Looking at the unseen: combining animal bio-logging andstable isotopes to reveal a shift in the ecological niche ofa deep diving predator

Frederic Bailleul, Matthieu Authier, Simon Ducatez, Fabien Roquet, Jean-Benoıt Charrassin,Yves Cherel and Christophe Guinet

F. Bailleul (Frederic.Bailleul@dfo-mpo.gc.ca), M. Authier, S. Ducatez, Y. Cherel and C. Guinet, Centre d’Etudes Biologiques de Chize,UPR 1934 du Centre National de la Recherche Scientifique, FR-79360 Villiers en Bois, France. (Present address of F. B.: Ecology and Biologyof Marine Mammals, Maurice Lamontague Inst., 850 route de la Mer, PO Box 1000 Mont-Joli, QC, Canada, G5H 3Z4.) � F. Roquet andJ.-B. Charrassin, Unite Scientifique du Museum 402/Laboratoire d’Oceanographie et du Climat: Experimentation et Approches Numeriques,Dept Milieux et Peuplements Aquatiques, Museum National d’Histoire Naturelle, 43 rue Cuvier, FR-75231 Paris Cedex 05, France.

Understanding how marine top predators exploit their environment is a central topic in marine ecology. Among allmethodologies used to investigate this part of ecology, electronic devices are very useful to track animals’ movements andforaging habitats, but they do not provide any dietary information. Stable isotopes provide information on trophic levelsbut remain imprecise to identify small spatial-scale habitats. In this study, we combined the two approaches to obtain asynoptic view of the foraging behaviour variability of southern elephant seals Mirounga leonina. Our results suggestedmarked differences in distribution, diving behaviour, foraging habitats, trophic levels, and dietary habits of elephant sealsaccording to their sex and age. Thus, we characterized main foraging habitats over the Kerguelen-Heard Plateau andthe Antarctic shelf for juvenile males, while females foraged mainly in oceanic waters of the Polar Frontal Zone and theAntarctic Zone. In addition, we highlighted the ontogeny of niche partitioning in this sexually dimorphic species. Whilefemales did not exhibit a major dietary shift in relation to their age and their breeding status, a different picture emergedfor males. Young males had a trophic level identical to that of all females. However, at 3�4 yr of age, males showeda progressive increase in trophic level. The inter-annual combination of bio-logging and stable isotopes could providea powerful tool to investigate possible shifts in ecological niche between years according to environmental changes.

A better understanding of foraging behaviour of toppredators should contribute to resolve a number ofimportant ecological issues, such as the distribution andavailability of resources along with their spatial andtemporal variability. In addition, it can provide insightsinto partitioning processes within the ecological niche of agiven species since intra-specific competition according toage, sex, or size has been identified as a major component ofthe species niche width (Schoener 1989). In many species,adult males and females differ considerably in body size andshape (Darwin 1871) which can result in individuals ofdifferent sexes having different ecological niches, such as thecarpet python Morelia spilota imbricata for which extremesex-based niche divergence has been reported (Pearson et al.2002). Few studies, however, address the ontogeny of nichepartitioning in sexually dimorphic species. Moreover,studies on niche partitioning remain difficult in practice,particularly in the oceanic environment.

Since the 1980s, the development of miniaturizedarchival data loggers and satellite transmitters have enabledbiologists to understand much about the pelagic behaviour

of marine top predators (Ropert-Coudert and Wilson2005). Recently, new technologies have been developed torecord not only the behaviour of marine predators, but alsoto describe the ambient environment through which theymove (Fedak 2004, Biuw et al. 2007). Marine predators cantherefore be used to monitor and measure changes inoceanographic conditions, induced for instance by globalwarming. Marine top predators provide numerous researchopportunities for scientists. Firstly, many species exhibit aterrestrial phase during their annual cycle (e.g. for breedingor moulting) during which they can be captured andequipped with electronic devices. Secondly, their foragingbehaviour reflects the patchiness of oceanic biologicalproduction, a pattern generally associated with disconti-nuities in physical properties (e.g. temperature and salinity)(Pinaud and Weimerskirch 2005), thereby providinginformation on the spatial and temporal heterogeneity ofthe marine environment. Hence, coupling marine ecologyand oceanography substantially increases our knowledge ofbiophysical interactions and our understanding of marineecological patterns and processes. However, the use of

Ecography 33: 709�719, 2010

doi: 10.1111/j.1600-0587.2009.06034.x

# 2010 The Authors. Journal compilation # 2010 Ecography

Subject Editor: Donglas A. Kelt. Accepted 14 September 2009

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electronic devices remains costly, provides no informationon the diet of these marine predators, and needs to becomplemented with other techniques.

