Download Food web structure of three guilds of natural enemies: predators

Journal of Animal Ecology 2008, 77, 191–200
doi: 10.1111/j.1365-2656.2007.01325.x
Food web structure of three guilds of natural enemies:
predators, parasitoids and pathogens of aphids
Blackwell Publishing Ltd
F. J. F. Van Veen1,2*, C. B. Müller2†, J. K. Pell3 and H. C. J. Godfray1,2‡
1
NERC Centre for Population Biology and 2Division of Biology, Imperial College London, Silwood Park Campus,
Ascot, Berks, SL5 7PY, UK; and 3Plant and Invertebrate Ecology Division, Rothamsted Research, Harpenden, Herts,
AL5 2JQ, UK
Summary
1. Most communities of insect herbivores are unlikely to be structured by resource competition,
but they may be structured by apparent competition mediated by shared natural enemies.
2. The potential of three guilds of natural enemies (parasitoids, fungal entomopathogens and
predators) to influence aphid community structure through indirect interactions is assessed. Based
on the biology, we predicted that the scope for apparent competition would be greatest for the predator
and least for the parasitoid guilds.
3. Separate fully quantitative food webs were constructed for 3 years for the parasitoid guild,
2 years for the pathogen guild and for a single year for the predator guild. The webs were analysed
using standard food web statistics designed for binary data, and using information-theory-based
metrics that make use of the full quantitative data.
4. A total of 29 aphid, 24 parasitoid, five entomopathogenic fungi and 13 aphid specialist predator
species were recorded in the study. Aphid density varied among years, and two species of aphid were
particularly common in different years. Omitting these species, aphid diversity was similar among
years.
5. The parasitoid web showed the lowest connectance while standard food web statistics suggested
the pathogen and predator webs had similar levels of connectance. However, when a measure based
on quantitative data was used the pathogen web was intermediate between the other two guilds.
6. There is evidence that a single aphid species had a particularly large effect on the structure of the
pathogen food web.
7. The predator and pathogen webs were not compartmentalized, and the vast majority of
parasitoids were connected in a single large compartment.
8. It was concluded that indirect effects are most likely to be mediated by predators, a prediction
supported by the available experimental evidence.
Key-words: Coccinellidae, Entomophthorales, keystone, phytophagous, Syrphidae.
Introduction
Ecological communities may be haphazard collections of
weakly interacting species or they may be structured by
ecological processes such as competition, predation and
parasitism. While resource competition has played a major
role in explaining the structure of many ecological communities
*Correspondence author. E-mail: [email protected]
†Present address: Institute of Environmental Sciences, University of
Zürich, Winterthurerstrasse 190, 8057 Zürich, Switzerland.
‡Present address: Department of Zoology, University of Oxford,
South Parks Road, Oxford OX1 3PS, UK.
[e.g. plants (Tilman 1982); intertidal invertebrates (Menge
1976; Paine 1984)] it is unlikely to play a significant role in
contemporarily structuring communities of herbivorous
insects. The latter often consist of species that are restricted to
feeding on nonoverlapping sets of plant species and therefore
cannot interact through interference or resource competition.
However, interactions may occur through shared natural
enemies – predators, parasitoids or pathogens – and these
indirect interactions may be important in influencing community structure. The simplest type of indirect interaction is
apparent competition in which the presence of one species
leads to higher densities of a common natural enemy, which
consequently causes increased mortality and a lower population
© 2007 The Authors. Journal compilation © 2007 British Ecological Society
192
F. J. F. Van Veen et al.
density of a second species. This idea, which has a long
pedigree in ecology (Jeffries & Lawton 1984; Abrams 1987;
Holt & Kotler 1987; Holt & Lawton 1994; Abrams & Matsuda
1996; van Veen, Morris & Godfray 2006b), was first formally
explored by Holt (1977) and its principles were experimentally
demonstrated by Bonsall & Hassell (1997, 1998). Just like
interference and exploitation competition, apparent competition and related interactions can also structure ecological
communities (Jeffries & Lawton 1984; Lawton 1986; Godfray
1994; Hawkins 1994).
There is as yet only limited experimental evidence for
apparent competition and related indirect effects among
herbivorous insects (Berdegue et al. 1996; van Veen et al.
