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Journal of Animal
Ecology 2001
70, 273 – 288
Invasion of a stream food web by a new top predator
Blackwell Science, Ltd
GUY WOODWARD and ALAN G. HILDREW
School of Biological Sciences, Queen Mary University of London, London, E1 4NS, UK
Summary
1. A new top predator, the dragonfly Cordulegaster boltonii Donovan, ‘invaded’ a
stream with a well-described food web.
2. The pre-invasion web was species-poor but complex, with prevalent intraguild predation, cannibalism and omnivory. Such characteristics differ from expectations based
upon the early food web literature, but are consistent with more recent empirical webs
and theoretical developments.
3. Exhaustive sampling was necessary to describe web structure, with the gut contents
of several hundred individuals being required to reach the asymptote of the total number
of links for individual species. There was no single ‘standard’ sample size that was applicable for estimating the number of links: sampling ‘x’ guts gave a different fraction of
the asymptotic value for different species. Smaller predators were more prone to underestimation of links than larger species higher in the web.
4. The number of feeding links, trophic status and the degree of omnivory increased
progressively with predator body size, both within and among species. The diet of
each predator species (or instar) was effectively a subset of the diet of the next largest
predator.
5. The invader was extremely polyphagous and fed at all trophic levels. Mean chain
length increased by half a link following the invasion. Web complexity, and omnivory
in particular, also increased. Pre- and post-invasion webs displayed intervality and
rigid circuitry. The resident predators were frequently eaten by the invader, but the only
significant predators of C. boltonii were larger conspecifics. Although no species
have yet been deleted, there has been a 21% increase in links for a 6% increase in species
since the invasion, suggesting that the members of the web had become more tightly
packed within niche space. Most prey species were eaten by every predator species
(including C. boltonii), indicating the potential for strong apparent competition within
the web.
Key-words: connectance, intraguild predation, niche overlap, omnivory, ontogenetic
diet shifts.
Journal of Animal Ecology (2001) 70, 273–288
Introduction
Although food webs provide an important conceptual
link between population and community ecology, there
remains a shortage of well-described webs (Lawton
1989; Cohen et al. 1993; Hall & Raffaelli 1993). Most
food web theory has developed from two main sources:
a small number of ‘real’ food webs of variable quality
(see Cohen 1978; Pimm 1982; Briand 1983), and simulated webs modelled using the techniques pioneered
by May (1972, 1973). The principal predictions of these
© 2001 British
Ecological Society
Correspondence: Dr G. Woodward, IERM, University of
Edinburgh, Mayfield Road, Edinburgh, EH9 3JU, UK.
Fax: + 44 (0)131 662 0478. E-mail: [email protected]
theoreticians, apparently supported by empirical data,
were that webs would be simple and food chains short
(Pimm 1980, 1982). Complex trophic interactions, such
as omnivory (feeding at more than one trophic level),
feeding loops (e.g. species a eats species b eats species a)
and cannibalism, should be rare because they destabilize web structure (Pimm 1982; Yodzis 1984). This negative relationship between complexity and stability,
which contradicted previous ecological ideas (see
Elton 1927, 1958; MacArthur 1955), has been a central
tenet of community ecology since the early 1970s (Polis
1998).
However, such food web theory has been increasingly questioned (McCann, Hastings & Huxel 1998;
Borrvall, Ebenmann & Jonsson 2000). Several authors
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G. Woodward &
A.G. Hildrew
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273–288
have argued that the poor quality of the empirical data
(e.g. the webs presented in Cohen 1978; Briand 1983)
undermines the validity of theoretical predictions derived
from the early webs (Paine 1988; Hall & Raffaelli 1993;
Polis 1994). Notable shortcomings of many original
food webs are that they are merely subsets of larger webs,
some infer the presence of feeding links (see Cohen
1978) and most are poorly resolved taxonomically,
particularly among the lower trophic levels (Hildrew
1992). Several contain biological impossibilities, with
taxa such as crustaceans and birds being described as
basal species (see Briand 1983; Briand & Cohen 1984).
Further, some of the patterns that were reported among
these webs may simply be spurious autocorrelations
between web statistics (Bengtsson 1994). These catalogues
of webs were nevertheless used by various authors to formulate models, to compare ‘real’ webs with models, and
to analyse structural patterns among these supposedly
natural systems (reviewed by Hall & Raffaelli 1993).
Many more recent food webs, including that of our
study site Broadstone Stream (see Lancaster & Robertson
1995), bear little resemblance to their predecessors, in
that they are highly connected and therefore appear to
refute established theory. Further, supposedly destabilizing interactions such as omnivory, cannibalism,
mutual predation and long food chains now appear to
be far more common than previously thought (see
Sprules & Bowerman 1988; Warren 1989; Winemiller
1990; Martinez 1991; Polis 1991). Recent models even
suggest that complexity might enhance stability, if most
of the trophic links are weak (McCann et al. 1998;
Borrvall et al. 2000). There is increasing empirical
evidence that the majority of links within a web may
indeed be weak (e.g. Paine 1992; Raffaelli & Hall 1992,
1996).
Species’ invasions provide opportunities to study
how food webs develop and have been modelled extensively (e.g. Mithen & Lawton 1986; Law & Blackford
1992), although empirical data are scarce. Food web
assembly models predict that invasion and establishment within a system is more likely if the invader differs
from other species (e.g. Mithen & Lawton 1986). These
models support the idea that apparent competition
(sensu Holt 1977) may be a means by which the ratio
of predators to prey remains roughly constant in natural webs ( Jeffries & Lawton 1985; Mithen & Lawton
1986).
The food web of Broadstone Stream has been
‘invaded’ recently by a new top predator, the nymph of
the Golden-ringed Dragonfly, Cordulegaster boltonii
Donovan (Anisoptera: Cordulegasteridae). This community has been studied intensively since the early
1970s, and the description of the pre-invasion food web
is exceptionally detailed (Hildrew, Townsend & Hasham
1985; Lancaster & Robertson 1995). Although the
‘invading’ predator had occasionally been recorded in
Broadstone previously, it was extremely rare (< 0·1
nymphs m–2), and was frequently absent from samples.
For this reason, we refer to the population explosion as
Fig. 1. Head capsule widths of the two large resident predator species [Sialis fuliginosa and Plectrocnemia conspersa
(redrawn after Lancaster & Robertson 1995) ] within Broadstone
Stream, and the invading top predator [Cordulegaster boltonii
(redrawn after Askew 1988) ].
an invasion, rather than an irruption sensu stricto. The
invasion peaked in the summer of 1995, during which
time the abundance of C. boltonii reached 70 nymphs
m–2, an increase of nearly three orders of magnitude.
This density was comparable with those of the two
largest resident predators, the larvae of the alderfly
Sialis fuliginosa Pict. (Megaloptera: Sialidae) and the
caddis Plectrocnemia conspersa (Curtis) ( Trichoptera:
Polycentropodidae). These resident predators and the
invader are drawn to scale in Fig. 1; the marked size
differences emphasize the potential for C. boltonii to
usurp the residents at the top of the food web.
