Seasonal Variation in Guild Structure of the Puget ... - Springer Link

Estuaries and Coasts (2008) 31:790–801 DOI 10.1007/s12237-008-9064-5

Seasonal Variation in Guild Structure of the Puget Sound Demersal Fish Community Jonathan C. P. Reum & Timothy E. Essington

Received: 27 November 2007 / Revised: 2 May 2008 / Accepted: 12 June 2008 / Published online: 8 July 2008 # Coastal and Estuarine Research Federation 2008

Abstract Identification of food web linkages is a major aim in ecology because it provides basic information on trophic flows and the potential for interspecific interactions. In addition, policy and restoration measures mandated to conform to ecosystem-based management principals can benefit from information on temporal and spatial variability in communitylevel interactions. Here, we analyzed guild structure of the demersal fish assemblage in Puget Sound, WA, a temperate estuarine system on the US west coast. Using diet information from 2,401 stomachs collected across three seasons (fall, winter, and summer), we identified guild membership for 21 fish species, examined seasonal guild switching, and tested for seasonal shifts in predation and for differences in the degree of diet overlap at the assemblage level. We accounted for ontogenetic variation in diet by dividing species into large (L) and small (S) size classes when appropriate. Using cluster analysis and a permutation approach, we identified seven significant guilds that were typified by predation on benthic invertebrates, pelagic invertebrates, and piscivory. Of the 18 species with more than one season of diet information, six switched guilds (Pacific sanddab L, sturgeon poacher, Pacific tomcod S, speckled sanddab, rex sole, and rock sole S). At the assemblage level, we tested for seasonal differences in prey use between seasons by performing an analysis of similarities based on Bray–Curtis diet similarities and found no significant difference. However, diet overlap was significantly higher in the summer than the fall and winter (with summer> fall>winter) indicating that diets within the assemblage converged in the summer. These results indicate that analyses of J. C. P. Reum (*) : T. E. Essington School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, WA 98195, USA e-mail: [email protected]

guild structure and diet overlap can reveal seasonal variation in community trophic structure and highlight intra-annual food web variation in the Puget Sound demersal fish community. Keywords Guild structure . Competitive interactions . Diet overlap . Food habits . Estuary . Multivariate analysis . Flatfish . Puget Sound

Introduction Estuaries support a suite of commercially important species, offer critical nursery habitats for fish, provide refuge and sustenance to migratory animals, and support local economies through the harvest of natural resources. Despite their importance, estuaries also suffer from human impacts that have the capacity to damage ecological processes that sustain resident and migrant populations (Jackson et al. 2001; Lotze et al. 2006). Alteration of habitat, regulation of riverine inputs, shoreline development, pollution, and overfishing are pervasive problems (Kennish 2002). Because of the importance of estuaries and their degradation by human use, they have become the focus of restoration efforts and the development of ecosystem-based management. These measures, however, are often limited by insufficient information on food web structure and energy flows. This observation is particularly true for Puget Sound, the second largest estuary in the USA. Declining fish stocks and loss of habitat (Musick et al. 2000; PSWQAT 2002) have spurred interest in developing recovery strategies that account for ecological processes (Palsson et al. 1998; PSP 2007). These efforts are presently hampered by a limited understanding of food web structure. In temperate systems like Puget Sound, however, consideration of food habits from only a single season or averaged across a year may provide misleading indications of the