2006b). The three main categories of natural enemies that
might mediate these interactions are predators, parasitoids
and pathogens. Short-term apparent competition between
herbivorous arthropods mediated by predators has been
demonstrated in field experiments (Karban, HougenEitzmann & English-Loeb 1994; Müller & Godfray 1997;
Rott, Müller & Godfray 1998) and has been shown to prevent
the establishment of some aphid species in a field even though
they were common in the aerial plankton (Müller & Godfray
1999). There is also evidence for apparent competition
mediated by parasitoids among leafhoppers (Settle & Wilson
1990) and among rainforest leafminers (Morris, Lewis &
Godfray 2004). The advantages of providing alternative hosts
for the natural enemies of crop and forestry pests that presupposes indirect effects between herbivores have also received
much attention (e.g. Landis, Wratten & Gurr 2000; van Veen,
Memmott & Godfray 2006a).
Food webs provide a valuable means of assessing the
potential for indirect effects and for generating testable
hypotheses (Cohen, Brian & Newman 1990). Traditional food
webs consist of sets of binary links between ‘trophic species’
representing feeding interactions. These are particularly
sensitive to sampling effort (Polis 1991; Bersier, BanaekRichter & Cattin 2002). The use of trophic species also makes
interpreting food web structure difficult (Sugihara, Bersier
& Schoenly 1997; Solow & Beet 1998; Yodzis & Winemiller
1999), particularly when studying population-level processes
where distinguishing among species is important. The alternative is to construct quantitative webs where the densities of all
biological species and trophic links are given in the same units
(Memmott & Godfray 1994; van Veen et al. 2006b).
Communities of hosts and parasitoids provide good systems
for study using quantitative food webs, because the trophic
links between hosts and parasitoids are relatively easy to
establish and to quantify and a number of such parasitoid
webs have now been described (Memmott, Godfray & Gauld
1994; Müller et al. 1999; Rott & Godfray 2000; Schönrogge
& Crawley 2000; Henneman & Memmott 2001; Valladares,
Salvo & Godfray 2001; Lewis et al . 2002). However,
herbivorous insects are attacked not only by parasitoids
but also by predators and pathogens and it is as yet unclear
whether webs of the links between these guilds and their
host/prey will show similar properties to those of the
parasitoids.
The aim of this study was to construct sets of quantitative
food webs for the three guilds of natural enemies attacking
a community of aphids and to compare their properties, in
particular with regard to the potential for apparent competition.
The aphids (Aphidoidea) are a superfamily of phloem-sucking
insects (Hemiptera: Sternorrhyncha). They are extensively
attacked by predators, parasitoids and pathogens. We reasoned
that natural enemies that required a prolonged intimate
association with the host would evolve over time to be highly
specialized with a narrower host range. The two groups of
koinobiont parasitoids that attack aphids (Aphidiinae
(Ichneumonoidea: Braconidae) and Aphelinidae (Chalcidoidea)) lay single eggs inside live aphids and the larva may
suspend development until the aphid has become an adult
(Powell 1982; Askew & Shaw 1986). During this period the
parasitoid is susceptible to attack by the host immune system
and to survive it has to tolerate or disable the host defences,
representing an intimate relationship with the host. The most
important aphid pathogens are fungi from the Zygomycetes,
order Entomophthorales. The conidia (spores) germinate on
the aphid cuticle and invade the haemolymph and internal
organs. However, unlike the parasitoids, the fungus does not
suspend development and hence the interaction may be less
intimate (Pell et al. 2001). Finally, specialist aphidophagous
predators such as ladybirds (Coccinellidae); hoverfly larvae
(Syrphidae); predatory midge larvae (Cecidomyiidae); lacewing
larvae (Chrysopidae) and species of Anthocoridae (Hemiptera)
(Dixon 1985) exploit aphids as prey rather than as hosts
for reproduction. Predators generally do not require being
adapted to a close and prolonged interaction. We hypothesized
that connectance would decrease from predator guilds through
pathogen guilds to parasitoid guilds on the grounds that the
more intimate the relationship between aphid and natural
enemy, the greater the degree of specialization that would
evolve. Hence, we expected predators to show the greatest
potential to mediate apparent competition. As a corollary of
this, we expected species diversity to increase from predator
guilds through pathogen guilds to parasitoid guilds as niche
space became more finely divided.
Methods
We studied the aphid–natural enemy community in a damp field
(Rush Meadow) at Silwood Park, Berkshire, UK. The study site was
18 000 m2 in size, trapezoidal in shape, and surrounded on three
sides by damp woodland dominated by Alnus, Salix and Betula, and
on the fourth side by a higher, dryer, heavily grazed field. The plant
community in the field was typical for a poorly drained mesotrophic
grassland and consisted of patches of MG9 Holcus lanatus–
Deschampsia cespitosa grassland and MG10 Holcus lanatus–Juncus
effuses rush-pasture, according to the British National Vegetation
Classification (Rodwell 1998). A full list of plant species from which
aphids were recorded is given in the Appendix.