The combination of the invader and the food web in
our study was particularly fortuitous, for two reasons.
First, because the community of the acidic Broadstone
Stream is relatively species-poor it has been possible
to characterize both the structure of the food web and
species interactions in great detail over the past 25 years
(e.g. Hildrew & Townsend 1976; Hildrew et al. 1985;
Lancaster & Robertson 1995). Throughout this extensive
time-series C. boltonii is the only species to have invaded
successfully and become established. Although a few
other taxa have also ‘invaded’, they are extremely rare
and/or persist for less than one generation (e.g. the
mayfly Paraleptophlebia submarginata (Stephens) and
the caddis Rhyacophila dorsalis (Curtis)). Secondly,
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Invasion of
a food web
descriptive and experimental studies suggest that predation can have strong effects upon the Broadstone
community (see Hildrew & Townsend 1982; Lancaster,
Hildrew & Townsend 1991), although a recent mathematical model (Speirs et al. 2000) suggests that predation causes only modest reductions in equilibrial densities
of the prey. Top predators can have powerful effects
upon food web structure (e.g. McPeek 1998): a large,
voracious and polyphagous predator such as C. boltonii
clearly had the potential to alter both the architecture
and dynamics of the Broadstone food web profoundly.
Our main objective was to provide a rigorous and
well-resolved description of the post-invasion food web
and to compare its structure with the pre-invasion web.
We were able to construct both taxonomic and trophic
webs, to compare the statistics of webs of varying taxonomic resolution, and to quantify partially the web on
the basis of per capita predator impact. We then sought to
use our results to assess competing theories on food webs.
Methods
 
Broadstone Stream (51°05′N 0°03′E; 120 m above
sea-level) is a spring-fed acidic headwater (pH 4·7–6·6:
ENSIS, unpublished data) of the River Medway,
within the Ashdown Forest SSSI, a lowland heath in
Sussex (see Hildrew & Townsend 1976 for a detailed
site description). The acidity of the stream excludes
fish, resulting in an invertebrate-dominated community, most members of which are insect larvae. The preinvasion web contains 24 macroinvertebrate taxa and
11 microcrustacean taxa (Table 1) (see also Lancaster
& Robertson 1995). The trophic significance of the
soft-bodied meiofauna within the web is currently
being resolved (J. Schmid-Araya, A.L. Robertson &
A.G. Hildrew, unpublished data). Among the common
predators, there are two large species (Sialis fuliginosa
Table 1. Key to web components in Fig. 3. Predators marked with an asterisk (*) were not included in the calculation of food web
statistics, due to insufficient data (see Methods)
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273– 288
Key
Trophic level
Trophic element
a
b
c
d
e
f
g
h1
h2
h3
h4
Basal resources
Iron bacteria
Fine particulate organic matter ( FPOM)
Coarse particulate organic matter (CPOM)
Terrestrial invertebrates
Pisidium sp. ( Bivalvia)
Simulium sp. (Simuliidae)
Niphargus aquilex Schiödte (Amphipoda)
Diacyclops spp. (Cyclopoida: Cyclopinae)
Paracyclops fimbriatus Fischer (Cyclopoida: Eucyclopinae)
Eucyclops serrulatus Fischer (Cyclopoida: Cyclopinae)
Acanthocyclops vernalis Fischer (Cyclopoida: Cyclopinae)
Acanthocyclops robustus Sars (Cyclopoida: Cyclopinae)
Bryocamptus spp. ( Harpacticoida: Canthocamptidae)
Attheyella crassa (Sars) (Harpacticoida: Canthocamptidae)
Moraria brevipes (Sars) (Harpacticoida: Canthocamptidae)
Alona quadrangularis (O.F. Müller) (Cladocera: Chydoridae)
Alona rustica T.Scott (Cladocera: Chydoridae)
Ostracoda
Other microinvertebrates
Heterotrissocladius marcidus (Walker) (Chironomidae: Orthocladiinae)
Micropsectra bidentata (Goetghebuer) (Chironomidae: Chironominae)
Prodiamesa olivacea ( Meigen) (Chironomidae: Prodiamesinae)
Oligochaeta
Leuctra nigra Oliver ( Plecoptera: Leuctridae)
Nemurella pictetii Klapalek ( Plecoptera: Nemouridae)
Brillia modesta ( Meigen) (Chironomidae: Orthocladiinae)
Polypedilum albicorne ( Meigen) (Chironomidae: Chironominae)
Tipulidae
Potamophylax cingulatus (Stephens) (Trichoptera: Limnephilidae)
Macropelopia nebulosa (Meigen) (Chironomidae: Tanypodinae)
Trissopelopia longimana (Staeger) (Chironomidae: Tanypodinae)
Zavrelimyia barbatipes ( Kieffer) (Chironomidae: Tanypodinae)
Plectrocnemia conspersa (Curtis) ( Trichoptera: Polycentropodidae)
Sialis fuliginosa Pict. ( Megaloptera: Sialidae)
Cordulegaster boltonii Donovan (Anisoptera: Cordulegasteridae)
Bezzia sp. (Ceratopogonidae)
Platambus maculatus (L.) (Coleoptera: Dytiscidae)
Siphonoperla torrentium ( Pictet) ( Plecoptera: Chloroperlidae)
Pedicia sp. ( Tipulidae)
Dicranota sp. ( Tipulidae)
h5
h6
h7
h8
h9
h10
i
j
k
l
m
n
o
p
q
r
s
t
u
v
w
x
z
aa*
bb*
cc*
dd*
ee*
1° consumers
Predators
JAE497.fm Page 276 Thursday, March 29, 2001 5:24 PM
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G. Woodward &
A.G. Hildrew
and Plectrocnemia conspersa) and three small species
(the larvae of the tanypod midges Macropelopia nebulosa ( Meigen), Trissopelopia longimana (Staeger) and
Zavrelimyia barbatipes (Kieffer)) in addition to the
invader, C. boltonii. The prey assemblage is composed
largely of detritivorous stoneflies and chironomids.
Broadstone has a very restricted hyporheos, the usual
vertical extent being 5 cm (Rundle 1988). Basal resources
are dominated by allochthonous detritus, especially
coarse particulate organic matter (CPOM).
 
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273–288
Surber samples (sample-unit area 0·0625 m2; mesh
aperture 330 µm) were taken between October 1995
and April 1997, disturbing the sediment to a depth of
5 cm. Samples were preserved immediately in 5% formalin, and subsequently sorted in the laboratory. In
October 1995 the entire acidic length of the stream
(about 780 m) was sampled in 15 contiguous 50-m
reaches (with the exception of a 30-m inaccessible section), to assess the spatial extent of the invasion. Within
each reach 10 Surber sample-units were taken; six were
randomly dispersed and four from leaf-packs (i.e. total
n = 150). A 200-m section (340 – 540 m from the source)
was sampled subsequently on alternate months (with
an additional sample in May 1996) between April 1996
and April 1997, inclusive. Thirty randomly dispersed
sample-units were taken on each occasion.