Estuaries and Coasts (2008) 31:790–801

energetic importance of different prey groups (e.g., Greenstreet et al. 1997) or the potential for competition between community members. In recent studies, detailed seasonal surveys of food webs in a range of systems have revealed dynamic linkages (Warren 1989; Thompson and Townsend 1999; Woodward et al. 2005; Akin and Winemiller 2006), indicating that food webs constructed using diet information from a single season are unlikely to resemble food webs in other seasons. Seasonal changes in prey abundance and varying degrees of opportunistic feeding among predators can result in the temporary appearance of unique guilds or the shuffling of predators between guilds. At the assemblage level, simple feeding rules relating prey availability and competition for resources between predators predict that, during productive periods in which a few easily captured prey species are widely abundant, predator diets will converge. That is, diet overlap will increase as community members feed on a common set of abundant prey. In food-limited periods, predators will diverge in diet as they revert to more specialized feeding behavior (Pianka 1980, 1988; Farias and Jaksic 2007). One method for analyzing and summarizing complex food webs relies on the concept of guilds. Guilds by definition denote sets of species that share a similar resource such as prey (Root 1967) and are commonly used in fish diet analyses to identify major feeding groups (Garrison and Link 2000; Bulman et al. 2001; Gaskett et al. 2001). Because prey resources may be limited, identifying guild relationships provides insight into which community members have the potential for strong interspecific competition (Pianka 1980; MacNally 1983). In addition, since guild members have similar linkages within a food web, identifying guilds permits simplification of complex food webs in to tractable components which may aid studies of energy flows and ecosystem dynamics (Baird and Ulanowicz 1989; Greenstreet et al. 1997; Fulton et al. 2004). The demersal fish community constitutes one of the most diverse and abundant communities in the Puget Sound ecosystem. Despite its importance, few empirical studies have evaluated species or assemblage-level patterns in diet. Food habits information is available for a small subset of commercially and recreationally important species (Karp and Miller 1977; Simenstad 1979; Fresh et al. 1981) and information on seasonal food habits are limited (e.g., Wingert et al. 1979). To date, no studies have intensively sampled the demersal fish community in order to resolve seasonal patterns in guild variation. Within the Sound, pronounced seasonal cycles in phytoplankton and macroalgae production (Winter et al. 1975; Campbell et al. 1977) influence abundance levels of pelagic and benthic primary consumers (Strickland 1983) which may ultimately impact prey preferences among higher predators. If the fish assemblage consists of feeding generalist, we might expect substantial variation in their feeding habits in response to seasonal variation in prey abundances.

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This study was conducted to improve our understanding of food web structure among the demersal fish community. Our primary rationale was to provide the first comprehensive, synoptic analysis of feeding habits of this fish community as part of a larger effort to develop tools to aid ecosystemmanagement. Our second objective was to evaluate seasonal variation in trophic structure as measured by guild structure. Specifically, we examined seasonal switching between guilds by individual species, tested for assemblage-level seasonal shifts in diet and assessed patterns of dietary convergence between seasons.

Methods Data Collection We collected demersal fish in a depth-stratified trawl survey conducted in October 2004 and March and July 2005. Stations were haphazardly selected to provide broad geographic coverage along the eastern side of the central basin of Puget Sound (the largest of five basins; Fig. 1). At each station, individual sample sites were located at 20, 40, 80, and 160 m. All trawls were performed using a 400-mesh Eastern otter trawl lined with 3.2 cm mesh in the codend and with a head rope and foot rope of 21.4 and 28.7 m, respectively. 122°40'0"W

122°20'0"W

47°50'0"N

1

47°50'0"N

Edmonds

2 3 47°40'0"N

47°40'0"N

4

Elliot Bay

5 47°30'0"N

N

47°30'0"N

6 Kilometers 0212.5 5 50

122°40'0"W 122°30'0"W 122°20'0"W Fig. 1 Survey map of trawl stations in Puget Sound, WA. Contour lines delineate the 20, 40, 80, and 160 m isobaths. In the fall, trawls were performed at stations 1–4, in the winter at stations 1–6, and in the summer at stations 1–3, 5, and 6

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Trawl tow distances ranged from 200 to 500 m. In our initial survey in October 2004, we visited four stations located between Elliot Bay and Edmonds (Fig. 1). At each station, we selected sites at each of the four depths. In March, we chose to increase the spatial extent of the survey by visiting two additional stations and only sampling sites within each station at 40 and 160 m. Finally, in July 2005, we selected five stations that included three of the stations sampled during October and the two additional stations sampled in March. At each station, we sampled sites at four depths. Thus, the depth and breadth of the survey was adjusted in an iterative fashion as we analyzed the data, but preserved overlapping coverage between subsequent surveys. This adaptive sampling design was necessary because of constraints on boat and crew time and because of the absence of prior data upon which we could base our study design. For each sampling site, stomachs of large fish (>15 cm) were dissected, checked for fullness and if they held contents were frozen or preserved in 80% ethanol for sorting in lab. Fish smaller than 15 cm were frozen whole and later dissected in lab. Diets Stomach contents were identified to the lowest taxon possible and weighed. For statistical analyses, prey taxa were aggregated into functional groups that reflected similar habitat preferences, body size ranges, and susceptibility to predation. We categorized prey into seven functional groups including an unknown prey category: zooplankton, polychaetes, bivalves, pelagic invertebrates (nekton), small mobile benthic invertebrates (1 cm wide), and sedentary benthic invertebrates. Details of the taxonomic composition of each functional group are presented in Table 1. Functional prey group wet weight was standardized to percent of total diet wet weight for each individual sampled. To maximize the amount of diet information, we assumed that unidentifiable stomach contents consisted of prey proportional to the weight of the known prey categories and subsequently prorated the unknown diet proportion across the remaining prey categories. To account for possible ontogenetic changes in diet, species with abundant small size classes were divided into body size categories. Fish 30% were categorized as large. Statistical Analysis Preliminary analysis showed large variance in diet composition between and within stations for each season so stomachs from each species/size category were averaged. This precluded analyses of spatial patterns in diet, but did permit seasonal diet comparisons. We only included in the analysis those species/size categories for which we had at least ten non-

