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Keywords:

  • Arctic;
  • Bayesian mixing models;
  • marine mammals;
  • metabolic routing;
  • polar bears;
  • stable isotopes

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

1. Using measurements of naturally occurring stable isotopes in animal tissues is useful for monitoring diets of wide-ranging species that would otherwise be logistically difficult to evaluate. However, differential metabolic routing of macromolecules within a consumer can be problematic when using stable isotope analysis of bulk tissues to trace dietary input.

2. We used stable isotope (δ13C, δ15N) analysis to examine polar bear Ursus maritimus diet, which includes both lipid-rich blubber and the proteinaceous tissues of their marine mammal prey. Because the proportion of proteins and lipids consumed may depend on prey type and size, it was necessary to consider metabolic routing of these macromolecules separately in isotope mixing models.

3. Bayesian mixing models (MixSIR, version 1.04) were used to separately estimate protein (δ13C, δ15N) and lipid (δ13C) dietary inputs. We used existing knowledge of the relative lipid and protein intake for polar bears and isotopic information from both macromolecules to estimate overall diet composition.

4. The results for both male and female polar bears indicated that smaller prey (e.g. ringed seal Pusa hispida) contributed the largest proportion to the protein-metabolic pathway. In contrast, the largest proportion of the lipid-metabolic pathway for both sexes tended to consist of larger prey (e.g. bearded seal Erignathus barbatus).

5. The diet composition of male polar bears consisted of more large than small prey. Diet estimates for females overlapped to some degree with males but tended to consist of less large prey.

6.Synthesis and applications. Monitoring polar bear diet may help determine the effects of climate-induced environmental changes in Arctic marine ecosystems including shifts in prey composition. Additionally, tracing origins of anthropogenic pollutants is currently a priority for wildlife managers concerned with the health of marine mammals. However, our results indicate using stable isotopes to infer dietary inputs when proportions of macromolecules fluctuate amongst food sources requires the sampling and analysis of multiple tissues representing distinct macromolecular metabolic pathways. In such cases, utilizing only proteinaceous tissues for analysis will result in erroneous dietary source estimates and inaccuracies when examining trophic-level transfer of contaminants, especially those that are lipophylic.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Conventional methods of investigating animal diets have included the examination of stomach contents, faecal analysis and direct observation of feeding. Because of biases and limitations associated with each of these methods (Reynolds & Aebischer 1991; Spaulding, Krausman & Ballard 2000; Redpath et al. 2001), researchers have increasingly employed measurements of naturally occurring endogenous tracers such as stable isotopes. Stable isotope techniques have been used to reconstruct both paleo and contemporary diets of a variety of species (West et al. 2006; Fox-Dobbs, Leonard & Koch 2008) and also to examine food web structure, niche breadth and contaminant pathways (Newsome et al. 2007; Schmidt et al. 2007; Cardona-Marek et al. 2009). The application of stable isotope methods to estimate dietary contributions or trophic level is possible because consumer tissue isotope values reflect those in their diet and thus act as ecological tracers throughout the food web (Deniro & Epstein 1978, 1981; Tieszen & Boutton 1989). Diet reconstruction using stable isotopes is advantageous because it allows evaluation of assimilated nutrients over ecologically relevant time-scales rather than just recently ingested items (Tieszen et al. 1983; Hobson & Clark 1992). The ability to examine previously assimilated nutrients from tissue samples is particularly useful for monitoring wide-ranging or migratory species whose diets would otherwise be logistically difficult and costly to evaluate for extended time periods. Stable isotope analysis is therefore a useful technique for examining the diet of highly mobile marine predators such as polar bears Ursus maritimus Phipps 1774.

The diet of polar bears inhabiting the Arctic sea ice is primarily composed of marine mammals and consists of blubber augmented with muscle and other proteinaceous tissues such as skin and viscera (Lønø 1970; Stirling & McEwan 1975; Stirling & Archibald 1977). Blubber in marine mammals is principally composed of lipid and contains little protein, whereas muscle tissue is a significant source of protein but contains limited amounts of lipid (Best 1985; Beck, Smith & Hammill 1993; Gales, Renouf & Noseworthy 1994). Within a bear, protein and lipid may be differentially routed because it is metabolically more efficient to utilize dietary lipid for endogenous lipid stores and energy, and dietary proteins for body protein synthesis (Pond 1981; Hobson & Bairlein 2003; Wortinger 2007). Therefore, stable isotope diet studies should consider that isotopes from different dietary components are not distributed uniformly amongst a bear’s tissues (Schwarcz 1991; Phillips & Koch 2002; Martinez del Rio et al. 2009). As a result, polar bear tissues may not reflect isotopic composition of the overall diet, but rather the composition of specific dietary macromolecules preferentially used to synthesize a given tissue type (Gannes, Obrien & Delrio 1997; Hobson & Stirling 1997; Podlesak & McWilliams 2006; Voigt et al. 2008; Hobson, Stirling & Andriashek 2009).

Stable isotope diet studies have typically used proteinaceous tissues with lipids removed to represent the diet of polar bears as a wholly carnivorous diet of marine mammal muscle and blubber (Bentzen et al. 2007, 2008). However, using such a protein-metabolic pathway to draw inferences regarding the overall diet of a consumer is only valid if the proportion of protein to lipid consumed is the same from all prey sources. Best (1985) reports that two captive polar bears given the opportunity to regulate their consumption of muscle and blubber over a 5-month period consumed c. 20% muscle and 80% blubber. These estimates for protein intake are similar to the long-term protein requirements for the closely related grizzly bear U. arctos (Felicetti, Robbins & Shipley 2003). However, even though bears regulate their protein intake to meet, but not exceed, physiological requirements over long time periods (Robbins et al. 2007), the ratio of lipid to protein consumed by polar bears during each feeding event may depend on prey type and size. Polar bears preferentially consume the blubber portion of a carcass (Stirling 1974; Stirling & McEwan 1975; Stirling & Archibald 1977) and large prey often consists of enough blubber to satiate a polar bear. In addition, the intake of protein vs. lipid during scavenging events will depend on how much of a carcass remains, which may also be related to prey type and size.