Over the past 15 yr, stable isotope analysis has emergedas a powerful and complementary approach for recon-structing diet and large-scale movement on a large numberof individuals when direct observations are not possible(Rubenstein and Hobson 2004). Ratios of nitrogen(15N/14N, as d15N) and carbon (13C/12C, d13C) are themost commonly used. Nitrogen in the protein ofconsumers is typically enriched in 15N relative to dietarynitrogen; consequently, d15N serves as indicator of con-sumer trophic position (Vanderklift and Ponsard 2003).By contrast, d13C is roughly constant along the food chainand is mainly used to determine primary sources in atrophic network and to indicate inshore vs offshore, orpelagic vs benthic contribution to food intake (Hobsonet al. 1994, Cherel and Hobson 2007, Cherel et al. 2007).Previous studies have found a clear geographical d13Cgradient in particulate organic matter (POM) in thesouthern hemisphere. Characteristically, high d13C valuesare located in warm subtropical waters in the north, whilelow values are located in cold Antarctic waters in thesouth (Trull and Armand 2001). By this technique,distribution and trophic levels of numerous subantarcticand Antarctic predators have been identified (Quillfeldtet al. 2005, Cherel and Hobson 2007). Here we combinebio-logging with stable isotopes to assess the foragingecology of a mammalian top predator, the southern ele-phant seal Mirounga leonina.

Southern elephant seals undertake extensive post-moultingmigrations to search for prey throughout the SouthernOcean (Gales and Burton 1989, Bornemann et al. 2000),the different populations forming a circumpolar distribu-tion (Biuw et al. 2007). These animals are known to makecontinuous, deep dives throughout their foraging route(Hindell et al. 1991a), with up to 90% of their pelagiclife (ca 8�10 months yr�1) spent diving. They generallydive to 500 m, although some individuals regularly reach1500 m and exceptionally to 2000 m (Campagna et al.1999). Dives average 20�30 min, allowing 50 to 70 divesper day (McConnell et al. 1992). Moreover, elephant sealsregularly perform what is believed to be resting or foodprocessing dives during which they spend extended perioddrifting passively in the water column (Webb et al. 1998,Biuw et al. 2003). The rate of vertical change in depthduring these ‘‘drift’’ dives largely reflect the body conditionof seals (Webb et al. 1998). Indeed, non-fasting individualstend to become more buoyant and consequently increasetheir vertical drift rates compared to fasting individuals.Thus, over a given time period, changes in drift rate valuesprovide an index of foraging success (Biuw et al. 2003,2007, Bailleul et al. 2007a). Adult elephant seals alsoexhibit substantial sexual size dimorphism, with maleson average five to six times larger than females. Based onsize alone, a 2500 kg male has a daily energy requirementthree times that of a 500 kg female (Boyd et al. 1994).This probably explains the sexual segregation observed inadult foraging areas; adult males forage more over or alongthe edge of continental shelves, while adult females mainly

target pelagic waters (Hindell et al. 1991b, Campagnaet al. 2007). The combined characteristics of wide-rangingmovements and frequent deep dives make elephantseals ideal platforms for the deployment of oceanographicsensors to characterize their foraging environment and togather physical oceanographic measurements (Campagnaet al. 2000, Charrassin et al. 2008).

This study provides the first synoptic view of theforaging behaviour variability of a southern elephant sealpopulation over a 4-yr period in relation to oceanogra-phic features, age, and sex. Previous studies conductedon Macquarie Island revealed spatio-temporal segregationaccording to age, with younger elephant seals remainingcloser to the island and spending more time at lowerlatitudes than older seals (Field et al. 2007a). Furthermore,age-related diet differences, both in prey species composi-tion and size, due to a progressive change in diving abilityand haul-out pattern, were interpreted as a means toreduce intraspecific food competition in this population(Field et al. 2007b).

The aim of this study was thus two-fold: 1) tocharacterize, from an oceanographic point of view, theforaging habitats of male and female elephant seals usingtemperature and salinity data obtained from loggers dep-loyed on individuals of varying size; and 2) to combinethese results with those obtained from stable isotope mea-surements of blood, to investigate the ontogeny of spatialand dietary niche partitioning according to sex and age ofsouthern elephant seals of the Kerguelen Island population.

