Importance of Eating Capelin: Unique Dietary Habits of ... - Springer Link

Importance of Eating Capelin: Unique Dietary Habits of Hudson Bay Beluga T.C. Kelley, L.L. Loseto, R.E.A. Stewart, M. Yurkowski, and S.H. Ferguson

Abstract Beluga whales (Delphinapterus leucas) fill an important ecological and economic role in Hudson Bay. However, little is known about their diet and a better understanding of beluga populations is required. Though Arctic cod (Boreogadus saida) are important forage fish species for many circumpolar marine predators, beluga are opportunistic feeders and may feed on a variety of prey items. Here, we compare the fatty acid profile of two key forage fish, Arctic cod and capelin (Mallotus villosus), to determine the relative importance of each species to the diets of beluga during the 1980s in three Canadian Eastern Arctic beluga populations: Western Hudson Bay, Cumberland Sound, and the High Arctic. First, we compared the two prey species using a Principle Component Analysis (PCA) to determine the fatty acids that best described each species. Five fatty acids dominated the Arctic cod profile (the 20 and 22 carbon length monounsaturates 20:1n7, 20:1n9, 22:1n9, 22:1n11, 22:1n7), and five fatty acids were representative of the capelin profile (18:2n6, 16, 22:6n3, 22:5n6, and 20:4n6). The levels of these ten fatty acids were significantly different between the two fish species. A discriminant function analysis followed by univariate tests, were performed on beluga fatty acid profiles to determine if populations could be differentiated. Results demonstrated significant differences among the three beluga populations. Finally, to examine the qualitative dietary importance of Arctic cod and capelin among the three beluga populations all fatty acid profiles were evaluated together with a PCA. We found the fatty acid profiles that segregated the Hudson Bay beluga population from others appeared to be associated with a capelin diet relative to the other beluga populations that appeared to feed more heavily on Arctic cod. The difference in fatty acid profiles and diet between the northern populations and the Hudson Bay population is discussed relative to possible environmental explanations.

T.C. Kelley (*) Department of Environment and Geography, University of Manitoba, Winnipeg, MB R3T 2N2, Canada e-mail: [email protected] S.H. Ferguson et al. (eds.), A Little Less Arctic: Top Predators in the World’s Largest Northern Inland Sea, Hudson Bay, DOI 10.1007/978-90-481-9121-5_3, © Springer Science+Business Media B.V. 2010

53

54

T.C. Kelley et al.

Keywords Feeding ecology • Fatty acids • Food web • Blubber • Hudson Bay • High Arctic • Cumberland Sound • Delphinapterus leucas • Mallotus villosus • Boreogadus saida

Introduction Beluga whales (Delphinapterus leucas) are an integral part of the eastern Canadian Arctic marine ecosystem, an important species in the diet of local Inuit, and provide economic resources to the community of Churchill, Manitoba through whale-watching tourism. Little is known about their diet in Hudson Bay, although Arctic cod (Boreogaidus saida) is an important prey species for many beluga populations (Seaman et al. 1982; Welch et al. 1992; Dahl et al. 2000; Loseto et al. 2009). However, beluga are opportunistic feeders and prey on a variety of items including redfish (Sebastes marinus), halibut (Reinhardtius hippoglossoides), and shrimp (Pandalus borealis) in Greenland (Heide-Jorgensen and Teilmann 1994). Pacific salmon (Oncorhynchus spp.) were dominant prey items to the Alaskan beluga populations (Frost and Lowry 1981). Finally, beluga have been observed feeding on capelin (Mallotus villosus) in the Churchill River estuary in summer (Watts and Draper 1986). Capelin is a temperate cold-water fish species (Carscadden and Vilhjálmsson 2002). They are adapted to living at the edge of Arctic waters (Vilhjálmsson 2002) and move into warmer and coastal waters to spawn (Vesin et al. 1981; Carscadden et al. 1989). Capelin respond quickly to changes in climate and a simplified prediction of temperature increases of 2–4°C would result in capelin shifting distribution 4–18° latitude north (Rose 2005). Increased ice cover and decreased water temperatures associated with prolonged cold periods has been associated with the movement of capelin to non-traditional, warmer waters (Carscadden et al. 2001). Thus, increased temperatures in Hudson Bay may lead to changes in capelin habitat use and prevalence, resulting in unknown impacts on beluga. Conversely, Arctic cod are typically associated with sea ice, especially along ice pressure ridges (Moskalenko 1964) and ice cracks (Lønne and Gulliksen 1989). These habitats are thought to provide refuge from predators such as ringed seals (Phoca hispida) as well as provide prey to feed on (Gradinger and Bluhm 2004). Evidently, Arctic cod is better adapted than other fish species to the environmental conditions in the far north (Tynan and DeMaster 1997) as they are adapted to feed and live under the ice (Dunbar 1981; Gradinger and Bluhm 2004). Sea ice cover in Hudson Bay is seasonal, with a near complete ice cover for most of the year (November–June) and ice free conditions in the summer (Saucier et al. 2004). The effects of climate change are greatest at higher latitudes and Hudson Bay is expected to exhibit one of the highest rates of warming (Parkinson et al. 2008; Gagnon and Gough 2005; Parkinson et al. 1999). Ice-associated species, such as beluga, Arctic cod, and the food web they depend on will be affected by this shift in climate (Stirling et al. 2004; Ferguson et al. 2005; Stirling and Parkinson 2006). Changes in Arctic cod distribution may lead to changes in