Polar bears in the Beaufort Sea have access to four species of marine mammal prey: ringed seals Pusa hispida Schreber 1775, bearded seals Erignathus barbatus Erxleben 1777, beluga whales Delphinapterus leucas Pallas 1776 and bowhead whales Balaena mysticetus Linnaeus 1758; however, consumption of bowhead and most consumption of beluga whales is through scavenging. We hypothesized polar bears would consume proportionately more lipid when eating large prey such as bearded seals, beluga whales, and bowhead whales and conversely, would consume proportionately more protein from small prey (i.e. ringed seals, Fig. 1). To test this hypothesis, we separately analysed and compared the isotopic composition of dietary protein and lipid by using both proteinaceous and lipid tissue samples. We predicted that isotopic diet reconstruction using proteinaceous tissues would indicate a greater consumption of small prey than would methods utilizing lipid tissues. Current estimates of the approximate consumption of protein and lipid by polar bears were then used to combine mixing model source estimates for each tissue type to determine polar bear diet. Combined models incorporating both protein- and lipid-metabolic pathways were compared with those using the more orthodox approach of analysing proteinaceous tissues only.

image

Figure 1.  Photographs of various type and size of prey commonly eaten by polar bears in the Beaufort Sea. Prey items are shown in order of size, smallest to largest. (a) Newborn ringed seal pup (muscle and small amount of blubber available can be consumed by a polar bear in one meal), (b) adult ringed seal (muscle and blubber components can be eaten by a polar bear in one meal), (c) adult bearded seal (blubber alone can satiate a polar bear) and (d) bowhead whale carcass (blubber alone can satiate several polar bears). A pencil (14 cm) in photograph (a) and saw (47 cm) in photographs (b) and (c) are shown for size references.

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Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Collection of polar bear and prey tissues

Adult polar bears (≥5 years; 21 male, 26 female) were captured on sea ice over the continental shelf in the southern Beaufort Sea (Fig. S1, Supporting information). Bears were located using a helicopter and immobilized via remote injection (Stirling, Spencer & Andriashek 1989). All polar bear captures occurred between 6 April and 9 May 2005. Animal handling procedures were approved by the University of Alberta Biological Sciences Animal Policy and Welfare Committee. Blood was drawn from the femoral vein into sterile Vacutainer® tubes with no additives. Adipose tissue samples were collected from the rump of each bear using 8 mm biopsy punches. A vestigial premolar removed at capture was used to determine age (Calvert & Ramsay 1998). Muscle and blubber samples were collected from potential prey species of polar bears throughout the Beaufort Sea from 2003 to 2007 (Table 1). Ringed seal and bearded seal samples were collected opportunistically from the remains of seals that had been killed by polar bears. Beluga and bowhead whale tissues were sampled from Inuit community-based harvests throughout the southern Beaufort Sea.

Table 1.   The mean δ13C and δ15N values of tissues collected from adult male and female polar bears and potential prey sources in the Beaufort Sea, 2003–2007
SpeciesTissuenMean δ13C (‰) ±SEMean δ15N (‰) ±SE
Ringed sealMuscle45−20·6 ± 0·118·3 ± 0·2
Blubber34−27·0 ± 0·1
Bearded sealMuscle10−17·8 ± 0·416·8 ± 0·3
Blubber7−25·5 ± 0·5
Beluga whaleMuscle11−18·1 ± 0·117·7 ± 0·2
Blubber10−24·4 ± 0·1
Bowhead whaleMuscle3−19·2 ± 0·214·3 ± 0·6
Blubber3−26·1 ± 0·6
Polar bear (male)Whole blood21−19·3 ± 0·120·3 ± 0·1
Adipose21−25·7 ± 0·1
Polar bear (female)Whole blood26−19·6 ± 0·120·6 ± 0·1
Adipose26−26·2 ± 0·1

Stable isotope analysis

Muscle from prey and whole blood from polar bears were freeze-dried and then soaked in a 2:1 chloroform : methanol solution to remove lipids prior to analysis. Adipose tissue samples from polar bears and blubber from prey were soaked in the same solvent mixture to obtain lipids for isotope analysis (Bond, Esler & Hobson 2007). Muscle and blood samples were homogenized into a powder with a mortar and pestle. Approximately 1 mg of each muscle and blood sample and 0·6 mg of each lipid sample were weighed into tin capsules and combusted in a Europa 20 : 20 continuous-flow isotope-ratio mass spectrometer (Department of Soil Sciences, University of Saskatchewan). Laboratory standards of whale baleen (BWB II) and egg albumen were analysed for every five unknowns. Based on standard deviations of within-run replicate measurements of standards, analytical error was estimated to be ±0·1‰ for δ13C and δ15N measurements. Stable isotope values are presented in the standard δ-notation as parts per thousand (‰) relative to Vienna Pee Dee Belemnite (δ13C) and atmospheric air (δ15N) standards.

Statistical analyses and isotope mixing models

We used stable isotope mixing models to estimate the contribution of carbon and nitrogen from various prey to polar bear tissues. For n isotopes and >n + 1 possible dietary sources, no unique solution is possible (Phillips & Gregg 2003; Moore & Semmens 2008). However, probability based models are available to constrain the range of potential prey inputs in these cases. We used MixSIR (version 1.04), a stable isotope source-partitioning mixing model that utilizes a Bayesian framework to estimate the probability distributions of the proportional contribution for each possible prey source (Moore & Semmens 2008). All our models were run with uninformative priors (Moore & Semmens 2008).

We assessed the relative contribution of each prey source to both the protein- and lipid-metabolic pathways in polar bears by conducting separate stable isotope mixing models for each macromolecule pathway. For protein, mean prey isotope values for lipid-free muscle and associated standard deviations were used as source data and isotope values from lipid-free polar bear whole blood represented the consumer mixture. In the lipid-mixing models, mean isotope values and the associated standard deviations from prey blubber lipid were used as source data and isotope values from polar bear adipose lipid represented the consumer mixture. Because lipid is nitrogen-deficient (Bearhop et al. 2002; Minami & Nakamura 2005; Camin et al. 2007), only δ13C values could be used to assess source contributions to the lipid-metabolic pathway.