Estuaries and Coasts (2008) 31:790–801 Table 1 Taxonomic composition of functional prey groups used in cluster analysis Functional group

Prey taxonomy

Small mobile benthos

Brachyura (1 cm wide), Octopoda Gastropoda, Echinodermata, Echiura Polychaeta Bivalvia Amphipoda, Copepoda, Euphausiidae, Isopoda, Heterpoda Caridae, Hippolytidae, Mysidae, Pandalidae, Pasiphaeidae, Sergestidae, Teuthoidea Pisces, Clupeidea, Gadidae, Embioticidae, Plueronectidae, Salmonidae Crustaceans, invertebrates

Large mobile benthos Sedentary benthos Polychaetes Bivalves Zooplankton Pelagic invertebrates

Fish

Unknown invertebrates

empty stomachs, though most had >30 stomachs. One exception was made for large spiny dogfish in the fall for which we had nine non-empty stomachs. This exception was made because this species is particularly abundant and known to exhibit heavy piscivory (Tanasichuk et al. 1991). The ecological significance of this fish outweighed concerns of potential sampling error associated with the small sample size, though caution was taken in diet interpretation. We examined community guild structure and seasonal guild switching using a cluster analysis approach. First, diet overlap was determined using the Bray–Curtis (B–C) similarity index (Bray and Curtis 1957). This similarity measure takes in to account both the number of shared prey groups and their relative abundance in each diet comparison. The similarity value ranges from 0% (no shared species) to 100% (all prey species are shared and consumed in the same proportion) with intermediate values indicating the degree of partial diet overlap. Prey groups that are mutually absent from two diets (double zeros in abundance) are excluded from the similarity calculation. This is desirable because joint absences may simply reflect different sampling intensities and may not necessarily relate a shared negative feeding preference (Legendre and Legendre 1998; Clarke et al. 2006). The resulting B–C similarity matrix which included species/size categories from all seasons was submitted to a clustering algorithm employing group averaging. The resulting dendrogram was depicted to visually inspect patterns in diet overlap. To objectively identify sets of species that possess statistically similar diets (i.e., share guild membership) we used the similarity profile test routine (SIMPROF; Clarke and Gorley 2005) which relies on a diet permutation approach. Although permutation techniques for identifying significant guild


structure have been developed and implemented in previous studies (Jaksic and Medel 1990; Winemiller and Pianka 1990; Garrison and Link 2000), the approach used here is relatively new and therefore we outline the conceptual basis of the test. Briefly, SIMPROF is a permutation test of the null hypothesis that a specified set of samples do not differ from each other in multivariate structure. In this case, we tested whether diet as described by the seven functional prey categories differed between species. At each successive split in the dendrogram, the null hypothesis of no internal structure (i.e., no discrete guilds) was tested by comparing a test statistic that related the area under the curve generated by plotting the rank of the B–C similarities (from smallest to largest) against their ordered B–C similarity values (the similarity profile) to a null distribution of test statistics obtained by randomly permuting the underlying diet matrix. A significant result (P0.3 between the original prey proportion values and the final ordination axes) were depicted alongside the species ordination (Tabachnick and Fidell 1996). NMDS was performed using the R statistical package “vegan”.

