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      Using Stable Isotope Analysis to Understand the Migration and Trophic Ecology of Northeastern Pacific White Sharks ( Carcharodon carcharias)

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          Abstract

          The white shark ( Carcharodon carcharias) is a wide-ranging apex predator in the northeastern Pacific (NEP). Electronic tagging has demonstrated that white sharks exhibit a regular migratory pattern, occurring at coastal sites during the late summer, autumn and early winter and moving offshore to oceanic habitats during the remainder of the year, although the purpose of these migrations remains unclear. The purpose of this study was to use stable isotope analysis (SIA) to provide insight into the trophic ecology and migratory behaviors of white sharks in the NEP. Between 2006 and 2009, 53 white sharks were biopsied in central California to obtain dermal and muscle tissues, which were analyzed for stable isotope values of carbon (δ 13C) and nitrogen (δ 15N). We developed a mixing model that directly incorporates movement data and tissue incorporation (turnover) rates to better estimate the relative importance of different focal areas to white shark diet and elucidate their migratory behavior. Mixing model results for muscle showed a relatively equal dietary contribution from coastal and offshore regions, indicating that white sharks forage in both areas. However, model results indicated that sharks foraged at a higher relative rate in coastal habitats. There was a negative relationship between shark length and muscle δ 13C and δ 15N values, which may indicate ontogenetic changes in habitat use related to onset of maturity. The isotopic composition of dermal tissue was consistent with a more rapid incorporation rate than muscle and may represent more recent foraging. Low offshore consumption rates suggest that it is unlikely that foraging is the primary purpose of the offshore migrations. These results demonstrate how SIA can provide insight into the trophic ecology and migratory behavior of marine predators, especially when coupled with electronic tagging data.

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          Tracking apex marine predator movements in a dynamic ocean.

          Pelagic marine predators face unprecedented challenges and uncertain futures. Overexploitation and climate variability impact the abundance and distribution of top predators in ocean ecosystems. Improved understanding of ecological patterns, evolutionary constraints and ecosystem function is critical for preventing extinctions, loss of biodiversity and disruption of ecosystem services. Recent advances in electronic tagging techniques have provided the capacity to observe the movements and long-distance migrations of animals in relation to ocean processes across a range of ecological scales. Tagging of Pacific Predators, a field programme of the Census of Marine Life, deployed 4,306 tags on 23 species in the North Pacific Ocean, resulting in a tracking data set of unprecedented scale and species diversity that covers 265,386 tracking days from 2000 to 2009. Here we report migration pathways, link ocean features to multispecies hotspots and illustrate niche partitioning within and among congener guilds. Our results indicate that the California Current large marine ecosystem and the North Pacific transition zone attract and retain a diverse assemblage of marine vertebrates. Within the California Current large marine ecosystem, several predator guilds seasonally undertake north-south migrations that may be driven by oceanic processes, species-specific thermal tolerances and shifts in prey distributions. We identify critical habitats across multinational boundaries and show that top predators exploit their environment in predictable ways, providing the foundation for spatial management of large marine ecosystems. ©2011 Macmillan Publishers Limited. All rights reserved
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            Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for ?13C analysis of diet

            The use of stable carbon isotopes as a means of studying energy flow is increasing in ecology and paleoecology. However, secondary fractionation and turnover of stable isotopes in animals are poorly understood processes. This study shows that tissues of the gerbil (Meriones unguienlatus) have different δ13C values when equilibrated on corn (C4) or wheat (C3) diets with constant 13C/12C contents. Lipids were depleted 3.0‰ and hair was enriched 1.0‰ relative to the C4 diet. Tissue δ13C values were ranked hair>brain>muscle>liver>fat. After changing the gerbils to a wheat (C3) diet, isotope ratios of the tissues shifted in the direction of the δ13C value of the new diet. The rate at which carbon derived from the corn diet was replaced by carbon derived from the wheat diet was adequately described by a negative exponential decay model for all tissues examined. More metabolically active tissues such as liver and fat had more rapid turnover rates than less metabolically active tissues such as hair. The half-life for carbon ranged from 6.4 days in liver to 47.5 days in hair.The results of this study have important implications for the use of δ13C values as indicators of animal diet. Both fractionation and turnover of stable carbon isotopes in animal tissues may obscure the relative contributions of isotopically distinct dietary components (such as C3 vs. C4, or marine vs. terrestrial) if an animal's diet varies through time. These complications deserve attention in any study using stable isotope ratios of animal tissue as dietary indicators and might be minimized by analysis of several tissues or products covering a range of turnover times.
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              Isotopic ecology ten years after a call for more laboratory experiments.

              About 10 years ago, reviews of the use of stable isotopes in animal ecology predicted explosive growth in this field and called for laboratory experiments to provide a mechanistic foundation to this growth. They identified four major areas of inquiry: (1) the dynamics of isotopic incorporation, (2) mixing models, (3) the problem of routing, and (4) trophic discrimination factors. Because these areas remain central to isotopic ecology, we use them as organising foci to review the experimental results that isotopic ecologists have collected in the intervening 10 years since the call for laboratory experiments. We also review the models that have been built to explain and organise experimental results in these areas.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2012
                15 February 2012
                : 7
                : 2
                : e30492
                Affiliations
                [1 ]Hopkins Marine Station of Stanford University, Pacific Grove, California, United States of America
                [2 ]University of California Santa Cruz, Santa Cruz, California, United States of America
                [3 ]Scripps Institute of Oceanography, University of California San Diego, San Diego, California, United States of America
                [4 ]Monterey Bay Aquarium, Monterey, California, United States of America
                [5 ]Point Reyes National Seashore, Inverness, California, United States of America
                [6 ]University of California Davis, Davis, California, United States of America
                [7 ]Max-Planck-Institut für Ornithologie, Radolfzell, Germany
                [8 ]Montana State University, Bozeman, Montana, United States of America
                Dalhousie University, Canada
                Author notes

                Conceived and designed the experiments: ABC SLK SJJ. Performed the experiments: ABC SLK BXS. Analyzed the data: ABC SLK BXS DJM. Contributed reagents/materials/analysis tools: ABC SLK DJM SJJ CRP SDA TKC PEK BAB. Wrote the paper: ABC DJM SLK BXS SJJ CRP BAB.

                Article
                PONE-D-10-04202
                10.1371/journal.pone.0030492
                3280240
                22355313
                ddee2073-15af-4bcd-8371-156985f10ed8
                Carlisle et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 1 November 2010
                : 18 December 2011
                Page count
                Pages: 15
                Categories
                Research Article
                Biology
                Ecology
                Community Ecology
                Marine Biology
                Zoology
                Earth Sciences
                Geochemistry
                Marine and Aquatic Sciences
                Oceanography
                Oceans

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                Uncategorized

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