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. 2021 Jun 8;9(1):coab036. doi: 10.1093/conphys/coab036

Regional, seasonal and age class blubber fatty acid signature analysis of harbour seals in Alaska from 1997 to 2010

Victoria M Neises 1,✉, Shawna A Karpovich 2, Mandy J Keogh 2, Ryan S King 1, Stephen J Trumble 1
Editor: Frank Seebacher
PMCID: PMC8628356  PMID: 35685345

Lay Summary

This is the first study to document large-scale regional, seasonal and age class blubber fatty acid (FA) differences in Alaskan harbour seal populations. With this information as a baseline, harbour seal FAs can be used to assess species and ecosystem level changes to climate change.

Abstract

Alaskan harbour seal populations are currently listed as a species of special concern. Although there is evidence of recent stabilization or even partial recovery of harbour seal numbers in areas of historic decline, most populations have not made substantial recoveries. To date, few data exist regarding spatial and seasonal changes in blubber fatty acids (FAs) for Alaskan harbour seal populations. The purpose of this study was to qualitatively investigate harbour seal blubber FA profiles for regional, seasonal and age class differences. Blubber FA concentrations were analysed using MANOVA and linear discriminant analysis (LDA) from 760 individual harbour seals across Bristol Bay, Kodiak, Prince William Sound and Southeast Alaska from 1997 to 2010. Our results suggest spatial and seasonal differences are largely driven by monounsaturated FAs, most notably 14:1n-5, 16:1n-7 and 18:1n-7. In addition, our data revealed a progression in blubber FAs from pups to adults, with a shift from saturated FAs and short-chained monounsaturated FAs in the pup blubber to more long-chain monounsaturated FAs and polyunsaturated FAs in adults. Lastly, harbour seals pups had elevated saturated FA 16:0 concentrations when compared to other age classes, regardless of location or period. With this vast spatial and seasonal FA information, we believe future sampling of blubber FAs from Alaskan harbour seal populations could be a useful tool in assessing the response of this species and its ecosystem to changes associated with natural and anthropogenic pressures.

Introduction

Harbour seals (Phoca vitulina) are one of the most globally abundant pinniped species (Jeffries et al., 2003), inhabiting temperate and subarctic waters of the North Pacific, North Atlantic and contiguous seas (Hoover-Miller, 1994; Blundell et al., 2011). They are opportunistic, generalist predators existing at or near the apex of marine food webs (Bromaghin et al., 2013). While generally non-migratory, local harbour seal movements are associated with extrinsic factors, including tides, season and food availability, as well as intrinsic factors, such as reproduction and breeding (Scheffer and Slipp, 1944; Fisher, 1952; Bigg, 1969; Hastings et al., 2004). Given their abundance, trophic position and relatively non-migratory attributes, harbour seals contribute and function as indicators of marine ecosystem health (Ross, 2000; Boyd and Murray, 2001; Mos et al., 2006; Sergio et al., 2006; Heithaus et al., 2008; Schmitz et al., 2010).

Alaskan harbour seal populations extend from Southeast Alaska, west through the Gulf of Alaska and Aleutian Islands, to the Bering Sea north to Cape Newenham and the Pribilof Islands (NOAA, 2019). Local or regional trends in harbour seal population numbers, monitored intermittently since the 1970s, reveal diverse spatial patterns in Alaskan populations, with some regions experiencing extreme population declines (>60%; NOAA, 2019). For example, on Tugidak Island, near Kodiak Island, Alaska, population counts of harbour seals declined ~80% during the 1970s and 1980s (Pitcher, 1990; Jemison et al., 2006). Additionally, in Prince William Sound, harbour seal populations declined by ~63% between 1984 and 1997 (Frost et al., 1999; Ver Hoef and Frost, 2003), and in Southeast, harbour seal counts in Glacier Bay National Park declined by 93% from 1979 to 2009 (Hoover-Miller et al., 2011). These drastic declines (Loughlin et al., 1992; Trites and Larkin, 1996) led to increased cause/effect research efforts including evaluating dietary shifts through analysis of faecal and stomach contents and blubber fatty acids (FAs) (Merrick et al., 1987; Alverson, 1992; Springer, 1992), as well as the effect of disease, contaminants and predation (Barron et al., 2003; Mathews and Pendleton, 2006; Hueffer et al., 2011).

Profiling FAs from adipose tissue is a conventional technique used to determine foraging patterns and dietary differences in marine mammals (Iverson et al., 1997; Iverson et al., 2002; Beck et al., 2007a, b). Dietary patterns can be established because pinnipeds deposit dietary FAs into adipose tissue with little modification or in a predictable way (Cooper, 2004; Iverson et al., 2004). While the greatest contributor to blubber FA composition in monogastric predators, such as pinnipeds, is diet (Budge et al., 2006), predator profiles are also influenced by the biosynthesis of certain FAs and the reduced deposition of others, resulting in FA profiles that will never exactly match that of their prey (Budge et al., 2006; Iverson, 2009). Despite this, the FA profile of a predator’s adipose tissue has been shown to reflect the FA profile of consumed prey in marine mammals (Iverson, 1993; Iverson et al., 2001; Budge et al., 2004; Budge et al., 2006; Cooper et al., 2006; Iverson, 2009) and, due to this deposition, has been shown to provide an integrated record of dietary intake over a period of weeks to months (Iverson et al., 2004; Budge et al., 2006; Iverson, 2009).

The FA profile of a predator can be used to investigate diet in two ways: quantitative fatty acid signature analysis (QFASA) allows the predators diet to be estimated using the FA profile of the predator and that of its prey (Iverson et al., 2004). However, adequate data on the FA composition of all potential prey species and an understanding of how a predator metabolizes individual FAs (calibration coefficients; Iverson et al., 2004) are required. In the absence of prey FA and calibration data, FA profiles of predators can detect qualitative dietary changes and differences among demographic groups (Iverson et al., 1997; Walton et al., 2000; Beck et al., 2005; Beck et al., 2007b), based on the established understanding that FA structures are transferred across trophic levels largely unchanged (Ackman and Eaton, 1966; Cook, 1991). Despite its limitations (Grahl-Nielsen et al., 2003, 2004; Thiemann et al., 2004), the qualitative use of FAs have been useful in disclosing spatial, seasonal, age class and sex differences in cetaceans and pinnipeds (Iverson et al., 1995; Walton et al., 2000; Olsen and Grahl-Nielsen, 2003; Beck et al., 2005, 2007a, b; Meynier et al., 2008; Strandberg et al., 2008) providing a foundation for studies of foraging ecology, reproduction and toxicology based on the analysis of marine mammal blubber. Moreover, FA studies involving harbour seal populations have revealed spatial, seasonal and age class differences in harbour seal populations in Canada (Smith et al., 1997), Norway (Andersen et al., 2004) and WA, USA (Bromaghin et al., 2013).

Alaskan harbour seal populations are currently listed as a species of special concern (Alaska Department of Fish and Game, 1998). Although there is evidence of recent stabilization or even partial recovery of harbour seal numbers in areas of historic decline, most populations have not made substantial recoveries (NOAA, 2019). While harbour seal populations are believed to have been impacted by past prey regime shifts (Anderson and Piatt, 1999), there is a lack of knowledge surrounding how future dietary shifts may be expressed in the physiology of the harbour seal. Having a baseline account of harbour seal blubber FAs would allow subsequent changes to not only be monitored for the purpose of examining harbour seal diet changes over time, but to also provide a means to indirectly examine changes on an ecosystem level.

In this study, we qualitatively investigated the blubber FA profiles of 760 Alaskan harbour seals encompassing a 14-yr time period and tested for regional, seasonal and age class differences. We hypothesized that the FA profiles of these Alaskan harbour seals would differ by region given previous work conducted by Iverson et al. (1997) that characterized regional differences in blubber FA profiles. While season and age class differences in blubber FA profiles for Alaskan harbour seals has not been extensively studied, we predicted that the FA profile of these seals would differ by season and age class given the known temporal variation in prey assemblages throughout their Alaskan range (Pitcher and Calkins, 1979; Pitcher 1980a, b; Harvey, 1989; Iverson et al., 1997; Smith et al., 2019), and historically documented differences in prey consumption between age classes (Hoover-Miller, 1994).

