CONTENTS Introduction Methods Data Continuity Across the Time Series Summary Statistics Results Discussion Acknowledgments References Cited Appendix A List of Acronyms
NOAA Technical Memorandum NMFS-NE-159
An Overview and History of the Food Web Dynamics Program of the Northeast Fisheries Science Center,Jason S. Link and Frank P. Almeida
National Marine Fisheries Serv., Woods Hole Lab., 166 Water St., Woods Hole, MA 02543
Web version posted November 26, 2004Citation: Link JS, Almeida FP. 2000. An Overview and History of the Food Web Dynamics Program of the Northeast Fisheries Science Center, Woods Hole, Massachusetts. US Dep Commer, NOAA Tech Memo NMFS NE 159; 60 p.
Information Quality Act Compliance: In accordance with section 515 of Public Law 106-554, the Northeast Fisheries Science Center completed both technical and policy reviews for this report. These predissemination reviews are on file at the NEFSC Editorial Office.
We provide an overview of the National Marine Fisheries Service (NMFS), Northeast Fisheries Science Center (NEFSC), Food Web Dynamics Program (FWDP). The FWDP’s food habits database is one of the largest in the world and extends from 1973 to present. This database covers the entire Northeast U.S. Continental Shelf Ecosystem and has over 250,000 stomachs from more than 120 predators, with more than 1,200 different types of prey collected. We discuss the differences in sampling protocols and priorities over the history of the program, and address issues of time-series continuity. For most species, diet can be adequately characterized with an examination of 500-1,000 stomachs. The basic diet composition for 38 predators, including economically and ecologically important species, demonstrates that most members of the fish community of this ecosystem are generalists, exhibiting a broad diet as either a benthivore, planktivore, or piscivore. Many major ecosystem and multispecies issues in fisheries management can only be addressed with a knowledge derived from food habits data such as those described in this document.
INTRODUCTIONAs the history of the fishes themselves would not be complete without a thorough knowledge of their associates in the sea, especially such as prey upon them or in turn constitute their food, it was considered necessary to prosecute searching inquiries on these points....In his seminal report to Congress published in 1873, Baird called for a research program to explore five potential causes of declines in fish stocks in Southern New England waters, and thereby established the precursors to the Woods Hole scientific community and NMFS. Two of the five major causes proposed by Baird consider trophic dynamics.Spencer Baird (1873)
The research objectives of the FWDP are to: 1) assess predation mortality relative to fishing mortality for commercially important fishes; 2) mechanistically and predictively model species interactions that impact the status of these stocks, particularly critical life stages; 3) relate changes in diet to changes in population level growth rates; and 4) better understand the Northeast U.S. Continental Shelf Ecosystem. In this document, we provide a history of food web dynamics research, review the food habits data collection and analytical methods, and give an overview of the FWDP food habits database at the NEFSC.
Baird’s (1873) report was in direct response to declining fish populations in nearshore Southern New England waters. In contrast, there were consistently productive offshore fisheries for Atlantic halibut, haddock, Atlantic cod, and similar species for the next seven or eight decades. However, by the 1950s, after the halibut fishery had effectively collapsed, there were indications that haddock populations were also declining. Specific surveys were initiated in the late 1950s and were expanded in the 1960s to track these trends. Additionally, collection of basic biological information on haddock had begun in 1953 to determine the relationship between the distribution and abundance of this species and the availability of benthic fauna (USFWS 1954). Since there was already an active Benthic Ecology Program (BEP) at the Woods Hole Laboratory (Steimle et al. 1995) from Baird’s inclusive interest in all aspects of the ecosystem, and since haddock are principally benthivores, the BEP undertook examination of haddock stomachs (Table 1). From the BEP perspective, the examination of stomachs was an alternative sampling method to categorize the benthic fauna of the region. In 1963, a standardized bottom trawl survey was initiated (see “Methods” section), designed to provide quantitative abundance indices for virtually all finfish species and to concurrently collect selected biological data as was feasible. Opportunistic stomach sampling continued on these surveys until 1966.
By the late 1960s, there was a clear, documented decline in the gadid-flatfish species complex of fish. In addition, Atlantic herring began a rapid decline in the late 1960s, followed by Atlantic mackerel in the early 1970s. Given this ubiquitous decline, a multispecies management scheme was formalized in 1974 to include a two-tiered quota system; the first tier placed single species total allowable catch limits on the international fleet prosecuting fisheries in the Northwest Atlantic, while the second placed a limit on the overall multispecies catch (Hennemuth and Rockwell 1987). This approach reaffirmed the need for broad biological information from as many species as possible.
Protocols for stomach sampling during 1969-72 varied and were generally categorical due to a lack of resources. The efforts during this period identified the major trophic interactions during a time of precipitous change in the fish community, and characterized the diets of major groundfish species (Maurer 1975; Maurer and Bowman 1975; Bowman et al. 1976; Edwards and Bowman 1979; Langton and Bowman 1980; Bowman 1981).
In 1973, the Feeding Ecology Project (FEP) was formed to initiate more systematic stomach collections. In the mid- to late 1970s, the issue of recruitment became increasingly important due to a massive decline in fish biomass. At this time, Atlantic herring and Atlantic mackerel were added to the stomach sampling protocol due to their potential as larval fish predators (Jossi and Marak 1983). Two new programs were formed in response to the change in focus toward factors affecting recruitment. The Food Chain Dynamics Investigation (FCDI) was formed to extend the work of the FEP, while an Ecosystem Modeling Investigation (EMI) primarily studied the mortality of prerecruits. The need to quantify species interactions was also recognized as an important issue, and reports detailing refined and quantified characterizations of the diet for many major species were produced as a first step to address this issue (Michaels and Bowman 1982; Bowman and Michaels 1984).
In the late 1970s and early 1980s, the focus of the programs remained on attempting to link recruitment variability with predation, particularly to match predator consumption rates to observed larval fish mortalities (Grosslein et al. 1980; Sissenwine 1984; GLOBEC 1991). Additionally, attempts to model the energy and production budgets of the region, especially Georges Bank, were initiated. The emphasis on the importance of predation was extended to all life stages for more species throughout the 1980s, with continual effort given to refining estimators of diet and consumption. As the fish community continued to undergo drastic changes, studies to evaluate these patterns were also undertaken.