From April to October all plants in the field were scanned for
aphids. When noted on a particular plant species, the density of each
aphid species on that plant species was estimated by counting twice
a month the number of individuals per ‘plant unit’. The plant unit
was chosen to be a relatively constant unit of vegetation, often the
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 191–200
Aphid natural enemies 193
individual plant in the case of herbaceous forbs, a flowering stem in
the case of grasses fed on by aphids that congregate on flower
spikes, or a 30 cm terminal shoot in the case of shrubs where aphids
feed on young growth. On every fortnightly sampling occasion a
minimum of 300 units of every plant species were chosen at random,
stratified over forty 20 × 20 m grid cells covering the whole site. At
the same time as the aphids were surveyed, predator, parasitoid and
pathogen densities were estimated by counting the number of predator
individuals, parasitoid mummies (parasitoid pupae attached to the
plant substrate) and pathogen-infected cadavers associated with
each plant unit. Plant abundance was estimated by recording the
number of plant units per m2 at 3-m intervals along 15 parallel
transects. The transects were placed at 20-m intervals over the whole
site and care was taken that they ran through each of the forty
20 × 20 m grids. Estimates of plant density per m2 allowed us to
translate all the relative estimates of aphid and natural enemy
densities to absolute figures with units per m2.
To assess the composition of the parasitoid and pathogen
communities, a sample of parasitoid mummies and infected cadavers
was taken to the laboratory on each sampling date for identification.
For each plant species on which parasitoid mummies were observed
we collected a maximum of 200 mummies every fortnight or fewer
when they were rare. The target sample size for fungus-infected
cadavers was 50. The parasitoid mummies were reared individually
in gelatine capsules and the adult insects identified using the keys in
Mackauer (1959), Stary (1966), Gärdenfors (1986) and Pungerl
(1983). Some species boundaries were resolved using cellulose acetate
allozyme electrophoresis (see Appendix in Müller et al. 1999). The
fungus-infected cadavers were placed on wet filter paper and inverted
over microscope slides in 9 cm diameter Petri dishes overnight at
room temperature. The discharged conidia on the microscope slide
were fixed and stained in cotton blue (diluted to 10% in lactophenol)
and identified from their gross conidial morphology using the
descriptions of Wilding & Brady (1984), Humber (1989) and Keller
(2006). Although 29 species of Entomophthorales have been recorded
from aphids worldwide (Keller 2006), many are extremely rare and
we are confident that our identifications are accurate in the vast
majority of cases. The aphids were identified using the keys of Heie
(1986, 1992, 1994, 1995).
For the predators we concentrated on specialist predators of
aphids, specifically Coccinellidae (adults and larvae), Syrphidae
(larvae), Chrysopidae (larvae), Anthocoridae (adults and nymphs)
and Cecidomyiidae (larvae). These were identified using the standard
identification manuals for each group. The abundance of each species
and developmental stage was estimated as counts per plant unit and
later translated into density per m2, as described above.
Unlike the parasitoid and fungal pathogens where the aphid
mummy/cadaver is a natural unit to compare across species, predators
vary greatly in size and obtain different amounts of sustenance from
aphids of different size. To correct for this, in calculating link density
we assumed that the volume of food eaten is proportional to metabolic
rate, and that this scales with the 3/4 power of body size, the most
common though not the only reported relationship (reviewed in
Glazier 2005). Thus in the predator food webs the aphids are scaled
by their volume, and the predators by their ‘collective appetite’.
Another challenge with building a predator web is that the unit of
measurement is of a predator individual on a host plant rather than
the actual predation event itself. This is different from the data
underlying the pathogen and parasitoid webs where the mummy/
cadaver is the interaction incarnate. Difficulties arise when there are
more than one prey species present on the same plant at the same
time. Therefore, we constructed two alternative interpretations of
the predator web that are likely to bracket what actually occurs in
the field. In the first we assume that each predator feeds on the
aphids on a particular host plant in proportion to their abundance.
In the second we assume that the predator feeds only on the most
abundant prey species (leading to a reduced number of trophic
links). Below we shall call the two types of web proportional and
specialized predator webs, respectively. We present data for predators
in 1996, pathogens in 1997 and 1998, and parasitoids for 1996–98.