The predators used for gut contents analysis were
C. boltonii (n = 614 guts), S. fuliginosa (n = 450 guts),
P. conspersa (n = 559 guts), M. nebulosa (n = 543 guts),
T. longimana (n = 1039 guts) and Z. barbatipes (n = 824
guts). Gut contents analysis was also performed on
three rarer species, the stonefly Siphonoperla torrentium
( Pictet) (n = 59 guts) and the tipulids Dicranota sp.
(n = 102 guts) and Pedicia sp. (n = 24 guts). Gut contents analysis was performed on individuals of all
macroinvertebrate predators collected in the Surber
samples on each occasion, excepting only the two pentaneurids (T. longimana and Z. barbatipes) which were
randomly subsampled in August and October 1996 when
they were extremely abundant. Subsampling reduced
processing time but, nevertheless, over 400 pentaneurid
guts were analysed in each of these 2 months. Additional gut contents data for the tanypods collected during the same period (J. Schmid-Araya, A. Robertson &
A.G. Hildrew, unpublished: M. nebulosa n = 145 guts;
T. longimana n = 310 guts; Z. barbatipes n = 340 guts)
have also been included in our analysis. To ensure sufficient data to characterize the invader’s diet, additional qualitative samples of at least 30 C. boltonii
nymphs were collected on each sampling occasion (a
total of 248 additional nymphs). Diet analysis was
performed by removing the foregut, which was then
mounted in euparal and examined at 400 × magnification. This technique was used for all predators, except the
smaller tanypods, which were mounted whole. Since
prey were ingested whole, or in large fragments, most
items could be identified to species. Prey were identified
using a combination of published keys (Appendix 1)
and reference slides of taxa collected from Broadstone.
Sampling effort was standardized in the postinvasion webs by constructing yield–effort curves (sensu
Cohen et al. 1993) for links and species; only species
that had reached an asymptote for their feeding links
were included in the calculation of food web statistics.
However, species that did not meet this criterion were
shown in the food web diagram by dashed lines. The
pre-invasion webs were based on those described by
Hildrew et al. (1985) and Lancaster & Robertson (1995).
Yield–effort curves were not available for these earlier
webs but, as sample-sizes were greater than in the
current study, we assume that asymptotes were also
reached. Links that were detected in these earlier studies, but that were omitted from the web [e.g. intraguild
predation among the tanypods (see Hildrew et al. 1985) ],
have been included in the pre-invasion webs described
here. The pre-invasion links from the tanypods to the
microcrustacea, for which no data were available, were
assumed to be the same as they were after the invasion.
This assumption is justified on the grounds that S.
fuliginosa and P. conspersa had the same links to the
microcrustacea pre- and post-invasion.
     
The pre- and post-invasion food webs compared were
qualitative ‘connectance’ webs, i.e. they depict only the
presence or absence of trophic elements and feeding
links. Because there is little seasonal variation in the
structure of the web (see Lancaster & Robertson 1995)
summary webs were constructed by pooling data from
all sampling occasions. Feeding links from the primary
consumers to the basal resources were derived from the
web of Hildrew et al. (1985) and the subsequent, more
detailed, version published by Lancaster & Robertson
(1995). Double-headed arrows in figures represent feeding cycles (mutual predation). Circular arrows indicate
cannibalism.
Both ‘taxonomic’ webs (webs 1 and 2) and ‘trophic’
webs (webs 3 and 4) were drawn ( key to taxa in Table 1).
Taxa that shared predators and food resources were
lumped in the trophic webs but separate in the taxonomic webs. In addition, the most species-rich taxonomic and the most complete trophic webs (i.e. those
including C. boltonii and the resolved microcrustacean
subset) are presented in matrix format (sensu Cohen
et al. 1993) in Table 2. The derivation of the other
webs is described in footnotes to Table 2. Two levels of
taxonomic resolution were used for each type of web.
First, the ‘macroinvertebrate’ web described by Hildrew et al. (1985) was used as the template for webs 1a
and b (taxonomic webs) and webs 3a and b (trophic
webs). Secondly, the more resolved webs, that included
the microcrustacean subset, described by Lancaster &
Robertson (1995) formed the template for webs 2a and
b (taxonomic webs) and webs 4a and b (trophic webs).
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© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273– 288
The diets of Platambus maculatus (L.) (Coleoptera;
Dytiscidae) and Bezzia sp. (Diptera; Ceratopogonidae)
could not be described from gut contents analysis because
both are suctorial predators. Three other predators not
included in the previously published webs, Siphonoperla torrentium, Dicranota sp. and Pedicia sp. were very
rare (< 1% total web abundance) and sample sizes were
too small to describe their diets accurately. The links
for these three species detected in this study, however,
are shown by dashed lines on the food web diagram.
Siphonoperla torrentium was sporadically present in the
stream previously, but was omitted from the earlier webs
due to its rarity. Dicranota and Pedicia were also found
in the stream previously but were then lumped within the
Tipulidae as primary consumers (Hildrew et al. 1985).
Because of inadequate data, the five predator taxa listed
above were not used to calculate food web statistics.
A quantitative subset of the food web was constructed
for the six predators to compare per capita intraguild
predation and evaluate trophic status. The strength of
links was calculated as the percentage of the benthic
abundance, estimated from Surber samples, of the
‘prey’ species present in the guts of an individual ‘predator’. Link strength was then arcsin transformed (into
radians) to calculate a mean value for each link across
all sampling occasions. Although previous studies have
converted the instantaneous standing crop in the guts
into consumption rates for P. conspersa (e.g. Hildrew &
Townsend 1982), this was not done here because clearance rates for the other predators were not available
and may have differed from P. conspersa. The mean
individual biomass of each predator species was calculated from length–weight regressions following measurement of individuals collected in the benthic samples
( Woodward 1999).
In the pre-invasion webs Sialis fuliginosa was treated
as the top predator (after Hildrew et al. 1985), due to
the strong asymmetry in mutual predation between it
and Plectrocnemia conspersa. (i.e. it commonly ate
P. conspersa but was rarely consumed by P. conspersa).
Consequently, the mutual predation cycle between
S. fuliginosa and P. conspersa was treated as a single
link in the calculation of omnivory and chain length.
The same method was employed for all mutual predation cycles; the carnivore with the greater per capita
consumption of the other was defined as the ‘predator’,
and the other species was treated as the ‘prey’.