Materials and methods

Sample collection

Seven hundred and sixty (N = 760) harbour seals were captured, sampled and released between June 1997 and July 2010 (Table 1; MMPA NMFS Permit #s 1000, 358-1585, 358-1787 and ADFG ACUC 07-16) from four regions and classified as: Bristol Bay (BB), Kodiak (KOD), Prince William Sound (PWS) or Southeast Alaska (SEA) (Fig. 1). Samples were collected under ACUC 07-16 issued by the Alaska Department of Fish and Game.

Table 1. Number of harbour seal blubber samples collected between June 1997 and July 2010 (n = 760) by region, season and age class for each year sampled.

Year BB (n = 86) KOD (n = 72) PWS (n = 254) SEA (n = 348)
Fall (n = 86) Spring (n = 9) * Summer (n = 63) * Winter (n = 28) Spring (n = 33) Summer (n = 193) Fall (n = 170) Spring (n = 141) Summer (n = 37)
1997 10P
1998 8P
1999 23P
2000 BA/4sA/12Y/12P
2001 32A/4sA/5Y/9P 22P 1A/6sA/25Y/25P 4sA/3Y/1P
2003 6A/3SA 9A/6sA/12Y/6P 13A4/13sA/187/5P
2004 7A/7sA/7Y7P 3A/3sA/1Y/6P 6A/2sA/8Y/30P 16A4/3sA/8Y/3P
2005 11A/20sA/21Y/22P 8A/2sA/2Y/37P 114/4sA/10Y/6P
2006 16A/75A/12Y/40P 3A/6sA/4Y/13P
2008 1sA/9Y/10P
2009 7A
2010 2A/10sA/4Y/10P 3A/BsA/16Y/3P
Age class total 40A/8sA*/17Y*/21P 6A*/3sA* 63P* 7A*/7sA*/7Y*/7P* 9A*/6sA*/12Y*/6P* 28A/42sA/65Y/58P 30A/11sA*/22¥/107P 32A/28sA/38Y/43P 10A*/8sA*/16Y*/3P*
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A, adults; sA, subadults; Y, yearlings; P, pups.

BB, Bristol Bay; KOD, Kodiak; PWS, Prince William Sound; SEA, Southeast Alaska.

*Samples that were omitted from regional, seasonal and/or age class analysis.

Figure 1.

Figure 1

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Alaskan harbor seal (Phoca vitulina) sampling locations for Bristol Bay (BB, triangles, n = 86). Kodiak (KOD, squares, n = 158), Prince William Sound (PWS, circles, n = 254), Southeast Alaska (SEA, diamonds, n = 348).

Harbour seals were captured using multifilament seine nets (Jeffries et al., 1993) and monofilament gillnets (Blundell et al., 2011) for terrestrial and glacial fjords captures, respectively. Animals were manually restrained and subsequently sedated with 0.25 mg/kg of diazepam administered intravenously using a 2.5- or 3.5-inch 18 g spinal needle (Blundell et al., 2014). Harbour seals were weighed to the nearest 0.1 kg using a digital hanging scale. Sex was determined visually and basic morphometrics (curvilinear length and axillary girth; Blundell and Pendleton, 2008) were measured to the nearest 1 cm. A small incision was made in the skin and full-depth blubber cores (surface to muscle interface with no epidermal tissue) were collected from the right hip using a 6-mm biopsy punch after prepping the area with betadine and 70% ETOH. All blubber core samples were immediately placed into 100% chloroform and stored at −20°C while in the field (<14 d), then transferred into a −80°C ultracold freezer until processing.

Harbour seal age was estimated using a model that incorporates sex, curvilinear length and mass (Blundell and Pendleton, 2008). To validate this model, 109 harbour seals from this study were also aged using annual tooth cementum growth rings (Matson’s laboratory, Milltown, MT; Blundell and Pendleton, 2008). Harbour seals were grouped into four age classes: pups (<0.75 yrs), yearlings (0.75 yrs > 1.75 yrs), subadults (F, 1.75 yrs < 3.75 yrs; M, 1.75 yrs < 5.75 yrs) and adults (F, >3.75 yrs; M, >5.75 yrs) (Blundell and Pendleton, 2008). Females were considered adults at 4 yrs, whereas males were considered adults at 6 yrs based on age of sexual maturity (Lydersen and Kovacs, 2005). June and July pup and yearling body morph estimates were secondarily verified using recorded physical observation, as pup and yearling body morph measurements are similar during those months (Samaranch and González, 2000) and new pup pelage is easily distinguished from yearling pelage that has weathered for 1 yr (Daniel et al., 2003).

Laboratory procedures

Harbour seal FA quantification analysis protocols followed Beck et al. (2007b). Briefly, lipids were extracted from full-depth blubber cores applying a modified Folch method using chloroform and methanol (Folch et al., 1957; Iverson et al., 2001). Extracted lipids were derivatized to FA methyl esters (FAME) as described in Iverson et al. (1997). FAME from samples collected prior to 2000 were analysed at Dalhousie University in Halifax, Nova Scotia, as described in Budge et al. (2002). After 2000, FAME were analysed at the Applied Science, Engineering and Technology laboratory at the University of Alaska Anchorage, as described in Dodds et al. (2004). Compatibility of sample analysis was performed by comparing Steller sea lion (Eumetopias jubatus) blubber FA samples analysed between laboratories, as described in Beck et al. (2007b). In both laboratories, specific FAs were identified using known standard mixtures (Sigma, Supelco, Matreta and/or Nu-check Prep), silver nitrate chromatography and gas chromatography/mass spectrometry (Beck et al., 2007b). Individual FAs are reported as percent weight of the total FAs analysed and are designated using shorthand nomenclature of carbon chain length: number of bonds and location (n-x) of the double bond nearest the terminal methyl group. For example, an FA with a carbon chain length of 16, one double bond and the location of this double bond is 7 carbons back from the terminal methyl group would be designated as 16:1n-7 (Budge et al., 2006).

Statistical analysis

Harbour seal blubber samples were classified by season, as summer (1 June to 31 August), autumn (1 September to 30 November), winter (1 December to 28 February) or spring (1 March to 31 May). Based on previous DNA analysis, there are currently 12 recognized harbour seal stocks in Alaska (NOAA, 2019). Neighbouring stocks were combined, with KOD encompassing North and South Kodiak stocks and SEA encompassing the Glacier Bay/Icy Straight and Lynn Canal/Stephens Passage stocks. Both BB and PWS included only the BB and PWS stocks, respectively.

General linear models (MANOVA) and LDA were used to examine regional, seasonal and age class differences in the FA profiles of harbour seals. Initial MANOVAs were performed to determine blubber FA differences between regions, seasons and age classes. Statistical significance was accepted at probabilities of 0.05 or less. Supervised LDA was applied to identify linear combinations that best classified FAs into regions, seasons and age classes. LDA is a statistical method used to distinguish in groups a collection of objects, having a set of cases whose group membership is known a priori (Busetto et al., 2008). Blubber FA signatures were normalized (Budge et al., 2006; Williams et al., 2009) and transformed using a centered logratio (CLR) transformation (Filzmoser et al., 2009) to fulfil the assumptions of normality, skew and homogeneity of variance for MANOVA and LDA. A subset of 14 FAs was selected from a total set of 62 FAs (Table 2), based on those considered to be the most abundant (>1% total of the sum of all samples; Noren et al., 2013), and accounted for 90.13 ± 1.91% of total FAs by lipid weight. Due to uneven sampling within regions and because harbour seal diet varies seasonally (Pitcher and Calkins, 1979; Pitcher 1980a,b; Harvey, 1989; Iverson et al., 1997; Smith et al., 2019), the analysis was pooled among years and hierarchically structured, with regions, seasons within regions and age classes within seasons (Table 1). To assure the covariance matrices are homogeneous, the total number of samples must exceed the number of FA variables (Pituch and Stevens, 2016). While this would allow us to include sample sizes 15 or greater, only sample sizes greater than 20 (n = 20) were used in the analysis to increase the reliability of the results (Budge et al., 2006; Pituch and Stevens, 2016). A confusion matrix was generated to determine overall error rates and specific error level association. All LDA models were evaluated for model error using a Wilks’ lambda MANOVA. All statistical analysis was conducted in R v.3.4.2 (R Core Team, 2017). LDA was conducted using LDA function in the MASS package v.7.3-52 (Ripley et al., 2020).

