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      Tissue Turnover Rates and Isotopic Trophic Discrimination Factors in the Endothermic Teleost, Pacific Bluefin Tuna ( Thunnus orientalis)

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          Abstract

          Stable isotope analysis (SIA) of highly migratory marine pelagic animals can improve understanding of their migratory patterns and trophic ecology. However, accurate interpretation of isotopic analyses relies on knowledge of isotope turnover rates and tissue-diet isotope discrimination factors. Laboratory-derived turnover rates and discrimination factors have been difficult to obtain due to the challenges of maintaining these species in captivity. We conducted a study to determine tissue- (white muscle and liver) and isotope- (nitrogen and carbon) specific turnover rates and trophic discrimination factors (TDFs) using archived tissues from captive Pacific bluefin tuna (PBFT), Thunnus orientalis, 1–2914 days after a diet shift in captivity. Half-life values for 15N turnover in white muscle and liver were 167 and 86 days, and for 13C were 255 and 162 days, respectively. TDFs for white muscle and liver were 1.9 and 1.1‰ for δ 15N and 1.8 and 1.2‰ for δ 13C, respectively. Our results demonstrate that turnover of 15N and 13C in bluefin tuna tissues is well described by a single compartment first-order kinetics model. We report variability in turnover rates between tissue types and their isotope dynamics, and hypothesize that metabolic processes play a large role in turnover of nitrogen and carbon in PBFT white muscle and liver tissues. 15N in white muscle tissue showed the most predictable change with diet over time, suggesting that white muscle δ 15N data may provide the most reliable inferences for diet and migration studies using stable isotopes in wild fish. These results allow more accurate interpretation of field data and dramatically improve our ability to use stable isotope data from wild tunas to better understand their migration patterns and trophic ecology.

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          Most cited references18

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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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            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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              Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers.

              By switching great skuas Catharacta skua from one isotopically distinct diet to another, we measured diet-tissue discrimination factors and tested the assumption that dietary nitrogen and carbon isotope signatures are incorporated into blood and feathers at similar rates. We also examined the effects of metabolic rate and looked for evidence of isotopic routing. We found that blood delta(15)N and delta(13)C signatures altered after the diet switch at similar rates (14.4 d and 15.7 d, respectively). Qualitative analyses imply that the same was true with feathers. Mass balance calculations suggest that only a small amount of lipid is likely to be involved in the synthesis of blood and feathers. Differences in diet-tissue discrimination factors before and after the diet switch may mean that toward the end of the experiment, some of the nutrients for blood synthesis had been coming from stores. Repeated measures mixed models provided evidence that increases in metabolic rate might accelerate fractional turnover rates in blood. There is a need for more laboratory-based experimental isotope studies in order to address further questions that this study has raised.
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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
                2012
                7 November 2012
                : 7
                : 11
                : e49220
                Affiliations
                [1 ]Tuna Research and Conservation Center, Hopkins Marine Station of Stanford University, Pacific Grove, California, United States of America
                [2 ]Hopkins Marine Station of Stanford University, Pacific Grove, California, United States of America
                [3 ]Department of Geology and Geophysics, University of Hawai'i at Manoa, Honolulu, Hawai'i, United States of America
                [4 ]Monterey Bay Aquarium, Monterey, California, United States of America
                Universitat de Barcelona, Spain
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DJM. Performed the experiments: DJM. Analyzed the data: DJM SYL BNP ABC. Contributed reagents/materials/analysis tools: DJM SYL CJF BAB. Wrote the paper: DJM SYL BNP ABC BAB.

                Article
                PONE-D-12-06741
                10.1371/journal.pone.0049220
                3492276
                23145128
                fd6658c2-0ca4-4ea9-83f9-4b692a934592
                Copyright @ 2012

                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
                : 6 March 2012
                : 8 October 2012
                Page count
                Pages: 13
                Funding
                This work was funded by the Tuna Research and Conservation Center, Monterey Bay Aquarium, and Lerner-Grey fund of the American Natural History Museum. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Anatomy and Physiology
                Physiological Processes
                Energy Metabolism
                Biochemistry
                Metabolism
                Metabolic Pathways
                Nitrogen Metabolism
                Tissue Distribution
                Chemical Biology
                Marine Biology
                Fisheries Science
                Marine Ecology
                Zoology
                Ichthyology

                Uncategorized
                Uncategorized

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