect can be either positive or negative partly because the host has its own
particular nutrient requirements and variable sensitivity to each particular nematode arid susceptibility of the host varies according to the species or strain of nematode under consideration. Each
element affects both the growth of the infected plant and the development of the parasite. These·
complex phenomena have been the subject of several tentative experiments, particularly with several
$pecies of Meloidogyne on various market garden crops and for Heterodera avenae on cereals.
The results obtained are not easily applicable in practical agriculture.
Certain fertilizers can have a direct nematicidal effect, for example ammoniacal nitrogen or formulations containing sulphate in rice fields. It must not be forgotten that soil treatments against nematodes affect the microflora and thus have indirect effects on the utilisation by the plant of nutrient
elements applied.
Study of these problems remains fragmentary, few investigations are comparable and research has
not been sufficiently comprehensive.
.
Resume
D'une maniere generale les nematodes phytophages, qui attaquent le systeme radiculaire des plantes,
affectent selectivement leur nutrition minerale et en particulier diminuent I'absorption de la potasse.
Reciproquement les elements foumis it l'hiHe influencent le developpement des nematodes qui le
parasitent, ainsi que certains caracteres physiologiques de leur descendance immediate.
Cet effet peut etre positif ou negatif pour un meme element, d'une part selon l'hote qui a ses propres
besoins nutritionnels et une sensibilite variable vis-it-vis de chaque nematode particulier et d'autre
part pour un meme hote selon l'espece ou la race du nematode considere. Chaque element agit
en propre it la fois sur la croissance de la plante infestee et sur le developpement du parasite. De
plus ces actions interferent selon la formule minerale utilisee, ce phenomene complexe a fait l'objet
de quelques tentatives d'analyses experimentales, en particulier pour plusieurs especes de Meloidogyne sur diverses plantes maraicheres et pour Heterodera avenae en presence de graminees cerealieres. Les resultats n'apparaissent pas transposables aisement it la pratique.
Certaines formes de fertilisation peuvent de plus avoir une action nematicide directe, tel l'azote
ammoniacal ou les formulations en sulfate dans les rizieres. On ne doit pas oublier non plus que les
traitements realises contre les nematodes dans le sol affectent la microflore et agissent indirectement
sur l'utilisation par les vegetaux des elements fertilisants qui leur sont apportes comme de coutume.
Les etudes sur ces problemes restent donc fragment aires, peu comparables entre elles et tres incompletes aussi bien sur le plan theorique que sur celui des experimentaiions agronomiques.
291
1. General considerations
Treatises on agricultural nematology, whether old or recent, are somewhat discreet
about the role which mineral nutrition of the host might play in relation to nematode
attack. This indicates a gap in research which is the more surprising because over the
years a number of interesting, but often contradictory, observations have been made
on this subject.
Filipjev and Schuurmans-Stekhoven [10] published in 1941 a treatise which was, for the
period, very comprehensive and this records observations made early in the century by
several German and Russian authors: thus, Bogdanov [5] emphasised the similarity
between the symptoms caused on beet by Heterodera schachtii and certain nutrient
deficiencies. Subsequently experiments by Krueger [20] and Korab [19] on the same
problem showed that appropriate fertilizer treatment of beet moderately affected by
the parasite resulted in normal yields and that potassium was particularly important,
followed by nitrogen and then phosphate.
Stracham and Tay/or [3J] obtained similar results with H. rostochiensis and potato,
the application of sulphate of potash increasing yield considerably. A positive effect of
superphosphate was also demonstrated by Reinmuth [28]. Trudgill [32] explained the
inhibition of growth in the potato by a deficiency in potassium uptake and possibly
also in phosphorus as shown by analysis of young shoots as early as five weeks after
planting.
Several authors later studied the effects of urea and calcium cyanamide on the same
parasitic association. It seems that there was a direct toxic effect on the nematode
larvae in addition to the straightforward fertilizer effect by substances which, at least
in the case of the second, become more phytotoxic at high rates. The result is that at
low rates, cyanamide increases both crop yield and the population ofthe new generation
of nematodes, while as the rate increases the crop yield is increasingly diminished but
the final number of nematode larvae is decreased. At low rates the effect is to retard
hatching rather than to cause death of the larvae leading one to think that we are here
concerned with an effect on the host - parasite relationship.
Decker's [9] excellent manual of plant nematology devotes a chapter to this subject
but, as the author says, results on the effects of fertilizers are only fragmentary and do
not go far enough to disentangle the various phenomena which may be concerned. In
contrast, the effects of additions of organic matter in various forms have been more
thorougWy studied and their direct or indirect effects on the various soil organisms
which are antagonistic to nematodes are well known.
Recent work by Curtis [7] showed a direct effect of potassium fertilizer on sugar beet
resistance to Heterodera schachtii. A high potassium content in the fertilizer increased the size of beet and also reduced the number of nematode cysts formed on the
roots. Straight potassium chloride works in the same way and if the phenomenon is
studied in detail, it is found that the root exudates from plants which have received
potassium are less effective in inducing hatching of larvae from the cysts. On the other
hand the larvae thus obtained are more aggressive to the beet and the beet plants
treated in this way are more receptive to the larvae.
All these results demonstrate the diversity of the positive and negative effects concerned of which the resultant is the apparent degree of resistance observed, whether
expressed in terms of crop yield or final nematode population. There is evidence from
field trials of fertilizer having effects in improving resistance.
292
2. Results concerning nematodes in the mediterranean region
It is known that several species of the genus Meloidogyne which cause galls on the roots
of the plants they attack are among the most noxious nematodes of mediterranean
crops. We shall first review the numerous results which are available on the role of host
nutrition relating to this genus.
2.1. Influence of potassium nutrition of the host on the development of Meloidogyne
The first critical results on the influence of host nutrition were published by Otei/a
[23, 24] and were concerned with potassium which played a dominant role. He treated
seedlings of Lima bean (Phaseolus lunatus) with inocula of varying strength of
M. incognitagrown in nutrient solution (Hoagland and Snyder [17]) with varying
rates of monopotassium phosphate at 0.5, 6.0 and 10 milliequivalents per litre. Growth
was significantly increased by all rates especially when the inoculum was strong.
Mineral cQntent of the plants was affected in the same way and the addition of excess
potassium to the medium re-established the normal level of this element in the plant
unless infection was at a very high level. Nematode reproduction was directly affected
in an unexpected manner because at low potassium levels, reproduction of Meloidogyne
was greater when the plants were initially heavily infected than when they were less so
and the rate of multiplication increased in both cases with K enrichment of the medium.
This shows that we are not concerned with a weak parasite.
These results were confirmed by the later work of Marks and Sayre [21] who compared the multiplication of three root knot eelworms M. incognita, M. javanica
and M. hapla, in the roots of a cucumber cultivar (Cucumis sativa) grown in nutrient
solutions (Hewitt [15]) containing 2.20, 78 and 155 mgl-1 of K. They found that the
development of M. incognita accelerated with increase in potassium concentration
giving a significantly higher population when this element was present in excess. On the
other hand, the development of the other two species was not influenced by potassium.
2.2. The combined role of NPK in Meloidogyne development
Bird [3] studied the effects of deficiency of each of the major elements: N, P, K, Ca,
Mg, S and Fe in the nutrition of a susceptible tomato .cultivar on M. javanica. There
was accelerated development in most cases of deficiency as compared with complete
nutrition, most marked with N deficiency and quite marked with deficiency of Mg, Fe
or K. (The initial nematode population was low to avoid prejudice against the host
and to ensure that there was competition between individuals). Bird considered that
metabolic imbalance in the host resulted in the production of substances that favoured
growth of the parasite or that the latter responded to 'stress' by developing more
rapidly and producing males in tomatoes deficient in N. This phenomenon which is
not rare in this parthenogenetic species is connected with poor conditions in the host.
Davide and Triantaphyllou [8] did similar work with M. incognita on tomato deficient
in each of the three major elements, N, P and K, or their combinations, initially
infected at a moderate level (400 larvae per plant). The rate of development of the
nematode appeared to be slower in all cases of deficiency than in plants fed normally
and the percentage of lesions was also higher.
293
Faced with the apparent contradiction, Bird [4] re-investigated the effect of N
deficiency in a more refined experiment using M. javanica and tomato. The experimental conditions were very closely defined in order to make them reproducible and he
concluded that with a low level of infection (40 larvae per plant) there was an acceleration in development on deficient plants while, on the other hand, with a moderate level
of infection (400 larvae per plant) the rate of development was significantly less than on
normally fed plants. Very high nematode population (4000 larvae per plant) reduced
the rate of development in all cases. The number of lesions appeared to be related to the
balance between the severity of infection and the fresh weight of the plant at the time.
At very high levels of infection tomato growth was depressed in all cases, but more so
under N deficiency. Bird thus considered that there was no real contradiction between
the results of the various authors because none of the experiments were strictly comparable: they varied in using different species of Meloidogyne, different host plants,
various growth media, types of deficiency and initial infection levels.
More recent Indian work concerned with different host plants has confirmed the fact
that these nematodes, when the infestation is high enough, develop more rapidly on
plants abundantly supplied with nutrients. Haque et al. [13] made observations on
okra attacked by M. incognita and attributed the latter's multiplication to growth
of the root mass. They say also that due to alteration of the vascular system NPK
content of the roots increases with a corresponding decrease in the concentration of
these three elements in the aerial parts of the plant. Variations in the concentrations of
each of these elements in the substrate affect in various ways the assimilation of the
others, but the most marked effect is always that of potassium. The same authors [14]
in extending the study to other plants say that the normal requirement of the plant for
potassium plays an important part when comparing okra, tomato and egg plant.
They observed that, unlike the other two the growth of egg plant, whether or not infected, is better at the K x 1 rate than at K x 2 (obtained by adjustment of the standard
Long Ashton nutrient solution (Hewitt [16]). Once the plant's needs for potassium
are satisfied, the stimulating effect of potassium on the nematode population (which is
observed whatever the initial level of infection) then becomes more prejudicial than
the tolerance which it also provokes.
All the above references emphasise the effects of potassium and nitrogen applications
on the relation between Meloidogyne species and their hosts; phosphorus appears to be
less important. Nevertheless a study by Widdowson et al. [36] shows that, under certain
conditions in New Zealand, it is necessary to increase by five times the dressing of
phosphorus given to white clover to compensate for blocking of its metabolism due to
simultaneous infection by M. hapIa and Heterodera tri/olii; but these authors did not
analyse the separate roles of both species which could be very different and synergism
could always be involved.
One can consider that a great part of the results discussed above is brought about by
the influence of the nutrition of the host plant on that of the nematodes which it
harbours; but this could also influence other mechanisms involved in the plantnematode relationship. This is shown by the studies of Shands and Crittenden [30]
concerning soja attacked by M. incognita acrita. The addition of Nand K promoted
the penetration by larvae of the roots of a variety considered to be resistant (where they
did not cause galling). It also caused more galls to be formed on more or less susceptible varieties. Similar effects may not be found with all plants, but their possible importance should not be neglected.
294
2.3. Influence of fertilizers on development of the cereal nematode Heterodera avenae
H. avenae is endemic to the Mediterranean area and its economic importance should
not be under-estimated. There are numerous, though imperfectly identified, strains
which attack most of the cereals and particularly varieties of high potential yield which
are taking the place of traditional varieties. The influence of cultural practices,
including the use offertilisers, which is one of the essential features involved in possible
improvement, has only been very little studied.
Mukhopadhyaya et al. [22] using material originating in India in pot experiments found
that applications of the three major elements, alone or in combination always increased
grain yield. Significant responses were obtained except with K on wheat and with P on
barley. Cyst counts at the end of the experiment were lower with potassium but increased under all the other treatments. When K was applied with Nand P, the final cyst
count was lower than when it wa~ applied on its own. In summary, N alone increased
both grain yield and cyst count, N + P increased grain yield more than cyst count and
K, whether applied alone or in combination with the others did not affect yield, but
reduced nematode development. These findings apply to the conditions of the experiment with 200 cysts per kg soil, that is ten to forty times lower than one commonly
finds on infested soils in that country but fairly comparable with what is found in the
Mediterranean area albeit with different races of the parasite.
These results would have considerable practical value if they could be translated into
practice in the field. Various investigations made in Australia indicate that high N
dressings increase yield (Davies cited by Wallace [35] and Barry et al. [l]) but in the
case of the latter this was not economic. P as superphosphate combined with zinc
sulphate also increased yield (Wallace [35]) but all these treatments also increased the
final nematode population, which, as other authors have shown, is due to increased
root growth. In discussing their results, Barry et al. conclude after reference to other
Australian work that increasing application ofN fertilizer should not be recommended
except in particular conditions. In years when there was a response to fertilizer it was
greater when the fertilizer was applied at the time of sowing rather than a week later.