We constructed and compared single (δ13C) and dual (δ13C and δ15N) isotope mixing models for the polar bear protein pathway. This comparison was conducted to determine if the inclusion of additional isotope values available in proteinaceous tissues (i.e. δ15N) would confound comparisons between protein- and lipid-based mixing models. Before constructing single isotope mixing models, δ13C values of male and female polar bears were compared using separate Student’s t-tests for blood and lipid. When δ13C values differed significantly in either blood or lipid, males and females were treated as separate consumers and thus each had their own set of mixing models. Similarly, before constructing dual-isotope mixing models, a Hotelling’s T2-test was used to compare blood δ13C and δ15N values simultaneously between male and female polar bears. Separate mixing models were used when significant differences occurred. These two-isotope protein-based mixing model results were used in combination with source estimates from the lipid-based models to determine the diet of polar bears.

Because the gross composition of polar bear diet was estimated to be 20% muscle and 80% blubber (Best 1985), we multiplied the estimated contributions of each source in the protein- and lipid-metabolic pathways by 0·20 and 0·80, respectively, to estimate the proportions of protein and lipid consumed from each prey relative to total protein and lipid intake. Estimated source contributions from each metabolic pathway were then combined by adding the lower and upper values from the range of feasible solutions for matching sources in each pathway to establish a minimum and maximum contribution for each prey to the overall diet. We were interested in examining the contribution of small prey (ringed seal) relative to large prey (bearded seal, beluga whale and bowhead whale) in each metabolic pathway, so we aggregated large prey source contributions a posteriori to constrain the number of sources in our mixing model results (Phillips, Newsome & Gregg 2005). We also performed an a posteriori aggregation of large prey on the overall diet estimates for polar bears that combined results from the protein- and lipid-metabolic pathways.

There are no data on diet-tissue isotopic discrimination values for polar bears fed a known diet. However, we extracted values from published data for captive carnivores feeding on known carnivorous diets (i.e. animal flesh) to estimate discrimination factors between prey muscle and polar bear whole blood. We used the mean of 18 carbon and nitrogen red blood cell and serum discrimination factors from a table summarizing published values in Caut, Angulo & Courchamp (2009). The discrimination values utilized were for marine and terrestrial carnivores, which included black bears U. americanus, grizzly bears and a variety of seal species (Hilderbrand et al. 1996; Hobson et al. 1996; Kurle 2002; Lesage, Hammill & Kovacs 2002; Felicetti et al. 2003). Values of 1·21‰ (SD = 0·85) for δ13C and 2·75‰ (SD = 1·03) for δ15N were derived and added to isotope values for all prey muscle samples. We assumed no discrimination between prey lipid and polar bear lipid (Gannes, Obrien & Delrio 1997; Podlesak & McWilliams 2007; Hobson, Stirling & Andriashek 2009).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Male polar bears had higher blood and lipid δ13C values than females (blood, t = 3·15, d.f. = 45, < 0·01; lipid, t = 3·72, d.f. = 45, < 0·001) (Table 1); therefore sex-specific δ13C protein- and lipid-metabolic pathway mixing models were created. When blood δ13C and δ15N values of males and females were compared simultaneously, there were also significant differences (Hotelling’s T2 : F2,44 = 8·67, < 0·001) and thus separate two-isotope (δ13C and δ15N) protein-metabolic pathway mixing models were used for each sex. Sample sizes for prey lipid were often smaller than sample sizes for muscle because virtually all of the blubber had been consumed at many kills (Table 1). For all mixing models we present results before and after aggregation of large prey. Source estimates subsequent to aggregating large prey are presented to demonstrate the combination of results from the protein- and lipid-metabolic pathways (Fig. 2). The same methods for combining estimates from both metabolic pathways were used on source estimates for all individual prey (summarized in Table 2). Source estimates from single isotope (δ13C) protein-mixing models had substantial overlap with estimates from dual-isotope (δ13C and δ15N) protein-mixing models (Table 2). Therefore, inclusion of δ15N in dual-isotope protein models was unlikely to confound comparisons between results from protein- and lipid-metabolic pathways.

image

Figure 2.  Flow chart diagram showing contributions of protein and lipid from ringed seals and large prey to (a) adult male polar bears and (b) adult female polar bears. Source contributions were estimated separately for protein- and lipid-metabolic pathways and represent 5th to 95th percentiles of MixSIR estimates. All large prey sources were combined a posteriori (Phillips, Newsome & Gregg 2005). The contributions to the protein-metabolic pathway were adjusted to amount to 20% of the overall diet, whereas contributions to the lipid-metabolic pathway were adjusted to amount to 80% (based on Best 1985).

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Table 2.   The estimated contribution of potential prey to the protein- and lipid-metabolic pathways of female and male polar bears in the Beaufort Sea. The results shown are prior to combining all large-bodied prey and represent 5th to 95th percentiles of MixSIR estimates
Polar bear sexPrey sourceMetabolic pathwayIsotope(s)Contribution (%) to each pathwayContribution to overall diet (weighted by pathway*) (%)Total contribution (%)
  1. *Contributions to the protein-metabolic pathway (two-isotope models only) were adjusted to amount to 20% of the overall diet, whereas contributions to the lipid-metabolic pathway were adjusted to amount to 80% (based on Best 1985).

FemaleRinged sealProteinδ13C75–93 33–70
Proteinδ13C, δ15N73–8815–18
Lipidδ13C22–6518–52
Bearded sealProteinδ13C0–9 2–32
Proteinδ13C, δ15N0–110–2
Lipidδ13C2–382–30
Beluga whaleProteinδ13C0–10 1–22
Proteinδ13C, δ15N0–130–3
Lipidδ13C1–241–19
Bowhead whaleProteinδ13C1–20 2–51
Proteinδ13C, δ15N2–190–4
Lipidδ13C2–592–47
MaleRinged sealProteinδ13C62–86 15–44
Proteinδ13C, δ15N63–7813–16
Lipidδ13C2–352–28
Bearded sealProteinδ13C0–13 2–41
Proteinδ13C, δ15N0–140–3
Lipidδ13C3–472–38
Beluga whaleProteinδ13C0–15 10–33
Proteinδ13C, δ15N1–170–3
Lipidδ13C13–3810–30
Bowhead whaleProteinδ13C2–32 3–52
Proteinδ13C, δ15N7–271–5
Lipidδ13C3–592–47

