Marine Biology

, 163:243 | Cite as

Behavioural lateralization and shoaling cohesion of fish larvae altered under ocean acidification

  • A. F. Lopes
  • P. Morais
  • M. Pimentel
  • R. Rosa
  • P. L. Munday
  • E. J. Gonçalves
  • A. M. Faria
Original paper


Recent studies have shown that the behaviour and development of coral reef fish larvae is hampered by projected future CO2 levels. However, it is uncertain to what extent this effect also occurs in temperate species. The effects that elevated pCO2 (~2000 µatm) levels, which are expected to occur in coastal upwelling regions in the future, have on shoaling behaviour and lateralization (turning preference) of fish, were tested in temperate sand smelt Atherina presbyter larvae. The hypothesis that behavioural changes are caused by interference of high CO2 with GABA-A receptor function was tested by treating larvae with a receptor antagonist (gabazine). Routine swimming speed did not differ between control and high pCO2, but exposure to high pCO2 for 7 days affected group cohesion, which presented a more random distribution when compared to control fish. However, this random distribution was reversed after 21 days of exposure to high CO2 conditions. Lateralization at the individual level decreased in fish exposed to high pCO2 for 7 and 21 days, but gabazine reversed this decline. This adds to the growing body of evidence that the effects of a more acidified environment on fish larvae behaviour are likely due to altered function of GABA-A receptors. Overall, our results suggest that future pCO2 levels likely to occur in temperate coastal ecosystems could have an adverse effect on temperate larval fish behaviour.


Swimming Speed Ocean Acidification High pCO2 Near Neighbour Distance Elevated pCO2 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by the Project ACIDLARVAE (PTDC/MAR-EST/4627/2012), a postdoc Grant to AF (SFRH/BPD/68673/2010), and through the Pluriannual Program (PEst-OE/MAR/UI0331/2013), financed by Fundação para a Ciência e a Tecnologia. The authors would like to thank C. Quiles, D. Rodrigues, G. Franco, J. Castro and P. Coelho for support in the field. Thanks also to the four anonymous reviewers whose suggestions greatly improved a previous version of the manuscript.


This study was funded by Fundação para a Ciência e a Tecnologia through the Project ACIDLARVAE (PTDC/MAR-EST/4627/2012), a postdoc Grant to AF (SFRH/BPD/68673/2010), and the Pluriannual Program (PEst-OE/MAR/UI0331/2013).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All applicable national and institutional guidelines for the care and use of animals were followed.


  1. Allan BJM, Domenici P, McCormick MI, Watson SA, Munday PL (2013) Elevated CO2 affects predator-prey interactions through altered performance. PLoS ONE 8:e58520. doi: 10.1371/journal.pone.0058520 CrossRefGoogle Scholar
  2. Andersson A, Mackenzie F (2012) Ocean acidification: setting the record straight. Biogeosciences 9:893–905. doi: 10.5194/bgd-8-6161-2011 CrossRefGoogle Scholar
  3. Atkinson MJ, Bingman C (1997) Elemental composition of commercial seasalts. J Aquaric Aquat Sci VIII 2:39–43Google Scholar
  4. Bibost AL, Brown C (2013) Laterality influences schooling position in rainbowfish, Melanotaenia Spp. PloS ONE 8(11):e80907. doi: 10.1371/journal.pone.0080907 CrossRefGoogle Scholar
  5. Bignami S, Sponaugle S, Cowen RK (2013) Response to ocean acidification in larvae of a large tropical marine fish. Rachycentron canadum. Glob Change Biol 19(4):996–1006. doi: 10.1111/gcb.12133 CrossRefGoogle Scholar
  6. Bignami S, Sponaugle S, Cowen RK (2014) Effects of ocean acidification on the larvae of a high-value pelagic fisheries species, mahi-mahi Coryphaena hippurus. Aquat Biol 21:249–260. doi: 10.3354/ab00598 CrossRefGoogle Scholar