The use of urea resulted in fewer cysts than sulphate of ammonia leading to a preference for the former at equivalent rates of application.
It seems then, in summary, that the reaction of cereals contaminated with Heterodera
towards fertilisers does not differ appreciably from that of the hosts of other species of
Heterodera studied in Europe, but there is only fragmentary information on the
problem and a lack of information on the practical effects of potassium dressings.
2.4. Influence of fertilizers on other host-nematode complexes
The literature contains a few more fragmentary studies relating to other types of
nematode.
. Otei/a and Elgindi [27] studied the behaviour of a cotton cultivar in the presence of the
reniform nematode, Rotylenchulus reni/ormis. This species caused a significant reduction in the uptake of N, K and Mn and deficiency of the two former elements accentuated the damage observed. Development and reproduction rate of the nematode were
dependent ori mineral nutrition. Potassium deficiency prevented it reaching the egg
laying stage and the rate of reproduction increased in proportion to the supply of
available potassium. The same authors [26] had already studied this case in 1972
finding that the nematode had a role in the development of Fusarium with which it is
295
often associated. It was apparent in the rather complicated results obtained (complicated because varieties of varying resistance to fungus were included) that the presence
of the nematode always increased the number of plants affected by the Fusarium. The
higher the concentration of potassium in the medium (it varied from 50 to 1000 ppm)
the higher the percentage of plants which were free from fungal attack; higher levels of
potassium were required to produce the same effect when both parasites were present.
This indicated that this element had a similar action on the tolerance of cotton to both
pathogens and each of them required the appropriate fertilizer level as it was also
demonstrated in the study of their respective influence on the uptake of potassium by
the plant.
Oteifa et al. [25] studied in a similar way the influence of fertilizer on the pathogenicity
to cotton of another nematode, Tylenchorhync'lus latus. Application of the three
elements generaIly increased the rate of reproduction of the nematode and, at the same
time, the tolerance of the plant. The latter was particularly improved by the application of potassium, either alone or in combination with the other elements.
If these results contradict those obtained with many other nematodes, it appears that
certain groups react differently. This is the case with Pratylenchus of which the many
species are often very pathogenic to many crops in the Mediterranean area, as indeed
they are throughout the world.
According to Willis [37] reproduction of P. penetrans, which causes much damage to
lucerne, is not affected by potassium fertilizer which greatly increases forage production. There seems to be no interaction, while the potassium fertilizer significantly
increases K concentration in the leaf, nematode infestation decreases it relatively little.
The latter reduces K removal from the soil which is thus left at a higher level in exchangeable K. Collins [6] observed similar results with P. scribneri in the USA. This
species was more abundant on many crops where the soils had not received fertilizer or
where they lacked N or P. On the contrary in the case of cotton or maize, lack of potassium results in a reduction in population. Collins also observed that it was not the same
for other nematodes in the same cultural systems such as: Helicotylenchus dihystera,
Meloidogyne incognita and Xiphinema americanum which were favoured by generous
manuring and discouraged by lack of P and K.
3. Direct effect of fertilizers on plant nematodes
Various results lead one to think that certain forms of mineral fertilizer have a direct
effect on the nematodes themselves. This should be taken into consideration to avoid
erroneous interpretation of general effects. Thus Eno et al. [10] studying the effect of
anhydrous ammonia on various pathogens in the soil, observed a reduction in nematode
population at 300 ppm of ammonium N in the soil and their almost complete destruction when the concentration reached 600 ppm, a concentration which is found in the
zones where the treatment has been applied. Various other authors also confirm the
effect of ammonium N in reducing nematode populations: Birchjield et al. [2] on
Rotylenchulus reniformis and Walker and Post [34] on Pratylenchus penetrans.
Concerning the mechanisms involved, Johnson and Shamiyeh [18] showed that
applying ammonium N to the soil inhibited egg laying by M. incognita if the concentration is high enough (380 mg/kg). This effect, first observed after ploughing in large
amounts of lucerne (4% of the soil mass) is found whatever form of ammoniacal N is
296
used, for example ammonium nitrate or sulphate of ammonia to mention two materials
commonly used in agriculture.
Scotto La Massese et al. [29] confirmed this type of effect following heavy application of ammonium nitrate to citrus infected with Tylenchulus semipenetrans. The
very high rates applied (10.5 kg, that is 3 kg N per 15 years old tree) resulted in almost
total disappearance of the'nematode. According to the author, possible explanations
are: phytotoxicity to the roots which will limit the multiplication of the parasite at the
same time as it affects vegetative growth of the tree: increase in the osmotic pressure of
the soil solution (the treatment is effectively confined to an area of 30 m 2 around each
tree, representing a soil volume of about 10 m3 and a volume of water between 1000
and 2000 litres): nitrification of ammonia being slow on the alkaline soil of the experiment, there could be accumulation of nitrites which have marked nematicidal properties (Walker [33]).
Other phenomena may also be concerned; thus, in studying the effects of fertilizers
applied to rice on the losses caused by Hirschmaniella oryzae in Senegal, Fortuner [12]
found that a dressing of sulphate of potash and potassium metaphosphate at sowing,
followed by urea top dressing (135 kg N, 40kg P and 50 kg K) had no effect on yield in
the absence of nematodes. However, when the nematode population was normal for
the area (a mean of 2000 per litre of soil and 250 per gramme ofroots) yield was increased by 35%. Nematodes always reduced the yield, whether or not fertilizers were
applied. Among possible explanations for this behaviour, the author suggests an increase in sulphate reduction of bacterial origin resulting from the application of
sulphur in the fertilizer. This could have a depressive effect on both the rice and' the
nematodes. Whim nematodes are present these counteract each other, while, if they are
absent, only the depressive effect on the rice is evident and this would mask the
beneficial effect of the fertilizer. This does not exclude the classic explanation that a
better nutrient supply is needed when the roots are damaged, while healthy. roots are
capable of obtaining their needs from a soil less well supplied.
4. Conclusion
Analysis of results quoted in the literature shows that fertilizer, and specifically potas:
sium, modify the behaviour of plants infested with nematodes. The study of the
physiological mechanisms which may be involved has scarcely been begun and usually
results are only available on overall effects produced in particular cases. Each worker
has his own methods and few results are comparable. It is well known that many
factors other than nutrition are concerned in the susceptibility of the plant to nematode
attack (temperature, quantity and quality of light, photoperiodism, humidity, the
nature of the soil etc...).
So far as concerns the plant one must take account of the individual susceptibility of
the cultivar, and even of the clone, to the nematode under consideration and of its
normal response to each type of fertilizer under the given conditions. One should also
recognise that in the nematodes the characterisation of species is often difficult and that
there are in many of them, races and biotypes each with a particular physiology. In
Meloidogyne, in which reproduction. is often parthenogenetic, each popull;ttion is in
practice made up of a series of parallel clonal lines distinguished only by their varying
behaviour. It is not hardly surprising therefore that results obtained in different parts
of the world vary so much when the number of investigations is so limited.
297
This way of research should be exploited to the maximum. It is of interest to both
agronomists and nematologists and its practical applications could be considerable
because the possibilities for treatment by nematicides are very limited on account of
their high cost, the cultural precautions which are needed and the high toxicity of
the chemicals used. Here again the importance of host nutrition must be taken into
account; it is known that most of the substances used can, through their effects on soil
micro-organisms, modify the effects of fertilizers applied to the soil.
The needs and the physiology of plants growing under such conditions are no longer
the same and it will be necessary in consequence to adapt fertilizer formulae and
timing of application.
We may hope that new results will come forward soon to explain the contradictions
and elucidate the fundamental mechanisms which are involved. The number of
investigations published recently indicates a reawakening of the interest which these
problems have aroused for many years.
5. Bibliography
1. Barry, E. R., Brown, R.H. and E/liot, B. R.: Cereal cyst nematode (Heterodera avenae) in Victoria:
influence of cultural practices on grain yields and nematode populations. Aust. J. expo Agric.
Anim. Husb. 14, 566-571 (1974).
2. Birchjield, W., Parr, J. B. and Smith, S.: Nematicidal and fungicidal activity of potassium azide in
liquid anhydrous ammonia. Plant Dis. Re. 53, 923-926 (1969).
3. Bird, A. F.: The effect of some single element deficiencies on the growth of Meloidogynejavanica.
Nematologica 5,78-85 (1960).
4. Bird, A. F.: The effect of nitrogen deficiency on the growth of Meloidogyne javanica at different
population levels. Nematologica 16, 13-21 (1970).
5. Bogdanov, S. 1901-1903: In: Filipjev, I.N. and Schuurmans Steckhoven Jr, J.H.: A manual of
Agricultural Helminthology, E.J. Brill, Leiden, 544 (1941).
6. Collins, R.J.: Relationship of fertilizer treatments and cropping sequence to populations <if
plant-parasitic and free-living nematodes. Diss. Abstr. Sect B, 32, 6770-6771 (1972).
7. Curtis, G.J.: The effect of potassium chloride on the infestation of sugar beet by beet eelworm,
Heterodera schachtii Schmidt. Ann. appl. BioI. 54, 269-280 (1964).
8. Davide, R. G. and Triantaphyllou, A. c.: Influence of the environment on development and
sex differentiation of root-knot nematodes. n. Effect of host nutrition. Nematologica 13, 1.11117 (1967).
9. Decker, H.: Phytonematologie, Biologie und Bekampfung pflanzenparasitarer Nematoden.
Deutscher LandwirtschaftsverIag, Berlin, 526 pp., 1969.
10. Eno, c.F., Blue, W. G. and Good, J. M.: The effect of anhydrous ammonia on nematodes, fungi,
bacteria and nitrification in some Florida soils. Proc. Soil. Sci Soc. Am. 19, 55-58 (1955).
11. Filipjev, I.N. and Schuurmans Stekhoven, J.H.: A manual of agricultural helminthology.
E. J. Brill, Leiden: 878 pp., 1941.
12. Fortuner, R.: Fertilisation du rjz et degiHs causes par le nematode Hirschmanniella oryzae
(Van Breda de Haan) Luc et Goodey. C. r. Ac. Agr. de France (in press) (1976).
13. Haque, Q.A., Khan, A. M. and Saxena, S.K.: Studies on the effect of different levels of certain
elements on the development of root-knot. L Effect of NPK levels on growth of okra and rootknot development. Indian J. Nematol. 2, 35-41 (1972).
14. Haque, Q.A., Khan, A.M. and Saxena, S.K.: Studies on the effect of different levels of certain
elements on the development of root-knot. 11. Effect of different levels of potassium on growth
and root-knot development on okra, egg plant and tomato. Indian J. Nematol. 4, 25-30 (1974).
15. Hewitt, E.J.: Sand and water culture methods used in the study of plant nutrition. Comm. Agric.
Bur, 241 pp., 1952.
16. Hewitt, E.J.: Sand and water culture methods used in plant nutrition. Comm. Agric. Bur., 1966.
17. Hoagland, D. R. and Snyder, W. R.: Nutrition of the strawberry plant under controlled conditions.
Proc. Amer. Soc. hort. Sci. 30, 288-294 (1933).
298
18. Johnson, L.F. and Shamiyeh, N.B.: Effect of soil amendments on hatching of Meloidogyne
incognita eggs. phytopathology 65,1178-1181 (1975).
19. Korab, I. 1925-1930: In: Filipjev, I.N. and Schuurmans Stekhoven Jr., J.H.: A manual of Agricultural Helminthology, E.J. Brill, Leiden, 545-547, (1941).
20. Krueger: In: Filipjev, I.N. and Schuurmans Stekhoven Jr., J.H.: A manual of Agricultural
Helminthology, E.J. Brill, Leiden, 544-545, (1941).
21. Marks, C. F. and Sayre, R. M:: The effect of potassium on the rate of development of the rootknot nematodes Meloidogyne incognita, M. javanica and M. halpa. Nematologica 10, 323-327
(1964).
22. Mukhopadhyaya, M. c., Dalal, M.R., Shakuntala Saran and Kharub, S.S.: Studies on the Molya
disease of wheat and barley. Indian J. Nematol. 2, 11-20 (1972).
23. Oteifa, B.A.: Effects of potassium nutrition and amount ofinoculu'm on rate of reproduction of
Meloidogyne incognita. J. Wash. Acad. Sc. 41, 393-395 (1951).
