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      Hibernation in an Antarctic Fish: On Ice for Winter

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          Abstract

          Active metabolic suppression in anticipation of winter conditions has been demonstrated in species of mammals, birds, reptiles and amphibians, but not fish. This is because the reduction in metabolic rate in fish is directly proportional to the decrease in water temperature and they appear to be incapable of further suppressing their metabolic rate independently of temperature. However, the Antarctic fish (Notothenia coriiceps) is unusual because it undergoes winter metabolic suppression irrespective of water temperature. We assessed the seasonal ecological strategy by monitoring swimming activity, growth, feeding and heart rate ( f H) in N. coriiceps as they free-ranged within sub-zero waters. The metabolic rate of wild fish was extrapolated from f H recordings, from oxygen consumption calibrations established in the laboratory prior to fish release. Throughout the summer months N. coriiceps spent a considerable proportion of its time foraging, resulting in a growth rate (G w) of 0.18±0.2% day −1. In contrast, during winter much of the time was spent sedentary within a refuge and fish showed a net loss in G w (−0.05±0.05% day −1). Whilst inactive during winter, N. coriiceps displayed a very low f H, reduced sensory and motor capabilities, and standard metabolic rate was one third lower than in summer. In a similar manner to other hibernating species, dormancy was interrupted with periodic arousals. These arousals, which lasted a few hours, occurred every 4–12 days. During arousal activity, f H and metabolism increased to summer levels. This endogenous suppression and activation of metabolic processes, independent of body temperature, demonstrates that N. coriiceps were effectively ‘putting themselves on ice’ during winter months until food resources improved. This study demonstrates that at least some fish species can enter a dormant state similar to hibernation that is not temperature driven and presumably provides seasonal energetic benefits.

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          Physiological Energetics

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            Physiology: hibernation in a tropical primate.

            The Madagascan fat-tailed dwarf lemur, Cheirogaleus medius, hibernates in tree holes for seven months of the year, even though winter temperatures rise to over 30 degrees C. Here we show that this tropical primate relies on a flexible thermal response that depends on the properties of its tree hole: if the hole is poorly insulated, body temperature fluctuates widely, passively following the ambient temperature; if well insulated, body temperature stays fairly constant and the animal undergoes regular spells of arousal. Our findings indicate that arousals are determined by maximum body temperatures and that hypometabolism in hibernating animals is not necessarily coupled to a low body temperature.
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              Constant darkness is a circadian metabolic signal in mammals.

              Environmental light is the 'zeitgeber' (time-giver) of circadian behaviour. Constant darkness is considered a 'free-running' circadian state. Mammals encounter constant darkness during hibernation. Ablation of the master clock synchronizer, the suprachiasmatic nucleus, abolishes torpor, a hibernation-like state, implicating the circadian clock in this phenomenon. Here we report a mechanism by which constant darkness regulates the gene expression of fat catabolic enzymes in mice. Genes for murine procolipase (mClps) and pancreatic lipase-related protein 2 (mPlrp2) are activated in a circadian manner in peripheral organs during 12 h dark:12 h dark (DD) but not light-dark (LD) cycles. This mechanism is deregulated in circadian-deficient mPer1-/-/mPer2m/m mice. We identified circadian-regulated 5'-AMP, which is elevated in the blood of DD mice, as a key mediator of this response. Synthetic 5'-AMP induced torpor and mClps expression in LD animals. Torpor induced by metabolic stress was associated with elevated 5'-AMP levels in DD mice. Levels of glucose and non-esterified fatty acid in the blood are reversed in DD and LD mice. Induction of mClps expression by 5'-AMP in LD mice was reciprocally linked to blood glucose levels. Our findings uncover a circadian metabolic rhythm in mammals.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2008
                5 March 2008
                : 3
                : 3
                : e1743
                Affiliations
                [1 ]Department of Physiology, University of Birmingham, Edgbaston, Birmingham, England
                [2 ]British Antarctic Survey, Natural Environment Research Council, Cambridge, England
                [3 ]Department of Biological Sciences, University of Bangor, Bangor, Wales
                University of Sheffield, United Kingdom
                Author notes
                * To whom correspondence should be addressed. E-mail: dr.hamish.campbell@ 123456gmail.com

                Conceived and designed the experiments: HC SE. Performed the experiments: HC. Analyzed the data: HC. Contributed reagents/materials/analysis tools: KF CB LP SE. Wrote the paper: HC SE.

                Article
                07-PONE-RA-03155R1
                10.1371/journal.pone.0001743
                2254195
                18320061
                1a33cef4-254f-42bd-9089-b50f9c46a629
                Campbell 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
                : 28 December 2007
                : 6 February 2008
                Page count
                Pages: 9
                Categories
                Research Article
                Ecology/Behavioral Ecology
                Ecology/Physiological Ecology

                Uncategorized
                Uncategorized

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