  7. Bisazza A, Dadda M (2005) Enhanced schooling performance in lateralized fishes. Proc R Soc B 272:1677–1681. doi: 10.1098/rspb.2005.3145 CrossRefGoogle Scholar
  8. Bisazza A, Rogers LJ, Vallortigara G (1998) The origins of cerebral asymmetry: a review of evidence of behavioural and brain lateralization in fishes, reptiles and amphibians. Neurosci Biobehav Rev 22(3):411–426. doi: 10.1016/S0149-7634(97)00050-X CrossRefGoogle Scholar
  9. Bisazza A, Cantalupo C, Capocchiano M, Vallortigara G (2000) Population lateralisation and social behaviour: a study with 16 species of fish. Laterality 5(3):269–284. doi: 10.1080/713754381 Google Scholar
  10. Borges AV, Gypens N (2010) Carbonate chemistry in the coastal zone responds more strongly to eutrophication than to ocean acidification. Limnol Oceanogr 55:346–353. doi: 10.4319/lo.2010.55.1.0346 CrossRefGoogle Scholar
  11. Brauner CJ, Baker DW (2009) Patterns of acid–base regulation during exposure to hypercarbia in fishes. In: Glass ML, Wood SC (eds) Cardio-respiratory control in vertebrates: comparative and evolutionary aspects, pp 43–63. Springer. Doi:  10.1007/978-3-540-93985-6_3
  12. Briffa M, De La Haye K, Munday PL (2012) High CO2 and marine animal behaviour: potential mechanisms and ecological consequences. Marine Pollut Bull 64:1519–1528. doi: 10.1016/j.marpolbul.2012.05.032 CrossRefGoogle Scholar
  13. Cabeçadas L, Oliveira AP (2005) Impact of a Coccolithus braarudii bloom on the carbonate system of Portuguese coastal waters. J Nannoplankton Res 27(2):141–147Google Scholar
  14. Cai WJ, Hu X, Huang WJ, Murrell MC, Lehrter JC, Lohrenz SE, Chou WC, Zhai W, Hollibaugh JT, Wang Y, Zhao P, Guo X, Gundersen K, Dai M, Gong GC (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nat Geosci 4:766–770. doi: 10.1038/ngeo1297 CrossRefGoogle Scholar
  15. Chivers PD, Dixson DL, White JR, McCormick MI, Ferrari MCO (2013) Degradation of chemical alarm cues and assessment of risk throughout the day. Ecol Evol 3(11):3925–3934. doi: 10.1002/ece3.760 CrossRefGoogle Scholar
  16. Chivers DP, McCormick MI, Nilsson GE, Munday PL, Watson SA, Meekan M, Mitchell MD, Corkill KC, Ferrari MCO (2014) Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference. Glob Change Biol 20(2):515–522. doi: 10.1111/gcb.12291 CrossRefGoogle Scholar
  17. Chung WS, Marshall NJ, Watson SA, Munday PL, Nilsson GE (2014) Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors. J Exp Biol 217(3):323–326. doi: 10.1242/jeb.092478 CrossRefGoogle Scholar
  18. Clark PJ, Evans FC (1954) Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35(4):445–453. doi: 10.2307/1931034 CrossRefGoogle Scholar
  19. Dadda M, Bisazza A (2006) Does brain asymmetry allow efficient performance of simultaneous tasks? Anim Behav 72:523–529. doi: 10.1016/j.anbehav.2005.10.019 CrossRefGoogle Scholar
  20. Dadda M, Koolhaas WH, Domenici P (2010) Behavioural asymmetry affects escape performance in a teleost fish. Biol Lett 6(3):414–417CrossRefGoogle Scholar
  21. Delcourt J, Poncin P (2012) Shoals and Schools: back to the heuristic definitions and quantitative references. Rev Fish Biol Fish 22:595–619. doi: 10.1098/rsbl.2009.0904 CrossRefGoogle Scholar
  22. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res 34:1733–1743. doi: 10.1016/0198-0149(87)90021-5 CrossRefGoogle Scholar
  23. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication, Sydney, p 3Google Scholar
  24. Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75. doi: 10.1111/j.1461-0248.2009.01400.x CrossRefGoogle Scholar
  25. Dlugokencky E, Tans P (2015) Trends in atmospheric carbon dioxide. National Oceanic and Atmosphere Administration, Earth System Research Laboratory (NOAA/ESRL).
