Botanical Journal of the Linnean Society, 73: 187-216. With 11 figures
July/September/October 1976
The structure of the arthropod community on
bracken
J. H. LAWTON
Department of Biology, University of York,
York YO1 5DD
The species of herbivorous arthropods known to feed on bracken in Britain are listed and the
seasonal changes in the structure of this arthropod community are discussed.
CONTENTS
Introduction
. . . . . .
The herbivore community
. .
Seasonal changes in the community
Seasonal changes in the bracken
Discussion
. . . . . .
Acknowledgements
References
. . . . . .
Appendices
. . . . . .
. . .
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187
187
193
198
202
207
208
209
INTRODUCTION
Bracken is very common throughout the world, and the fact that it has a
reputation for being a particularly difficult plant for herbivores to exploit
makes it an unusually interesting species to study.
This paper examines the assemblage of herbivorous arthropods that feed on
the plant with particular reference to the British Isles. Firstly, it summarizes
the species of herbivorous arthropods known to feed on bracken in Britain, and
attempts to compare this with other plant species. Secondly, the seasonal
changes in the structure of the community are considered, both in terms of the
number of species involved and in terms of the abundance of herbivores per
frond. Finally, from these observations, certain suggestions about seasonal
changes in the plant’s defence-mechanisms against herbivores are made.
THE HERBIVORE COMMUNITY
An annotated list of the 40 or so species of herbivorous arthropods known
to be associated with bracken in the British Isles is provided in Appendix 1.
Table 1 provides a summary. Not all of these are equally common; the ‘key
species’ found on most areas of bracken (based on samples taken at over 50
187
]. H. LAWTON
188
Table 1. Summary of the numbers of species of herbivorous
arthropods within various taxonomic groups, feeding on
bracken in the British Isles. The data in the first column are
derived from Appendix 1, excluding species of very uncertain
status. Column two lists the more common 'key-species' (see
text) excluding the rhizome feeding hepialids
Group
Acari
Coleoptera
Collembola
Diptera
Hemiptera: Heteroptera
Hemiptera: Homoptera
Hymenoptera
Lepidoptera
Number of species
in each group
Approximate numbers
of 'key-species'
2
(1)
1
1
9
0
1
5
2
4
1
4
11
10
4-5
3-4
l: 40
18-20
sites throughout the British Isles) are as follows. (The number after each species
refers to its position in Appendix 1.)
Acari
Collembola
Diptera
Chamobates sp.
Bourletiella viridescens
Chirosia parvicornis
Chirosia hystricina
Dasyneura filicina
Dasyneura pteridicola
(39)
(2)
.(9)
(8)
(10)
(11)
Usually at least one other species
will also be present, most probably
or
or
Hemiptera
Hymenoptera
Phytoliromyza hilarella
Chirosia flavipennis
Chirosia albitarsis
Monalocoris filicis
Macrosiphum ptericolens
Philaenus spumarius
Criomorphus pteridis
Aneugmenus padi
Stromboceros delicatulus
Strongylogaster lineata
(3)
(7)
(5)
(13)
(15)
(16)
(17)
(20)
(22)
(23)
In addition, it is usual to find at
least one and often two of the
other possible species.
THE ARTHROPOD COMMUNITY ON BRACKEN
Lepidoptera
189
Paltodora cytisella
(30)
Pe trop hora chlorosa ta
(3 1)
Unidentified ‘Micro’.
(38)
In addition, it is usual to find at
least one of the other possible
species. (The rhizome-feeding
hepialids have not been considered,
because of the difficulties involved
in locating the larvae.)
It is clear that out of the complete list of 40 species, between 18 and 20
species of herbivorous arthropod occur commonly. However, it is unusual to
have more than 10 or 12 species present at any one time.
Using this information, we may enquire whether there is anything odd or
unusual about the herbivore community on bracken. Specifically:
(a) Is there anything unusual about the total number of species; is it, as is
popularly thought, small by comparison with the number of species of
arthropods associated with other higher plants?
(b) Alternatively, is there anything unusual about the distribution of species
amongst the various higher taxa (e.g. orders or suborders); is the composition
of the herbivore assemblage unusual irrespective of the number of species
involved?
The problem of finding a standard against which to compare bracken in
order to be able to attempt an answer to these two questions is by no means
easy. Two sorts of comparative data have been assembled. The first involved
checking the accounts for the numerous species of higher plants (excluding
trees) that have appeared in the Biological Flora, published in the Journal of
Ecology between 1948 (Vol. 36) and 1973 (Vol. 61). The accounts give details
of the arthropods associated with each as far as they were known at the time
when they were written, and for these purposes are probably as near as one can
get t o a ‘random sample’ of higher plants, although unfortunately many of the
lists give the impression of being very incomplete. The second approach
attempted to take account of this fact, and also the point that bracken is a very
common and widespread plant, occurring in just over 90% of all the 10-km
squares in the British Isles and in all the vice-counties (Perring & Walters, 1962).
Since abundance, both now and in the past, is positively correlated with the
number of herbivores associated with British trees (Southwood, 1961), the
same may well be true of other types of vegetation. Comparing bracken with a
range of species which differ widely in abundance, as above, may therefore give
a distorted impression of what to ‘expect’ on the plant. In consequence a
comparison was made between the herbivores on bracken, and those on all the
plants (again excluding trees) in the Atlas of the British Flora (Perring &
Walters, 1962) that are equally widespread at the present time (with the
obvious caveat that this takes no account of past abundance). The 43 species of
plant are listed with their authorities in Appendix 2; nine of them are also in
the Biological Flora list. A few of the species included in the analysis are absent
from the Highlands of Scotland (and so occur in fewer of the 10-km squares)
190
J. H. LAWTON
but are so widespread and common elsewhere that it seemed sensible to include
them. Information on selected insect groups associated with each of these
plants was obtained by consulting the standard reference works listed in the
Appendix. The main groups not dealt with in this analysis (because of problems
in obtaining reliable data) were the Diptera (with the exception of
Agromyzidae, which were considered), the Collembola, Acari and most groups
within the Homoptera.
The data obtained for the eight species of plant common to both analyses
are, somewhat discouragingly, rather different, and confirm that the Biological
Flora lists tend to underestimate numbers, in one case doing this to a very
serious degree. This highlights the difficulties involved in assembling data of
this kind and emphasizes the point that the conclusions to be drawn from the
analyses are, of necessity, rather general and imprecise.
The full list of 40 species of herbivores associated with bracken in Britain is
surprisingly large number for a plant that is generally supposed to be difficult
for animals to eat. Only five species in the Biological Flora lists (Plantago
lanceolata L., P. media L., Ranunculus repens L., Senecio jacobaea L. and
Urtica dioica L.) have either more or the same number of species recorded in
association with them, and the remaining 92 plants (that is approximately 95%
of them) have less, most of them substantially so (Fig. 1). Allowance should
obviously be made for the fact that bracken has been particularly well studied,
and that the Biological Flora accounts probably underestimate the true number
of herbivore species involved. However, considering only the 18-20 ‘key
species’ on bracken still gives it more herbivores than 74 of the 97 other plant
species. Clearly, compared with a random sample of higher plants (other than
trees), bracken does not have an unusually small or impoverished number of
species of herbivores associated with it; if anything the reverse may be true.
This conclusion is not altered by considering only the very common and
widely distributed plants dealt with in the second analysis. Bracken has 25
species of insect in the groups considered, all of which are listed in the standard
reference works consulted (Appendix 2), so that this is not a number inflated
by ‘sampling effort’ on my part. The same reference works provided the
information for Fig. 2, which shows that 20 plants have more species associated
with them than bracken (in the groups considered) and that 23 have less.
Again, it must be concluded that compared with a sample of over 40 equally
widespread, common species of plants, bracken does not have an unusually
small or impoverished number of insects associated with it.