Table 2.

FA composition of blubber tissue from harbour seals in BB, KOD, PWS and SEA

BB KOD PWS SEA
FA Adult(n = 40) Subadult(n = 8) Yearling(n = 17) Pup(n = 21) Adult(n = 6) Subadult(n = 3) Pup(n = 63) Adult(n = 44) Subadult(n = 55) Yearling(n = 84) Pup(n = 71) Adult(n = 72) Subadult(n = 47) Yearling(n = 76) Pup(n = 153)
 Saturated
14:00 2.69 ± 0.06 2.54 ± 0.13 3.17 ± 0.12 3.35 ± 0.11 3.15 ± 0.18 3.55 ± 0.49 3.64 ± 0.06 4.59 ± 0.17 5.29 ± 0.15 5.32 ± 0.08 5.11 ± 0.09 4.86 ± 0.19 4.93 ± 0.17 5.49 ± 0.11 5.73 ± 0.08
15:00 0.33 ± 0.01 0.31 ± 0.01 0.28 ± 0.01 0.25 ± 0.00 0.23 ± 0.01 0.21 ± 0.01 0.24 ± 0.00 0.22 ± 0.01 0.21 ± 0.00 0.21 ± 0.00 0.23 ± 0.00 0.21 ± 0.01 0.19 ± 0.01 0.19 ± 0.00 0.21 ± 0.00
16:00 7.98 ± 0.18 7.90 ± 0.38 9.01 ± 0.17 10.30 ± 0.22 9.37 ± 0.54 9.08 ± 0.69 10.89 ± 0.11 8.39 ± 0.18 8.78 ± 0.24 9.66 ± 0.11 10.58 ± 0.13 9.33 ± 0.19 9.44 ± 0.23 10.13 ± 0.11 10.57 ± 0.08
7methyl 16:0 0.21 ± 0.01 0.20 ± 0.01 0.23 ± 0.01 0.22 ± 0.01 0.27 ± 0.03 0.23 ± 0.03 0.25 ± 0.01 0.13 ± 0.02 0.11 ± 0.01 0.12 ± 0.01 0.13 ± 0.01 0.16 ± 0.01 0.16 ± 0.01 0.14 ± 0.01 0.15 ± 0.01
17:00 0.23 ± 0.01 0.21 ± 0.02 0.18 ± 0.01 0.16 ± 0.01 0.16 ± 0.01 0.10 ± 0.01 0.17 ± 0.00 0.35 ± 0.08 0.22 ± 0.02 0.18 ± 0.02 0.12 ± 0.01 0.24 ± 0.03 0.25 ± 0.03 0.21 ± 0.02 0.11 ± 0.01
18:00 1.20 ± 0.03 1.22 ± 0.06 1.16 ± 0.05 1.20 ± 0.04 1.26 ± 0.09 1.19 ± 0.10 0.95 ± 0.03 1.16 ± 0.03 1.12 ± 0.03 1.20 ± 0.02 1.04 ± 0.03 1.14 ± 0.03 1.15 ± 0.05 1.15 ± 0.04 1.03 ± 0.02
 Monounsaturated
14:1n-5 0.92 ± 0.03 1.13 ± 0.14 1.48 ± 0.11 1.78 ± 0.12 0.81 ± 0.06 1.13 ± 0.07 2.68 ± 0.11 0.96 ± 0.04 1.14 ± 0.05 1.38 ± 0.05 1.79 ± 0.06 1.01 ± 0.04 1.38 ± 0.09 1.63 ± 0.05 1.72 ± 0.04
16:1n-11 0.43 ± 0.02 0.34 ± 0.02 0.36 ± 0.02 0.29 ± 0.01 0.23 ± 0.02 0.19 ± 0.05 0.31 ± 0.02 0.39 ± 0.03 0.39 ± 0.03 0.39 ± 0.02 0.47 ± 0.03 0.28 ± 0.01 0.23 ± 0.02 0.21 ± 0.01 0.20 ± 0.01
16:1n-9 0.52 ± 0.01 0.50 ± 0.03 0.50 ± 0.02 0.60 ± 0.02 0.39 ± 0.03 0.41 ± 0.02 0.68 ± 0.01 0.40 ± 0.01 0.38 ± 0.01 0.40 ± 0.01 0.49 ± 0.02 0.38 ± 0.01 0.42 ± 0.01 0.43 ± 0.01 0.47 ± 0.01
16:1n-7 15.55 ± 0.44 18.07 ± 1.20 20.59 ± 0.97 22.32 ± 0.84 13.79 ± 0.50 16.29 ± 1.02 29.83 ± 0.61 12.33 ± 0.33 13.51 ± 0.33 15.94 ± 0.38 20.39 ± 0.53 13.17 ± 0.30 15.68 ± 0.59 17.60 ± 0.40 18.81 ± 0.28
17:1 0.71 ± 0.02 0.70 ± 0.06 0.52 ± 0.04 0.48 ± 0.02 0.40 ± 0.03 0.35 ± 0.03 0.53 ± 0.01 0.21 ± 0.04 0.15 ± 0.02 0.22 ± 0.02 0.29 ± 0.02 0.26 ± 0.03 0.36 ± 0.02 0.30 ± 0.02 0.28 ± 0.01
18:1n-13 0.38 ± 0.01 0.32 ± 0.02 0.27 ± 0.01 0.20 ± 0.01 0.23 ± 0.02 0.17 ± 0.05 0.28 ± 0.01 0.31 ± 0.02 0.29 ± 0.02 0.24 ± 0.01 0.27 ± 0.01 0.19 ± 0.02 0.08 ± 0.01 0.07 ± 0.01 0.10 ± 0.01
18:1n-11 1.09 ± 0.10 0.63 ± 0.09 1.26 ± 0.27 0.86 ± 0.11 1.75 ± 0.20 1.53 ± 0.42 0.57 ± 0.06 3.61 ± 0.14 3.59 ± 0.19 2.79 ± 0.12 2.77 ± 0.14 1.99 ± 0.10 1.48 ± 0.11 1.32 ± 0.06 1.54 ± 0.05
18:1n-9 24.38 ± 0.48 24.47 ± 0.86 21.56 ± 0.60 23.36 ± 0.51 17.97 ± 0.62 22.96 ± 2.04 17.98 ± 0.30 26.89 ± 1.09 22.72 ± 0.80 26.22 ± 0.61 22.92 ± 0.72 27.47 ± 0.48 30.53 ± 0.72 29.01 ± 0.52 27.05 ± 0.35
18:1n-7 5.52 ± 0.20 6.21 ± 0.21 5.52 ± 0.19 5.34 ± 0.12 4.72 ± 0.34 5.77 ± 0.43 5.26 ± 0.10 4.72 ± 0.14 4.78 ± 0.15 4.76 ± 0.08 4.54 ± 0.11 4.25 ± 0.12 4.44 ± 0.12 4.43 ± 0.10 4.11 ± 0.05
18:1n-5 0.40 ± 0.02 0.35 ± 0.01 0.41 ± 0.03 0.41 ± 0.01 0.00 ± 0.00 0.01 ± 0.01 0.37 ± 0.01 0.25 ± 0.04 0.27 ± 0.03 0.25 ± 0.02 0.20 ± 0.03 0.24 ± 0.03 0.09 ± 0.03 0.09 ± 0.02 0.03 ± 0.01
18:1n-3 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 0.00 ± 0.00 0.36 ± 0.02 0.32 ± 0.02 0.00 ± 0.00 0.21 ± 0.03 0.18 ± 0.03 0.18 ± 0.02 0.24 ± 0.03 0.24 ± 0.03 0.31 ± 0.03 0.30 ± 0.02 0.41 ± 0.01
20:1n-11 3.26 ± 0.26 1.79 ± 0.29 2.17 ± 0.33 1.69 ± 0.22 2.66 ± 0.42 1.85 ± 0.61 0.86 ± 0.08 6.50 ± 0.39 6.66 ± 0.33 5.80 ± 0.19 4.32 ± 0.20 2.94 ± 0.17 2.06 ± 0.19 1.75 ± 0.10 1.93 ± 0.06
20:1n-9 2.18 ± 0.12 2.18 ± 0.42 3.07 ± 0.68 2.26 ± 0.35 1.38 ± 0.16 1.24 ± 0.13 0.66 ± 0.03 2.39 ± 0.11 2.35 ± 0.08 2.08 ± 0.06 1.63 ± 0.07 2.55 ± 0.09 2.16 ± 0.09 1.81 ± 0.06 1.79 ± 0.04
