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Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54

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Journal of Experimental Marine Biology and Ecology

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Resource partitioning by sympatric Steller sea lions and northern fur seals as revealed by biochemical dietary analyses and satellite telemetry

Jason N. Waite a,b,⁎, Stephen J. Trumble c, Vladimir N. Burkanov d,e, Russel D. Andrews a,b a School of Fisheries and Ocean Sciences, University of Alaska, 905 North Koyukuk Drive, 245 O'Neill Building, Fairbanks, Alaska, 99775, USA b Alaska SeaLife Center, PO Box 1329, 301 Railway Ave, Seward, Alaska, 99664, USA c Baylor University, One Bear Place #97388, Waco, Texas, 76798, USA d National Marine Mammal Laboratory, National Oceanic and Atmospheric Administration, 7600 Sand Point Way NE, Seattle, WA 98115, USA e Kamchatka Branch of the Pacific Institute of Geography, Far East Branch of Russian Academy of Sciences, 6 Partizanskaya Street, Petropavlovsk-Kamchatsky, 683000, Russia article info abstract

Article history: Over 1000 endangered Steller sea lions (SSL, Eumetopias jubatus Schreber, 1776) and approximately 14000 Received 28 October 2011 northern fur seals (NFS, Callorhinus ursinus L., 1758) breed sympatrically at the Lovushki Island complex, Received in revised form 13 February 2012 located in the northern Kuril Island chain in the Russian Far East, creating the potential for inter-specific Accepted 15 February 2012 competition for prey resources. The diets and foraging locations of both species were examined through Available online xxxx the analysis of δ15N and δ13C stable isotope (SI) ratios of vibrissae, fatty acid (FA) profiles of blubber biopsies, and telemetry data collected during the breeding seasons of 2007 and 2008. There were significant differences in Keywords: δ15 δ13 fi δ15 Fatty acids the mean Nand C values between SSL and NFS. Adult female SSL were signi cantly enriched in both N 13 Northern fur seal and δ C over adult female NFS (by 2.04‰±0.23‰ and 0.83‰±0.12‰, respectively), which indicates that the Resource partitioning sea lions were feeding at a higher trophic level and in a different geographical location than the fur seals. The Stable isotopes higher mean δ13C levels found in the sea lion vibrissae suggest that they fed nearshore and benthically, while Steller sea lion fur seals fed primarily offshore and pelagically. There were significant differences in the blubber FA profiles Telemetry between SSL and NFS, indicating that the two species have different foraging strategies with respect to the types and/or proportions of prey items consumed. Foraging behavior analysis also indicated that SSL foraged nearshore and benthically and breeding NFS foraged primarily offshore and pelagically. The combination of these methodologies suggests breeding NFS and SSL partition their forage resources by prey type, as well as spatially, which likely reflected the differences in provisioning strategies of the adults and the fasting abilities of their pups. © 2012 Elsevier B.V. All rights reserved.

1. Introduction changes in the prey base composition (Calkins and Goodwin, 1988; DeMaster and Atkinson, 2002; NMFS, 1995). After experiencing an Steller sea lions (SSL, Eumetopias jubatus Schreber, 1776) breed approximate 80% decline in population from 1955 to 1989, followed sympatrically with northern fur seals (NFS, Callorhinus ursinus L., by a slight increase, the abundance of non-pup SSL on Lovushki Island 1758) on four rookeries in the Russian Far East, including Lovushki has remained relatively stable at an average of 1039 SSL from 1995 to Island (48.5436° N, 153.6736° E) in the Kuril Island chain (Fig. 1). 2005 (Burkanov and Loughlin, 2005). After a slow recovery from Approximately 43% of the total SSL pup production in Russian waters eradication in the late 19th century, the NFS population also experienced occurs on these rookeries (Burkanov and Loughlin, 2005). Similar to a period of relative stability from approximately 1978–1988 (Kuzin, the Western stock of SSL in North American waters, the Asian stock 1999); however, a rapid increase in NFS population numbers ensued of SSL experienced a dramatic decline and has been unstable for the during the early 21st century, and the pup population grew to 12180 past four decades (Burkanov and Loughlin, 2005; Loughlin et al., pups by 2006 (Burkanov et al., 2007), placing the non-pup population 1992). Although the cause has not been determined, one hypothesis on Lovushki Island at an estimated 28420 adult and juvenile NFS when for the decline in North American waters is nutritional stress due to pups are assumed to comprise 30% of the total population (Kuzin, 1999). Non-interbreeding species occupying the same ecological niche and exploiting the same limited resources must modify how they ⁎ Corresponding author at: University of Alaska Fairbanks, School of Fisheries and exploit the available resources in order to reduce inter-specific com- Ocean Sciences, Fisheries Division, 17101 Point Lena Loop Road, Juneau, AK 99801 petition that may cause the absolute exclusion of one of the species. USA. Tel.: +1 907 796 5455; fax: +1 907 796 5446. SSL and NFS are both piscivorous, sexually dimorphic pinnipeds E-mail addresses: [email protected] (J.N. Waite), [email protected] (S.J. Trumble), [email protected] with similar ecological requirements and life history traits. With a (V.N. Burkanov), [email protected] (R.D. Andrews). 2–3 month overlap in breeding seasons (May–August) and pup nursing,

0022-0981/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2012.02.009 Author's personal copy

42 J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54

144° E 146° E 148° E 150° E 152° E 154° E 156° E

N Lovushki Islands Detail 52° N 52° N

Dolgaya Rock Antsiferov 50° N Paramushir 50° N Island

Vysokaya Rock

Raykoke Lovushki Islands Tyuleny 48° N 48° N Island Srednego

Brat Chirpoev

46° N Regional Area of Detail 46° N Urup Island Russia Iturup Island Medny Island 44° N 44° N Japan Pacific Ocean 0 100 200 300 km

144° E 146° E 148° E 150° E 152° E 154° E 156° E

Fig. 1. Location of study site. foraging could become competitive as adult females of both species are of physiological condition and maternal strategies (Newsome et al., central place foragers, alternating between periods of foraging at sea 2006; Sinisalo et al., 2008). The stepwise enrichment of 15N in tissues and nursing their pups on land (Gentry, 2002; Gentry and Kooyman, of ~3–5‰ per trophic level allows for the estimation of an organism's 1986; Mathisen et al., 1962; Pitcher and Calkins, 1981). relative trophic position in a food web (DeNiro and Epstein, 1981; To assess the level of dietary overlap, and thus competition for Minagawa and Wada, 1984). Carbon isotope ratios are less significant prey between two sympatric species, it is often necessary to consider in determining trophic position in marine mammals because of the foraging behavior and prey consumption over a range of time scales. weak isotopic fractionation of 13C (~0.1–1.1‰) across trophic levels Distribution of prey items may change over the course of the breeding of higher level consumers (DeNiro and Epstein, 1978; Hirons et al., season, prompting a change in foraging effort by one or more of the 2001a; Kurle and Worthy, 2001), but δ13C levels can be used to deter- resident predator species. Further, any one particular sampling effort mine relative foraging location (France, 1995; Hobson, 1999; Kurle may occur during an anomalous and/or ephemeral influx of a specific and Gudmundson, 2007; Kurle and Worthy, 2002). prey type, and depending on the type of sample collected, inferences Isotopic signatures of metabolically active tissues reflect recent regarding the overall dietary composition for the entire breeding season feeding activity, whereas tissues with slower biochemical turnover based on such samples may be erroneous. rates integrate SI from the diet over longer periods of time (Hobson The composition of SSL and NFS diets has been determined primarily and Clark, 1992; Kurle and Worthy, 2002; Lesage et al., 2002). Serum through the analysis of undigested prey remains recovered from has one of the fastest isotopic turnover rates (Lesage et al., 2002) stomach and intestinal contents, scats, and spews (Gudmundson et al., and its SI signature corresponds to dietary assimilation from feeding 2006; Trites et al., 2007; Waite and Burkanov, 2006; Waite et al., 2012; activity within the previous 10–20 days (Hilderbrand et al., 1996; Zeppelin and Ream, 2006). However, there are a number of biases MacAvoy et al., 2006). However, the collection of serum (as well as implicit to these techniques (Arim and Naya, 2003; Dellinger and most other tissues) is an invasive procedure and the compilation of Trillmich, 1988; Gales and Cheal, 1992; Harvey and Antonelis, 1994; large sample sizes may prove difficult. The isotopic composition of Staniland, 2002). On Lovushki Island, where inter-specificspatialmixing the biologically active portion of vibrissae (i.e., the root) reflects that of sympatric species occurs, it can be difficult to distinguish between of serum and corresponds to the previous 10–20 days of feeding activ- scats of different predator species without molecular techniques ity for SSL (Stegall et al., 2008). While SI analysis of vibrissae does not (Waite et al., 2011). Determination of diet among different age and identify specific prey species, it can provide a time-integrated record reproductive groups can also be difficult when relying on scats. Fur- of a predator's trophic level and general foraging location, possibly thermore, analysis of samples from a single collection effort only pro- over the entire lifespan of the animal (Hirons et al., 2001b). vides information on prey consumed during the animal's most recent Fatty acids (FA) are the primary constituents of lipids, and when foraging trip and results may be biased by opportunistic feeding during consumed, can provide an index of seasonal, sex, geographic as well the return trip from the primary foraging grounds or from voiding of as inter/intraspecific dietary differences (Beck et al., 2005; Grahl- gastrointestinal contents while at sea. Nielsen et al., 2005; Iverson et al., 1997; Meynier et al., 2008; Møller Naturally occurring stable nitrogen (15N) and carbon (13C) iso- et al., 2000; Thiemann et al., 2008). The period represented by the topes (SI) in pinniped tissues have been used successfully for the FA profile in the blubber of fur seals and sea lions may depend on reconstruction of diets and trophic position (Dehn et al., 2007; Hall- the physiological condition of the animal at the time of sampling. Aspland et al., 2005; Hobson et al., 1997), estimation of foraging loca- During periods of heavy feeding and weight gain, usually outside of tion (Aurioles et al., 2006; Burton and Koch, 1999), and investigation the breeding season, the FA profile may reflect either the current Author's personal copy