If the total number of species involved is not unusual, the composition of
the assemblage decidedly is. If the to,tal numbers of species in each group on
each plant in the Biological Flora accounts are added up, we obtain some sort
of impression of an ‘average’ or ‘expected’ distribution of species amongst
the various higher taxa of herbivorous arthropods. This can then be compared
with the bracken community (Table 2). The observed distribution of species
amongst the various higher taxa departs very significantly from the ‘expected’
distribution, considering both the complete faunal list, and also the ‘key
species’ on bracken. In both instances, the Hymenoptera (and hence the
sawflies) make the single largest contribution to the values of x2 obtained. I t
would be unwise to assign an exact probability level to the value of x’for the
THE ARTHROPOD COMMUNITY ON BRACKEN
191
26
TOTAL INSECTS.
22
.....
11
"i3
I
14
is:
....
.!!I
"&
10
.iE
::0
z
6
2
0
Number of species of arthropod !mainly insects I associated with the plant
Figure 1. The total numbers of species of insects and mites associated with 97 species of higher
plants (excluding trees) for which adequate information is available in the Biological Flora. The
data for bracken, using the full faunal list given in Appendix 1, is shown for comparison. Only
five species of plant have more arthropod species recorded as being associated with them than
bracken.
43'COMMON'PLANTS
0
...'
t:
~
e:
~
t
~ t ~ : '
9
t
~
~
s
t
Numbers of insacl species(selected groups only) per plant
Figure 2. The numbers of species of insect (selected groups-see text for details) associated with
43 very common and widespread species of higher land-plants in Britain (the plant species and
insect groups examined are listed in Appendix 2). Bracken has 25 species of insects from these
groups associated with it.
J. H. LAWTON
192
Table 2. A comparison of the composition of the herbivore community on
bracken with a ‘standard’ derived by summing all the records from accounts
given in theBioZogicaZ Flora, excluding trees (see text for details). Minor groups
(e.g. Collembola) have been omitted from the analysis
Bracken
‘Key-species’
All records
Total Biological
Flora records
Group
Coleoptera
Diptera
Heteroptera
Homoptera
Hemiptera
Hymenoptera
Lepidoptera
146
162
44
152
196
43
359
Observed
‘expected’
Observed
1
9
2
4
5.96
6.62
1.79
6.21
0
-
-
1.75
14.66
4
5
4
3.89
0.85
7.13
5
-
-
11
10
P
2.90
3.22
25.5
see text
56.2
XZ
probability
‘expected’
< 0.001
‘key species’, because the ‘expected’ value for Hymenoptera in this case is
less than 1. This is likely to lead to errors in a xz analysis (Snedecor & Cochran,
1967: 235)’ but in the present case these are unlikely to be very serious,
because the nominal probability is P < 0.001.
This very simple analysis provides good evidence that bracken has a
disproportionately large number of sawfly-species associated with it. This is
borne out by the second analysis carried out on 43 common and widespread
plant species. Only one of these (Filipendulu) has more sawflies in total (12),
and none of them have as big a proportion of species in this group. Most of the
other taxa listed in Table 3 are fairly close to their ‘expected’ values, the only
other point of note being the complete absence of any species of Coleoptera in
the ‘key species’ group, and the fact that only one species is known to eat the
plant at all.
In view of the widely held notion that bracken is particularly difficult for
herbivores to exploit, the conclusions concerning the total numbers of species
Table 3 . A summary of the species listed in Appendix 1 in various
feeding categories
Number of species feeding
Groups
Coleoptera
Collembola
Diptera
Heteroptera
Homoptera
Hymenoptera
Lepidoptera
Acari
Totals
Only on
bracken
On bracken
and other
ferns
Many types of
higher plantsnot only ferns
0
0
1
0
0
4
2
1
7
0
5
0
1
1
3
1
11
1
0
0
0
2
3
6
0
14
13
No information
THE ARTHROPOD COMMUNITY ON BRACKEN
193
associated with it are surprising. It may well be that the unusual balance in the
composition of its herbivore community is related to its toxicity, but if this is
indeed so, the reasons for it are obscure.
A list of species gives no indication of seasonal variations in the structure of
the community; this is considered in the next section.
SEASON CHANGES IN THE COMMUNITY
The information in this section is based entirely on samples taken from a
study on Skipwith Common, which lies 15 km to the south of the City of York
(SE 657377), some 10 m above sea-level. The site is a small level area, roughly
0.3 ha in extent, surrounded on three-sides by woodland; the area itself is
completely open and entirely dominated by bracken, with no other vegetation.
Samples were taken regularly during 1972 and 1974 but only very
infrequently during 197 3 . Sampling was carried out by carefully separating and
cutting off individual fronds at ground-level over a white sheet, and by rapidly
placing them in a position where the active animals were unable to escape (in
alcohol, in a large polythene bag or in a steep-sided tray, depending on the size
of the frond and the season). The areas to be sampled were selected at random
on the study area, and fronds picked haphazardly within each area. Sampling
was carried out from the emergence of the young croziers in May, until the first
frosts browned the bracken at the end of the season. On each sampling
occasion, not less than 20, normally approximately 50, and at times up to 230
fronds were examined. In the case of the gall-forming or mining Diptera and
Lepidoptera representative samples of the galls or mines were dissected to
check for the presence of living larvae and for parasites. N o attempt was made
to sample the rhizomes.
Figure 3 suggests that a sample of 20 randomly selected fronds will normally
be sufficient to establish the presence or absence of most of the herbivore
species in the stand at any one time, the cumulative-frequency curve becoming
asymptotic from 16 fronds onwards. Only very rarely did general collecting in
the area by sweep-netting or by examining ‘interesting-looking’ (rather than
randomly-selected) fronds turn up a ‘new species’ not revealed by the routine
samples.
....*----...
10
-
16-17AUG. 1972
9,
I
5
10
I
15
15
CUMULATIVE FRONDS SEARCHED
20
20
1
I
a5
a5
Figure 3. The cumulative number of species of herbivores found o n bracken with increasing
numbers of fronds searched (Skipwith Common, Yorkshire, August 1972).
J. H. LAWTON
194
2-
r
M
W
LT
2e
0
Figure 4. A. The total numbers of herbivore species on bracken at Skipwith Common,
Yorkshire, between May (when the fronds first emerge) and the end of September (when they
‘brown’ in the first frosts). Data for three consecutive years are shown; the curve was fitted by
eye.
B. Changes in the Brillouin Index of species-diversity ( H ) with season for the herbivore guild on
bracken at Skipwith Common, Yorkshire.
The data obtained in this way provided information on three aspects of the
community-namely the total number of herbivore species present at any one
time (‘species number’ or ‘species density’), the number of species relative to
the number of individuals of all species (‘species diversity’ sensu-stricto), and
the mean abundance of each species. The standard Brillouin measure of the
species diversity of the samples was used (Pielou, 1966).
Data from all three years’ samples have been used to build up a picture of the
changes in species-number and species-diversity with season. Because it is
obviously not sensible to combine several years’ population counts, however,
THE ARTHROPOD COMMUNITY O N BRACKEN
195
only the data for 1972 have been used to examine changes in speciesabundance (with one exception-see Fig. 5). The data in this case are presented
simply as the mean number of individuals per ten fronds sampled, with no
attempt to put confidence intervals on these estimates.
Figure 4 show that both the total number of species (Fig. 4A) and species
diversity ( H ) (Fig. 4B) tend to increase with season, from very low values in
May and early June to a maximum in late August. Species diversity ( H ) , but
not the total number of species, tends t o fall again during September. This
decrease in H during September is almost entirely due to a substantial increase
in the numbers of the aphid Macrosiphum (see below), which markedly reduces
the ‘evenness’ or ‘equitability’ component of the index, without any change in
the total number of species; H therefore falls. It is clear from Fig. 4 that all
three years follow the same general pattern.
Changes in the abundance of each species are more complex. Figure 5A-D
summarizes the information for 1972. One of the most important things to
note is that the total number of individuals of all species (Fig. 5D) again tends
to increase with season in much the same manner as the total number of kinds
of species and species-diversity.
