Temporal Variation in Western Hudson Bay Ringed Seal Phoca Hispida Diet in Relation to Environment
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Vol. 481: 269–287, 2013 MARINE ECOLOGY PROGRESS SERIES Published May 7 doi: 10.3354/meps10134 Mar Ecol Prog Ser Temporal variation in western Hudson Bay ringed seal Phoca hispida diet in relation to environment Magaly Chambellant1,4,*, Ian Stirling2,3, Steven H. Ferguson1,4 1Department of Biological Sciences, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada 2Wildlife Research Division, Science and Technology Branch, Environment Canada, Edmonton, Alberta T6H 3S5, Canada 3Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada 4Fisheries and Oceans Canada, Winnipeg, Manitoba R3T 2N6, Canada ABSTRACT: We present the first study of ringed seal Phoca hispida feeding habits in western Hudson Bay (WHB) using stomach content analysis and stable isotope analysis (SIA). Ringed seals were sampled during 9 Inuit subsistence harvests in Arviat, Nunavut, Canada, over the period 1991 to 2006. During the open-water season in summer and fall, ringed seals fed mostly on sand lance Ammodytes spp. In the spring, when annual sea ice was still present, Arctic cod Boreogadus saida and capelin Mallotus villosus were also important in the diet, and consumption of inverte- brates was higher than in the open-water period. From SIA, adult ringed seals exploited slightly more benthic habitats than immature individuals. Sand lances were the main prey consumed throughout the study period, but strong interannual variation occurred. When break-up of the sea ice in spring was relatively late, as in the early 1990s, ringed seal consumption of sand lance and total energy input was lower than in subsequent years of the study, despite a higher importance of sculpins (Cottidae) in the diet. The consumption of other fish species changed in the 2000s: Arctic cod declined whereas capelin increased in importance. Our results suggest that ringed seals in WHB are sand lance specialists, and their population dynamics are, at times, strongly regulated by bottom-up processes. KEY WORDS: Bottom-up regulation · Feeding habit · Stable isotope · Stomach content · Index of global importance · Ammodytes spp. Resale or republication not permitted without written consent of the publisher INTRODUCTION (Gagnon & Gough 2005). A reduction of sea ice extent and snow depth, likely a result of increasing Over the last 40 yr, Hudson Bay (HB), a large Cana- air and water temperatures, has also been reported dian inland sea, ice-covered from November to June in HB (Ferguson et al. 2005, Gagnon & Gough 2005, (Saucier et al. 2004), has experienced major climatic Stirling & Parkinson 2006, Parkinson & Cavalieri changes that reflect the warming that is occurring 2008, Galbraith & Larouche 2011). globally (IPCC 2007). Break-up of the sea ice in These changes to the atmosphere–ice–ocean cou- spring in western Hudson Bay (WHB) is now occur- pling are predicted to influence oceanic primary pro- ring earlier than it did in the 1970s, at a rate of about ductivity with subsequent cascading effects through 7 to 10 d decade−1 (Gagnon & Gough 2005, Stirling & the marine food web. As well as possible shifts in Parkinson 2006). Together with a delayed freeze-up prey distribution and availability, loss of sea ice habi- in the fall, the earlier ice break-up resulted in an tat will likely result in changes in distribution, repro- increase in the length of the open-water season duction, and ultimately survival and abundance of *Email: [email protected] © Inter-Research and Fisheries and Oceans Canada 2013 · www.int-res.com 270 Mar Ecol Prog Ser 481: 269–287, 2013 Arctic species dependent on sea ice (Tynan & and nutritional stress, through decreased marine pro- DeMaster 1997, Laidre et al. 2008). Evidence of such ductivity, was proposed as a possible explanation changes has been reported in HB for ice-associated (Chambellant et al. 2012a). However, ringed seal diet species, such as thick-billed murres Uria lomvia preferences and variation have not been adequately (Gaston et al. 2005) and polar bears Ursus maritimus studied anywhere in HB (McLaren 1958, Breton- (Stirling et al. 1999, Regehr et al. 2007, Stirling & Provencher 1979, Stirling 2005, Chambellant 2010), Derocher 2012). preventing the assessment of the proposed nutri- The ringed seal Phoca hispida, one of the smallest tional stress hypothesis. phocids (McLaren 1993), is distributed throughout Traditionally, diet studies of pinnipeds have prima- the ice-covered waters of the circumpolar Arctic and rily depended on recovery of soft and hard parts in is the most abundant pinniped species of the north- gastrointestinal tracts or faeces, providing both qual- ern polar regions (Frost & Lowry 1981). Sexually itative and quantitative information on prey con- mature ringed seals depend on stable ice with suffi- sumed. However, there are also several limitations cient snow cover for females to build subnivean birth associated with this technique which may bias diet lairs