  26. Domenici P, Allan BJM, McCormick MI, Munday PL (2012) Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biol Lett 8(1):78–81. doi: 10.1098/rsbl.2011.0591 CrossRefGoogle Scholar
  27. Domenici P, Allan BJM, Watson SA, McCormick MI, Munday PL (2014) Shifting from right to left: the combined effect of elevated CO2 and temperature on behavioural lateralization in a coral reef fish. PLoS ONE 9(1):e87969. doi: 10.1371/journal.pone.0087969 CrossRefGoogle Scholar
  28. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192. doi: 10.1146/annurev.marine.010908.163834 CrossRefGoogle Scholar
  29. 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. J Comp Physiol B 182(7):921–934. doi: 10.1007/s00360-012-0668-5 CrossRefGoogle Scholar
  30. Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B (2008) Evidence for upwelling of corrosive “Acidified” water onto the continental shelf. Science 320(5882):1490–1492. doi: 10.1111/j.1461-0248.2009.01400.x CrossRefGoogle Scholar
  31. Feely RA, Doney S, Cooley S, Greeley D (2010) Oceans acidification: present status and future conditions in a high-CO2 world. Oceanography 22(4):36–47. doi: 10.5670/oceanog.2009.95 CrossRefGoogle Scholar
  32. Ferrari MCO, Dixson DL, Munday PL, McCormick MI, Meekan MG, Sih A, Chivers DP (2011) Intrageneric variation in antipredator responses of coral reef fishes affected by ocean acidification: implications for climate change projections on marine communities. Glob Change Biol 17:2980–2986. doi: 10.1111/j.1365-2486.2011.02439.x CrossRefGoogle Scholar
  33. Forsgren E, Dupont S, Jutfelt F, Amundseen T (2013) Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish. Ecol Evol 3(11):3637–3646. doi: 10.1002/ece3.709 CrossRefGoogle Scholar
  34. Frommel AY, Schubert A, Piatkowski U, Clemmesen C (2012) Egg and early larval stages of Baltic Cod, Gadus Morhua, are robust to high levels of ocean acidification. Mar Biol 160(8):1825–1834. doi: 10.1007/s00227-011-1876-3 CrossRefGoogle Scholar
  35. Hamilton TJ, Holcombe A, Tresguerres M (2014) CO2-induced ocean acidification increases anxiety in Rockfish via alteration of GABAA receptor functioning. Proc R Soc B 281:20132509. doi: 10.1098/rspb.2013.2509 CrossRefGoogle Scholar
  36. Hofmann GE, Smith JE, Johnson KS, Send U, Micheli F, Paytan A, Price NN, Peterson B, Takeshita Y, Matson PG, Crook ED, Kroeker KJ, Martz TR (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6(12):e28983. doi: 10.1371/journal.pone.0028983 CrossRefGoogle Scholar
  37. Hurst TP, Fernandez ER, Mathis JT (2013) Effects of ocean acidification on hatch size and larval growth of walleye pollock (Theragra chalcogramma). ICES J Mar Sci 70(4):812–822. doi: 10.1093/icesjms/fst053 CrossRefGoogle Scholar
  38. Jutfelt F, Hedgärde M (2013) Atlantic cod actively avoid CO2 and predator odour, even after long-term CO2 exposure. Front Zool 10:81. doi: 10.1186/1742-9994-10-81 CrossRefGoogle Scholar
  39. Jutfelt F, Bresolin de Souza K, Vuylsteke A, Sturve J (2013) Behavioural disturbances in a temperate fish exposed to sustained high-CO2 levels. PLoS ONE 8(6):e65825. doi: 10.1371/journal.pone.0065825 CrossRefGoogle Scholar
  40. Lachkar Z (2014) Effects of upwelling increase on ocean acidification in the California and Canary Current systems. Geophys Res Lett 41(1):90–95. doi: 10.1002/2013GL058726 CrossRefGoogle Scholar
  41. Lai F, Jutfelt F, Nilsson GE (2015) Altered neurotransmitter function in CO2-exposed stickleback (Gasterosteus aculeatus): a temperate model species for ocean acidification research. Conserv Physiol 3(1):cov018. doi: 10.1093/conphys/cov018 CrossRefGoogle Scholar
