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JAE497.fm Page 273 Thursday, March 29, 2001 5:24 PM 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 JAE497.fm Page 274 Thursday, March 29, 2001 5:24 PM 274 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, JAE497.fm Page 275 Thursday, March 29, 2001 5:24 PM 275 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 276 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). JAE497.fm Page 277 Thursday, March 29, 2001 5:24 PM 277 Invasion of a food web © 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 JAE497.fm Page 278 Thursday, March 29, 2001 5:24 PM 278 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 Invasion of a food web 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 JAE497.fm Page 285 Thursday, March 29, 2001 5:24 PM 285 Invasion of a food web © 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 JAE497.fm Page 286 Thursday, March 29, 2001 5:24 PM 286 G. Woodward & A.G. Hildrew © 2001 British Ecological Society, Journal of Animal 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). 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