Results A total of 6,768 stomachs were collected and 2,401 had identifiable contents. All seasons combined, we obtained diet information from seven pleuronectids, two bothids, four scorpaeniforms, two gadids, one chaemerid, one clupeid, one embiotocid, one rajid, one squalid, and one zoarcid. Diet samples from both large (>30% of maximum total length) and small (30% of the maximum total length and therefore were not divided into size categories. For the

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fall, winter, and summer, 22, 13, and 20 species/size categories, respectively, had sufficient sample sizes to be included in the analyses (Table 2). In the winter, five species/size categories that were abundant in the fall were rare in the winter (Pacific tomcod, spiny dogfish, staghorn sculpin, and walleye pollock L and S) and we found no prey items in stomachs belonging to three other species (longnose skate L, Pacific herring, Pacific sanddab S, shiner perch, and slender sole). However, sand sole was common in the winter, resulting in nine fewer species/size categories as compared to fall (Table 2). For the summer relative to fall, Pacific sanddab S, rock sole, and staghorn sculpin were rare in the survey and no stomach contents were found for Shiner perch, but blacktip poachers, bluespotted poachers, and blackbelly eelpouts were more numerous (Table 2). Cluster analysis and tests for significant guild structure provided evidence for seven different guilds with distinct diet compositions (Fig. 2). Each guild contained species with diet similarities ranging from ~45% to 90% with an average withinguild diet similarity ranging from 65% to 81% (Table 3). Predation on polychaetes and bivalves was common in the fish community and subsequently dominated the diets of three different guilds but with varying proportions (Table 3, Fig. 3). For the bivalve/polychaete feeders (BP), polychaete/ bivalve feeders (PB), and polychaete feeders (PF) guilds,

members consisted solely of small-mouthed flatfishes (English sole, rock sole, C-O sole, Dover sole L and S, speckled sanddab, and rex sole) from all seasons. PF was the largest guild (11 species/size classes), followed by PB (5) and BP (5). The remaining guilds consisted of small mobile benthic feeders (SMB), zooplankton feeders (ZF), pelagic invertebrate/ small mobile benthic feeders (PelSMB), and piscivores (PIF; Table 3). The largest guild, ZF (14 species/size categories), was comprised largely of diets from the fall and summer (Pacific sanddab S, three species of poacher, shiner perch, and Pacific herring), but included winter walleye pollock S and rock sole S (Fig. 2). The remaining guilds contained 12 (PelSMB), five (PIF), and three (SMB) members. Longnose skates, gadids, and two species of flatfish (rock sole S, Pacific sanddab L) primarily from fall and summer comprised the PelSMB guild (Fig. 2, Table 3). Spiny dogfish from the fall and summer and staghorn sculpin and large-mouthed flatfishes (Pacific sanddab L, sand sole) from the winter comprised PIF. SMR was comprised of summer rex sole and fall and winter sturgeon poacher. Of the 18 species/size categories that were sampled in two or three seasons, six changed guilds: Pacific sanddab L, Pacific tomcod S, rex sole, rock sole S, speckled sanddab, and sturgeon poacher (Table 4). There was no common pattern in guild switching among species/size categories that changed guild.

Table 2 Counts of stomachs with (without) identifiable prey for each season. L, large body size class; S, small body size class Common name

Scientific name

Fall

Winter

Summer

Blackbelly eelpout Blacktip poacher Bluespotted poacher C-O sole Dover sole L Dover sole S English sole Longnose skate L Longnose skate S Pacific herring Pacific sanddab L Pacific sanddab S Pacific tomcod Spotted ratfish Rex sole Rock sole L Rock sole S Sand sole Shiner perch Slender sole Speckled sanddab Spiny dogfish Staghorn sculpin Sturgeon poacher Walleye pollock L Walleye pollock S

Lycodes pacificus Xeneretmus latifrons Xeneretmus triacanthus Pleuronichthys coenosus Microstomus pacificus

0 (3) 0 (5) 0 (0) 22 (99) 26 (22) 13(24) 176 (477) 12 (16) 29 (0) 35 (169) 122 (258) 10 (0) 36 (159) 56 (285) 81 (160) 120 (187) 10 (0) 0 (2) 91 (436) 36 (74) 15 (150) 9 (63) 39 (15) 10 (37) 38 (0) 10 (183)

0 0 0 31 10 0 49 0 11 0 32 0 0 37 20 65 27 18 0 0 36 0 0 10 10 0

29 (10) 50 (9) 38 (1) 14 (18) 70 (109) 0(0) 77 (230) 10 (40) 26 (0) 24 (21) 51 (149) 0 (0) 23 (42) 20 (199) 19 (32) 82 (143) 0 (0) 0 (5) 0 (74) 43 (118) 10 (24) 33 (127) 0 (3) 22 (23) 19 (0) 18 (49)