For both sexes, results from the protein-metabolic pathway mixing models differed from those of the lipid-metabolic pathway mixing models, indicating that each prey did not contribute equally to both metabolic pathways (Tables 2, Fig. 3). Protein-based models predicted a higher contribution from ringed seals than lipid-based models, with ringed seals being the highest contributor to the dietary protein intake of both male and female polar bears. Lipid-metabolic pathway mixing models for males predicted a higher contribution of lipid from large prey compared with ringed seals. Source estimates for female lipid intake also tended towards more large prey; however, there was substantial overlap between ringed seal and large prey estimates. Overall diet of males consisted of a greater proportion of prey larger than ringed seals. Estimates for the proportion of ringed seals vs. large prey in the overall diet of females overlapped. However, overall dietary source estimates for females tended towards more ringed seals when compared with overall diet estimates for males. Results using previous methods of analysing only proteinaceous tissues (see ovals in Fig. 2 from the protein pathway) tended to overestimate the proportion of small prey and underestimate the amount of large prey. These discrepancies between the protein-only source estimates vs. those using combined protein and lipid estimates were greatest for males.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Carnivores consume both lipid and protein from their prey and these macromolecules may be preferentially routed to analogous tissues within their bodies (Ambrose & Norr 1993; Tieszen & Farge 1993). Most studies of predator foraging using stable isotopes generally assume the amount of lipid ingested is either negligible or that the ratio of protein to lipid consumed is equal across prey types. The results of our mixing models indicate that such assumptions may not hold true and support the prediction that dietary protein and lipid are preferentially routed within the predator. Polar bear diet estimates derived from the protein- and lipid-metabolic pathways differed substantially and because results were similar for the single (δ13C) and dual-isotope (δ13C and δ15N) protein-mixing models, the addition of δ15N measurements to protein-mixing models could not account for this difference. Protein-based models for both sexes of polar bears predicted greater contributions of small-bodied prey (ringed seals) when compared with lipid-based models. Unequal intake of protein and lipid amongst various types and sizes of prey is likely to be the main cause of differing source estimates between the protein- and lipid-based stable isotope mixing models.

Polar bears are capable of consuming up to 20% of their body mass in a single meal (Best 1977), which in the Beaufort Sea would be c. 40 kg for adult females and 84 kg for adult males (based on Derocher 1991). The body mass of small prey such as ringed seals allows adult polar bears to consume all edible proteinaceous and lipid tissue in one feeding event (Stirling & McEwan 1975). In contrast to ringed seals, larger prey consists of enough lipid tissue to satiate a polar bear. Adult bearded seals, based on data from a similar sized northern phocid seal, the hooded seal Cystophora cristata, would have roughly 80 kg of lipid tissue available for consumption (Kovacs et al. 1996). Beluga or bowhead whales (total body mass of 1500–100 000 kg; O’Corry-Crowe 2002; Rugh & Shelden 2002) would also allow bears to become satiated on lipid tissue alone, sometimes for many days in succession.

The availability of young ringed seal pups prior to the onset of sampling polar bear tissues in the spring may also have contributed to the proportionately higher amount of ringed seals in the protein relative to lipid portion of the diet. Ringed seal pups are born throughout late March and April and newborns have relatively small amounts of lipid (Stirling & McEwan 1975; Lydersen, Hammill & Ryg 1992; Lydersen & Hammill 1993). Consequently, ringed seal pups probably contribute proportionately more protein to the diet of polar bears relative to other prey items (Fig. 1). In contrast, the bearded seal pupping season does not begin until early May (Smith 1981; Watanabe et al. 2009) making it unlikely that polar bear tissues sampled for this study would contain significant amounts of assimilated nutrients from bearded seal pups.

Polar bears in the Beaufort Sea reach their lightest weights in late winter and then rely on a 2–3 month hyperphagic period, during optimal seal hunting conditions that occur in the spring, to gain adipose reserves necessary to ensure survival through the rest of the year (Stirling & Øritsland 1995; Stirling 2002). Therefore, our adipose biopsies collected in April and May likely represented recently acquired nutrients and not long-term endogenous reserves. Blood samples were also likely to represent recently acquired nutrients because the half-life of red blood cells is about 28 days in captive black bears Ursus americanus (Hilderbrand et al. 1996). The specific isotopic turnover of whole blood and adipose tissue in polar bears is unknown. However, laboratory experiments indicate adipose tissue and whole blood have similar isotopic turnover rates in small mammals (Tieszen et al. 1983; MacAvoy, Macko & Arneson 2005). For these reasons, it is reasonable to assume that our polar bear blood and adipose tissue samples were representative of isotopic diet contributions over the same time period.

In contrast to protein intake, consumption of lipid by male polar bears was predominantly from large prey and their overall diet also reflected a higher proportion of large prey compared with adult females. Because diet estimates using fatty acid analysis indicate males eat a higher proportion of bearded seals relative to females (Thiemann et al. 2007; Thiemann, Iverson & Stirling 2008), it is likely that a large portion of their large prey isotopic signal resulted from bearded seals. Polar bears display a high degree of sexual dimorphism with adult females being approximately half the size of adult males (Derocher & Wiig 2002; Derocher, Andersen & Wiig 2005). Therefore, it is less likely for females to be able to prey on bearded seals, especially adults (Stirling & Derocher 1990; Thiemann, Iverson & Stirling 2008). Estimates of the proportion of small vs. large prey for the lipid-metabolic pathway, and consequently the overall diet, of female polar bears were less conclusive than for males due to a high degree of overlap in mixing model source estimates. Nonetheless, it is clear that both small and large prey are important to the overall diet of female polar bears. However, we suggest that much of the large prey consumed by females resulted from scavenging.

Proteins and lipids often serve different nutritional needs in wild animals and their relative importance is expected to vary depending on age, growth, and reproductive stage (Krapu 1981; Beck, Bowen & Iverson 2003; Parker, Barboza & Gillingham 2009). In high latitude marine systems, diets rich in lipids are often of crucial importance to a wide array of taxa as a form of energy and as a means of providing insulation (Young 1976; Prestrud & Nilssen 1992; Harington 2008). The accurate evaluation of which prey provides protein and lipid sources to consumers in these systems is therefore fundamental to understanding their nutritional ecology. The isotope approach presents a relatively new means of quantifying the origins of these two fundamental macromolecules in animal diets. However, failure to consider both protein and lipid contributions to higher-order consumers such as polar bears could result in overestimating the importance of some food sources and underestimating or excluding key nutritional inputs. Thus, conservation biologists interested in using isotope techniques to examine predator–prey relationships and identify food resources for species of conservation concern need to consider which tissues should be sampled to adequately measure the contributions of all dietary macronutrients. Our methods should also be considered in light of seasonal changes to dietary macromolecular composition. For example, migratory birds tend to consume lipid-rich diets during stopover feeding events (Blem 1980; Bairlein 1998) and failure to incorporate contributions to the lipid-metabolic pathways during seasonal migrations is likely to result in erroneous diet estimates using stable isotope measurements.

