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EFFECTS OF PREVIOUSLY DAMAGED STRAWBERRY PLANTS
ON TETRANYCHUS URTICAE KOCH (ACARI: TETRANYCHIDAE)

Nancy Mabel GRECO and Norma Elba SÁNCHEZ 1
(Accepted October 2002)
TETRANYCHUS URTICAE
INDUCED RESPONSES
INDUCED SUSCEPTIBILITY
STRAWBERRY
WESTERN AUSTRALIA
ARHODEOPORUS
NEW SPECIES
DESCRIPTION
S: We report the effect of initial damage on subsequent populations of
Tetranychus urticae Koch in two strawberry cultivars. In ‘Selva’ cultivar the
damage levels assayed were 622.50 and 2458.75 mite-days/plant. In ‘Milsei
Tudla’ they were 1157.80, 2339.15 and 4101.20 mite-days/plant. After the
damage, the plants were kept free of mites during 15 days. Then, excised leaves of
‘Selva’ plants and whole ‘Milsei Tudla’ plants were infested with 10 females,
counting the offpring at different intervals. In ‘Selva’ cultivar, the number of eggs
and immatures of T. urticae as well as the egg-days/female-days ratio were higher
in plants exposed to the highest level of damage. This effect was not detected in
‘Milsei Tudla’. The stage survival rates and the duration of stages were unaffected by previous damage in both cultivars. The demographic pattern found in
‘Selva’ cultivar suggests that induced susceptibility against T. urticae is due
primarily to differences in fecundity.
I
Plants often respond to herbivore feeding by changing chemically, physically and even morphologically
(E-L et al., 1998). Induced responses have
been reported from a diverse range of plant species
(K & B, 1997) and may influence current or subsequent populations of the same or different species of herbivores. Those induced responses
that reduce herbivore survival, reproductive output
or preference for a plant are termed ‘induced resistance’ and have important implications for the evolution and population ecology of the plants and their
herbivores (K & M, 1989; K &
B, 1997; A, 1998, 1999, 2000; D
et al., 2000; U, 2000). On the other hand,
some plants may become either more preferred by
herbivores or more suitable in terms of increased
herbivore performance or population size after they
have been damaged. This effect is termed ‘induced
susceptibility’ and has been reported for many plant
species as well (K & B, 1997). Moreover, there are many examples in which herbivore performance was not affected by previous damage to the
host plant (H & N, 1979; L, 1984;
C & N, 1984).
Spider mites are important generalist herbivores
and many authors have studied the effects of induced
resistance on their populations (MM, 1970;
K & C, 1984; K, 1988; S
and D, 1989, E-L & K, 1988,
1991; K & N, 1995). This mechanism has
been intensively studied in cotton plants, the population of Tetranychus urticae Koch being reduced in
1. Centro de Estudios Parasitológicos y de Vectores (UNLP-CONICET), 2 No 584 (1900), La Plata, Argentina.
Acarologia, 2003. XLIII, 1 : 59-65.
— 60 —
plants that had previously been damaged by mites
(K & C, 1984; H & K,
1986; K, 1987; B & K, 1989). Mite
population increase was inversely related to the levels
of initial damage and there was no evidence of a
damage threshold.
On strawberry, there is evidence of induced resistance (S & D, 1989) and induced susceptibility (K, 1888). However, the existence of
a damage threshold that should be exceeded to produce both responses, and the relationship between
the strength of the responses and the initial level of
herbivory, are still unknown.
In this paper we report the effects of different levels
of initial damage on subsequent populations of T.
urticae in two strawberry cultivars.
Materials and methods
Two experiments were performed in a greenhouse
with no supplement of heat or light at any time. The
mean maximum and minimum temperatures were
35.10 fi 10 and 10.70 fi 3.40; 36.90 fi 4.50 and 12.40
fi 2.30 °C, in experiment 1 and 2, respectively. The
mean maximum and minimum relative humidities
were 89.16 fi 6.43 and 29 fi 7.74; 89.08 fi 15.99 and
42.83 fi 13.74, in experiment 1 and 2, respectively.