Importance of Eating Capelin: Unique Dietary Habits of Hudson Bay Beluga

55

whale migration, distribution, and abundance patterns (Tynan and DeMaster 1997; Laidre et al. 2008). Beluga diets are poorly understood because whales harvested in summer typically have empty stomachs and faeces are difficult to collect due to their deliquescence. Direct observation of feeding by marine mammals has been accomplished (Watts and Draper 1986; Harwood and Smith 2002), though it is often difficult. Recently, techniques using fatty acid signatures have been used to obtain information on diet, foraging locations, and population structure of many animals, including marine mammals, because fatty acids are predictably incorporated into consumer fat tissue, integrating diet over weeks to months (Kirsch et al. 2000; Iverson et al. 2004; Thiemann et al. 2007). This technique assumes that a prey species’ fatty acid signatures are reflected in the tissues of its predator, making fatty acids an ideal diet biomarker. In the 1980s, as part of investigations into beluga stock identity (Stewart 1994), blubber and prey samples were collected and processed to examine stock differences, but were never published. The dataset is unique as it pro‑ vides a glimpse into beluga feeding habits during the 1980s that is otherwise unavailable. Here we resurrect those data to: (1) determine if Arctic cod and capelin can be distinguished from each other based on their fatty acid profiles; (2) determine if Hudson Bay beluga have different diets than the other two populations; (3) evaluate the relative importance of these species in beluga whales harvested in Hudson Bay, Cumberland Sound and Grise Fjord; (4) assess whether we can statistically discriminate among the three populations of beluga using fatty acid markers; and (5) provide retrospective data by which modern analysis can assess climate change impacts.

Methods Sample Collection Samples used for this study were collected in the Eastern Arctic, from Arviat, Pangnirtung and Grise Fjord (Fig. 1). The whale samples represent three different beluga whale populations; beluga from Arviat are whales belonging to the western Hudson Bay population; beluga from Grise Fjord are from the High Arctic population; and samples from Pangnirtung belong to the Cumberland Sound population (Stewart 1994). The samples (n = 97) were collected between 1983 and 1987 from whales harvested by Inuit during annual subsistence hunts. Sixty-five samples were collected in Arviat, 17 in Grise Fjord, and 15 in Pangnirtung. Eight capelin samples were collected in Arviat in 1987 and 28 Arctic cod samples were collected in Resolute Bay in 1988.

56

T.C. Kelley et al.

