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Trophic Position and Foraging Ecology of Ross, Weddell, and Crabeater Seals Revealed by Compound-Specific Isotope Analysis

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Trophic Position and Foraging Ecology of Ross, Weddell, and Crabeater Seals Revealed by Compound-Specific Isotope Analysis Vol. 611: 1–18, 2019 MARINE ECOLOGY PROGRESS SERIES Published February 14 https://doi.org/10.3354/meps12856 Mar Ecol Prog Ser OPENPEN ACCESSCCESS FEATURE ARTICLE Trophic position and foraging ecology of Ross, Weddell, and crabeater seals revealed by compound-specific isotope analysis Emily K. Brault1,*, Paul L. Koch2, Daniel P. Costa3, Matthew D. McCarthy1, Luis A. Hückstädt3, Kimberly T. Goetz4, Kelton W. McMahon5, Michael E. Goebel6, Olle Karlsson7, Jonas Teilmann8, Tero Harkonen7,9, Karin C. Harding10 1Ocean Sciences Department, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, USA 2Earth and Planetary Sciences Department, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, USA 3Ecology and Evolutionary Biology, University of California, Santa Cruz, 100 Shaffer Road, Santa Cruz, CA 95064, USA 4National Institute of Water and Atmospheric Research, 301 Evans Bay Parade, Wellington 6021, New Zealand 5Graduate School of Oceanography, University of Rhode Island, 215 S Ferry Rd, Narragansett, RI 02882, USA 6Antarctic Ecosystem Research Division, NOAA Fisheries, Southwest Fisheries Science Center, 8901 La Jolla Shores Dr., La Jolla, CA 92037, USA 7Department of Environmental Research and Monitoring, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden 8Department of Bioscience - Marine Mammal Research, Aarhus University, Frederiksborgvej 399, 4000 Roskilde, Denmark 9Martimas AB, Höga 160, 442 73 Kärna, Sweden 10Department of Biological and Environmental Sciences, University of Gothenburg, Box 463, 405 30 Gothenburg, Sweden ABSTRACT: Ross seals Ommatophoca rossii are one of the least studied marine mammals, with little known about their foraging ecology. Research to date using bulk stable isotope analysis suggests that Ross seals have a trophic position intermediate between that of Weddell Leptonychotes weddellii and crab - eater Lobodon carcinophaga seals. However, con- sumer bulk stable isotope values not only reflect trophic dynamics, but also variations in baseline isotope values, which can be substantial. We used compound-specific isotope analysis of amino acids (CSI-AA) to separate isotopic effects of a shifting Weddell seal female and her pup in McMurdo Sound, base line versus trophic structure on the foraging Antarctica. ecology of these ecologically important Antarctic Photo: Daniel P. Costa pinnipeds. We found that Ross seals forage in an open ocean food web, while crabeater and Weddell seals forage within similar food webs closer to shore. with a krill-dominated diet. Our results redefine the However, isotopic evidence suggests that crabeater view of the trophic dynamics and foraging ecology of seals are likely following sea ice, while Weddell seals the Ross seal, and also highlight the importance of target productive areas of the continental shelf of quantifying base line isotope variations in foraging West Antarctica. Our CSI-AA data indicate that Ross studies. seals have a high trophic position equivalent to that of Weddell seals, contrary to prior conclusions from KEY WORDS: Ross seal · Weddell seal · Crabeater nitrogen isotope results on bulk tissues. CSI-AA indi- seal · Compound-specific isotopes · Amino acids · cates that crabeater seals are at a trophic position Antarctica · Foraging ecology · Trophic dynamics lower than that of Ross and Weddell seals, consistent © The authors 2019. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un - *Corresponding author: [email protected] restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 2 Mar Ecol Prog Ser 611: 1–18, 2019 1. INTRODUCTION predator’s diet, perhaps 1 to 2 d (Dellinger & Trill- mich 1988, Burns et al. 1998). In addition, soft tissues The Ross seal Ommatophoca rossii is one of the are more completely digested than hard tissues, re - least studied marine mammals (Bengtson et al. 2011, sulting in biases towards prey with indigestible hard Würsig et al. 2018). The total population estimate for parts (Burns et al. 1998, Staniland 2002, Arim & Naya this species is around 200000, considerably less than 2003, Yonezaki et al. 2003). Given these drawbacks, the estimates for other Antarctic true seals, which are recent research on Antarctic seal ecology has often approximately one million individuals for Weddell used bulk stable isotope values. seals Leptonychotes weddellii and 10 to 15 million Measurements of bulk tissue stable carbon (δ13C) individuals for crabeater seals Lobodon carcino - and nitrogen (δ15N) isotope values (i.e. the weighted phaga (Laws 1977, Bengtson et al. 2011, Würsig et al. average of all components within a tissue) have been 2018). All 3 of these pinniped species have circum - used to indicate a predator’s foraging region and polar distributions (Laws 1977, Würsig et al. 2018). trophic position (Boecklen et al. 2011). The δ13C and Ross seals have fairly small and narrow bodies (with δ15N values of a consumer are the isotopic values