20:1n-7 0.70 ± 0.05 0.68 ± 0.04 0.52 ± 0.05 0.32 ± 0.02 0.32 ± 0.02 0.29 ± 0.04 0.29 ± 0.02 0.36 ± 0.03 0.26 ± 0.01 0.23 ± 0.01 0.21 ± 0.02 0.37 ± 0.04 0.24 ± 0.01 0.21 ± 0.01 0.20 ± 0.00
22:1n-11 0.84 ± 0.10 0.52 ± 0.16 0.80 ± 0.27 0.49 ± 0.12 0.42 ± 0.15 0.34 ± 0.25 0.06 ± 0.01 2.24 ± 0.22 2.37 ± 0.15 2.13 ± 0.11 1.08 ± 0.10 1.09 ± 0.09 0.74 ± 0.09 0.71 ± 0.07 0.81 ± 0.04
22:1n-9 0.20 ± 0.02 0.10 ± 0.02 0.14 ± 0.03 0.11 ± 0.02 0.00 ± 0.00 0.03 ± 0.03 0.03 ± 0.00 0.28 ± 0.02 0.24 ± 0.02 0.23 ± 0.01 0.11 ± 0.01 0.35 ± 0.03 0.39 ± 0.04 0.30 ± 0.02 0.21 ± 0.02
 Polyunsaturated
16:2n-4 0.33 ± 0.01 0.33 ± 0.02 0.25 ± 0.01 0.24 ± 0.01 0.01 ± 0.04 0.46 ± 0.05 0.26 ± 0.01 0.38 ± 0.02 0.43 ± 0.02 0.36 ± 0.02 0.34 ± 0.02 0.40 ± 0.02 0.47 ± 0.02 0.49 ± 0.02 0.48 ± 0.01
16:3n-6 0.24 ± 0.01 0.27 ± 0.01 0.30 ± 0.02 0.22 ± 0.01 0.21 ± 0.02 0.00 ± 0.00 0.19 ± 0.01 0.07 ± 0.02 0.12 ± 0.03 0.18 ± 0.02 0.19 ± 0.02 0.08 ± 0.02 0.06 ± 0.02 0.05 ± 0.02 0.02 ± 0.01
16:4n-1 0.13 ± 0.01 0.16 ± 0.01 0.18 ± 0.02 0.10 ± 0.01 0.16 ± 0.02 0.41 ± 0.04 0.15 ± 0.01 0.27 ± 0.03 0.39 ± 0.03 0.35 ± 0.02 0.36 ± 0.03 0.43 ± 0.02 0.37 ± 0.03 0.42 ± 0.02 0.48 ± 0.02
18:2n-6 1.13 ± 0.03 0.93 ± 0.03 0.90 ± 0.04 0.90 ± 0.03 1.13 ± 0.03 1.21 ± 0.14 0.67 ± 0.02 1.06 ± 0.02 1.00 ± 0.02 0.95 ± 0.01 0.93 ± 0.02 0.89 ± 0.02 0.77 ± 0.03 0.77 ± 0.02 0.79 ± 0.01
18:3n-3 0.40 ± 0.03 0.26 ± 0.01 0.27 ± 0.02 0.28 ± 0.03 0.44 ± 0.03 0.59 ± 0.09 0.20 ± 0.01 0.49 ± 0.02 0.44 ± 0.01 0.40 ± 0.01 0.37 ± 0.01 0.47 ± 0.02 0.36 ± 0.02 0.37 ± 0.02 0.36 ± 0.01
18:4n-3 0.59 ± 0.03 0.47 ± 0.03 0.52 ± 0.05 0.42 ± 0.04 0.70 ± 0.06 1.45 ± 0.06 0.42 ± 0.02 0.97 ± 0.05 1.00 ± 0.04 0.90 ± 0.02 0.90 ± 0.04 0.85 ± 0.04 0.68 ± 0.05 0.74 ± 0.04 0.83 ± 0.03
20:2n-6 0.29 ± 0.01 0.26 ± 0.01 0.26 ± 0.01 0.27 ± 0.01 0.29 ± 0.01 0.22 ± 0.02 0.31 ± 0.01 0.20 ± 0.01 0.16 ± 0.01 0.18 ± 0.00 0.23 ± 0.01 0.19 ± 0.01 0.13 ± 0.01 0.15 ± 0.01 0.20 ± 0.00
20:4n-6 0.94 ± 0.01 1.08 ± 0.07 0.93 ± 0.07 0.78 ± 0.04 0.95 ± 0.04 0.73 ± 0.04 1.25 ± 0.02 0.51 ± 0.03 0.43 ± 0.02 0.45 ± 0.01 0.66 ± 0.04 0.58 ± 0.03 0.49 ± 0.02 0.48 ± 0.01 0.56 ± 0.01
20:4n-3 0.53 ± 0.04 0.34 ± 0.02 0.32 ± 0.02 0.27 ± 0.02 0.56 ± 0.03 0.56 ± 0.04 0.26 ± 0.01 0.53 ± 0.05 0.41 ± 0.02 0.35 ± 0.01 0.38 ± 0.02 0.65 ± 0.02 0.52 ± 0.02 0.49 ± 0.02 0.46 ± 0.01
20:5n-3 5.84 ± 0.21 6.10 ± 0.44 5.96 ± 0.25 4.40 ± 0.29 6.17 ± 0.23 6.94 ± 1.06 4.81 ± 0.12 4.35 ± 0.23 4.27 ± 0.18 4.09 ± 0.14 4.24 ± 0.16 6.01 ± 0.23 5.42 ± 0.20 5.22 ± 0.14 4.95 ± 0.11
21:5n-3 0.35 ± 0.01 0.35 ± 0.01 0.33 ± 0.01 0.28 ± 0.01 0.35 ± 0.01 0.45 ± 0.02 0.35 ± 0.01 0.18 ± 0.03 0.18 ± 0.02 0.23 ± 0.02 0.27 ± 0.02 0.30 ± 0.03 0.35 ± 0.03 0.40 ± 0.03 0.37 ± 0.02
22:4n-6 0.32 ± 0.02 0.36 ± 0.03 0.25 ± 0.03 0.19 ± 0.01 0.31 ± 0.02 0.16 ± 0.03 0.23 ± 0.01 0.14 ± 0.01 0.10 ± 0.01 0.09 ± 0.00 0.11 ± 0.01 0.15 ± 0.01 0.08 ± 0.01 0.08 ± 0.01 0.08 ± 0.01
22:5n-6 0.25 ± 0.01 0.28 ± 0.02 0.20 ± 0.01 0.16 ± 0.01 0.22 ± 0.02 0.00 ± 0.00 0.15 ± 0.00 0.06 ± 0.01 0.03 ± 0.01 0.05 ± 0.01 0.06 ± 0.01 0.03 ± 0.01 0.01 ± 0.01 0.02 ± 0.01 0.02 ± 0.00
22:6n-3 10.16 ± 0.25 9.78 ± 0.42 9.09 ± 0.32 9.18 ± 0.52 10.80 ± 0.34 10.91 ± 1.99 7.82 ± 0.17 7.96 ± 0.47 6.94 ± 0.26 6.64 ± 0.20 6.84 ± 0.21 8.86 ± 0.27 7.59 ± 0.31 7.01 ± 0.22 6.92 ± 0.11
% Total FA
 Saturated 13.39 ± 0.10 13.12 ± 0.22 14.63 ± 0.18 16.04 ± 0.18 15.15 ± 0.31 15.00 ± 0.43 16.77 ± 0.11 15.34 ± 0.11 16.18 ± 0.11 17.15 ± 0.09 17.68 ± 0.11 16.41 ± 0.10 16.60 ± 0.12 17.74 ± 0.10 18.31 ± 0.07
 Monounsaturated 57.56 ± 0.19 58.47 ± 0.45 59.61 ± 0.30 60.92 ± 0.29 45.88 ± 0.38 53.40 ± 0.68 60.80 ± 0.18 62.66 ± 0.19 63.82 ± 0.17 63.80 ± 0.14 62.18 ± 0.15 57.35 ± 0.15 61.16 ± 0.21 60.72 ± 0.16 60.21 ± 0.11
 Polyunsaturated 29.05 ± 0.07 28.40 ± 0.16 25.76 ± 0.10 23.04 ± 0.09 38.97 ± 0.27 31.61 ± 0.29 22.43 ± 0.04 21.99 ± 0.06 19.99 ± 0.04 19.05 ± 0.03 20.14 ± 0.04 26.25 ± 0.05 22.23 ± 0.05 21.54 ± 0.04 21.48 ± 0.03
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Values are mean ± SE percent of total FA by weight for all FAs that averaged ≥0.2% in any age class/region group.

