Impaired learning of predators and lower prey survival under elevated CO2: A consequence of neurotransmitter interference

Global Change Biology

Volumn 20, Issue 2, 2014, Pages 515-522

  Chivers, Douglas P ^a   Mccormick, Mark I ^b   Nilsson, Göran E ^c   Munday, Philip L ^b   Watson, Sue Ann ^b   Meekan, Mark G ^d   Mitchell, Matthew D ^b   Corkill, Katherine C ^b   Ferrari, Maud C O ^e  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b JAMES COOK UNIVERSITY   (Australia)

^c UNIVERSITY OF OSLO   (Norway)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

CO2; GABA A receptors; Global change; Learning; Neurotransmitter; Ocean acidification; Predator recognition; Survival

Indexed keywords

ACIDIFICATION; CARBON DIOXIDE; GLOBAL CHANGE; LEARNING; PHYSIOLOGY; PREDATOR-PREY INTERACTION; RECRUITMENT (POPULATION DYNAMICS); SURVIVAL;

POMACENTRIDAE; VERTEBRATA;

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CARBON DIOXIDE; NEUROTRANSMITTER; PYRIDAZINE DERIVATIVE;

ANIMAL; ARTICLE; AUSTRALIA; CORAL REEF; DRUG ANTAGONISM; DRUG EFFECT; FISH; FOOD CHAIN; GABA-A RECEPTORS; GLOBAL CHANGE; LEARNING; LONGEVITY; OCEAN ACIDIFICATION; PHYSIOLOGY; PREDATOR RECOGNITION; SURVIVAL;

CO2; GABA-A RECEPTORS; GLOBAL CHANGE; LEARNING; NEUROTRANSMITTER; OCEAN ACIDIFICATION; PREDATOR RECOGNITION; SURVIVAL;

ANIMALS; AUSTRALIA; CARBON DIOXIDE; CORAL REEFS; FISHES; FOOD CHAIN; GABA-A RECEPTOR ANTAGONISTS; LEARNING; LONGEVITY; NEUROTRANSMITTER AGENTS; PYRIDAZINES;

EID: 84891663218     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.12291     Document Type: Article

References (49)