Approximately sixty days before the beginning of
each experiment, ‘Selva’ and ‘Milsei Tudla’ strawberry runner plants (Fragaria x ananassa Duchesne)
were planted in 15-cm plastic pots. Plants were kept
free of mites through daily inspection with a hand
lens. Eggs or active mites were removed with the help
of a fine camel’s—hair brush. Adult T. urticae females used in the experiments were taken from a colony
maintained on both cultivars. The experiments were
performed on ‘Selva’ and ‘Milsei Tudla’ plants with
similar number of leaves (≈12 leaves).
Experiment 1: On 17 July, ‘Selva’ plants were infested (first infestation) with 5 and 10 female mites
(5 replicates per treatment), while 8 control plants
F. 1: Total number of mites, eggs, immatures and adult females of
T. urticae per leaf, in previously damaged strawberry plants by
T1: 622.50, T2: 2458.75 active mite-days and C: undamaged
control.
— 61 —
received no mites. Treatments and replicates were
randomly interspersed on the floor of the greenhouse. Immature (larval instar and first and second
nymphal instar) and adult mite were recorded by
examining each leaflet with a pocket lens of 10X
magnification at 7 day intervals for 21 days. The mean
density per plant was estimated and mite-days were
calculated by the trapezoidal method (C, 1993)
to assess the intensity of initial damage. After that, all
the leaves were washed with a piece of wet cotton and
brushed to remove the mites. Then, the plants were
allowed to grow free of mites for approximately 15
days. One new and completely expanded leaf of each
plant was excised at the base of the petiole with a
razor blade. The petiole was placed in water into a
plastic tube (height 7 cm, diameter 2 cm). B and
K (1989) suggest that mites placed on excised
leaves may provide a reliable bioassay for leaf quality
since they found that the effects of excising the cotton
leaves did not negate the effect caused by previous
damage. Each leaf was inspectioned under binocular
lens to make sure that it had neither eggs nor activemites and was infested with 10 female mites (second
infestation). Treatments and replicates were placed at
random on a table in the centre of the greenhouse.
Female mites were chosen at random from the colony
so the effect of age on fecundity would be randomised. The total number of mites: eggs, immatures
and female adults, were counted on each leaf at 3-5
day intervals while the leaf was turgescent (19 days).
To compare the total number of mites between treatments at each census during the second infestation, a
Kruskal-Wallis test was conducted since the variances were not homogeneous, and a Mann-Whitney U
test for each pair of treatments was computed.
Experiment 2: On 27 August, ‘Milsei Tudla’ plants
were infested (first infestation) with 10, 15 and 30
female mites (7-9 replicates per treatment), while 7
control plants received no mites. Mite counts were
made at 4-7 day intervals for 24 days and active
mite-days was calculated. After that, all the mites
were removed and plants were maintained, by perio-
F. 2: Total number of mites, eggs, immatures and adult females of
T. urticae per plant, in previously damaged strawberry plants by
T1: 1157.80, T2: 2339.15, T3: 4101.2 active mite-days and C:
undamaged control.
— 62 —
dic inspection, free of mites for approximately
15 days. Ten female mites (second infestation)
were placed on the leaves of the entire plant. Mite
counts were made by examining each leaflet with a
pocket lens of 10X magnification at 7 day intervals
for 21 days. At the first and second infestations, treatments and replicates were randomly interspersed.
Two-way ANOVA (with treatment and time as main
effects) was used to test for significant differences
in the total number of mites during the second
infestation.
In both experiments the stage specific survival rates
and the duration of stages (eggs and immatures) were
estimated by a method for analysing stage-frequency
data (M, 1985). An estimation of the fecundity
was obtained by the ratio egg-days/female-days.