  42. Lambert N, Grover L (1995) The mechanism of biphasic GABA responses. Science 269(5226):928–929. doi: 10.1126/science.7638614 CrossRefGoogle Scholar
  43. Maneja RH, Frommel AY, Browman HI, Clemmesen C, Geffen AJ, Folkvord A, Piatkowski U, Durif CMF, Bjelland R, Skiftesvik AB (2013) The swimming kinematics of larval Atlantic cod, Gadus morhua L., are resilient to elevated seawater pCO2. Mar Biol 160(8):1963–1972. doi: 10.1007/s00227-012-2054-y CrossRefGoogle Scholar
  44. Masuda R, Shoji J, Nakayama S, Tanaka M (2003) Development of schooling behavior in Spanish Mackerel Scomberomorus niphonius during early ontogeny. Fish Sci 69(4):772–776. doi: 10.1046/j.1444-2906.2003.00685.x CrossRefGoogle Scholar
  45. McElhany P, Busch DS (2012) Appropriate pCO2 treatments in ocean acidification experiments. Mar Biol 160:1807–1812. doi: 10.1007/s00227-012-2052-0 CrossRefGoogle Scholar
  46. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurements of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907. doi: 10.4319/lo.1973.18.6.0897 CrossRefGoogle Scholar
  47. Melzner F, Thomsen J, Koeve W, Oschlies A, Gutowska MA, Bange HW, Hansen HP, Körtzinger A (2013) Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar Biol 160:1875–1888. doi: 10.1007/s00227-012-1954-1 CrossRefGoogle Scholar
  48. Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Døving KB (2009a) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci USA 106(6):1848–1852. doi: 10.1073/pnas.0809996106 CrossRefGoogle Scholar
  49. Munday PL, Donelson JM, Dixson DL, Endo GGK (2009b) Effects of ocean acidification on the early life history of a tropical marine fish. Proc Biol Sci 276(1671):3275–3283. doi: 10.1098/rspb.2009.0784 CrossRefGoogle Scholar
  50. Munday PL, Dixson DL, Mccormick MI, Meekan M, Ferrari MCO, Chivers DP (2010) Replenishment of fish populations is threatened by ocean acidification. Proc Natl Acad Sci USA. 107(29):12930–12934. doi: 10.1073/pnas.1004519107 CrossRefGoogle Scholar
  51. Munday PL, Watson S-A, Chung W-S, Marshall NJ, Nilsson GE (2014) Response to ‘The importance of accurate CO2 dosing and measurement in ocean acidification studies’. J Exp Biol 217:1828–1829. doi: 10.1242/jeb.105890 CrossRefGoogle Scholar
  52. Munday PL, Welch M, Allan B, Watson S-A, McMahon S, McCormick MI (2016) Effects of elevated CO2 on predator avoidance behaviour by reef fishes is not altered by experimental test water. PeerJ 4:e2501. doi: 10.7717/peerj.2501 CrossRefGoogle Scholar
  53. Murray CS, Malvezzi A, Gobler CJ, Baumann H (2014) Offspring sensitivity to ocean acidification changes seasonally in a coastal marine fish. Mar Ecol Prog Ser 504:1–11. doi: 10.3354/meps10791 CrossRefGoogle Scholar
  54. Nakayama S, Masuda R, Tanaka M (2007) Onsets of schooling behavior and social transmission in Chub Mackerel Scomber Japonicus. Behav Ecol Sociobiol 61(9):1383–1390. doi: 10.1007/s00265-007-0368-4 CrossRefGoogle Scholar
  55. Nilsson GE, Dixson DL, Domenici P, McCormick MI, Sørensen C, Watson SA, Munday PL (2012) Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat Clim Change 2(3):201–204. doi: 10.1038/nclimate1352 CrossRefGoogle Scholar
  56. Pimentel M, Pegado M, Repolho T, Rosa R (2014) Impact of ocean acidification in the metabolism and swimming behavior of the dolphinfish (Coryphaena hippurus) early larvae. Mar Biol 161(3):725–729. doi: 10.1007/s00227-013-2365-7 CrossRefGoogle Scholar