J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54 43 diet or an integration of dietary FA over periods of weeks to months dart with a 35-mm-long biopsy tip for SSL and a 20-mm-long tip for (Beck et al., 2005; Iverson et al., 2007). NFS. Of these samples, two were from adult female SSL, one from a The existence of a dietary overlap as determined through these indi- juvenile male SSL, and two from adult male NFS, resulting in a total ces may be indicative of direct competition between the sympatric of 41 NFS and 16 SSL blubber samples. Sampling location for remotely predators only if the actual foraging locations of each predator species collected biopsies was the pectoral region, midway between the fore- overlap. In cases where the species and sizes of the prey items con- flippers. Samples collected in 2007 were stored in 2.0 mL cryovial sumed overlap, intra- and inter-specific competition for food resources tubes at −20 °C. Samples collected in 2008 were flushed with nitro- can be minimized by spatial partitioning of the foraging grounds (Baylis gen gas and stored in liquid nitrogen. All samples were transferred et al., 2008; Robson et al., 2004). With the recent development of GPS to −80 °C upon returning from the field, approximately 1–2 months tags suitable for use on marine mammals, location and movement after collection. can be tracked at high levels of accuracy, thereby providing corollary Concurrent with vibrissa and blubber collection, telemetry instru- evidence in cases where the species of prey items consumed appear ments were attached to 14 adult female northern fur seals and 13 to overlap. Depending on the method used to attach the instruments, adult female Steller sea lions. In 2007, each animal was instrumented pinnipeds can be tracked for up to several months before the batteries with an Mk10-F TDR with FastLoc GPS receiver (Wildlife Computers, fail or the instrument is lost during molt. Thus, it is possible to examine Inc., Redmond, WA), which was attached dorsally to the head using the foraging behavior of a pinniped over the course of its entire 5-min epoxy. At least one other instrument was attached dorsally, breeding season without multiple disturbances of the rookery. approximately two-thirds towards the tail of each animal, usually a Similar life history traits and ecological requirements, along with variant of the Mk10 TDR customized to record different variables recent growth in the population of both NFS and SSL in the Kuril along with depth measurements. Some NFS were transported back Islands, suggest the potential for elevated inter-specific competition to the support vessel upon capture prior to instrumentation for for food resources. The level of inter-specific competition might not other research purposes before being released on or near the rookery. be accurately assessed solely through the analysis of scats and All SSL were instrumented on the rookery. Instruments deployed on spews. Therefore, we combined the analysis of δ15Nandδ13Cstable NFS and SSL in 2007 were recovered when the animals were recap- isotope values of vibrissal roots, fatty acid profiles of blubber, and satel- tured after visual and VHF tracking of the animals indicated that at lite telemetry to examine the use of prey resources of sympatrically least one foraging trip had been made. NFS and SSL in 2007 were breeding SSL and NFS on Lovushki Island. We compared the results recaptured between 3–39 and 8–12 d post-deployment, respectively. with data from concurrently collected scats and spews (Waite et al., Instrument deployments for NFS in 2008 were similar; however, SSL 2012) to assess the convergence of data representing different time were equipped with Mk10-AFL satellite transmitters and did not scales and to gain further understanding of the foraging ecology and have to be recaptured to recover the data. Results of a concurrent resource partitioning of these two species. study on the effects of tag size on diving behavior suggest that the tags attached to the northern fur seals in this study had no discern- 2. Methods able effect on foraging trip duration and only minor effects on dive duration (Skinner et al., 2011). Depending on the instrument model, 2.1. Sample collection depths were recorded at either 1.0 or 2.0 Hz at a resolution of 0.1 m. Upon examination of the tracking data, it was determined that one During the breeding seasons of 2007 and 2008, vibrissae were col- SSL had not left the rookery before it had been recaptured and lected from NFS (n=95) and SSL (n=63) on Lovushki Island, Russia. those data were excluded from analysis. Of the NFS, samples were collected from 45 live adult females, 5 dead adult females, 23 live pups, and 20 dead pups. Vibrissae were also 2.2. Laboratory analyses collected from a single dead adult NFS male and a dead NFS juvenile of unrecorded sex. Vibrissae collection from live adult animals was Vibrissae were soaked in a Branson 3510 ultrasonic water bath performed under gas anesthesia (Heath et al., 1996) whereas samples (Branson Ultrasonics Corporation, Danbury, Connecticut, USA) at 25 °C from pups were collected under manual restraint. Adult animals were for a minimum of 10–20 min or until the root sheath was sufficiently anesthetized for 30–120 min while procedures were performed for softened to allow easy removal. The surfaces of the vibrissae were concurrent research projects, such as deuterium oxide dilution for then cleaned with a solution of chloroform-methanol volumetrically body composition analysis. Vibrissae samples from dead animals mixed at a 2:1 ratio to remove any contaminating lipids. The vibrissal were collected opportunistically on the rookery. Of the SSL, samples roots were cut at 0.1–0.4 cm from the proximal end to obtain segments were collected from 19 live adult females, 9 dead adult females, 11 of 0.800–1.200 mg, which were weighed to the nearest 0.001 mg on a live pups, and 24 dead pups. From 2 adult female NFS and 4 adult fe- Sartorius CP2P scale (Sartorius AG, Goettingen, Germany) into Costech male SSL, vibrissae were collected twice over a period of 4–6 weeks. 3.5×5 mm pressed tin capsules (Costech Analytical, Valencia, California, Of the 158 animals sampled, vibrissae were collected from 21 NFS USA). Stable isotopes were analyzed either on a Finnigan Delta V Plus and 6 SSL mother–pup pairs. Sampling of vibrissae consisted of mass spectrometer (Thermo Scientific, Waltham, Massachusetts, USA) removing the longest vibrissa with root intact from the left cheek. coupled to a Carlo Erba elemental analyzer or a Finnigan DeltaplusXP Each vibrissa was measured (nearest mm) both before and after mass spectrometer interfaced with a Costech ECS4010 elemental ana- removal. On subsequent samplings of recaptured animals, the longest lyzer. Results are expressed in δ notation and are calculated as 13 15 vibrissa on the right cheek was removed. All samples were air-dried δX=1000×[(Rsample /Rstandard) −1], where δX is δ Corδ Ninparts 13 12 15 14 and stored in paper envelopes at room temperature until analysis. per thousand (‰)andRsample and Rstandard are the C/ Cor N/ N Concurrent with vibrissae collection, blubber biopsies were taken ratios of the sample and standard, respectively. Isotopic compositions from live female NFS (n=39) and SSL (n=13) from the right dorsal are standardized relative to atmospheric N2 for nitrogen and Vienna– area just anterior to the rear flipper insertion point. SSL biopsies were Pee Dee Belemnite limestone for carbon. collected during the second week of June in 2007 (n=6) and third FA methyl esters (FAME) were prepared as described in Iverson week of June in 2008 (n=7). NFS samples were collected from the et al. (1997). Protocols for preparing and analyzing samples collected third week of June through the end of July in 2007 (n=26) and in 2007 followed Dodds et al. (2004). Samples were analyzed on a HP during the third week of July in 2008 (n=13). An additional five 5890 Series II Plus (Hewlett-Packard, Palo Alto, CA) GC-FID using a biopsies were collected remotely using a crossbow during the third 60 m×0.25 mm ID×0.25 μm DB-23 column. The injector tempera- week of July 2008 following Hoberecht et al. (2006), using a biopsy ture was 300 °C with a 1 μl injector split ratio of 20:1. Column flow Author's personal copy