Graphs of predator overlap (links joining predators
that share prey) and prey overlap (links joining prey
that share predators) graphs were constructed from the
food webs (sensu Hall & Raffaelli 1993). If these graphs
can be represented in one dimension, they are termed
interval graphs (Cohen 1978). Food webs with predator
overlap graphs that can be represented in one-dimensional
interval graphs occur more frequently than would be
expected by chance (Cohen 1978; Pimm 1982). Consequently, the presence of ‘intervality’ suggests that actual
resource use can be characterized by a single niche
dimension more often than would be the case in ran-
domly constructed webs: this appears to be supported
by the recent ‘niche model’ of food web structure developed by Williams & Martinez (2000). Predator overlap
graphs from interval webs also often possess ‘rigid circuitry’ (sensu Sugihara, Bersier & Schoenly 1997). A
circuit exists where a route can be traced between some
or all of the vertices (elements) along the links in an
overlap graph and back to its starting point. An overlap graph is defined as a rigid circuit if, for all circuits
with more than three vertices, a shorter circuit can be
traced, e.g. a to b to c to d to a can be ‘short-circuited’
by a to b to d to a. Although rigid circuits are more
common in nature than would be expected by chance,
their ecological significance is still unclear (Hall &
Raffaelli 1993; Sugihara et al. 1997).
     
Maximum food chain length was calculated as the
maximum number of trophic elements that could be
included in a food chain from a basal resource to a top
predator. Mean and modal values of all food chains
between a top predator and the basal resources were also
calculated. The ratio of predator to prey species was
calculated after Jeffries & Lawton (1985), where ‘prey’
species do not consume metazoans and ‘predators’ do.
Connectance was calculated as C = 2 L/S(S – 1)
(after Pimm 1982), where L is the number of realized
trophic links observed (excluding cannibalism) and S is
the number of trophic elements in the web. Directed
connectance (referred to as C′ henceforth) was also
calculated, as C′ = L/S 2 (after Martinez 1991); this
metric was used because it is less susceptible to variations
in web size than other derivations of connectance
(Bengtsson 1994). Web complexity (SC′max ) was calculated by including competitive links, where a food
resource was shared. Links between two species that
were both predatory and competitive were counted
only once. The mean number of links per species, d,
was calculated as L/S. Omnivory was measured in
three ways. First, the percentage of omnivores (i.e.
species or trophic elements that fed at more than one
trophic level) within the web was calculated. Secondly,
omnivory was also expressed as G/L, where G is the
number of closed omnivorous links. A closed omnivorous link was defined as a feeding path from a predator
to a prey more than one trophic level away, that could
be traced back to the predator via at least one intermediate trophic level (after Lancaster & Robertson 1995).
Consequently, G measures same-chain omnivory.
Where mutual predation loops (a eats b eats a) existed
each cycle was counted once, as a linear chain to the
predator with the greater per capita consumption of the
other predator. Cannibalistic loops were also excluded
from the calculation of G and L. By excluding mutual
predation and cannibalism, the estimates of omnivory
presented here are conservative. An ‘index of omnivory’,
Oi , was also derived, as G /number of links from all
potential omnivores. Finally, basal resources were
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G. Woodward &
A.G. Hildrew
Table 2. Food web matrices. The letters and numbers at the top of each column identify the predators, while the letters and
numbers at the left of each row identify the prey, according to the key supplied in Table 1. Two Acanthocyclops species, h4 and h4i
(Table 1), were lumped because they could not be resolved to species satisfactorily in predator guts. Zero and one indicate the
absence and presence of a feeding link, respectively. Feeding cycles and cannibalism within the matrix are indicated within
parentheses: these cycles were designated values of zero for the calculation of the food web statistics (Table 3). Only two webs are
presented, for brevity; the construction of the other webs, as derived from those presented here, is given below*
(a) Web 2b (post-invasion taxonomic web with resolved microcrustacea)
z
x
w
t
u
v
s
r
o
n
q
p
l
j
k
i
h1
h2
h3
h4
h5
h6
h7
h8
h9
h10
m
g
e
f
d
a
b
c
z
x
w
t
u
v
s r o n q p l
j
k i
h1 h2 h3 h4 h5 h6 h7 h8 h9 h10 m g e f
(1)
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0
1
0
1
1
0
0
1
1
0
0
1
1
0
0
0
(1)
(1)
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
1
1
1
0
0
1
1
0
0
0
(1)
(1)
(1)
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
0
(1)
0
(1)
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
0
1
0
1
1
0
1
1
0
0
1
1
0
1
0
0
0
(1)
(1)
(1)
1
0
1
1
1
1
1
1
1
1
1
0
0
1
0
1
1
0
1
0
1
1
1
0
1
1
0
1
0
0
0
0
0
(1)
(1)
0
0
1
1
1
1
1
1
1
1
0
0
0
1
1
1
0
1
0
1
1
0
0
1
1
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
(b) Web 4b (post-invasion trophic web with resolved microcrustacea)
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273–288
z
x
w
t
u
v
s
r
onq
p
lh10
jkif
h1
h2
h3
h4
h5
h6
h7
z
x
w
t
u
v
s
r
onq
p
lh10
jkif
h1
h2h9
h3
h4
h5
h6
h7
h8
m
g
e
(1)
1
1
1
1
1
1
1
1
1
1
1
1
0
0
1
0
1
1
(1)
(1)
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
(1)
(1)
(1)
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
0
(1)
0
(1)
1
1
1
1
1
1
1
1
0
0
0
0
1
0
1
0
0
(1)
(1)
(1)
1
0
1
1
1
1
1
0
0
1
0
1
1
0
0
0
0
0
(1)
(1)
0
0
1
1
1
1
0
0
0
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
JAE497.fm Page 279 Thursday, March 29, 2001 5:24 PM
279
Invasion of
a food web
Table 2. Continued.
h8
m
g
e
d
a
b
c
z
x
w
t
u
v
s
r
onq
p
lh10
jkif
h1
h2h9
h3
h4
h5
h6
h7
h8
m
g
e
0
1
0
0
1
0
0
0
0
1
0
0
1
0
0
0
1
1
1
1
1
0
0
0
1
1
0
0
1
0
1
0
1
1
1
0
1
0
1
0
1
1
0
0
1
0
1
0
0
0
0
0
1
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
1
1
1
0
0
0
0
0
0
1
1
0
0
0
0
0
1
1
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
1
0
0
0
0
0
0
1
1
0
*For the pre-invasion webs (webs suffixed by ‘a’ in Table 3, i.e. web 1a), rows and columns representing ‘z’ (Cordulegaster boltonii) were
excluded. In webs 1a and 1b and 3a and 3b h1–h10 were grouped as a single trophic species, ‘h’, with each predator preying upon ‘h’
included in the calculation of food web statistics, rather
than employing a restrictive analysis whereby only
consumers are considered.