Through the early 1990s, an emphasis continued on the importance of predation, particularly larval mortality (Almeida et al. 1999). In the mid-1990s, the FWDP was formed to extend efforts of the FCDI and EMI, with a focus on the fish community as an entity. Trophodynamic, aggregate biomass, and multispecies modeling efforts were initiated to continue exploring the causal mechanisms responsible for the observed changes in the fish community. The current, broad focus of the FWDP is to examine all trophic aspects of ecosystem dynamics in the U.S. waters of the Northwest Atlantic.
The FWDP has two major sources of data. Both sources provide primarily stomach content information, i.e., diet composition, total and individual prey weights or volumes, and prey length. The more extensive source is the standard, multispecies, NEFSC Bottom Trawl Survey Program. These surveys were designed to monitor trends in abundance and distribution and to provide data and samples to study the biology and ecology of the fishes and invertebrates inhabiting the Northeast U.S. Continental Shelf Ecosystem. During the surveys, food habits data are collected for a variety of species.
Additionally, "process-oriented" cruises are conducted periodically to address specific questions related to the trophic dynamics of the fishes in the ecosystem. While an important component of the overall trophic dynamics research program, the data from these cruises are not included in this report. Other databases, not described in this document, encompass the prey fields of these fishes and include zooplankton, ichthyoplankton, and benthos.
The series of standardized bottom trawl surveys conducted in the Northwest Atlantic from Cape Hatteras, NC, to Nova Scotia (approximately 85,300 nm2, or 293,000 km2) is the central element in a broadscale ecological and fishery research program at the NEFSC (Figure 1). Surveys have been conducted continuously in the fall since 1963, and in the spring since 1968; seasonal surveys have also been conducted in summer and winter on an intermittent basis.
Trawl stations are selected using a stratified random design that provides unbiased estimates of a species availability to the trawl gear in relation to distribution. Strata were defined based on water depth, latitude, and historical fishing patterns. Within each stratum, stations are assigned randomly. The number of stations allotted to a stratum are in proportion to its area (approximately one station per 200 nm2, or 690 km2); however, a minimum of two stations are assigned to small strata in order to calculate their means. The surveys are conducted in depths of approximately 27-366 m; however, greater depths are occasionally sampled in the deep canyons along the continental shelf break. Once onboard, the catch is sorted and weighed (to the nearest 0.1 kg) by species, with individuals measured (to the nearest 1.0 cm) and categorized by sex and maturity stage. Subsamples of key species are eviscerated for feeding ecology and other studies. Geographic location, depth, and hydrographic data are also collected at each station. A complete description and evaluation of the Bottom Trawl Survey Program can be found in Grosslein (1969), Azarovitz (1981), and SWG/NEFC (1988).
Processing the Catch
From 1963 to 1992, all species were weighed and measured prior to biological sampling. If a species was also destined to be sampled for other biological studies (e.g., feeding ecology, age and growth, maturity staging), each individual fish processed was measured a second time. This "double measuring" invariably resulted in some inconsistent, mismatched fish lengths between the overall length frequency records for the species and the individual lengths recorded for biological samples. In addition, routine biological samples were generally collected using length categories (usually 10 cm), with sampling targets based on a 6-hr watch schedule. For example, the scientific crew were required to process 10 silver hake ranging in length from 0-10 cm, 10 ranging in length from 11-20 cm, etc., for special sampling per watch.
Beginning with the 1992 winter survey, the ondeck processing protocols were modified to: 1) eliminate "double measuring", 2) give individual identification numbers to each fish sampled for biological studies, 3) sample on a one-individual-per-one-centimeter basis, and 4) require that samples be collected at every station.
Food Habits Sampling
During 1963-66, the food habits sampling protocol required examination of a random selection of fish species from each station for at-sea prey identification and a qualitative estimate of diet composition. No criteria were set for numbers of samples to collect; the number of stomachs examined was determined by the length of time available between trawl stations and the expertise of the onboard staff (Langton et al. 1980). From 1969 to 1972, samples were collected from up to 20 (but not less than 5) stomachs from each species caught at each station. Each stomach sample was preserved by size class at sea in 10% buffered Formalin for later processing in the laboratory. Because these data have not undergone standard audit procedures and are currently unavailable in digital format, they were not used in these analyses.
Beginning in 1973, a systematic approach to collecting stomachs was initiated. The 1973-80 period was divided into two 4-yr blocks with different groups of primary demersal and pelagic species sampled during each block. (See Table 2 for an overview of stomach samples requested by species during the 1973-99 time series. Appendix A contains detailed sampling protocols and lists of species.) The survey area was divided into five broad geographic regions, and a maximum of 100 stomachs per species per cruise, with no more than 10 per station, were requested (Langton et al. 1980). In addition, from 1977 to 1980, samples from 42 other, less commonly encountered species were also requested. Individual samples were preserved at sea in 10% buffered Formalin for further processing. Prey composition (percentage), weight (0.01 g), number, total stomach weight (0.01g), and lengths (millimeters) of fish prey were determined upon examination in the laboratory. Prey identification was to the lowest taxon feasible.
In 1981, a significant change to the at-sea sampling protocol was made. While the stomachs of major species such as Atlantic cod, haddock, silver hake, yellowtail flounder, winter flounder, Atlantic herring, and Atlantic mackerel continued to be individually preserved, all other species had prey examined and identified at sea. In addition, a volumetric measurement of stomach contents (0.1 cm3) was initiated. The protocol also required sampling a specific number of fish for priority species per length class at every station (see Appendix A). Shipboard stomach processing also included percent diet composition, prey number, and prey lengths. These changes were implemented because laboratory processing of large numbers of samples proved too costly, and fish prey identification is assumed to be more accurate when stomach contents are fresh. This change in protocol placed an additional burden on seagoing staff to identify both fish and invertebrate prey while onboard ship. Many workshops were and are still conducted, and a variety of identification aids have been placed onboard ship to educate staff in the identification of prey species.
Since 1985, all stomach samples have been processed, and prey identified, at sea. Because of the time limitation at each station, from 1985 to 1991, systematic sampling focused on eight principal species: white hake, red hake, pollock, Atlantic herring, Atlantic mackerel, Atlantic cod, silver hake, and spiny dogfish (with the latter three receiving the highest priority). Eighteen other species were processed as time permitted (see Appendix A). Each of the eight principal species had target sampling levels per 6-hr watch, with an overall cap of 50 stomachs per station.
