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Marine Ecology Progress Series 370:239 Vol. 370: 239–247, 2008 MARINE ECOLOGY PROGRESS SERIES Published October 28 doi: 10.3354/meps07673 Mar Ecol Prog Ser Stable isotopes reveal the trophic position and mesopelagic fish diet of female southern elephant seals breeding on the Kerguelen Islands Y. Cherel1,*, S. Ducatez1, C. Fontaine1, P. Richard2, C. Guinet1 1Centre d’Etudes Biologiques de Chizé, UPR 1934 du CNRS, BP 14, 79360 Villiers-en-Bois, France 2Centre de Recherche sur les Ecosystèmes Littoraux Anthropisés, UMR 6217 du CNRS-IFREMER-ULR, Place du Séminaire, BP 5, 17137 L’Houmeau, France ABSTRACT: Trophic interactions between organisms are the main drivers of ecosystem dynamics, but scant dietary information is available for wide-ranging predators during migration. We investi- gated feeding habits of a key consumer of the Southern Ocean, the southern elephant seal Miroun- gia leonina, by comparing its blood δ13C and δ15N values with those of various marine organisms, including crustaceans, squid, fishes, seabirds and fur seals. At the end of winter, δ13C values (–23.1 to –20.1‰) indicate that female elephant seals forage mainly in the vicinity of the Polar Front and in the Polar Frontal Zone. Trophic levels derived from δ15N values (trophic level = 4.6) show that the southern elephant seal is a top consumer in the pelagic ecosystem that is dominated by colossal squid. The mean δ15N value of seals (10.1 ± 0.3‰) indicates that they are not crustacean eaters, but instead feed on crustacean-eating prey. Surprisingly, most of the previously identified prey species have isotope δ13C and δ15N values that do not fit with those of potential food items. The most singular pattern to emerge from δ15N values of predators and prey is that female seals are likely to feed on myctophid fishes, not squid or Patagonian toothfish. We therefore suggest that they occupy a unique trophic niche amongst the guild of air-breathing, diving vertebrates by feeding on mesopelagic fish at great depths. In turn, this finding emphasizes the role of myctophids in oceanic waters and will help to quantify and model fluxes of matter and energy within the pelagic ecosystem of the Southern Ocean. KEY WORDS: Cephalopod · Mesopelagic fish · Myctophid · Pelagic ecosystem · Southern Ocean · Squid Resale or republication not permitted without written consent of the publisher INTRODUCTION unknown because M. leonina forage far away from land and have almost empty stomachs when they re- The southern elephant seal Mirounga leonina is the turn. Indeed, stomach lavage has collected only hard largest phocid species and its abundance and body parts of prey species, mainly cephalopod beaks, thus mass make it a major consumer of marine resources in suggesting a strong bias and overestimation towards the Southern Ocean (Guinet et al. 1996, Hindell et al. items that resist digestion and accumulate over time 2003). The use of sophisticated electronic devices over (Rodhouse et al. 1992, Green & Burton 1993, Slip 1995). the last decade has shown that, depending on age and Moreover, dietary samples are only representative of sex, southern elephant seals forage in deep waters (300 the very last portion of the trip, not of prey consumed to 600 m) over wide marine areas during their postmolt over the entire foraging area. These biases lead to the and postbreeding trips (Hindell et al. 1991, 2003, Biuw common, but poorly supported, thought that southern et al. 2007). The identities of their prey are still largely elephant seals are mainly teuthivorous (Whitehead et *Email: [email protected] © Inter-Research 2008 · www.int-res.com 240 Mar Ecol Prog Ser 370: 239–247, 2008 al. 2003), and thus to the estimation that their total an- (Biuw et al. 2007), we focused on subantarctic and nual consumption was about 4.5 million tonnes of prey, Antarctic swarming crustaceans (2 euphausids and primarily oceanic squid (Santos et al. 2001). 1 hyperiid amphipod), 2 main subantarctic and Antarc- Since disentangling the trophodynamics within food tic squid, and the 4 most abundant myctophid fishes webs is an important first step for a better overall that form the bulk of mesopelagic fish biomass in the understanding of ecosystem functioning, recently de- Southern Ocean (Kozlov 1995). Remains from all these veloped methods of diet analysis, e.g. fatty acids and species were previously found in variable amounts in stable isotopes, are now increasingly used to investi- stomach contents of elephant seals (Slip 1995, Field et gate the feeding habits of major consumers. These al. 2007). We also determined the δ13C and δ15N values methods are based on the common principle that ‘you of Patagonian toothfish living in slope waters, because are what you eat’, i.e. the biochemical composition of the species was suggested to be a main prey of ele- molecules and tissues of consumers reflects that of phant seals (Brown et al. 1999). The third dataset was their food in a predictable manner (Kelly 2000). For built using recently published δ13C and δ15N values of example, consumer tissues are enriched in 15N