44 J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54 was 1.0 ml min− 1 with temperature ramped from 125 °C to 240 °C at each trip, was calculated using the R packages “argosfilter” (Freitas, 3 °C min− 1 for a total runtime of 40.0 min. Peaks from 10% of the 2010) and “sp” (Bivand et al., 2008), respectively. Water depth was samples were verified with GC-MS on a Varian CP-3800 GC equipped estimated at each bout location through interpolation of 30-arc- with a Varian Saturn 2200 MS. second bathymetric data (The GEBCO_08 Grid, version 20091120, Blubber biopsies collected in 2008 were processed by a separate http://www.gebco.net). lab. Protocols for preparing and analyzing these samples for FAs using a Varian 3900 gas chromatograph-flame ionization detector 2.4. Statistical analyses (GC-FID) followed Budge et al. (2006) with the following modifica- tions: Column CP-Select for FAME (CP7419) 100 m×0.25 mm Analysis of variance (ANOVA) was used to examine equality of ID×0.25 μm. The injector temperature was 250 °C with a 1 μl injector δ13C and δ15N isotope means between species (NFS or SSL), age split ratio of 50:1. Column flow was 1.0 ml min-1 programmed at class (adult female or pup, nested within species), and year (nested 210 °C for 9.0 min and ramped at 15 °C min− 1 to 260 °C for 7.7 min. within age class). Repeated measures were included using a com- Detector temperature was set at 300 °C with a hydrogen flow of pound symmetry structure for the within-subject covariance matrix. 30 ml min− 1 and air flow of 300 ml min− 1. The internal standard Consistency of variance across groups was tested using Brown– was C19:0 (Fluka 72332). Each fatty acid recovered was calculated Forsythe tests of homogeneity (Brown and Forsythe, 1974) and any as a percent of the cumulative of all fatty acids in the blubber. A set factors displaying heterogeneity were modeled as dispersion effects. of 40 standard historical marine FAME were used in the GC-FID analysis, Denominator degrees of freedom for tests of fixed effects were calcu- and 38 were used with the GC-MS. The NIST (National Institute of lated using general Satterthwaite approximations (Satterthwaite, Standards and Technology) library was utilized with GC-MS to confirm 1946). Tukey–Kramer multiple comparison tests of differences be- peaks matched with standards, and additionally, to identify novel peaks tween least-squares means were performed for significant factors. using highest probability methods. Mann–Whitney tests were used to test for differences between live and dead animals of each species and age-class combination and 2.3. Telemetry data Wilcoxon signed rank tests were used to examine differences in iso- tope ratios between mother–pup pairs and repeated samples from Latitude and longitude coordinates were calculated from the the same animal. FastLoc GPS data using software provided by the instrument manu- Relative FA concentrations are expressed as mass percent of total facturer and resultant GPS tracks were analyzed using the R package FAs and are designated according to the nomenclature of the Interna- “trip” (Sumner, 2010). Erroneous coordinates were removed based tional Union of Pure and Applied Chemistry (IUPAC) of carbon-chain- on a maximum swim speed between sequential GPS coordinates of length:number-of-double-bonds and location of the double bond 3ms–1 using an algorithm presented in McConnell et al. (1992). nearest the terminal methyl group (n–x). Relative FA concentrations Tracks were divided into individual trips based on periods when the were arcsine-square-root transformed prior to statistical treatment. animal was hauled out on dry land. Distance and duration of each trip Multivariate analysis of variance (MANOVA) was used to examine >3 h was measured. Based on movement and dive patterns, trips differences in FA profiles between species and years. Data from blub- b3 h were not considered to be representative of foraging effort, but ber samples collected in both years were examined simultaneously rather representative of departure due to rookery disturbance wherein via Principal Component Analysis (PCA) using FAs present in amounts the animals remained primarily in the surf zone and performed few ≥0.5% in at least one species in one year. Since samples from each dives. Only complete round-trips that both initiated and terminated year were analyzed in separate labs using different methods, FA on the rookery were analyzed. NFS trips that began immediately upon data were then examined via PCA for each year individually, using release from the support vessel were not included in the analysis. the set of FAs present for that particular year only. Because these mul- Depth data collected at 2.0 Hz were sub-sampled to 1.0 Hz by ex- tivariate techniques require that the number of samples in each group cluding records recorded on the half-second. Depths were zero-offset to be examined exceed the number of variables, only FAs that occur corrected (ZOC) to account for drifts in the calibration of the pressure on the extended dietary fatty acid list presented by Iverson et al. transducer. Depths were corrected by finding the minimum depth (2004) were used. Linear regression was used to examine the rela- within a 20-minute moving window and then subtracting that tionship between each principle component (PC) and δ13C and δ15N depth from all depth measurements within each window. of vibrissae of NFS and SSL from which both samples were taken. Dive profiles from TDR records were analyzed using the R package ANOVA was used to examine the equality of levels of saturated, “diveMove” (Luque, 2007). Dives b4 m in depth were excluded from monounsaturated, and polyunsaturated FAs between species and the analysis because they could not reliably be distinguished from the years. Tukey–Kramer multiple comparison tests of differences be- random noise that could not be corrected for during the ZOC proce- tween means were performed for significant factors. dure. Duration, maximum depth, and post-dive surface interval Differences in FA profiles between species for both years com- were determined for each dive, with the dive depth defined as the bined were also examined using a classification and regression tree maximum depth reached within a single dive. A bout ending criterion (CART) analysis on the relative FA concentrations using the R package (BEC) was calculated for each animal by modeling a mixture of two “rpart” (Therneau and Atkinson, 2010). CART is a non-parametric random Poisson processes to the histogram-like data of log frequency data classification technique with fewer restrictions on sample size, versus the interval mid-points of each dive (Sibly et al., 1990). Each number of variables, and normality of data than parametric methods. dive in a series of >5 dives was assigned to a specific bout if its CART is an iterative technique that recursively partitions the data into post-dive surface interval was less than the BEC calculated for that groups that are as different as possible based on the variable that particular animal. Dives not meeting these criteria were classified as explains the largest amount of variation at each iteration. The set of 22 isolated dives and excluded from further bout analyses. A geographi- FAs that were quantified by both labs were used for the CART analysis. cal location was assigned to each dive through a time-based linear Generalized linear mixed models with repeated measures were interpolation method using the GPS coordinates whose time stamps used to test for differences in dive depth and duration, trip length bounded the corresponding TDR time stamp of the beginning of and duration, and bout location between NFS and SSL and between each dive. The position of the first dive in each bout was used as the years. An autoregressive covariance structure of order 1 (AR1) was position for the entire bout. A directional vector consisting of the used to model the serial correlation among observations within bearing and distance between the bout location and the trip start each animal. Tukey post-hoc tests were performed on significant in- location, defined as the last on-land GPS coordinate recorded for teraction terms. For these analyses, V-shaped dives (dives in which Author's personal copy

J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54 45 the bottom time accounted for b5% of the total dive duration) were Table 1 15 excluded as they are considered transit or exploratory dives and not Least-square mean (±SD) δ N values for vibrissal roots of northern fur seals and Steller sea lions collected during the summer of 2007 and 2008 on Lovushki Island, representative of foraging effort (Kuhn et al., 2009; Le Boeuf et al., Russia. Matching superscript letters indicate groups with significant differences. 1988). Dives >900 s were excluded as they were likely the result of instrument error or a failure for the ZOC procedure to correctly 2007 2008 Total separate multiple dives (n=6). Watson's test for circular uniformity n ‰ n ‰ n ‰ was used to examine directionality of bout locations and Watson's Northern fur sealsa 50 14.73±0.92d 45 14.07±1.07d 95 14.26±1.07 two-sample test of homogeneity was used to examine differences in Adult femalesb,c 31 14.09±1.11 19 13.48±1.13 50 13.91±1.77 mean bout directions between species. Live 26 14.36±0.82 19 13.48±1.13 45 14.31±0.80 All means are reported±SD. Statistical analyses were performed Dead 5 13.83±0.80 5 13.83±0.80 Pupsc 18 15.53±0.81 25 14.51±1.15 43 14.95±1.11 at the 95% significance level using SAS version 9.1 (SAS Institute Inc, Live 9 15.25±0.48 14 14.59±1.16 23 14.85±1.10 Cary, North Carolina) and R version 2.11.1 (R Development Core Dead 9 15.81±0.81 11 14.43±1.16 20 15.05±1.07 Team, 2010). Adult male 1 18.43±0.0 1 18.43±0.0 Juveniles 1 14.32±0.0 1 14.32±0.0 3. Results (unknown sex) Steller sea lionsa 17 16.59±0.78 46 16.50±1.09 63 16.57±1.03 Adult femalesb,c 6 16.16±0.51 22 16.06±0.61 28 16.19±0.69 3.1. Stable isotopes Live 6 16.16±0.51 13 15.77±0.58 19 15.89±0.61 Dead 9 16.35±0.63 9 16.35±0.63 c Mean nitrogen and carbon isotope values differed between Pups 11 17.13±0.73 24 16.93±0.59 35 16.93±0.71 Live 11 16.73±0.56 11 16.73±0.56 species and age class (Fig. 2). Ratios of stable nitrogen isotopes Dead 11 17.13±0.73 13 17.12±0.58 24 17.13±0.64 (Table 1) were significantly higher in SSL than in NFS (ANOVA:

F1, 129 =176.42, pb0.001). Adult female SSL were enriched over adult female NFS by 2.15‰±0.22‰ (ANOVA with Tukey–Kramer 15 fi post-hoc test, t74 =−9.63, pb0.001). The range in δ N values for difference between SSL pups and adult females. There was no signi cant SSL and NFS was 14.58‰ to 17.60‰ and 10.92‰ to 15.84‰, respec- difference in δ13C levels between years or between live and dead SSL tively. Pups, overall, had a significantly higher mean δ15N value than and NFS (p>0.05). adult females (F2, 124 =21.27, pb0.001). Nitrogen isotope values of Values of both isotope ratios differed between vibrissae collected NFS vibrissae in 2007 were enriched by 0.89‰±0.18‰ over values from known pairs of mothers and pups. NFS pups were significantly δ15 b fi in 2008 (Tukey–Kramer, t154 =4.91, pb0.001), but there was no dif- enriched in N over their mothers (V=9, p 0.001) and had signi - ference between years for SSL (p=0.627). There was no significant cantly lower δ13C values (V=216,pb0.001). SSL pups were also signif- difference in mean δ15N values between live and dead SSL and NFS icantly enriched in δ15N over their mothers (V=1, p=0.031) and had (p>0.05). significantly lower δ13C values (V=19, p=0.047). The mean nitrogen Mean stable carbon isotope values (Table 2) were also significantly enrichment of pups over their mothers was 0.98‰±0.20‰ (range ‰ ‰ ‰ ‰ ‰ higher in SSL than in NFS (ANOVA: F1, 151=122.69, pb0.001). Adult -0.37 to 3.61 )forNFSand1.16 ±0.33 (range -0.13 to female SSL were enriched over adult female NFS by 2.04‰±0.23‰ 2.02‰) for SSL. The mean depletion of carbon was 0.42‰±0.09‰ ‰ ‰ ‰ ‰ (ANOVA with Tukey–Kramer post-hoc test, t74 =-8.71, pb0.001). The (range -0.63 to 1.26 ) for NFS pups and 0.44 ±0.26 (range range in δ13C values for SSL and NFS was −15.44‰ to −17.93‰ and -0.13‰ to 2.02‰) for SSL pups. However, not all mother–pup pairs -16.94‰ to -19.19‰, respectively. Overall, NFS adult females were followed this pattern. Of the 21 NFS pairs, two (9.5%) of the pups had significantly enriched in δ13C over NFS pups by 0.52‰±0.11‰ lower δ15N values than their mothers, one (4.8%) had a higher δ13C δ15 (Tukey–Kramer, t157 =4.67, pb0.001) but there was not a significant value than its mother, and two pups had N values that were almost identical to their mothers (9.5%). Of the six SSL pairs, one (16.7%) had alowerδ15N value and one had a higher δ13C value than its mother. Isotopic values from repeated samplings of the same animal were Dead NFS Male not significantly different. Mean δ15NvaluesofNFS(n=2) and SSL 18.2 (n=4) vibrissae sampled later in the breeding season were 0.38‰± 0.08‰ and 0.50‰±0.75‰ higher than vibrissae sampled from the 17.4 same animal earlier in the breeding season, respectively. Mean δ13C Dead SSL Pups values of vibrissae sampled from NFS and SSL later in the breeding Live SSL Pups ‰ ‰ ‰ ‰ 16.6 Dead SSL Females season were 1.07 ±0.26 and 0.51 ±0.56 lower than vibrissae sampled from the same animal earlier in the breeding season, respec- 15.8 Live SSL Females tively. Although these differences were not significant, sample sizes may be too small to make any strong statistical inferences. N (‰) Dead NFS Pups 15 15.0 δ Live NFS Pups 3.2. Fatty acids 14.2 Live NFS Females fi Dead NFS Females Sixty and 54 FAs were identi ed in greater than trace amounts ≥ 13.4 ( 0.5%) in samples from both NFS and SSL, respectively, collected in 2007 and 2008. Of these, a set of 22 FAs were quantified in both 12.6 years by both labs (Table 3). In both years, the major saturated fatty acids (SFA) found in both NFS and SSL blubber samples were 14:0 −18.6 −18.0 −17.4 −16.8 −16.2 −15.6 and 16:0 and the major monounsaturated fatty acids (MUFA) were 18:1n-9 and 20:1. In 2007, SSL blubber samples contained higher δ13C (‰) levels of 16:1 than in 2008. In 2007, the major polyunsaturated fatty acid (PUFA) was 22:6n-3, and in 2008 the major PUFA were 18:2n-6, Fig. 2. Mean (±SD) δ15N and δ13C values for vibrissal roots of northern fur seals and fi Steller sea lions collected during the breeding seasons of 2007 and 2008 on Lovushki 22:2, 20:5n-3, and 22:6n-3. There was a signi cant difference in Island, Russia. overall levels of SFA (F2,53 =109.2, pb0.005), MUFA (F2,53 =42.81, Author's personal copy

46 J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54

Table 2 Least-square mean (±SD) δ13C values for vibrissal roots of northern fur seals and Steller sea lions collected during the summer of 2007 and 2008 on Lovushki Island, Russia. Matching superscript letters indicate groups with significant differences.

2007 2008 Total

n ‰ n ‰ n ‰

Northern fur sealsa 50 −17.92 ±0.57 45 −18.19±0.54 95 −18.05±0.58 Adult femalesb,c 31 −17.76 ±0.67 19 −18.03±0.48 50 −17.88±0.92 Live 26 −17.62 ±0.51 19 −18.03±0.48 45 −17.81±0.54 Dead 5 −17.87 ±0.40 5 −17.87±0.40 Pupsc 18 −18.35 ±0.51 25 −18.30±0.50 43 −18.32±0.52 Live 9 −18.27 ±0.54 14 −18.38±0.49 23 −18.34±0.53 Dead 9 −18.44 ±0.39 11 −18.22±0.46 20 −18.31±0.49 Males 1 −16.82±0.00 1 −16.82±0.00 Juveniles 1 −18.01 ±0.00 1 −18.01±0.00 Steller sea lionsa 17 −17.11 ±0.49 46 −17.15±0.54 63 −17.12±0.56 Adult femalesb 6 −17.18 ±0.54 22 −16.94±0.61 28 −16.93±0.69 Live 6 −17.18 ±0.54 13 −16.98±0.58 19 −17.06±0.57 Dead 9 −16.90±0.63 9 −16.90±0.63 Pups 11 −17.06 ±0.66 24 −17.33±0.59 35 −17.30±0.65 Live 11 −17.47±0.56 11 −17.47±0.56 Dead 11 −17.06 ±0.66 13 −17.19±0.58 24 −17.13±0.59

pb0.005), and PUFA (F2,53 =166.34, pb0.005) in both species be- and 5 showed significant species by year interaction (pb0.05 in each tween years. NFS blubber contained significantly higher levels of SFA case). than SSL in 2007 (t1,53 =2.94, pb0.005, Tukey post-hoc test) and sig- The same set of 16 FAs that was used in the MANOVA was used in nificantly lower levels in 2008 (t1,53 =−4.07, pb0.005). There were the PCA analysis for the combined years. The first 2 principle compo- no significant differences in overall levels of MUFA between species nents (PC) in the analysis of all samples accounted for 74.9% of the in either year, nor was there a significant difference in overall levels total variance in the FA profiles. PC1 clearly separated the two years of PUFA between species in 2007. However, NFS blubber from 2008 and, although not as strongly, the two species within each year. PC1 contained significantly higher overall levels of PUFA compared to SSL represented a gradient from samples containing higher relative levels samples (t1,53 =2.51, p=0.015). of 18:2n6, 18:3n3, and 20:3n-6 to samples higher in 18:1n-9, 22:1n-9, FA profiles were significantly different between species (MANOVA: and 18:3n-3. PC2 separated the predator species within each year

F16,38 =28.77, pb0.001) and between years (F16,38 =430.37, pb0.001) and represented a gradient from samples with higher concentrations with a significant species by year interaction (F16,38 =39.32, pb0.001). of 20:5n-3, 22:0, and 18:1n-9 to samples higher in 20:1, 20:4n-6, Of these FAs, 12 showed significant differences between species and 22:6n-3 (Fig. 3). (MANOVA, test of between-subject effects, pb0.05 in each case), 14 For samples collected in 2007, 11 FAs were used in the PCA. The showed significant differences between years (pb0.05 in each case), first 3 PCs in this analysis accounted for 84.6% of the total variance in FA profiles. PC1 and PC3 each separated the predator groups,

Table 3 while PC2 did not. Samples along PC1 represented a gradient from Mean relative concentration (±SD) of the 22 fatty acids quantified in northern fur seal higher concentrations of 20:5n-3, 16:1, and 18:3n-3 to samples (NFS) and Steller sea lion (SSL) blubber from 2007 to 2008. SFA: saturated fatty acids; MUFA: monounsaturated fatty acids; PUFA polyunsaturated fatty acids.

2007 2008

NFS SSL NFS SSL 20:1 2008 SSL remote biopsies 20:4n−6 22:6n−3 Fatty acid n=26 n=6 n=15 n=10

14:0 6.54±1.33 8.68±0.64 3.20±0.85 4.47±4.81 16:0 18.78 ±3.11 16.65±2.43 9.76±2.09 6.49±5.98 18:0 6.24±1.12 2.33±0.27 1.20±0.54 6.56±6.20 20:0 0.43±0.15 0.17±0.02 2.46±0.85 2.78±2.31 M 22:0 0.04±0.05 0.0±0.0 0.94±0.62 2.27±2.09 M SFA 32.04 ±2.70 27.82±3.01 17.55±2.21 22.57 ±4.74 14:1 0.15±0.10 0.93±0.02 0.50±0.15 0.27±0.41 15:1 ––0.18±0.23 1.47±1.33 16:1 4.37±1.73 15.54±1.52 3.93±1.32 2.17±1.83 18:1n-9 34.38 ±2.75 31.22±1.47 16.61±8.06 25.68 ±13.06 20:1 12.04 ±3.01 8.06±1.03 9.80±2.59 4.62±4.62 Principle component 2 22:1n-9 1.96±0.71 1.50±0.24 0.41±0.43 0.32±0.38 24:1 0.57±0.25 0.40±0.02 2.92±3.72 1.25±0.89 MUFA 53.47 ±3.98 57.65±1.35 34.35±8.79 35.77 ±14.07 2007 NFS 18:2n-6 1.63±0.25 1.72±0.39 12.77±1.39 14.32 ±4.84 2007 SSL 18:3n-6 0.13±0.05 0.05±0.05 3.50±1.51 1.91±1.20 2008 NFS 18:3n-3 0.55±0.20 0.53±0.07 0.01±0.00 – −1.5 −1.0 −0.5 0.0 0.5 2008 SSL 20:5n−3 22:0 20:2 0.53±0.10 0.24±0.05 1.58±0.89 0.71±0.76 18:1n−9 18:3n−6 −0.4 −0.2 0.0 0.2 18:1n−9 20:3n-3 0.22±0.05 0.08±0.02 1.99±0.51 1.10±0.73 18:2n−6 22:1n−9 20:3n-6 0.15±0.05 0.11±0.02 2.95±0.97 3.09±2.56 20:3n−6 Principle component 1 18:3n−3 20:4n-6 0.50±0.20 0.41±0.12 0.88±0.81 1.92±3.10 20:5n-3 1.99±1.33 4.32±0.81 0.67±0.97 10.54 ±7.11 Fig. 3. Plot of PC1 and PC2 from principle components analysis on fatty acid composi- 22:2 ––11.40±5.07 0.34±0.91 tion of blubber of northern fur seals (NFS, circles) and Steller sea lions (SSL, triangles) 22:6n-3 8.75±2.65 6.94±1.86 12.32±2.48 7.58±7.49 collected in 2007 (open shapes) and 2008 (filled shapes). Two male NFS are indicated PUFA 14.45 ±3.47 14.41±2.47 48.06±7.44 41.52 ±10.78 by the letter “M”. Author's personal copy

