A stable isotope (δ13C, δ15N) model for the North Water food web: implications for evaluating trophodynamics and the flow of energy and contaminants

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Abstract

The North Water Polynya is an area of high biological activity that supports large numbers of higher trophic-level organisms such as seabirds and marine mammals. An overall objective of the Upper Trophic-Level Group of the International North Water Polynya Study (NOW) was to evaluate carbon and contaminant flux through these high trophic-level (TL) consumers. Crucial to an evaluation of the role of such consumers, however, was the establishment of primary trophic linkages within the North Water food web. We used δ15N values of food web components from particulate organic matter (POM) through polar bears (Ursus maritimus) to create a trophic-level model based on the assumptions that Calanus hyperboreus occupies TL 2.0 and there is a 2.4‰ trophic enrichment in 15N between birds and their diets, and a 3.8‰ trophic enrichment for all other components. This model placed the planktivorous dovekie (Alle alle) at TL 3.3, ringed seal (Phoca hispida) at TL 4.5, and polar bear at TL 5.5. The copepods C. hyperboreus, Chiridius glacialis and Euchaeta glacialis formed a trophic continuum (TL 2.0–3.0) from primary herbivore through omnivore to primary carnivore. Invertebrates were generally sorted according to planktonic, benthic and epibenthic feeding groups. Seabirds formed three trophic groups, with dovekie occupying the lowest, black-legged kittiwake (Rissa tridactyla), northern fulmar (Fulmarus glacialis), thick-billed murre (Uria aalge), and ivory gull (Pagophilia eburnea) intermediate (TL 3.9–4.0), and glaucous gull (Larus hyperboreus) the highest (TL 4.6) trophic positions. Among marine mammals, walrus (Odobenus rosmarus) occupied the lowest (TL 3.2) and bearded seal (Erignathus barbatus), ringed seal, beluga whale (Delphinapterus leucas), and narwhal (Monodon monoceros) intermediate positions (TL 4.1–4.6). In addition to arctic cod (Boreogadus saida), we suggest that lower trophic-level prey, in particular the amphipod Themisto libellula, contribute fundamentally in transferring energy and carbon flux to higher trophic-level seabirds and marine mammals. We measured PCB 153 among selected organisms to investigate the behavior of bioaccumulating contaminants within the food web. Our isotopic model confirmed the trophic magnification of PCB 153 in this high-Arctic food web due to a strong correlation between contaminant concentration and organism δ15N values, demonstrating the utility of combining isotopic and contaminant approaches to food-web studies. Stable-carbon isotope analysis confirmed an enrichment in 13C between POM and ice algae (–22.3 vs. –17.7‰). Benthic organisms were generally enriched in 13C compared to pelagic species. We discuss individual species isotopic data and the general utility of our stable isotope model for defining carbon flux and contaminant flow through the North Water food web.

Introduction

In contrast to the Northeast Water Polynya off eastern Greenland, the North Water of northern Baffin Bay is an area of immense biological activity, with high populations of seabirds and marine mammals (Stirling, 1980; Falk et al., 1997). Populations of dovekie (Alle alle), a small planktivorous seabird, alone are estimated to range from 14 to 30 million pairs (Salmonsen, 1981; Nettleship and Evans, 1985; Boertman and Mosbech, 1998). The polynya also is thought to support large numbers of beluga (Delphinapterus leucas), narwhal (Monodon monoceros), and seals (Finley and Renaud, 1980; Stirling, 1980; Stirling et al., 1981; Richard et al., 1998), and is used seasonally by the endangered eastern population of the bowhead whale (Balaena mysticetus; Holst and Stirling, 1999). Most of these animals are used by aboriginal peoples of both Canada and Greenland for food and so are also important from an economic and contaminants perspective (Muir et al., 1988; Braune, 1994). However, such populations of animals represent but the most conspicuous components of a highly productive marine food web consisting of at least five trophic levels (Hobson and Welch, 1992a). What role all components of the North Water food web play in energy or contaminant flux is currently unknown.