of body masses up to about 250 kg) with short snouts primary producers, the base of the food web, with and small mouths. Weddell and crabeater seals are modifications resulting from each trophic transfer, generally larger than Ross seals, having body masses when energy is transferred from one trophic level to up to about 600 kg (Würsig et al. 2018). Weddell seals another (e.g. Lorrain et al. 2009, Graham et al. 2010, have bulkier bodies with small heads relative to their Jaeger et al. 2010, Brault et al. 2018). These modifica- body sizes and short snouts, while crabeater seals tions are predictable and described further below have slender bodies with long, upturned snouts. Ross (Minagawa & Wada 1984). Stable isotope analysis seals are not commonly ob served, which is likely has the advantage of providing an integrated view of because they spend most of their time at sea and in an animal’s diet over longer time scales (weeks to habitats that are logistically challenging to access years depending on the tissue) than the traditional (Laws 1977, Würsig et al. 2018). Thus, several key procedures (Vander Zanden et al. 2015). Carbon iso- aspects of Ross seal biology remain poorly under- tope values show little 13C-enrichment with trophic stood, including their preferred prey, foraging habi- transfer. Thus, consumer δ13C values are often thought tat, and behavior. In contrast, many studies have to closely reflect values at the base of food webs, been conducted on crabeater and Weddell seals, and making them useful for studying the foraging areas thus more information is available on their ecology of a predator. Spatial changes in the δ13C of primary (Hückstädt et al. 2012a, Arcalís-Planas et al. 2015, producers (often referred to as ‘baseline’ δ13C values) Goetz et al. 2017). may reflect variations in their environmental condi- Diets of Antarctic predators, such as Ross, Weddell, tions, such as dissolved inorganic carbon δ13C values, and crabeater seals, may consist of various fish, dissolved CO2 concentrations, CO2 drawdown, and cephalopods, and zooplankton species (Laws 1977, temperature (reviewed in McMahon et al. 2013). Pinkerton et al. 2010). Possible fish prey include They may also reflect physiological characteristics of Antarctic toothfish Dissotichus mawsoni, Antarctic the primary producers, including internal biological silverfish Pleuragamma antarcticum, and cod ice- parameters (e.g. growth rate) and structure (e.g. cell fishes Trematomus spp. Glacial squid Psychroteuthis size and geometry of phytoplankton) (McMahon et glacialis is a cephalopod and known diet component al. 2013). Provided the primary processes driving of some Antarctic consumers. Antarctic krill Euphau- variation are known, bulk δ13C values of an animal sia superba are key prey for an array of predators. can give valuable information on its foraging habitat. Other krill species, such as ice krill E. crystal- The Southern Ocean is known to have considerable 13 13 lorophias may contribute to their diets. In the sub - spatial variation in baseline δ C (δ Cbaseline) values sequent text, ‘krill’ refers to various species within (Rau et al. 1982, Quillfeldt et al. 2010, Brault et al. the order Euphausiacea. Krill are crustaceans that 2018). Several studies have observed decreasing are largely herbivorous and form the link between δ13C values with increasing latitude, with offsets be - primary producers (phytoplankton in marine systems) tween about 55 and 79° S of approximately 3‰, and apex predators. largely reflecting variations in sea surface tempera- Conventional techniques for studying an animal’s ture (Rau et al. 1982, Graham et al. 2010, Quillfeldt et diet, such as scat and stomach content analysis, have al. 2010, Magozzi et al. 2017, Brault et al. 2018). significant limitations when applied to Antarctic pin- In contrast to carbon isotopes, trophic transfers nipeds. These methods capture only a snapshot of a have a considerable affect on an animal’s δ15N val- Brault et al.: Antarctic seal foraging ecology 3 ues. Since a consumer’s tissues become enriched in studies suggesting that D. mawsoni may comprise 15N by ~2−5‰ with each trophic transfer (e.g. pri- nearly the entire daily diet of Weddell seals during mary producers to herbivores to carnivores) due to the spring and summer in McMurdo Sound (Plötz the preferential loss of 14N during amino acid metab- 1986, Ponganis & Stockard 2007, Ainley & Siniff olism (Minagawa & Wada 1984), δ15N values are 2009, Goetz et al. 2017). Hard parts of D. mawsoni often used to indicate an animal’s trophic position. are not consumed and thus not detected via scat and Yet variations in baseline (i.e. primary producer) δ15N stomach content analyses, techniques that have been 15 (δ Nbaseline) values also occur and are passed on, with used for much of the prior research on Weddell seal additional change due to trophic transfers, to upper foraging ecology (see Goetz et al. 2017). Recently, trophic level predators (McMahon et al. 2013). Nutri- Goetz et al. (2017) assessed Weddell seal foraging 13 15 ent source (e.g. nitrate, ammonium, or N2 fixation), ecology with bulk δ C and δ N measurements of microbial transformations (e.g.
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