The majority of food web statistics have been designed for
qualitative, binary webs where species and links among them are
scored as either present or absent. Quantitative webs contain richer
information. We follow Bersier et al. (2002; see also Ulanowicz &
Wolff 1991) and use a series of metrics based on Shannon (1948)
information theory. To prevent repetition we introduce them when
they are used in the Results but they are largely based on the statistic
⎡
⎛x ⎞⎤
x
h( x ) = Exp ⎢−∑ i Log ⎜ i ⎟ ⎥ ,
⎝ x ⎠ ⎥⎦
⎢⎣ i x
where x is a vector of quantities such as species densities indexed by
i = 1 ... n, and x is the sum of the quantities. When all species have the
same density then h(x) reaches its maximum, which is equal to n. The
further quantity h′(x) = h(x)/n, which takes a value between 0 and 1,
is a scaled measure of evenness. We shall refer to these below as the
diversity metrics h and h′.
Results
FOOD WEBS
Quantitative food webs were constructed to describe the
interactions between aphids and their primary parasitoids in
3 years (Fig. 1), aphids and entomopathogenic fungi in 2 years
(Fig. 2) and aphids and the guild of predators specialized on
this food resource in 1 year (Fig. 3).
In drawing the webs we use the same conventions as in our
earlier work (Müller et al. 1999). Hosts are arranged as a
series of bars in a lower register with the width of each bar
proportional to the aphid’s cumulative abundance over the
year. The total host density is given in the legend below, the
units being cumulative aphids per m2 (aphids were sampled
every 2 weeks and their densities added together to get a
cumulative total). Natural enemies are arranged as a series
of bars in an upper register with again the width of each bar
being proportional to species’ cumulative abundance. The
width of the natural enemy bars are magnified relative to
those of the aphids by the factor given in the upper legend.
The predator web has been scaled to account for differences in
body size and the units of abundance are now related to biomass
rather than number of individuals. Natural enemies and
aphids are linked by triangular wedges, the relative widths of
which at the natural enemy register represent the contribution
of each aphid species to the diet or host range of the natural
enemy. All species are numbered and their identities are
provided in Table 1.
Visual comparison of the food webs in Fig. 1 shows some
support for our hypotheses. The predator food web for 1996 is
clearly much more connected than the parasitoid web of the
same year. Below we first present statistics on the annual
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 191–200
194 F. J. F. Van Veen et al.
Fig. 2. The quantitative aphid–fungal pathogen food webs
constructed in 1997 and 1998. The conventions used for drawing the
webs are described in the first section of the Results. The species
identities of the codes in the figure are given in Table 1.
Fig. 1. The quantitative aphid–parasitoid food webs constructed in
each of the 3 years of the study. The conventions used for drawing the
webs are described in the first section of the Results. The species
identities of the codes in the figure are given in Table 1.
variation in host/prey abundance and then present the
qualitative and quantitative food web statistics to compare
the natural enemy guilds.
but even after omitting D. holci there was only a weak nonsignificant correlation between abundances in the final year
and in either of the two earlier years (ρ26 = 0·13, ρ26 = 0·14,
respectively). There were greater differences in evenness
among years (Table 2) with the diversity metrics h and h′
showing relatively low diversities in years 1 and 3. We have
already mentioned that in year 3 D. holci was particularly
common, and in year 1 the thistle aphid Capitophoris carduinis
was relatively common making up 70% of all aphid individuals
recorded. If these two dominant species are omitted and
the metric h recalculated (h1 in Table 2) then all 3 years show
similar diversities.
COMPARISON OF GUILDS
HOST/PREY ABUNDANCE
Species numbers and predator–prey ratios
In the 3 years of the study the number of aphid species
recorded in the site remained approximately equal: 23–25 of a
total of 29 (Table 2). Aphid densities were approximately the
same in the first 2 years but about seven times higher in the
final year (Table 2). Part of the reason for the higher density in
1998 was the colonization of the field site by Diuraphis holci,
which became the most abundant aphid (55% of all individuals).
However, even omitting this species, abundances were about
three times higher in year 3.