24. Oteifa, B.A.: Potassium nutrition of the host in relation to infection by a root-knot nematode
Meloidogyne incognita. Proc. Helmintol. Soc. Wash. 19, 99-104 (1952).
25. Oteifa, B.A., Elgindi, D. M. and Diab, K.A.: Cotton yield and population dynamics of the stunt
nematode Tylenchorhynchus latus under mineral fertilization trials. Potash. Rev. 23/31, 7 pp.,
1965.
26. Oteifa, B.A. and EIgindi, A. Y.: Interrelationships of Rotylenchulus reniformis, Fusarium osysporum f. vasinfectum and potassium nutrition of cotton, Gossypium barbadense. Abstr. Xlth Int.
Symp. Nematology, Reading 1972, 53 (1972).
27. Oteifa, B. A. and Elgindi, D. M.: Host nutrition in relations to infection by the reniform nematode
Rotylenchulus reniformis. Abstr. XIInd Int. Symp. Nematologia, Granada: 78, 1974.
28. Reinmuth, E.: Die Kartoffelnematode (Heterodera schachtii Schmidt). Beitriige zur Biologie
und Bekiimpfung. Z. pflanzenkrankh. 39, 241-276 (1929).
29. Scotto La Massese, c., Vassy, R. and Zaouchi, H.: Elimination de Tylenchulus selJ1ipenetrans
par des apports azotes appliques a des clementiniers greffes sur bigaradiers. Nematol. Mediterr.
1,29-34 (1975).
.
30. Shands, WA. and Crittenden, H. W: The influence of nitrogen and potassium on the relationship of Meloidogyne incognita acrita and soybeans. Phytopathology 47, 454 (1957).
31. Stracham, J. and Taylor, T.H.: Potato eelworm. J. Minist. Agric. 23, 941-947 (1926).
32. Trudgill, D.L.: Mechanisms of damage to potatoes by Heterodera rostochiensis. Abstr. XIth
Int. Symp. Nematol., Reading, 3-8 Sept., 77, (1972).
33. Walker, J. T.: Population of Pratyle.nchus penetrans relative to decomposing nitrogenous soil
amendments. J. Nematol. 3, 43-49 (1975).
34. Walker, J. T. and Post, A.: Reduction of lesion nematode populations by decomposing nitrogenous amendments. Abst. Phytophatol. 58, 1055 (1969).
35. Wallace, H. R.: The ecology and control of the cereal root nematode. J. Aust. Inst. agric. Sci. 31,
178-186 (1965).
36. Widdowson, J. P., Yeates, G. W. and Healy, W. B.: The effect ofroot nematodes on the utilisation
of phosphorus by white clover on a yellow brown loam. N.Z. J. agric. Res. 16, 77-80 (1972).
37. Willis, C.B.: Effect of potassium fertilization and Pratylenchus penetrans on forage yield an·d
potassium content of alfalfa. Abstr. 2nd Intern. Congr. Plant Pathol., Minneapolis, Minn.
5-12 Sept. 1973, No. 1099, 1973.
299
Potassium Nutrition of Cotton, Gossypium barbadense,
in Relation to Nematode Infection by
Meloidogyne incognita and Rotylenchulus reniformis*
Prof. B. A. Oteifa, Ph. D~ and A. Y. Elgindi, Ph. D., Department of Agricultural Zoology and Nematol· ,
ogy, Faculty of Agriculture, Cairo University, Giza/Egypt
Summary
Population behaviour of M. incognita was primarily' governed by the amount of available root,
rather than the potassium nutritional status of the host. On the other hand, the reproductive activity
of R.reniformis was mainly influenced by the host potassium concentration despite the amount of
root space. In general, higher levels of potassium application to infected plants exerted a remarkable
beneficial effect on host growth response,
Resume
Le comportement de la population de M. incognita depend plut6t de la masse racinaire qui est
disponible que de l'etat de nutrition potassique de la plante-h6te. D'autre-part, l'activite reproductrice de R. reniformis est influencee principalement par la teneur en potassium de l'h6te et ceci
independamment du volume racinaire. D'une maniere generale, l'application de doses elevees de
potassium aux plantes infestees exerce un ;ffet tres positif sur la croissance de I'h6te. '
1. Introduction
The rQot-knot nematode, Meloidogyne incognita and the reniform nematode, Rotylenchulus reniformis' constitute at present a problem in the cotton production areas of
Egypt (Oteifa [i7), Oteifa and Salem [20}, Oteifa et al: [19} and Salem and Taha
[23}). Potash fertilizers generally induce certain tolerance to nematode and wilt
diseases (Bessey [l}, Elgindi et al. [6], Hellinja [9], Oteifa et al. [18], Rast [22j,
Sharoubeem et ai, [26} and Young et al. [27]). Studies on the interrelationships of
nematode infection and host potassium nutrition are often limited and sometimes are
not clear as indicated by contradictions in the literature, e. g. Bird [2], Davide and
'Triantaphyllou [4}, Dropkin and Boone [5}, Haque et al. [8}, Ismail [1 I}, Kirkpatrick
et al. [l2}, Marks and Sayre [13], Oteifa [14, 15, 16}, Shafiee [24} and Shands and
Crittenden [25}. Since annual flooding of the river Nile was the key source of Egypt's
potash soil amendment in the surrounding plains it was found desirable to study
the significance of host potassiuin nutrition in relation to infection by the predominant
nematodes of cotton, M. incognita and R. reniformis.
* This research was supported in partby Grant Number FG,-EG-119 US Department of Agticulture.
301
2. Materials and Methods
Glazed pots, 15 cm diameter, were filled with clean steam-sterilized 60-mesh quartz
sand. Nutrient stock solutions of Hoagland and Arnon [10] at different potassium
concentration levels were employed. Solutions containing 25, 100, 250 and 500 ppm K
to represent deficient (Kr), Iow (KI), optimum (K p ) and excess (Kx) were prepared
and adjusted to pH 6.8. Four seeds of a long staple cotton, Gossypium barbadense
cv. Giza 67 were sown per pot and watered with distilled water. After germination,
plants were thinned to two seedlings per pot and the representative solutions were
supplied at the rate of 150 ml per pot. An inoculum of 2000 newly hatched larvae
per pot of Meloidogyne incognita and/or Rotylenchulus renijormis were pipetted around
the base of seedlings. For each potassium level the following four treatments: C= Control without nematode infection; M = Meloidogyne infection alone; R = Rotylenchulus
infection alone and M + R= Meloidogyne and Rotylenchulus infections together, were
applied. Each treatment was replicated eight times and the experiment was carried out
in the greenhouse at 26-30°C. Pots were provided with the representative nutrient
solutions twice a week and flushed with distilled water once a week to avoid any
accumulation of salts. After 9 weeks from inoculation, plants were gently removed,
their roots were washed free of sand and data on plant fresh weights and nematode
counts were recorded. Residual nematodes in pots were recovered by Byrd et af. [3]
flotation-sieving technique while those within or on roots were detected by the lactophenol acid-fuchsin method (Goodey [7]). For chemical determinations, leaves and
roots of each plant were separately oven dried at 700C, ashed, prepared in solutions
and potassium contents were measured by the standard flame spectrophotometer
procedure.
3. Results
3.1. Effect of potassium host nutrition on nematode activity
Data on the comparative development and reproduction of M. incognita and R. renijormis under different host potassium levels (Table 1) indicate a general trend in the
increase of nematode population with the increase in potassium supply. Although
there was no significant difference in total penetrating nematode stages and total
eggmasses per root as well as total residual larvae per pot between Kr and KI treatments, their numbers were significantly lower than the K p and K x treatments. In the
root-knot nematode, M. incognita, despite that their total number of eggmasses per
root was significantly increased with potassium increment, yet differences in -their
numbers per g fresh weight of root tissue were not significant. However, with the
reniform nematode, R. renijormis it is evident that despite the relative increase of
eggmasses production per root system with the increase in potassium levels, numbers
of eggmasses per g fresh weight of root were significantly decreased with the increase
in potassium concentration. A similar trend in both nematodes' behaviour was noticed
when they were inhabiting the same root system except that their numbers were
relatively lower than when they were alone, a phenomenon which indicates a competition between both nematodes for food and space. In this respect, the reniform
nematode, R. renijormis seems to have a more competitive influence since population
302
of the root-knot' nematode, M. incognita was remarkably affected by its presence
(Table 1).
Table 1. Effect of potassium host concentrations on hatching, penetration and development of
Meloidogyne incognita and Rotylenchulus reniformis.
Nutrient solution
Nematode treatments"
ppmK
Total hatch*
per root
Total 'penetrate
per root
Total eggmass
per root
Mean eggmass
per g root
(M. incognita) - M
25
100
250
500
LSD 0.05
0.01
830
866
982
1052
40
47
186
218
360
436
37
46
26
42
87
121
13
17
18
17
15
16
5
6
415
460
617
705
. 51
62
97
114
172
223
20
26
113
82
64
45
7
10
8
17
38
51
7
12
8
(R. reniformis) - R
25
100
250
500
LSD 0.05
0.01
1105
1136
1240
1297
36
44
(M. incognita) - M + R
25
100
250
500
LSD 0.05
0.01
346
370
525
605
35
47
90
117
190
237
33
41
II
II
8
5
7
48
66
125
172
19
24
72
54
42
33
6
8
(R. reniformis) - M + R
25
lOO
250
500
LSD 0.05
0.01
938
976
1088
1170
43
52
330
372
551
655
48
60
* Sum of residual larvae in sand after plant removal.
** M =M. incognita alone, R';R. reniformis alone, M + R=M; incognita and R. reniformis together.
3.2. Effect of potassium host nutrition on growth ,response and K contents of infected plants
When the pathogenic effects ·of M. incognita and R. renijormis either alone or in
combination were determined on. the vegetative growth and K contents of cotton
under the different potassium nutritional treatments (Figures 1. 2) it was evident that
nematodes caused· a significant reduction in shoot fresh weights of plants provided
with Kf, KI, and Kp. Although differences between the pathogenic effects of M. incognita and R. renijormis, whether alone or together, on cotton suppIie(fwlth::Kf were
negligible there was a pronounced significant difference between the two nematodes
~!}\
303
o
Control
BJ (M)
[:j (R)
15
~
I
5:
•
L.5.D.
(M+R)
I
.05.01
l.!>
~
10
:c
III
UJ
lE
a..
~
z
5
L:5
~
-25-
-100-
-250-
-500-
POTASSIUM CONCENTRATIONS IN PPM
Fig. 1. Effect of potassium host nutrition on the vegetative growth of cotton infected with M.
incognita and/or R. reniformis.
-0..... 0 .....
A-Leaves
Control
B-Root
(M)
_ . _ (R)
40
.....•.. '" (M+R)
.0
30
.'
.0'"
l.!>
~
o
10
4
.. '
..
0
e~e
.~~~
e
j/
25
100
250
500
25
100
250
500
POTASSIUM CONCENTRATIONS IN PPM
Fig. 2. Effect of potassium host nutrition on the potassium contents of leaves (A) and roots (B) of
cotton plants infected with M. incognita and/or R. reniformis.
304
when they solely infected the plants supplied with either K, or K p . When both nematodes inhabited the same root tissue their pathological effects were not significantly
different from the effect of R. renijormis alone. This indicates that R. renijormis has a
rather more influential effect than M. incognita. On the other hand, when plants were
supplied with K x differences in shoot fresh weights of control plants from nematized
ones, whether alone or both, were insignificant. As a matter of fact the growth response
and amounts of translocated potassium in leaves (Figure 2A) in the infecting plants
receiving K x were almost in equivalence with those healthy plants which received K p .
Although nematode infections, in general,decreased the amount of absorbed potassium, R. renijormis infection did not interfere with the element translocation to the
vegetative growth while M. incognita infection retained considerable amounts in the
root system (Figure 2B).
4. Discussion
The addition of excess potassium to a sand medium gave higher larval hatch, penetration of host roots as well as eggmasses development of M. incognita as compared to
plants receiving Kf or K 1 • However, when number of eggmasses development was
computed on a per g of root basis rather thanper plant, differences in numbers were
negligible. Thus, in spite of the K p or K x plants, having more available root sites for
nematode penetration and development than the Kf or KI plants, the factor of potassium nutritional status of the host seems to have no effect on nematode growth and
development In the meantime, plants grown under the highest potassium level were
capable of tolerating the increase in nematode population. With reference to R. renijormis, the increment in potassium levels caused a similar response in the nematode
population per plant. However, when numbers of eggmasses development were
counted per g of root basis a significant reduction was resulted. This indicates that K
may inhibit the activity of R. renijormis by interfering with its rate of growth and
development. Growth of infected plants responded highly to the excess potassium
level. When both nematodes were co-inhabiting the same root tissue each nematode
behaved as if it were alone. The presence of R. renijormis, however, seems to have an
inhibitory influence on the development of M. incognita. Histopathological studies by
Oteija et al. [21] also confirmed those findings.