Material and methods

Seal capture and blood sampling

From 2003 to 2007, male and female elephant seals froma broad range of mass and size were captured at theKerguelen Islands (49820?S, 70820?E) using a canvas head-bag. All seals were measured from nose to tail to thenearest cm and a blood sample was taken from extraduralintravertebral vein after foraging trips. As body lengthreflects age (Le Boeuf and Laws 1994, Bell et al. 2005),we used variability into this measurement to contrastyounger and older individuals. Blood was sampled,centrifuged, and stored frozen until analysis, from everyelephant seal equipped with data loggers (see below) insummer (December�March). In addition, 10 seals weresampled each month from autumn to early winter 2006(April�August). Females included both juvenile and adultanimals, whereas all males were juveniles.

Deployment of devices

Forty-six southern elephant seals (24 adult females and22 juvenile males) were equipped with Argos SatelliteRelayed Data Loggers; 43 (24 females and 19 males) wereequipped with Conductivity Temperature Depth sensors(CTD-SRDLs) and three (all males) with TemperatureDepth only sensors (TD-SRDLs). All the adult females and18 juvenile males were equipped between November and

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March, before their departure for the post-moult foragingtrip. The four remaining juvenile males were equipped inSeptember, during a brief winter visit on land. Seven sealsfor which recording duration was too short (B33 d) wereremoved from analyses and, consequently, the followingresults were computed for 18 post-moult females and 21post-moult immature males. We selected males and femalesof similar size to reduce effects of size on behaviouraldifferences between the sexes.

Seals were anesthetized using a 1:1 combination ofTiletamine and Zolazepam (Zoletil 100) which was injec-ted intra-venously (McMahon et al. 2000, Field et al.2002), and were subsequently weighed to the nearestkg (Le Boeuf et al. 2000). Then, data loggers were gluedto the head of the seals, using quick-setting epoxy(Araldite AW 2101), after cleaning the hair with acetone(Hindell et al. 1999). Devices (105�70�40 mm, 545 g,and cross-sectional area 28 cm2) were designed and manu-factured by the Sea Mammal Research Unit (SMRU), Univ.of St Andrews, to collect and transmit locations, pressure,temperature, and conductivity. Temperature and conduc-tivity were measured with an accuracy of 90.0058C and90.01 mS cm�1, respectively. Housings of the deviceswere pressure-rated to 2000 m (accuracy�2 m). Datawere sampled every 2 s but the Argos data system did notenable all records to be transmitted; to compensate for this,we applied a pseudo-random method to schedule thetransmission of an unbiased data sample of the storedrecords (Fedak 2004). This new generation of loggertransmits the collected information by satellite almost inreal time and allows us to relate animal’s pelagic behaviourwith the ambient oceanic environment.

Seal locations

Locations were determined during satellite uplinks by theArgos system. The accuracy of locations provided by Argoswas provided in several categories: class 3 was accurate to150 m, class 2 to 350 m, class 1 to 1 km, class 0 over to1 km, and classes A, B, and Z had no accuracy assigned.Unrealistic locations were rejected using a forward/back-ward averaging filter (McConnell et al. 1992) based on theassumption that seals rarely travel at speeds �3 m s�1.Tracks in this study are based on an average of 441591623 points. This corresponds to 10�20 Argos locations peranimal per day. The path is based on a simple time-basedlinear interpolation between selected locations.

Diving behaviour and seal body condition

Each surface tracking location is associated with divingparameters, such as dive duration, maximum dive depth, orpost-dive interval. On any dive, a seal was assumed to be atthe bottom of the dive whenever depth exceeded 80% of themaximum depth reading (Lesage et al. 1999, Schreer et al.2001). Using a dive classification method we identified sixdifferent categories (Hindell et al. 1991a, Bailleul et al.2007b). Here, we were only interested in benthic dives(square-shaped dives observed on the seafloor) usually