The abundances of individual aphid species were highly
correlated between the first 2 years (Pearson, ρ23 = 0·85)
The results for this section are summarized in Table 3. We
recorded 24 species of parasitoid in total of which between 12
and 19 were found in any particular year. Parasitoid densities
varied, roughly in line with those of the aphids, and were
particularly high in 1998. Only five species of entomopathogenic
fungi were recorded, all but one present in both years. Pathogen
densities were considerably higher in 1998 compared with
1997. We found 13 species of specialized aphid predator in
the one year we studied this guild (Table 3). We have not
attempted to calculate an overall predator density because
of their great variation in mass. The marked unevenness in
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 191–200
Aphid natural enemies 195
Fig. 3. The quantitative aphid–predator food web constructed in
1996. The conventions used for drawing the webs are described in the
first section of the Results and are similar to the parasitoid and
pathogen webs except (i) aphids and predators are scaled by biomass
and appetite, respectively, and (ii) two versions of the predator web
are drawn assuming narrow prey range on a plant (specialist web) and
random predation ( proportional web). In both cases see the Methods
for more detail. The species identities of the codes in the figure are
given in Table 1.
natural enemy densities meant that the diversity metrics h
took values considerably lower than the species numbers. The
parasitoid figure for 1998 is strongly affected by the presence
of the common A. varipes (omitting this species increases the
value of h to 7·2).
The different numbers of species in each guild of natural
enemies are reflected in changes in the natural enemy to aphid
ratio (the equivalent of the standard predator–prey ratio)
though the differences are less marked for the ratio of the
diversity statistics (Table 3). To calculate the quantitative
predator–prey ratio we measured predator density not in
terms of individuals but of biomass (see Methods). Doing this
increases the quantitative measure of aphid diversity from 3·6
to 7·5 because larger aphids tended to be rarer than smaller
aphids.
CONNECTANCE AND COMPARTMENTALIZATION
The number of links in the seven food webs varies from 20 in
the 1996 parasitoid web to between 61 and 83 in the predator
web (depending on assumptions about predator specialization)
(Table 4). There was considerable variation between years for
the guilds we studied in more than one season. There were
fewer trophic links in 1996, the year when the least number of
parasitoid species was recorded. More surprising is the over
threefold increase in number of links involving fungal
pathogens between 1997 and 1998. As noted above, pathogens
were much more common in the second year and through a
purely sampling effect it was possible to detect many more
relatively rare associations. Also in 1998 the nettle aphid
Microlophium carnosum was the most important host of all
species of pathogens. In 1997 M. carnosum was rare, which
might account for the paucity that year of pathogenic fungi.
Variation in link densities means that the diversity metric,
h, is always considerably lower than the number of trophic
links. We checked to see if any particularly common association
had a major effect on the statistic and found that only one link
made a major difference, that between D. holci and A. varipes
in the 1998 parasitoid web – omitting this increased link
diversity to 10·25 (h′ = 0·24). In the pathogen webs the h
statistic increased between years by a factor of 1·5, much less
than the threefold increase in raw link numbers because h is
far less affected by the discovery of a few instances of rare
associations. Compared with both the parasitoid and pathogen
webs, the quantitative measure of the number of links involving
predators is high, and (see h′ in Table 4) nearer the qualitative
measure. There are thus more predator links, and they tend
to be more even. Finally note that there is relatively little
difference in the quantitative measure of link abundance in
the ‘proportional’ and ‘specialized’ predator webs. This is
reassuring as it suggests our precise assumptions about
predator behaviour will not affect the conclusions, at least
those derived from the quantitative statistics.
From the food web we can calculate the average host or
prey range of the different natural enemies. For the parasitoids
it varies from 1·5 to 2·5 between years while for the pathogens
it is 3·7 in the first year and nearly 10 in the second. For the
predator web it is 4·7 if we assume specialized feeding and 6·4
for proportional feeding. Calculating the average quantitative
measure of host range (mean h(links per host)) gives a simpler
picture: parasitoids and pathogens have relatively narrow
host ranges with equivalent host ranges between 1 and 2 while
the figure for predators is c. 3·8 and only slightly affected by
our assumption about feeding specialization.
Connectance is defined as the proportion of all possible
links that is realized. Because we only recorded host–natural
enemy associations we define connectance here as the number
of links divided by the product of host and natural enemy
numbers (Müller et al. 1999; Lewis et al. 2002). If every natural
enemy fed on every host or prey then this measure equals 1.
Adapting Bersier et al. (2002) we define the quantitative
(weighted) equivalent to be h(links) divided by aphid times
natural enemy species. This measure ranges from 0 to 1 and
reaches the maximum when every natural enemy attacks
every host or prey with equal intensity.