ANOVA was used for statistical testing of treatment
effects. Tests for homogeneity of variances were
conducted on all data sets before ANOVA. Only
data of ratio egg-days/female-days in experiment
1 did not satisfy variance homogeneity and were
log transformed before analysis. Means were compa-
red by Tukey test and the significance level was set at
P< 0.05.
R
ANOVA results for the effect of different levels of
initial damage on subsequent populations of T. urticae and on survival and duration of the stages of both
experiments, are summarised in T 1.
Experiment 1: In the second infestation the total
number of mites, which includes the individuals of all
the developmental stages, differed among treatments
(H = 7.895, df = 2, P = 0.019) only at 14 days after the
beginning of the infestation, and was higher in treatment 2 than in the control (Z = 2.867, P = 0.004)
(Fig.1 A). The number of eggs and immatures also
differed at this date and was higher in treatment 2
than in the control (F. 1 B and C). Survival and
duration of egg and immature stages (T 2) were
unaffected by previous damage. The ratio eggdays/female-days was higher in treatments 1 and 2
than in the control (P < 0.05).
Eperiment 1
‘Selva’
Dependent variable
Experiment 2
‘Milsei Tudla’
Source of variation
F
df
P
F
df
P
Total number of mites
Treatment
Date
Interaction
-
-
-
0.215
71.432
0.358
3, 108
3, 108
9, 108
0.886
0.000
0.952
Eggs
Treatment
Date
Interaction
5.103
6.172
3.492
2, 80
4, 80
8, 80
0.008
0.000
0.002
0.012
45.173
0.076
3, 108
3, 108
9, 108
0.998
0.000
0.999
Immature
Treatment
Date
Interaction
5.257
107.362
4.979
2, 80
4, 80
8, 80
0.007
0.000
0.000
0.933
105.542
1.107
3, 108
3, 108
9, 108
0.427
0.000
0.364
Female
Treatment
Date
Interaction
1.190
22.530
0.774
2, 80
4, 80
8, 80
0.309
0.000
0.626
0.337
52.344
0.565
3, 108
3, 108
9, 108
0.799
0.000
0.823
Egg Survival
Immature Survival
Treatment
Treatment
0.025
0.244
2, 15
2, 80
0.975
0.786
1.328
0.705
3, 27
3, 27
0.287
0.557
Egg Duration
Immature Duration
Treatment
Treatment
0.829
2.521
2, 15
2, 15
0.456
0.114
1.235
0.445
3, 27
3, 27
0.316
0.723
Egg-days/Female-days
Treatment
7.474
2, 15
0.006
0.171
3, 27
0.915
T 1: ANOVA results for the effect of different levels of initial damage on subsequent populations of T. urticae in ‘Selva’ and ‘Milsei Tudla’
strawberry.
— 63 —
Survival
Duration of stage
Egg
Treatment
Immature
Mean fi SD
Egg
Immature
Mean fi SD
N
Experiment 1
622.50 mite-days/plants
2458.75 mite-days/plants
Control
0.704 fi 0.152
0.687 fi 0.147
0.705 fi 0.147
0.498 fi 0.246
0.574 fi 0.220
0.478 fi 0.255
6.800 fi 1.608
7.704 fi 2.239
6.046 fi 2.579
13.724 fi 1.308
12.254 fi 0.779
14.106 fi 1.825
5
5
8
Experiment 2
1157.80 mite-days/plants
2339.15 mite-days/plants
4101.20 mite-days/plants
Controls
0.944 fi 0.020
0.946 fi 0.022
0.957 fi 0.015
0.962 fi 0.012
0.964 fi 0.020
0.953 fi 0.022
0.962 fi 0.022
0.971 fi 0.016
6.190 fi1.350
6.172 fi 1.741
5.484 fi1.095
5.047 fi 1.117
5.160 fi 2.071
5.015 fi 1.501
4.704 fi 1.901
3.804 fi 1.585
8
9
7
7
T 2: Survival and duration of egg and immature stages of T. urticae on previously damaged strawberry plant and control without damage.