A fundamental requirement to understanding energy flow through complex marine food webs from primary carbon fixation through upper trophic-level consumers is knowledge of trophic linkages among organisms. Such knowledge is also key to modeling the flux of persistent contaminants that may bioaccumulate or biomagnify in marine food webs (Muir et al., 1995; Jarman et al (1996), Jarman et al (1997); Atwell et al., 1998). An important objective of the International North Water Polynya Study (NOW) was to establish a trophic food web model in order to understand basic aspects of the ecology of key groups of organisms and to provide a template to assist in the modeling of energy and contaminant flow. In the last decade, tracing sources of primary productivity to and relative trophic level of organisms in marine food webs has been advanced by the use of measurements of naturally occurring stable isotopes of elements such as carbon (13C/12C) and nitrogen (15N/14N) (Michener and Schell, 1994). This approach is based on the principle that the stable isotope ratios in consumer tissues can be related in a predictive way to those in their diet (DeNiro and Epstein (1978), DeNiro and Epstein (1981)). For carbon, there appears to be little (i.e. approx. 1‰) or no change in the relative abundance of 13C between trophic levels following the primary producer to primary consumer link (Hobson and Welch, 1992a), so that this isotope is useful as an indicator of sources of primary productivity in simple systems where two isotopically distinct sources are present (e.g., phytoplankton vs. ice algae) (Hobson et al., 1995). Stable-carbon isotope values are also relatively enriched in benthic or inshore food webs relative to pelagic food webs (Hobson and Welch, 1992a; Hobson et al., 1994; France, 1995a). For nitrogen, enrichment in 15N occurs with trophic level, an effect that appears to be relatively constant and typically 3–4‰ (Michener and Schell, 1994). Relative trophic position thus can be modeled using stable-nitrogen isotope measurements alone, an approach that recently has provided insights to the behavior of contaminants in marine food webs (Broman et al., 1992; Rolff et al., 1993; Atwell et al., 1998). The combined use of stable-carbon and stable-nitrogen isotope measurements of marine organisms, together with more conventional dietary approaches, can thus be used to provide important new information on trophic relationships and feeding ecology, including spatial use of habitat (Hobson and Welch, 1992a; Hobson et al., 1994; Michener and Schell, 1994; Kelly, 2000; Lawson and Hobson, 2000).

Following the isotopic research conducted in the Northeast Water Polynya (Hobson et al., 1995), this paper presents the results of an isotopic survey of the North Water food web, from particulate organic material (POM) through seals and seabirds. We intend this as a broad overview to provide a model of trophic relationships among key organisms. We used stable-carbon isotope measurements to interpret sources of primary productivity and stable-nitrogen isotope analysis to provide estimates of relative trophic position. We also address the utility of this information for the broader NOW objectives of modeling carbon flux and contaminant flow through the food web. Future papers will deal with various taxa in more detail, as well as more specific questions of spatial and temporal patterns in stable isotope signatures (e.g., Schell et al., 1998).

Section snippets

Field collections

Sampling of food web components was based primarily on collections made during the April–July 1998 NOW cruise onboard the CCGS Pierre Radisson. Samples of POM were obtained by filtering surface (<50 m) waters onto precombusted glass GFF filters and stored frozen. Ice-algae samples, obtained opportunistically during June from ice cores or from floating mats, were sieved through 0.1-mm screen to remove zooplankton and then frozen. Zooplankton samples were obtained primarily by towing a 4-m2

15N trophic model

Mean stable-nitrogen isotope measurements varied considerably among taxa (5.1–21.1‰) and followed a general enrichment with trophic level (Table 1, Fig. 1). The most depleted δ15N values were measured for ice algae and POM, and the most enriched for seabirds and marine mammals. This difference allowed us to depict trophic level of several organisms relative to the calanoid copepod, C. hyperboreus, which we assumed occupied trophic level (TL) 2 (i.e. a primary herbivore). Assuming additionally

Patterns in 15N and the trophic model

Our isotopic investigation of the North Water marine food web has revealed a general pattern of enrichment in 15N with trophic level. This pattern is similar to that found by Hobson and Welch (1992a) for the adjacent Lancaster Sound region and also for the Northeast Water Polynya (Hobson et al., 1995), providing further evidence of the utility of this approach for trophic modeling in marine systems (Michener and Schell, 1994). We used a single trophic enrichment factor of 3.8 for nitrogen

Acknowledgements

Funding for this project was provided in part by a Natural Science and Engineering Research Council (NSERC), the Canadian Wildlife Service, the Polar Continental Shelf Project and a National Science Foundation (NSF) Grant to G. Hunt Jr. We thank the many scientists of the International North Water Polynya Study (NOW), who assisted us, especially I. Stirling for invaluable guidance and assistance in the field and laboratory, D. Andriashek and N. Lunn for excellent assistance with collections,

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