In this study, similarities between source estimates provided by the lipid pathway and those for the overall diet were probably due to the greater weight (80%) we placed on the lipid pathway based on previous studies of bear nutrition. However, in some instances, weights given to each metabolic pathway may need to be altered. For example, subadult bears have higher protein requirements and intakes because they are still growing and their smaller size, combined with their inexperience at hunting, makes them reliant on scavenging the largely proteinaceous remains of kills made by other polar bears (Stirling & McEwan 1975; Derocher, Lunn & Stirling 2004). Additionally, an individual’s ability to optimize protein and lipid intake may depend upon the availability of various prey species, which fluctuates with seasonal sea ice dynamics (Stirling & McEwan 1975; Derocher et al. 1990; Polischuk, Norstrom & Ramsay 2002). During spring, polar bears are typically in a hyperphagic period (Ramsay & Stirling 1988; Derocher & Taylor 1994); however, at other times of the year when hunting efficiencies are lower, bears may not always be able to maximize lipid intake.

Understanding the diet of upper-level marine mammals is of particular importance for conservation management, examinations of contaminant exposure and monitoring for shifts to ecosystem structure (Loseto et al. 2009). Climate-induced changes to predator–prey relationships may cause major adjustments to Arctic marine ecosystems (Higdon & Ferguson 2009) and changes in foraging behaviour have already been observed in polar bears (Stirling et al. 2008; Cherry et al. 2009). Effective monitoring of Arctic marine ecosystems will be facilitated by surveying top predators, which will allow wildlife managers to respond in a proactive manner. Intrinsic tracers in the form of stable isotope measurements offer a practical means of monitoring diet composition of polar bears and many other species of conservation concern. However, the results of this study indicate that previous methods of only isotopically analysing proteinaceous tissues will not accurately estimate the proportion of various prey species to the overall diet of polar bears. The methods we present for combining source estimates from multiple metabolic pathways to more accurately reflect the overall diet have implications for stable isotope practitioners examining diet in any species that gain disproportionate amounts of dietary macromolecules from various food sources. For example, other bears (e.g. Fortin et al. 2007) as well as marine predators such as killer whales Orcinus orca and seals consume varying proportions of lipid and protein from different sizes and types of prey (Jefferson, Stacey & Baird 1991; Budge et al. 2002; Herman et al. 2005). In addition, careful consideration should be given to choosing appropriate tissues for stable isotope analysis when examining relationships between diet and contaminant exposure (i.e. Krahn et al. 2007; McHugh et al. 2007; Bentzen et al. 2008). It is inappropriate to use only stable isotope tracers from proteinaceous tissues when making dietary inferences related to trophic level contaminant transfer because many contaminants primarily accumulate in lipid (Jarman et al. 1996; AMAP 2002; Gray 2002) and because we have demonstrated a decoupling of the protein- and lipid-metabolic pathways. However, separately analysing and then combining contributions to individual metabolic pathways requires reasonable estimates of the proportion of various macromolecules in the overall diet. In addition to field-based investigations, feeding experiments with captive animals aimed at measuring the consumption of various macromolecules in simulated ecological and physiological scenarios are required to refine the use of isotopic tracers for diet reconstruction.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

We especially thank Dennis Andriashek and Evan Richardson for assistance with field work and collection of specimens. We thank Lisa Loseto, Department of Fisheries and Oceans Canada, Derek Muir, Environment Canada, and Tuktoyaktuk Hunters and Trappers Committee for providing whale tissue samples. Photograph D, Fig. 1, was provided by Susanne Miller, United States Fish and Wildlife Service. We gratefully acknowledge financial and logistic support from ArcticNet, Canadian Wildlife Federation, Canadian Wildlife Service, Circumpolar/Boreal Alberta Research, Inuvialuit Game Council, Natural Sciences and Engineering Research Council of Canada, Northern Scientific Training Program, Northwest Territories Department of Environment and Natural Resources, Polar Continental Shelf Project, Polar Bears International, United States Geological Survey, and World Wildlife Fund (Canada).

