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      Stable Isotope and Signature Fatty Acid Analyses Suggest Reef Manta Rays Feed on Demersal Zooplankton

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          Abstract

          Assessing the trophic role and interaction of an animal is key to understanding its general ecology and dynamics. Conventional techniques used to elucidate diet, such as stomach content analysis, are not suitable for large threatened marine species. Non-lethal sampling combined with biochemical methods provides a practical alternative for investigating the feeding ecology of these species. Stable isotope and signature fatty acid analyses of muscle tissue were used for the first time to examine assimilated diet of the reef manta ray Manta alfredi, and were compared with different zooplankton functional groups (i.e. near-surface zooplankton collected during manta ray feeding events and non-feeding periods, epipelagic zooplankton, demersal zooplankton and several different zooplankton taxa). Stable isotope δ 15N values confirmed that the reef manta ray is a secondary consumer. This species had relatively high levels of docosahexaenoic acid (DHA) indicating a flagellate-based food source in the diet, which likely reflects feeding on DHA-rich near-surface and epipelagic zooplankton. However, high levels of ω6 polyunsaturated fatty acids and slightly enriched δ 13C values in reef manta ray tissue suggest that they do not feed solely on pelagic zooplankton, but rather obtain part of their diet from another origin. The closest match was with demersal zooplankton, suggesting it is an important component of the reef manta ray diet. The ability to feed on demersal zooplankton is likely linked to the horizontal and vertical movement patterns of this giant planktivore. These new insights into the habitat use and feeding ecology of the reef manta ray will assist in the effective evaluation of its conservation needs.

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          A rapid method of total lipid extraction and purification.

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            Biology, ecology and conservation of the Mobulidae.

            The Mobulidae are zooplanktivorous elasmobranchs comprising two recognized species of manta rays (Manta spp.) and nine recognized species of devil rays (Mobula spp.). They are found circumglobally in tropical, subtropical and temperate coastal waters. Although mobulids have been recorded for over 400 years, critical knowledge gaps still compromise the ability to assess the status of these species. On the basis of a review of 263 publications, a comparative synthesis of the biology and ecology of mobulids was conducted to examine their evolution, taxonomy, distribution, population trends, movements and aggregation, reproduction, growth and longevity, feeding, natural mortality and direct and indirect anthropogenic threats. There has been a marked increase in the number of published studies on mobulids since c. 1990, particularly for the genus Manta, although the genus Mobula remains poorly understood. Mobulid species have many common biological characteristics although their ecologies appear to be species-specific, and sometimes region-specific. Movement studies suggest that mobulids are highly mobile and have the potential to rapidly travel large distances. Fishing pressure is the major threat to many mobulid populations, with current levels of exploitation in target fisheries unlikely to be sustainable. Advances in the fields of population genetics, acoustic and satellite tracking, and stable-isotope and fatty-acid analyses will provide new insights into the biology and ecology of these species. Future research should focus on the uncertain taxonomy of mobulid species, the degree of overlap between their large-scale movement and human activities such as fisheries and pollution, and the need for management of inter-jurisdictional fisheries in developing nations to ensure their long-term sustainability. Closer collaboration among researchers worldwide is necessary to ensure standardized sampling and modelling methodologies to underpin global population estimates and status. © 2012 The Authors. Journal of Fish Biology © 2012 The Fisheries Society of the British Isles.
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              Using Stable Isotope Analysis to Understand the Migration and Trophic Ecology of Northeastern Pacific White Sharks (Carcharodon carcharias)

              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 (δ13C) and nitrogen (δ15N). 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 δ13C and δ15N 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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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                22 October 2013
                : 8
                : 10
                : e77152
                Affiliations
                [1 ]School of Biomedical Sciences, The University of Queensland, St Lucia, Queensland, Australia
                [2 ]Climate Adaptation Flagship, CSIRO Marine and Atmospheric Research, Dutton Park, Queensland, Australia
                [3 ]Manta Ray and Whale Shark Research Centre, Marine Megafauna Foundation, Praia do Tofo, Inhambane, Mozambique
                [4 ]Biophysical Oceanography Group, School of Geography, Planning and Environmental Management, The University of Queensland, St Lucia, Queensland, Australia
                [5 ]Centre for Applications in Natural Resource Mathematics, The University of Queensland, St Lucia, Queensland, Australia
                [6 ]Wild Me, Praia do Tofo, Inhambane, Mozambique
                [7 ]School of Biological Sciences, Moreton Bay Research Station, The University of Queensland, Dunwich, Queensland, Australia
                [8 ]Wealth from Oceans Flagship, CSIRO Marine and Atmospheric Research, Hobart, Tasmania, Australia
                Aristotle University of Thessaloniki, Greece
                Author notes

                Competing Interests: This study was funded by the Australian Research Council Linkage Grant (LP110100712), Earthwatch Institute Australia, Sea World Research and Rescue Foundation Inc. and Sibelco Pty Ltd. Field work was supported by Casa Barry Lodge and Peri-Peri Divers in Mozambique, and Lady Elliot Island Eco Resort and Manta Lodge and Scuba Centre in Australia. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: LC CR AR MB PN. Performed the experiments: LC CR AM FJ KT SW PN. Analyzed the data: LC CR AR PN. Contributed reagents/materials/analysis tools: AR AM MB PN. Wrote the paper: LC CR AR FJ AM MB KT SW PN.

                Article
                PONE-D-13-07262
                10.1371/journal.pone.0077152
                3805558
                24167562
                f86cc34e-e082-4d2e-b6c1-5a19790e76c8
                Copyright @ 2013

                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
                : 15 February 2013
                : 31 August 2013
                Page count
                Pages: 15
                Funding
                This study was supported by the Australian Research Council Linkage Grant (LP110100712), Earthwatch Institute Australia, Sea World Research and Rescue Foundation Inc. and Sibelco Pty Ltd. Field work was supported by Casa Barry Lodge and Peri-Peri Divers in Mozambique, and Lady Elliot Island Eco Resort and Manta Lodge and Scuba Centre in Australia. Funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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