J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54 47 with higher concentrations of 20:1, 22:1n-9, and 20:2. Samples along Table 4 PC2 represented a gradient from higher concentrations of 16:0, Summary of dive depth and duration for northern fur seals (NFS) and Steller sea lions (SSL) in 2007 and 2008. 20:1n-9, and 16:1 to samples with higher concentrations of 22:6n-3, 18:2n-6, and 20:4n-3. PC3 represented a gradient from higher concen- Species ID Total Max Mean Max Mean trations of 16:0, 20:4n-6, and 18:1n-9 to samples with higher concen- dives depth depth±SD duration duration± trations of 18:2n-6, 16:1, and 22:1n-9. (m) (m) (sec) SD (sec) For samples collected in 2008, 14 FAs were used in the PCA and NFS NFS-07-03 2421 84.0 12.1±9.8 190 29.8±24.6 the first 3 PCs accounted for 76.6% of the total variance. PC1 separated NFS-07-04 1557 70.5 9.5 ±7.9 204 26.4±27.6 NFS-07-05 2879 64.0 12.4±10.7 200 32.8±26.8 the samples into 3 distinct groups: NFS, SSL sampled in June, and NFS-07-24 422 57.0 24.4±10.3 134 56.8±22.6 SSL sampled in July by remote biopsy. With the exception of one NFS-07-25 857 82.5 25.4±14.6 105 45.6±20.5 SSL, PC2 clearly separated the predator species, while PC3 did not. NFS-07-27 526 59.0 24.6±11.5 109 53.2±22.9 PC1 represented a gradient from samples with higher concentrations NFS-08-01 774 59.5 19.6±11.1 133 46.9±30.6 NFS-08-02 1625 89.5 21.5±16.1 403 41.3±32.2 of 20:5n-3, 18:1n-9, and 22:0 to samples higher in 22:6n-3, 16:0, and NFS-08-07 1132 93.5 22.2±16.8 207 44.5±33.6 20:3n-6. PC2 represented a gradient from samples enriched in 16:1, NFS-08-09 1927 102.5 15.8±8.8 226 44.4±30.7 20:2, and 20:1 to samples with higher concentrations of 18:2n-6, NFS-08-10 765 90.0 19.3±16.6 150 36.0±27.7 20:4n-6, and 20:3n-6. PC3 represented a gradient from samples NFS-08-13 1761 66.0 20.3±8.4 172 32.8±21.0 enriched in 20:3n-3, 18:3n6, and 20:4n-6 to samples with higher NFS-08-14 950 45.0 11.1±6.2 329 34.3±30.8 NFS-08-15 645 69.0 20.0±15.2 150 39.8±30.5 concentrations of 20:1, 16:1, and 20:3n-6. Summary 18241 102.5 18.1±11.9 403 40.3±28.4 Both PC2 and PC3 from the combined-year PCA were significant SSL SSL-07-01 396 278.0 32.5±47.8 197 59.7±65.7 predictors of foraging location (PC2: F1,48 =20.52, pb0.005; PC3: SSL-07-04 101 146.0 68.8±52.2 372 150.8±96.5 SSL-07-05 70 115.5 49.9±35.1 337 163.4±104.6 F1,48 =6.18, p=0.016) and trophic level (PC2: F1,48 =10.80, p=0.002; PC3: F =11.78, p=0.001) based on δ13C and δ15N levels SSL-08-01 1181 196.0 36.1±41.2 344 101.8±79.0 1,48 SSL-08-02 452 180.0 42.0±46.8 360 112.5±85.0 fi of vibrissae, respectively. PC3 from the 2007 PCA was a signi cant pre- SSL-08-05 2753 328.0 34.3±47.2 1280 97.9±83.9 dictor of trophic level (F1,29 =13.70, pb0.001), but none of the princi- SSL-08-11 603 152.0 30.1±36.8 352 110.1±88.4 ple components were significant predictors of foraging location. SSL-08-12 1720 280.0 36.0±37.3 400 103.8±74.7 Both PC1 and PC2 from the 2008 PCA were significant predictors of SSL-08-13 1751 304.0 39.7±41.8 480 96.4±71.1 SSL-08-14 2562 288.0 19.3±35.4 444 71.6±70.9 both trophic level (PC1: F1,17 =10.18, p=0.005; PC2: F1,17 =5.42, SSL-08-15 1547 296.0 42.5±51.1 344 105.9±82.6 p=0.032) and foraging location (PC1: F1,17 =20.47, pb0.005; PC2: SSL-08-17 1248 320.0 47.4±52.9 368 131.1±84.8 F1,17 =6.03, p=0.025). Summary 14374 328.0 43.1±43.6 1280 113.2±82.6 CART analysis of FA profiles of NFS and SSL from both 2007 and 2008 correctly classified 94.7% of the samples (38 of 41 NFS and 16 of 16 SSL). At the first branch, 68.8% of the SSL were separated from 303.4±72.4° (Table 6, Fig. 5). SSL made 488 bouts with a mean the remaining samples based on elevated levels of 20:5n-3. The distance and bearing from land of 4.0±4.2 km and 139.3±72.9°. remaining SSL samples, along with 7.3% (n=3) of the NFS samples, Bouts made by NFS were significantly further from land (F1,22 = were separated at the next branch based on elevated 14:0. Of these 75.45, p b0.001) and in a significantly different direction (Watson's SSL samples, 60% were the three samples taken in late July of 2008 by remote biopsy. The remaining two samples were collected in Table 5 June of 2007. The majority of NFS samples (92.7%) were all classified Summary of foraging trip durations and distances for northern fur seals (NFS) and Steller based on lower 20:5n-3 and 14:0 concentrations. sea lions (SSL) in 2007 and 2008.

Species ID Trips Max trip Mean trip Max trip Mean trip 3.3. Telemetry duration duration± distance distancE± (h) SD (h) (km) SD (km) During the period of TDR data collection, 14 NFS performed 25 925 fi b NFS NFS-07-03 14 124.2 34.9±43.4 282.7 89.0±110.8 dives and after ltering for erroneously long dives and dives 4m,18 NFS-07-04 15 128.5 29.5±46.5 366.2 74.2±129.7 241 dives remained for analysis. The mean dive depth and duration NFS-07-05 18 163.6 36.2±46.7 223.9 87.3±101.8 for NFS was 18.4±11.9 m and 40.3±28.4 s and the mean maximum NFS-07-24 1 121.6 121.6±0.0 360.5 360.5±0.0 dive depth was 73.7±16.7 m. Twelve SSL performed 14 754 dives, of NFS-07-25 1 118.5 118.5±0.0 341.0 341.0±0.0 NFS-07-27 1 92.7 92.7±0.0 165.4 254.2±0.0 which 14 384 were used for analysis. The mean dive depth and duration NFS-08-01 1 133.1 133.1±0.0 293.7 293.7±0.0 for SSL was 43.1±43.6 m and 113.2±82.6 s and the mean maximum NFS-08-02 2 103.7 94.7±12.9 239.3 217.1±31.4 dive depth was 240.3±76.5 m (Table 4). The mean dive depth for SSL NFS-08-07 3 82.1 59.6±38.5 245.8 172.0±107.6 NFS-08-09 3 103.4 78.8±32.4 283.5 201.2±101.0 was significantly deeper than that of NFS (F1,22=41.62, pb0.001) and the mean dive duration for SSL was significantly longer than that NFS-08-10 6 86.8 25.2±30.4 310.9 96.6±106.1 b NFS-08-13 3 137.5 77.7±67.9 267.2 154.2±135.4 of NFS (F1,22 =72.11, p 0.001). The mean maximum dive depth for NFS-08-14 2 131.8 80.1±73.3 269.0 165.4±146.4 SSL was significantly deeper than that of NFS (Welch's t11.9=7.39, NFS-08-15 4 88.7 26.3±41.8 171.9 55.3±80.8 pb0.001). SSL made the majority of their dive bouts in waters b150 m Summary 74 163.6 44.6±21.0 366.2 112.6±52.0 (cumulative percentages: 68.2% b50 m, 85.3% b100 m, 90.3% b150 m). SSL SSL-07-01 4 10.0 7.3 ±2.9 35.4 21.7±14.7 SSL-07-04 2 7.5 7.5 ±0.0 18.1 17.8±0.4 NFS made only 16.9% of their dive bouts in waters b150 m, while SSL-07-05 2 16.2 12.2±5.7 58.5 36.1±31.8 76.7% of bouts were made in waters >500 m depth. SSL-08-01 9 131.6 50.8±50.5 69.7 16.2±12.1 Seventy-four forging trips were made by NFS during the period of SSL-08-02 10 65.2 14.4±18.2 44.0 12.5±10.0 GPS data collection (Table 5, Fig. 4). The mean trip length and dura- SSL-08-05 37 53.2 13.4±12.4 82.8 17.9±17.8 tion made by NFS was 112.6±52.0 km and 44.6±21.0 h. SSL made SSL-08-11 17 69.2 23.2±22.4 46.9 17.1±13.8 SSL-08-12 26 32.1 9.4 ±7.7 31.2 10.5±7.4 211 foraging trips with a mean trip length and duration of 23.0± SSL-08-13 21 69.7 27.9±23.3 138.9 34.2±32.9 8.7 km and 18.5±12.0 h. Trips made by NFS were significantly longer SSL-08-14 23 96.1 18.8±23.1 78.9 22.7±20.9 in both distance (F1,22 =33.21, pb0.001) and duration (F1,22 =21.17, SSL-08-15 28 72.0 21.4±20.7 166.8 34.8±39.0 pb0.001) than those made by SSL. NFS made a total of 669 diving bouts SSL-08-17 32 58.2 15.3±14.1 51.7 16.1±12.7 with a mean distance and bearing from land of 46.4±10.0 km and Summary 211 131.6 18.5±12.0 166.8 23.0±8.7 Author's personal copy