Results
Yield– effort curves (Fig. 2) suggested that sampling
effort was sufficient to describe accurately the feeding
links for the six dominant predators (i.e. Cordulegaster
boltonii, Sialis fuliginosa, Plectrocnemia conspersa,
Macropelopia nebulosa, Trissopelopia longimana and
Zavrelimyia barbatipes) and the size of the web. The
three engulfing predators not previously included in
the web ( i.e. Pedicia, Dicranota and Siphonoperla torrentium) were too rare to characterize their diet and
were therefore omitted from the calculation of web statistics. The approach to the asymptote was far shallower
for links than for the cumulative number of species:
over 300 guts were required to describe C. boltonii’s
links, whereas only 30 Surber samples were needed
to detect every species in the community. Also, the
sample size needed to characterize the diet decreased
as the body-size and trophic status of predators
increased: about twice as many Z. barbatipes guts were
required to reach the asymptote than was the case for
C. boltonii.
All of the food webs, both before and after the invasion, were highly interconnected; every predator ate
virtually every prey species (Fig. 3; Tables 2 and 3). A
notable exception was Pisidium (pea mussels), which
appeared invulnerable to predation. All six dominant
predator species were cannibals, especially in their later
instars. Mutual predation also occurred in many permutations among these six species. In theory, the presence of such feeding loops precludes the calculation of
the number of trophic levels (Pimm 1980). However,
the loops within Broadstone were strongly asymmetric
and size-driven, with the larger species having much
stronger per capita effects upon the smaller species than
vice versa (Fig. 4). Consequently, the largest predator,
C. boltonii, was placed at the top of the ‘predator’ web
and Z. barbatipes, the smallest, at the base.
Table 3. Food web statistics for pre-invasion (i.e. before 1995) and post-invasion summary food webs for Broadstone Stream
Linkage complexity
Web
Taxonomic webs
1a Pre-invasion
1b Post-invasion
2a Pre-invasion
(resolved microcrustacea)
2b Post-invasion
(resolved microcrustacea)
Trophic webs
3a Pre-invasion
3b Post-invasion
4a Pre-invasion
(resolved microcrustacea)
4b Post-invasion
(resolved microcrustacea)
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273– 288
S
L
d
C
Food chain length
C′
24 109 4·5 0·39 0·19
25 128 5·1 0·43 0·21
SCm′ ax
Predation
Max Mean Mode p:p
Lp/L
Omnivory
%
G
G/L
Oi
8·4
9·0
7
8
4·91
5·33
5
6
0·43 0·71
0·50 0·76
25·0 427 3·92
28·6 851 6·65
5·27
8·51
33 146 4·4 0·28 0·13 11·9
7
4·88
5
0·22 0·72
17·2 511 3·50
4·69
34 170 5·0 0·30 0·15 12·2
8
5·38
5
0·26 0·76
20·0 967 5·69
7·27
18
19
63 3·5 0·41 0·19
76 4·0 0·44 0·21
5·3
5·7
7
8
4·73
5·23
5
5
0·36 0·71
0·40 0·76
35·7 222 3·52
40·0 448 5·89
4·63
7·34
26
97 3·7 0·30 0·14
8·6
7
4·74
5
0·31 0·74
19·2 329 3·39
4·39
27 112 4·2 0·32 0·15
8·9
8
5·31
5
0·38 0·77
22·2 587
5·24 6·60
S = number of trophic elements, L = number of links, d = links per species, C = connectance, C′ = directed connectance,
SC m′ ax = linkage density, p:p = number of predator species: number of prey species, G = number of closed omnivorous links,
Lp = number of predatory links, Oi = Index of Omnivory (G/number of links from potential omnivores). Construction of the webs
is described in Methods.
JAE497.fm Page 280 Thursday, March 29, 2001 5:24 PM
(a) Benthos
Cumulative % of taxa detected
280
G. Woodward &
A.G. Hildrew
100
50
0
0
50
100 150 200
Cumulative number of Surber samples
(b) Gut contents : dominant predators
Cumulative % of feeding links detected
100
0
0
P. conspersa
S. fuliginosa
C. boltonii
50
500
0
1000
500
1000
0
500
1000
100
50
T. longimana
M. nebulosa
0
0
500
0
1000
1000
Z. barbatipes
2000
0
1000
2000
(c) Gut contents : rare predators
100
*Dicranota sp.
*Pedicia sp.
50
0
0
75
150
0
75
150
*S. torrentium
0
75
150
Cumulative number of guts examined
Fig. 2. Yield–effort curves for trophic elements and feeding links in web 1b (see Table 3). (a) Presence of taxa detected in the
benthos (sample-unit = 0·0625 m2 quadrat). (b) Presence of feeding links for the six dominant predator species (sample-unit
= 1 gut). The arrows represent the point at which all predators overlapped in diet (i.e. where the food web became interval).
(c) Presence of feeding links for three rare predator species (sample-unit = 1 gut).
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273–288
The invader was, like the other predators, highly
polyphagous: C. boltonii preyed upon 86% of the animal
taxa in the ‘macroinvertebrate’ web (web 1b). However,
most taxa were rare in the diet and there were marked
ontogenetic shifts: Plectrocnemia conspersa, N. pictetii
and cyclopoids dominated the diet of large, medium and
small C. boltonii, respectively (Fig. 5). The diet broadened
as an individual grew, with successively larger taxa being
added, while most of the smaller taxa were retained
(Fig. 6). This expansion of diet with increasing bodysize mirrored patterns when comparing among predator species, and highlighted the presence of upper
triangularity (sensu Warren & Lawton 1987) in the web.
C. boltonii fed at every carnivorous trophic level.
This was only partially related to ontogenetic shifts in
the diet (life-history omnivory). Although small C. boltonii fed only upon the primary predators and primary
consumers, large C. boltonii fed on all trophic levels,
but were apparently unable to take some of the smaller
prey species. Omnivory increased with instar number
of C. boltonii until instar 6, after which an asymptote
appeared to be reached (Fig. 7).
Every measure of both web complexity and chain length
increased following the invasion (Table 3). Although
the magnitude of these increases varied with the statistic
measured, it was largely irrespective of the taxonomic or
trophic resolution of the web. The values for C, C′, food
chain length, Lp /L, p:p, and the percentage of omnivores
in the simpler trophic webs were broadly similar to their
counterpart taxonomic webs. However, G was sensitive
JAE497.fm Page 281 Thursday, March 29, 2001 5:24 PM
281
Invasion of
a food web
Fig. 3. The invaded Broadstone Stream food web (redrawn after Lancaster & Robertson (1995) with additional links included):
web 2b. This web represents the most highly resolved post-invasion taxonomic web.
C. boltonii
z
S. fuliginosa
M.nebulosa
x
w
P. conspersa
u
T. longimana
t
v
Z.barbatipes
Mean per capita consumption as % (arcsin transformed) of individual ‘prey’
population. Arrows indicate direction of energy flow.
0·09–0·1
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273– 288
0·03–0·049
0·07–0·89
0·01–0·029
0·05–0·069
<0·01
Fig. 4. Subset of the Broadstone Stream food web showing per capita predation among the six dominant predators (mean values
from May 1996 to April 1997). The area of each circle is proportional to log 10 mean dry weight individual–1. The direction of the
arrows indicates the direction of energy flow. The width of the arrows represents instantaneous consumption as percentage (arcsin
transformed) of the standing crop of each ‘prey’ species.