The data for individual species or groups of species, which contribute to this
overall picture may be summarized briefly as follows. Paltodora caterpillars
(Fig. 5A) occur for only a very restricted period at the start of the season; their
growth is rapid and well synchronized, and they show a remarkably ‘standard’
exponentially decaying survivorship curve; by mid-June all the mines are
empty. The early fronds are also colonized by adult Monalocoris (Fig. 5A)
which have overwintered as adults and which oviposite and then die. By
mid-July the young instars of Monalocoris appear and grow rapidly; survival
then appears to be fairly good during August and September, prior to the new
generation of adults overwintering. Criomorphus (Fig. SC), in contrast,
overwinters as half-grown nymphs, and for a brief period in late May these may
be extremely abundant. The new generation builds up in numbers from August
onwards, contributing significantly to the total increase in the abundance of
herbivores at this time.
The aphid (Macrosiphum), as expected, shows no clear separation of
life-history stages by season. Numbers of both nymphs and adults tend to be
reasonably high in the early spring (Fig. 5C) and then fluctuate markedly; only
one was found on over 200 fronds, for example, after very heavy rain in
mid-July. A substantial increase occurs in the autumn, with numbers rising to
over 100 per ten fronds, when it is by far the commonest species present. The
small collembolan BourZetieZZa (Fig. 5B) also has no clear separation of instars
with season. Numbers build up quickly in the spring and then fluctuate very
little during the rest of the season.
Sawfly caterpillars, present taxonomic problems. It is clear, however, from
Fig. 5A that they become comparatively abundant only from late July
onwards. The rather extended total season appears to be due both to a
succession of species, each with a rather different mean oviposition date, and
the long adult-flying season of some of the more common species like
Aneugmenus padi and Strongylogaster lineata.
Like the sawflies, the gall-forming and mining Diptera (Fig. 5B) build up in
numbers only during July and August; by September virtually all the mines or
J. H. LAWTON
196
loor
"I
D
1m
I
Figure. 5. Seasonal changes in abundance of selected species of herbivores or groups of
herbivores on bracken at Skipwith Common, Yorkshire. All data refer to 1972, with the
exception of the bracketed points for Monalocoris (A) and Macrosiphum (C), which are for
1974.
197
THE ARTHROPOD COMMUNITY ON BRACKEN
galls are empty. Again, as in the sawflies, oviposition and hatching in these
Diptera appear to be over sufficiently long periods of time to obscure the
patterns of larval survival. Figure 5B shows the combined numbers of both
Dasyneura species. On the Skipwith study area filicina is the most abundant
species with pteridicola present in insignificant numbers by comparison. If
anything, pteridicola tends to occur slightly later in the season than filicina.
It is obviously too early in the study to form any clear ideas about
population control in any of these species, although a number of points are
already obvious. Figure 6 shows the relationship between the number of
bracken fronds per 0.25 m 2 and the numbers of Criomorphus nymphs and
adults in the same 0.25 m2 area, at Skipwith on one day in mid-June. Overall
population density per unit area in this species is obviously dependent on frond
density, so that despite an apparent super-abundance of food, Criomorphus
shows clear evidence of resource limitation. It is not at all clear why there
should be such a low limit on the number of Criomorphus per frond at this time.
Data are also accumulating on the predators and parasites of each of the main
12
n
10
.
E
"'
6
jj
4
z
3
g
Y=0·58X+0-72
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•
•
•
•
•
•
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•
•
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CRIOMORPHUS 13th June 1972.
•
•
•
•
•
•
• •
• ••
10
11
12
13
14
Numbar of fronds par 0·25m 2
Figure 6. The relationship between the number of Criomorphus per 0.25 m 2 and the number of
bracken fronds in the same area, on one day in June 1972 on the Skipwith Common study area.
herbivore species: levels of predation and parasitism on all the key-species that
have been examined to date appear to be high, but without further work to
'breed out' some of these parasites, further comments are impossible. The
general level of parasite attack, however, suggests that in several species they
are likely to play a major part in population control.
We may summarize the main conclusion of this section as follows. Both the
total number of species of herbivores and species diversity tend to increase with
season on bracken, being lowest in May and highest in August or September.
Similarly, the total number of animals, considering all herbivores together,
reaches a maximum towards the end of the season. Only one species (Paltodora
sp.) attains its maximum numbers on the plant in the early spring. With few
exceptions, the majority of herbivore species individually show their maximum
abundance after, rather than before, mid-July. The evidence strongly suggests
that bracken in May and June may not be an easy resource for herbivores to
exploit.
14
J. H. LAWTON
198
SEASONAL CHANGES IN THE BRACKEN
Seasonal changes in the levels of several constituents of bracken have been
well documented, either in attempts to find uses for what is essentially a useless
weed, or in attempts to understand why it is so poisonous to stock.
Conveniently, several are also known to play an important part in determining
either the quality or toxicity of the plant from the point of view of a
herbivorous arthropod. The following substances or concentrations are most
relevant to the present discussion: protein (Ferguson & Armitage, 1944;
Hunter, 1953; Moon & Pal, 1949; Shearer, 1945; Smith & Fenton, 1944);
lignins and tannins (Ferguson & Armitage, 1944; Moon & Pal, 1949); silicate
(Ferguson & Armitage, 1944; Moon & Pal, 1949); cyanide (Moon & Raafat,
1951); and thiaminase levels (W. C. Evans, 1976).
May
June
July
Aug.
Sepl.
Ocl.
No!.
Figure 7. Crude-protein levels in bracken during the growing season, derived from published
accounts in the literature. The sources of information are listed in the text.
Figure 7 summarizes the available data on changes in protein levels either in
the whole above-ground parts of the plant or in the ‘stem’ (petiole and rachis)
and ‘leaves’ (presumably the primary pinnae) separately. The data are from
widely separate localities (near Edinburgh, Perthshire, Galashiels, Berkshire and
Suffolk), so there is no reason to doubt the generality of the relationship. The
protein content of bracken falls steadily throughout the season. The data all
refer to percent ‘crude protein’; and although not always stated by the authors,
in general this appears to have been obtained by the standard conversion
‘percent N x 6.25’ (Golterman, 1969). (In the case of Hunter’s data, this
conversion was actually carried out on the figures for Nlevels given in his
Table 1.) Whilst modern analytical techniques may be able to make some
improvement on these figures, the other inescapable conclusion from Fig. 7 is
that, except in early spring (May), the protein content in bracken is rather low,
and by August and September it is unlikely to be in excess of 1 5 % on a
10
-
T
A
M
8 After Moon and Pd(19491
3.-D 2 Lr 6 L
.
l
-
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isQ 4 / O / O
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0
May
I
June
0
A
-
1
O
0
0
-
I
I
July
Aug.
-----+?em’
Sept.
I
Ocl.
Nov.
Figure 8. Changes in lignin and tannin levels in bracken during the growing season, derived from
published accounts in the literature. The sources of information are listed in the text.
dry-weight basis. By ‘normal’ standards, therefore (e.g. Feeney, 1970;
Southwood, 1973), bracken-feeding herbivores face a progressive deterioration
in ‘food quality’ throughout the season.
Precisely the same conclusions may be drawn from an examination of lignin,
tannin and silicate levels (Figs 8 and 9), all of which tend to increase
throughout most of the season, and all of which might be expected to make the
plant progressively tougher, more difficult to eat or more difficult to digest.
Chemical analysis of ‘lignins’ and ‘tannins’ is generally acknowledged to be
rather difficult, so that the precise levels of these compounds shown in Fig. 8
may not be exact. The seasonal trends, however, are clear.
In the face of what may be interpreted as a progressive deterioration in
certain of the standard components of ‘food quality’ in the plant, the
concomitant increase shown by the grazing arthropods in species number,
species diversity and species abundance is unexpected. A sensible working
J. H. LAWTON
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hypothesis would be that an additional compound or compounds, the effects
of which are sufficiently great to over-ride the changes in ‘food quality’
outlined above, must decrease during the season. Two compounds, at the
present time, are known to show this behaviour, namely the cyanide content of
the plant (Fig. 10, after Moon & Raafat, 1951) and thiaminase levels (Fig. 1,
W. C. Evans, 1976). Total HCN levels fall progressively with season, from levels
as high as 28.7 and 34.1 mg. HCN per 100 g dry matter to effectively zero by
May
Juna
Julv
Aug.
Sapl.
OcI:
Figure 10. Cyanide levels (as total HCN) in bracken during one growing season calculated and
plotted from data given by Moon & Raafat (1951). The curve is fitted by eye.