The present work demonstrates the potential significance of potash application in
reducing nematode hazards on cotton plants. Results justify the need for future
extensive field trials to evaluate the role of potash fertilizers in cotton fields infested
with nematodes. The recent changes in Egypt's basic agricultural features after the
.High Dam, especially the lack of the generous supply of silt rich in potassium, heighten
the importance of increasing yields on the resultant poorer lands.
5. Bibliography
1. Bessey, E.A.: Root-knot nematode and its control USDA Bull.' 217,89 (1911).
2. Bird, A.F.: The effect of some single element deficiencies on the growth of Meloidogynejavanica.
Nematologica 5, 78-85 (1960).
3. Byrd, D. W., Nusbaum, C. J. and Barker, K. R.: A rapid flotation-sieving technique for extracting
nematodes from soil. Plant Dis. Reprtr. 50, 954-956 (1966).
305
4. Davide, R. G. and Triantaphyllou, A. c.: Influence of the environment on development and sex
differentiation of root-knot nematodes. n. Effect of host nutrition. Nematologica 13, 111-117
(1957).
5. Dropkin, V.H. and Boone, W.R.: Analysis of host-parasite relationships of root-knot nematodes
by single larva inoculations of excised tomato roots. Nematologica 12, 225-236 (1966).
6. Elgindi, A. Y., Oteifa, B.A. and Khadr, A. S.: Interrelationships of Rotylenchulus reniformis,
Fusarium oxysporum f. vasinfectum and potassium nutrition of cotton, Gossypium barbadense.
Potash Review Sub. 23, No.5, 1-5 (1974).
7. Goodey, J.B.: Laboratory methods for work with plant and soil nematodes. Tech. Bull. No.2,
p. 72, Ministry of Agriculture, Fisheries and Food, London (1963).
8. Haque, Q.A., Khan, A.M. and Saxena, S.K: Studies on the effect of different levels of certain
elements on the development of root-knot. I. Effect of NPK levels on growth of okra and rootknot development. Indian J. Nematology 2,35-41 (1972).
9. Hel/inja, J.A.: Influence of nematodes on the yield and composition of sugar beets. Mededeel
Inst. Sinkerbietentedt 12, 163-182 (1942).
10. Hoagland, D.R. and Arnon, D.I.: The water culture method for growing plants without soil.
Calif. Agric. Expt. Sta. Circular 347 (1950).
11. /smail, W.: Effect of different levels of potassium on the development of root-knot and reniform
nematodes on certain vegetables. Ph. D. Thesis, p.176, Aligarh Muslim Univ. India, 1975.
12. Kirkpatrick, J.D., Fisher, E.G. and Parker, KG.: Population levels of Pratylenchus penetrans
and Xiphinema americanum in relation to potassium fertilization of Montmorecy sour cherries
on Mazzard rootstock. Phytopathology 40, 543 (1959).
13. Marks, C. F. and Sayre, R. M.: The effect of potassium on the rate of development of the rootknot nematodes, M. incognito, M. javanica and M. hapla. Nematologica 10, 323-327 (1964).
14. Oteifa, B.A.: Effects of potassium nutrition and amount of inoculum on rate of reproduction
of Meloidogyne incognito., J. Wash. Acad. Sci. 41, 393-395 (1951).
15. Oteifa, B.A.: Potassium nutrition of the host in relation to infection by root-knot nematode,
M. incognito.. Proc. Helminth. Soc. Wash. /9, 99-104 (1952).
16. Oteifa, B.A.: Development of the root-knot nematode, M. incognito. as affected by potassium
nutrition of the host. Phytopathology 43, 171-174 (1953).
17. Otei/a, B. A.: The reniform nematode problem of Egyptian cotton production. Jour. Parasitology
56, 255 (1970).
18. Otei/a, B.A., Elgindi, D. M. and Diab, KA.: Cotton yield and population dynamics of the stunt
nematode, Tylenchorhynchus latus under mineral fertilization trials. Potash Review. Sub. 23,
1-7 (1965).
19. Otei/a, B.A., Elgindi, D. M. and Eleraqi, M. S.: Evaluation of some granular systemic nematicides
for the control of Rotylenchulus reniformis on Egyptian cotton. Fac. Agric. Ain Shams Univ.
Res. Bull. 514, 1-13 (1971).
20. Otei/a, B.A. and Salem, A.A.: Biology and histopathogenesis of the reniform nematode,
Rotylenchulus reni/ormis, on Egyptian cotton, Gossypium barbadense. Actas HI Congr. Un.
Fitopat. Medit., Oeiras, 22-28 Outobro (1972).
21. Oteifa, RA., Elsherif, M.A. and Osman, A.A.: Histopathogene~is of Rotylenchulus reniformis
and Meloidogyne incognito. as coinhabitants in roots of tomato Lycopersicon esculentum. Fac.
Agric. Cairo Univ. Bull. In Press.
22. Rast, L.E.: Control of cotton wilt by use of potash fertilizers. J. Am. Soc. Agronomy 14,
222-224 (1922).
23. Salem, A.A. and Taha, A.H.: Nematodes associated with cotton plants in Menia Governorate
with special reference to the efficiency of DBCP in controlling Meloidogyne incognito.. Zagazig
Jour. Agric. Res. 1, 311-320 (1974).
24. Shafiee, M. F.: Histo- and physiopathological studies of pepper, Capsicum frutescens, infected
with Pratylenchus penetrans, Meloidogyne incognito. acrita and M. hapla, Ph. D. Thesis, p.I13,
Rutgers Univ. USA, 1962.
25. Shands, W. A. and Crittenden, H. W.: The influence of nitrogen and potassium on the relationship
of M. incognito. acrita and soybeans. Phytopathology 47, 454 (1957).
26. Sharoubeem, H.H., Naim, M.S. and Habib, A.A.: Potassium, Nitrogen and Phosphorus in
relation to the incidence of cotton wilt caused by Fusarium oxysporum f. vasinfectum. J. Microbiology UAR 2, 1-8 (1967).
27. Young, V. H., Janssen, G. and Ware, J. 0.: Cotton wilt studies. IV. Effect of fertilizers on cotton
wilt. Ark. Sta. Bull. 272 (1932).
306
Fertilizers in Regard to Plant Resistance to Pests:
Their Role in FAO's Integrated Pest Control Programme
L.Brader, FAO/UNEP Global Programme Coordinator. Integrated Pest Control
FAO Plant Protection Service, Rome/Italy
Summary
The study of the impact of fertilizer use on pest control is not an important element of FAO's current
activities. However, its importance will certainly increase with the development of integrated pest
control programmes. For the time being, emphasis is on three groups of crops: cotton, rice and
sorghum/millet/maize. A review of literature shows that fertilizer application may have a considerable effect on the development of major pest species. It is necessary to improve our information
on the economic, consequences of fertilizer use as far as pest control is concerned. An unbalanced
situation may reduce considerably the benefits to be drawn from fertilizer. For a pest control strategy,
we need more information on the numerical response of pests to fertilize application and on the
population dynamics of the various species. Only then will we be able to fully evaluate the significance of fertilizers for plant health.
Resume
L'etude de I'impact de I'emploi des engrais sur la lutte contre les ravageurs n'est pas un element
important des travaux actuels de la FAO. Cependant, l'importance attribuee it cette question ira
certainement en croissant avec le developpement de programmes de lutte integree. Pour l'instant,
!'interet de la FAO se concentre sur trois groupes de cultures: cotonnier, riz ainsi que sorgho/mil/
mais. L'etude de la litterature montre que l'application des engrais peut avoir un effet considerable sur
le developpement des principales especes de ravageurs. II est necessaire d'ameliorer nos connaissances sur les consequences economiques de l'emploi des engrais en ce qui concerne la protection
des vegMaux. Une situation mal equilibree pourrait reduire considerablement l'effet benefique de
l'emploi des engrais. Pour une strategie de lutte contre les ravageurs, nous avons besoin de details
supplementaires sur la reaction numerique des ravageurs it l'emploi des engrais et sur la dynamique
des popu!ations des differentes especes de ravageurs. C'est ainsi que nous serions en mesure d'evaluer
pleinement l'importance de l'utilisation des engrais et la sante des plantes.
1. Introduction
FAO is currently involved in plans for the development and application of integrated
pest control programmes in the following three groups of crops: ,cotton, rice ,and
sorghum/millet/maize. The discussion of this paper will therefore be restricted to these
crops. It should also be made clear immediately that fertilizers have not generally been
considered an important factor in respect to the control of pests. (Pests defined as all
organisms causing 10 sses to crops.) However, it is evident that increased fertilizer usage,
307
through its impact on the crop's development will have considerable consequences for
pest control strategies. Various aspects to be considered include
- changes in the total habitat of the crop and subsequently in micro-climatic conditions. This will certainly interfere not only with the numbers of species already
present, but also possibly with the species composition;
- direct effect of food quality on the reproduction capacity of the pest species concerned;
- the plant's capacity to recuperate from damage, which will generally be increased
through enhanced and well-balanced fertilizer usage;
- in the same category could also be placed the avoidance of damage through correct
timing of fertilizer application. For example, in Chile early N application on
maize is used to enhance stalk formation, thus avoiding lesser cornstalk borer
(Elasmopalpus Iignosellus Zeller) damage.
The above-mentioned points deal mainly with the direct biological relationship between fertilizer usage and pest control. From an economic standpoint, it might be
stated that crop protection measures are often necessary to optimize returns on
fertilizer input and vice versa. These are indirect consequences, while, for the developmentof control methods as such, one is interested merely in direct relationships
between the application of a certain amount of fertilizer of a certain quality and the
numerical response of the major pest species to this in a given crop situation.
To increase the transfer of knowledge, FAO has so far organized two conferences
directly related to integrated pest control. These were held respectively in October 1965
and December 1972. These conferences serve to guide FAO's policy in the area of
integrated pest control and to inform member countries on the most recent developments. Another important contribution in this respect is the FAO Panel of Experts on
Integrated Pest Control. In regular sessions, this group studies and evaluates recent
developments and recommends action to be taken. In this paper, we shall first see how
far fertilizers have been part of the discussion within the framework of these two
specific activities. Subsequently, we will briefly discuss the topic of this paper in
relation to the three main groups of crops mentioned. We will conclude with a short
discussion on possible future developments.
It should be noted that no observations on pest incidence are carried out within the
framework of the FAO Fertilizer Programme. It is therefore not possible in the current
state of affairs to contribute directly to a better knowledge in this area. The same is true
for the complex interactions between fertilizers, weeds and crop production.
2. Integrated Pest Control
'Integrated control is a pest management system that, in the context of the associated
environment and the population dynamics of the pest species, utilizes all suitable
techniques and methods in as compatible a manner as possible and maintains the pest
populations at levels below those causing economic injury. This broad definition implies
the fullest use of natural mortality factors complemented when necessary by artificial
methods . . ; Implicit in this definition is also that imposed control measures, notably
conventional pesticides, should be used only where economic injury thresholds would
308
otherwise be exceeded. Integrated control is not dependent upon any specific control
procedure, but for each situation coordinates relevant techniques with the natural
(regulating and limiting) elements of the environment.' (FAO [1973])
The two basic aspects of integrated pest control are
- the acquisition of sufficient knowledge about crop losses caused by various pest
species and the subsequent establishment of the economic damage threshold; and
- the development of more selective pest control techniques.
The economic damage threshold is defined as the numbers of a pest species that, when
not controlled, would result in crop losses the value of which is equal to the cost of
the control measure. This level of crop loss is called the economic injury threshold.
At this stage CD/CA= 1, CD being the cost of damage, CA the cost of application
(Headley, J. C. [1973]). The economic damage threshold is lower than the economic
injury threshold, as the effect of a control measure is always somewhat delayed.
Figure 1 gives a shematic representation of the economic damage threshold.
One of the drawbacks of the so-called broad spectrum pesticides is their high toxicity
towards beneficial organisms. These parasites and predators are capable in many
instances of killing a very large part of the pest species. To maintain their activity, it
is therefore necessary to use selective control techniques which kill the pest species
concerned but do not counteract directly, or counteract as little as possible, the
activity of the beneficial organisms. Various approaches are possible. We will brieflY
discuss chemical c.ontrol, biological control, host plant resistance and cultural practices.