Connectance is low (≤ 0·1) in the parasitoid web, variable in
the pathogen web (0·16 and 0·38) while in the predator web
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 191–200
196
F. J. F. Van Veen et al.
Table 1. Identity of species in the food webs
Code
Aphid name (host plants in brackets:
for names see Appendix)
1
2
3
4
5
8
9
10
11
12
13
14
15
16
17
18
20
21
23
24
25
26
27
28
29
30
36
39
40
Capitophorus carduinis (1)
Aphis fabae cirsiiacanthoides (1, 2)
Uroleucon cirsii (1, 2)
Microlophium carnosum (3)
Aphis urticata (3)
Brachycaudus cardui (4)
Acyrthosiphon pisum (5, 6, 14)
Macrosiphum funestum (7)
Amphoraphora rubi (7)
Aphis ruborum (7)
Aphis rumicis (8)
Metopolophium albidum (9)
Sitobion spp. (avenae & fragariae) (10)
Megoura viciae (6)
Aphis spp. on Epilobium (11)
Sitobion ptericolens (12)
Aphis jacobaeae (4)
Aphis salicariae (13)
Aphis sarothamni (14)
Megourella purpurea (6)
Sitobion fragariae (on primary host) (7)
Macrosiphum euphorbiae (15, 4, 16)
Metopolophium dirhodeum (9, 17)
Diuraphis holci (18)
Hydaphis foeniculi (16)
Hyalopteroides humilis (17)
Aphis fabae (15, 19, 16)
Myzus sp. (15, 20, 21, 22, 1)
Cavariella angelica (16)
Code
Parasitoid name
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
17
19
20
23
24
25
26
29
30
Aphidius matricariae
Aphidius urticae
Aphidius microlophii
Aphidius picipes
Praon dorsale
Aphidius eadyi
Aphidius ervi
Aphidius rubi
Aphelinus abdominalis
Aphidius rhopalosiphi
Aphelinus varipes
Ephedrus plagiator
Praon volucre
Trioxys acalephae
Lysiphlebus fabarum
Praon abjectum
Ephedrus lacertosus
Aphidius funebris
Ephedrus cerasicola
Trioxys centaureae
Ephedrus niger
Trioxys pallidus
Trioxys sp. 1
Aphidius salicis
1
2
3
4
5
Pathogen name
Pandorra neoaphidis
Entomophthora planchoniana
Zoophthora phalloides
Conidiobolus obscurus
Neozygites microlophi
Code
Predator name
Family
1
2
3
6
7
8
9
11
16
19
21
22
23
Adelia bipunctata
Anthocoris nemoralis
Aphidoletes aphidimyza
Chrysoperla carnea
Coccinella septempunctata
Episyrphus balteatus
Epistrophe eligans
Eupeodes luniger
Orius sp.
Propylea quattuordecimpunctata
Scaeva pyrastri
Syrphus ribesii
Syrphus vitripennis
Coccinellidae
Anthocoridae
Cecidomyiidae
Chrysopidae
Coccinellidae
Syrphidae
Syrphidae
Syrphidae
Anthocoridae
Coccinellidae
Syrphidae
Syrphidae
Syrphidae
All Braconidae except
9 and 11, Aphelinidae
Table 2. Numbers, density and diversity of aphids in the 3 years of
the study
Number of aphid species
Total aphid density
Diversity h(aphid density)
Diversity h′(aphid density)
Diversity h1(aphid density)
Code
1996
1997
1998
23
285
3·6
0·16
9·8
23
307
8·6
0·38
8·6
25
2014
4·9
0·20
7·5
it varies between 0·20 and 0·28. However, adopting the
quantitative measure of connectance, the parasitoid web is
clearly the least connected, the pathogen web intermediate
and the predator web the most connected (Table 4). The two
different assumptions we made about predator feeding had
only a minor effect on connectance (0·10 vs. 0·09). The only
particular link having a significant strong influence was the
D. holci–A. varipes association in the 1998 parasitoid web;
without it, quantitative connectance is 0·024.
Table 3. Numbers, density and diversity of natural enemies in the years they were studied, and enemy:aphid ratios
Parasitoids
Number of species
Density of natural enemy
Diversity h(enemy density)
Diversity h′(enemy density)
Enemy:aphid ratio
h(enemy):h(aphid) density ratio
Pathogens
Predators
1996
1997
1998
1997
1998
1996
12
13
2·4
0·23
0·52
0·65
19
4
6·1
0·32
0·83
0·70
17
61
3·4
0·20
0·68
0·69
4
3
2·4
0·60
0·17
0·27
5
84
2·3
0·46
0·20
0·47
13
*
4·2
0·32
0·57
0·56
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 191–200
Aphid natural enemies 197
Table 4. Numbers and diversity of aphid–enemy trophic links, and measures of host/prey range, connectance and compartmentalization
Parasitoids
Number of links
Diversity h(links)
Diversity h′(links)
Host/prey range
h(host/prey range)
Connectance
h(Connectance)
Number of compartments
h1(compartments)
h2(compartments)
Pathogens
Predators
1996
1997
1998
1997
1998
1996P
1996S
20
2·38
0·12
1·67
1·24
0·07
0·009
3
1·89
2·17
39
8·16
0·21
2·05
1·48
0·09
0·019
1
1
1
42
3·76
0·09
2·47
1·38
0·10
0·009
5
2·35
1·99
15
2·94
0·20
3·75
1·41
0·16
0·032
1
1
1
48
4·47
0·09
9·60
1·98
0·38
0·036
1
1
1
83
30·87
0·37
6·38
3·89
0·28
0·103
1
1
1
61
27·97
0·46
4·69
3·67
0·20
0·094
1
1
1
Compartmentalization is the degree to which a food web is
divided into nonconnected subwebs. Both the pathogen and
predator webs are fully connected, as is the 1997 parasitoid
web. In 1996 one host–parasitoid association (the most
common) and in 1998 four pairs of associations (including the
two most common) were not linked to the rest of web giving
two and five compartments, respectively.