48 J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54

Northern fur seals Steller sea lions −500 0 −50 −100 0 −500 Shiashkotan

−2000 −1000 0 Kharimkotan

−2000

0 0 −100

−100 Shiashkotan −100 −3000

−100 Lovushki −50 Lovushki −500

−50 −2000

−1000 Matua −100 −500 0 0 10 20 30 km −500 0 5 10 km 48.3°N 48.5 °N 48.7 °N 48.9 °N 48.0°N 48.5 °N 49.0 °N 49.5 °N 152.5 °E 153.0 °E 153.5 °E 154.0 °E 154. 5°E 153.5 °E 153.7 °E 153.9 °E 154.1 °E

Fig. 4. Plot of typical foraging trips made by northern fur seals (left panel) and Steller sea lions (right panel). Dashed box in left panel represents region illustrated in right panel. test of homogeneity, U=0.3719, pb0.01) than those made by SSL. terms of prey items consumed. Mean levels of δ13C suggest that the Both SSL (Watson's test of uniformity, U2 =4.48, pb0.01) and NFS SSL in this study foraged nearshore and benthically while the NFS (U2 =18.50, pb0.01) bout locations exhibited strong directionality fed offshore and pelagically, and mean levels of δ15N indicated that (Fig. 6). Bouts made by NFS in 2007 (298.0±82.0°) were in a signifi- adult female SSL on Lovushki Island fed at a higher trophic level cantly different direction from those made in 2008 (252.8±55.1°) than adult female NFS. Hobson et al. (1997) found similar results for (U=2.20, pb0.001). the δ15N levels of NFS and SSL samples collected in the Pribilof Islands and Gulf of Alaska, respectively. Hobson et al. (1997) also found no 4. Discussion significant difference in δ13C values; however, these values may be a result of the different geographical locations in which the samples 4.1. Resource partitioning were collected. Differences in the relative composition of FAs in the blubber indi- Stable isotope analysis indicated that adult female SSL and NFS cate that adult female NFS and SSL on Lovushki Island partitioned on Lovushki Island partitioned the forage resources spatially and in the forage resources through differences either in the prey species

Table 6 Summary of dive bouts and bout ending criteria (BEC) for northern fur seals (NFS) and Steller sea lions (SSL) in 2007 and 2008.

Species ID BEC (s) Total bouts % of dives occurring Mean dives Mean bout Mean distance from Mean bearing from in bouts per bout±SD duration±SD (mins) shore±SD (km) shore±SD (deg)

NFS NFS-07-03 65.6 101 70.1 27.4±34.2 17.5±17.1 47.3±25.1 309.9±39.2 NFS-07-04 101.1 88 73.9 24.7±28.1 16.6±16.9 85.0±44.1 333.6±55.3 NFS-07-05 71.7 148 64.3 21.9±26.8 16.8±17.0 41.8±24.3 308.3±36.5 NFS-07-24 97.9 15 77.1 25.4±19.8 40.0±39.9 42.8±5.0 277.7±15.5 NFS-07-25 50.3 19 75.7 36.4±44.9 39.3±39.2 55.1±20.9 281.8±13.5 NFS-07-27 53.4 16 78.8 28.0±39.2 39.9±4.0 58.8±8.8 297.4±28.8 NFS-08-01 67.2 27 75.4 25.0±23.9 26.7±26.5 62.8±21.8 277.9±10.9 NFS-08-02 53.5 31 78.8 47.5±55.1 41.8±41.8 50.3±20.0 274.5±6.6 NFS-08-07 42.3 35 64.1 28.5±36.7 16.1±15.9 34.9±18.9 303.1±34.9 NFS-08-09 50.9 58 62.2 25.2±31.9 23.4±23.6 24.3±12.2 133.3±45.7 NFS-08-10 64.0 25 53.4 21.4±27.0 19.7±19.5 23.7±15.0 314.8±62.5 NFS-08-13 44.4 50 70.7 27.6±30.4 22.5±22.6 31.6±21.2 326.6±64.3 NFS-08-14 58.0 38 75.7 32.7±95.5 17.2±17.3 46.0±20.9 252.0±22.2 NFS-08-15 68.9 18 76.8 33.1±64.1 31.4±31.4 17.8±12.7 175.1±34.8 Summary 669 69.6 27.8±25.2 21.5±20.7 46.4±10.0 303.4±72.4 SSL SSL-07-01 143.6 21 68.8 18.9±22.5 24.7±41.8 4.0 ±4.1 102.7±23.8 SSL-07-04 264.1 7 70.1 13.7±11.6 40.7±55.9 1.8 ±1.3 79.4±19.3 SSL-07-05 211.7 7 72.8 21.7±21.7 30.6±23.7 2.3 ±3.9 231±69.1 SSL-08-01 179.2 33 83.5 29.9±32.2 813.3±857.9 2.7 ±1.7 229.0±41.4 SSL-08-02 140.2 21 61.7 13.3±8.7 219.0±411.3 2.9 ±2.3 177.2±72.9 SSL-08-05 111.9 86 71.8 23.0±25.9 206.4±406.2 3.8 ±4.6 115.5±39.9 SSL-08-11 243.7 22 85.2 23.4±14.1 919.3±787.7 17.8±21.6 95.9±16.9 SSL-08-12 148.8 50 90.1 31.2±23.3 367.8±698.1 2.3 ±2.1 122.9±41.7 SSL-08-13 158.5 73 58.6 14.1±11.1 216.4±404.1 6.9 ±7.7 92.6±34.2 SSL-08-14 114.3 47 87.2 46.6±95.3 337.2±915.8 4.1 ±4.1 119.4±44.6 SSL-08-15 182.9 65 72.3 17.2±9.7 317.5±610.6 4.3 ±4.0 137.8±38.7 SSL-08-17 148.1 56 62.7 14.0±9.7 217.3±384.9 2.8 ±1.5 140.8±47.9 Summary 488 75.2 20.1±24.3 309.2±466.5 4.0 ±4.2 139.3±72.9 Author's personal copy

J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54 49

Northern fur seals Steller sea lions and northern fur seals −500 0 −50 −100 0 −500 Shiashkotan

−2000 −1000 0 Kharimkotan

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0 0 −100

−100 Shiashkotan −100 −3000

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−1000 Matua −100 −500 0 0 10 20 30 km −500 0 5 10 km 48.0 °N 48.5 °N 49.0 °N 49.5 °N 48.3 °N 48.5 °N 48.7°N 48.9°N 152.5 °E 153.0 °E 153.5 °E 154.0 °E 154.5 °E 153.5 °E 153.7 °E 153.9 °E 154.1 °E

Fig. 5. Locations of typical foraging bouts made by northern fur seals (left and right panel, solid triangles) and Steller sea lions (right panel, open circles). Dashed box in left panel represents region illustrated in right panel. selected or in the proportion of different prey items consumed. The technique, storage methods, storage time, FA extraction and analysis FA composition of the blubber of both species was significantly differ- methods, or temporal differences in prey consumption. The use of ent between years, which may be the result of differences in sampling multiple labs for the analysis of FA samples is not recommended

Fig. 6. Rose diagrams of northern fur seal (top) and Steller sea lion (bottom) bout location bearings from Lovushki Island in 2007 and 2008. Area of each sector is proportional to the frequency. Author's personal copy