THE ARTHROPOD COMMUNITY ON BRACKEN
20 1
late September. The relationship between these HCN levels, and the mean
number of herbivore species present at the same dates on the Skipwith study
area is shown in Fig. 11. This certainly suggests that HCN levels may influence
the numbers of species able to feed on bracken, in a manner that over-rides the
seasonal deterioration in other components of the diet. Also note, however,
that a very similar relationship would be obtained using the thiaminase levels,
shown on page 119, which is perhaps fortunate, because it is now apparent that
the cyanide in bracken may not always be ‘available’ as a defensive compound.
Cyanide production in plants is usually (though by no means invariably)
controlled by the action of /3-glucosidase enzyme or enzymes on a cyanogenic
glucoside (Jones, 1972, 1973); bracken appears to be typical, and contains the
glucoside prunasin (Berti & Bottari, 1968; R. Eyjolfsson, in Swain &
Cooper-Driver, 1973). When the cells of a plant containing both enzyme and
glucoside are damaged, by either a herbivore or an experimenter, the enzyme
I)
c
*-
ng HCN per lOOu 1drywt.l 01 bracken.
Figure 11. Cyanide levels in bracken (as Fig. lo), plotted against the mean number of species of
herbivores read from the curve shown in Fig 4A.
acts on the glucoside to produce HCN. It is now know that several species of
plant (e.g. Lotus corniculatus L.) are polymorphic, some individuals containing
neither the enzyme nor the glucoside, and some only the enzyme. Obviously
these plants are never cyanogenic. Others, however contain the glucoside but
no enzyme, and still others have both. Work on bracken collected from
different sites within ten miles of the city of York (and by Cooper-Driver,
1976) shows that this plant, too, is polymorphic, and that only some stands
have both enzyme and glucoside. The plants in one area, however, all tend to
be the same. Bracken from the Skipwith study area has the glucoside, but no
enzyme, which immediately casts doubt on the significance of the relationship
shown in Fig. 11, because analysis for total HCN content of a plant, along the
lines carried out by Moon & Rafaat, will not distinguish between plants
containing glucoside but no enzyme and plants with both. This is because
experimental digestion of the glucoside with conc. HC1 brings about a release of
HCN from the glucoside in much the same manner as when it is acted on by the
enzyme, At the moment, it is a mute point whether having the glucoside but
not the enzyme offers any potential for protection to a plant againt grazing by
J. H . LAWTON
202
a herbivore (T. J. Crawford-Sidebotham, pers. comm.). In general, one might
expect that cyanide will not be released by such a plant, although it is possible
that some cyanide may still be produced by acids during digestion. Obviously
this problem requires considerably more investigation before it is possible to
say what role, if any, the cyanide content of bracken plays in determining the
composition and abundance of the grazing arthropod community associated
with it.
Because of these uncertainties about the ‘availability’ of cyanide in the plant,
the parallel changes in thiaminase levels are fortunate. The use of a thiaminase
as a defensive compound is considerably less familiar than the use of cyanide,
and the reasons for thinking that it may act in this way must briefly be
summarized. The plant’s thiaminase activity is discussed in detail by W. C.
Evans (1976); Braid (1959) reviews the early literature. Since all seven of the
main B vitamins, including vitamin B1 (thiamine), are absolutely essential for
normal insect development (Dadd, 1973) the presence of very active specific
compounds that could prevent vitamin B1 utilization appears to present serious
problems for a herbivorous arthropod (note that bracken certainly contains
vitamin B1 -Berti & Bottari, 1968). Further, anti-thiamine activity would
appear to be rare in the plant kingdom; it does occur in most other
pteridophytes but in virtually none of a wide variety of angiosperms that have
been examined (Kenten, 1956. Fujita, in Kenten, 1957). The problem may
therefore be a very unusual one for herbivorous arthropods to deal with.
In addition to cyanide, therefore, high levels of thaiminase in the Spring
provide a very good basis for thinking that the plant will be particularly toxic
at this time. Presumably, if the plant has ‘functional’ cyanide it will be even
more toxic. It is not surprising that a consideration of ‘food quality’ changes
alone are insufficient to account for the observed seasonal dynamics of the
arthropod community on bracken.
DISCUSSION
Cyanide, thiaminase and changes in food quality are not the only possible
defence mechanisms possessed by the plant, and it would seem desirable, at this
stage, to review all its known, potential anti-herbivore devices; this is done first
as an unqualified list of the possible (rather than probable) mechanisms,
followed by a discussion of the evidence in support of each, where this has not
already been assembled, and some of the consequences which develop logically
as we consider them. There are at least eight possible types of defence
mechanisms, falling roughly into three categories as follows:
<Foodquality’
(a)
(b)
Protein levels
Amino-acid composition
Specific toxins
(c)
(d)
(e)
(f)
(g)
Cyanide
Ecdysones
Phenols, lignins and tannins
Thiaminase
Carcinogens and other miscellaneous compounds
THE ARTHROPOD COMMUNITY ON BRACKEN
203
The “Set a thief to catch a thief” principle
(h)
Ants
The crude-protein analyses already dealt with suggest that the arthropods
feeding or attempting to feed on bracken face difficult nutritional problems,
because during most of the summer the quantity of protein in the pinnae is
considerably below that usually regarded as optimal for many insects
(Southwood, 1973). Obviously, the value of a diet for growth, development
and reproduction depends not only on the total amount of protein, but also on
the relative proportions of each of the constituent amino-acids. Bracken may
also have an unusual amino-acid composition (Berti & Bottari, 1968; Smith &
Agiza, 195 l), although the evidence here should be viewed with caution (W. C.
Evans, pers. comm.). It may be, however, that the ‘balance’ of amino-acids is
an additional problem facing a herbivore which feeds or attempts to feed on
the plant.
The declining ‘quality’ of the bracken during the growing season is
aggravated by rising tannin lignin and silicate levels (Figs 8 and 9). The
similarity between bracken fronds and the leaves of oak-trees (Feeney, 1970) in
this respect is striking; and for many of the same reasons that were discussed by
Feeney it may not be coincidence that, instead of just chewing or biting the
entire pinnae, a large part of the herbivore guild on bracken are miners,
gall-formers or sucking hemiptera-strategies which may be able to exploit parts
of the plant of above average ‘food-quality’. The sawflies are an obvious and
important exception. Unlike the Lepidoptera on oak (which feed in exactly the
same way, but have their maximum abundance and diversity early in the
spring), bracken sawflies reach their maximum abundance and diversity late in
the season, when the fronds are simultaneously high in tannin and low in
protein. It is interesting t o speculate whether the unusually large proportion of
species in this group feeding on bracken is in any way linked with their longer
evolutionary history compared with that of Lepidoptera. On the other hand, if
this is the case, the apparent inability of the British sawfly-species to exploit
the plant earlier in the season is puzzling, in view of the fact that at least one
closely related, common, North American species (Strongyloguster multicinctus
Norton) does so successfully (Hogh, 1966). For some reason, sawflies may be
unusually sensitive to high cyanide levels, thiaminase levels, or both, but not to
high tannin levels.
In contrast to the sawflies, the three common Lepidoptera on the plant show
very different behaviour, reinforcing the view that it is high tannins and low
proteins that present problems for this group. In Yorkshire, Petrophoru
chlorosutu occurs in June and July before ‘food quality’ has declined too far
and before the maximum abundance of sawflies. On the other hand, it occurs
after both cyanide and thiaminase levels have declined from their initial high
concentrations. If the former is ‘available’ and the latter really is toxic, the two
other Lepidoptera (Pultodoru and the unidentified ‘micro.’), which occur even
earlier in the year, have presumably had to evolve means of detoxifying or
avoiding their effects. That the enzyme rhodanese (Jones, 1973; Parsons &
Rothschild, 1964) detoxifies cyanide is one such possibility.