1. Almany GR, Webster MS (2006) The predation gauntlet: early post-settlement mortality in reef fishes. Coral Reefs, 25, 19-22.
2. Barry JP, Widdicombe S, Hall-Spencer JM (eds) (2011) Effects of Ocean Acidification on Marine Biodiversity and Ecosystem Function. Oxford University Press, Oxford.
3. Brauner CJ, Baker DW (2009) Patterns of acid-base regulation during exposure to hypercarbia in fishes. In: Cardio-Respiratory Control in Vertebrates: Comparative and Evolutionary Aspects (eds Glass ML, Wood SC), pp. 43-63. Springer, Berlin.
4. 2 and marine animal behaviour: potential mechanisms and ecological consequences. Marine Pollution Bulletin, 64, 1519-1528.
5. Brown GE, Smith JF (1998) Acquired predator recognition in juvenile rainbow trout (Oncorhynchus mykiss): conditioning hatchery-reared fish to recognize chemical cues of a predator. Canadian Journal of Fisheries and Aquatic Sciences, 55, 611-617.
6. Chivers DP, Smith RJF (1994) The role of experience and chemical alarm signaling in predator recognition by fathead minnows, Pimephales promelas. Journal of Fish Biology, 44, 273-285.
7. Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience, 5, 338-352.
8. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research, 34, 1733-1743.
9. Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecology Letters, 13, 68-75.
10. Dlugokencky E, Tans P (2013) Trends in atmospheric carbon dioxide. Available at: http://www.esrl.noaa.gov/gmd/ccgg/trends/ (accessed 6 May 2013).
11. Domenici P, Allan B, McCormick MI, Munday PL (2012) Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biology Letters, 8, 78-81.
12. Doney SC (2010) The growing human footprint on coastal and open-ocean biogeochemistry. Science, 328, 1512-1516.
13. 2 problem. Annual Review of Marine Science, 1, 169-192.
14. Esbaugh AJ, Heuer R, Grosell M (2012) Impacts of ocean acidification on respiratory gas exchange and acid-base balance in a marine teleost, Opsanus beta. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 182, 921-934.
15. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. Ices Journal of Marine Science, 65, 414-432.
16. Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Canadian Journal of Zoology, 88, 698-724.
17. Ferrari MCO, Dixson DL, Munday PL, McCormick MI, Meekan MG, Sih A, Chivers DP (2011a) Intrageneric variation in antipredator responses of coral reef fishes affected by ocean acidification: implications for climate change projections on marine communities. Global Change Biology, 17, 2980-2986.
18. 2 equation - qualitative and quantitative effects of ocean acidification on predator-prey interactions. Ecology Letters, 14, 1143-1148.
19. Ferrari MCO, Manassa RP, Dixson DL et al. (2012a) Effects of ocean acidification on learning in coral reef fishes. PLoS ONE, 7, e31478.
20. Ferrari MCO, McCormick MI, Munday PL, Meekan MG, Dixson DL, Lonnstedt O, Chivers DP (2012b) Effects of ocean acidification on visual risk assessment in coral reef fishes. Functional Ecology, 26, 553-558.
21. Gagliano M, McCormick MI, Moore JA, Depczynski M (2010) The basics of acidification: baseline variability of pH on Australian coral reefs. Marine Biology, 157, 1849-1856.
22. Gattuso J-P, Gao K, Lee K, Rost B, Schulz KG (2010) Approaches and tools to manipulate the carbonate chemistry. In: Guide to Best Practices for Ocean Acidification Research and Data Reporting, (eds Riebesell U, Fabry VJ, Hansson L, Gattuso J-P), pp. 41-52. European Union, Luxembourg.
23. Hoey AS, McCormick MI (2004) Selective predation for low body condition at the larval-juvenile transition of a coral reef fish. Oecologia, 139, 23-29.
24. 2, acidified oceans. Marine Ecology-Progress Series, 373, 295-302.
25. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters, 13, 1419-1434.
26. Larson JK, McCormick MI (2005) The role of chemical alarm signals in facilitating learned recognition of novel chemical cues in a coral reef fish. Animal Behaviour, 69, 51-57.
27. Lonnstedt OM, McCormick MI, Meekan MG, Ferrari MCO, Chivers DP (2012) Learn and live: predator experience and feeding history determines prey behaviour and survival. Proceedings of the Royal Society B-Biological Sciences, 279, 2091-2098.
28. Luthi D, Le Floch M, Bereiter B et al. (2008) High-resolution carbon dioxide concentration record 650, 000-800, 000 years before present. Nature, 453, 379-382.
29. McCormick MI (2009) Behaviourally mediated phenotypic selection in a disturbed coral reef environment. PLoS ONE, 4, 1-8.
30. Meekan MG, Wilson SG, Halford A, Retzel A (2001) A comparison of catches of fishes and invertebrates by two light trap designs, in tropical NW Australia. Marine Biology, 139, 373-381.
31. Meinshausen M, Smith SJ, Calvin K et al. (2011) The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Climatic Change, 109, 213-241.
32. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurements of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography, 18, 897-907.
33. Mitchell MD, McCormick MI, Ferrari MCO, Chivers DP (2011a) Coral reef fishes rapidly learn to identify multiple unknown predators upon recruitment to the reefs. PLoS ONE, 6, e15764.
34. Mitchell MD, McCormick MI, Ferrari MCO, Chivers DP (2011b) Friend or foe? The role of latent inhibition in predator and non-predator labelling by coral reef fishes. Animal Cognition, 14, 707-714.
35. Munday PL, Wilson SK (1997) Comparative efficacy of clove oil and other chemicals in anaesthetization of Pomacentrus amboinensis, a coral reef fish. Journal of Fish Biology, 51, 931-938.
36. Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Doving KB (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proceedings of the National Academy of Sciences of the United States of America, 106, 1848-1852.
37. Munday PL, Dixson DL, McCormick MI, Meekan M, Ferrari MCO, Chivers DP (2010) Replenishment of fish populations is threatened by ocean acidification. Proceedings of the National Academy of Sciences of the United States of America, 107, 12930-12934.
38. 2 levels on coral reef fishes: what hope for the future? Journal of Experimental Biology, 215, 3865-3873.
39. 2 levels alter fish behaviour by interfering with neurotransmitter function. Nature Climate Change, 2, 201-204.
40. 2 system calculations. In: ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US. Department of Energy, Oak Ridge, TN, USA.
41. Ohde S, Van Woesik R (1999) Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bulletin of Marine Science, 65, 559-576.
42. Orr JC, Fabry VJ, Aumont O et al. (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature, 437, 681-686.
43. 2 emissions after the 2008-2009 global financial crisis. Nature Climate Change, 2, 2-4.
44. 2 emissions. Proceedings of the National Academy of Sciences of the United States of America, 104, 10288-10293.
45. 2. Science, 305, 367-371.
46. Shamberger KEF, Feely RA, Sabine CL et al. (2011) Calcification and organic production on a Hawaiian coral reef. Marine Chemistry, 127, 64-75.
47. 2 conditions. Global Change Biology, 19, 1632-1641.
48. Simpson SD, Munday PL, Wittenrich ML, Manassa R, Dixson DL, Gagliano M, Yan HY (2011) Ocean acidification erodes crucial auditory behaviour in a marine fish. Biology Letters, 7, 917-920.
49. Widdicombe S, Spicer JI (2008) Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? Journal of Experimental Marine Biology and Ecology, 366, 187-197.