Pesticides will certainly continue to be the main element in the future of pest control.
Their efficiency, availability and easy applicability make them in most instances the
best· tools we have. Two possibilities are open:
- the use of broad spectrum pesticides in such a way that they kill the smallest possible
number of parasites and predators. This would include timing of application to
correspond with periods when beneficial organisms are least active, and application
techniques, including soil application and reduced dosages, which avoid damage to
beneficial organisms;
- the use of selective pesticides which have a low toxicity toward useful organisms.
Some of these pesticides have recently become available on the market.
Biological control is an important element in integrated pest control. The safeguard of
naturally occurring beneficial organisms will be an important element in each programme. The action of these organisms has been increased by massive multiplication
in the laboratory and subsequent release at the opportune time. Another approach is
the introduction and adaptation of parasites of predators not yet available in the area.
Many examples of successful introduction are available, in citrus growing for example.
Breeding for more resistant host plants, when successful, is considered one of the
cheapest methods of pest control. Work in this area has been considerably intensified
in recent years.
Cultural practices are certainly the oldest means of reducing the impact of pests.
However, the availability of very efficient modern control means and the need for
intensified agriculture tend to abandon rotation patterns, well separated crop seasons,
or the careful removal of crop remains after harvest. However, it is felt that through
cultural practices we can in many caSes still significantly reduce the importance of
certain pest species.
309
Integrated pest control tries to integrate these various control means in such a way
that a stable and lasting pest control situation is created. It is thus part of the total
complex of agricultural practices, so that when we discuss fertilizer use and plant
health we automatically enter the framework of integrated pest control.
Integrated control programmes have been developed for crops such as deciduous
fruits and cotton, where intensive use of pesticides was being made. The introduction
of these programmes has generally led to a reduction of more than 50% in the amount
of pesticides used.
3. Review of FAO documents
The changes in economic importance of pest species following intensification of
agricultural production have been noted on a number of occasions. Newsom [1965]
reviews some of the literature in his contribution to the FAO Symposium held in 1965.
But he does not discuss it specifically in relation to increased fertilizer usage. This
aspect was brought forward in a contribution on host plant resistance to the FAO
Conference on Ecology in Relation to Plant Pest Control held in 1972 (Brader [1973]).
The following was noted on that occasion:
'Nutrition of the host plant is certainly an important factor to manipulate insect
populations. However, present knowledge is far too limited to predict future developments in this field of research. Nitrogen, as a determining factor will prove in general
of little practical importance in the manipulation of insect populations. The economic
importance ofnitrogen fertilizers is such that it will most certainly prove impossible to
reduce the amounts used. A better insight into the mechanisms of its action could
provide information on the possibilities of disturbing the balance of insect nutrition.'
The FAO Panel of Experts on Integrated Pest Control has emphasised on various
occasions the significance of cultural control practices in integrated pest control
programmes. Before the intensive use of synthetic organic pesticides, cultural practices
were among the main factors used for the control of pests and diseases. In its Third
Session, held in Rome, 10-16 September 1970 (FAO [1971]) this point was discussed
in some detail, and the report contains the following statement:
'The implementation of integrated pest control programmes depends on the understanding of some aspects of the ecology of the agro-ecosystem which, of course, is
profoundly affected by all other practices involved in the production of a crop. At the
research and development stage, there is therefore a special need for collaboration
between scientists in the different disciplines. For example, collaboration with agronomists and soil chemists is essential where cultural practices and soil fertility affect
pest incidence.'
In the report of its Fourth Session, held in 1972, the Panel of Experts brings up this
question again (FAO [1973]):
'A certain amount of research in the disciplinary field contributary to integrated pest
control implementation has already been initiated, but the Panel is concerned that much
remains to be done and that this research must be carried on in localised agricultural
ecosystems in the various important crop production regions of the world.'
310
J
In fact, this is still the situation of the art today. We are well aware that fertilizers may
to some extent increase or reduce the numbers of certain pest species. However, the
information so far available is almost exclusively of a qualitative character. To be
useful in a pest control programme, it must be quantified to better predict its impact on
pest population changes and the subsequent need for additional control measures.
In this respect, it should also be recognised that our activities concern mainly the
agriculture in developing countries. The amount of fertilizer used in those conditions
is generally low compared to that in developed countries. And the concern of applying
fertilizers is primarily based on the necessity of increased crop production.
4. Fertilizer usage and pest problems
The various publications on soil fertility and fertilizers are logically mostly concerned
with the productivity changes for the crops concerned. It is undoubtedly true that Jhese
changes can be very dramatic. For the crop protection man, however, it becomes a
question of how this affects the population dynamics of pests and diseases. Unhappily,
he does not often have the necessary training, time, or facilities to find an adequate
answer to these questions. The little that we know about it is mostly reviewed in the
other contributions to this symposium. We will therefore limit ourselves to a review of
some of the recent literature related to the crops considered within FAO's integrated
pest control programme.
Cotton
Cotton is known for being attacked by a multiplicity of pest species and for the heavy
damage that it suffers when no control measures are taken. In the tropical countries,
insect pests in particular are certainly the main factor determining the outcome of
cotton production; The importance of a certain number of diseases has been 'considerably reduced through the breeding of resistant varieties. It is generally found that
fertilizers, especially nitrogen, can considerably stimulate the development of various
pest species. Adkisson [1958J points to the fact that heavy applications of fertilizers
usually prolong the growing season for cotton by keeping the plants succulent and
fruiting later. He states that there is evidence that this practice may aggravate insect
problems since (1) the longer fruiting period furnishes a source. of food for a rapid
build-up of large numbers of insects in the season, and (2) highly fertilized, succulent
plants may attract insects from unfertilized fields in which plants are no longer
succulent or fruiting. In experiments studying the impact of fertilizer application on
Heliothis zea populations, it was found that there were two to three times more larvae
in the fertilized plots than in the unfertilized checks. This was found for both unsprayed
and sprayed plots. Adkisson draws the conclusion that the rates of fertilizer application
had as much influence on the number of bollworms as the insecticide applications. The
significant increase of bollworm attack is mainly ascribed to the more luxurious
growth of the cotton plant under fertilized conditions, making it more attractive as an
oviposition site. More boil weevils (Anthonomus grandis Boheman) were attracted to
311
cotton as nitrogen fertilization was increased from 35 to 105 Ib./acre, and a greater
number of squares and boils were damaged by weevils. An increase of about 30% was
noted. However, the percentage of damaged fruits did not vary significantly, and thus
yield also increased substantially with higher fertilization. (Mistric [1968]).
In Nigeria, increased nitrogen fertilizer application resulted in such an increase in pest
attack, mainly of the bollworm Heliothis armigera, that yields became less under
unsprayed conditions (Hayward [1973]). It was demonstrated that efficient pest
control contributed far more to the final yield of cotton than did the application of
nitrogenous fertilizer. The same type of effect was found in the Sudan for whiteflies
and to a lesser extent for jassids (Jackson et al. [1973]). In this case, a comparison
was made between experimental plots with 128.3 kg N/ha and without fertilizer. Over
five growing seasons, the maximum number of jassids was on an average three
times higher in the fertilizer plots; for whiteflies the increase was about four-fold.
In a survey of control possibilities of diseases in the USA, Brown and Ware [1958]
gave some general statements which are of interest here. Balanced fertilizer containing
ample potash controlled fusarium wilt (Fusarium oxysporum f. vasinfectum). For the
control of root rot (Phymatotrichum omnivorum), fall plowing with phosphate additions is recommended. Starting fertilizer can reduce the impact of Rhizoctonia
(Rhizoctonia solani). The impact of potash addition on wilt resistance was studied
recently again by El Gindy et al. [l974] in laboratory experiments. The reactions of
wilt susceptible and resistant varieties of Gossypium barbadense toward combined or
single infections of Fusarium oxysporum f. vasinfectum and the nematode Rotylenchus
reniformis at various levels of potash was evaluated. In susceptible varieties, significant
reduction in wilt was noticeable only at 500 ppm K with the fungus alone and at
1000 ppm K when the nematode was also present. In the resistant varieties, no wilting
occurred under these conditions at 100 ppm and 500 ppm respectively. Under field
conditions, the beneficial effect ofK addition towards the control of Verticilium dahliae
in certain K-deficient soils in San Joaquin Valley, California, was also clearly proven
( Hafez et al. [1975]).
These selected examples clearly demonstrate a direct effect (negative or positive) of
certain fertilizers on various pest species. It would certainly be of considerable interest
to extend this type of research with a direct view to decreasing the impact of pest attack
on crop production.
Rice
In rice, the amount of information on the effect of fertilizers in the development of
pests is much more limited. But the findings so far also indicate that nitrogen fertilizer
has a stimulating effect on a number of pest species. The incidence of rice gall midge,
for example, increased considerably when increased amounts of N were used. On an
average, on plots receiving 60 kg N/ha the gall midge attack was increased by about
30%, compared to unfertilized plots, while 120 kg N/ha compared to 60 kg N/ha gave
an increase of about 50% (Narayanan et al. [1973]). Mixed fertilizers containing equal
portions of N, P Z0 5 and KzO proved to increase significantly the incidence of the stem
borer, Tryporyza incertulas (about 30%) and the leaf roller Cnapholocrocis medinalis
(also by about 30%) (Raj and Morachan [1973]). These facts are of particular importance in view of the high yielding varieties which are characterised by their better
response to increased application of fertilizer, particularly nitrogen (Hayashi [1972]).
312
Sorghum/millet/maize
Information on the pest complex of sorghum and 'millet is very limited, but most likely
we will find for these crops the same trends as described above. Fertilizers, particularly
nitrogen, will most probably increase the damage caused by pests and diseases. For
" maize, it was found that the plants became susceptible to stem rot (Fusarium culmorum and F. moniliforme) when grown under potash deficiency (Siebold [1974]).
Plants that were fertilized seemed to suffer greater damage from Diatraea saccharalis
under certain conditions than the non-fertilized ones (Parisi et al. [1973]). For, these
crops also, fertilizers interfere with pest control problems, but, here again, no clear
picture can yet be drawn.
Economic aspects
So far we have discussed only the biological relationship between fertilizer usage and
pest attack. It would probably be very unwise to try to give an answer to the question
of whether fertilizers or pest control contribute more to crop production improvement.
The situation will differ from crop to crop and will depend largely on the degree
of intensity of use of other crop production factors. We tend to believe that the two
complement each other and that the best profit can thus be drawn when they ar~ used'
in a well-balanced combination. To partially demonstrate this we would like to cite the
example of a cotton experiment carried out in the Chad Republic, where three levels of
fertilizers were combined with three levels of pest control (Brader and Atger [1971]).
The fertilizers used contained per 100 kg, 27 kg N, 18 kg P 2 0 S and 6 kg S. The
insecticide used was Endrin/DDT at 300/900 g active ingredient per spray per ha.
Results are given in Table 1.
It should be noted that this experiment was carried out on relatively rich soils and that
pest incidence was very severe. Under those conditions, pest control contributed
relatively more to the total production increase than fertilizer application. The strongest
fertilizer effect was achieved at 5 pesticide applications; pest control gave the best
result at 220 kg of fertilizer. But these figures will be quite different under other soil
fertility and pest incidence conditions.
The example given does, however, clearly demonstrate the economic consequences
of fertilizer application. This has become even more relevant in recent years as the
cost of pesticides has increased. It is therefore essential that we obtain a better insight
into possible changes in the pest complex and the consequent need for control measures.
We might loose the benefits to be drawn from fertilizer use if plant protection costs
become too high.
Table 1. Combined effect of fertilizer use and pest control measures. Production of seed cotton in
Kg/ha
Num ber of pesticide
applications
Fertilizer
0
5
10
479
1236
1823
Mean
1179
100%
0
220 kg/ha
"Mean
612
1681
2008
615
2030
2385
659
1649
2072
1434
122%
1677
142%
110 kg
100%
290%
364%
313
5. Discussion
It is evident from the definition of integrated pest control given at the beginning of
section 2 that full consideration should be given to those practices (fertilization
included) that interact in some way with the development of the pest species concerned.