JAE497.fm Page 282 Thursday, March 29, 2001 5:24 PM
282
G. Woodward &
A.G. Hildrew
25
Cordulegaster
y = 9·95 + 9·46x; r2 = 0·67; P < 0·001
Sialis
Plectrocnemia
Platambus
Cordulegaster
10
20
Macropelopia
Sialis
Number of taxa ingested
Trissopelopia
Zavrelimyia
Ceratopogonidae
Potamophylax
Tipulidae
Nemurella
Leuctra nigra
13
Plectrocnemia
11
15
14
7
M. nebulosa
8
6
12
9
10
5
2
4
Ostracoda
Cyclopoidea
Cladocera
Oligochaeta
Harpacticoida
Simulium
5
Prodiamesa
3
1
Micropsectra
Other meiofauna
Brillia
Polypedilum
0
–0·5
Heterotrissocladius
Terrestrial
0
0·5
1
Cordulegaster median head capsule width (log10 mm) per instar
Cyclopoidea
Ostracoda
Cladocera
Harpacticoida
Other microinvertebrates
1
2
3
4
5
6
7
8
9 10 11 12 13 14
Cordulegaster boltonii instar
Fig. 5. Ontogenetic shifts in the diet of the invading top
predator, Cordulegaster boltonii. The area of each circle is
proportional to the percentage of prey items accounted for by
each prey item within a given instar of C. boltonii (excluding
the non-feeding prolarva). Data are pooled over seven
sampling occasions (n = 614 nymphs).
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273–288
to trophic grouping, being between about two-thirds and
one-half of its value in trophic webs compared with the
equivalent taxonomic webs. Despite these differences
in the total number of omnivorous links, the relative
measures of omnivory, G/L and Oi, were comparable
between trophic and taxonomic webs (Table 3). SCmax
′
in the taxonomic webs was between 1·4 and 1·6 times
greater than in the equivalent trophic webs.
Generalism was marked within the webs. For example, within the invaded ‘macroinvertebrate’ web
(web 1b) every prey species shared at least three predators with every other prey species (except Pisidium sp.,
which were not eaten), and 62% of prey were eaten by
all six predator species. Because of these high levels of
trophic similarity, predator overlap (Fig. 8) and prey
overlap ( Fig. 9) graphs from both before and after the
invasion could be collapsed into one dimension, i.e. they
were interval. Intervality was detected after analysing
the gut contents of up to 20 individuals of each predator species (arrows on Fig. 2 represent sample size of
each predator species at which intervality occurred).
The pre- and post-invasion food webs also displayed
rigid circuitry.
Fig. 6. Total number of prey taxa recorded in the guts of
Cordulegaster boltonii against median head capsule width per
instar of the predator (samples are pooled over seven
sampling occasions; n = 614 nymphs). Data labels represent
instar number. Dotted vertical lines above the trend line
denote the smallest instar of C. boltonii found with the named
prey (themselves macroinvertebrate predators) in the gut
contents. Dotted vertical lines below the trend line denote
the largest instar of C. boltonii found with the named prey
(microcrustacea /meiofauna) in the gut contents.
Discussion
Summary food webs, where links and species are added
progressively over many sampling occasions, can obscure
temporal changes, especially in strongly seasonal systems (Hall & Raffaelli 1993; Thompson & Townsend
1999). However, the generalism of the predators, the
considerable size-range of predators and prey and the
persistence of taxa throughout the year, suggested
that almost all of the links shown in the Broadstone
Stream summary web could be detected on any sampling occasion, if sampling were sufficiently exhaustive (Lancaster & Robertson 1995). This contrasts
with more temporally variable webs (cf. Warren 1989;
Closs & Lake 1994; Tavares-Cromar & Williams 1996;
Thompson & Townsend 1999).
The large sample sizes required to describe the
feeding links within the Broadstone web raises several
important points. The number of gut contents samples
needed to characterize a predator’s diet in our study
was at least one order of magnitude greater than the
sample size used in many other studies (e.g. TavaresCromar & Williams 1996; Thompson & Townsend
1999). If the characteristics of the yield–effort curves
for Broadstone are applicable to other systems, then
studies with sample sizes of less than several hundred
individuals may grossly underestimate the number of
links. The magnitude of this problem may also be
JAE497.fm Page 283 Thursday, March 29, 2001 5:24 PM
(a)
Log10 proportion of Cordulegaster’s total
omnivorous links realized per instar
283
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0
10
6
–0·5
7
8
13
11
14
9
12
5
–1
3
–1·5
2
–2
4
1
–2·5
(b)
1·5
10
Log (G/L) per instar
10 11
8
6
7
1
13
14
12
9
5
3
0·5
2
4
1
0
–0·4
–0·2
0
0·2
0·4
0·6
0·8
1
Cordulegaster median head capsule width (log10 mm) per instar
Fig. 7. (a) Omnivory within each of the 14 instars of
Cordulegaster boltonii (all samples pooled over seven
sampling occasions; n = 614 nymphs). (b) G is the number of
closed omnivorous links (see Methods) for each instar and
L is the total number of links for each instar. Data labels
represent instar number. Note logarithmic axes.
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273– 288
autocorrelated with web size, as species-rich communities often contain a greater proportion of rare species
(Tokeshi 1999) that are less likely to appear in a predator’s guts. Further, the shape of the yield–effort curves
for the Broadstone predators was species-specific,
suggesting that ‘standardizing’ effort by examining ‘x’
number of guts per species is inappropriate, as this will
give a different fraction of the asymptote value for
different species. Also, the sample size at which the
asymptote was reached decreased with trophic status in
Broadstone, despite higher predators having broader
diets. This suggested that links from intermediate
species at the lower trophic levels may be particularly
prone to underestimation. Consequently, our data suggest that there is no single arbitrary ‘standard’ for all
species in a community, and we urge caution in interpreting the structure of webs where sample sizes are
small.
When compared with most webs published in the
early literature, the complexity of the Broadstone web
is striking (cf. the webs presented in Cohen (1978) and
Briand (1983) ). However, our results agreed with those
from more recent and better-described webs (see Hall
Fig. 8. Predator overlap graphs (links join predators that
share prey). Letters correspond with species as described in
the legend to Fig. 1. (Both pre- and post-invasion overlap
graphs are interval because all predators can be placed in one
dimension. Both graphs also display rigid circuitry.)
& Raffaelli 1993; Williams & Martinez 2000). Food
chains are also long compared with the early webs and,
at a maximum, may be shown to include more than 10
links following resolution of the soft-bodied meiofauna
(J. Schmid-Araya, A.L. Robertson & A.G. Hildrew,
unpublished data). Both linkage complexity and food
chain length increased still further following the invasion
of C. boltonii.
Until very recently food web theory predicted that,
due to its supposed destabilizing effect, complexity
would be rare in natural webs (May 1973; Cohen 1978;
Pimm 1982). Freshwater webs are a conspicuous exception, in that many are relatively complex, with frequent
omnivory and feeding loops (see Hildrew et al. 1985;
Sprules & Bowerman 1988; Warren 1989; Martinez
1991; Bengtsson 1994; Lancaster & Robertson 1995).