50 J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54 due to differences in extraction and analysis methods, equipment, (06:00 to 18:00) than SSL (4.8% and 17.2% of dive bouts, respectively), and personnel, possibly making the different datasets incomparable presumably because their prey has migrated to deeper, inaccessible to one another. However, despite the significant between-year differ- depths during the day. ences represented by the first PC in the combined-years PCA, the The 7.8 h median SSL trip duration in 2007 was similar to the 7.5 h same general pattern of resource partitioning represented by the median trip duration estimated through visual observations reported second PC was exhibited for both years. in Burkanov et al. (2011); however, the median SSL trip duration in Telemetry data indicated that adult female SSL and NFS foraged in 2008 was slightly longer (10.3 h). SSL in 2007 and 2008 were tracked significantly different locations. SSL focused most of their foraging an average of 9.6±2.2 and 35.9±8.4 days, respectively. In 2008, effort in the shallow waters within 4.0 km of the rookery (Fig. 4). 77.8% of SSL were tracked beyond the 30 days recorded by visual obser- Almost 70% of dive bouts occurred in waters b50 m depth (Fig. 5) vations in previous years, suggesting that an increase in trip duration and the average dive depth of 43.1 m suggests that SSL primarily may occur later in the season. However, the 2.5 h increase in median foraged benthically. The top panels of Fig. 7 show a series of flat- trip duration is within the range of the interannual variation reported bottomed dives of increasing depth, indicative of benthic foraging for other rookeries in the Russian Far East (Burkanov et al., 2011). (Gales and Mattlin, 1997; Hindell et al., 1991; Le Boeuf et al., 1992; Merrick and Loughlin, 1997; Thompson et al., 1998) as the sea lion 4.2. Convergence of results moved farther away from the rookery into deeper water. In contrast, NFS traveled much greater distances, foraging an average of 46.4 km Each of the three methodologies used in this study have inherent from the rookery (Fig. 4) in the waters of the northern Kuril Basin. limitations that, when used on their own, prevent the determination While the average dive depth of NFS was 18.1 m, the majority of of dietary compositions with respect to the specific prey items and dive bouts took place in water depths of >500 m (Fig. 5), indicating quantities consumed. For example, while there is no effect on 13C en- that the NFS foraged pelagically. The lower panels of Fig. 7 show a richment in animal tissues (Hobson et al., 1993; Kempster et al., series of shallow dives that exhibit a substantial amount of wiggle 2007; Teeri and Schoeller, 1979), the interpretation of δ15N values during the bottom phase of the dive, indicative of pelagic foraging can be affected by the physiological state of an animal, including nu- (Bengtson and Stewart, 1992; Gentry et al., 1986; Schreer and Testa, tritional stress due to fasting, pregnancy, or lactation (Fuller et al., 1996). 2004; Kurle and Worthy, 2001). During the breeding season, adult fe- NFS foraged primarily nocturnally and focused their foraging male SSL and NFS with dependent pups undergo episodic fasts while effort within a narrow window of time centered on midnight; 92.8% nursing and hence may be under some degree of nutritional stress, (n=621) of dive bouts occurred between the hours of 20:00 and which limits us to making only general inferences on the specific 04:00. This behavior is consistent with that of other fur seal species diet of SSL and NFS based on nitrogen SI data. Similarly, specific pred- feeding on pelagic vertically migrating prey items (Bengtson and ator diets generally cannot be determined based solely on the relative Stewart, 1997; Georges et al., 2000; Goebel et al., 1991; Trillmich concentration of FAs. However, fish and cephalopods have a species- et al., 1986). SSL also foraged primarily nocturnally, but substantial specific combination of FAs, and while within-species variation exists foraging effort began much earlier in the afternoon; 17.2% (n=83) due to differences in geographical location, age, size, and time of year, of dive bouts occurred between the hours of 14:00 and 20:00, and this variation is typically less than the between-species variation 71.7% (n=345) of dive bouts occurred between the hours of 20:00 (Budge et al., 2002; Iverson et al., 2002). Thus, while a reference and 04:00. Additionally, NFS foraged much less during the day library of prey FAs specific to this particular study location is not

Steller sea lion 0 0

−20 −20

−40 −40

Depth (m) −60 −60 −80 −80 23:14:17 23:30:56 23:47:36 00:04:16 23:46:59 23:53:38 Northern fur seal 0 0

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−40 −10

Depth (m) −60 −15

−80 −20

10:55:31 11:12:10 11:28:50 11:45:30 10:55:31 10:58:00 Time (hh:mm:ss) Time (hh:mm:ss)

Fig. 7. Time-depth trace of typical Steller sea lion (upper panel) and northern fur seal (lower panel) dives on Lovushki Island in 2007 and 2008. Left panels represent 1 h. Right panels represent the 3 individual dives highlighted by the grey boxes. Author's personal copy

J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54 51 currently available, qualitative inferences may be made based on dif- NFS between 2007 and 2008 (Waite et al., 2012), which may explain ferences in the FA profile of prey types collected in other geographic the different isotopic values found in this study and further support regions within a similar period. In addition, while time-depth re- the convergence of the stable isotope and scat data. corders and GPS receivers can give fine-scale data on predator move- A common theme in the PCA and CART analyses of FA was the sep- ment and dive patterns, these methods provide no direct means of aration of species based on levels of 20:5n-3, which was significantly determining specific prey items consumed. Despite the limitations higher in SSL samples than in NFS samples. Although 20:5n-3 tends to each of these methods, inferences of specific dietary compositions occur at relatively high concentrations in most fish and squid species, can be made when the results of all three techniques are examined northern smoothtongue has relatively lower amounts (S. Iverson, simultaneously in conjunction with data on trophic position, geo- pers. comm.), while hexagrammids have increased concentrations graphic distribution, preferred habitat, and foraging strategies of (Iverson et al., 2002). Squid were the second most common NFS potential prey items. These inferences can be corroborated using prey item identified in scats and spews (Waite et al., 2012) and can results from previously published results diets estimated from concur- vary greatly in levels of 18:1n-9, ranging from 3.32 to 13.96% rently collected scats and spews. (Iverson et al., 2002; Stowasser et al., 2006), with most species having Atka mackerel (Pleurogrammus monopterygius), the primary relatively high levels of 20:5n3 (Iverson et al., 2002). NFS samples summer prey of SSL on Lovushki Island (Waite et al., 2012), sampled contained low levels of 18:1n-9; however, the low levels of 20:5n-3 in the Russian Far East have an estimated trophic level of 3.3–3.9 contrast with the FA composition of most squid species. Squid species (Brodeur and Livingston, 1988; Onishchick, 1997; Zolotov and tend to have relatively low lipid content and it is unclear how much Tokranov, 1991). In contrast, the primary prey of breeding NFS on their FA profile would affect the FA composition of NFS blubber Lovushki Island, based on numerical dominance (Waite et al., 2012), in comparison to northern smoothtongue, which has substantially have relatively lower estimated trophic levels: northern smoothtongue higher lipid content. Although scat data indicated an increase in (Leuroglossus schmidti) from the Bering Sea have an estimated trophic squid consumption and a concurrent decrease in northern smooth- level of 3.1–3.2 (Balanov et al., 1994; Gorbatenko and Il'inskii, 1992) tongue consumption by NFS between 2007 and 2008, NFS FA profiles and Gonatid squids (Gonatopsis sp) range from 3.2 to 3.4 (Gorbatenko showed a significant decrease in the levels of 20:5n-3 between 2007 et al., 2008; Pauly et al., 1998). Using published data on stomach and 2008 (ANOVA with Tukey–Kramer post-hoc test, t53=2.66, contents, Pauly et al. (1998) estimated the trophic position of both p=0.049)aswellasasignificant increase in 18:1n-9 (t53 =7.55, NFS and SSL as 4.2. However, based on the diet estimates derived pb0.001), which is not necessarily consistent with what would be from scat data (Waite et al., 2012) and the trophic positions of the expected based on the relative concentration of these two FAs in these prey, it would be expected for breeding female SSL on Lovushki Island prey. However, FA profiles of blubber from lactating female pinnipeds to be at a higher trophic level than breeding female NFS. This expecta- may also be affected by the selective mobilization of certain fatty acids tion was confirmed by the higher mean δ15N levels of the vibrissal from the blubber store for milk synthesis (Trumble et al., 2010; roots from SSL examined in this study. Wheatley et al., 2008). The milk of gray seals (Halichoerus grypus, Similarly, foraging location inferred from mean δ13C levels of Grahl-Nielsen et al., 2000) and hooded seals (Cystophora cristata, vibrissal roots was corroborated by the distribution and habitat of Iverson et al., 1995)issignificantly enriched in most of the polyunsatu- prey items identified from scats and spews (Waite et al., 2012). rated n-3 FAs (such as 20:5n-3) and depleted in monounsaturated FAs During the summer spawning season, Atka mackerel are demersal with 18 carbon atoms (such as 18:1n-9). Iverson et al. (1995) also and spawn in nearshore waters at depths from the inter-tidal zone found that the milk of hooded seals contained consistently higher levels to 200 m (Gorbunova, 1962; McDermott and Lowe, 1997). Northern of 20:5n-3 than blubber. Therefore, the observed decrease in 20:5n-3 smoothtongue and accessible squid species are mid-water shelf and and increase in 18:1n-9 between 2007 and 2008 in NFS blubber mesopelagic prey items, usually located farther offshore, and thus samples may be consistent with an increase in squid consumption. would generally be expected to have relatively lower δ13C levels com- As with SI data, without a reference library specific to the prey pared to Atka mackerel. items in this particular region, the FA data may be best used to Mean δ15N and δ13C values for Atka mackerel collected from near- make inferences on trophic level and foraging location rather than by waters (n=2) was 12.4±0.1‰ and −20.3±0.1‰, respectively, to determine the specific prey species consumed. While PC1 from for lipid-free tissue and 10.3±0.7‰ and −21.4±0.2‰, respectively, the combined-years PCA primarily separated samples by year, PC2 for squid beaks (n=3) recovered from NFS stomachs (J. Waite, and PC3 were both significantly correlated with δ13C and δ15N levels unpub. data). Cherel and Hobson (2005) found that the lower beaks of vibrissae. For example, PC2 represents a gradient from nearshore of Antarctic squid (Psychroteuthis glacialis) were enriched in δ13Cby and benthic foraging to offshore and pelagic foraging and from higher 1.4±0.5‰ (SD) and impoverished in δ15N by 2.7±0.4‰ compared to lower trophic level feeding. to the buccal masses. The application of these correction factors to The prey items that would be encountered based on the foraging our Gonatid squid beaks results in estimated δ15N and δ13C values behavior of SSL, as determined through satellite telemetry, fits our for tissue of approximately 13.0‰ and −22.1‰, respectively. The expectations based upon estimates of diet composition and foraging lower δ13C values of the squid compared to the Atka mackerel coin- location through the analysis of scats, SI, and FA. Lovushki is situated cide with both the expected habitats of these prey items as well as on a narrow, shallow shelf that extends approximately 40 km south- the lower δ13C values of the NFS vibrissal roots compared to SSL. west from the southern tip of Shiashkotan Island (48.7° N 154.0° E). The δ15N values of both prey items are comparable, which possibly Sea floor depths >200 m occur within 7–8 km of Lovushki, resulting reflects the overlap in their estimated trophic position. There are no in a relatively small region with suitable bathymetry for spawning published data on the stable isotope ratios of northern smoothtongue Atka mackerel, thus concentrating this prey species within a short from nearby waters, but based on their estimated trophic position distance from the rookery. SSL made far fewer foraging bouts north- and mesopelagic habitat, we would expect δ13C values similar to west of the rookery where bottom depths >200 m occur in as little squid and δ15N values lower than both Atka mackerel and squid. as 3 km, and instead, concentrated their foraging effort where water Both would coincide with the lower δ13C and δ15N levels found in depths increased less rapidly. As well as diving deeper than NFS, SSL the vibrissal roots of breeding NFS. also dove for longer durations. Atka mackerel often hide amongst During this study, we observed a significant increase in δ15N levels the rocks and kelp during the spawning season (Gorbunova, 1962), in breeding NFS from 2007 to 2008. Scat and spew data indicated which may increase the amount of time required to be located and an increase in the consumption of cephalopods and a concurrent captured by predators (Bowen et al., 2002), thus increasing dive decrease in the consumption of northern smoothtongue by breeding duration and bottom times. Author's personal copy