In 1992, with the implementation of new ondeck sample processing protocols (described earlier), the focus shifted from per-watch targets to per-station, length-based sampling. During 1992-93, stomach samples from 23 species were requested with maximum levels set by species and station. First priority was assigned to Atlantic cod, silver hake, spiny dogfish, and skates. In 1994, after concerns were eliminated that the per-station protocols would overwhelm the at-sea technical staff, the maxima were removed.
From 1995 to 1998, the primary objective of sampling continued to be to provide data to estimate predation on larval and juvenile stages of fish, particularly gadids, and sampling priorities were given to Atlantic cod, spiny dogfish, silver hake, Atlantic herring, and fourspot flounder, with the addition of little, winter, and thorny skates during the spring surveys.
In 1999, after an examination of data obtained during the previous surveys to determine an adequate sample size for characterizing predator diets (see "Stomach Sampling Effort Coverage" section), the sampling protocol was modified again to collect samples from a broad variety of species. While a low level of monitoring of historically priority species was maintained, the priority was shifted to commercially or ecologically important species that appeared to be undersampled in previous schemes. The sampling focus reemphasized benthivorous fishes, and attempted to be more inclusive of the entire fish community. Sample ranges (in fish length) were set for each species, generally one stomach per 5-cm length range for most species, and one stomach per 10-cm range for elasmobranchs. This protocol assumes that small per-station sample sizes over a wide range of species across many hundreds of stations will allow for adequate characterization of diets.
Once collected, whether on log sheets recorded at sea or in the laboratory, the data are entered into a computerized database (currently Oracle), audited, documented, and archived for analysis. This database is maintained on the NEFSC network computer system. In addition to the data collected from the Bottom Trawl Survey Program, data from the many special, process-oriented, cruises examining species- or life stage-specific interactions are also online, but are not included in this analysis due to their more focused nature.
DATA CONTINUITY ACROSS THE TIME SERIES
Taxonomic resolution was more detailed for invertebrate species during the earlier (pre-1981) period of the database. To correct for potential differences in the resolution of prey taxonomy between in-lab and at-sea sampling, we established four prey categories. These categories span the lowest taxonomic level feasible (often genus and species) to a very broad class- or phylum-level category (Table 3). For most analyses, invertebrate prey are grouped into order or family level, while fish prey are maintained at the lowest level feasible. If specific time periods or prey species are of interest, a lower taxonomic resolution is appropriate. However, for most purposes, a broader resolution is preferable given the differences in protocol across the time series.
In order to convert from stomach volume to stomach weight (or vice versa) to account for differences in sampling protocols across the time series, we executed a least-squares linear regression, with no intercept, to convert stomach-content data from volume (0.1 cm3) to mass (0.1 g). This regression was done using all species that had simultaneous weight and volume measurements. Both a regression for all species combined and regressions for individual major species were calculated.
A conversion factor for volume to weight of 1.1:1 was determined from simple linear regression to be the most appropriate coefficient for all predator species (Table 4). This coefficient (i.e., 1.1) is similar to those obtained from other studies (Bowman 1982; Tanasichuk et al. 1991). For those fishes that are piscivores and molluscivores (e.g., red hake and goosefish), the coefficient is slightly higher, whereas for those that are planktivores (e.g., Atlantic mackerel) and other benthivores (e.g., windowpane and fourspot flounder), the coefficient is slightly lower, reflecting the different densities of different prey items. The variation of coefficients among species does not significantly depart from the overall coefficient of 1.1.
We plotted the number of stomachs sampled versus the number of prey species observed in the diet for each species. The stomach sample size at which an asymptote was reached indicated adequate information to characterize the diet of that predator. Similar to species-area curves (Preston 1962), an asymptote indicates a low probability of revealing novel prey items with examination of additional stomachs.
The number of stomachs examined versus the number of prey items observed generally indicated that an asymptote was reached between 500 and 1,000 stomachs. Figures 2-4 show the relationships graphically. For example, we can categorize the general diets of spiny dogfish, silver hake, Atlantic cod, white hake, pollock, yellowtail flounder, winter skate, and bluefish without expecting many more additional prey items in new stomach observations (Figures 2A-F, and 3A,E). Conversely, the plots indicate that we do not have adequate sample sizes for such species as smooth skate, witch flounder, Atlantic halibut, and alewife (Figures 3B-D,F). The species that are specialists such as the planktivorous Atlantic herring and Atlantic mackerel and the benthivorous thorny skate (Figures 4A-C) generally reach an asymptote at a lower number of stomachs than do more omnivorous species such as spiny dogfish, Atlantic cod, and silver hake.
There are over 250,000 stomach records currently in the database. Predator sizes range from 1 cm to 2.5 m (Table 5). More than 120 species have been sampled, with 27 species having more than 2,000 stomachs sampled, and 42 species having more than 200 stomachs sampled. Approximately 30-40% of the stomachs examined are empty, varying across species.
Mean stomach contents generally reflect the diet composition (discussed later) and maximum size of the predator (Table 5). As a group, elasmobranchs are the largest fishes we sample, are generally piscivorous, and subsequently have the largest mean stomach contents. Exceptions include some of the skates and rays that feed primarily on benthos. Many pelagic piscivores also have large mean stomach contents. Goosefish, Atlantic cod, white hake, pollock, lumpfish, Atlantic halibut, Atlantic sturgeon, and groupers all have large mean lengths and mean stomach weights. Other than Atlantic sturgeon, most of these species are noted piscivores, particularly at the larger sizes. Conversely, the planktivores have the smallest mean stomach weights, reflecting their smaller size and zooplankton diet. Most other species have intermediate stomach weights.
There are over 500,000 prey records in the database. Prey sizes range from 0.1 mm to 1 m. There are 1,304 distinct prey items comprising 10 major taxa: arthropods, mollusks, fishes, polychaetes, echinoderms, cnidarians, poriferans, ctenophores, bryozoans, and urochords. The top 10 prey items by percentage occurrence for all predators include decapod crustaceans (principally shrimps), gammarids and other amphipods, unidentified and miscellaneous fishes (“other fishes”), unidentified and miscellaneous crustaceans (“other crustaceans”), euphausiids, polychaetes, ctenophores, cephalopods (principally squids), bivalves, and copepods (Figure 5).
