Impaired learning of predators and lower prey survival under elevated CO 2 : a consequence of neurotransmitter interference DOUGLAS P. CHIVERS*, MARK I. MCCORMICK † , GO ¨ RAN E. NILSSON ‡ , PHILIP L. MUNDAY † , SUE-ANN WATSON † , MARK G. MEEKAN § , MATTHEW D. MITCHELL † , KATHERINE C. CORKILL † andMAUD C. O. FERRARI ¶ *Department of Biology, University of Saskatchewan, Saskatoon, SK S7N 5E2, Canada, †ARC Centre of Excellence for Coral Reef Studies, School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia, ‡Programme for Physiology and Neurobiology, Department of Biosciences, University of Oslo, Oslo, NO 0316, Norway, §Australian Institute of Marine Science, UWA Ocean Sciences Centre (MO96), Crawley, WA Australia, ¶Department of Biomedical Sciences, WCVM, University of Saskatchewan, Saskatoon, SK S7W 5B4, Canada Abstract Ocean acidification is one of the most pressing environmental concerns of our time, and not surprisingly, we have seen a recent explosion of research into the physiological impacts and ecological consequences of changes in ocean chemistry. We are gaining considerable insights from this work, but further advances require greater integration across disciplines. Here, we showed that projected near-future CO 2 levels impaired the ability of damselfish to learn the identity of predators. These effects stem from impaired neurotransmitter function; impaired learning under ele- vated CO 2 was reversed when fish were treated with gabazine, an antagonist of the GABA-A receptor – a major inhibitory neurotransmitter receptor in the brain of vertebrates. The effects of CO 2 on learning and the link to neuro- transmitter interference were manifested as major differences in survival for fish released into the wild. Lower sur- vival under elevated CO 2 , as a result of impaired learning, could have a major influence on population recruitment. Keywords: CO 2 , GABA-A receptors, global change, learning, neurotransmitter, ocean acidification, predator recognition, survival Received 15 May 2013 and accepted 30 May 2013 Introduction Burning of fossil fuels, production of cement and large- scale land-use changes have resulted in the concentra- tion of carbon dioxide (CO 2 ) in the atmosphere rising at an unprecedented rate (Raupach et al., 2007; Peters et al., 2012). Atmospheric CO 2 now exceeds 395 ppm (Dlugokencky & Tans, 2013), higher than any time in the past 800 000 years (Luthi et al., 2008). If the current CO 2 emissions trajectory is maintained atmospheric CO 2 could exceed 900 ppm by the end of the century (Meinshausen et al., 2011). The amount of CO 2 dis- solved in the surface ocean is increasing in line with atmospheric CO 2 because of the equilibration of gas partial pressures at the air–sea interface (Doney, 2010). About 30% of the excess CO 2 produced since the indus- trial revolution has been absorbed by the oceans (Sabine et al., 2004). Carbon dioxide reacts with water to generate carbonic acid, bicarbonate and hydrogen ions, which increases the acidity of the water, a process known as ocean acidification. Moreover, increasing hydrogen ions bond with carbonate ions to form more bicarbonate, leading to a reduction in carbonate-ion sat- uration (Orr et al., 2005; Fabry et al., 2008). The net effect of the increased uptake of atmospheric CO 2 at the ocean surface is higher ocean pCO 2 , reduced seawater pH and a change in the concentration of carbonate and bicarbonate ions. Many fundamental biological processes, including metabolism, growth, calcification and reproduction are known to change when ocean chemistry changes (Fabry et al., 2008; Widdicombe & Spicer, 2008; Doney et al., 2009; Kroeker et al., 2010; Briffa et al., 2012) and a diver- sity of taxa are affected by ocean acidification (Fabry et al., 2008; Kroeker et al., 2010; Barry, 2011). In general, fishes have received less attention than other taxa, but damselfish, common on reefs around the world, are rapidly becoming a model system to study such effects. Recent studies show that exposure to elevated CO 2 causes fish to respond inappropriately to homing odours (Munday et al., 2009) and cues associated with predation, including predators odours and alarm cues (Dixson et al., 2010; Ferrari et al., 2011a). Fish exposed Correspondence: Douglas P. Chivers, tel. + 306 966 4419, fax + 306 966 4461, e-mail: doug.chivers@usask.ca © 2013 John Wiley & Sons Ltd 1 Global Change Biology (2013), doi: 10.1111/gcb.12291