characterizing a foraging activity, and drift dives. Fromthe time-depth profiles of drift dives, we identified theputative drift segment by fitting the best regression linethrough the inflection points (Fig. 1 in Biuw et al. 2003).The slope coefficient (positive or negative) of this linecorresponded to the drift rate (m s�1). The rate of verticalchange in depth during these ‘‘drift’’ dives is largely a resultof the body condition. While lean tissue is denser thanseawater, lipid tissue is less dense and animals with a largeproportion of lipid will therefore be more buoyant (Webbet al. 1998). Thus, fatter seals show positive drift rates(i.e. positive drift dive), while leaner seals show negativedrift rates (i.e. negative drift dive). Only dives for which thedepth of the shallowest inflection point was at least 10 mand for which the drift phase represented �40% of thetotal duration were used (Biuw et al. 2003). The dailyaverage of drift rate was calculated. Then, the slopecoefficients of each fitting regression (drift rates vs time)drawn over three successive days, were observed. Positiveslopes indicate that foraging searching activity was success-ful over this period. Furthermore, and as proposed byBailleul et al. (2007a), we mapped these results onto a0.58 grid to obtain spatially explicit indications of changesin the seals’ body condition (Crocker et al. 1997, Biuwet al. 2003). The overlap between areas where elephant sealsboth improved their body condition, and were found tospend more time than expected at the bottom of their divesfor a given diving depth (Bailleul et al. 2008), provided aspatial index of foraging success.

Temperature and salinity profiles

The Southern Ocean fronts are narrow regions of sharphorizontal gradients of water properties that mark theboundaries of different water masses (Fig. 1a). Thesestructures are defined by representative values of tempera-ture and salinity at 200 m depth where each frontgenerally is best marked (Park et al. 1998). Over theAntarctic continental shelf, water characteristics are com-pletely different (i.e. clearly below zero 8C) from thosefurther offshore. Going north from the Antarctic con-tinent, the Antarctic Slope Front (ASF) has been identifiedwith the most shoreward penetration of the 08C isothermat depths below the Winter Water (Ainley and Jacobs1981). The Southern Antarctic Circumpolar CurrentFront (SACCF) is defined by a temperature of 1.58Cand a salinity of ca 34.6 psu at 200 m depth (Park et al.1998). The Polar Front (PF) is approximated by thenorthern limit of the subsurface temperature minimum of28C at the 100�300 m depth layer (Park et al. 1993,Belkin and Gordon 1996). Although the SubantarcticFront (SAF) is less well defined, values of 68C and 34.3psu are considered as subsurface expressions of this front inthe Indian sector (Park et al. 1993). Values of 108C and34.8 psu at 200 m depth are adopted to define theSubtropical Front (STF) (Park et al. 1993).

In this study, we defined the Frontal Zone as the arealocated between the STF (northern limit) and the PF(southern limit), the Antarctic Circumpolar Current Zone

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as the area located between the PF and the SACCF, and theAntarctic Zone as the area located between the SACCF andthe Antarctic continent, with a subdivision, named trulyAntarctic waters, and located between the ASF and the

continent (Fig. 1a). Water masses and oceanic areas visitedby foraging seals were characterized according to thetemperature-salinity (T-S) measurements recorded at200 m depth (Fig. 1a’).

Figure 1. (a) Physical oceanography in the Southern Indian Ocean. Isobaths are represented in the background. Colored lines indicateoceanographic fronts as revealed by SST gradients. From north to south these are: Subtropical Front (STF), Sub-Antarctic Front (SAF),Polar Front (PF), Southern Antarctic Circumpolar Current Front (SACCF), and Antarctic Slope Front (ASF). In this study, we refer tothe Frontal Zone domain as the area encompassed between the STF and the PF (modified from Park et al. 1993, Orsi et al. 1995).(a’) 200 m temperature-salinity values sampled by all elephant seals, thus indicating the water masses they visited. (b) Foraging trips of21 males (black lines). (b’) 200 m depth temperature-salinity diagram reveals that males foraged mostly south of the Polar Front and inAntarctic waters. (c) Foraging trips of 18 females (red lines) and (c’) 200 m depth T/S diagram exhibits a wider oceanographicdistribution than males, with individuals mainly concentrated within the Frontal Zone.

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Bathymetry

To complement the oceanographic data collected by theinstrumented animals, we estimated ocean depth fromthe ETOPO 2 database (2? latitude-longitude resolution).Ocean depth was extracted under each filtered Argoslocation of individuals and was used to confirm identifica-tion of benthic dives: diving depth equivalent to oceandepth on dive location.