It is well known that small changes in the reproduction rate of insect or mite species
may have considerable consequences in the overall population levels and thus on the
amount of damage caused. And this will in turn command the intensity of pest control
needed. Hensley [1971], for example, demonstrated that the introduction of a slightly
more resistant sugarcane variety permitted a notable decrease in the application of
non-selective control measures against the sugarcane borer, Diatraea saccaralis. If we
thus see that the application of fertilizers can change the incidence of rice stemborers
and rice leafrollers by 30% or even triple the attack by the cotton bollworm, Heliothis
zea, it becomes undeniable that more attention should be paid to these facts.
This is particularly so in integrated pest control, as the system is built on the principle
of maintaining the pest populations beneath the economic injury threshold. In this
approach, it is thus not intended to achieve a maximum kill, but to maintain the pest
populations at a level which is economically acceptable. And in such a situation, slight
changes in the development of the species concerned may considerably interfere with
the effectiveness of the control methods used.
The usefulness of any control strategy depends on the predictability of its impact on
population changes of the pest species concerned. Thus, for a useful evaluation of
fertilizers in plant health, we need a gOOQ knowledge of the numerical response of the
pest species. In the literature to date this is not yet available. To exploit it we would
also need a rather detailed knowledge of the population dynamics of the various pest
species. In the crops discussed above, this knowledge is often lacking in countries where
FAO is active. Close collaboration between plant nutrition and plant protection
scientists is therefore essential and will certainly prove fruitful.
In 1975, FAO, in collaboration with the United Nations Environment Programme,
started the Cooperative Global Programme for the Development and Application ofIntegrated Pest Control in Agriculture. This should provide for a considerable extension of
current field activities. For the time being, this programme will concentrate on the
three groups of crops mentioned earlier, developing inter-country programmes which
will rely mainly on existing national activities. It is hoped to strengthen national capabilities in integrated pest control with the help of a relatively small amount of foreign
expertise. Emphasis is on demonstration of the feasibility of integrated pest control and
on information transfer through intensive training. For this, it is proposed to set up
demonstration study areas where conventional control will be compared with new
integrated pest control programmes. These areas will also serve to identify research
needs. It is expected that close collaboration with national research institutes will allow
part of the problem-oriented research to be carried out by these institutes. It is through
this research element that the question of fertilizers will also be considered. This does
not necessarily need to be limited to the direct relationship discussed above, but it will
most certainly also concern aspects such as the possibility of shortening the seedling
stage of the plant in order to avoid the damage caused by many seedling pests, timing
and dosage of fertilizers to compensate for damage caused at a certain point of the
growing stage, and choice of fertilizers which could create changes in the growing cycle
of a crop and thus enable a partial escape from pest attack.
314
Decisive in all this work will be the economic outcome of the total package of measures
contributing to inc!eased agricultural production, and it is on this basis that we hope
to develop the most suitable crop protection programmes.
crop
damage
1
.
CD/CA=1 ~J---------------------/
I
I
I'
I
I
I
I
I
I
I
I
A
:>
B
numbers of a
pest species
Figure 1. Schematic representation of a relationship between pest numbers and crop damage to
illustrate the determination of the economic injury threshold (B) and the economic damage threshold (A). CD = cost of damage, CA = cost of application.
References
I. Adkisson, P.L.: The influence of fertilizer applications on populations of Heliothis zea (Boddie),
and certain insect predators. J. Econ. Ent. 51, 757-759 (1958).
2. Brader, L.: Ecological basis for insect pest control - Host plant resistance. Proc. FAO Conf.
Ecology in relation to plant pest control, Rome, 55-64 (1973).
3. Brader, L. and Atger, P.: Activite de I'IRCT en 1969-70. Station Centrale de Bebedjia, Section
d'Entomologie, Cot. Fibr. Trop. 26, 20-21 (1971).
4. Brown, H.B. and Ware, J.O.: Cotton. McGraw Hill Book Co., Inc., New York, 566 pp. (1958).
5. El-Gindy, A. Y., Oteifa, B. A. and Khadr, A. S.: Relations entre Rotylenchus reniformis, Fusarium
oxysporum f. vasinfectum et la nutrition potassique du cotonnier, Gossypium barbadense. Revue
de la Potasse 23/43, 1-5 (1974).
6. FAO: Report of the third session of the FAO Panel of Experts on Integrated Pest Control. Rome,
AGP: 1970/Mj7, 38 pp. (1971).
7. FAO: Report of the fourth session of the FAO Panel of Experts on Integrated Pest Control,
Rome, AGP: 1973/M/5, 35 pp. (1973).
8. Hafez, A.A.R.; Stout, P.R. and De Vay, J.E.: Potassium uptake by cotton in relation to Verticillium wilt. Agron. J. 67 (3), 359-361 (1975).
9. Hayashi, K.: Current development and relating problems of rice varieties with high yielding
potential. Int. Rice Comm. Newsletter 21 (4), 18-31 (1972).
315
10. Hayward, J.A.: Relationship between pest infestation and applied nitrogen on cotton in Nigeria.
Cotton Grow. Rev. 49, 224-235 (1973).
11. Headley, J. c.: Environmental Quality and the Economics of Agricultural Pest Control. EPPO
Bull. 3 (3), 51-61 (1973).
12. Hensley, S.D.: Management of sugarcane borer populations in Louisiana, a decade of change.
Entomophaga 16, 491-505 (1973).
13. Jackson, J.E.; Burhan, H.O. and Hassan, H.M.: Effects of season, sowing date, nitrogenous
fertilizer and insecticide spraying on the incidence of insect pests on cotton in the Sudan Gezira.
J. Agric. Sci., Camb. 81, 491-505 (1973).
14. Mistric, W. J.: The effects of nitrogen fertilization on cotton under boil weevil attack in North
Carolina. J. Econ. Ent. 61, 282-283 (1963).
15. Narayanan, K.; Chandrasekaran, J.; Meerzainudeen, M. and Jayaraj, S.: Effect of graded levels
of nitrogen on the incidence of rice gall midge. Madras Agric. J. 60 (7), 572 (1973).
16. Newsom, L.D.: Essential role of chemicals in crop protection. Proc. FAO Symposium on
Integrated Pest Control 2, 95-108 (1966).
17. Parisi, R.A.; Ortega, A. and Reyna, R.: El daiio de Diatraea saccharalis Fabricius (Lepidoptera:
Pyralidae) en relacion con la densidad de plantas, nivel de fertilidad e hibridos de maiz, en
Argentina, Agrociencia 13, 43-63 (1973).
18. Raj, S. M. and Marachan, Y. E.: Effect of fertilisation and diazinon application on the incidence
of stem borer and leaf roller on rice. Madras Agric. J. 60 (7),431-435 (1973).
19. Siebold, M.: The influence of potash on stemrot in grain maize. Results from two years' field
experiments in E. Bavaria. Potash Review 23 (44/5), 1-4 (1974).
316
Contribution to the Discussion:
The Effect of K on Insect and Mite Development
S. Perrenoud, Ing. agr., International Potash Institute, Bern/Switzerland
A survey of 144 references in the literature concerning the effect of potassium on
damage to agricultural and forest crops caused by insects and mites is summarised in
Table 1 and Figure 1.
Table 1. Number of references showing effects of K on insect and mite development
LowK
or nil
Development stimulated
No effect on development
Development decreased
.
.
36
19
8
Medium K
0
8
17
HighK
17
18
21
100
50
K-, KN, K+: as for Tab. 1
~ Developement depressed
11
Developement unchanged
•
Developement stimulated
Fig. 1. Effect ofK on insect and mite development
It seems that low potassium supply frequently favours the development of insects and
mites while adequate or high potassium has a depressant or neutral effect. High
nitrogen and high N: K ratios often stimulate insects and mites. It folIows that increasing N should be balanced with K. In addition to effects on pest development, plants
receiving welI balanced fertilizer are better able to withstand attack and recover
better and more rapidly. Fertilizer effects depend on various factors such as soil type
and soil fertility and further research is needed before practical recommendations
can be made.
317
Contributions to the Discussion on Fertilizer Interaction with Pests and Diseases
in Forest Trees
Dr. H.Baule, Staufenberg(Lutterberg(Federal Republic of Germany
I.
I should like to comment on the questions treated up to now during the Colloquium:
Considering papers from the whole field of plant cultivation, the following statements
can be made on the questions treated so far:
The view of Primavesi and Primavesi [1964], that any plant disease is connected with
an earlier and exactly defined specific mineral deficiency, seems to be well-founded.
This was confirmed by Merker [1969] who pointed out the relationship between
nutrient deficiency and water economy of the trees and concluded that reductions in
attacks by bark beetle, sapwood borer, oak burncow, pine shoot moth, spruce and pine
sawfly, gipsy moth and black arches moth are correlated with the osmotic pressure of
the trees. According to Holstener-Jorgensen and Eiselstein [1969], however, the
assumption that excessive water supply due to a high ground water level is the cause of
the increased susceptibility of beech to beech scale disease has not yet been confirmed.
The conditions found in the inner bark play an important part in pest and disease
attacks. Changes in the nutrient ratio and other growth factors have an effect on
phloeophagus beetles spending most of their life cycle, including all immature stages,
in the bark (White, Wells and Clark [1970]). Significant correlations have been
found between the nutrient contents of the inner bark and the needles of the same tree.
Heimann [1971] thinks that the major advantage of fertilizer application, as an
alternative to the use of pesticides, can be seen in a 'deliberate disturbance of the ionic
balance in the feeding habitat of the parasites'. In this he considers the change in the
Na-K relationship to be the decisive factor. 'The so-called luxury consumption of K
seems to be detrimental to many of the pests feeding on these plants'. Primavesi,
A. M. C. [1964], came to similar conclusions. The same is true of numerous statements
in the recently published survey by Chaboussou [1973] on the role of K and cation
equilibrium in the resistance of plants to pests and diseases.
Attention should be paid to an adequate N :K ratio since Nand K play a major part in
resistance to adverse agencies: while N reduces the resistance, K improves it (Grossmann [1970J). Cheng and Tu [1970J also underlined that this is a decisive factor in
obtaining high yields of jute free from stem rot. Rowan [1971] found that black root
rot of slash pine was dependent on temperature. High soil temperatures and heavy N
dressings produced the most severe root rot symptoms, whereas K did not increase
disease severity at either temperature.
Nutrient analyses provide valuable information in this respect since changes in the
nutrient content of the assimilatory organs and tissues will be observed after the attack
by pests and diseases (Sinner and Rehfuess [1972J; Martin [1972J). Such induced
changes must be taken into account in all diagnoses in order to avoid confusion of
cause and effect.
Plant constituents which influence attack by pest and disease cannot be treated here in
detail. Any study of fertilizer treatment should consider the effect on the synthesis of
lactic acid, alkaloids, non-protein nitrogenous compounds, such as asparagine, and on
soluble amides or amino acids, which may be easily utilized by pathogens. The same
applies to phenols which can be affected adversely by excessive N (Shigo [1973]).
318
These protect plants from infestation, especially from attack by rust fungi, and are
often found in greater amounts in more resistant plants than in those readily susceptible
to diseases and pests.
At a 1973 meeting in Munich, it was reported that cuticular waxes and terpenes play
an important part in reducing fungal diseases (Schiitt [1973J). It is our task to find
out which nutrients, which forms of nutrients, and which nutrient combinations may
exert a favorable influence on the synthesis of these waxes' and terpenes. The same
applies to those types of virus and bacteria increasingly used at present for pest control
but which bear no harm to the environment (Skatulla [1973 J). Certain hormones, less
known inhibitors (Klingstrom and Johansson [1972J), nutrients and agents essential
for the parasites, and all mechanisms affecting anatomic and histological reactions,
for example the structure of stomata, the strengthening of cell walls, and the synthesis
of separating tissue are among these factors. This suggests a need for new research
which, if it is thorough, may eventually produce evidence to support the view of an
American forester: 'We may choose to fertilize to prevent pest attacks (Criff [1970 J).
References
Primavesi, A. and Primavesi, A. M. C.: Beziehung zwischen Pflanzenernahrung und Pflanienkrankheiten. Z. Pfl.Ernahrung, Diingung, Bodenkunde 105, H. 1, 22-27 (1964).
Merker, E.: Die Zuverlassigkeit der Bestandesdiingung gegen Waldschadlinge. Waldhygiene 8,
Nr.l-4, 1-100 (1969).
Holstener-Jorgensen, H. and Eiselsiein, L.M.: Investigation into the possibility of root drowning
as a cause of Cyptococcus fagi attacks and other diseases in beech stands. Soertryk af Det
Forstlige Fors0gsvaesen i Danmark beretning nr. 250, bd. XXXII, n. 2 (1969).