We can measure how the disparity in compartment size
affects a quantitative measure of compartmentalization by
calculating either h(species per compartment) or h(number of
associations per compartment); in Table 4 these are labelled
h1(compartments) and h2(compartments), respectively. Using
the second quantitative measure the 1996 web is now more
divided than the 1998 web.
Discussion
We predicted that the predator guild would show the highest
degree of linkage and connectedness, parasitoids the least,
and with fungal pathogens intermediate but nearer parasitoids
than predators. The food web data confirm our initial
hypothesis. The predator web contains more links than the
parasitoid or pathogen webs, the average number of aphid
species attacked per predator species tends to be greater than
the host range of parasitoids and pathogens, and predator
food web connectance tends to be higher than for the other
guilds. The exception to these trends is the pathogen web for
1998 when a large number of rare associations increases
both average host range and connectance. However, if we
adopt the quantitative measures of these two statistics, which
de-emphasizes rare and so presumably less important interactions, the data are in very good agreement with the hypothesis.
Quantitative link diversity is approximately the same for
the parasitoid and pathogen guilds, and nearly double for
predators. Quantitative connectance is highest for predators
and lowest for parasitoids, and intermediate for pathogens. In
the year that both the predator and the parasitoid web were
sampled the quantitative connectance differed by a factor
of 10.
The main motivation behind this study was to compare
the potential for apparent competition mediated by the three
guilds of aphid natural enemies. The majority of aphids
present in our community cannot compete directly because
they feed on different host plants (375 of the 406 possible pairwise aphid competition coefficients are zero for this reason).
If our community is structured by biotic interactions then
they must be mediated by processes other than resource and
interference competition. A likely route is that aphid species
on different host plants interact through shared natural enemies.
The analysis of the webs clearly shows that predators have the
greatest potential for mediating apparent competition.
While we present parasitoid data for 3 years, a weakness of
the study is that we studied the predator and pathogen guilds
for only 1 and 2 years, respectively. However, over the 3 years
the number of aphid species remained relatively constant
despite marked differences in overall aphid density. The
major difference between the 3 years was that in the first and
last years two different species of aphid were particularly
abundant. If these species are omitted then aphid diversity
(measured by the h statistic) as well as species number are
similar across years. Although this does not avoid the problem
of studying different guilds in different years it is reassuring
that interannual differences are not more pronounced. Moreover, the magnitude of the differences observed among the
webs of the different guilds, as opposed to differences among
years within guilds, strongly indicate that it is unlikely that the
observed effects were down to chance.
We conclude that indirect interactions such as apparent
competition which might structure aphid communities are
most likely to be mediated by predators. This is supported by
a series of experiments we have carried out with aphids from
this community in which we have compared the dynamics of
aphids feeding on one species of host plants in the presence or
absence of a second species of aphid feeding on a different
plant species (Müller & Godfray 1997; Rott et al. 1998; and
unpublished). We also know that some species that are absent
from our study community despite the presence of their host
plant are able to persist if protected from aphid–specialist
predators (Müller & Godfray 1999).
We have so far failed to demonstrate parasitoid-mediated
(unpublished results) or pathogen-mediated (Pope et al. 2002)
apparent competition. However, the pathogen food web
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 191–200
198
F. J. F. Van Veen et al.
Fig. 4. Quantitative overlap diagram for the
1998 fungal pathogen web. Aphid species are
represented as nodes arrayed in a circle; the
nodes are linked if they share a common
natural enemy. A statistic (dij) is calculated
that describes the probability that a natural
enemy attacking one species of aphid (i)
developed on a second species ( j). It is
assumed that the natural enemy population is
well mixed and does not consist of host races.