Parophrys vetula Raja rhina Raja rhina Clupea harengus pallasi Citharichthys sordidus Microgadus proximus Hydrolagus colliei Glyptocephalus zachirus Lepidopsetta bilineata Psettichthys melanostictus Cymatogaster aggregate Lyopsetta exilis Citharichthys stigmaeus Squalus acanthias Leptocottus armatus Podothecus acipenserinus Theragra chlacogramma

(0) (0) (0) (147) (10) (0) (159) (19) (0) (45) (96) (0) (18) (216) (13) (108) (7) (21) (148) (35) (95) (2) (8) (6) (0) (9)


795

Fig. 2 Guild structure of the demersal fish community in Puget Sound. Diets for fish from each season are included in the dendrogram. Season codes precede species name: F, fall; W, winter; S, summer. Where applicable, body size proceeds species name: L, large; S, small

S Slender sole F Pacific tomcod S F Slender sole S Walleye pollock L S Speckled sanddab Group g S Longnose skate L Pelagic inverts/ F Longnose skate S Sm mobile benthos feeders S Longnose skate S (PelSMB) W Longnose skate S F Walleye pollock L F Longnose skate L S Pacific sanddab L S Rex sole Group f W Sturgeon poacher Sm mobile benthos (SMB) F Sturgeon poacher S Bluespotted poacher F Shiner perch F Pacific sanddab S S Pacific herring W Walleye pollock S S Blackbelly eelpout W Rock sole S Group e F Walleye pollock S Zooplankton feeders (ZF) F Pacific herring S Pacific tomcod S S Walleye pollock S F Pacific sanddab L S Sturgeon poacher S Blacktip poacher F Speckled sanddab F Dover sole S S C-O sole F C-O sole W Rex sole Group d F Rex sole Polychaetes feeders (PF) F Dover sole S W C-O sole F Dover sole L S Dover sole L W Speckled sanddab S Ratfish F Ratfish Group c W English Sole Bivalves/Polycheates feeders (BP) F Rock sole S W Ratfish S Rock sole L S English sole Group b F English sole Polycheates/Bivalves feeders (PB) W Rock sole L F Rock sole L W Pacific Sanddab L F Staghorn sculpin Group a F Spiny dogfish Piscivores (PIF) S Spiny dogfish W Sand sole 0

20

40 60 Similarity

To test for assemblage-level differences in diet between seasons, we focused on a subset of 11 species for which we had diet information in all three seasons. Ordination of diets produced a configuration that clumped guild members together well, but did not reveal a discernable community shift in predation between seasons (Fig. 4). Tests for differences in average similarity between seasons supported this observation, indicating no significant differences (one-way ANOSIM, R=−0.041, P=0.875). Tests for assemblage-level differences in diet overlap, however, indicated significant differences between seasons (one-way ANOVA, df=2, 30; F=20.32, Pfall>summer. These results indicate that summertime convergence in diet is detectable at the assemblage level. For example, C-O sole, Dover sole, English sole, and longnose skate S remained in the same guilds for each season, but summer diets were closer to the ordination centroid indicating increased prey diversity and greater overlap in diet with the remainder of the community (Fig. 4). For fish that changed guilds between seasons, diets in the winter were less diverse (Fig. 5).

Discussion The main findings from our work indicate that one third of the species/size classes that we examined switched guilds between two or three seasons. Furthermore, based on seasonal patterns in diet overlap, diets tended to converge during the productive summer and diverge in the less productive winter. This demonstration of seasonal convergence in diet in a temperate demersal fish assemblage corroborates theoretical Fig. 3 Prey composition for each guild