Tracking the abundance of these groups can indicate major changes in ecosystem dynamics and foreshadow changes to upper trophic levels, particularly commercially valuable fishes (Christensen 1996; Jennings and Kaiser 1998). Major fish prey include northern sand lance, gadids (principally silver hake), clupeids, anchovies, and Atlantic mackerel. In addition to the large number of empty stomachs, unidentified fish, unclassified crustaceans, and well digested prey were observed most frequently in the stomachs, indicating that much of the observed prey is highly digested and difficult to identify.
Various information can be obtained from stomach content examination (Hyslop 1980; Bowen 1996; Cortes 1997) depending upon the question being addressed. Although sampling priorities shifted between species across the history of the program, most of the major species were sampled continuously over the time series (Table 2). Given the slightly different sampling protocols described previously, we treated each stomach as a random sample in one of three possible statistical designs: unweighted random, stratified, or two-stage clustered. From these food habits data, percent frequency of occurrence of prey items, total stomach contents as either volume or weight, and percent mean diet composition of prey items can be estimated for a given species.
The percent frequency of occurrence can be calculated as
where nij is the number of stomachs of predator j in which prey item i occurs, and Nj is the total number of predator j stomachs examined.
The simple, unweighted, percent mean diet composition () can be calculated as either weight or volume. For weight, it can be calculated as
where k represents an individual fish, wij is the stomach weight of prey i in predator j, and
is the total weight of all ni prey species in predator j. Percent mean diet composition may also be calculated as a ratio of means (Malvestuto 1996),
inclusive or exclusive of empty stomachs, where
Although not calculated in this document, these diet parameters can be estimated across several statistical groups or factors (s). Examples include: 1) temporal factors such as decade, year (or year blocks), season, month, or time of day; 2) spatial factors such as geographic region, stratum, or statistical area; 3) abiotic factors such as depth, sediment type, wind speed and direction, current speed and direction, temperature, or salinity; and 4) predator factors such as length, weight, age, condition factor, or sex.
A weighted mean () to estimate mean weight of prey i in predator j for statistical group s may be calculated as
where t represents an individual bottom trawl tow, Njts is the number of predator j stomachs in tow t for statistical group s, Nts is the number of tows in statistical group s, and
If one sums across all statistical groups, the weighted mean of prey i in predator j () becomes
where Ns is the number of statistical groups and Njs is the total number of predator j in statistical group s. Mean stomach weight of predator j for all prey combined () can similarly be estimated for a statistical group as
and across all statistical groups as
which, as in our case, if one evaluates all elements in a cluster such that Nts equals the total number of all tows (Nt), then EQ 12 is a direct simplification of a two-stage weighted cluster mean (Schaeffer et al. 1990). From EQ 9 and 12, a weighted mean diet composition can also be estimated for any prey i in predator j:
We principally report the simple arithmetic (unweighted mean ratio inclusive of empty stomachs, i.e., EQ 3 with statistical grouping across all factors) mean diet composition for these predators in this document. Variance estimators for each of these estimators can also be calculated, with caveats from normal, Poisson, negative binomial, gamma, lognormal, delta, or similar statistical distributions (e.g., Zar 1984; Pennington 1996; Tirasin and Jorgensen 1999). Given the central limit theorem and generally large sample sizes, we presume underlying normal distributions of the data, although a delta or delta-gamma approach is appropriate given the large number of zero values in the database.
Diet of Major Species
The two sharks regularly sampled for food habits have dissimilar diets. Spiny dogfish (Figure 6A) consume mostly pelagic prey, with clupeids, squids, scombrids, ctenophores, shrimps, and other fishes being major prey items. Smooth dogfish is a benthivore, feeding principally on decapod crabs (Figure 6B).
The skates are principally benthivores (Figure 7 and Figure 8), with amphipods, polychaetes, bivalves, and various decapods (crabs and shrimp) being major prey items. Winter skate is more piscivorous than the other skates, consuming high proportions of northern sand lance and Atlantic herring in its diet. Smooth skate is more pelagic than the other skates, consuming higher proportions of euphausiids and decapod shrimps than other prey in its diet. All skates have a relatively catholic diet.
The planktivores (e.g., Atlantic herring, Atlantic mackerel, alewife, northern sand lance, butterfish) have diets dominated by well digested prey, reflecting both their faster digestion and our difficulty in identifying smaller prey (Figure 9 and Figure 10). Copepods, euphausiids, amphipods (primarily hyperiids), mysids, and northern sand lance are the other major prey items of these fishes. Well digested prey were likely one or more of these zooplankton or small fish prey items.
Similarly, the squids have a diet that is also dominated by well digested prey, probably a result of prey mastication from the beak of these predators (Figure 11). Squids are highly cannibalistic and piscivorous.
The principal gadids Atlantic cod, haddock, and pollock are dietary generalists (Figure 12). These three species’ diets form a continuum from benthic to pelagic prey, with the haddock diet more benthic (e.g., brittle stars, polychaetes, amphipods), the cod diet in between, and pollock diet more pelagic (e.g., euphausiids, northern sand lance, decapod shrimps). Clupeids, northern sand lance, and other gadids (mainly silver hake, although there is some cannibalism) are the major fish prey of these species.
The hakes are primarily pelagic predators, consuming mainly euphausiids, clupeids, squids, decapods, and other gadids (Figure 13 and Figure 14). These species exhibit a broad diet that is principally fish and/or shrimp in composition.
The flatfishes can be largely categorized as either squid-and-fish eaters (i.e., Atlantic halibut and fourspot and summer flounders) or worm-and-amphipod eaters (i.e., windowpane and yellowtail, winter, and witch flounders) (Figure 15, Figure 16, and Figure 17). The notable exception is American plaice which primarily consumes echinoderms (Figure 15B) -- more similar to haddock (Figure 12B) than to other flatfishes. Windowpane and fourspot flounder exhibit a broad diet. The morphology of these flatfishes suggests benthic feeding, thus the high degree of piscivory exhibited by some species is noteworthy.