The width of the line connecting species i
and j at i is proportional to dij. The diameter
of the node represents aphid abundance, and
the degree to which it is coloured black di.
The species identities of the codes in the
figure are given in Table 1. The diagram
shows that species 4 (nettle aphid Microlophium
carnosum) may act as a major source of
fungal spores attacking other aphid species.
described here suggests that one species, the nettle aphid
Microlophium carnosum, may be particularly important as a
source of fungal pathogens attacking other aphid species. In
1998 when nettle aphids were abundant they were responsible
for a large proportion of the total fungal cadavers recorded.
In Fig. 4 we display the 1998 fungal food web in a different
way, as a quantitative overlap graph (Müller et al. 1999). The
figure shows the importance of M. carnosum (species ‘4’ in the
diagram): it is more strongly connected to other aphids
through shared fungal pathogens than any other species, and
it acts as a source of pathogens attacking these other species.
We predict that under meteorological conditions favouring
fungal pathogens the presence of nettle aphids will negatively
influence the population dynamics of other species feeding on
nearby host plants.
The density of pathogens between the 2 years was dramatically different with much higher densities in 1998, both in
absolute terms and relative to the aphids. Although outbreaks
(epizootics) of entomopathogenic fungi are often associated
with wet conditions we cannot attribute the low densities in
1997 to unsuitable meteorological conditions. Weather data
for the study site show that temperature, total rainfall and
number of rain days are very similar in the summers of 1997
and 1998. It is possible that the high pathogen densities in
1998 were due to the higher aphid densities, especially of
M. carnosum, which would have allowed for more efficient
transmission of the pathogens.
Food webs contain information only about the trophic
interactions in a community while populations may interact
by other means, which can affect community structure. For
example, plants responding to herbivore attack by releasing
volatile chemicals that attract parasitoids (Turlings, Tumlinson
& Lewis 1990; Guerrieri et al. 1999). Interactions among the
guilds of natural enemies may also play a role. It is known that
predators may enhance transmission of fungal pathogens,
but also interfere with pathogen and parasitoid efficacy by
consuming infected and parasitized hosts (Pell et al. 1997;
Roy et al. 1998; Roy, Pell & Alderson 2001; Baverstock,
Alderson & Pell 2005). How such trait-mediated indirect
effects affect the populations within a complex community is
still unclear but in simple experimental insect communities,
both trophic and trait-mediated interactions determine species
persistence and community structure (van Veen, van Holland
& Godfray 2005).
Phytophagous insect assemblages are some of the most
diverse ecological communities on the planet. While much
progress has been made in recent decades in understanding
the dynamics of communities structured chiefly by resource
competition (Tilman 1994; Menge 1995; Hubbell 2001)
progress has been slower in the case of plant-feeding insects.
One problem has been the difficulty in describing community
structure, and in identifying the patterns that require an
ecological explanation (if of course they exist). We hope
that the construction of quantitative food webs and related
approaches to determine systematically the structure of insect
communities (Novotny et al. 2002, 2006) may help address
this and stimulate the experimental work that will be required
to test hypotheses about the nature of the processes concerned.
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 191–200
Aphid natural enemies 199
Acknowledgements
Financial support for this project was provided by the UK Natural Environment
Research Council. A team of field assistants lead by Irma Adriaanse helped
with data collection. The predator data were collected by Richard Cooke.
Robert Belshaw assisted with parasitoid identification.
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Handling Editor: Kevin McCann
Appendix
Plant species from which aphids and natural enemies were sampled. Codes correspond to codes listed after the aphids in Table 1
Code Plant name
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
Cirsium palustre
Cirsium arvense
Urtica dioica
Senecio jacobea
Lotus uliginosus
Lathyrus pratensis
Rubus fruticosus
Rumex obtusifolius, R. crispus + hybrids
Arrhenatherum elatius (vegetative stage)
Flowering grasses: Agrostis spp., Anthoxanthum odouratum,
Arrhenatherum elatius, Dactylus glomerata, Deschampsia
cespitosa, Holcus lanatus, Holcus mollis, Poa spp.
Epilobium spp.
Pteridium aquilinum
Chamerion angustifolium
Cytisus scoparius
Galium aparine
Angelica sylvestris
Dactylus glomerata (vegetative stage)
Holcus mollis (vegetative stage)
Lysimachia vulgaris
Glechoma hederacea
Ranunculus repens
Veronica chamaedrys
© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Journal of Animal Ecology, 77, 191–200