Other spring species may avoid the potentially toxic effects of cyanide by
the manner in which they feed. Thus three characteristic early-spring species
204
J. H. LAWTON
(Criomorphus, Macrosiphum and Monalocoris) are all Hemiptera, and therefore
possibly able to feed from the plant without crushing the tissue and releasing
HCN. On the other hand, if cyanide does serve to prevent ‘true’ grazers (rather
than sucking insects) from exploiting bracken, the fact that levels tend to
decline quickly after the early part of the season would seem to reduce its
usefulness to the plant considerably from this point of view. It is interesting to
note, however, that there is also a fall in cyanide levels in older leaves, coupled
with a parallel increase in tannin levels, in the North American shrub
Heteromeles (Dement & Mooney, 1974). There may be physiological constraints on the plant which make it unprofitable to maintain high levels of both
types of defensive compound at the same time. Alternatively, switching
strategies in this way could also make things much more difficult for the
herbivores.
Until more is known of the location of the thiaminase in the plant’s tissues,
the ways in which chewing and sucking herbivores respectively avoid its effects
must remain problematic.
Ecdysones and related sterols that are analogous to insect moulting
hormones have now been found in a wide range of plant species (Rees, 1971;
Swain & Cooper-Driver, 1973), of which bracken was one of the first (Kaplanis,
Thompson, Robins & Bryce, 1967); it is now known to contain at least five
such compounds, of which a-ecdysone and 20 hydroxyecdysone are the most
important (Kaplanis et aZ., 1967; Berkoff, 1969; Cooper-Driver, 1976).
Probably because they have no clearly defined role to play in the growth of the
plant (R. D. Firn, pers. comm.), it has been tempting to assign to these
phytoecdysones a defensive role against herbivores, presumably by interfering
with the insect’s growth and development. Unfortunately, the experimental
evidence that ecdysones do have a defensive role to play against herbivorous
arthropods is shaky. The fact that a number of species normally feed on
bracken is certainly not evidence that these compounds do not have a defensive
role to play (and this is obviously also true for example of the other
compounds like thiaminase and cyanide). All that this proves is that in the
evolutionary ‘race’ between the plant and its herbivores, certain herbivores will
apparently find ways round almost anything that the plant can produce-given
time. The question of what proportion of the herbivore species are restricted
to the one food plant or type of plant and what proportion are ‘generalists’ is
obviously very relevant here, and will be returned to later. The role of these
‘defence mechanisms’ may well be to prevent most herbivores from exploiting
the plant; and the more that cannot, the better from the plant’s point of view.
Locusts (Schistocerca gregariu (Forskal)) fed air-dried, remoistened bracken,
which was collected in the autumn and contained appreciable quantities of
ecdysones, developed rather slowly but more or less normally (Carlisle & Ellis,
1968), which suggests, at first sight, that ecdysones are not an important
defence mechanism. (Interestingly, although this experiment was actually
designed to examine the defensive role of ecdysones against non-specialist
herbivores, it could also be used to question the defensive role of thiaminase as
well. Conveniently, the fact that thiaminase levels are now known to decline
markedly with season appears to remove this difficulty. Thiaminase activity is
also depressed by air drying (Haag & Weswig, 1948)).
Unpublished work (Lawton, in prep.) with Schistocerca confirms Carlisle &
THE ARTHROPOD COMMUNITY ON BRACKEN
205
Ellis’s results with air-dried bracken collected in September. Fresh bracken
collected from Skipworth Common in the Spring and fed to both adult and
young locusts produced quite different results. They died, after first refusing to
eat the plant from about the second or third day of the experiment, although
initially they would feed on it (see also Cooper-Driver, 1976: 40-2).At the
moment it is not known what comDonent or components are responsible for
this dramatic difference between fresh spring bracken and the autumn, air-dried
plant. Cyanide is one obvious possibility and thiaminase another. It confirms
the fact that spring bracken is a particularly nasty thing for herbovorous insects
to eat, despite its superficial appearance of being a ‘high-quality’ food resource.
In many ways, however, experiments of this type are very crude. Locusts are
very unusual herbivores in that they are naturally ‘super-generalists’, with the
ability to feed successfully on a very wide range of plant species; in fact this is
one of the things that makes them so useful for this type of experiment. But
because they are ‘super-generalists’ their capacity to cope with and to
detoxify plant toxins may be unusually high, so that negative results with
locusts are not very helpful. Feeding experiments involving the whole plant,
with the attendant problem of assigning effects to specific compounds, also
leave much to be desired. The obvious alternative approach is to use artificial
diets (for a particularly good example see Rehr, Feeney & Janzen, 1973) with
the required toxins, or suspected toxins, added. This has been done by Robbins
et al. (1968) with five species of insect and a range of ecdysones and ecdysone
analogues. The five species tested differed markedly in their responses to the
same compound and to subtly different compounds, whilst the effects on
immature stages were often very different from the effects on the maturation
and development of ovaries in adult females. Thus 20-hydroxyecdyson (one of
the principle constituents of bracken) was one of the least active constituents
when tested on immature stages, but it had a marked effect on egg production
in adult houseflies. Without testing each of the major ecdysone types found in
the plant in this way, preferably with a sensible range of herbivorous insects
that are likely to encounter it in the field, it is impossible to say anything
further about the role of ecdysones in the defence of the plant against grazing
arthropods, except that a positive role is still a possibility.
The remaining possible chemical defence-mechanisms of the plant may be
dealt with briefly in passing, because their effects on arthropods are unknown.
They include a range of the simpler phenolics or their precursors (Gliessman &
Muller, 1972; Swain & Cooper-Driver, 1973; Cooper-Driver, 1976) that have
been tentatively assigned a defensive role in other plants (Levin, 1971) and a
carcinogenic compound or compounds (I. A. Evans, et aZ., 1971, 1974). The
young growing tips of the plant appear t o be more carcinogenic than the stalks
(Hirono, 1973), which is again in keeping with the generally more toxic nature
of the plant in the Spring. Finally, an unidentified compound or compounds
causing retinal degeneration in sheep (Mason, Barnett, Blackemore & Rees
Evans, 1973; Watson et aZ., 1972) and “a glucoside with insecticidal and
fungicidal properties” (which is presumably not the cyanogenic glucoside?)
patented by Celec Corporation that has been prepared from the plant (Braid,
1959).
Even allowing for the fact that some of these compounds will eventually be
shown to be unimportant as far as grazing arthropods are concerned, this is an
206
J . H. LAWTON
impressive list, and fully justifies the view that bracken is a ‘nasty plant’. This
may be particularly so if the possibility of ‘synergistic’ interactions between
these various compounds exists. It may be difficult for a herbivore t o detoxify
more than one defensive compound at any time, and the seasonal changes of
strategy employed by the plant may also complicate things further.
In passing, one other possible defence mechanism of a quite different nature
which we may call the ‘set a thief to catch a thief’ principle, may be noted. The
function of the ‘extra-floral nectaries’, which appear in the axils of the
pinnae of the plant during the Spring and early Summer, has been discussed by
Braid (1959), Schremmer (1969) and Tryon (1941). Darwin (1877) gives a very
precise account, pointing out that the liquid which they secrete is very
attractive t o ants, and draws a parallel between bracken and certain other plants
(including ant acacias) that attract these insects apparently for defensive
purposes against grazing animals. As in many other places, ants certainly visit
the young fronds in large numbers on the Skipwith study area during the
spring, in order t o exploit the secretion from the ‘nectaries’. It is interesting t o
ask whether these ants provide any defence for the plant in return. Fronds with
ants do not have any fewer bracken-specific herbivores on them, on average,
than fronds without ants (unpubl. data), but the obvious and rather simple
experiment of adding different, non-adapted herbivores and seeing what the
ants do has not been carried out. If the ants d o have a defensive role, they are
providing it for a plant which already has a large number of other possible
defence-mechanisms. As such, it would be quite a different role from that of
the ants in the genus Acacia (Rehr et al., 1973).
Given that bracken has so many potential defences against being eaten, the
question raised earlier of how many of the species which feed on it are
‘specialists’ and how many are ‘generalists’ becomes particularly interesting.