The other major piscivores (e.g., goosefish, weakfish, and bluefish) consume a broad variety of fishes and squids (Figure 18). Pelagic prey such as anchovies, clupeids, northern sand lance, longfin inshore squid, and gadids (principally silver hake) are the major dietary items of these predators, with weakfish consuming prey whose ranges are centered further to the south (e.g., sciaenids, butterfish), and with goosefish consuming more benthic prey (e.g., sea robins, bothids, pleuronectids, skates) than bluefish.
Scup are primarily benthivores, whereas black sea bass and Acadian redfish consume shrimp and other fishes (Figure 19). Black sea bass and scup both have a broad range of prey represented in their diets, but specialize on decapods and polychaetes, respectively.
Sea raven are benthic piscivores, consuming several different fish prey (Figure 20). Longhorn sculpin are also benthic and piscivorous, but primarily consume a broader mix of benthic invertebrates (i.e., decapod crabs, amphipods). Similar to American plaice, the ocean pout diet consists of a high proportion of echinoderms. All three of these fish exhibit a relatively broad, benthic diet.
The diet summaries presented here extend previous documentation for many of these fish species (e.g., Wigley 1956; Sherman et al. 1978; Edwards and Bowman 1979; Grosslein et al. 1980; Bowman 1981, 1983; Cohen et al. 1981, 1982; Langton 1982, 1983; Durbin et al. 1983; Bowman and Michaels 1984; Bowman et al. 1984; Hahm and Langton 1984; Overholtz et al. 1991). For further details on a particular species or species group, we refer the reader to these more specific documents. In general, we can categorize the diets of most species with more than 1,000 stomachs examined. For example, we know that Atlantic cod typically consume a wide mix of benthic invertebrates, herrings, silver hake, shrimps, and northern sand lance (Figure 12A), and that spiny dogfish typically consume ctenophores, shrimps, and smaller pelagic fishes (Figure 6A). How the diets of these species alter across seasons, location, size classes, or decades is described elsewhere, although the major diet compositions are generally consistent (Garrison and Link 2000).
Many of the species over the period of this time series have been undersampled (Table 5, Figure 3B-D,F) due to logistical constraints and changing priorities. One of the challenges is to focus on species we know little about despite their limited commercial value. For example, it would have been difficult to predict 30 yr ago that goosefish would currently be the most valuable finfish in the NMFS Northeast Region (Clark 1998), yet, fortunately, information was collected for this species. These data demonstrated the importance of this species as a piscivore. These undersampled species, as well as protocols to better address the frequency of empty stomachs and well digested prey, merit further examination.
Most species in this fish community are generalists, with a few pelagic or benthic specialists. Garrison and Link (2000) have categorized six major feeding groups, including benthivores (e.g., Figure 7, Figure 8, Figure 15B-C, and 16C), planktivores (e.g., Figure 9 and Figure 10), piscivores (e.g., Figure 18), pelagic (small fish and shrimp) feeders (e.g., Figure 13 and Figure 14), demersal invertebrate feeders (e.g., Figure 12), and crab specialists (e.g., Figure 6B). Given the broad diets, high degree of omnivory (Link 1999), and generalist feeding nature of most species in this community, most predator-prey interaction strengths are mild in this ecosystem (Link 1999; Sissenwine et al. 1982). Thus, the population-level impacts of changes in prey (potentially impacting growth) or predators (potentially impacting survivability) are likely less significant than if this were an ecosystem of specialists with strong interactions.
We have documented the changing priorities and protocols of the food habits sampling over the history of this program (Table 1 and Table 2; Appendix A). Despite these caveats, this is a unique data set to assist with understanding the ecosystem dynamics of the Northwest Atlantic. To our knowledge, there are no other data sets that span 25 yr for more than 120 species over an entire continental shelf.
The importance of the food-habits time series is enhanced given its potential role in at least partially explaining the notable dynamic nature of the Northwest Atlantic fish community (Mayo et al. 1992; Boreman et al. 1997; Clark 1998; Fogarty and Murawski 1998). Briefly, in the past 30-40 yr, the abundance of commercially desirable gadids (e.g., Atlantic cod and haddock) and flatfishes (e.g., yellowtail flounder) has declined, with a concurrent increase in the abundance of less desirable elasmobranchs (e.g., spiny dogfish and skates) and small pelagic species (e.g., Atlantic herring and Atlantic mackerel). These changes were caused primarily by a significant increase in fishing pressure exerted on gadids and flatfishes beginning in the early 1960s with the arrival of distant-water fleets. Even with the foreign fleets largely displaced from the U.S. Exclusive Economic Zone in 1977, effective effort on the fish stocks has remained high, and for many species, stock biomass dropped to historically low levels in the 1990s due to the increased capacity and efficiency of the domestic fleet (Clark 1998; Fogarty and Murawski 1998). These phenomena are not limited to just this ecosystem; other ecosystems around the world exhibit similar patterns (NRC 1999). There is high heuristic value in exploring from a trophic ecology perspective why the multispecies trajectory proceeded as it did in this ecosystem, particularly to assess how the multispecies trajectory may proceed in the future.
Professor Baird’s (1873) concerns remain appropriate, and are still relevant to ongoing ecosystem investigations (e.g., Sherman 1991; Sherman et al. 1993; Christensen et al. 1996; Larkin 1996; Jennings and Kaiser 1998; NRC 1999). Central to ecosystem considerations are species interactions. In many food webs, predation can be a major ecological process affecting fish populations (Sissenwine 1984; Bax 1991, 1998; Christensen 1996) and the major source of mortality for fish (e.g., Sissenwine et al. 1984; Keast 1985; Mittelbach and Persson 1998). Multispecies, trophodynamic, food web, and ecosystem models are tools to give insights into fish communities where classical fisheries methods are unable to do so (e.g., Steele 1974; Andersen and Ursin 1977; Helgason and Gislason 1979; May et al. 1979; Mercer 1982; Kerr and Ryder 1989; Daan and Sissenwine 1991). For example, how important is natural mortality to a given fish stock (Sissenwine 1984), what are the system-level emergent properties from a fish community and how are they altered with overfishing (Jennings and Kaiser 1998), or what levels of biomass tradeoff are we willing to accept among a given species mix? Quantifying the food habits of these species is at the heart of these and similar questions.