that are critical to protect newborn pups from determination. Differential digestion rates of large the cold and predators such as polar bears, Arctic and small, hard and soft prey and rapid transit rate foxes Vulpes lagopus, and humans (McLaren 1958, are examples of such limitations (Murie & Lavigne Smith & Stirling 1975, Smith et al. 1991, Furgal et al. 1986, Tollit et al. 1997, Bowen 2000, Hammill et al. 1996). Following reproduction and moulting in 2005). Furthermore, stomach contents can only pro- spring, when minimal feeding occurs, ringed seals vide information on prey ingested shortly before col- feed intensively during the open-water season in late lection and thus may not reflect the diet over time summer and fall to replenish their fat reserves, as and space. Consequently, indirect methods have reflected by a clear pattern of seasonal variation in recently been developed to provide insight on mar- the thickness of subcutaneous fat depositions ine predator diets, including analyses of stable iso- (McLaren 1958, Breton-Provencher 1979, Ryg et al. tope (SI) ratios (Hobson et al. 1996, Lawson & Hobson 1990). Ringed seals consume a large variety of prey 2000) and fatty acids in their tissues (Iverson et al. species across their range, but only a few prey taxa 2004, Thiemann et al. 2008). (2 to 4) generally dominate the diet in a specific loca- Stable isotope analysis (SIA) is based on the natu- tion (McLaren 1958, Weslawski et al. 1994, Siegstad ral occurrence of different isotopes of the same ele- et al. 1998). Arctic cod Boreogadus saida and inverte- ment and their differential fractionation during bio- brates such as mysids (Mysidae), hyperiid amphipods logical processes. In marine food web studies, (Amphipoda), and euphausiids (Euphausiacea) are nitro gen (N) SI ratio (15N/14N, labelled δ15N) indi- consistent prey of ringed seals, but diet composition cates the relative trophic level of an organism and varies with geographical location, season, life stage, trophic relationships between organisms in an eco- and/or sex (Bradstreet & Finley 1983, Smith 1987, system, while carbon (C) SI ratio (13C/12C, labelled Siegstad et al. 1998, Holst et al. 2001, Labansen et al. δ13C) reflects feeding habitat (e.g. benthic vs. pela- 2007). gic, freshwater vs. ma rine, in shore vs. offshore) and Considering their position near the top of the Arctic general geographic locations (water masses of dif- food web and their high degree of adaptation to ferent isotopic signatures; see reviews by Kelly 2000 exploit sea ice habitat for reproduction and survival, and Newsome et al. 2010). Due to the specific pro- ringed seals should be good indicators of ecosystem tein turnover rate of each tissue, the isotopic signa- changes (e.g. Harwood et al. 2012). In HB, where ture of a specific tissue provides information on prey ringed seals occur near the southern limit of their dis- assimilated over a specific timescale (Kurle & Wor- tribution (Frost & Lowry 1981), changes in population thy 2002). Tissues with a high turnover rate (liver, dynamics because of climate warming will likely kidney, serum) represent food ingested days or occur prior to changes at higher latitudes. Because weeks before collection, tissues with a lower turn- marked changes in the patterns of sea ice duration over rate (muscle, red blood cells) represent food and, conversely, of open water have already been ingested months before, and inert tissues (whisker, documented in HB, this is an appropriate ecosystem fur, tooth) represent the SI signature of prey con- in which to test hypotheses related to shifts in ringed sumed as they were forming over months or an seal diet, energy budget, body condition, reproduc- entire lifetime. Although models have been devel- tion, and survival. Low reproductive rates and pup oped to estimate the contribution of different a priori survival have been reported in the 1990s in WHB, potential prey species to predator diet using C and Chambellant et al.: Ringed seal diet in Hudson Bay 271 N SI ratios (Phillips & Gregg 2003, Moore & Sem- MATERIALS AND METHODS mens 2008), several limitations (e.g. prey need to have distinct isotopic signatures) hinder the assess- Sample collection ment of species composition in the diet using SIA, especially for diversified diets. Using SIA is thus a Ringed seals were sampled in 1991, 1992, and complementary method to more traditional hard- 1998 to 2000 by the Canadian Wildlife Service and part reconstruction techniques, and this combination in 2003 to 2006 by Fisheries and Oceans Canada has been successively used to explore pinniped (DFO), Winnipeg, in the HB community of Arviat, feeding habits (e.g. Dehn et al. 2007). Nunavut (NU), Canada (Fig. 1), from the Inuit sub- In this study, we examined the diet of ringed seals sistence fall harvest (September through Novem- in WHB over 9 sampling years between 1991 and ber), when ringed seals feed in open water. In 2006, using both stomach contents and C and N SI 1991, 1992, 2004, and 2005, samples were also col- ratios in muscle tissue.