52 J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54

The prey types that would be encountered based on the movement at least after day 5 (Arnould et al., 2001). Optimal patch choice is of NFS also fit our expectations based on the results obtained using partly decided by the extent of competition for prey within a given other techniques. Gonatid squid (Gonatopsis sp.) are characterized area (Pyke et al., 1977) and in response to reduced prey availability, by distinct diurnal migrations to the epipelagic zone at night (Nesis, such as might occur when competition for prey resources is high. 1989). Trawl studies conducted in the Sea of Okhotsk in 1989–1993 Therefore, the adult female NFS in this study may have increased found that G. borealis made up approximately 97% (43.0–77.3 thou- their trip duration and distance to exploit richer prey sources in sand tons) of the squid biomass that migrated to the epipelagic zone order to reduce inter-specific competition with the larger SSL while at night (Lapko, 1996). Off northern Japan, G. borealis is found at staying within the fasting abilities of their dependent pups. depths of 500–700 m during the day where the temperatures are typ- ically 3–5 °C and migrate to the epipelagic layers at night, where the 5. Conclusions water temperature rapidly increases to 5–10 °C beginning at 100 m (Watanabe et al., 2006). A similar temperature profile, albeit colder, Analysis of stable nitrogen and carbon isotopes in vibrissal roots, can be found in the waters where the NFS in the present study concen- fatty acids in blubber, and dive behavior and movement data indi- trated their foraging efforts. During the summer, an influx of warm cated that breeding female SSL and NFS on Lovushki Island partition water from the Sea of Japan causes two anticyclonic eddies to form foraging resources both by prey species and foraging location. These in the southern Sea of Okhotsk (Wakatsuchi and Martin, 1991). The findings are corroborated by data from concurrently collected scat upper 100 m of these eddies are characterized by water that is warmer and spews. Although the exact dietary composition cannot be directly and more saline, while the lower layers are characterized by water determined using the resultant data, biochemical analyses have several that is colder and less saline, compared to the surrounding waters of advantages over the analysis of scats and spews and are complementa- the Kuril Basin. In July, water temperatures in the upper 100 m reach ry. Since SI in vibrissal roots and FA in blubber are integrated over a almost 8 °C and quickly drop to 1–2 °C below 100 m. The strongest period of weeks to months, they provide dietary information that of these eddies has a diameter of 100–200 km and usually forms covers a greater period than a single scat collection effort. Therefore, approximately 240 km to the west of Lovushki Island. Thus, with events such as short-term influxes of a particular prey species, although foraging bouts occurring at a mean distance of 41.9 km from shore, it often important, are less likely to bias estimates of diet composition is likely that the NFS in this study foraged at the edge of this eddy to over longer time periods. Of the three methods, SI analysis is generally exploit abundant aggregations of squid. This hypothesis could be less costly and complicated and the samples are easier and less invasive explored by comparing foraging trip locations with spatial patterns to obtain. This study did not find a significant difference in stable of remotely-sensed oceanographic features, such as sea surface tem- isotope levels between live and dead animals, further expanding the perature, sea surface height, or chlorophyll-a concentration (Fossette opportunity to collect samples in a non-invasive manner. et al., 2010; Johnston et al., 2005; Lea, 2003; Ream et al., 2005). The clear spatial partitioning of the foraging grounds, based on the Northern smoothtongue are located at depths of 200–1000 m directionality and distance from shore of adult female dive bout loca- during the day but migrate to 0–200 m at night (Sobolevskii and tions, allows both species to coexist within the same geographical re- Sokolovskaya, 1994; Sobolevskii et al., 1996). Furthermore, northern gion despite an increase in the population of both predator species. smoothtongue have the highest biomass of any mesopelagic fish in This partitioning of geographic space likely reflects the differences the Sea of Okhotsk (Il'inskii and Gorbatenko, 1994) and annually con- in foraging abilities of the adults, the fasting abilities of their pups, sume 2 million tons of larval and small squid (Lapko, 1996). Thus, a and the local bathymetric and oceanographic conditions. However, strong correlation between the distribution of squid and northern no information is currently available regarding the foraging location smoothtongue would be expected, and NFS foraging on squid would of non-breeding NFS. There was a significant overlap between the likely take advantage of the presence of an abundant prey item with diets of breeding SSL and non-breeding NFS (Waite et al., 2012), a higher energy density. This is reflected in the strong correlation and as NFS outnumber the SSL by an order of magnitude, there is sub- in the occurrence of these two prey items in NFS scats and spews stantial potential for inter-specific competition for dietary resources collected on Lovushki (Waite et al., 2012). between these two groups, especially if there is a significant overlap Choice in foraging location may be influenced by the fasting ability in foraging range. Further, the occurrence of an ecological perturba- of dependent pups as changes in foraging location may affect the tion influencing the existing prey resources for either species could length of time a pup must fast while the female is foraging. SSL also substantially increase the potential for inter-specific competition. pups show a rapid metabolic adaptation to fasting with an increased reliance on lipid catabolism within 16 h of the onset of a fast but Acknowledgements begin to lose lean body tissue after reverting to protein catabolism after approximately 2.5 days of fasting (Rea et al., 2000). Traveling We thank A. Altukhov, S. Norberg, P. Permyakov , T. Shulezhko, J. – at a speed of 1.7–2.1 m s 1, the speed at which the minimal cost of Skinner, B. Smith, and A. Tretyakov, as well as many others from the transport has been estimated to occur for SSL (Hindle et al., 2010; Russian Far East Marine Mammals Research Program and the Alaska Rosen and Trites, 2002), it would take 38–47 h to travel the 80 km SeaLife Center for their assistance in the collection of samples. We to the edge of the seasonal Kuril Basin eddy and back to the rookery. thank P. Rivera for her invaluable assistance in the processing of Therefore, it is unlikely that adult female SSL would be able to make vibrissae samples, as well as K. Young and S. Quinn for processing this trip to take advantage of the abundant, high-energy northern blubber samples and assisting in fatty acid profile determination. We smoothtongue before their pups began to lose significant body also thank M. Short and J. McIntyre for their statistical advice, as well mass. The mean SSL foraging trip duration of SSL of approximately as M. Castellini, L. Rea, and S. Atkinson for their helpful comments on half a day and mean distance between the rookery and foraging loca- this manuscript. Fatty acid analysis was supported in part through tions of only 3.1 km likely reflects a balance between acquiring larger NOAA funding (NA08NMF4390544) to ADF&G. Research was con- amounts of an abundant, but lower energy density prey item such ducted under permits from Russian permitting agencies, the Federal as Atka mackerel, reducing the cost of transport associated with Veterinary and Agricultural Control Service (Rosselkhoznadzor, extended foraging trips, and reducing their trip durations to within Sakhalin Region), Sakhalin-Kuril Territorial Department of the Federal the fasting limits of their young. While data on the fasting capability Committee of Fisheries of Russia (Goskomrybolovstvo) and the Federal of NFS pups have not been published to date, Antarctic fur seal Environmental Control Service (Rosprirodnadzor) of the Ministry of (Arctocephalus gazelle) pups begin to spare protein within 2–3 days Natural Resources of Russia, was approved by the Institutional Animal after the onset of a fast and do not revert to protein catabolism until Care and Use Committee of the Alaska SeaLife Center, and was funded Author's personal copy

J.N. Waite et al. / Journal of Experimental Marine Biology and Ecology 416-417 (2012) 41–54 53 by grants from NOAA to the Alaska SeaLife Center and the National Gales, N.J., Cheal, A.J., 1992. Estimating diet composition of the Australian sea lion (Neophoca cinerea) from scat analysis: an unreliable technique. Wildl. Res. 19, Marine Mammal Laboratory. Additional funding and logistical support 447–456. was provided by North Pacific Wildlife Consulting. [SS] Gales, N.J., Mattlin, R.H., 1997. Summer diving behaviour of lactating New Zealand sea lions, Phocarctos hookeri. Can. J. Zool. 75, 1695–1706. Gentry, R.L., 2002. Northern fur seals. In: Perrin, W.F., Würsig, B., Thewissen, J.G.M. (Eds.), Encyclopedia of Marine Mammals. Academic Press, San Diego, CA, pp. 813–817. References Gentry, R.L., Costa, D.P., Croxall, J.P., David, J.H.M., Davis, R.W., Kooyman, G.L., Majluf, P., McCann, T.S., Trillmich, F., 1986. Synthesis and Conclusions. In Fur Seals: Maternal Arim, M., Naya, D.E., 2003. 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