Experiment 2: In the second infestation the total
number of mites (F. 2A), the number of eggs (F.
2B), the number of individuals of the immature stage
(F. 2C) and the number of adult females (F. 2D),
did not differ among treatments at each census date.
Survival and duration of egg and immature stages
were unaffected by previous damage. The ratio eggdays/female-days was similar between treatments
(T 2).
The mean time of one generation was approximately 19 and 14 days in experiment 1 and 2, respectively
(F. 1D and 2D). Survival of eggs and immatures
was lower in experiment 1 than in experiment 2.
While the duration of the egg stage was very similar in
the two experiments, the duration of the immature
stage was much shorter in experiment 2 (T 2).
D
The results of our experiments indicate that the
different levels of initial damage assayed did not
reduce subsequent populations of T. urticae. On the
contrary, in ‘Selva’ cultivar, T. urticae populations
were higher on leaves from plants previously exposed
to the highest level of damage (2458.75 mitedays/plants). These findings suggest a) inducible susceptibility in this cultivar and b) a threshold level that
should be exceeded for this inducible susceptibility.
The stage specific survival rates and the duration of
stages were unaffected by previous damage while the
number of eggs and immatures, and the egg-days/
female-days ratio was higher in previously damaged
‘Selva’ strawberry plants. The demographic pattern
reported in this study suggests that induced susceptibility in this cultivar against T. urticae was primarily
due to differences in fecundity. The discovering that
plant conditioning primarily affects fecundity, not
survivorship or development rate, has been reported
by several studies on induced resistance (H et al., 1986; B & K, 1989).
The two independent experiments carried out in
this study differed in methodology and cultivar.
Moreover, temperatures and humidity also differed.
Variations of temperature, humidity and photoperiod affect T. urticae developmental time and survival
(H and S, 1985). In experiment 1 the number of eggs and immatures per leaf from day 14 to 19
decreased. Although the excised leaves in this experiment kept turgescent until day 19, a lost of nutritional
quality could not be discarded as a posible reason of
the abundance decrease.
The observed differences in the mean time of one
generation, survival of eggs and immatures as well as
the duration of immature stages between experiments, could be attributed to the reasons cited above.
The induced susceptibility that was observed only in
‘Selva’ cultivar could be associated with constitutive
cultivar susceptibility. Kielkiewicz (1988) found that
no resistance was developed in susceptible strawberry
leaves, but previous mite infestations induced attractiveness of these leaves. Constitutive plant resistance
or susceptibility to mites has been poorly investigated
in strawberry (S & B, 1984), and have not
been studied in the ‘Selva’ and ‘Milsei Tudla’ cultivars at all.
— 64 —
Because plant responses to feeding show a high
degree of plasticity, it is necessary to study such
responses over a variety of environments to fully
characterise them (K & B, 1997). The
induced responses should ideally be measured over a
range of damage levels, representing a range of environments differing in herbivore loads (U,
2000). K (1987) noticed that the effect of induced cotton responses upon spider mite populations
was variable ranging from a four-fold reduction in
population growth to no reduction. Strength of this
phenomenon in cotton varied seasonally and was the
greatest when conditions were unfavourable for mite
growth.
Results of the present study and those of S
and D (1989) and K (1988), indicate
the variability in the response of strawberry plants to
the effect of previous mite feeding. Further research
is needed to provide a better understanding of these
mechanisms and of the effects that these responses
have on T. urticae.
A
We thank Susana Gamboa and Juan C. Zembo of
Facultad de Ciencias Agrarias y Forestales, Universidad Nacional de La Plata, for providing strawberry
runner plants, Mariela Theiller for technical assistance, and Gabriela Simonetto for improving the
English version of the manuscript.
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