Fig. 1 Map showing beluga harvest locations that took place at Grise Fiord, Pangnirtung and Arviat. Beluga from Grise Fiord are representative of the High Arctic population, whales from Pangnirtung are part of the Cumberland Sound population and whales from Arviat are from the western Hudson Bay population

Lipid and Fatty Acid Extraction Whole fish were homogenized for lipid extraction, whereas beluga blubber samples were first trimmed to remove oxidized surfaces, and sub-sampled for analysis. Lipids were extracted using 40 ml of 1:1 chloroform-methanol. The lipid phase was


57

collected, washed and filtered (using fiber-glass paper). This lipid phase was then used to prepare fatty acid methyl esters. The lipids were transesterfied using 5% methanolic HCl and the samples flushed with nitrogen gas then heated at 100°C for 90 min. The fatty acid methyl esters were extracted twice with distilled hexane and purified with toluene on Silica Gel G thin-layer plates. Methyl esters in hexane were analyzed using a Varian 2100 gas chromatograph converted to use Supelcowax 10 capillary glass columns (60 m × 0.75 ID). The peak areas were measured and converted to area percentage by a computing integrator (Shimadzu Chromatopak model C-R3A, Kyoto, Japan). Fatty acids were identified by relative retention times based on comparisons to authenticated fatty acid retention times, by use of log relative retention time versus carbon number plots, and by comparison of equivalent chain lengths as described by Jamieson (1975). Each fatty acid was described using the shorthand nomenclature of A:Bn-X, where A represents the number of carbon atoms, B the number of double bonds, and X the position of the double bond closest to the terminal methyl group.

Data Analysis Fatty acids were recorded as a percent of the total number of fatty acids present. Of the 107 fatty acids recorded, for subsequent analyses we used 29 fatty acids that are not manufactured by higher level predators, but are incorporated into the blubber as a result of consuming specific, identifiable prey items (Iverson et al. 2004). Fatty acid percents were log-transformed prior to the multivariate analyses (Kenkel 2006; Aitchison 1986). Iverson et al. (2004) developed the Quantitative Fatty Acid Signature Analysis (QFASA) method of quantifying the proportion of individual prey species consumed by predators by feeding captive seals a known diet. QFASA has not been calibrated for beluga or cetaceans, so we used principle components analysis (PCA) to perform a qualitative investigation of dietary preferences. PCA has been used to perform qualitative analyses of predator diets (e.g. Loseto et al. 2009; Dahl et al. 2000; Iverson et al. 1997), and though it cannot be used to make quantitative statements about prey consumption, it can provide some insight into the diet of predators. Fish species that plot close to beluga populations on a PCA score plot have relatively similar fatty acid profiles suggest they are important diet items to the particular beluga population (Dahl et al. 2000; Loseto et al. 2009).

Prey Species Identification First we compared fatty acid signatures of capelin (n = 8) and Arctic cod (n = 28) using a PCA with a covariance matrix (SYN-TAX© Ordination 2000). The method gives

58

T.C. Kelley et al.

equal weight to abundant and rare fatty acids which was necessary as many of the fatty acids accounted for less than 5% of the total fatty acid composition of the lipid. The PCA is a qualitative test that indicated five fatty acids could characterize Arctic cod and five characterized capelin. We compared these signatures quantitatively, to determine if the prey species had identifiable differences by comparing the mean proportion of the ten fatty acids found to be associated with both prey species (t-test).

Beluga Study Site Discrimination A discriminant function analysis (DFA) (SYSTAT 11®) was performed on beluga samples using the 29 fatty acids known to be incorporated into the blubber from prey with little biotransformation (Iverson et al. 2004). The purpose of this test was to determine if there was a significant difference in the diet among the beluga sampled from the three communities. The DFA showed significant differences between the three populations, so we tested the influence of Arctic cod and capelin consumption in the three populations by comparing the prevalence of ten representative prey fatty acids previously identified (five for each species) using an ANOVA. Significant differences in fatty acids profiles would suggest differences in the feeding behaviour of whales hunted near each community. We determined that there were significant differences between the fatty acids associated with Arctic cod and capelin in each of the communities so a PCA with a covariance matrix (SYN-TAX© Ordination 2000) was performed to determine which of the prey species most associated with the three beluga populations. This information was analysed qualitatively, by determining the graphical proximity of the prey species to the populations of beluga. Prey species situated in close proximity to a beluga population on the PCA was interpreted as being important in the diet of that population, while a prey species situated far from a population was interpreted as having low importance in the diet of that population.