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
  • AMAP. (2002) AMAP Assessment: Persistent Organic Pollutants in the Arctic. Arctic Monitoring and Assessment Programme 2004, Oslo, Norway.
  • Ambrose, S.H. & Norr, L. (1993) Experimental evidence for the relationship of the carbon isotope ratios of whole diet and dietary protein to those of bone collagen and carbonate. Prehistoric Human Bone-Archaeology at the Molecular Level (eds J.B.Lambert & G.Grupe), pp. 137. Springer-Verlag, Berlin, Germany.
  • Bairlein, F. (1998) The effect of diet composition on migratory fuelling in garden warblers (Sylvia borin). Journal of Avian Biology, 29, 546551.
  • Bearhop, S., Waldron, S., Votier, S.C. & Furness, R.W. (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiological and Biochemical Zoology, 75, 451458.
  • Beck, C.A., Bowen, W.D. & Iverson, S.J. (2003) Sex differences in the seasonal patterns of energy storage and expenditure in a phocid seal. Journal of Animal Ecology, 72, 280291.
  • Beck, G.G., Smith, T.G. & Hammill, M.O. (1993) Evaluation of body condition in the northwest Atlantic harp seal (Phoca groenlandica). Canadian Journal of Fisheries and Aquatic Sciences, 50, 13721381.
  • Bentzen, T.W., Follmann, E.H., Amstrup, S.C., York, G.S., Wooller, M.J. & O’Hara, T.M. (2007) Variation in winter diet of southern Beaufort Sea polar bears inferred from stable isotope analysis. Canadian Journal of Zoology, 85, 596608.
  • Bentzen, T.W., Follmann, E.H., Amstrup, S.C., York, G.S., Wooller, M.J., Muir, D.C.G. & O’Hara, T.M. (2008) Dietary biomagnification of organochlorine contaminants in Alaskan polar bears. Canadian Journal of Zoology, 86, 177191.
  • Best, R.C. (1977) Ecological energetics of the polar bear (Ursus maritimus). Proceedings of the 1975 Predator Symposium (eds R.L.Phillips & C.Jonkel), pp. 203211. University of Montana Press, Missoula.
  • Best, R.C. (1985) Digestibility of ringed seals by the polar bear. Canadian Journal of Zoology, 63, 10331036.
  • Blem, C.R. (1980) The energetics of migration. Animal Migration, Orientation and Navigation (ed. S.A.Gautreaux), pp. 125218. Academic Press, Toronto, Canada.
  • Bond, J.C., Esler, D. & Hobson, K.A. (2007) Isotopic evidence for sources of nutrients allocated to clutch formation by harlequin duck. The Condor, 109, 698704.
  • Budge, S.M., Iverson, S.J., Bowen, W.D. & Ackman, R.G. (2002) Among- and within-species variability in fatty acid signatures of marine fish and invertebrates on the Scotian Shelf, Georges Bank, and southern Gulf of St. Lawrence. Canadian Journal of Fisheries and Aquatic Sciences, 59, 886898.
  • Calvert, W. & Ramsay, M.A. (1998) Evaluation of age determination of polar bears by counts of cementum growth layer groups. Ursus, 10, 449453.
  • Camin, F., Bontempo, L., Heinrich, K., Horacek, M., Kelly, S.D., Schlicht, C., Thomas, F., Monahan, F.J., Hoogewerff, J. & Rossmann, A. (2007) Multi-element (H,C,N,S) stable isotope characteristics of lamb meat from different European regions. Analytical and Bioanalytical Chemistry, 389, 309320.
  • Cardona-Marek, T., Knott, K.K., Meyer, B.E. & O’Hara, T.M. (2009) Mercury concentrations in southern Beaufort Sea polar bears: variation based on stable isotopes of carbon and nitrogen. Environmental Toxicology and Chemisry, 28, 14161424.
  • Caut, S., Angulo, E. & Courchamp, F. (2009) Variation in discrimination factors (Delta N-15 and Delta C-13): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology, 46, 443453.
  • Cherry, S.G., Derocher, A.E., Stirling, I. & Richardson, E. (2009) Fasting physiology of polar bears in relation to environmental change and breeding behavior in the Beaufort Sea. Polar Biology, 32, 383391.
  • Deniro, M.J. & Epstein, S. (1978) Influence of diet on distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42, 495506.
  • Deniro, M.J. & Epstein, S. (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta, 45, 341351.
  • Derocher, A.E. (1991) Population dynamics and ecology of polar bears in western Hudson Bay. PhD dissertation, Univeristy of Alberta, Edmonton.
  • Derocher, A.E., Andersen, M. & Wiig, Ø. (2005) Sexual dimorphism of polar bears. Journal of Mammalogy, 86, 865901.
  • Derocher, A.E., Lunn, N.J. & Stirling, I. (2004) Polar bears in a warming climate. Integrative and Comparative Biology, 44, 163176.
  • Derocher, A.E. & Taylor, M.K. (1994) Density-dependent population regulation of polar bears. In: T.MK (ed.) Density-Dependent Population Regulation Of Black, Brown, and Polar Bears. International Conference on Bear Research and Management Monograph Series, 3, 2530.
  • Derocher, A.E. & Wiig, Ø. (2002) Postnatal growth in body length and mass of polar bears (Ursus maritimus) at Svalbard. Journal of Zoology, 256, 343349.
  • Derocher, A.E., Nelson, R.A., Stirling, I. & Ramsay, M.A. (1990) Effects of fasting and feeding on serum urea and serum creatinine levels in polar bears. Marine Mammal Science, 6, 196203.
  • Felicetti, L.A., Robbins, C.T. & Shipley, L.A. (2003) Dietary protein content alters energy expenditure and composition of the mass gain in grizzly bears (Ursus arctos horribilis). Physiological and Biochemical Zoology, 76, 256261.
  • Felicetti, L.A., Schwartz, C.C., Rye, R.O., Haroldson, M.A., Gunther, K.A., Phillips, D.L. & Robbins, C.T. (2003) Use of sulfur and nitrogen stable isotopes to determine the importance of whitebark pine nuts to Yellowstone grizzly bears. Canadian Journal of Zoology, 81, 763770.
  • Fortin, J.K., Farley, S.D., Rode, K.D. & Robbins, C.T. (2007) Dietary and spatial overlap between sympatric ursids relative to salmon use. Ursus, 18, 1929.
  • Fox-Dobbs, K., Leonard, J.A. & Koch, P.L. (2008) Pleistocene megafauna from eastern Beringia: paleoecological and paleoenvironmental interpretations of stable carbon and nitrogen isotope and radiocarbon records. Palaeogeography, Palaeoclimatology, Palaeoecology, 261, 3046.
  • Gales, R., Renouf, D. & Noseworthy, E. (1994) Body composition of harp seals. Canadian Journal of Zoology, 72, 545551.