Stable isotopes analysis

Before isotopic analysis, blood was dried in an oven at�408C and powdered. Sub-samples were then weighed(0.3�0.4 mg) with a microbalance, packed in tin containers,and nitrogen and carbon isotope ratios determined by acontinuous flow mass spectrometer (Micromass Isoprime)coupled to an elemental analyser (Euro Vector EA 3024).Lipids were depleted in 13C relative to proteins andcarbohydrates (Post et al. 2007), but the low lipid contentof whole blood usually does not require lipid extraction(Cherel et al. 2005). We nevertheless carefully checked C:Nratios of the samples, and lipids were extracted fromtwo blood samples using cyclohexane to avoid bias in theinterpretation of d13C values due to varying lipid contentsamong samples. Replicate measurements of internal labora-tory standards (acetanilide) indicated measurement errorsB0.15 and B0.20� for d13C and d15N, respectively.

Both d13C and d15N values were analysed with mixturemodels using WinBUGS 1.4.3 (Spiegelhalter et al. 2003).Mixture models are useful whenever the data are hetero-geneous and composed of several (hidden) groups. TheBayesian framework allows a natural flow of all uncertain-ties in the model and the fitting of less-standard orcomplex models (Gelman et al. 2004). As there was aclear relationship between d15N and body length in malesbut not in females (Fig. 6), we modelled d15N for malesas mixture of two distributions, with the probability ofbelonging to one or the other distribution dependinglinearly (on a logit scale) on body length. A critical lengthbeyond which the nitrogen isotopic signature of malesincreased substantially was thereby estimated. We thenused this threshold length to discriminate between largeand small individuals, and analyzed the carbon signa-ture of both sexes. We modelled the signature of largeindividuals only as a mixture of two Gaussians, whereasd13C of small individuals was modelled as a simpleGaussian. Sex was included as a factor. Convergencewas assessed visually and statistically using, respectively,the Gelman-Rubin and Heidelberger-Welch diagnostics(Cowles and Carlin 1996). Weakly-informative and non-informative priors were used (Gelman et al. 2008).

Results

Distribution at sea

Males weighed more than females (362969 vs 311943 kg;n�21 and n�18, respectively; t�2.77, p�0.009) but

were similar in body length (243918 vs 234912 cm;t�1.95, p�0.06). Males equipped between Novemberand March were longer than those equipped in Septem-ber (248913 vs 225917 cm; n�17 and n�4, respec-tively; t�2.804, p�0.03). No difference was observed inbody mass between these two categories (t�0.842, p�0.44).

Seal tracks

The mean recording duration for animals equippedbetween November and March was shorter for malesthan for females (116941 d (:4 months) vs 175942 d(:6 months); n�17 and n�18, respectively; t�4.14,pB0.001), as was the mean total distance covered(771893229 vs 11 97292460 km; t�4.36, pB0.001),and the maximum distance reached from the colony(168491104 km vs 24629849 km; t�2.33, p�0.02)(Fig. 1b�c). The mean recording duration for the fourmales equipped in September was 54915 d.

Geographic areas visited

The T-S distribution at 200 m depth was plotted from thecomplete data set. Results showed that elephant seals fromKerguelen Islands visited six distinct areas during thisstudy, each separated by the main physical fronts of theSouthern Ocean and the bathymetry from the others,and bracketed in the North by the Subtropical Front andin the South by the Antarctic continent (Fig. 1a�a’ and 2).Kerguelen elephant seals visited all oceanic zones, but theyappeared to favor the Antarctic Zone and the FrontalZone (Fig. 3). However, we observed marked sex differ-ences in distributions. The majority of males targetedeither the truly Antarctic waters or the Kerguelen-Heardplateau (Fig. 1b�b’, 2a, 3). Only the 4 males equippedin September were located in the Frontal Zone. Bycontrast, adult females remained in the pelagic domainmainly within the Frontal Zone. They often traveled inthe ACC Zone, but seldom entered truly Antarctic waters(Fig. 1c�c’, 2b, 3).

Location of feeding

Of 193 354 dives recorded, 6988 were identified as driftdives; 3717 of these were negative drift dives, while 3271were positive ones. The mean maximum depth of drift diveswas 3699168 m with no difference between positiveand negative ones (t�1.57, p�0.11) or between sexes(t�1.29, p�0.19).