White, J.D., Wells, G. G. and Clark, E. W.: Variations in the inorganic composition of inner bark
.' and needles ofioblolly pine with tre.e height and soil series. Canadian Journal of Botany 48, No. 6,
1079-1084 (1970).
Heimann, H.: The deliberate disturbance of the cationic environment as an alternative to pesticides
in plant protection. Israel Journal agric. Res. 21, 2, April (1971).
Primavesi, A.M.G.: Kaliaufnahme und Schadlingsanfalligkeit von landwirtschaftlichen Kulturen
in den Tropengebieten Brasiliens. Kali-Briefe des Internationalen Kali-Institutes Bern, Fachgeb.23, 30. Folge, Juni (1964).
.
Chaboussou, F.: Le role du potassium et de I'equilibre cationique dans la resistance de la plante aux
parasites et aux maladies. Au service de I'agric. (SCPA) No. 2, Doc. technique 16, 1-26 (1973).
Grossmann, F.: Einfluss der Ernahrung der Pflanzen auf den Befall durch Krankheitserreger und
Schadlinge. Landw. Forschung, So. Heft 25/1 (1970).
Cheng, Y. H. arid Tu, G. C.: Effect of nitrogen and potash fertilizer on the occurence of stem rot of
jute. Taiwan Agric. Quarterly, VoI. IV, No. 4, 93-100, Dez. (1970).
Rowan, S.J.: Soil fertilization fumigation, and temperature affect severity" of black root rot of slash
pine. Phytopathology 61,184-187, Febr. (1971).
Sinner, K.F. and Rehfuess, K.E.: Wirkungen einer Fomes annosus-Kernfa~le auf den Ernahrungszustand alterer Fichten (Picea abies Karst.), Allg. Forst- u. J.-Ztg., 143. Jg., 3/4,74-80 (1972).
Martin, N.E.: Influence of blister rust on inorganic solute concentrations in western white pine.
Phytopathology 62, 226-229 (1972).
Shigo, A .L.: Insect and disease control: Forest fertilization relations. Forest fertilizations symposium
•
Proceedings USDA Forest Service General Technical Report NE -3, 117-121 (1973).
Schiitt, P.: Die Phyllosphare, eine Zone hoher biologischer Aktivitat. Vortrag, gehalten anI. der
ForstIichen Hochschulwoche in Miinchen, 29.-31.10. (1973).
Skatulla, U.: Einsatz von Viren, Bakterien und Hormonen als Alternativezum chemischen Forstschutz. Vortrag, gehalten anI. der ForstIichen Hochschulwoche in Miinchen, 29.-31.10. (1973).
Klingstrom, A. E. and Johansson, S. M.: Antagonism of scytalidium Isolates against Decay Fungi.
Phytopathology 63, 473-479 (1972).
.
Criff/Cooperative Res. in Forest Fertilization, Univ. Florida, School Forest, Dep.Soiis, Ann'ual
Report (1970).
. .
319
11. A Note on the Papers by Messrs. Dimitri and Bogenschfitz
Dr. H.Baule, Staufenberg/Lutterberg/Federal Republic of Germany
Needle and leaf eating insects and some others that breed in the bark are known to
react to N fertilizers by a reduction in the severity of attack (Ohnesorge [1957],
Schwenke [1960], Biittner [1961] and Merker [1960,1963,1967]). Needle analysis
showed increased values for P, K, Mg and Ca as well as for N (Merker [1967]). These
experiments were done on relatively fertile sites so that N fertilizer influenced the
absorption of other nutrients.
N fertilizer is known to mitigate attack by: Bupalus piniarius, the pine looper moth
(Schwenke [1961]); Diprion pini, the pine sawfly (Schwenke [1960]); Lymantria
monacha, the black arches moth (Biittner [1956]); Ips curvidens, the fir bark beetle
(Merker [1967]); Ips typographus, the engraver beetle (Merker [1967]); Pristiphora
abietina (Ohnesorge [1957]; Merker [1960, 1963]; Biittner [1961]); Brachyderes
incanus (Bischoff [1967]) and Evetria buoliana, the pine shoot moth (Schindler and
Baule [1964], Schindler [1967]).
To discuss the influence of fertilizer treatment we shall consider Evetria buoliana. In a
fertilizer experiment at Tinnen, Emsland/F.R.G., Schindler and Baule [1964] found
that 5 years after establishment and 3 years from the start of fertilizer treatment attack
by Evetria was at 50% regardless of treatment. This suggested treatment in March 1960
with 6 kg/ha Gesarol-50 paste (3 kg active ingredient) applied to all 14 plots of the trial
which resulted in an initial reduction in the number of pine shoot moths. But, in May
1963 there was a new and severe attack (Figure 1) when counts of damaged terminal
shoots showed results quite different from those of 1960. Fertilized plots were distinctly
less attacked than the untreated plots by from 27-46%, the greatest reduction being
observed on the two NPKMg plots. These data show that the nutrients applied evidently needed a few years to take effect against pine shoot moth. The experiment
included tests of the effects of N, P, KMg, K ZS0 4 and B. Due to increasing parasitization of pine shoot moth caterpillars the severity of attack in 1964 was reduced on all
areas but there was a tendency for fertilizer to reduce its severity further by from 59 to
71 %, and this on plots treated with fertilizer seven years previously! The attack was
effectively reduced to levels which were no longer economically significant.
Schindler obtained similar results in a fertilizer experiment laid down in 1958 in the
Langenloh (Dudenhofen) forest district near Dieburg/F.R.G. Though the average
attack per 100 terminal shoots was lower in this experiment, done under different
climatic and site conditions from Tinnen, the pine shoot moth population was reduced
320
%
50
"0
(l)
..>::
Cl
Treatment with
pesticide
March 1960
40
...,
...,ro
ro
.....{f1
30
0
0
..c:
{f1
-s::
ro
's
20
!-<
Q)
E-o
10
:::"
Year
Age of pine
Height of pine
1959
4
O. 6
~
60
61
62
5
6
7
1. 5 m
63
8
64
9 years
1.5-3 m
Figure 1. Attack of Evetria (Rhyacionia) buoliana on nonfertilised plots (black columns) and
NPKMg plots (shaded columns).
by about a half on all plots treated with N, P, K, or Mg alone or in combination. The
same was true for NPKMgCa but where lime only was applied the attack was at the
same level as in the control.
Pritchett and Smith [1972] measured the effect of fertilizers on insect attack, in which
Rhyacionia spp. comprised 95% of the insect population, on 3 year old pine in the US
Lower Coastal Plain. Figure 2 shows the effect ofP and K fertilizers in reducing attack.
Observations by Eidmann and Ingestad [1963] do not agree. with the above findings.
They found that on the Island of Gotland on a calcareous soil that treatment of pines
with 100 kg/ha N improved growth but also considerably increased attack by insects,
particularly Evetria buoliana, saying that this result was due to the extreme conditions
of the site. Growing under extreme deficiency of both water and nutrients the stunted
trees could obviously 'offer only very unfavourable living conditions to Evetria and
other species'. The initial improvement in growth caused by fertilizer would first create
conditions more favourable for attack, since the optimum for Evetria lies between the
extremes of vigorous growth and marked stunting. Unbalanced N treatment could
hilVe caused dilution of P and K supplies again providing conditions suitable for
attack.
Summarizing, Evetria buoliana and other biting insects find the most favourable
conditions in those areas which are slightly more fertile than the poorest locations. It is
only by radical improvement of the site through applying large amounts of fertilizer
containing all the major nutrients that one can achieve the 50% reduction in attack
(Figure 3). But we must not overlook the fact that while N may be effective in com321
30
eQ
....0tIl
20
Q)
tIl
.S
>.
.0
'0
Q)
..I<:
0
«l
.... 10
..,
«l
tIl
Q)
Q)
~
Eo<
0+-""'-......_ ..........................- 1 - - - & - o 22.5 90
Control
N added. kg/ha
o
22.5
90
Padded. kg/ha
(+90 K)
NPK
Figure 2. Average effects of fertilizer treatments on prevalence of insect damage to 3-year-old slash
pines in five experiments. Extract from the publication by W.L.Pritchett and W.H.Smith: 'Fertilizer responses in young pine plantations'. Soil Sci. Soc. Am. Proc. 36, 4, 660-663 (1972).
o
>.
!
I
Relatively sltght
attack
Danger zone for
I
Increased attack by
Bucking Insects owing
I
Location with I
extreme
I
nutrient
I
poverty and I
inadequate
I
water supply I
Slightly
improved
location
Radically
improved
location
to nutrient supply
being unbalanced.
partlculary with
too high a proporUon
of nitrogen
- - ..........1
Increasing grO\vth Intensity
. Figure 3. Schematic representation of attack by eating and sucking insects on forest trees.
bating biting insects it can increase susceptibility to sucking insects especially when
nutrient imbalance is involved (cf. Figure 3 right). Biittner [1963] has shown for
example, that there was an explosive increase in aphid population when heavy N
dressings were applied to pine (cf. also Schwerdtfeger [J 963]) .
322
References
Ohnesorge, B.: Untersuchungen tiber die Populationsdynamik der Kleinen Fichtenblattwespe,
Pristiphora abietina (Christ.) (Hym. Tenthr.). Z. angew. Entomol., 40, 443-493 (1957).
Schwenke, W.: Uber die Wirkung der Walddtingung auf die Massenvermehrung der Kiefernbuschhornblattwespe (Diprion pini L.) 1959 in Mittelfranken und die hieraus ableitbaren gradologischen Folgerungen.Z. angew. Entomol., 46, 371-378 (1960).
Biittner, H.: Der Einfluss von Dtingestoffen auf Mortalitat und Entwicklung forstlicher Schadinsekten tiber deren Wirtspflanzen. Schriftenreihe d. Landesforstverw. Baden-Wtirttemberg 11
(1961).
Merker, E.: Die Bekiimpfung von Waldschadlingen durch geeignete Dtingung der Bestandesboden.
XI. Int. Entomologen-Kongress Wien, Verhandl. Il, 198-202, 4962 (1960).
Merker, E.: Die Bekampfung der Kleinen Fichtenblattwespe durch Dlingung der Bestandesboden.
AFJZ 134, 72-76 (1963).
Merker, E.: Die ktinstIiche Erhohung der Pflanzenresistenz gegen Borkenkiifer. AFJZ 138, 13-24
(1967).
Schwenke, W.: Walddlingung und Schadinsekten. Anz. Schiidlingskde. 34, 9, 129-134 (1961).
Biittner, H.: Die Beeintriichtigung von Raupen einiger Forstschiidlinge'durch mineralische Dlingung
der Futterpflanzen. Naturwissenschaften 43, 454-455 (1956).
Bischoff, M.: Untersuchungen von Frassschiiden des Graurlisslers (Brachyderes incanus L.) auf
Dlingungs-Versuchsflachen. DFuH 22, 131-135 (1967).
Schindler, U. and Baule, H.: Forstliche Dtingung und Kiefernknospentriebwicklerbefali. AFZ 19,
534-537 (1964).
Schindler, U.: Einfluss der Dtingung auf Forstinsekten. Vortrag, gehalten anlassl. d. vom Internationalen Kali-lnstitut Bern veranstalteten 5. KoIloquiums liber Forstdlingung in JyvaskyliijFinnland vom 22.-26.Aug. (1967).
Pritchett, W.L. and Smith, W.H.: Fertilizer responses in young pine plantations. Soil Sci. Soc.
Am. Proc. 36, 4, 660-663 (1972).
Eidmann, H. and 1ngestad, T.: Erniihrungszustand, Zuwachs und InsektenbefaIl in einer Kiefernkultur. Studia Forestalia Suecica (Stockholm) 12, 1-22 (1963).
SchwerdtJeger, F.: Oekologie der Tiere. I. Autokologie. P.Parey, Hamburg-Berlin. 1963.
323
Contribution to the Discussion on Nematodes and Insects
P. Martin-Prevel, Director of Research, Plant Physiology Department, Institut de Recherches sur
les Fruits et Agrumes (IRFA/GERDAT), Montpellier/France
Nematodes
The lower mineral content of plants attacked by nematodes is usually explained by
the effect of the latter on absorption by the roots, but, in the case of pineapples, we
have indirect proof that they cause loss through the roots of minerals contained in the
plant. Work carried out by my colleagues J.J. Lacoeuilhe, R. Gerout and J. Marchal in
the Ivory Coast shows that pineapples which receive all their Nand K by foliar
fertilization have poorer above-ground development and lower Nand K content the
more severe the nematode attack. Certainly their roots must excrete Nand K; among
other things their leaf content of Ca and Mg is higher indicating increased absorption
due to antagonistic effects of the excreted K.