Table 3 summarizes the results of such an analysis. Of the total list of species in
Appendix 1 (excluding two of unknown feeding specificity), 11 are found only
on bracken, another 14 on bracken and other ferns (and in most of these cases
bracken is the principal food plant) and 1 3 polyphagous species feed on
a very wide range of plants as well as bracken and ferns. Whereas a majority of
the sawflies (8 out of 11) are specialist fern-feeders, only 3 out of 10 of the
Lepidoptera are known to fall into this category, again perhaps suggesting a
replacement of the latter by the former in this feeding niche. A consideration
of only the 18-20 ‘key-species’ shows that a very high proportion of these are
specialist bracken- or bracken-and-other-fern feeders; only two species
(Bourletiella and Philaenus) that feed with any regularity on the plant are
polyphagous and the latter is curiously ‘patchy’ in its occurrence. The large
number of bracken specialists amongst the ‘key-species’ is exactly what might
be expected given the apparently highly toxic nature and low quality of the
plant as a food resource for herbivores. This immediately, however, raised the
problems of how the 1 3 polyphagous species listed in Table 3 are able t o
exploit the plant, and why, with the exception of Philaenus and Bourletiella,
they do not do so with greater regularity. Either they rely on the occasional
break-down of the plant’s defence mechanisms (which seems unlikely) or they
are able t o tolerate and detoxify a wide range of defence mechanisms in many
different plant-species of very variable quality. Most of them would, in fact,
qualify for the term ‘super-generalist’; and it may weli form part of their
T H E ARTHROPOD COMMUNITY O N BRACKEN
207
normal life-history strategy to change host plants sporadically and unpredictably, which is why we d o not find them regularly on bracken. By doing so,
this would give them repeated temporary advantages (by ‘escape’ in time and
space) over their own specific parasites and predators. The fact that all the
(rare) records of insect outbreaks and serious defoliation of bracken in Britain
that I can find have involved super-generalists is consistent with this view.
Specific examples from the Lake District include large-scale defoliation in
September 1945 by Spilosoma lutetim and Ceramica pisi, and in July 1949 by
Phyllopertha horticola (J. P. Rogerson, pers. comm.).
Although discussion has been confined almost entirely to bracken in Britain,
the limited information on bracken arthropods in other areas of the world is in
general agreement with the picture built up in this paper. The community in
Central Europe, although slightly richer than in Britain, is virtually identical in
its composition (Simmons, 1967; Wieczorek, 1973), and although similar
faunal lists are not available for other parts of the world, North American
literature, for for example, confirms the large number of sawflies adapted to
feeding on the plant (Beer, 1955; Hogh, 1966; Smith, 1969).
The general absence of Coleoptera also appears to be typical, and is in line
with the situation on ferns in general (Linssen, 1959; 206), although in two
areas of the world specific bracken-feeding Coleoptera have been recorded:
Hawaii has two species (Swezey, 1922) and Papua and New Guinea one (Gray,
1970). The question of why certain groups of arthropods are able to exploit
the plant so successfully whilst other normally successful groups appear unable
to do so is very broad, and it is not proposed to deal with it here.
For the animal ecologist, bracken is a fascinating plant. Its tendency to form
dense, stable monocultures, involving a clearly defined guild of herbivores
which interact in as yet poorly understood ways with the defence mechanisms
of their host plant and in still more poorly understood ways with their own
predators and parasites presents an opportunity to study, in one and the same
community, several areas of fundamental importance in community ecology.
Explicitly or by inference this paper raises more problems than it solves; but
the problems which it raises are obviously worth pursuing.
ACKNOWLEDGEMENTS
A very large number of people have helped with and contributed to this
study. The Yorkshire Naturalists’ Trust gave me permission to work on their
reserve at Skipwith Common; Ann Fisher and Sue Fawcett did a great deal of
the routine work with their usual care, interest and skill; Dr Terry
Crawford-Sidebotham taught me about cyanogenesis, and made his own
facilities for analysing cyanide freely available; Dr Richard Firn taught me
about ecdysones in plants; Peter Skidmore, A. C. Pont and Drs \I. F. Eastop,
Stuart McNeill, John Whittaker and Tom Wood helped me with identification
of all the various groups. Drs Jo. Anderson, John Beddington and Stuart
McNeill all made helpful and constructive comments on the manuscript. To all
these friends, colleagues and organizations I am extremely grateful. Stuart
McNeill, in particular, first suggested that bracken would be fun to look at; he
was right.
208
J . €-I. LAWTON
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1158-60.
SCHREMMER, F., 1969. .?xtranuptiale Nectarien. Beobachtungen an Salix eteagnos Scop. und Pteridium
aquilinum (L.) Kuhn. Ost. bot. Z., 1 1 7: 205-22.
SHEARER, G . D., 1945. Some observations on the poisonous properties of bracken (Pteris aquilina). J.
comp. Path., 55: 301-7.
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(Polypodiaceae) PANS (C), 13: 200-3.
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SNEDECOR, G.
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337-58.
b.
APPENDIX 1
A list o f tlw prirzcipal arthropods wliicli f e e d
012
bracken in t h e British Isles
The information in this list is derived from the literature, supplemented by correspondence and field collections from over 50 localities in widely separated areas of Britain.
Predators and species primarily associated with the litter or dead fronds, have been excluded.
A few of the most important synonyms are listed where confusion in the older literature
is possible.
A separate bibliography is provided at the end of the appendices.
INSECTA
Coleoptera
Scarabaeidae
1. Phyllopertha horticola (L.)
Common and widespread: a polyphagous insect attacking a wide range of trees and
herbaceous vegetation, including bracken.
Note. A number of other non-carnivorous adult Coleoptera may be collected o n bracken
from time to time, sometimes in quite large numbers, and particularly in t h e spring, but
J. H. LAWTON
210
their relationships with the plant are uncertain. They include several Elateridae (e.g. the
very common and widspread Dalopius marginatus (L.)) and the rare Dirhagus pygmaeus
(F.) (Eucnemidae) as well as, amongst others, Helodidae (e.g. Cyphon padi (L.) and
Cyphon variabilis Thunb.) and even some Lathridiidae (e.g. Cartodere ruficollis Marsh).
I t is probable that some of these species are attracted to the ‘nectaries’ (see text).
Collembola
Sminthuridae
2. Bourletiella viridescens Stach, S . Gisin
Widespread throughout Europe on poor, dry vegetation in lowland areas (Gisin,
1960). I t is very common on bracken in the North of England (Yorkshire, Cumberland,
Westmorland) in North Wales, and in Oxfordshire and Berkshire, and will probably
prove to be common throughout Britain. Precisely what Bourletiella is feeding on is
uncertain-but the epidermis, sporangia or surface micro-organisms are all possibilities.
Note. Two other Sminthurid Collembola have also been collected less frequently in the
North of England (a Srnintkurus sp. and a Dicyrtoma sp.). The species, and whether
they are feeding o n the fronds, remains to be determined.
Diptera
Agromyzidae
3 . Phytoliriomyza hilarella (Zett.)
The larvae mine t h e pinnules: it is widespread in England, and has also been recorded
from Ireland and Scotland (Hering, 1957; Spencer, 1972).
syn. Pteridomyza h.
Phytobia h
Praspedomyza h.
Agromyza h.
Note. Recently, Phytolfriomyza pteridii sp. nov. has been described (Spencer, K . A.,
1973, Entomologist’s Gaz., 24, 315-7). This adds one more species to the know faunal
list for the plant. The mines appear t o be indistinguishable from those of P. hilarella, on
present information.
Anthomyiidae
T h e life-histories and taxonomy of the fern feeding species in this group are discussed
by Cameron (1930), Meilcle (1937), Collin (1955), Hering (1957) and Hennig (1966).
The early literature is confusing and some of the more important synonyms are listed
where appropriate.
4. Chirosia albifrons Tiens.
Adults have been recorded sparingly on bracken between May and July in Cornwall,
Hants, Berks., Worcester and Cambs. In view of t h e life-histories of other species in the
group, the larvae probably mine some part of the plant, but its life-history appears to be
unknown.
5 . Chirosia albitarsis Zett.
The larvae appear to mine both the stem (i.e. petiole and rachis) and the ‘leaf-stems’
(i.e. the stems of t h e pinnae). I t is common and widespread throughout Britain from the
north of Scotland t o the southern counties of England.
THE ARTHROPOD COMMUNITY ON BRACKEN
211
6. Chirosia crassiseta Stein
The larvae of this species also appear to mine the stems of the plant, but it is less
widely distributed than albitarsis, being confined to the southern half of England.