Ave. proportion

% Contribution to guild similarity

0.74 0.09 0.41 0.33 0.57 0.17 0.67 0.08 0.61 0.09 0.68 0.07 0.54 0.19

85.1 7.1 45.6 37.8 69.4 17.5 85.0 5.7 84.6 8.6 96.9 1.7 67.5 20.2

expectations and empirical examples from terrestrial communities (Pianka 1988). Our work also highlights the need to quantify community diets on ecologically meaningful time scales such as seasons in order to properly characterize guild structure and system energy flows. The guilds identified in the Puget Sound demersal fish community were broadly classified as pelagic (ZF), benthic (BP, PB, PF, SMB), benthic and pelagic (PelSMB), and piscivorous (PI). In a global survey of resource partitioning in marine fishes, Ross (1986) noted similar major gradients in prey preference and attributed these gradients to habitat differences among predators and gape limitation. Depending on whether fish were associated with the seafloor or water column, diets reflected invertebrates from the predator’s respective habitat. Consumption of fish, he noted, was constrained largely by gape limitation. In Puget Sound, fish assigned to benthic guilds were nearly all flatfishes but did include spotted ratfish, a species known to associate primarily with benthic habitat. The diversity of species that comprised the pelagic guilds was greater, representing seven different families, all of which had varying degrees of association with benthic and pelagic habitat. For example, bluespotted poacher

100%

Fish Lg mobile benthos

75%

Pelagic inverts Sedentary benthos Bivalve Zooplankton Sm mobile Polychaetes

50% 25% 0%

PF

PIF

PB

BP

ZF

SMB PelSMB


797

Table 4 Guild membership of species for each season (for abbreviations see Fig. 2) Species

Fall

Winter

Summer

Blackbelly eelpout Blacktip poacher Bluespotted poacher C-O sole Dover sole L Dover sole S English sole Longnose skate L Longnose skate S Pacific herring Pacific sanddab L Pacific sanddab S Pacific tomcod S Ratfish Rex sole Rock sole L Rock sole S Sand sole Shiner perch Slender sole Speckled sanddab Spiny dogfish Staghorn sculpin Sturgeon poacher Walleye pollock L Walleye pollock S

Rare Empty Absent PF PF PF PB PelSMB PelSMB ZF ZF ZF PelSMB BP PF PB BP Rare ZF PelSMB PF PIF PIF SMB PelSMB ZF

Absent Absent Absent PF PF Empty BP Empty PelSMB Empty PIF Empty Rare BP PF PB ZF PIF Empty Empty PF Rare Rare SMB Rare ZF

ZF ZF ZF PF PF Empty PB PelSMB PelSMB ZF PelSMB Rare ZF BP SMB PB Rare Rare Empty PelSMB PelSMB PIF Rare ZF PelSMB ZF

Change

No change

X X X X X X X X X X X X

X X X X X X

In cases in which the number of diet samples were insufficient to determine guild membership, the reason is noted (absent, no individuals were captured in the survey; rare, less than 20 individuals were captured; empty, >20 individuals were caught, but stomachs held no contents)

is considered to be associated with the seafloor while Pacific tomcod S and Pacific herring forage higher in the water column. An important reason for assessing guild membership within a community is that it can identify sets of species 11

1

2 1 7 7

3

8 3 88

10

9

9 2

5 11

PB

5

PI 6

Sedentary benthos

9 PelSMB

Fish

4

5 10

7 BP

Zooplankton

ZF

3 6 6

Polychaetes

11

PF 2 1

which may potentially interact. Intra-guild competition is often assumed to be stronger than interguild competition because of increased overlap in resource use (Pianka 1980). If omnivory is common, however, competition between any pair of predators may be weak. In Puget Sound, guilds

4 4

SMB

Pelagic inverts

Bivalve Sm mobile benthos

10

Fig. 4 a NMDS ordination plot (left) depicting Bray–Curtis diet similarity (stress 12.9). b Vector loadings (right) indicating gradients in ordinate space for each prey group. Triangle, fall; circle, winter; square, summer. For (a), species codes are: 1, C-O sole; 2, Dover sole;

3, English sole; 4, longnose skate S; 5, Pacific sanddab (large); 6, spotted ratfish; 7, rex sole L; 8, rock sole L; 9, speckled sanddab; 10, sturgeon poacher; 11, walleye pollock S. Prey categories with strong loadings (r>0.3) are depicted in (b)