We thank the hundreds of individuals who have collected food habits data over the course of the Bottom Trawl Survey Program. We thank past and present members associated with the FWDP for their foresight in creating, auditing, maintaining, and supporting this database of unprecedented scale and scope, especially (listed alphabetically): R. Bowman, E. Broughton, R. Edwards, M. Fogarty, R. Fritz, B. Griswold, M. Grosslein, J. Hauser, M. Hill, B. Kaminer R. Langton, R. Maurer, N. McHugh, C. Milliken, T. Morris, R. Rountree, R. Theroux, and R. Wigley. We particularly thank M. Grosslein, M. Fogarty, and W. Michaels for their discussions to clarify earlier portions of the history of this program. We thank M. Fogarty, M. Grosslein, C. Milliken, J. Gibson, and W. Gabriel for their constructive comments on earlier versions of the manuscript.
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Andersen, K.P.; Ursin, E. 1977. A multispecies extension to the Beverton and Holt theory, with accounts of phosphorus circulation and primary production. Medd. Dan. Fisk.-Havunders. 7:319-435.
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Stomach Sampling Protocols Used during NEFSC Bottom Trawl Surveys, 1963-99
STOMACH SAMPLING PROTOCOL DURING 1963-66
General procedures are as follows:
1. After completion of other duties, randomly select fish from baskets for stomach content examination.
2. Record cruise number, station number, and species sampled at top of log. Record length (cm), sex, and maturity stage of each fish examined.
3. Dissect out stomach and empty contents onto measuring board. Sort, identify, and record prey items (record as empty when applicable).
4. Measure all fish and crab prey (total or fork length for fish and carapace width for crabs).
STOMACH SAMPLING PROTOCOL DURING 1967-72
Preserve in 10% neutral buffered Formalin up to 20 (but not less than 5) stomachs per species per catch, selecting individuals at random (i.e., without regard to size) from the sorted catch. If time does not permit sampling all those species with >5 individuals in each catch (usually there are 4-6 species with >5 individuals), then give first priority to the most abundant species, but seek to obtain some samples of all but the rare species for the entire cruise. Note that certain species (e.g., Atlantic herring, silver hake) may yield only small or occasional catches but they should get high priority because they represent a large biomass.
In a few cases when there is a very wide range in size for a given species (e.g., “small” versus “whale” size category of Atlantic cod), random selection will not be suitable, and separate samples from each size category will be desirable.
Label jar tops with cruise number, station number, species, and number of stomachs, and repeat data on label inside jar. Do not overfill jars; allow about 2-inch air space at top.
STOMACH SAMPLING PROTOCOL DURING 1973-76
Stomachs will be collected only from species listed in Table A1. Fifty stomachs should be collected for each species in each strata set per cruise. No more than 10 stomachs per species should be collected for any one station, and the same species should not be sampled at two consecutive stations.
When the catch of a species is large, the stomach samples should be taken randomly with respect to fish length. When fish are small, they should be preserved whole after puncturing the gut cavity. Only one species shall be placed in any one jar. After removing the stomach from a large fish, make a label showing cruise number, station number, maturity stage, species, sex, and length (cm). Wrap the stomach and the label in cheesecloth, and secure with a cable tie. Stomachs from the same species collected at the same station may be preserved together in one jar. NEVER PUT MORE THAN ONE SPECIES OR FISH FROM DIFFERENT STATIONS IN THE SAME JAR. Label the jar cap with cruise number, station number, species, and the number of stomachs in the jar. See Table A2 for examples of stomach and jar cap labels. Use 10% Formalin as a preservative.
Collect 50 young of the year (YOY) of the species listed in Table A1 for each strata set. They should be preserved whole, and the jar cap labeled as aforementioned. The lengths which are less than or equal to those listed in Table A1 signify YOY. Be sure to slit the gut cavity.
If it appears that the necessary stomachs from each strata set will not be collected as the cruise progresses, disregard the above directions and take all stomachs possible until 50 have been collected for each species, then collect using the normal procedure.
STOMACH SAMPLING PROTOCOL DURING 1977-80
Fish and squid stomachs will be collected from the species listed in Table A3, Table A4, and Table A5. The collection is based on three separate needs as follows: 1) offshore priority species, 2) inshore priority species, and 3) miscellaneous species. Stomach sampling takes priority over any other non-NEFC sampling.
On all groundfish cruises sampling inshore strata, the inshore priority species listed in Table A4 will be sampled for food habits studies. Collect 150 fish representing the entire size range of each species listed.
The species chosen for the miscellaneous collection were selected because little or no food habit data have previously been collected, or additional information about their food habits is needed. Table A5 is a guide to those miscellaneous species needed from specific areas, and to those miscellaneous species needed from any area. Many of the fish included in this collection are not very abundant, and few will probably be encountered.
Stomach samples should be taken from fish representing the length range of a given species caught at any station. It is important that the largest and smallest fish be included in the collection, along with the predominant size group (i.e., stratified by length). No more than 10 stomachs per given species need to be collected at any one station, and the same species should not be sampled at two consecutive stations. If it appears that the necessary number of stomachs will not be collected as the cruise progresses, disregard the above directions and take all stomachs necessary to complete the collection, then sample normally.
Stomachs from large fish will be excised, and a label indicating cruise number, station number, species, length (cm), sex, and maturity stage will be completed (see Table A6), and together they shall be wrapped in cheesecloth and secured with a cable tie. Smaller fish may be preserved whole after puncturing the gut cavity and completing a label denoting cruise number, station number, and species. Stomachs of the same species collected at the same station may be preserved together in one jar. NEVER PUT STOMACHS OF MORE THAN ONE SPECIES OR ONE STATION IN THE SAME JAR. Use 10% Formalin as a preservative. Label the jar cap with cruise number, station number, species, and number of stomachs in the jar (see Table A6). List stomachs collected on the tally sheet provided by the Food Habits Project for your convenience.
Juvenile fish may be identified by utilizing the lengths listed with each species in Table A3. The lengths of fish less than or equal to those indicated signify juvenile fish.
Additional samples may be collected if time permits.
