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      Long-term exposure to elevated carbon dioxide does not alter activity levels of a coral reef fish in response to predator chemical cues

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          Abstract

          Abstract

          Levels of dissolved carbon dioxide (CO 2) projected to occur in the world’s oceans in the near future have been reported to increase swimming activity and impair predator recognition in coral reef fishes. These behavioral alterations would be expected to have dramatic effects on survival and community dynamics in marine ecosystems in the future. To investigate the universality and replicability of these observations, we used juvenile spiny chromis damselfish ( Acanthochromis polyacanthus) to examine the effects of long-term CO 2 exposure on routine activity and the behavioral response to the chemical cues of a predator ( Cephalopholis urodeta). Commencing at ~3–20 days post-hatch, juvenile damselfish were exposed to present-day CO 2 levels (~420 μatm) or to levels forecasted for the year 2100 (~1000 μatm) for 3 months of their development. Thereafter, we assessed routine activity before and after injections of seawater (sham injection, control) or seawater-containing predator chemical cues. There was no effect of CO 2 treatment on routine activity levels before or after the injections. All fish decreased their swimming activity following the predator cue injection but not following the sham injection, regardless of CO 2 treatment. Our results corroborate findings from a growing number of studies reporting limited or no behavioral responses of fishes to elevated CO 2.

          Significance statement

          Alarmingly, it has been reported that levels of dissolved carbon dioxide (CO 2) forecasted for the year 2100 cause coral reef fishes to be attracted to the chemical cues of predators. However, most studies have exposed the fish to CO 2 for very short periods before behavioral testing. Using long-term acclimation to elevated CO 2 and automated tracking software, we found that fish exposed to elevated CO 2 showed the same behavioral patterns as control fish exposed to present-day CO 2 levels. Specifically, activity levels were the same between groups, and fish acclimated to elevated CO 2 decreased their swimming activity to the same degree as control fish when presented with cues from a predator. These findings indicate that behavioral impacts of elevated CO 2 levels are not universal in coral reef fishes.

          Electronic supplementary material

          The online version of this article (doi:10.1007/s00265-017-2337-x) contains supplementary material, which is available to authorized users.

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          Most cited references61

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          Ocean acidification: the other CO2 problem.

          Rising atmospheric carbon dioxide (CO2), primarily from human fossil fuel combustion, reduces ocean pH and causes wholesale shifts in seawater carbonate chemistry. The process of ocean acidification is well documented in field data, and the rate will accelerate over this century unless future CO2 emissions are curbed dramatically. Acidification alters seawater chemical speciation and biogeochemical cycles of many elements and compounds. One well-known effect is the lowering of calcium carbonate saturation states, which impacts shell-forming marine organisms from plankton to benthic molluscs, echinoderms, and corals. Many calcifying species exhibit reduced calcification and growth rates in laboratory experiments under high-CO2 conditions. Ocean acidification also causes an increase in carbon fixation rates in some photosynthetic organisms (both calcifying and noncalcifying). The potential for marine organisms to adapt to increasing CO2 and broader implications for ocean ecosystems are not well known; both are high priorities for future research. Although ocean pH has varied in the geological past, paleo-events may be only imperfect analogs to current conditions.
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            Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish.

            The zebrafish (Danio rerio) is emerging as a promising model organism for experimental studies of stress and anxiety. Here we further validate zebrafish models of stress by analyzing how environmental and pharmacological manipulations affect their behavioral and physiological phenotypes. Experimental manipulations included exposure to alarm pheromone, chronic exposure to fluoxetine, acute exposure to caffeine, as well as acute and chronic exposure to ethanol. Acute (but not chronic) alarm pheromone and acute caffeine produced robust anxiogenic effects, including reduced exploration, increased erratic movements and freezing behavior in zebrafish tested in the novel tank diving test. In contrast, ethanol and fluoxetine had robust anxiolytic effects, including increased exploration and reduced erratic movements. The behavior of several zebrafish strains was also quantified to ascertain differences in their behavioral profiles, revealing high-anxiety (leopard, albino) and low-anxiety (wild type) strains. We also used LocoScan (CleverSys Inc.) video-tracking tool to quantify anxiety-related behaviors in zebrafish, and dissect anxiety-related phenotypes from locomotor activity. Finally, we developed a simple and effective method of measuring zebrafish physiological stress responses (based on a human salivary cortisol assay), and showed that alterations in whole-body cortisol levels in zebrafish parallel behavioral indices of anxiety. Collectively, our results confirm zebrafish as a valid, reliable, and high-throughput model of stress and affective disorders.
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              Ocean pCO2 calculated from dissolved inorganic carbon, alkalinity, and equations for K1 and K2: validation based on laboratory measurements of CO2 in gas and seawater at equilibrium

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                Author and article information

                Contributors
                +46 730 302270 , josefin@teamsundin.se , josefin.sundin@neuro.uu.se
                Journal
                Behav Ecol Sociobiol
                Behav. Ecol. Sociobiol. (Print)
                Behavioral Ecology and Sociobiology
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0340-5443
                5 July 2017
                5 July 2017
                2017
                : 71
                : 8
                : 108
                Affiliations
                [1 ]ISNI 0000 0004 1936 9457, GRID grid.8993.b, Department of Neuroscience, , Uppsala University, ; Uppsala, Sweden
                [2 ]ISNI 0000 0004 1936 9377, GRID grid.10548.38, Department of Zoology/Functional Zoomorphology, , Stockholm University, ; Stockholm, Sweden
                [3 ]ISNI 0000000121548364, GRID grid.55460.32, Section of Integrative Biology, , University of Texas, ; Austin, TX USA
                [4 ]ISNI 0000 0001 0658 7699, GRID grid.9811.1, Department of Collective Behaviour, Max Planck Institute for Ornithology, , University of Konstanz, ; Konstanz, Germany
                [5 ]ISNI 0000 0001 0328 1619, GRID grid.1046.3, , Australian Institute of Marine Science, ; Townsville, Queensland Australia
                [6 ]ISNI 0000 0004 1936 9596, GRID grid.267455.7, Great Lakes Institute for Environmental Research, , University of Windsor, ; Windsor, Ontario Canada
                [7 ]ISNI 0000 0001 1516 2393, GRID grid.5947.f, Department of Biology, , Norwegian University of Science and Technology, ; Trondheim, Norway
                [8 ]ISNI 0000 0004 1936 826X, GRID grid.1009.8, , University of Tasmania and CSIRO Agriculture and Food, ; Hobart, Tasmania Australia
                Author notes

                Communicated by J. Lindström

                Article
                2337
                10.1007/s00265-017-2337-x
                5498585
                b55cace1-8ca8-4406-880e-a98f47407d9e
                © The Author(s) 2017

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 28 February 2017
                : 8 June 2017
                : 14 June 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001862, Svenska Forskningsrådet Formas;
                Award ID: 2013-947
                Award ID: 2009-596
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;
                Award ID: 637-2014-449
                Award ID: 621-2012-4679
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100001388, Wenner-Gren Foundation;
                Funded by: Wenner-Gren Foundation
                Funded by: FundRef http://dx.doi.org/10.13039/501100000522, Company of Biologists;
                Award ID: JEBTF-150422
                Funded by: Fulbright Foundation
                Funded by: Endeavour Research Fellowship (AU)
                Categories
                Original Article
                Custom metadata
                © Springer-Verlag GmbH Germany 2017

                Ecology
                climate change,ocean acidification,pomacentridae,olfaction,alarm cue
                Ecology
                climate change, ocean acidification, pomacentridae, olfaction, alarm cue

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