Females’ foraging areas, where index of foraging successwas maximal, were mainly located within the Frontal Zonebetween the Subantarctic and Polar Fronts and, to a lesserextent, in the Antarctic Zone (Fig. 4a). Males foragedprimarily in truly Antarctic waters (over the Antarctic shelf)and over the Kerguelen plateau (Fig. 4b), where 52 and58% of dives were benthic, respectively. Both sexes travelled

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through the ACC Zone, where no major foraging activitywas identified by the method of analysis we used.

Stable isotopes analysis

We collected blood samples, after foraging trips, from 180elephant seals (112 females and 68 males), 174 of whomwere also measured (111 females and 63 males). The 39seals (18 females, 21 males) equipped with a satellite tagwere also blood sampled and included in the total. Nomales were blood sampled during spring. Among the blood-sampled animals, no difference was observed betweenthe mean body length of males and females (211932 vs213933 cm; n�63 and n�111, respectively; t�0.350,p�0.729).

Nitrogen isotopes

Males had a much broader range in their d15N signaturethan females and this range was skewed toward highervalues compared to females (males: 9.5�12.6�; females:9.4�11.2�; n�63 and n�111, respectively). Femaleswere characterised by a unimodal distribution of d15Nvalues, which was not associated with body size (Fig. 5)(mean�10.290.1� and standard deviation�0.2490.03�); in contrast, d15N increased with size amongmales (Fig. 5). d15N values in males were a mixtureof two distributions; 47.4% (95% Confidence Interval(CI)�34.9: 60.3) of all males were B210 cm (95%CI�192: 226). These ‘‘small males’’ had a mean nitrogensignature identical to that of females. In contrast, 52.6%(95% CI�39.7: 65.1) of males larger than this thresholdlength (hereafter ‘‘big males’’) had a mean d15N value of11.1� (95% CI�10.8: 11.5) with a standard deviation of0.4� (95% CI�0.2: 1.1). Hence, a difference of 0.9�(95% CI�0.5: 1.2) in d15N value was observed betweensmall and big males.

Carbon isotopes

For both sexes, the distribution of d13C for large individualswas bimodal, while that of small individuals was unimodal(Fig. 6). We therefore modelled d13C in light of thispattern. Both males and females exhibited a similar rangein their blood d13C signature, with two males exhibitingthe highest values (�18.6 and �18.1�) and one femalethe lowest (�23.6�, Fig. 6). Using the estimated d15Nthreshold of males (see above), 54.8% (95% CI�39.7:69.5) of all the individuals were grouped as large, includ-ing 65.3% (95% CI�62.0: 68.8) females and 34.7%(95% CI�31.3: 38.0) males. The d13C distribution oflarge males and large females was modelled as a mixtureof distributions of mean �21.7� (95% CI��22.5:�21.1) and �20.6� (95% CI��21.2: �19.6, Fig. 6),respectively. Small individuals of both sexes had a unimodal

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Figure 3. Proportion of time spent by subadult males (in black)and adult females (in light gray) in different pelagic zones betweenthe Subtropical Front (STF see Fig. 1 and text for otherabbreviations) and Truly Antarctic Waters (TAW) found overthe Antarctic shelf.

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Figure 2. Frequency distribution of water depths (bathymetry (m)) in which (a) males and (b) females foraged (Fig. 1). The principalmode of each distribution highlights that juvenile males foraged mainly in neritic waters, while adult females prefer oceanic waters toforage.

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distribution of d13C values with a mean of �21.0�(95% CI��21.4: �20.7, Fig. 6).

Discussion

The ecological niche of an organism depends on not onlywhere it lives but also on what it does there (Odum 1959).Therefore, the application of bio-logging together andstable isotopes is potentially a powerful way to investi-gate the ecological niche of marine top predators. Indeed,stable isotopes inform on the trophic levels (d15N)of consumers and on their foraging habitats (d13C) atlarge spatial scales (Cherel and Hobson 2007). On theother hand, the use of electronic devices is much better todepict the animals’ movements and behaviours, but it givesno dietary information. Generally, the shorter temporalwindows integrated by blood sample isotopes contrastwith the relative long record duration obtained by satellitetags, which naturally separates both techniques. However,in large mammals, blood integrates over a period of2�3 months (Hilderbrand et al. 1996). Therefore, in ourstudy, the two methods (bio-logging vs isotopes) presenta significant temporal overlap at the end of the forag-ing trips allowing some coherent interpretations. In thisway, our large data set (collected over four consecutiveaustral winters) highlights some marked differences in thedistribution, diving behaviour, foraging habitats, trophic

levels, and dietary habits of juvenile male and adult femaleelephant seals at Kerguelen Islands.