STOMACH SAMPLING PROTOCOL DURING 1981-84
The Feeding Ecology Project requires stomach content samples from the species listed in Table A7 whenever they occur in trawl catches. It is especially important that we document the size and species of fish prey being consumed by piscivorous predators in the Georges Bank - Nantucket Shoals area (Strata 9-25). Predators of immediate concern are silver hake, Atlantic cod, and spiny dogfish. Sampling of these and other species, which are listed in their order of priority in Table A7, should be conducted as follows.
Stomach contents (and stomach tissue) of silver hake, Atlantic cod, yellowtail flounder, haddock, winter flounder, Atlantic mackerel, and Atlantic herring are to be preserved according to the length categories and numbers given in Table A7, throughout the entire survey area. Stomachs from different species, length categories, or stations should never be put in the same jar. Small fish may be preserved whole. All jars shall be labeled on the inside and outside (jar cap) to indicate ship, cruise number, station number, species, number of fish, and length category. Samples will be preserved in 10% Formalin.
STOMACH CONTENTS EXAMINED AT SEA
Stomach contents of spiny dogfish, pollock, white hake, red hake, and goosefish are to be examined at sea. Details are given in the “Procedure for Examining Stomach Contents at Sea [1981-84]” section. If time permits, the examination of nonpriority species such as large sharks, skates, rays, summer flounder, bluefish (i.e., fish eating species) or predominant species in the catch, other than those listed in Table A7, will be useful to personnel in the Feeding Ecology Project. Any additional samples received will be appreciated.
NUMBER OF SAMPLES
If sampling time becomes critical at any particular station, only five randomly chosen individual fish of the three top priority species (i.e., silver hake, Atlantic cod, and spiny dogfish) need be sampled. No more than 40 individual fish, in total, need be sampled at any one station under any circumstances.
PROCEDURE FOR EXAMINING STOMACH CONTENTS AT SEA [1981-84]
1. Record pertinent information such as vessel, cruise number, station number, and predator species in the space provided at the top lefthand corner of the log.
2. Inspect the buccal cavity (inside of mouth) for signs of regurgitated food and the esophageal area (via the body cavity) for inversion. Also check the gills to be sure the fish was freshly caught (white or pink gills indicate the fish was probably from a previous station). If any of the above conditions exist, discard the fish.
3. Determine the length (cm), sex, and maturity stage of the fish, and record this information on the appropriate line of the log (simply circle the sex and maturity stage; i.e., F = female, M = male, I = immature, D = developing, R = ripe [or spawning], S = spent, and Rt = resting).
4. Excise the stomach and empty the contents onto a tray or sieve. The fullness measurement is recorded on the “Fullness” line of the log as the estimated volume (in cubic centimeters) made up by the stomach contents. If the stomach is empty, record the fullness measurement as “0” and proceed to the next fish. The volume may be estimated to the nearest 0.5 cm3 by comparing the appropriately sized, premeasured piece of wood to the volume made up by the stomach contents.
5. It will be helpful if the relative state of digestion of the prey items is recorded. If the stomach contents (as a whole) appear relatively fresh (“FR”), partly digested (“PD”), or well digested (“WD”), they should be recorded as such in the “State of Digestion” column of the log.
6. The stomach contents may now be spread apart and separated into prey groups. An estimate of the percentage that each prey group makes up of the total stomach content volume should be written on the line of the log corresponding to the particular prey. If prey can readily be identified to species, the name may be written into one of the open spaces, and the percentage recorded as indicated earlier. The number and size (or mean size) of organisms may also be recorded, either along with the percentage, or in the “Comments” section of the log. A small number of prey species (or groups) usually account for a large percentage of a fish’s food. Some organisms are common food for many species of fish. Organisms repeatedly noted in the stomachs of a particular species (or in the stomachs of several species), and not identified to species, should be preserved in 10% Formalin and brought back to the laboratory for identification. The stomach contents of all fish recorded on a particular log should be saved in the same jar when returning material to the laboratory for identification. The “Pisces” (i.e., fish) column of the log should never be used if the fish found in the stomach can be identified to any lower classification. The length(s) and number of fish prey should always be recorded (the total length at time of ingestion may be estimated if fish prey are in pieces or partially digested).
7. Space for pathological information is provided at the bottom of the log. Simply circle the abbreviation for the affected organ and/or record additional information in the “Comments” section of the log.
STOMACH SAMPLING PROTOCOL DURING 1985-91
The Northeast Fisheries Center seeks stomach content data for the priority species listed in Table A8 whenever they occur in trawl catches. It is especially important to document the size and species of fish prey being consumed by piscivorous predators in the Georges Bank - Southern New England area (Strata 1-25). The stomach contents of all fish are to be examined at sea (see “Procedure for Examining Stomach Contents at Sea [1985-91].”). If time permits, the sampling of species not listed in Table A8 such as large sharks and rays (i.e., fish-eating species) or any other predominant species in the catch will also be desirable. Table A9 lists 18 secondary species for which a random sample of 10 fish should be taken for each watch.
If sampling time is inadequate to achieve target numbers of priority species, then try to obtain at least five individual fish (randomly chosen) of each of the top three priority species in the catch. However, if possible, it is desirable to sample about 50 fish in total at each station to provide large enough samples to detect spatial and temporal shifts in diet.
PROCEDURE FOR EXAMINING STOMACH CONTENTS AT SEA [1985-91]
1. Record pertinent information such as vessel, cruise number, station number, and predator species in the spaces provided at the top of the log. Please use entire common name of predator (and prey) fishes when completing the log.
2. Inspect the buccal cavity (inside of mouth) for regurgitated food and the esophageal area (via the body cavity if necessary) for signs of stomach inversion. Also inspect the gills to be sure the fish was freshly caught (white or pink gills indicate the fish is probably from a previous station). If any of the above conditions exist, discard the fish.
3. Determine the length (cm) (as per standard survey measurements), sex, and maturity stage of the fish, and record that information in the appropriate spaces of the log (see codes for sex and maturity stage at the top of log).
4. Excise the stomach and empty the contents onto a clean measuring board. Determine and record the stomach fullness (volume to the nearest 0.5 cm3) by comparing the appropriately sized volumetric gauge to the entire volume of the bolus. If the stomach is empty, record stomach fullness as “0.0” and proceed to the next fish.