Complex webs appear to be more widespread than
JAE497.fm Page 284 Thursday, March 29, 2001 5:24 PM
284
G. Woodward &
A.G. Hildrew
Pre-invasion
z
x
d
w
z
x
e
t
f
u
d
e
w
g
g
t
v
h
s
i
ijkf
u
Web 1a
r
q
lh
k
p
s
m
l
o
n
m
x
z
d
w
r
f
u
h
s
i
j
g
ijkf
v
m
n
Web 3b
lh
s
l
o
e
u
k
p
d
t
v
r
z
p
w
g
q
onq
x
e
t
Web 1b
v
j
Web 3a
m
r
onq
p
Post-invasion
w
x
z
d
e
t
f
u
v
g
h
Key to ‘prey’ taxa
s
r
i
j
q
k
p
o
n
m
l
d. Terrestrial invertebrates
e. Pisidium sp.
f. Simulium sp.
g. N. aquilex
h. Microcrustacea
i. Other meiofauna
j. H. marcidus
k. M.bidentata
l. P. olivaceae
m. Oligochaeta
n. L. nigra
o. N. pictetii
p. B. modesta
q. P. albicorne
r. Tipulidae
s. P. cingulatus
t. M.nebulosa
u. T. longimana
v. Z. barbatipes
w. P. conspersa
x. S. fuliginosa
z. C. boltonii
Fig. 9. Prey overlap graphs ( links join prey that share predators) for pre- and post-invasion ‘macroinvertebrate’ webs (i.e. webs 1 and
3 as described in Tables 2 and 3).Both pre- and post-invasion overlap graphs are non-interval because f and g cannot be placed
in one dimension with the other members of Graph a and g cannot be placed in Graph b. Both graphs display rigid circuitry.
© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273–288
previously thought (Hall & Raffaelli 1993; Williams &
Martinez 2000), however, and in recent years have been
described from terrestrial (Polis 1991), estuarine (Huxham, Beaney & Raffaelli 1996) and marine (Yodzis
1998) systems.
Nevertheless, omnivory within Broadstone is extreme,
even when compared with the more recently published
webs, and exceeds that of any web of which we are
aware. The two most frequently cited reasons for high
omnivory are ontogenetic dietary shifts (life-history
omnivory) and donor-controlled dynamics (DeAngelis
1975; Pimm 1982). McCann et al. (1998) and Borrvall
et al. (2000) have also demonstrated recently that
omnivory can stabilize web structure, if most links
are weak.
Insect larvae, dominant in the Broadstone community, pass through a wide size spectrum as they develop
and their diet often shifts from small to large prey. This
was only partially true for C. boltonii, however, and the
largest instars still fed at every carnivorous trophic
level and on virtually every metazoan larger than the
Harpacticoida. The diet of dragonflies is often broad
since they can take both very large and very small prey
by the use of the labial mask and the labial palps,
respectively (Corbet 1999). The other predators also
expanded their diet as they grew, by adding progressively
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© 2001 British
Ecological Society,
Journal of Animal
Ecology, 70,
273– 288
larger prey but retaining most of the smaller taxa (see
also Hildrew et al. 1985; Lancaster & Robertson 1995).
Life-history omnivory therefore had little effect upon
the total number of omnivorous links per species,
although it undoubtedly influenced linkage strength.
Although the maximum size of prey that could be handled set upper limits upon trophic status and omnivory
for the predators (Figs 3 and 5), virtually every prey
species below this ceiling was vulnerable to every predator. Consequently, the relative size of predators and
prey created upper triangularity in the web (cf. Warren
& Lawton 1987).
Because prey abundance generally increases towards
the bottom of a food web, a predator will encounter
more prey items at the lower trophic levels (assuming
an equal per capita probability of encounter). In systems
where prey are scarce, as in acid streams, it is difficult to
envisage a predator ignoring any potential prey item,
once encountered, irrespective of its trophic status.
Further, the high mobility and constant redistribution
of the Broadstone benthos (Townsend & Hildrew
1976), combined with overlapping life-histories (Lancaster & Robertson 1995), ensures that the predators
encounter a wide range of potential prey. Within the
Broadstone web, omnivory might mitigate the supposedly destabilizing effect of lengthening food chains;
although maximum chain length increased by one link,
mean chain length increased by only half a link following the invasion (Table 3).
Limited taxonomic resolution and the analysis of
subset webs, rather than whole community webs, tend
to overestimate omnivory (Hall & Raffaelli 1993).
Neither of these artefacts is applicable to the Broadstone webs, however, suggesting that the prevalence of
omnivory is a real phenomenon. Further, the detection
of omnivorous loops is a strong function of sampling
effort; over 300 guts had to be analysed to describe all
of the links for C. boltonii alone, in addition to those of
the other omnivores that it preyed upon. Consequently,
omnivory and other measures of complexity may have
been underestimated for many webs, simply due to an
inadequate sampling effort.
Donor-controlled dynamics, resulting from allochthonous inputs of detritus, have been suggested as a
possible explanation for the high omnivory within
Broadstone ( Lancaster & Robertson 1995). Although
detrital inputs may govern overall productivity, some
strong top-down effects on prey by predators are also
evident ( Hildrew 1992). For example, Plectrocnemia
conspersa can consume up to 2·8% day–1 of the standing
crop of its prey in Broadstone in the summer (Hildrew
& Townsend 1982) and can depress the abundance of
favoured prey species, such as the stonefly Nemurella
pictetii Klapalek, in enclosure/exclosure experiments
( Lancaster et al. 1991). In similar field experiments
C. boltonii depleted P. conspersa and N. pictetii strongly
in summer but had little effect in winter, or on other
taxa ( Woodward 1999). The distribution of link strength
within the Broadstone web therefore appears to be
negatively skewed; a few prey suffer strong predation,
whereas most species are largely unaffected (Lancaster
et al. 1991; Woodward 1999). Linkage strength is also
temporally skewed; the guts of most of the predators
are empty most of the time, especially outside the summer
months (Hildrew et al. 1985; Lancaster & Robertson
1995). These patterns suggest that many of the links
within the Broadstone web may be weak for most of the
time (see also Speirs et al. 2000).
Recent models, such as those developed by McCann
et al. (1998) and Borrvall et al. (2000), have challenged
early food web theory by showing that stability can be
enhanced by complexity, if most links are weak. This
phenomenon was actually pointed out by May (1972)
in his seminal modelling paper, but appears to have
been largely ignored by food web ecologists ever since.
Since weak interactions are generally unlikely to be
published (Sih et al. 1985), this may account for the
overemphasis on strong feeding links (Polis 1998).
