Behavioural responses of fish groups exposed to a predatory threat under elevated CO2.

Most of the studies dealing with the effects of ocean acidification (OA) on fish behaviour tested individuals in isolation, even when the examined species live in shoals in the wild. Here we evaluated the effects of elevated CO2 concentrations (i.e. ∼900 μatm) on the shelter use and group cohesion of the gregarious damselfish Chromis viridis using groups of sub-adults exposed to a predatory threat. Results showed that, under predatory threat, fish reared at elevated CO2 concentrations displayed a risky behaviour (i.e. decreased shelter use), whereas their group cohesion was unaffected. Our findings add on increasing evidence to account for social dynamics in OA experiments, as living in groups may compensate for CO2-induced risky behaviour.

[1]  I. Nagelkerken,et al.  Species Interactions Drive Fish Biodiversity Loss in a High-CO2 World , 2017, Current Biology.

[2]  M. C. Ferrari,et al.  Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectusThe present review is one in the special series of reviews on animal–plant interactions. , 2010 .

[3]  F. Millero,et al.  A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media , 1987 .

[4]  S. Simpson,et al.  Ocean acidification boosts larval fish development but reduces the window of opportunity for successful settlement , 2015, Proceedings of the Royal Society B: Biological Sciences.

[5]  P. Munday,et al.  Altered brain ion gradients following compensation for elevated CO2 are linked to behavioural alterations in a coral reef fish , 2016, Scientific Reports.

[6]  J. Pandolfi,et al.  Predicting evolutionary responses to climate change in the sea. , 2013, Ecology letters.

[7]  L. Crowder,et al.  Larval Size and Recruitment Mechanisms in Fishes: Toward a Conceptual Framework , 1988 .

[8]  S. Lefevre.  Are global warming and ocean acidification conspiring against marine ectotherms? A meta-analysis of the respiratory effects of elevated temperature, high CO2 and their interaction , 2016, Conservation physiology.

[9]  P. Munday.  Transgenerational acclimation of fishes to climate change and ocean acidification , 2014, F1000prime reports.

[10]  M. C. Ferrari,et al.  Ocean acidification and responses to predators: can sensory redundancy reduce the apparent impacts of elevated CO2 on fish? , 2013, Ecology and evolution.

[11]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[12]  J. Krause,et al.  Physiological mechanisms underlying animal social behaviour , 2017, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  P. Munday,et al.  Behavioural lateralization and shoaling cohesion of fish larvae altered under ocean acidification , 2016 .

[14]  E. Santos,et al.  Near-future CO2 levels impair the olfactory system of a marine fish , 2018, Nature Climate Change.

[15]  Rui J.M. Rocha,et al.  Impact of air exposure on the photobiology and biochemical profile of an aggressive intertidal competitor, the zoanthid Palythoa caribaeorum , 2016, Marine Biology.

[16]  P. Munday,et al.  Habitat preferences of coral-associated fishes are altered by short-term exposure to elevated CO2 , 2013 .

[17]  T. Pitcher.  Functions of Shoaling Behaviour in Teleosts , 1986 .

[18]  P. Munday,et al.  Food ration does not influence the effect of elevated CO2 on antipredator behaviour of a reef fish , 2018 .

[19]  G. Kwan,et al.  CO2-induced ocean acidification does not affect individual or group behaviour in a temperate damselfish , 2017, Royal Society Open Science.

[20]  S. Dupont,et al.  Evolution in an acidifying ocean. , 2014, Trends in ecology & evolution.

[21]  J. Steffensen,et al.  Fish swimming in schools save energy regardless of their spatial position , 2014, Behavioral Ecology and Sociobiology.

[22]  P. Munday,et al.  Elevated CO2 affects the behavior of an ecologically and economically important coral reef fish , 2013 .

[23]  P. Munday,et al.  Shoaling reduces metabolic rate in a gregarious coral reef fish species , 2016, Journal of Experimental Biology.

[24]  R. Feely,et al.  Ocean acidification: the other CO2 problem. , 2009, Annual review of marine science.

[25]  A. Dickson.  Standard potential of the reaction: , and and the standard acidity constant of the ion HSO4− in synthetic sea water from 273.15 to 318.15 K , 1990 .

[26]  D. Barceló,et al.  Differential behavioural responses to venlafaxine exposure route, warming and acidification in juvenile fish (Argyrosomus regius). , 2018, The Science of the total environment.

[27]  M. Milazzo,et al.  Ocean acidification does not impair predator recognition but increases juvenile growth in a temperate wrasse off CO2 seeps. , 2017, Marine environmental research.

[28]  Russell V. Lenth,et al.  Least-Squares Means: The R Package lsmeans , 2016 .