Data captured in boldface indicate 14 FAs containing an average of >1% total FA that were used in analysis.

Results

Harbour seal blubber samples revealed nine FAs [saturated FA (SFA): 14:0, 16:0; monounsaturated FA (MUFA): 16:1n-7, 18:1n-7, 18:1n-9, 20:1n-11; polyunsaturated FA (PUFA): 20:5n-3, 22:5n-3, 22:6n-3] with a concentration above 3%, making up 82.7 ± 2.6% of the total blubber FAs by weight (Fig. 2). Overall, MUFAs accounted 60.8 ± 0.05%, PUFAs accounted for 22.4 ± 0.01% and SFA 16.8 ± 0.03% of total blubber FAs (n = 62).

Figure 2.

Figure 2

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Variation in percent composition by weight (±SE) of 14 selected fatty acids by region.

Regional analysis

MUFAs accounted for 58.9 ± 0.1% of total blubber FAs for BB seals, while PUFAs and SFAs made up 26.9 ± 0.03% and 14.3 ± 0.06%, respectively (n = 86). In KOD, MUFAs accounted for 59.3 ± 0.2%, while PUFAs and SFAs made up 24.2 ± 0.05% and 16.6 ± 0.1%, respectively (n = 72). In PWS, MUFAs accounted for 63.1 ± 0.08% total blubber FAs, while PUFAs and SFAs accounted for 20.1 ± 0.02% and 16.8 ± 0.05%, respectively (n = 254). Lastly, within SEA, MUFAs accounted for 59.9 ± 0.07% total blubber FAs, while PUFAs and SFAs accounted for 22.6 ± 0.02% and 17.6 ± 0.05%, respectively (n = 348).

Harbour seal blubber FA profiles differed significantly by region (MANOVA: F42,2235 = 101.3, P < 0.001). Bonferroni post hoc analysis revealed that FAs differed significantly between regions with PWS and SEA seals differing most significantly from BB and KOD seals (P < 0.001; Fig. 2).

LDA also indicated statistically significant differences in the blubber FA profiles of harbour seals by region (Wilks Inline graphic = 0.03, P < 0.001; Fig. 3) with an overall classification success rate of 94.7%. Blubber FA profiles were correctly classified as PWS, SEA, BB and KOD, 97.2%, 95.4%, 90.7% and 87.5% of the time, respectively. Harbour seals from SEA were separated from BB, KOD and PWS seals by MUFA 18:1n-9, while seals from BB, KOD and PWS were separated by 18:1n-7, 20:1n-11 and 22:6n-3 (first discriminant function; Fig. 3). Along the second discriminant, MUFA 16:1n-7 separated BB from KOD, while 14:1n-5 separated PWS from BB and KOD (Fig. 3).

Figure 3.

Figure 3

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Regional LDA Results: Discriminant analysis of 4 regions (BB n = 86, KOD n = 158, PWS n = 254, SEA n = 348) using the 14 fatty acids that had the greatest average variance with the average scores of the two discriminant functions that classified fatty acids to regions with a 94.7% success rate.

Prince William Sound

Blubber FA profiles of seals from PWS differed significantly between seasons (F28,460 = 6.4, P < 0.001) and age classes (F42,693 = 4.5, P < 0.001) as well as the interaction between season and age class (F84,1404 = 1.3, P = 0.04), suggesting that age class FA profiles differed among seasons.

LDA also indicated differences by season (MANOVA: Wilks Inline graphic= 0.51, P < 0.001; Fig. 4A), age class (MANOVA: Wilks Inline graphic= 0.23, P < 0.001; Fig. 5A) and summer age class (MANOVA: Wilks Inline graphic= 0.19, P < 0.001; Fig. 5C), with overall classification success of 81.5%, 65.8% and 65.8%, respectively. Although there was an overlap in FA profiles among seasons, harbour seals sampled during summer were distinguished from seals sampled during spring and winter via 16:1n-7 (first discriminant; Fig. 4A), while seals sampled during spring were separated by 22:6n-3 and 18:1n-7 and seals sampled during winter by 22:5n-3 (second discriminant; Fig. 4A). Within age classes and summer specific age classes, FAs overlapped among age classes from pups to adults with SFA 16:0 separating age classes along both discriminant functions (Fig. 5A and C). Most seasonal misclassifications occurred among spring and winter with both being misclassified as summer 57.6% and 46.4% of the time, respectively, while most age class misclassifications occurred with subadults misclassified as adults and yearlings 21.8% and 31.0% of the time, respectively. Adults were also misclassified as subadults 31.8% of the time. Within the summer season, the greatest age class misclassifications occurred between adults and subadults misclassified as each other 46.5 and 31.0%, respectively. Pups had a classification success rate of 86.2%.

Figure 4.

Figure 4

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Seasonal LDA Results for Prince William Sound and Southeast Alaska: (A) Prince William Sound Seasonal LDA (spring n = 33, summer n = 193, winter n = 28) using the 14 fatty acids that had the greatest average variance with the average scores of two discriminant functions that classified fatty acids to seasons with a 81.50% success rate; (B) Southeast Alaska Seasonal LDA (fall n = 170, spring n = 141, summer n = 37) with the average scores of two discriminant functions that classified fatty acids to season with a 73.28% success rate.

Figure 5.

