Exercise changes behaviour

Summary Exercise, which may be defined as bodily movement produced by the contraction of skeletal muscle and which increases energy expenditure above basal levels, is essential for fitness-related activities such as foraging, migration and dispersal. The frequency with which individuals engage in exercise depends on a range of intrinsic and environmental factors. Exercise itself can modify behaviour by inducing endocrine changes and by a training effect that increases physiological capacities. Here, we test the hypothesis that exercise changes behaviour and that there is positive feedback so that performing exercise increases the likelihood of performing exercise-related behaviours. We show that there was a training effect that improved sustained swimming performance of mosquitofish (Gambusia holbrooki) exposed to chronic exercise in flowing water for 4 weeks compared to sedentary controls. Exercised fish also became bolder and were quicker to leave a refuge, showed an increasing tendency to explore unfamiliar environments, and were more aggressive than sedentary fish. These physiological and behavioural changes reverted back to control levels when exercised fish assumed a sedentary lifestyle again. We used the calcium channel blocker nifedipine to decrease swimming performance of exercised fish to control levels, which allowed us to determine whether increased locomotor capacity per se influences behaviour. We show that reducing the swimming performance of exercised fish also reduced exploration and aggression, but it did not affect the latency to leave a refuge (boldness). Our data show that behavioural phenotypes are not fixed. Exercise changes behaviour and may thereby alter interactions between individuals and dispersal. Environmental changes that demand increased levels of exercise induce behavioural responses that are likely to increase the success of individuals under these changed conditions.

[1]  Frank W. Booth,et al.  Reduced physical activity and risk of chronic disease: the biology behind the consequences , 2008, European Journal of Applied Physiology.

[2]  E. Revilla,et al.  A movement ecology paradigm for unifying organismal movement research , 2008, Proceedings of the National Academy of Sciences.

[3]  G. Quinn,et al.  Experimental Design and Data Analysis for Biologists , 2002 .

[4]  J. Husak,et al.  FASTER LIZARDS SIRE MORE OFFSPRING: SEXUAL SELECTION ON WHOLE‐ANIMAL PERFORMANCE , 2006, Evolution; international journal of organic evolution.

[5]  A. Sih,et al.  Behavioral Syndromes: An Integrative Overview , 2004, The Quarterly Review of Biology.

[6]  J. Hawley,et al.  Exercise: it's the real thing! , 2009, Nutrition reviews.

[7]  L. Sneddon,et al.  Physiological constraints on contest behaviour , 2007 .

[8]  Arthur F Kramer,et al.  Exercise, cognition, and the aging brain. , 2006, Journal of applied physiology.

[9]  R. Rhodes,et al.  Personality correlates of physical activity: a review and meta-analysis , 2006, British Journal of Sports Medicine.

[10]  A. Ward,et al.  Aggression‐induced fin damage modulates trade‐offs in burst and endurance swimming performance of mosquitofish , 2011 .

[11]  F. Seebacher,et al.  Low Levels of Physical Activity Increase Metabolic Responsiveness to Cold in a Rat (Rattus fuscipes) , 2010, PloS one.

[12]  K. Smith,et al.  Muscle protein synthesis in response to nutrition and exercise , 2012, The Journal of physiology.

[13]  S. Knecht,et al.  High impact running improves learning , 2007, Neurobiology of Learning and Memory.

[14]  D. Jenkins,et al.  Behavioral constraints for the spread of the eastern mosquitofish, Gambusia holbrooki (Poeciliidae) , 2007, Biological Invasions.

[15]  W. Kindermann,et al.  Changes in β-Endorphin Levels in Response to Aerobic and Anaerobic Exercise , 1992 .

[16]  G. Pyke Plague Minnow or Mosquito Fish? A Review of the Biology and Impacts of Introduced Gambusia Species , 2008 .

[17]  R. Meeusen,et al.  Exercise and Brain Neurotransmission , 1995, Sports medicine.

[18]  Richard W. Brill,et al.  Selective advantages conferred by the high performance physiology of tunas, billfishes, and dolphin fish , 1996 .

[19]  Steven J. Stanton,et al.  Testosterone and sport: Current perspectives , 2012, Hormones and Behavior.

[20]  A. Farrell,et al.  Differences in Thermal Tolerance Among Sockeye Salmon Populations , 2011, Science.