[29]  Paolo Domenici,et al.  Context-dependent variability in the components of fish escape response: integrating locomotor performance and behavior. , 2010, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[30]  D. Wallace,et al.  MS Excel Program Developed for CO2 System Calculations , 2011 .

[31]  M. Meekan,et al.  Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference , 2014, Global change biology.

[32]  Shoaling fish can size-assort by chemical cues alone , 2013, Behavioral Ecology and Sociobiology.

[33]  R. R. Krausz.  Living in Groups , 2013 .

[34]  F. Jutfelt,et al.  Juvenile Atlantic cod behavior appears robust to near-future CO2 levels , 2015, Frontiers in Zoology.

[35]  D. Lecchini,et al.  Larval sensory abilities and mechanisms of habitat selection of a coral reef fish during settlement , 2005, Oecologia.

[36]  M. Dadda,et al.  Enhanced schooling performance in lateralized fishes , 2005, Proceedings of the Royal Society B: Biological Sciences.

[37]  M. Fine,et al.  The Red Sea Simulator: A high‐precision climate change mesocosm with automated monitoring for the long‐term study of coral reef organisms , 2018 .

[38]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[39]  C. Culberson,et al.  MEASUREMENT OF THE APPARENT DISSOCIATION CONSTANTS OF CARBONIC ACID IN SEAWATER AT ATMOSPHERIC PRESSURE1 , 1973 .

[40]  Anthony R. Ives,et al.  Three points to consider when choosing a LM or GLM test for count data , 2016 .

[41]  L. Dill,et al.  Cost/benefit analysis of group and solitary resting in the cowtail stingray, Pastinachus sephen , 2005 .

[42]  P. Domenici,et al.  Living in a high CO2 world: a global meta-analysis shows multiple trait-mediated fish responses to ocean acidification , 2018 .

[43]  P. Munday,et al.  Effect of elevated carbon dioxide on shoal familiarity and metabolism in a coral reef fish , 2016, Conservation physiology.

[44]  M. Meekan,et al.  Effects of ocean acidification on visual risk assessment in coral reef fishes , 2012 .

[45]  P. Munday,et al.  Diel CO2 cycles reduce severity of behavioural abnormalities in coral reef fish under ocean acidification , 2017, Scientific Reports.

[46]  S. L. Lima,et al.  Behavioral decisions made under the risk of predation: a review and prospectus , 1990 .

[47]  Paolo Domenici,et al.  Escape behaviour of solitary herring (Clupea harengus ) and comparisons with schooling individuals , 1997 .

[48]  M. Meekan,et al.  Replenishment of fish populations is threatened by ocean acidification , 2010, Proceedings of the National Academy of Sciences.

[49]  I. Nagelkerken,et al.  Ecological complexity buffers the impacts of future climate on marine consumers , 2018, Nature Climate Change.

[50]  K. Calvin,et al.  The RCP greenhouse gas concentrations and their extensions from 1765 to 2300 , 2011 .

[51]  D. Sumpter,et al.  Fast and accurate decisions through collective vigilance in fish shoals , 2011, Proceedings of the National Academy of Sciences.

[52]  M. Meekan,et al.  Selective mortality associated with variation in CO2 tolerance in a marine fish , 2012 .

[53]  P. Munday,et al.  Elevated CO2 Affects Predator-Prey Interactions through Altered Performance , 2013, PloS one.

[54]  P. Munday,et al.  Effects of elevated CO2 on predator avoidance behaviour by reef fishes is not altered by experimental test water , 2016, bioRxiv.

[55]  J. Hall‐Spencer,et al.  Ocean acidification affects fish spawning but not paternity at CO2 seeps , 2016, Proceedings of the Royal Society B: Biological Sciences.

[56]  I. Nagelkerken,et al.  Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community‐level responses , 2016, Global change biology.

[57]  T. Pitcher,et al.  Vigilant behaviour and shoal size in minnows , 2010 .

[58]  James W. MacDonald,et al.  Elevated CO2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon (Oncorhynchus kisutch) , 2018, Global change biology.

[59]  B. L. Olla,et al.  The influence of hunger and predation risk on group cohesion in a pelagic fish, walleye pollock Theragra chalcogramma , 1997, Environmental Biology of Fishes.

[60]  G. Raby,et al.  Long-term exposure to elevated carbon dioxide does not alter activity levels of a coral reef fish in response to predator chemical cues , 2017, Behavioral Ecology and Sociobiology.

[61]  J. M. Cullen,et al.  Experiments on whether schooling by their prey affects the hunting behaviour of cephalopods and fish predators , 2009 .

[62]  G. Nilsson,et al.  Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function , 2012, Nature Climate Change.

[63]  M. Meekan,et al.  Putting prey and predator into the CO2 equation--qualitative and quantitative effects of ocean acidification on predator-prey interactions. , 2011, Ecology letters.