798


Fall

Winter

Summer

Fig. 5 NMDS of Bray–Curtis diet similarities (identical to Fig. 2) with convex hulls demarcating diet dispersion in ordinate space for each season. Dispersion in winter>fall>summer

identified species with shared prey items but predation on two or more functional groups was common throughout the fish community. The diversity of prey functional groups in diets suggests that the potential for competitive interactions, even within guilds, is minor. Our results are similar to conclusions from other temperate fish community diet studies (Garrison and Link 2000; Bulman et al. 2001) and agrees with the notion that competitive interactions in marine communities are diffuse due to pervasive omnivory and prey switching (Jennings and Kaiser 1998). However, to fully characterize the impact of competitive interactions between guild members in the Puget Sound fish community detailed manipulative experiments are required (MacNally 1983), a task which is logistically challenging. Seasonal convergence in diet during periods of abundant prey has been noted in other communities (Pianka 1980; Farias and Jaksic 2007) and suggests opportunistic feeding during periods of abundant prey. Because quantitative sampling of the vast number of pelagic and benthic prey species in the Sound was impractical, we assume that seasonal trends observed in past studies (Winter et al. 1975; Campbell et al. 1977; Miller et al. 1983; Strickland 1983) are similar to present day conditions. Namely, that summer coincides with the highest rates of primary production, zooplankton abundance and benthic invertebrate production while lower abundances of most primary consumers are observed in the fall followed by winter. As expected, diets converged in the summer and diverged in the winter, with fall showing intermediate levels of dispersion. Examination of diets from individual species indicates that fish such as English sole, C-O sole, rock sole, Dover sole, and speckled sanddab, which fed primarily on benthic prey in the winter, increased consumption of pelagic prey in the summer. Correspondingly, fishes that fed largely

on pelagic prey (sturgeon poacher, Pacific sanddab) increased consumption of benthic prey, leading to increased dietary overlap at the assemblage level in the summer. In marine fish communities piscivory can be an important source of mortality and typically constitutes a substantial energy pathway (Jennings and Kaiser 1998; Hall 1999). Within Puget Sound, significant piscivory (>10% of diet) was restricted to a small number of species and the intensity of piscivory varied drastically between seasons. Spiny dogfish were the largest and most abundant piscivores but were only present in the survey during the fall and summer. Sand sole were piscivorous but were captured solely in winter. For the non-migratory Pacific sanddab, piscivory was highest in the winter and less important in the fall and summer. Unfortunately, limited sample sizes and difficulty in identifying stomach contents precluded estimation of mortality due to piscivory on specific prey populations. In addition, because several well-known piscivores (six-gill shark, Pacific hake, lingcod, and various rockfishes and salmonids) were not adequately sampled by our survey, it is difficult to compare the magnitude of piscivory in the Puget Sound fish community with other estuarine assemblages. Despite these limitations, piscivory appears to vary with season indicating temporally varying mortality rates for prey populations. In coastal marine systems, the importance of benthic and pelagic energy sources to sustaining fish biomass varies widely. Detritus derived from vascular plants was identified as the dominant energy source in several shallow low-latitude estuaries (Darnell 1961; Currin et al. 1995; Schlacher and Wooldridge 1996; Akin and Winemiller 2006). In other systems, algal production played an important role (Peterson et al. 1985; Page 1997; Currin et al. 2003). In Chesapeake Bay, a large shallow estuary, detrital pathways were found to sustain sizable components of the food web (Baird and Ulanowicz 1989). Based on the assumption that benthic associated prey are primarily sustained by detrital energy pathways, diet information indicates that most of the Puget Sound fish biomass is sustained by benthic energy. Polychaetes, bivalves, and other benthos were common prey (>60% of diet) for most flatfish and ratfish which comprised ~67% of the total estimated groundfish biomass from a summer Sound-wide trawl survey (Quinnell and Schmitt 1991). For smaller segments of the fish community (gadids, longnose skates, Pacific herring, and shiner perch), species with diets dominated by pelagic prey (pelagic invertebrates, zooplankton) had a combined biomass of ~3%. The remaining fish with seasonal and intermediate dependency on pelagic resources comprised ~13% of the community biomass and ~17% of the biomass was comprised of species with unknown diets. These estimates are first order approximations but do indicate an overall reliance by the demersal fish community on benthic production, as seen elsewhere in estuaries along the US Pacific coast (Barry et al. 1996).


In the present study, we were unable to address several variables that are known to influence prey preference and may potentially impact guild classification. For example, environmental gradients structured across space and depth can lead to variability in food web structure. In Puget Sound, species richness in both intertidal and subtidal benthic invertebrate communities decline with longitude and depth (Llanso et al. 1998, Dethier and Schoch 2005) which is likely to influence fish diets. Because of limitations in sample sizes, we were unable to explore variation in space. In addition, ontogenetic shifts in diet are common in fish (Werner and Gilliam 1984) and we attempted to account for some of the ontogenetic variability by dividing samples into large (>30% of maximum total length) and small (