Figure 5

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Age Class LDA Results for Prince William Sound and Southeast Alaska: (A) Prince William Sound Age Class LDA (adult n = 44, subadult n = 55, yearling n = 84, pup n = 71) using the 14 fatty acids that had the greatest average variance with the average scores of the first two of three discriminant functions that classified fatty acids to seasons with a 65.80% success rate; (B) Southeast Age Class LDA (adult n = 72, subadult n = 47, yearling n = 76, pup n = 153) with the average scores of the first two of three discriminant functions that classified fatty acids to seasons with a 60.90% success rate; (C) Prince William Sound Summer Age Class LDA (adult n = 28, subadult n = 42, yearling n = 65, pup n = 58) with the average scores of the first two of three discriminant functions that classified fatty acids to age class with a 65.80% success rate; (D) Southeast Alaska Spring Age Class LDA (adult n = 32, subadult n = 28, yearling n = 38, pup n = 43) with the average scores of the first two of three discriminant functions that classified fatty acids to age class with a 45.39% success rate; (E) Southeast Alaska Autumn Age Class LDA (adult n = 30, yearling n = 22, pup n = 107) with the average scores of two discriminant functions that classified fatty acids to age class with a 80.50% success rate.

Southeast Alaska

Similar to seals from PWS, blubber FA profiles of seals from SEA differed significantly between seasons (F28,648 = 9.4, P < 0.001) and age classes (F42,975 = 5.8, P < 0.001) as well as the interaction between season and age class (F84,1968 = 1.9, P < 0.001), suggesting that within PWS age class FA profiles varied by season.

Statistically significant differences between seasons (MANOVA: Wilks Inline graphic= 0.40, P < 0.001; Fig. 4B) and age classes (MANOVA: Wilks Inline graphic= 0.33, P < 0.001; Fig. 5B) were confirmed with LDA, with an overall classification success of 73.3% and 60.9%, respectively. Autumn seals were primarily defined by MUFA 16:1n-7 (first discriminant; Fig. 4B), spring seals were defined by MUFAs 14:1n-5 (first discriminant) and 18:1n-7 (second discriminant) and summer seals were defined via 14:1n-5 (first discriminant) and 16:0 (second discriminant). Within age classes, adults and subadults were separated via MUFA 18:1n-9 and PUFA 20:5n-3 (first discriminant; Fig. 5B), while pups were distinguished by MUFA 16:1n-7 and SFA 16:0 (second discriminant). The greatest seasonal misclassifications occurring among summer seals, with 43.2% of summer seals misclassified as spring seals. Similar to PWS age classes, subadults were misclassified as adults and yearlings 36.2% of the time, while yearlings were misclassified as pups 52.6% of the time.

Within seasons, autumn seals statistically differed by age class (MANOVA: Wilks Inline graphic = 0.260, P < 0.001; 80.5% classification success; Fig. 5E), with yearling and pup FA profiles defined by MUFA 16:1n-7 (first discriminant; Fig. 5E) and pups further defined by SFA 16:0 (second discriminant; Fig. 5E). Spring seals also differed by age class (MANOVA: Wilks Inline graphic = 0.327, P < 0.001; Fig. 4D), with pups defined by SFA 16:0 (first discriminant; Fig. 5D) and subadults and yearlings defined by MUFA 18:1n-9 (second discriminant; Fig. 5D). This analysis correctly classified 80.5% of autumn seals into the correct age classes, while only 45.4% of spring seals were correctly classified into age classes. The most autumn misclassifications occurred among yearlings, with 100% misclassified as pups. There was a greater degree of misclassification in age classes for spring seals, with 52.6% of subadults and yearlings misclassified as pups.

Bristol Bay

Due to the sample distribution, only blubber FA profiles for pups and adults sampled in fall were analysed. Fall blubber FA profiles from BB individuals differed significantly between pups and adults (MANOVA: F14,46 = 26.4, P < 0.001; Fig. 6). Analysis of variance (ANOVA) conducted on each dependent variable revealed age class differences for SFAs 14:0 (F1,59 = 16.2, P < 0.001) and 16:0 (F1,59 = 21.1, P < 0.001), MUFAs 14:1n-5 (F1,59 = 40.2, P < 0 0.001), 16:1n-7 (F1,59 = 23.9, P < 0.001), 20:1n-11 (F1,59 = 11.8, P = 0.001) and PUFA 22:5n-3 (F1,59 = 9.5, P = 0.003).

Figure 6.

Figure 6

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Variation in percent composition by weight (±SE) of 14 selected fatty acids for autumn harbor seals in Bristol Bay (adults n = 40; pups n = 21).

Discussion

We found statistically significant differences in the blubber FA profiles of Alaskan harbour seals by region, season and age class, with MUFAs, and to a lesser degree, SFAs, identified as the primary FA groups for classification (Table 3). The MUFAs responsible for over 60% of the FA differences are 16:1n-7 and 18:1n-7, particularly between regions and seasons, while SFA 16:0 and MUFA 16:1n-7 appear to direct age class differences (Table 3).

Table 3.

Summary of Alaskan harbour seal blubber FAs identified through LDA and MANOVA (BB age class only)

Region Season Age class
BB 16:1n-7, 18:1n-7 Fall Adult 20:1n-11
Pup 14:0, 16:0, 14:1n-5, 16:1n-7
Spring 18:1n-7
Adult 22:5n-3
PWS 18:1n-7, 14:00 Summer 16:1n-7 Subadult 14:0
Yearling 18:0, 16:1n-7
Pup 16:00
Winter 14:1n,5
Adult 20:1n-11, 20:5n-3
Spring 14:1n-5, 18:1n-7, 14:00 Subadult 18:1n-9
SEA 18:1n-9 Yearling 16:0, 18:0
Pup 16:0, 18:0
Summer 14:1n-5, 16:00
Adult 22:5n-3, 18:1n-7
Yearling 16:1n-7, 18:0
Pup 16:0, 16:1n-7, 18:0
KOD 18:1n-7, 22:6n3
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Regional differences in blubber FA profiles

Regional analysis revealed that harbour seals sampled within BB, PWS and SEA had the greatest concentrations of 18:1n-9 in their blubber, whereas the concentration of the MUFA 16:1n-7 was highest in KOD seals (Fig. 2). The elevated levels of 16:1n-7 in KOD seals found in this study differ from those previously reported by Iverson et al. (1997) who found 18:1n-9 to be the most abundant FA in KOD, PWS and SEA harbour seal blubber. FA analysis on other phocid species have found similar trends to KOD seals, with Alaskan bearded (Erignathus barbatus) and ringed (Phoca pusa huspida) seals having the highest concentration of MUFA 16:1n-7, while ribbon (Histriophoca fasciata) and spotted (Phoca largha) seals appear to have increased levels of 18:1n-9 (Cooper et al., 2009). As 18:1n-9 is the most abundant monoenoic FA in fat deposits (Barboza et al., 2008), this difference may be an artefact of this study’s sampling distribution (KOD was primarily pups), an artefact of the sample size in the previous study (n = 8; Iverson et al., 1997), or regional differences in prey (Pitcher, 1980a,b; Hastings et al., 2004).

The statistically significant regional differences observed are consistent with previous studies of FA signatures of harbour seals (Iverson et al., 1997) and Steller sea lions (Beck et al., 2007b; Keogh et al., 2019) in Alaska. Regional differences in blubber FA profiles are possibly driven by diet differences tied to the bathymetry of each region, which influences prey distribution and variation (Bowen et al., 2002). Our data revealed that the blubber FA profile of harbour seals from SEA were significantly different from FA profiles of seals from BB, KOD and PWS (Fig. 3). The bathymetry of SEA is deeper closer to shore compared to KOD and PWS, resulting in seal dive profiles that are deeper (300 to >800 m) and more variable (Pickard, 1967; Hastings et al., 2001, 2004). It has been speculated that foraging in deeper waters provides more diverse prey types or sizes (since many prey species are stratified by size with depth in the water column), as well as more mobile prey that require greater pursuit and movement through many water depths (Bowen et al., 2002). Historical diet studies have documented differences between harbour seals in SEA to those in the Gulf of Alaska (Imler and Sarber, 1947; Pitcher, 1980a; Lowry et al., 1982; Burns and Gol’tsev, 1984). More recent studies using stable isotopes and faecal analysis indicate that the diet of harbour seals in Glacier Bay (SEA) varies when compared to the diet of seals in PWS, with Glacier Bay seals consuming capelin (Mallotus villosus), eelpout (Lycodes palearis), gunnels (Pholididae sp.), hake (Merluccius productus), shanny (Lumpenus maculatus), snailfish (Liparidinae sp.) and polychaetes, while seals in PWS uniquely consume eulachon (Thaleichthys pacificus), mackerel (Pleurogrammus monopterygius) and ronquil (Ronquilus jordani) (Herreman et al., 2009).