5. Separate the stomach contents into prey groups and record each group to the lowest taxon practical (see Watch Chief if necessary). Estimate the percentage that each prey group makes up of the total stomach content volume and write it on the corresponding line of the log. For each prey category, record the number (you may estimate for small organisms), individual sizes as per survey standards (or minimum, maximum, and average size in millimeters if more than 10 organisms are present), and state of digestion (see codes at top of log). It is only necessary to measure organisms >15 mm in length (e.g., fish, squid, crabs, and decapod shrimp). The length(s) and number of fish prey should be estimated to reflect the number and size at time of ingestion if only pieces or partly digested fish are present. Larvae and juvenile fish which can’t be identified should be preserved (with pertinent station information) for microscopic examination at the Woods Hole Laboratory. Organisms repeatedly observed as prey, but not identified to species, may occasionally be preserved (10% Formalin) and brought to the laboratory for positive identification.
STOMACH SAMPLING PROTOCOL DURING 1992-99
Information on predator-prey interactions among fishes is critical for recruitment and multispecies models. Routine stomach sampling on groundfish surveys provides an extremely valuable time series of gut-content data which is needed for evaluating major changes in the diets of fishes in relation to composition and abundance of their prey. The primary objective is to estimate predation on fish (particularly larval and juvenile stages). The current focus is on piscivorous species representing major components of the finfish biomass along the continental shelf off the northeastern United States.
First priority is assigned to silver hake, Atlantic cod, spiny dogfish, and skates. Sampling guidelines for these and other species are outlined in the accompanying Table A10, Table A11, and Table A12. Any unusual or interesting species not included in Tables A10-A12 can be sampled as time permits.
PROCEDURE FOR VOLUMETRIC EXAMINATION OF FISH STOMACHS AT SEA
1. Select fish according to priorities in Tables A10-A12.
2. Inspect gills to be sure fish was freshly caught (pale pink or white gills means fish is probably from an earlier station).
3. For each species sampled, use a separate log sheet. Print complete name of species. Abbreviations can be confused (e.g., “s. hake” could be silver hake or spotted hake).
4. Record each predator length to nearest centimeter following standard NEFSC survey methods. Record individual fish weight to the nearest gram. Record sex and maturity stage. Fill in “F” block with an “E” to show that the stomach was examined at sea. Excise stomach and empty stomach contents onto a clean measuring board or into a sorting tray.
5. If stomach is everted (blown) or shows signs of regurgitation (food in mouth), leave the “F” block and the “Fullness” section of the log blank. Record “BLOWN” as the prey name. Continue on to next fish.
6. If stomach is empty, record “0.0” in the “Fullness” section and record “EMPTY” as the prey name. Continue on to next fish.
7. If stomach contains food, estimate total volume of bolus using the volumetric gauges (i.e., “wind chimes”). Record volume to nearest 0.1 cm3. Trace amounts <0.1cm3 in volume should be recorded as 0.1cm3. ALWAYS USE GAUGE.
8. Sort stomach contents into separate piles of prey groups whenever possible. Prey should be identified to the lowest taxon practical. Fish prey should be identified to species as much as possible. Unidentified larval fish should be measured, recorded as “larval fish,” and preserved in the provided vials. Label vial lid with cruise number, station number, predator, and identification number. Invertebrate prey should at least be recorded to major taxonomic group (e.g., crab, polychaete, gammarid, bivalve) Use the illustrated prey sheet to aid identification and spelling, or ask the food habits representative on your watch. Unidentifiable remains should be recorded as “AR.”
9. Estimate and record percentage of total volume represented by each prey group. Record the average digestion for each group.
10. All fish, crabs, and squid should be measured using standard NEFSC survey methods. ALL species should be counted or have the count estimated by volume if possible. It is of critical importance to record the number and individual lengths of all fish prey. A MAXIMUM of 10 individuals should be measured to the nearest millimeter. If over 10 animals are present select a random subsample of 10 individuals and record their lengths to the nearest mm. For partly digested prey remains or large fragments of prey that cannot be accurately measured, estimate the length of the animal to nearest 10 mm at time of ingestion. Record these estimated lengths, followed by an “E” (e.g., 250E, 110E). Be sure to record the total number of prey present, not the number of prey measured. RECORD ALL PREY LENGTHS IN MILLIMETERS.
11. Use the “Remarks” section to note larval fish preserved for further identification, comments on prey, or general comments on feeding (i.e., net feeding or scallop draggers in vicinity). Remember to check “R” block if “Remarks” section is used.
IF YOU HAVE ANY QUESTIONS, ASK THE FOOD HABITS REPRESENTATIVE ON YOUR WATCH.
CRITERIA FOR ASSESSING DIGESTION STAGE
FRESH = No obvious sign of digestion. No skin discoloration. Crustacean carapace is hard. Prey are easily identifiable to family or species, but do not have to be identified to this level to fit category.
PARTIAL = Some recognizable external characteristics remain. Crustacean carapace is intact but soft. Prey can frequently be identified to family or species, but do not have to be identified to this level to fit category.
WELL = No external characteristics remaining. Prey cannot be identified to family or species using external features. Prey may sometimes be identified using otoliths or other remaining hard internal structures.
STOMACH SAMPLE PROCESSING
During 1992-93 surveys, sampling ranges (i.e., number of fish per range of length) and maximum stomach sampling levels were set by species and station. Refer to Table A10. Maxima were removed in 1994, and priority species were designated for each survey beginning in 1995. Refer to Table A11. In 1999, the composition of species to be sampled, sampling ranges, and sampling priorities changed. Refer to Table A12.
An effort should be made to complete all food habits sampling requested. If catches become overwhelming, complete stomach analyses in order of priority. At the Watch Chief’s discretion, a cap of five randomly selected fish may be placed on the number of stomachs examined, excluding empty or blown stomachs.
Acronyms BEP = Benthic Ecology Program (predecessor to the FEP) EMI = Ecosystem Modeling Investigation FCDI = Food Chain Dynamics Investigation (predecessor to the FWDP) FEP = Feeding Ecology Project (predecessor to the FCDI) FWDP = Food Web Dynamics Program GLOBEC = (U.S.) Global Ocean Ecosystems Dynamics Program NEFC = Northeast Fisheries Center (predecessor to the NEFSC) NEFSC = Northeast Fisheries Science Center NMFS = National Marine Fisheries Service YOY = young of the year