  57. Pitcher TJ (1983) Heuristic definitions of fish shoaling behaviour. Anim Behav 31(2):611–613. doi: 10.1016/S0003-3472(83)80087-6 CrossRefGoogle Scholar
  58. Plaut I (2001) Critical swimming speed: its ecological relevance. Comp Biochem Physiol A Mol Integr Physiol 131(1):41–50. doi: 10.1016/S1095-6433(01)00462-7 CrossRefGoogle Scholar
  59. Pörtner HO, Karl DM, Boyd PW, Cheung WWL, Lluch-Cota SE, Nojiri Y, Schmidt DN, Zavialov PO (2014) Ocean systems. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD et al (eds) Climate change 2014: impacts, adaptation, and vulnerability part A: global and sectoral aspects contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 411–484Google Scholar
  60. R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0Google Scholar
  61. Reum JCP, Alin SR, Harvey CJ, Bednarsek N, Evans W, Feely RA, Hales B, Lucey N, Mathis JT, McElhany P, Newton J, Sabine CL (2015) Interpretation and design of ocean acidification experiments in upwelling systems in the context of carbonate chemistryco-variation with temperature and oxygen. ICES J Mar Sci. doi: 10.1093/icesjms/fsu231 Google Scholar
  62. Riebesell U, Fabry VJ, Hansson L, Gattuso JP (2010) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourg, p 260Google Scholar
  63. Rogers LJ, Andrew RJ (2002) Comparative vertebrate lateralization. Cambridge University Press, New York, p 655CrossRefGoogle Scholar
  64. Rogers LJ, Zucca P, Vallortigara G (2004) Advantages of having a lateralized brain. Proc Biol Sci 7(271):S420–S422. doi: 10.1098/rsbl.2004.0200 CrossRefGoogle Scholar
  65. Sarazin G, Michard G, Prevot F (1999) A rapid and accurate spectroscopic method for alkalinity measurements in sea water samples. Water Res 33:290–294. doi: 10.1016/S0043-1354(98)00168-7 CrossRefGoogle Scholar
  66. Shaw EC, Munday PL, McNeil BI (2013) The role of CO2 variability and exposure time for biological impacts of ocean acidification. Geophys Res Lett 40:4685–4688. doi: 10.1002/grl.50883 CrossRefGoogle Scholar
  67. 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. Biol Lett 7:917–920. doi: 10.1098/rsbl.2011.0293 CrossRefGoogle Scholar
  68. Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28(4):575–589. doi: 10.1017/S0140525X05000105 discussion 589–633 Google Scholar
  69. Waldbusser GG, Salisbury JE (2013) Ocean acidification in the coastal zone from an organism’s perspective: multiple system parameters, frequency domains, and habitats. Annu Rev Mar Sci 6:221–247. doi: 10.1146/annurev-marine-121211-172238 CrossRefGoogle Scholar
  70. Welch Megan J, Watson SA, Welsh JQ, McCormick MI, Munday PL (2014) Effects of elevated CO2 on fish behaviour undiminished by transgenerational acclimation. Nat Clim Change 4(12):1086–1089. doi: 10.1038/nclimate2400 CrossRefGoogle Scholar
  71. Whitehead PJP, Bauchot ML, Hureau JC, Nielsen EN, Tortonese E (1986) Fishes of the north-eastern Atlantic and the Mediterranean, vol I–III. UNESCO, Paris, p 1473Google Scholar
  72. Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, kinetics, isotopes. Oceanogr Ser 65:1–341CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.MARE – Marine and Environmental Sciences CentreISPA-Instituto UniversitárioLisbonPortugal
  2. 2.Institute of Vertebrate BiologyAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  3. 3.MARE – Marine and Environmental Sciences Centre, Laboratório Marítimo da GuiaFaculdade de Ciências da Universidade de LisboaCascaisPortugal
  4. 4.Australian Research Council Centre of Excellence for Coral Reef StudiesJames Cook UniversityCairnsAustralia

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