[21]  W. Davison The Effects of Exercise Training on Teleost Fish, a Review of Recent Literature , 1997 .

[22]  B S Weir,et al.  Truncated product method for combining P‐values , 2002, Genetic epidemiology.

[23]  Denis Réale,et al.  Behavioural reaction norms: animal personality meets individual plasticity. , 2010, Trends in ecology & evolution.

[24]  A. Ward,et al.  Personality and social context , 2011, Biological reviews of the Cambridge Philosophical Society.

[25]  David C. Douglas,et al.  Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? , 2008, Proceedings of the Royal Society B: Biological Sciences.

[26]  B. Congdon Characteristics of dispersal in the eastern mosquitofish Gambusia holbrooki , 1994 .

[27]  F. Penedo,et al.  Exercise and well-being: a review of mental and physical health benefits associated with physical activity , 2005, Current opinion in psychiatry.

[28]  Theodore Garland,et al.  Performance, Personality, and Energetics: Correlation, Causation, and Mechanism* , 2012, Physiological and Biochemical Zoology.

[29]  V. R. Richards,et al.  Nifedipine Kinetics and Bioavailability After Single Intravenous and Oral Doses in Normal Subjects , 1983, Journal of clinical pharmacology.

[30]  M. Briffa,et al.  Is boldness a resource-holding potential trait? Fighting prowess and changes in startle response in the sea anemone, Actinia equina , 2012, Proceedings of the Royal Society B: Biological Sciences.

[31]  C. M. Lessells,et al.  Unrepeatable repeatabilities: a common mistake , 1987 .

[32]  D. Ely,et al.  Effect of voluntary exercise on open-field behavior and on aggression in the spontaneously hypertensive rat (SHR). , 1987, Behavioral and neural biology.

[33]  J. Stamps,et al.  Development of behavioural differences between individuals and populations of sticklebacks, Gasterosteus aculeatus , 2004, Animal Behaviour.

[34]  S. Åkesson,et al.  Long-distance migration: evolution and determinants , 2003 .

[35]  M. Järvilehto,et al.  Effects of training on functional variables of muscles in reared Atlantic salmon Salmo salar smolts: connection to downstream migration pattern. , 2011, Journal of fish biology.

[36]  F. Seebacher,et al.  Differences in locomotor performance between individuals: importance of parvalbumin, calcium handling and metabolism , 2012, Journal of Experimental Biology.

[37]  J. Godin,et al.  Boldness and Reproductive Fitness Correlates in the Eastern Mosquitofish, Gambusia holbrooki , 2010 .

[38]  N. Dingemanse,et al.  Integrating animal temperament within ecology and evolution , 2007, Biological reviews of the Cambridge Philosophical Society.

[39]  F. Booth,et al.  Lack of exercise is a major cause of chronic diseases. , 2012, Comprehensive Physiology.

[40]  R. James,et al.  How well do muscle biomechanics predict whole-animal locomotor performance? The role of Ca2+ handling , 2012, Journal of Experimental Biology.

[41]  F. Booth,et al.  Exercise and gene expression: physiological regulation of the human genome through physical activity , 2002, The Journal of physiology.

[42]  M. Moran Arguments for rejecting the sequential Bonferroni in ecological studies , 2003 .

[43]  T. E. Denton,et al.  Caudal fin regeneration in the mosquito fish, Gambusia affinis. An in vivo system for the study of ultraviolet radiation damage. , 1977, Radiation research.

[44]  S. Bertram,et al.  Behavioral correlations across activity, mating, exploration, aggression, and antipredator contexts in the European house cricket, Acheta domesticus , 2010, Behavioral Ecology and Sociobiology.

[45]  Jean Clobert,et al.  Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. , 2009, Ecology letters.

[46]  I. Vuori Physical inactivity is a cause and physical activity is a remedy for major public health problems , 2004 .

[47]  A. Kolok Interindividual variation in the prolonged locomotor performance of ectothermic vertebrates: A comparison of fish and herpetofaunal methodologies and a brief review of the recent fish literature , 1999 .

[48]  K. Renner,et al.  Stress induces rapid changes in serotonergic activity: restraint and exertion , 2000, Behavioural Brain Research.

[49]  M. Briffa,et al.  Whole-organism performance capacity predicts resource-holding potential in the hermit crab Pagurus bernhardus , 2010, Animal Behaviour.