The large overlap between BB and KOD FA profiles suggests a similar prey distribution between these two regions, despite physical separation via the Alaska Peninsula. Both areas have more expansive and shallower bathymetry compared to both PWS and SEA, with depths generally less than 100 m (Feder and Jewett, 1986; Loher et al., 1998; Drumm et al., 2016). In addition, there is a large amount of water mixing between these two regions, with currents flowing from the North Pacific into the Bering Sea and BB, as well as current waters moving from KOD through both Unimak Pass and Samalga Pass (Fig. 1) into the Aleutian North Slope Current that flows into BB (Drumm et al., 2006). Because of the current mixing and similar bathymetry between the regions, they are classified together into the same zoogeographic province (The Aleutian Province) that shares a similar invertebrate community structure (Drumm et al., 2006), likely leading to a similar vertebrate community structure.

Previous studies have reported that the diet of harbour seals in the Bering Sea resembles the diets of seals in the Gulf of Alaska (KOD and PWS) more closely than seals in SEA (Imler and Sarber, 1947; Pitcher and Calkins, 1979; Lowry et al., 1982; Hoover-Miller, 1994). This would also explain why our analysis separated BB, KOD and PWS from SEA. The elevated levels of 16:1n-7 and 18:1n-7 in the blubber FA profiles of BB and KOD seals (Fig. 2) reflect a higher proportion of benthic prey, such as capelin, flatfishes, Pacific sand lance (Ammodytes personatus) and octopus (Octopus sp.) (Pitcher and Calkins, 1979; Pitcher, 1980a,b), all of which exist in shallow (<100 m), near-shore environments and have higher proportions of n-7 isomers when compared to pelagic species (Iverson et al., 2002; Cooper et al., 2009). Conversely, harbour seals in PWS eat large concentrations of pollock, herring (Clupea pallasii) and salmon (Oncorhynchus sp.), which reside in deeper waters characteristic of PWS (Pitcher and Calkins, 1979; Pitcher, 1980a).

Seasonal differences in blubber FA profiles

Within regions, statistically significant seasonal differences in blubber FA profiles were evident in sampled harbour seals, indicating possible changes in dietary intake across seasonal scales. Due to inconsistent seasonal field sampling within regions, we were only able to examine seasonal differences for PWS and SEA. Seasonal misclassification rates for PWS (range: 4.2%–66.7%) and SEA (range: 17.6%–54.8%), suggest similarities between FA profiles within each region (Fig. 4). This seasonal overlap with individual FAs was expected given blubber FAs reflect weeks to months of diet (Budge et al., 2006); therefore, blubber samples at the beginning of one season may reflect diets spanning the previous season. In addition, the FA similarities among seasons may indicate the presence of prey items that are seasonally consistent in the diet of harbour seals in PWS and SEA.

Faecal and stomach analyses have reliably documented seasonal fluctuations in harbour seal diet that mirror seasonally abundant species (Pitcher and Calkins, 1979; Pitcher 1980a,b; Harvey, 1989). In SEA, whisker stable isotope analysis revealed that harbour seals shift between benthic and pelagic prey depending on the season, consuming proportionately higher trophic level benthic prey, such as rockfish (Sebastes sp.), flounder (Atheresthes stomias) and sculpin (Myoxocephalus sp.) in the autumn, and more pelagic prey from a higher trophic level in the spring (Smith et al., 2019). The shift towards proportionately more pelagic prey, such as adult salmon, herring, capelin and sand lance (Herreman et al., 2009; Bjorkland et al., 2015; Smith et al., 2019), which spawn in shallow water in the spring (Norcross et al., 2001; Arimitsu et al., 2008), may be advantageous for harbour seals because they contain higher concentrations of lipids compared to intertidal/demersal fish species, providing greater lipid intake (Anthony et al., 2000; Trumble et al., 2003) in preparation for pupping, breeding and moulting that occurs late spring through summer (Hoover-Miller, 1994).

Similar seasonal diet trends have been documented in PWS seals, which are thought to feed primarily on pollock in fall and winter, herring in winter and spring and salmon in the summer (Hoover-Miller, 1994). During the winter season, harbour seals within PWS make longer, deeper dives (Frost et al., 2001; Hastings et al., 2004) to forage on prey that form aggregated shoals deeper in the water column, such as herring and juvenile pollock (Brodeur and Wilson, 1996; Ryer and Olla, 1998; Helfman et al., 2009). During summer, harbour seals spend only ~40% of their time in the water due to pupping, breeding and moulting activities (Frost et al., 2001). During this time, summer seals appear to feed on prey that are more abundant and occur closer to shore, such as capelin and eulachon, as well as adult salmon that return to nearshore areas to spawn in summer (Robards et al., 1999; Frost et al., 2001). Pitcher (1986) showed that PWS harbour seal blubber thickness, and the percent of body weight made up of blubber increases during May–July, suggesting that in spring and summer seals are obtaining more energy with less time spent foraging.

LDA results suggest n-7 isomers, such as 16:1n-7 and 18:1n-7 are responsible for seasonal differences in the observed FA profiles, specifically summer and spring profiles in PWS and autumn and spring in SEA. Apart from the autumn months in SEA, it was surprising that n-7 FA was responsible for differences in spring and summer months, as these FAs are more common in benthic organisms (Iverson et al., 2002; Cooper et al., 2009). Current dietary knowledge of Alaskan harbour seals suggests these seals are consuming more pelagic prey during spring and summer (Hoover-Miller, 1994; Frost et al., 2001; Smith et al., 2019). Greater availability of pelagic prey is verified by Beck et al. (2007b) who recorded elevated levels of 20:1n-9, 20:1n-1 and 22:1n-11in Steller sea lion pups in SEA and PWS during similar summer and spring sampling time frames and locations, suggesting the pups and their mothers were likely consuming more opportunistically available pelagic prey items that display higher 20:1n-9 and 22:1n-11 concentrations (Cooper et al., 2009). Elevated 20:1n-9, 20:1n-11 and 22:1n-11 are also seen in ribbon and spotted seal FA profiles sampled during May and June on Little Diomede Island, Alaska, where these seals consume Arctic cod, as well as pollock, herring and capelin (Cooper et al., 2009). The results of this study suggest that benthic level prey items may compose a higher portion of harbour seal diets in PWS and SEA in spring and summer months. This has been reported in other phocid species in Alaska, as ringed seals in summer and spring have a higher proportion of 16:1n-7 compared to other phocids sampled in the same area (Cooper et al., 2009). In addition, Cooper et al. (2009) recorded elevated levels of n-7 isomers in Alaskan bearded seal blubber profiles, implying a shift towards a more benthic-dominated diet by bearded seals in the northern Bering Sea starting in the late 1970s. Similarly, the diet of seals in KOD is believed to have been impacted following the 1977 climate regime shift that reorganized the marine community structures in the western Gulf of Alaska (Anderson and Piatt, 1999; Small et al., 2003). While it is unlikely that benthic organisms contribute to a majority of the diet for seals in spring and summer months in SEA and PWS, interspecific dietary studies would determine if harbour seals might be modifying their diet due to competition with other species such as Steller sea lions, or if benthic prey are becoming more opportunistically available during those months.