relative cephalopods living in Kerguelen waters, based on to their food and, consequently, δ15N (15N/14N) mea- measurements of squid beaks (Cherel & Hobson 2005). surements serve as indicators of a consumer trophic The Kerguelen community is composed of almost all position. In contrast, δ13C (13C/12C) values vary little the main oceanic squid occurring in the Southern along the food chain and are mainly used to determine Ocean, including the giant and colossal squid. Finally, primary sources in a trophic network. In the marine we estimated the trophic level (TL) of elephant seals environment, δ13C values indicate consumer foraging using their δ15N values and compared it with those of areas (i.e. inshore versus offshore, pelagic versus ben- other consumers to verify the common assumption that thic) or latitudinal variation in the contribution to food marine mammals are top predators in marine ecosys- intake (Kelly 2000, Cherel & Hobson 2007). tems (Bradshaw et al. 2003, Field et al. 2007). In contrast to previous dietary analyses based on ex- amination of stomach contents, the use of fatty acids as trophic markers was consistent with elephant seals MATERIALS AND METHODS having a fish-based diet (Brown et al. 1999) or a fish and squid diet, depending on the location of the forag- Fieldwork was carried out at Kerguelen Islands ing grounds (Bradshaw et al. 2003), hence the call for (49° 21’ S, 70° 18’ E), located in the southern part of the further analyses to determine the relative importance of Polar Frontal Zone in the immediate vicinity of the Polar squid versus fish in its food (Brown et al. 1999). To our Front (Park & Gambéroni 1997). A blood sample was knowledge, the stable isotope method was only used taken from randomly chosen female southern elephant once for southern elephant seals, but, due to the lack of seals during the breeding period (early spring 2006), appropriate reference collections, prey species were and from lactating female Antarctic fur seals Arcto- not identified (Lewis et al. 2006). In the present study, cephalus gazella and adults of each species of penguin we determine whether blood δ13C and δ15N values can in spring 2002 (first dataset). Macaroni and rockhopper indicate the feeding habits of adult female southern penguins (Eudyptes chrysolophus and E. chrysocome elephant seal (hereafter elephant seal) breeding on the filholi, respectively) were captured just after their ar- Kerguelen Islands, southern Indian Ocean. We built up rival in the colony to breed, while king and gentoo pen- 3 unique datasets to interpret the δ13C and δ15N values guins (Aptenodytes patagonicus and Pygoscelis papua, of seals relative to those of various marine organisms respectively) were parent birds feeding chicks. The from the Southern Ocean. second dataset included pelagic crustaceans and fish The first dataset comprised isotopic data from Ker- that were collected at night in January 2005 in oceanic guelen penguins and fur seals, i.e. the guild of air- waters east of the Kerguelen Archipelago using an breathing diving vertebrates to which elephant seals International Young Gadoid Pelagic Trawl. Patagon- belong. Penguins and fur seals breeding in the south- ian toothfish Dissostichus eleginoides were caught on ern Indian Ocean occupy a wide range of trophic bottom longlines in Kerguelen slope waters in May niches, including pelagic/oceanic and benthic/neritic 2006, and warty squid Moroteuthis ingens during trawl species and both fish and crustacean eaters (Lescroel & operations in September 2006. Bost 2005, Lea et al. 2006, Cherel et al. 2007). The sec- To further constrain the foraging ecology of highly ond set of data included δ13C and δ15N values from soft migratory elephant seals, values of species spanning a tissues of the main known pelagic resources from the latitudinal gradient in carbon stable isotopes (Cherel Southern Ocean targeted by marine mammals and & Hobson 2007) were used. First, a subtropical species, seabirds. Since female elephant seals dive pelagically lactating female subantarctic fur seals Arctocephalus from Kerguelen to the Polar Front and Antarctic waters tropicalis from Amsterdam Island (37° 51’ S, 77° 31’ E), Cherel et al.: Southern elephant seal feeding habits 241 and second, a high-Antarctic species, Adélie pen- δ15N and δ13C values, respectively, which correspond guins Pygoscelis adeliae from Adélie Land (66° 40’ S, to the mean isotopic differences between lower beak 140° 01’ E) at the beginning of their breeding cycle. Fi- and muscle of cephalopods (Cherel & Hobson 2005, nally, barely digested Antarctic krill Euphausia superba Hobson & Cherel 2006). Data were statistically ana- and the squid Psychroteuthis glacialis were sorted from lysed using SYSTAT 9. Values are mean ± SD. emperor penguin vomits found on the sea-ice in Adélie Land (Cherel 2008). Once specimens of invertebrates and fish were iden- RESULTS tified, whole crustaceans and pieces of squid and fish muscle (see Table 1) were collected for isotopic ana- At Kerguelen, the 6 species of sympatric pinnipeds lysis and kept at –20°C.
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