Oceanic habitats identified by telemetry

Over a period of about six months (recording duration)satellite tracking revealed that both sexes ranged throughoutthe Southern Ocean. However, their foraging activity(locations of feeding) was confined to smaller areas: juvenilemales foraged mainly over the Kerguelen-Heard Plateauand over the Antarctic shelf, while most females foraged inoceanic waters of the Polar Frontal Zone and in Antarcticwaters generally associated with the Marginal Ice Zone.Overall, females focused their foraging activity on frontalsystems. These systems are known for their high pri-mary productivity (Holm-Hansen et al. 2004), presumablyrepresenting accessible and predictable high-food sourceareas for Kerguelen seals. Antarctic waters are also impor-tant foraging grounds for both male and female elephantseals, but males forage almost exclusively over the AntarcticPlateau, while females favour oceanic waters (see discussionin Bailleul et al. 2007b). Interestingly, the only male pelagictracks were performed by the 4 smallest individuals (i.e. theyoungest). Previous satellite tracking of naıve pups goingto sea for the first time (McConnell et al. 2002) as well as1�4-yr old juvenile males and females showed that bothsexes foraged in oceanic waters (Field et al. 2005). There-fore, satellite tracking suggests that juvenile males shift

Figure 4. Location of the most favorable foraging/feeding areas characterized using the residual First Bottom Time method (Bailleul et al.2008), and T/S diagrams at 200 m depth corresponding to these zones. (a) Females concentrated their foraging activity mainly within theFrontal Zone, and along the Marginal Ice zone. (b) Males foraged mainly either on the Kerguelen-Heard Plateau or on the Antarctic shelf.See Fig. 1 for abbreviations and line colors.

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their main foraging habitat with age, from predominantlyoceanic waters to predominantly neritic waters.

Additional information obtained from isotopes

The bimodal distribution of both male and female bloodd13C signatures (a proxy for their main foraging habitats)

suggested at least two distinct foraging regions. However,the most negative values observed for both males andfemales in the first model were larger than expected foranimals feeding in truly Antarctic waters (ca �25�24�;Cherel and Hobson 2007, Cherel 2008), while the secondmode coincided well with expected values for subantarcticwaters (�21.50 to �19.50�). Two males had lessnegative d13C values (��18.5�), suggesting feeding

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y = -2.242e-2x + 7.886e-5 x² + 1.187R² = 0.29 ; p < 0.001

Figure 5. Blood d15N values of elephant seals as a function of body length. Black dots and open triangles represent females and males,respectively. The line represents a 2nd order regression for males. No relationship was found for females.

Figure 6. Frequency distribution of blood carbon (d13C) and nitrogen (d15N) values according to the size and sex of elephant seals atKerguelen Island.

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north of the Subtropical Front, in subtropical waters, aforaging zone which was not clearly identified from satellitetracking data. The apparent mismatch between the largerthan expected d13C values and the satellite tracking datawhich documented the importance of foraging in theAntarctic (Bailleul et al. 2007a, b, Biuw et al. 2007; thisstudy) is likely to be the result of the integration time(2�3 months) of the isotopic signature in whole blood.Thus, the isotopic signature described only the most recent2�3 months of the seals’ foraging trips (Ducatez et al.2008). Moreover, the complete lack of very low Antarcticd13C values suggests that both male and female elephantseals that foraged in the Antarctic Zone also fed on theirway back to Kerguelen Islands, thus diluting their lowAntarctic d13C values by the input of higher d13C valuesfrom lower-latitude prey.

Ontogenic changes in foraging ecology

This study indicates that juvenile males have a broaderfeeding niche than females, and that this can be explainedby a progressive shift in trophic level with size (i.e. age). Nochange in d15N values was detected for female sealssuggesting that they did not exhibit major dietary shifts inrelation to size/age and regardless of their breeding status, asimmature and mature females had similar nitrogen signa-tures. A different picture emerged for juvenile males, withsmall individuals having d15N values identical to those offemales, and larger males retaining higher d15N values fora size �210 cm total length, that corresponds to an ageof ca 3�4-yr old (Bell et al. 2005).