Insects
Dr. Bogenschiitz will be interested in information concerning tropical forest pests
given by F. Brunck (Head of the Division of Entomology and Pathology at the
Tropical Forest Centre (GERDAT).
(1) Hypsipyla robusta Moore on Khaya ivorensis.
(a) Comparison of two sites in the same area of Ivory Coast.
- Yapo: severe attack, strong growth, leafN, P and K high, S deficient (less than 0.2%)
- AnguMMou: mild attack, less vigorous growth, leaf N, P and K rather low, S
normal (above 0.3%).
The S deficiency has to be confirmed by further work.
(b) Phytolina lata Scott on Chlorophora excelsa.
Growth at 1 year
Attack at 1 month
Attack at 1 year
Attack at 1 month
Attack at 3 months
Attack at 1 year
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.
.
.
.
.
.
Without fertilizer
(100)
12%
76%
K2 SO. 20 gjplant
120
4%
61%
Without fertilizer
Fert. formula
5-12-24
20 gjplant
7%
25%
68%
12%
25%
76%
General Remarks
I would like to take the opportunity to point out how dangerous it can be to speak of
the effects of fertilizer application without reference, in every case, to whether the
rates correspond to the needs of the plant. The effects of an element are very different,
for example, in the range of strong response to that element (maximum utilisation),
in the range of slight response and in the range of luxury consumption (part of it not'
utilised by growth processes). The side effects of an element can equally differ
according to soil conditions and conditions in the plant. Thus excess P can induce
Zn deficiency (the first description of zinc deficiency in pineapple was in fact of
lesions caused by Diaspines attacking deficient plants).
325
Contribution to the Discussion: The Effect of Fertilizers on the Health of Farm
Crops in Czechoslovakia - Some Research Results
Dr. J. Baier, Institute for Plant Nutrition, Prague/Czechoslovakia
High rates of fertilizers are used in Czechoslovakia, averaging 220 kg/ha (N + PzOs +
KzO) on all farm land and reaching 350 kg/ha on some arable farms. Some plant
health problems have been or are the subject of research.
The effect of fertilizers on the health of sugar beet was studied in long term trials
(VOP; Caca 1970). There was a close relation between foliar yellowing, cercosporiosis
and mildew attack and fertilization. Fertilizers, especially when well balanced, improved the health of crops whether applied at high or Iow rates. Phosphorus and particularly potassium had beneficial effects when applied in combination with nitrogen.
Vesely (1971) grew sugar beet continuously to study the spread of nematodes. The
attack was severe on plants with dark green leaves which had received much N while
there was no attack on plants with light green leaves. It seems that well nourished
plants, particularly with N, were more attractive to the beet nematode.
Baran (1974) studied the effect of varying NPK rates to maize on the occurence of
Rungsia maydis (Passerini). Even well balanced applications of the main nutrients
increased the occurence of the pest.
Vanova (1973) studied the effect of nutrition of spring barley (cv. Diamant) grown in
nutrient solution on susceptibility to powdery mildew (Erysiphe graminis DC).
N0 3-N increased susceptibility at high light intensity while at Iow light intensity the
effect was unclear. NHcN or urea decreased susceptibility as compared with N0 3 .
Potassium reduced susceptibility, while phosphorus had no definite effect.
Strnad (1975) examined the influence of Calixin in combination with various fertilizer
treatments on the occurence of mildew, using the same cultivar. In 1974, when the
attack was severe, Calixin had a large effect, yield being increased by 11.5% on the
average of all fertilizer treatments and the greatest reduction was achieved (14-16.3 %)
when Calixin was combined with high potassium fertilizer.
References
Baran, M.: Vplyv intenzivnej chemizacie kukurice na pocetnost vosiek Rungsia maydis (Passerini).
Agrochemia 14 (7), 213-215 (1974). (The influence of di.fferent intensities of maize fertilization on
the occurrence of aphids Rungsia maydis (Passerini).
Caca, z.: Zdravotni staY cukrovky ve vztahu k vyzive rostlin. Agrochemia 10 (6), 159-162 (1970).
(The health of sugar-beet in relation to nutrition).
Vtinovti, M.: Vliv vyzivy na nachylnost jarniho jecmene k padli travnimu Erysiphe graminis DC.
Ochrana rostlin 9 (2), 79-99 (1973). (The effect of nutrition on the susceptibility of spring barley
to powdery mildew (Erysiphe graminis DC).
Strnad, P.: Vysledky pokusu s aplikaci Calixinu ujarniho jecmene. Uroda XXlll (6), 211-212 (1975).
(The results of experiments with Calixin for treatment of spring barley).
Veselj, D.: Vicelete opakovane pestovani cukrovky a jeho vliv na rozsifen' fepnych nematodu.
Listy cukrovarnicke 87 (11), 241-244 (1971). (Maize growing repeated for several years and its
effect on the spread of beet nematodes)
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Report of the Co-ordinator of the 4th Session
Prof. Dr. D. Schroeder, Institute of Plant Nutrition and Soil Science,
Christian-Albrecht-University, KieljFederal Republic of Germany; member of the
Scientific Board of IPI
.
The Session was concerned with the relationships between fertilizer use and pests, in
other words: animals - mainly insects, mites and nematodes -, which attack plants and
crops. Little or no work has been done concerning slugs, birds and other animals. One
main paper and five communications were presented during the session, and in the
discussion three additional short contributions were given. Since you have participated
in the session and you are probably more or less familiar with the data presented, I do
not intend to discuss aB papers and discussion remarks in detaiL
As a soil scientist who is not directly involved in this special subject I can only try to
describe the impressions I received during the session on the present status of research
in this intricate field of investigation.
In my opinion, the relation between fertilization, pests and plant resistance is not as
close as it is with fungal, bacterial and virus diseases. A major reason may be that the
pests have the inherent ability to find suitable hosts which provide the appropriate
living conditions. Though the relationship between host and parasite might be
affectea by fertilization, in spite of the fact that a great number of data is available, the
scientific approach to this problem is still rather unsatisfactory. My personal feeling is
that up to now the level of research is restricted to observation and description of
phenomena. The results obtained are often contradictory and fragmentary. In addition
they are in most cases not comparable, as was pointed out by various speakers. This
may be due to the fact that investigations have been made with various species and
races of pests, with different host cultivars; with soils and substrates of various
properties under differing climatic conditions and by various methods. This means that,
in most cases, the results were affected by a great number of uncontroBed parameters
making causal interpretation of the results impossible.
Almost aB speakers stressed that results are of value only for a distinct location so that
general conclusions cannot be drawn. It is not therefore surprising that results concerning the influence of fertilizers on pests are reported as positive, negative, or without
effect.
It can be said with some certainty that crops and plants with good balanced mineral
nutrition are, on the one hand, favoured by pests because they provide a better food
supply but, on the other hand they are less affected by pest attack due to their better
growth and health through which the plant can 'escape' critical growth stages more
327
>,
rapidly while the destroyed or damaged parts of the plants are more easily replaced.
This can be summed up as follows: fertilizers often have ambivalent effects.
The above holds true especially for nitrogen. However in the case of phosphorus and
potassium and the other nutrients, this general statement is not yet justified, in spite of
the additional information given in the discussion. As far as potassium is concerned,
there seems to be at least a tendency that a good potassium status depresses development of insects and mites.
The collection of further data and the evaluation of more pot and field experiments is a
very important pre-requisite as a basis for further research. Then, research must
progress from the empirical phase to investigations in which causal interpretation is
possible. This means that we have to study only one or two parameters at a time under
controlled conditions, while other parameters are eliminated or held constant.
The final aim must be to uncover the physiological and biochemical mechanisms
involved in the influence of mineral nutrition on both resistance and susceptibility.
This is, of course, a difficult task but as an example I would like to mention the study
by my colleague Dr. Schulz who presented in a paper in the first session results
obtained in this way.
In his main paper Dr. Jones summarized the present state of knowledge as follows:
'There is no evidence in most pest-crop conditions, that fertilizers have more than a
marginal effect in a plant's real resistance to pests'.
We should, however, be optimistic, that one day in the near future we shall able - more
than at present - on the basis of deeper understanding of the causal connections, to
improve plant health with regard to pests by proper fertilizer management.
328
Closing Address
P. Chaudet, Former President of the Swiss Confederation, President of the International Potash
Institute, Rivaz/Switzerland
Professor Taysi, Members of the Scientific Board, Ladies and Gentlemen:
We have just completed several days of hard work. The 12th Colloquium was distinguished by the large number of scientific disciplines involved in our debate: soil
science, plant ~utrition, plant physiology, plant pathology, entomology, biology
among others. It has tried to erect a bridge between the two branches chiefly concerned in the Colloquium: plant nutrition and plant pathology. The twenty six
lectures and communications were evenly divided between the two disciplines.
As I indicated during the First Session, this Colloquium has been something of an
experiment which was undertaken not entirely without apprehension, but my impression at the end is one of success and real achievement in the following:
- a great deal of valuable factual information has been brought together in the
working sessions,
- the papers presented and the discussions have shown the limits of our knowledge in
the various fields,
- one imperative requirement has emerged from our deliberations: the necessity to
intensify research to obtain more precise information about the effects of fertilizers
on the resistance of plants to diseases and pests. As well as placing on record tte
existing information we have awakened renewed interest in the need for cooperation
between the specialists in the two fields of plant nutrition and plant pathology,
- the realisation of the aims of World food production depends in large measure on
the results obtained in these two disciplines. It is apparent from your discussions
that different workers use different methods in their research and that their results
are not easily compared. I think it is incumbent upon specialists in these sciences
. to decide on common parameters so that they can coordinate their results and thus
improve their efficacy. The ultimate aim of all research should be to produce
.
results which are of practical value to agriculture.
J have the impression that the participants in our twelfth Colloquium have taken full
advantage of the opportunity which it offered for the exchange of views with their
colleagues from other countries. I have already said that some among the organisers
of the Colloquium had doubts about the chances of a favorable outcome. It is therefore with all the more satisfaction that I can say, once again, what an important role
the International Potash Institute has played in the organisation of this scientific
329
meeting which has been the desire of so many for so long a time. I can only hope.
and that with confidence, that the Institute will in the future continue to occupy itself
with issues of equally great practical importance. It is to be hoped that the contacts
established during this Colloquium in Izmir will develop themselves in the future by
way of practical interdisciplinary cooperation in these problems of common interest.
I must not conclude my remarks on the results of your work here without expressing
my warmest thanks to the following, who have contributed so much:
- to the Minister of Agriculture, whose presence graced our opening session,
- to Dr. Kiroglu, Director General of Agricultural Research in Turkey,
- to Professor Taysi, President of the Colloquium,
- to the Rector of the University of Izmir,
- to the Dean of the Faculty of Agriculture,
- to the members of the Preparatory Committee: Prof. Mengel who did the lion's
share in the preparation of the scientific programme: Prof. Arnon and Prof. Malquori,
- to the coordinators, Prof. Laudelout, Monsieur Drouineau and Prof. Schroeder,
- to all the participants,
- to Dr. Hempler and Mr. Cohen who for several years have developed contacts with
agricultural research in Turkey and who have done much to prepare the ground
for the Colloquium,
.
- to Dr. Agme the representative of the I.P.I. in Turkey who has contributed much
to the smooth organisation here.
It must also not forget to include in my expression of gratitude the Directors of the
Institute, Dr. von Peter and Mr. Kiinzli with their collaborators Mr. Biiggli and
Mr. Perrenoud, Miss Murr and Miss Rohrbach.
We shall leave Izmir with happy memories of an enchanting country and of a welcome
which could not have been surpassed. We are particularly happy to have been able to
establish direct personal contact with the political and scientific authorities of a
people who will be called upon to make great efforts in the field of agricultural production. I learned yesterday that, I think I am correct, the area cultivated in Turkey extends
to 26 million hectares and that this has to provide for the needs of a population which
is increasing at the rate of one million each year. As the possibilities for extending the
cultivated area have already been exhausted, it is only through intensification that
those charged with the responsibility of providing for the needs of the people can
realise their aim. The matters with which we have been concerned here can contribute
much to matching agricultural production to the demands of increasing population.
We know well that we cannot afford to relax for a moment in our efforts to devise
means of solving these problems. The work of the International Potash Institute is of
increasing significance to all those who are concerned about the future of a society
whose continued existence depends upon the natural resources with which it has
been blessed.
It only remains for me to wish you well and a safe return to your homes and your
various fields of activity.
The Izmir Colloquium is now closed.
330