Effects of Ocean Acidification on Learning in Coral Reef Fishes

Ocean acidification has the potential to cause dramatic changes in marine ecosystems. Larval damselfish exposed to concentrations of CO2 predicted to occur in the mid- to late-century show maladaptive responses to predator cues. However, there is considerable variation both within and between species in CO2 effects, whereby some individuals are unaffected at particular CO2 concentrations while others show maladaptive responses to predator odour. Our goal was to test whether learning via chemical or visual information would be impaired by ocean acidification and ultimately, whether learning can mitigate the effects of ocean acidification by restoring the appropriate responses of prey to predators. Using two highly efficient and widespread mechanisms for predator learning, we compared the behaviour of pre-settlement damselfish Pomacentrus amboinensis that were exposed to 440 µatm CO2 (current day levels) or 850 µatm CO2, a concentration predicted to occur in the ocean before the end of this century. We found that, regardless of the method of learning, damselfish exposed to elevated CO2 failed to learn to respond appropriately to a common predator, the dottyback, Pseudochromis fuscus. To determine whether the lack of response was due to a failure in learning or rather a short-term shift in trade-offs preventing the fish from displaying overt antipredator responses, we conditioned 440 or 700 µatm-CO2 fish to learn to recognize a dottyback as a predator using injured conspecific cues, as in Experiment 1. When tested one day post-conditioning, CO2 exposed fish failed to respond to predator odour. When tested 5 days post-conditioning, CO2 exposed fish still failed to show an antipredator response to the dottyback odour, despite the fact that both control and CO2-treated fish responded to a general risk cue (injured conspecific cues). These results indicate that exposure to CO2 may alter the cognitive ability of juvenile fish and render learning ineffective.

[1]  R. Feely,et al.  Calcification and organic production on a Hawaiian coral reef , 2011 .

[2]  M. McCormick,et al.  Prey experience of predation influences mortality rates at settlement in a coral reef fish, Pomacentrus amboinensis , 2006 .

[3]  M. Hayashi,et al.  Fishes in high-CO 2 , acidified oceans , 2008 .

[4]  A. Wilson,et al.  Reintroduction of captive-born animals , 1994 .

[5]  J. LaRoche,et al.  Bioassays, batch culture and chemostat experimentation, Approaches and tools to manipulate the carbonate chemistry , 2010 .

[6]  Devra G. Kleiman,et al.  Reintroduction of Captive Mammals for Conservation Guidelines for reintroducing endangered species into the wild , 1989 .

[7]  Ulf Riebesell,et al.  Guide to best practices for ocean acidification research and data reporting , 2011 .

[8]  Lee Alan Dugatkin,et al.  Sexual Selection and Imitation: Females Copy the Mate Choice of Others , 1992, The American Naturalist.

[9]  P. Munday,et al.  Elevated carbon dioxide affects behavioural lateralization in a coral reef fish , 2012, Biology Letters.

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

[11]  R. Steneck,et al.  Coral Reefs Under Rapid Climate Change and Ocean Acidification , 2007, Science.

[12]  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.

[13]  A. S. Griffin,et al.  Social learning about predators: a review and prospectus , 2004, Learning & behavior.

[14]  L. Giraldeau,et al.  Social influences on foraging in vertebrates: causal mechanisms and adaptive functions , 2001, Animal Behaviour.

[15]  Corinne Le Quéré,et al.  Climate Change 2013: The Physical Science Basis , 2013 .

[16]  Morgan S. Pratchett,et al.  Climate change and the future for coral reef fishes , 2008 .

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

[18]  R. J. Smith,et al.  Foraging Trade‐offs in Fathead Minnows (Pimephales promelas, Osteichthyes, Cyprinidae): Acquired Predator Recognition in the Absence of an Alarm Response , 2010 .

[19]  Richard A. Feely,et al.  Impacts of ocean acidification on marine fauna and ecosystem processes , 2008 .

[20]  P. Munday,et al.  Ocean Acidification Affects Prey Detection by a Predatory Reef Fish , 2011, PloS one.