  • Gannes, L.Z., Obrien, D.M. & Delrio, C.M. (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology, 78, 12711276.
  • Gray, J.S. (2002) Biomagnification in marine systems: the perspective of an ecologist. Marine Pollution Bulletin, 45, 4652.
  • Harington, C.R. (2008) The evolution of Arctic marine mammals. Ecological Applications, 18, S23S40.
  • Herman, D.P., Burrows, D.G., Wade, P.R., Durban, J.W., Matkin, C.O., LeDuc, R.G., Barrett-Lennard, L.G. & Krahn, M.M. (2005) Feeding ecology of eastern North Pacific killer whales (Orcinus orca) from fatty acid, stable isotope and organochlorine analyses of blubber biopsies. Marine Ecology Progress Series, 302, 275291.
  • Higdon, J.W. & Ferguson, S.H. (2009) Loss of Arctic sea ice causing punctuated change in sightings of killer whales (Orcinus orca) over the past century. Ecological Applications, 19, 13651375.
  • Hilderbrand, G.V., Farley, S.D., Robbins, C.T., Hanley, T.A., Titus, K. & Servheen, C. (1996) Use of stable isotopes to determine diets of living and extinct bears. Canadian Journal of Zoology, 74, 20802088.
  • Hobson, K.A. & Bairlein, F. (2003) Isotopic fractionation and turnover in captive Garden Warblers (Sylvia borin): implications for delineating dietary and migratory associations in wild passerines. Canadian Journal of Zoology, 81, 16301635.
  • Hobson, K.A. & Clark, R.G. (1992) Assessing avian diets using stable isotopes 1. Turnover of C-13 in tissues. Condor, 94, 181188.
  • Hobson, K.A. & Stirling, I. (1997) Low variation in blood delta C-13 among Hudson Bay polar bears: implications for metabolism and tracing terrestrial foraging. Marine Mammal Sciences, 13, 359367.
  • Hobson, K.A., Stirling, I. & Andriashek, D.S. (2009) Isotopic homogeneity of breath CO2 from fasting and berry-eating polar bears: implications for tracing reliance on terrestrial foods in a changing Arctic. Canadian Journal of Zoology, 87, 5055.
  • Hobson, K.A., Schell, D.M., Renouf, D. & Noseworthy, E. (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Canadian Journal of Fisheries and Aquatic Sciences, 53, 528533.
  • Jarman, W.M., Hobson, K.A., Sydeman, W.J., Bacon, C.E. & McLaren, E.B. (1996) Influence of trophic position and feeding location on contaminant levels in the Gulf of the Farallones food web revealed by stable isotope analysis. Environmental Science and Technology, 30, 654660.
  • Jefferson, T.A., Stacey, P.J. & Baird, R.W. (1991) A review of killer whale interactions with other marine mammals: predation to co-existence. Mammal Review, 21, 151180.
  • Kovacs, K.M., Lydersen, C., Hammill, M. & Lavigne, D.M. (1996) Reproductive effort of male hooded seals (Cystophora cristata): estimates from mass loss. Canadian Journal of Zoology, 74, 15211530.
  • Krahn, M.M., Hanson, M.B., Baird, R.W., Boyer, R.H., Burrows, D.G., Emmons, C.K., Ford, J.K.B., Jones, L.L., Noren, D.P., Ross, P.S., Schorr, G.S. & Collier, T.K. (2007) Persistent organic pollutants and stable isotopes in biopsy samples (2004/2006) from southern resident killer whales. Marine Pollution Bulletin, 54, 19031911.
  • Krapu, J.L. (1981) The role of nutrient reserves in mallard reproduction. The Auk, 98, 2938.
  • Kurle, C.M. (2002) Stable-isotope ratios of blood components from captive northern fur seals (Callorhinus ursinus). Canadian Journal of Zoology, 80, 902909.
  • Lesage, V., Hammill, M.O. & Kovacs, K.M. (2002) Diet-tissue fractionation of stable carbon and nitrogen isotopes in phocid seals. Marine Mammal Science, 18, 182193.
  • Lønø, O. (1970) The polar bear (Ursus maritimus Phipps) in the Svalbard area. Norsk Polarinstitutt Skrifter, 149, 1103.
  • Loseto, L.L., Stern, G.A., Connelly, T.L., Deibel, D., Gemmill, B., Prokopowicz, A., Fortier, L. & Ferguson, S.H. (2009) Summer diet of beluga whales inferred by fatty acid analysis of the eastern Beaufort Sea food web. Journal of Experimental Marine Biology and Ecology, 374, 1218.
  • Lydersen, C. & Hammill, M.O. (1993) Activity, milk intake and energy-consumption in free-living ringed seal (Phoca hispida) pups. Journal of Comparative Physiology B, 163, 433438.
  • Lydersen, C., Hammill, M.O. & Ryg, M.S. (1992) Water flux and mass gain during lactation in free-living ringed seal (Phocu hispidu) pups. Journal of Zoology, 228, 361369.
  • MacAvoy, S.E., Macko, S.A. & Arneson, L.S. (2005) Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Canadian Journal of Zoology, 83, 631641.
  • Martinez del Rio, C., Wolf, N., Carleton, S.A. & Gannes, L.Z. (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biology Review, 84, 91111.
  • McHugh, B., Law, R.J., Allchin, C.R., Rogan, E., Murphy, S., Foley, M.B., Glynn, D. & McGovern, E. (2007) Bioaccumulation and enantiomeric profiling of organochlorine pesticides and persistent organic pollutants in the killer whale (Orcinus orca) from British and Irish waters. Marine Pollution Bulletin, 54, 17241731.
  • Minami, M. & Nakamura, T. (2005) Carbon and nitrogen isotopic fractionation in bone collagen during chemical treatment. Chemical Geology, 222, 6574.
  • Moore, J.W. & Semmens, B.X. (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters, 11, 470480.
  • Newsome, S., Martinez del Rio, C., Phillips, D.L. & Bearhop, S. (2007) A niche for isotopic ecology. Frontiers in Ecology and the Envronment, 5, 42904436.
  • O’Corry-Crowe, G.M. (2002) Beluga whale, Delphinapterus leucas. Encyclopedia of Marine Mammals (eds W.F.Perrin, B.Wursig & G.J.M.Thewissen), pp. 9499. Academic Press, San Diego, California.
  • Parker, K.L., Barboza, P.S. & Gillingham, M.P. (2009) Nutrition integrates environmental responses of Ungulates. Functional Ecology, 23, 5769.
  • Phillips, D.L. & Gregg, J.W. (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia, 136, 261269.
  • Phillips, D.L. & Koch, P.L. (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia, 130, 114125.
  • Phillips, D.L., Newsome, S.D. & Gregg, J.W. (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia, 144, 520527.
  • Podlesak, D.W. & McWilliams, S. (2006) Metabolic routing of dietary nutrients in birds: effects of diet quality and macronutrient composition revealed using stable isotopes. Physiological and Biochemical Zoology, 79, 534549.