However, a few recent studies have provided direct
empirical evidence that the majority of links within a
web may indeed be weak (e.g. Paine 1992; Raffaelli &
Hall 1992, 1996; Goldwasser & Roughgarden 1993;
Wootton 1997). Several other mechanisms that enhanced
stability in the models of McCann et al. (1998), in addition to omnivory, may also be operating within the
Broadstone web. For example, the highly interconnected predator overlap and prey overlap graphs ( Figs 7
and 8) suggested that competition among predators
(shared prey) and apparent competition among prey
(shared predators), which can stabilize web structure
(McCann et al. 1998), are prevalent within Broadstone.
However, these purported interactions have yet to be
investigated experimentally.
We have several lines of evidence that suggest that
the Broadstone web is stable. First, the only species to
have invaded and persistently proliferated within the
web over the past 25 years is C. boltonii; no other species have invaded successfully at the lower trophic
levels. The extreme generalism of the existing predators
should, theoretically, make it difficult for new prey species to invade, due to the potential for strong apparent
competition (sensu Holt 1977). A possible example
of this is provided by the mayfly Paraleptophlebia submarginata, which appears occasionally in the stream as
larvae, but in low numbers. It is highly mobile and suffers extremely strong mortality within Broadstone, due
to high encounter rate with predators, and disappears
rapidly from the prey assemblage soon after colonization (Woodward 1999). This species repeatedly colonizes the stream, but appears unable to persist. Because
the predators are extremely food-limited, with predation being constrained by encounter rate, even large
increases in prey abundance could be damped rapidly
by increased consumption (Woodward 1999; Speirs
et al. 2000). Thus, new colonists are likely to be consumed rapidly, without gaining the benefits of preyswitching when numbers are low. This might explain
the relative constancy of the Broadstone web, and
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Ecology, 70,
273–288
why the only successful invader was a top predator.
Although the web failed to resist the invasion of C. boltonii, it is only one of the many other potential colonists
that have not invaded; the large size of C. boltonii make
it less vulnerable to predation and therefore to apparent competition than other colonists. In addition, the
community is one of the most persistent among a range
of neighbouring streams, and is also resilient to disturbance (Gjerløv 1997). Enhanced stability following the
invasion of C. boltonii is also suggested by increased
damping of fluctuations in prey populations (Woodward
1999).
The high degree of overlap within the Broadstone
web resulted in intervality, the presence of which appears
to agree with the recent ‘niche model’ of Williams &
Martinez (2000). Williams & Martinez (2000) suggest
that intervality is better considered as a continuous,
rather than binary, variable because of the sensitivity
of this metric to the omission of a single link in large
complex webs. Although the presence of intervality in
our webs was not due to a sampling artefact, but was
related to the extent of generalist feeding, its existence
could be overlooked in less exhaustively sampled
webs. The lack of strong effects of taxonomic or trophic aggregation upon the food web statistics (except
omnivory) reflected the high degree of trophic equivalence in the generalist Broadstone web, a feature that
appears to be common in other insect-dominated webs
(cf. Sugihara et al. 1997).
The 21% increase in links for a 6% increase in species
following the invasion of a new top predator (Table 3,
web 3), combined with the increased ratio of predators
to prey, suggested that the species in the Broadstone
web had become more closely packed within niche
space (e.g. Warren 1995). This could lead to an intensification of both traditional and apparent competition. If coexistence is rendered less likely by trophic
similarity (e.g. Mithen & Lawton 1986) then we could
expect that either C. boltonii or P. conspersa, which
have very similar diets (Woodward 1999), will ultimately be deleted from the web. P. conspersa is also a
strongly favoured prey of C. boltonii. Further, negative
correlations between these two predators in both time
and space within Broadstone (Woodward 1999) suggest that a species deletion might eventually occur.
Increased food chain length following the invasion
was undoubtedly a consequence of the invader being
considerably bigger than the two next largest predators. It is striking that this apparently vacant trophic
level was not occupied until recently, especially as
C. boltonii populations have existed in the vicinity of
Broadstone for many years prior to the invasion, and
dragonflies are capable of colonizing over considerable
distances (Corbet 1999). The two most commonly cited
constraints upon the length of food chains are energy
flow ( Kaunzinger & Morin 1998) and dynamic stability
( Pimm & Lawton 1977; Pimm 1982). These two effects
upon food chain length may be linked, by acidity,
within Broadstone. Long chains are more likely to
persist in constant, rather than disturbed environments
(Lawton & Pimm 1978). There have been recent declines
in both press (mean acidity) and pulse (acid events; summer spates) disturbance within Broadstone ( Woodward
1999). Although a press disturbance may actually
stabilize a system by damping other potential disturbances, minimum pH (i.e. pulse disturbance) appears
to be a better predictor of stream community structure
than mean pH (Hämäläinen & Huttunen 1996). If this
is true, then the increase in food chain length might
reflect enhanced environmental stability within Broadstone. The length of food chains can also be limited by
basal productivity (Kaunzinger & Morin 1998), which
increases with pH in acid streams (Groom & Hildrew
1989). Consequently, a recent rise in the pH of Broadstone (Woodward 1999) may have permitted the
lengthening of food chains. Indeed, a decline in acidity
over large temporal (i.e. over a decade or more) and
spatial scales (i.e. over the 780 m acidified length of the
stream) within Broadstone are reflected by increases in
C. boltonii abundance (Woodward 1999).
These responses to pH might suggest that web structure might simply be determined by the direct physiological influence of acidity, rather than by any emergent
food web effects. For example, fish are commonly
excluded by acidity in streams (Brown & Sadler 1989).
However, biotic interactions can also play a role in
determining web structure, and that role can be
mediated by physicochemistry (e.g. Hildrew, Townsend
& Francis 1984). For example, C. boltonii occurs regularly in other streams with lower pH than Broadstone
(e.g. Rutt, Weatherley & Ormerod 1989), suggesting
that acidity alone was insufficient to prevent invasion
before the mid-1990s. The next largest predators,
P. conspersa and S. fuliginosa, are restricted to acid
conditions by biotic interactions (especially fish predation), rather than physiological constraints per se
(Hildrew et al. 1984; Lancaster 1988). Consequently,
we suggest that although some species are excluded
simply because of the low pH of the stream, others may
be prevented from invading by the structure of the
food web itself. Interactions between internal dynamics
(e.g. food web effects) and external factors (e.g. physicochemistry) may produce effects that are more complex than those of either influence acting alone. For
example, the deletion of fish from acid streams releases
large invertebrate predators from predation and/or competition and can, in turn, have strong effects upon the
lower trophic levels (Hildrew 1992). Further long-term
monitoring of the benthic community and experimental manipulation of the links within the Broadstone
web will provide valuable insight into the relationship
between web complexity, physiological constraints and
stability.
Acknowledgements
Financial support for this research project was provided
by a Natural Environment Research Council Studentship
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Grant to G. Woodward while studying at Queen Mary
University of London. We would like to thank the
numerous people who helped with the fieldwork, Jill
Lancaster for advice on the analysis of the food web
statistics and Jenny Schmid-Araya for providing additional gut contents data.
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