Results Prey Species Identification The first two axes of the prey PCA explained 45.2% and 12.3% of the variance respectively with no overlap along the first PCA axis (PC 1) (Fig. 2). To typify each species we selected fatty acids with the largest absolute values on PC 1. The five fatty acids representative of Arctic cod included the 20 and 22 carbon length monounsaturates (20:1n7, 20:1n9, 22:1n9, 22:1n11, 22:1n7). The five fatty acids that represented capelin included several omega 6s (18:2n6, 16:0, 22:6n3, 22:5n6, and 20:4n6) (Fig. 2). T-tests comparing the ten fatty acids associated with Arctic cod


59

Fig. 2 (a) PCA plot of Arctic cod (Boreogaidus saida) and capelin (Mallotus villosus), and (b) the fatty acids contributing to the segregation. Fatty acids associated with Arctic cod are 22:1n9, 22:1n11, 22:1n7, 20:1n7 and 20:1n9. Fatty acids associated with capelin are 18:2n6, 16:0, 22:6n3, 22:5n6 and 20:4n6

and capelin showed the proportion of fatty acids associated with the two prey species were significantly different between capelin and Arctic cod (Fig. 3, all t-tests P £ 0.001).

60

T.C. Kelley et al.

Fig. 3 Select fatty acids representing capelin and Arctic cod. T-tests comparing the mean concentrations of these fatty acids showed they were all significantly different at P £ 0.001. All values have been log adjusted. Error bars represent 95% confidence intervals

Beluga Study Site Discrimination and Diet The discriminant function analysis showed the fatty acid profiles were significantly different among the three populations of beluga (Wilk’s Lambda = 0.056, F58, 132 = 7.304, P £ 0.001; Fig. 4). The fatty acid most strongly driving Factor 1 was 22:6n3. The fatty acid most strongly driving Factor 2 was 22:1n11. These fatty acids were representative of capelin and Arctic cod, respectively (Figs. 2 and 3). Eight of the ten fatty acids were significantly different; 20:4n6 and 20:1n7 were not significantly different between populations (Table 1). Post-hoc comparisons between populations showed that whales from Arviat had significantly higher concentrations of fatty acids associated with capelin (P = 0.05) than either Grise Fjord or Pangnirtung, and significantly lower concentrations of fatty acids associated with Arctic cod than the other two communities (P = 0.05, Fig. 5). They also showed significant differences between Arviat and Grise Fjord and Arviat and Pangnirtung for fatty acids 16:0, 22:6n3, 22:5n6, 22:1n9, 22:1n11, and 22:1n7, with no significant differences between Grise Fjord and Pangnirtung for these fatty acids. Fatty acids 18:2n6 and 20:1n9 were significantly different between all communities. In the combined prey and beluga PCA, 82.2% of the variance was explained by the first two PCA axes (PC 1: 54.9%; PC 2: 27.3%, Fig. 6). The beluga populations separated along the X axis with Arviat and Pangnirtung separating with little overlap, and Grise Fjord overlapping both populations. While the populations of beluga were


61

6 4

Factor 2

2 0 –2 –4 Arviat Grise Fjord Pangnirtung

–6 –8 –6

–4

–2

0

2

4

6

8

Factor 1

Fig. 4 Discriminant function analysis of beluga fatty acid profiles from western Hudson Bay (Arviat), High Arctic (Grise Fjord), and Cumberland Sound (Pangnirtung) populations. Significant differences among populations were indicated (Wilk’s Lambda = 0.056, F58, 132 = 7.304, P £ 0.001). The factor most strongly influencing the PC 1 was 22:6n3, which is associated with capelin. The factor influencing the PC 2 axis was 22:1n11, a fatty acid associated with Arctic cod. Ellipses represent 95% confidence levels

Table 1 Results of ANOVA comparison of selected fatty acids between beluga populations

Fatty acid

df

F

p

16:0 2, 94 40.513