The importance of 14:1n-5 in our analysis was unpredicted given our values were relatively low compared to other FAs examined (0.92 ± 0.03% to 2.68 ± 0.11%, Fig. 2); however, they are similar to previously published concentrations of 14:1n-5 in harbour seals in PWS, KOD and SEA (1.76 ± 0.62% to 2.33 ± 0.72%; Iverson et al., 1997), as well as other phocids (ringed seal, 2.58 ± 0.36%; Strandberg et al., 2008). While 14:1n-5 is found in prey, it is predominantly a product of de novo biosynthesis (Ackman et al., 1988; Iverson et al., 1995; Iverson et al., 2004) and has been shown to be highly enriched in the outer blubber layer (Strandberg et al., 2008). The primary purpose of the outer layer of blubber is insulation for thermoregulation, and it is characterized as having relatively increased amounts of short-chain monounsaturated FAs (typically 14:1n-5 through 18:1n-7), which are adapted to low temperatures, and less available for metabolism (Strandberg et al., 2008). The importance of maintaining the thickness of this layer is clear for most marine mammal species, as a depletion of the insulating blubber layer would lead to increased metabolic costs of maintaining thermal balance (Strandberg et al., 2008). One possible biochemical mechanism involved in the maintenance of this layer could be efficient de novo synthesis of specific FAs (Strandberg et al., 2008), such as 14:1n-5. While an increase in 14:1n-5 in the winter months in PWS could be explained due to decreased water temperatures in the years sampled (NOAA, 2021) and a need for increased insulation, the importance of 14:1n-5 in summer and spring in SEA is less straightforward. Perhaps 14:1n-5 is being synthesized to replace other insulating FAs needed for metabolic purposes, in response to environmental pressures to increase insulation during those months, or to be utilized as a retainer for excess molecules, such as acetyl-CoA, triggered by hormonal insulin responses (Borer, 2013). While 14:1n-5 does not make up a large portion of the MUFAs in the blubber of these harbour seals during any season sampled, more recent sampling is needed to determine if 14:1n-5 is becoming more important in the structure of the blubber layer during spring and summer in SEA or if our findings are exclusive to this sampling time frame of 1–6 yrs (Table 1).

Age class differences in blubber FA profiles

Age class analysis for harbour seals sampled within PWS and SEA revealed a progressive change in FAs from pups to adults, with a shift from SFAs and short-chained MUFAs in the pup blubber to more long-chain MUFAs and PUFAs in adults (Fig. 5A and B). The largest number of misclassifications for both regions occurred between adults, subadults and yearlings (21.8%–36.2%) with subadults having the greatest diet overlap with other age classes. Diet overlap between adults and subadults has been documented from stomach and faecal analysis of harbour seals (Anderson et al., 2004) and suggests foraging similarities and comparable dive physiology among age classes. This is corroborated by Burns et al. (2005) who reported the oxygen storage capacity of harbour seal yearlings and adults are similar, despite the large difference in body size. In addition, these data appear to support diet overlap existing among yearlings, subadults and adults, with the greatest separation existing between adults and pups. This suggests age class FA differences between adults and subadults may be a result of inefficient foraging, versus physiological capacity (Lowry et al., 2001), whereas FA differences between adults and pups may be reflective of the development of mass-specific oxygen stores (Burns et al., 2005). This is evident in isotopic signature variation in harbour seal muscle and liver tissue, which reflects age specific foraging strategies, such that adults forage at higher tropic levels compared to pups (Young et al., 2010). Previous harbour seal prey studies in Alaska also suggest foraging differences between pups and adults, with pups feeding on smaller, easier caught prey items such as capelin, small pollock, tomcod, sand lance and shrimps (Pitcher and Calkins, 1979; Pitcher, 1980a, b).

Age class analyses revealed SFA 16:0 important in distinguishing among age groups with pups having elevated 16:0 concentrations in their blubber (Fig. 5A and B). A similar trend was also found when examining age classes within seasons (Figs 5C–E and 6). In addition, MUFA 16:1n-7 seems to be characteristic to yearlings in the summer and to pups in the spring and autumn months (Table 3). This could be explained by the age brackets used to distinguish age classes. The value of 0.75 was chosen as the threshold between pups and yearlings as a conservative bound to ensure that yearlings were not classified as pups (Blundell and Pendleton, 2008). While an estimated age was applied to all seals, it can be assumed that the FA profiles of PWS summertime pups likely originate from the mother, as pups in this region are typically birthed in June, and the majority pups sampled in summer were sampled mid to late June, prior to weaning (ADF&G personal communication). Therefore, 16:0 appears to be a distinguishing FA for pups (Fig. 5C). Studies on the larger hooded seal (Cystophora cristata) revealed that SFA 16:0 and MUFA 16:1n-7 are both elevated in the blubber of pups at birth at a ratio of 1.5 and 2.6 to that of their mothers (Iverson et al., 1995). A similar mother pup trend was observed in Weddell seals (Leptonychotes weddellii), with more saturated FAs and short chain MUFAs being selectively mobilized by mothers to pups, corresponding to increased levels of 14:0, 16:0 and 16:1n-7 in pup blubber (Wheatley et al., 2008). These authors speculated mothers produce lipid-rich milk with elevated SFAs and MUFAs to meet the pup’s thermoregulatory needs, and progressively increase protein needed for tissue growth as weaning approaches. SFAs may be higher in milk postpartum because of increased usable chemical energy to neonates (Wheatley et al., 2008), maximizing the energy the pup receives. An increase in MUFAs later in lactation offers optimal energy storage by providing higher caloric density compared to PUFAs and higher mobilization and oxidation rates when compared to SFAs (Maillet and Weber, 2006; Trumble and Kanatous, 2012). Similar accounts of elevated 16:0 in mother’s milk during lactation have been documented in northern elephant seals (Mirounga angustirostris; Fowler et al., 2014), grey seals (Halichoerus grypus; Grahl-Nielsen et al., 2000; Arriola-Ortiz, 2010) and hooded seals (Iverson et al., 1995). Our FA analysis suggests a similar response in elevated 16:0 levels may be occurring in the smaller harbour seal.

Conclusion

In summary, the 14-yr analysis of Alaskan harbour seal blubber FA profiles revealed regional, seasonal and age class differences. This study provides a comprehensive seasonal and spatial perspective of blubber FA profiles of Alaskan harbour seal populations and suggests the following: (i) MUFAs, particularly 16:1n-7 and 18:1n-7, can distinguish regional, seasonal and age class blubber FA profiles; (ii) there is an age class shift in blubber FAs with pup’s blubber containing more SFAs and short-chained MUFAs and adult’s characteristic of more long-chain MUFAs and PUFAs; and (iii) 16:0 is an important and distinguishing blubber FA for pups in Alaska.

Because Alaskan harbour seals have a high degree of site fidelity, they can be utilized as a sentinel species to monitor ecosystem health and provide insight into varying population dynamics. Due to the sample size and scope of this project, we were able to expand upon previously reported FA profiles to include the BB harbour seal population and provide the first detailed account of seasonal and age class blubber FA differences for PWS and SEA populations (Table 3). With this information as a baseline, we believe future sampling of blubber FAs from Alaskan harbour seal populations could be a useful tool in assessing the response of this species and ecosystems to changes associated with natural and anthropogenic pressures. We also hope this study guides future sampling timelines to include seasons and age classes currently lacking data in the hopes to expand this research to examine age class differences across seasons, as well as sex differences among age classes. Lastly, quantitative estimation of diet composition within regions, seasons and age classes using QFASA (Iverson et al., 2004) would be the next important step in understanding how prey variation is driving many of the differences we observed.

Funding

This work was supported by the National Marine Fisheries Service [NA57FX0367, NA87FX0300, NA17FX1080, NA04NMF4390140, NA07NMF4390143 and NA08NMF4390544].

Supplementary Material

CONPHYS-2020-139_Supplementary_Resubmit_coab036
Click here for additional data file. (10.5MB, docx)

Acknowledgements

We would like to thank the Alaska Department of Fish and Game staff, collaborators and volunteers involved in the field sampling and sample processing in the laboratory. We would also like to thank Gail Blundell for enabling FA sample collection and analyses as program leader at ADFG, as well as Stephanie Wong and Brandan Neises for their help developing the images and graphical scripts used in this manuscript.

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