  • Podlesak, D.W. & McWilliams, S.R. (2007) Metabolic routing of dietary nutrients in birds: effects of dietary lipid concentration on delta δ13C of depot fat and its ecological implications. Auk, 124, 916925.
  • Polischuk, S.C., Norstrom, R.J. & Ramsay, M.A. (2002) Body burdens and tissue concentrations of organochlorines in polar bears (Ursus maritimus) vary during seasonal fast. Environmental Pollution, 118, 2939.
  • Pond, C.M. (1981) Storage. Physiological Ecology: An Evolutionary Approach to Resource Use (eds C.R.Townsend & P.Calow), pp. 190219. Blackwell Scientific Publications, London, UK.
  • Prestrud, P. & Nilssen, K. (1992) Fat deposition and seasonal variation in body composition of arctic foxes in Svalbard. Journal of Wildlife Management, 56, 221233.
  • Ramsay, M.A. & Stirling, I. (1988) Reproductive-biology and ecology of female polar bears (Ursus maritimus). Journal of Zoology, 214, 601634.
  • Redpath, S.M., Clarke, R., Madders, M. & Thirgood, S.J. (2001) Assessing raptor diet: comparing pellets, prey remains, and observational data at hen harrier nests. Condor, 103, 184188.
  • Reynolds, J.C. & Aebischer, N.J. (1991) Comparison and quantification of carnivore diet by faecal analysis: a critique, with recommendations, based on a study of the fox (Vulpes vulpes). Mammal Review, 21, 97122.
  • Robbins, C.T., Fortin, J.K., Rode, K.D., Farley, S.D., Shipley, L.A. & Felicetti, L.A. (2007) Optimizing protein intake as a foraging strategy to maximize mass gain in an omnivore. Oikos, 116, 16751682.
  • Rugh, D.J. & Shelden, K.E.W. (2002) Bowhead whale, Balaena mysticetus. Encyclopedia of Marine Mammals (eds W.F.Perrin, B.Wursig & G.J.M.Thewissen), pp. 129131. Academic Press, San Diego, California.
  • Schmidt, S.N., Olden, J.D., Solomon, C.T. & Vander Zanden, M.J. (2007) Quantitative approaches to the analysis of stable isotope food web data. Ecology, 88, 27932802.
  • Schwarcz, H.P. (1991) Some theoretical aspects of isotope paleodiet studies. Journal of Archaeological Science, 18, 261275.
  • Smith, T.G. (1981) Notes on the bearded seal, Erignathus barbatus, in the Canadian Arctic. Canadian Technical Reports of Fisheries and Aquatic Sciences, 1042, 49.
  • Spaulding, R., Krausman, P.R. & Ballard, W.R. (2000) Observer bias and analysis of gray wolf diets from scats. Wildlife Society Bulletin, 28, 947950.
  • Stirling, I. (1974) Midsummer observations on behavior of wild polar bears (Ursus maritimus). Canadian Journal of Zoology, 52, 11911198.
  • Stirling, I. (2002) Polar bears and seals in the eastern Beaufort Sea and Amundsen Gulf: a synthesis of population trends and ecological relationships over three decades. Arctic, 55, 5976.
  • Stirling, I. & Archibald, W.R. (1977) Aspects of predation of seals by polar bears. Journal of the Fisheries Research Board of Canada, 34, 11261129.
  • Stirling, I. & Derocher, A.E. (1990) Factors affecting the evolution and behavioral ecology of the modern bears. International Conference of Bear Research and Management, 8, 189204.
  • Stirling, I. & McEwan, E.H. (1975) Caloric value of whole ringed seals (Phoca hispida) in relation to polar bear (Ursus maritimus) ecology and hunting behavior. Canadian Journal of Zoology, 53, 10211027.
  • Stirling, I. & Øritsland, N.A. (1995) Relationships between estimates of ringed seal (Phoca hispida) and polar bear (Ursus maritimus) populations in the Canadian Arctic. Canadian Journal of Fisheries and Aquatic Sciences, 52, 25942612.
  • Stirling, I., Spencer, C. & Andriashek, D. (1989) Immobilization of polar bears (Ursus maritimus) with Telazol in the Canadian Arctic. Journal of Wildlife Diseases, 25, 159168.
  • Stirling, I., Richardson, E., Thiemann, G.W. & Derocher, A.E. (2008) Unusual predation attempts of polar bears on ringed seals in the southern Beaufort Sea: possible significance of changing spring ice conditions. Arctic, 60, 1422.
  • Thiemann, G.W., Iverson, S.J. & Stirling, I. (2008) Polar bear diets and arctic marine food webs: insights from fatty acid analysis. Ecological Monographs, 78, 591613.
  • Thiemann, G.W., Budge, S.M., Iverson, S.J. & Stirling, I. (2007) Unusual fatty acid biomarkers reveal age- and sex-specific foraging in polar bears (Ursus maritimus). Canadian Journal of Zoology, 85, 505517.
  • Tieszen, L.L. & Boutton, T.W. (1989) Stable carbon isotopes in terrestrial ecosystem research. Stable Isotopes in Ecological Research (eds P.W.Rundel, J.R.Ehloringer & K.A.Nagy), pp. 167195. Springer-Verlag, New York.
  • Tieszen, L.L. & Farge, T. (1993) Effect of diet quality and composition on the isotopic composition of respiratory CO2, bone collagen, bioapatite, and soft tissues. Prehistoric Human Bone-Archaeology at the Molecular Level (eds J.B.Lambert & G.Grupe), pp. 123135. Springer-Verlag, Berlin, Germany.
  • Tieszen, L.L., Boutton, T.W., Tesdahl, K.G. & Slade, N.A. (1983) Fractionation and turnover of stable carbon isotopes in animale tissues: implications for δ13C analysis of diet. Oecologia, 57, 3237.
  • Voigt, C.C., Rex, K., Michener, R.H. & Speakman, J.R. (2008) Nutrient routing in omnivorous animals tracked by stable carbon isotopes in tissue and exhaled breath. Oecologia, 157, 3140.
  • Watanabe, Y., Lydersen, C., Sato, K., Naito, Y., Miyazaki, N. & Kovacs, K.M. (2009) Diving behavior and swimming style of nursing bearded seal pups. Marine Ecology Progress Series, 380, 287294.
  • West, J.B., Bowen, G.J., Cerling, T.E. & Ehleringer, J.R. (2006) Stable isotopes as one of nature’s recorders. Trends in Ecology and Evolution, 21, 408414.
  • Wortinger, A. (2007) Nutrition for Veterinary Technicians and Nurses. pp. 72. Wiley-Blackwell, Ames, Iowa.
  • Young, R. (1976) Fat, energy and mammalian survival. American Zoologist, 16, 699710.

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

Fig. S1. Map of study area showing polar bear capture locations in the Beaufort Sea (2005).

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