7 . Chirosia flavipennis F a l l h
The larvae mine the tips of the pinnules. Despite some uncertainty in the literature,
bracken is probably the principal or only host of this species (A. C. Pont, pers. comm.).
I t is widely distributed throughout Britain. See also Fonseca (1956).
syn. Pycnoglossa
8. Chirosia hystricina Rondani
The larvae mine the tips of the pinnules, producing a large ‘blister-mine’. Only
Hering’s (1957) life-history data are reliable (A. C. Pont, pers. comm.). I t occurs
commonly in the north of England and Scotland but is scarce in the south, where it has
been recorded in Surrey, Sussex, Norfolk and Berkshire.
syn. C. cinerosa Stein (nec Zett.)
C. cinerosa aut. (Hering)
C. hystrix Brischke
C. setifemur Ringdahl
Pycnoglossa hystrix Brischke
9. Chirosia parvicornis Zett.
The larvae mine the frond-tips of bracken and other ferns, causing them to curl u p
into a very characteristic ‘gall’. I t is perhaps the commonest and most widely
distributed Chirosia.
Note. I t is probable that the larvae of a number of other species in the genus Chirosia
and possibly also in the related Acrostilpna will prove to occur on bracken, though
probably not as their major host.
Cecidomyiidae
10. Dasyneura fi2icina (Kieff)
The larvae roll the edges of the pinnules, forming small green galls which eventually
turn black. Often extremely abundant when it occurs, it is widespread but locally
distributed throughout England (Darlington, 1968). Unlike the next species, it appears
to be confined to bracken (Buhr, 1964).
11. Dasyneura pteridicola Kieff
This second species also occurs on bracken (Cameron, 1930) and possibly a number
of other ferns (Buhr, 1964); it may occur on the same fronds asfilicina but appears t o
be rarer at least in northern England and its distribution in Britain is not well known,
although the galls are quite distinct, being ‘softer’, less thickened and paler in colour.
Hemiptera : Heteroptera
Miridae
The two fern-feeding species are discussed by Southwood & Leston (1959).
12. Bryocoris pteridis (Fallen)
Less frequently found on bracken than on Athyrium and Dryopteris: t h e species is
widely distributed throughout Britain.
J. H. LAWTON
212
13. Monalocoris filicis (L.)
Very common o n bracken, but also feeds on other ferns; this bug is widely
distributed throughout Britain.
Note. The nymphs (but not the adults) of a member of t h e Lygaeidae (Drymus
probably brunneus Sahlberg (S. McNeill, pers. comm.)) are common on bracken in
many areas. Their relationships with the plant are uncertain.
Hemiptera : Homoptera
Aphididae
14. Aphis fabae Scopoli
Alatae of this common British species settle on many plants, and have been collected
from bracken at several sites in the north of England, occasionally forming substantial
colonies; it is doubtful, however, whether it can persist o n bracken alone. (V. F. Eastop,
pers. comm.)
15. Macrosiphum ptericolens Patch
The species was first discovered on bracken during 1972 at t w o sites in Yorkshire
where it was extremely common. Subsequent observations show that it occurs o n
bracken in several other sites throughout the north of England (Lawton & Eastop,
1975). I t is now known to be widespread.
These appear t o b e the first records of the species in Europe although it is known
from ferns in the United States (Robinson, 1966), and its discovery can probably be
attributed to a lack of previous observation rather than a genuine extension of its range.
The North American literature recognizes two very similar species-pteridis Wilson and
ptericolens Patch-which may eventually prove to b e two ends of a continuous series; on
present evidence Yorkshire material is referable t o ptericolens (Lawton & Eastop,
1975).
Cercopidae
16. Pnilaenus spumarius (L.)
This extremely polyphagous species occurs regularly (as ‘cuckoo-spit’) on bracken in
many areas of Britain, although its occurrence may be very localized. The conditions
under which it will feed on bracken, and whether it is capable of completing its
life-history o n t h e plant, require investigation.
Delphacidae
17. Criomorphus pteridis (Spinola)
Confined to bracken, and common in many areas of England as far north as
Westmorland (Le Quesne, 1960) and in Ireland.
Hymenoptera
Tenthredinidae
See Benson (1952) and Lorenz & Kraus (1957)
18. Aneugmenus coronatus (Klug)
The larvae feed on bracken and also on Athyrium and Dryopteris. It is scarce in the
south of England, occurring as far north as Lancashire and Cheshire (see Buhr, 1964).
19. Aneugmenus furstenbergensis (Konow)
Occurs throughout England, Scotland and Ireland, but is scarce; the larvae are
thought to feed on bracken and other ferns.
THE ARTHROPOD COMMUNITY ON BRACKEN
21 3
20. Aneugmenus padi (L.)
Very common throughout Britain and Ireland, the larvae feeding on bracken and
other ferns.
21. Aneugmenus temporalis (Thomson)
The larvae are thought to feed on bracken and other ferns. Scarce throughout Britain
and Ireland.
22. Stromboceros delicatulus (Fallhn)
Common throughout Britain and Ireland, the larvae feeding on bracken and a number
of other ferns (Athyrium, Dryopteris, Onoclea, Polypodium).
2 3 . Strongylogaster lineata (Christ)
On bracken, Dryopteris and other ferns; very common throughout Britain and
Ireland.
24. Strongylogaster maculata (Klug)
Local throughout Britain and Ireland, feeding on bracken and Athyrium. I t is more
frequently encountered in northern England and Scotland.
25. Strongylogaster xanthoceros (Stephens)
Common in south and south-east England, apparently only o n bracken.
Note. A fourth species of Strongylogaster--S. mixta (Klug) (also known as Thrinax
mixta in earlier literature)-has been recorded feeding o n bracken b y Lorenz & Kraus,
(1957) and Simmonds (1967) but n o t by Benson (1952). Its food plant requires further
investigation. I t is rather rare in the south of England, b u t rather commoner in northern
England, Wales and Scotland. I t also occurs in Ireland.
26. Tenthredo colon Klug
Found throughout Britain, north t o Dumfries, but appears to be fairly rare: very rare
in Ireland. T h e larvae feed on a wide range of herbaceous vegetalion including bracken.
27. Tenthredo ferruginea Schrank
Common throughout Britain and Ireland, the larvae are polyphagous, feeding on
herbs and trees, as well as bracken.
28. Tenthredo livida L.
Equally polyphagous; a very common species, found throughout Britain and Ireland.
Note. Simmonds (1967) also records the polyphagous Empria excisa Th. o n bracken.
This is not confirmed by other workers nor by my own observations, and for the
present it is probably better to regard Empria as a very rare feeder on the plant.
Lepidoptera
The food-plants of British Lepidoptera are discussed b y Stokoe (1948) Allen (1949),
and Ford (1949), amongst others.
Arctiidae
29. Spilosoma luteum (Hufnagel)
Common throughout the British Isles; the caterpillars feed on many types of
low-growing plants, including bracken (Braid, 1959).
15
214
J . H. LAWTON
Gelechiidae
30. Paltodora cytisella (Curt.)
This species appears to be confined to bracken, the caterpillars mining the rachis and
petiole causing characteristic swellings. They may be locally very common and are
recorded from England and Ireland (Buhr, 1965)
Geometridae
3 1. Petrophora chlorosata(Scopo1i)
The caterpillars are confined to bracken. I t is a widespread and common species,
found throughout Britain and Ireland, but it appears to be most common in England
and Wales and rather local in Scotland.
syn. Lithina c.
Phasania petraria (Hb)
Hepialidae
32. Hepialus fusconebulosa (De Geer)
The caterpillars appear to be confined to the rhizomes of bracken; the species is
found throughout Britain, but is commoner in the north of England; it also occurs in
Ireland (see Meikle, 1937).
syn. H. velleda (Hubner)
3 3 . Hepialus hecta (L.)
Fairly common throughout Britain and also Ireland, the caterpillars feeding on the
rhizome, and on the roots of Taraxacum and possibly other plants.