[21]  Marcel E Visser,et al.  Keeping up with a warming world; assessing the rate of adaptation to climate change , 2008, Proceedings of the Royal Society B: Biological Sciences.

[22]  J. Leis Behaviour as input for modelling dispersal of fish larvae: behaviour, biogeography, hydrodynamics, ontogeny, physiology and phylogeny meet hydrography , 2007 .

[23]  S. Shettleworth Animal cognition and animal behaviour , 2001, Animal Behaviour.

[24]  Arie J van Noordwijk,et al.  Evidence for the Effect of Learning on Timing of Reproduction in Blue Tits , 2002, Science.

[25]  E. Maier‐Reimer,et al.  Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms , 2005, Nature.

[26]  M. McCormick,et al.  Influence of prey body characteristics and performance on predator selection , 2009, Oecologia.

[27]  Louie H. Yang,et al.  Grand Challenges : Behavior as a Key Component of Integrative Biology in a Human-altered World , 2010 .

[28]  S. Simpson,et al.  Ocean acidification erodes crucial auditory behaviour in a marine fish , 2011, Biology Letters.

[29]  M. Meekan,et al.  Larval production drives temporal patterns of larval supply and recruitment of a coral reef damselfish , 1993 .

[30]  M. Hayashi,et al.  Fishes in high-CO2, acidified oceans , 2008 .

[31]  M. C. Ferrari,et al.  Coral Reef Fish Rapidly Learn to Identify Multiple Unknown Predators upon Recruitment to the Reef , 2011, PloS one.

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

[33]  J. Zachos,et al.  Rapid Acidification of the Ocean During the Paleocene-Eocene Thermal Maximum , 2005, Science.

[34]  W. Collins,et al.  Global climate projections , 2007 .

[35]  M. Meekan,et al.  Intrageneric variation in antipredator responses of coral reef fishes affected by ocean acidification: implications for climate change projections on marine communities , 2011 .

[36]  P. Barbosa,et al.  Ecology of Predator-Prey Interactions , 2005 .

[37]  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 .

[38]  M. Hayashi,et al.  Physiological effects on fishes in a high-CO2 world , 2005 .

[39]  G. Almany,et al.  The predation gauntlet: early post-settlement mortality in reef fishes , 2006, Coral Reefs.

[40]  K. Døving,et al.  Ocean acidification impairs olfactory discrimination and homing ability of a marine fish , 2009, Proceedings of the National Academy of Sciences.

[41]  C. Page,et al.  Ocean acidification due to increasing atmospheric carbon dioxide , 2005 .

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

[43]  G. Mace,et al.  Creative conservation: interactive management of wild and captive animals. , 1996 .

[44]  S. Wilson,et al.  A comparison of catches of fishes and invertebrates by two light trap designs, in tropical NW Australia , 2001 .

[45]  M. McCormick,et al.  Size-selectivity of predatory reef fish on juvenile prey , 2010 .

[46]  Denis Allemand,et al.  Impacts of ocean acidification on coral reefs and other marine calcifiers : a guide for future research , 2006 .

[47]  R. Woesik,et al.  Carbon dioxide flux and metabolic processes of a coral reef, Okinawa , 1999 .

[48]  A. Ridgwell,et al.  Sedimentary response to Paleocene-Eocene Thermal Maximum carbon release: A model-data comparison , 2008 .

[49]  P. Doherty Light-traps: selective but useful devices for quantifying the distributions and abundances of larval fishes , 1987 .

[50]  Gerald G Singh,et al.  Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. , 2010, Ecology letters.

[51]  Andrew J. Watson,et al.  Ocean acidification due to increasing atmospheric carbon dioxide , 2005 .

[52]  M. C. Ferrari,et al.  Evolution and behavioural responses to human-induced rapid environmental change , 2011, Evolutionary applications.

[53]  S. Dupont,et al.  Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? , 2009 .

[54]  D. Chivers,et al.  Chemical alarm signalling in aquatic predator-prey systems: A review and prospectus , 1998 .

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

[56]  P. Munday,et al.  Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. , 2010, Ecology letters.

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

[58]  Daniel T. Blumstein,et al.  Training Captive‐Bred or Translocated Animals to Avoid Predators , 2000 .