Similar d15N values in small males and females isconsistent with similar dietary habits of 1�2 yr old juvenilemales and females found by Field et al. (2007a). However,our study reveals that males exhibit a significant shift intheir foraging ecology with age, thereby revealing anasymmetric foraging ecology between the two sexes. Femaleelephant seals cease growing at 3�4 yr of age, whereasmales undergo another period of growth until maturity(:7 yr) (Bell et al. 2005). Thus, at 3�4 yr of age, femalesmay attempt to increase their body fat reserves forupcoming breeding efforts, while males could invest morein growth, implying different dietary requirements. More-over, as they grow, males develop physiological capabilities(Irvine et al. 2000), compatible mouthparts (Maurer 1996),and adequate experience and associated learning (Langen1996) to exploit another ecological niche. Therefore, theshift in foraging strategy observed for males could beexplained by changes in energetic requirements probablystrongly related to changes in functional characteristics.

At present, it is unclear whether the higher d15N valuesof large juvenile males, compared to females and youngermales, reflects a shift in prey species, because large fish andsquid have higher trophic positions than small mesopelagicfish (Cherel et al. 2008), and/or in foraging habitat, becausethe d15N baseline level is higher over the Kerguelen Plateauthan in the adjacent oceanic waters (Trull et al. 2008).Foraging in different habitats, and thus on different preyspecies, is most likely to occur as fish and squid commu-nities found in neritic waters are generally different fromthose in oceanic waters (Duhamel 1997), and male elephant

seals increase and broaden their trophic range as they grow.Nitrogen values 2.6� higher than the mean d15N offemales observed in the largest males sampled in our studydo suggest that a shift in foraging by growing males isaccompanied by a change in trophic level. Only tissuesamples collected from subadult and adult males will enableus to answer clearly that question.

Indications on the seals’ diet

Although the relative proportions of squid and fish in thediet of elephant seals remained unknown, the former arereported to be the main prey items of juveniles (Greenand Burton 1993, Van den Hoff 2004). Nevertheless,Field et al. (2007b) recently reported that juvenile dietcontained more pelagic fish species than previouslythought. In the present work, a remarkable consistencyin d15N values was observed over a wide range of d13Cvalues for juveniles of both sexes and for adult females,suggesting that all seals fed at about the same trophic levelwhatever their foraging zones. Moreover, the nitrogenisotopic signature of myctophids fits well when comparedto the theoretical d15N value of elephant seal prey (Cherelet al. 2008). Our data thus contrast with the view thatelephant seals are squid consumers but are consistentwith the view that seals, at least adult females and juvenilesof both sexes, feed mainly on mesopelagic fish (see detailsin Cherel et al. 2008).

Perspectives

The combination of stable isotopes and satellite trackingprovides the first evidence of a spatial and trophic shift inelephant seals as they grow. The interanual monitoring ofthe isotopic signature of a large number of breedingfemales (Ducatez et al. 2008) should provide us with anew tool to investigate at the population level, theoccurrence of a possible shift in the main foraging grounds(Frontal Zone vs Antarctic waters) between years accordingto the ocean-climate conditions. Such a pattern wouldcontrast a limited number of tracked individuals thatstrongly suggests that breeding females use the samepreferred regions yearly and regardless of its localproductivity (Bradshaw et al. 2004).

Acknowledgements � This work was included in two differentinternational research programmes: SEaOS (Southern Elephantseals as Oceanographic Samplers) and MEOP (Marine MammalExploration of the Oceans Pole to Pole). This study wasalso included in a national research program (no. 109, HenriWeimerskirch) supported by the Inst. Paul Emile Victor (IPEV).The ‘‘Territoire des Terres Australes et Antarctiques Francaises(TAAF)’’, the ‘‘Region Poitou-Charentes’’, the ‘‘Centre Nationald’Etudes Spatiales’’ (CNES-programme Tosca) and the groupCORIOLIS � MERCATOR largely contributed to this study,which was also supported by the ANR-VMC 07 IPSOS-SEALprogram. The authors would like to thank the members of the53rd, 54th and 55th research missions at Kerguelen Islands,together with the IPEV logistical staff for their assistance inthe field. We wish particularly to thank M. Biuw, I. Field,C. McMahon, M. Hindell, Y.-H. Park, P. Richard andG. Guillou. We thank also all the members of the ‘‘Centre

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d’Etudes Biologiques de Chize’’ for their assistance in the smalldaily problems. The ethics committee of the French Polar Inst.(IPEV) approved this study. All animals in this study were caredfor in accordance with its guidelines.

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