34. Hepialus sylvina (L.)
Common in southern and eastern England, but occurs more locally throughout
northern England, and in Scotland as far north as Morayshire. The larvae feed o n the
rhizomes, and also occur in the roots of several other plants, including E'chiurn and
Rurnex.
Noctuidae
35. Cerarnica pisi (L.)
Fairly common throughout the British Isles. The caterpillars feed on a wide range of
herbs, shrubs and trees as well as bracken (Braid, 1959).
36. Euplexia lucipara (L.)
The caterpillars feed on a wide range of herbs, shrubs and trees as well as bracken and
other ferns. I t is a generally distributed species, common in the southern counties of
England.
37. Phlogophora meticulosa (L.)
The caterpillars of this species are again extremely polyphagous and it has been
recorded from a great variety of herbaceous vegetation and shrubs, including bracken. I t
is generally distributed throughout Britain.
Other Lepidoptera
38. An unidentified microlepidopteran, larger than Paltodoru (30) in the final instar and
darker in colour, is fairly common on the newly uncurling frond-tips, where it makes a
silken tube. I t has not been possible to identify this species.
Note. Some of the early literature (e.g. Scorer, 1913) also records other Lepidoptera o n
bracken, like the two noctuids Laconobia ( = Manestra) contigua (Denis & Schlif.) and
L. aleracea (L.). This is not confirmed by field sampling o r more recent literature.
THE ARTHROPOD COMMUNITY ON BRACKEN
21 5
ACARI
Cryptostigmata
39. Chamobates sp.
A small black oribatid mite, frequently extremely abundant on the undersides of the
frond. I t has been recorded in Oxfordshire, Berkshire, Norfolk, north Wales and the
north of England, and will probably prove t o be very widespread. T h e species, and
exactly what it is feeding on, remain to be determined. I t may perhaps, when more
information becomes available, be more correctly assigned as a member of the litter
fauna which occasionally wanders u p o n to the fronds, but its abundance seems to rule
out this explanation a t this stage.
Prostigmata
40. Phytoptus pteridis (Molliard)
A gall mite; this species appears to be rare and is not listed in Farkas (1965), although
Darlington (1968) says that it causes a rolled gall on the pinnules similar t o that caused
by Dasyneura (number 10) b u t that the gall is hairy: other descriptions of the damage
vary (e.g. Buhr 1964), and more than one species may be involved. I t has been recorded
in Britain in northern England and Ireland.
syn. Eriophyes p .
APPENDIX 2
A list of the common and widespread species of higher land-plants (excluding trees) for
which herbivore species-lists were compiled; this data provided a ‘yardstick’ against which
bracken fauna could be compared (see text). The reference works consulted in compiling the
faunal lists are shown in the bibliography at the end of the appendices.
Achillea millefolium L.
Angelica sylvestris L.
Anthoxanthum odoratum L.
Lathyrus pratensis L.
Lolium perenne L.
Lotus corniculatus L.
Bellis perennis L.
Plantago lanceolata L.
Plantago
L.
Poa annua L.
Potentilla anserina L.
Potentilla erecta (L.) Rausch.
Prunella vulgaris L.
Capsella bursa-pastoris (L.) Medic.
Centaurea nigra L.
Cerastium holosteoides Fr.
Cirsium arvense (L.) Scop.
Cirsium palustre (L.) Scop.
Cirsiurn vulgare (Savi) Ten.
Cynosurus cristatus L.
Dactylis glomerata L.
Deschampsia cespitosa (L.) Beauv.
Dryopteris filix-max (L.) Schott.
Filipendula ulmaria (L.) Maxim.
Galium aparine L.
Geranium robertianum L.
Ranunculus acris L.
Ranunculus repens L.
R u m e x acetosa L.
Senecio jacobaea L.
Senecio vulgaris L.
Stellaria media (L.) Vill.
Taraxacum officinale Weber
Trifolium pratense L.
Trifolium repens L.
Tussilago farfara L.
Hedera helix L.
Heracleum sphondylium L.
Holcus lanatus L.
Hypochoeris radicata L.
Urtica doica L.
Juncus effusus L.
Veronica chamaedrys L.
216
1. H. LAWTON
A list of selected groups of insects associated with each of these plants was compiled from
the following sources:
Coleoptera. Walsh & Dibb (1954)
Diptera : Agromizidae. Spencer (1972)
Herniptera : Heteroptera. Southwood & Leston (1959)
Hemiptera : Cicadomorpha and Fulgoromorpha. Le Quesne (1960, 1965, 1969)
Hymenoptera : Symphyta. Benson (1952, 1954, 1958)
Lepidoptera. Allen (1949); Ford (1949); Saunders (1939); Stokoe (1948).
REFERENCES (APPENDICES 1 and 2)
ALLAN, P. B. M., 1949. L,arval foodplants. London: Watkins & Doncaster.
BENSON, R. B., 1952, 1954, 1958. Handbooks f o r the identification o f British insects, VI, Part 2 a-c.
Hymenop tera: Symphyra. London: Royal Entomological Society.
BRAID, K. W., 1959. Bracken: a review of the literature. Hurley: Commonwealth Agricultural Bureaux.
BUHR, H., 1964-65. Bestimmungstabellen der Gallen (Zoo-und Phytocecidien) an Pjlanzen Mittel-und
Nordeuropas, 1 -2. Jena: Fischer Verlag.
CAMERON, A. E., 1930. Two species of anthomyiid diptera attacking bracken and their hymenopterous
parasites. Scorr. Nut., 182: 137-41.
COLLIN. J. E., 1955. Genera and species of Anthornyiidae allied to Chirosiu (Diptera). J . SOC.Br. Ent., 4:
94-100.
DARLINGTON, A,, 1968. Plant galls. London: Blandford.
FARKAS, H., 1965. Spinnentiere Eriophyidae (Gallmilben). Tierwelt Mitteleur., 3: 1 - 1 5 5 .
FONSECA, E. C. M. d’A., 1956. A review of the British subfamilies and genera of the family Muscidae
(Diptera). Trans. SOC.Br. Ent., 12: 1 1 3-28.
FORD, B. A., 1949. A guide to the smaller British Lepidtoptera. London: South London Entomol. &
Nat. Hist. SOC.
GlSlN, H., 1960. Collembolenfauna Europas. Geneva: Museum DHistoire Naturelle.
HENNIG, W., 1966. Die Fliegen der palaarktischen Region, Part 63a, Anthomyiidae: 58-65.
HERING, E. M., 1957. Bestimmungstabellen der Blattminen von Europa. Junk.
LAWTON, J. H. & EASTOP, V. F., 1975. A bracken-feeding Macrosiphum (Hemn., Aphididae) new to
Britain. Entomologist’s Gaz., 26: 135-8.
LE QUESNE, W. J., 1960, 1965, 1969. Handbooks f o r the identification of British insects Vol. II. Parts
2a.b, 3. Hemiptera. London: Royal Entomol. SOC.
LORENZ, H. & KRAUS, M., 1957. Die Larvalsystematik der Blattwespen (Tenthredinoidea und
Megalodon toidea). Berlin: Akademi-Verlag.
MEIKLE, A,, 1937. The insects associated with bracken. Agric. Prog., 14: 58-60.
ROBINSON, A. G., 1966. Review of the fern aphids of North America with descriptions of a new species
and a new genus. Can. E n t . , Y8: 1252-9.
SANUARS, E., 1939. A butterfly book f o r the pocket. Oxford: Clarendon Press.
SCORER, A. C., 1913. The entomologists log-book. London: Routledge.
SIMMONS, F. J., 1967. Possibilities of biological control of bracken Pteridium aquilinum (L.) Kuhn
(Polypodiaceae). P A N S (C), 13: 200-3.
SOUTHWOOD, T. R. E. & LESTON, D., 1959. Land and water bugs of the British Isles. London: Warne.
SPENCER. K. A., 1972. Handbooks f o r the identification o f British Insects, 10. Part 5 (g) Diptera:
Agromyzidae. London: Royal Entornol. Soc.
STOKOE, W. J . , 1948. The caterpillars of British moths, Series 1 and 2. London: Warne.
WALSH, G. B. & DIBB, J. B. 1954. (Eds). A coleopterist’s handbook. London: Amateur Entomol. Soc.