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Methods matter in repeating ocean acidification studies

Nature volume 586, pages E20–E24 (2020)Cite this article

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Matters Arising to this article was published on 21 October 2020

The Original Article was published on 08 January 2020

arising from T. D. Clark et al. Nature https://doi.org/10.1038/s41586-019-1903-y (2020)

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Fig. 1: Diagram describing the lines of evidence supporting an effect of elevated CO2 on fish behaviour.

Data availability

Water temperature data at 0.6 m for Lizard Island reported in the Supplementary Information were obtained from the publicly available database maintained by the Australian Institute of Marine Science (AIMS) at http:weather.aims.gov.au/#/station1166. Additional materials are available at https://doi.org/10.25903/7rz7-4640.

Code availability

No custom code was used in extracting or using the water temperature data from the AIMS database.

References

  1. Clark, T. D. et al. Ocean acidification does not impair the behaviour of coral reef fishes. Nature 577, 370–375 (2020).

    ADS  CAS  PubMed  Google Scholar 

  2. Munday, P. L., Jarrold, M. D. & Nagelkerken, I. in Fish Physiology: Carbon Dioxide Vol. 37 (eds Grosell, M. et al.) 323–368 (Elsevier, 2019).

  3. Munday, P. L. et al. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc. Natl Acad. Sci. USA 106, 1848–1852 (2009).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. Munday, P. L. et al. Replenishment of fish populations is threatened by ocean acidification. Proc. Natl Acad. Sci. USA 107, 12930–12934 (2010).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  5. Dixson, D. L., Munday, P. L. & Jones, G. P. Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol. Lett. 13, 68–75 (2010).

    PubMed  Google Scholar 

  6. Munday, P. L. et al. Effects of elevated CO2 on predator avoidance behaviour by reef fishes is not altered by experimental test water. PeerJ 4, e2501 (2016).

    PubMed  PubMed Central  Google Scholar 

  7. Jarrold, M. D., Humphrey, C., McCormick, M. I. & Munday, P. L. Diel CO2 cycles reduce severity of behavioural abnormalities in coral reef fish under ocean acidification. Sci. Rep. 7, 10153 (2017).

    ADS  PubMed  PubMed Central  Google Scholar 

  8. McMahon, S. J., Donelson, J. M. & Munday, P. L. Food ration does not influence the effect of elevated CO2 on antipredator behaviour of a reef fish. Mar. Ecol. Prog. Ser. 586, 155–165 (2018).

    ADS  CAS  Google Scholar 

  9. Munday, P. L., Cheal, A. J., Dixson, D. L., Rummer, J. L. & Fabricius, K. E. Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps. Nat. Clim. Change 4, 487–492 (2014).

    Article  ADS  CAS  Google Scholar 

  10. Ferrari, M. C. O. et al. Predation in high CO2 waters: prey fish from high-risk environments are less susceptible to ocean acidification. Integr. Comp. Biol. 57, 55–62 (2017).

    CAS  PubMed  Google Scholar 

  11. Ferrari, M. C. O. et al. 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 (2011).

    ADS  Google Scholar 

  12. Welch, M. J., Watson, S.-A., Welsh, J. Q., McCormick, M. I. & Munday, P. L. Effects of elevated CO2 on fish behaviour undiminished by transgenerational acclimation. Nat. Clim. Change 4, 1086–1089 (2014).

    ADS  CAS  Google Scholar 

  13. Ferrari, M. C. O., Wisenden, B. D. & Chivers, D. P. Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. Can. J. Zool. 88, 698–724 (2010).

    Google Scholar 

  14. Ferrari, M. C. O. et al. Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities. Glob. Change Biol. 21, 1848–1855 (2015).

    ADS  Google Scholar 

  15. Kats, L. B. & Dill, L. M. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5, 361–394 (1998).

    Google Scholar 

  16. Roggatz, C. C., Lorch, M., Hardege, J. D. & Benoit, D. M. Ocean acidification affects marine chemical communication by changing structure and function of peptide signalling molecules. Glob. Change Biol. 22, 3914–3926 (2016).

    ADS  Google Scholar 

  17. Jutfelt, F., Sundin, J., Raby, G. D., Krång, A.-S. & Clark, T. D. Two-current choice flumes for testing avoidance and preference in aquatic animals. Methods Ecol. Evol. 8, 379–390 (2017).

    Google Scholar 

  18. Domenici, P., Allan, B., McCormick, M. I. & Munday, P. L. Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biol. Lett. 8, 78–81 (2012).

    CAS  PubMed  Google Scholar 

  19. Domenici, P., Allan, B. J. M., Watson, S.-A., McCormick, M. I. & Munday, P. L. Shifting from right to left: the combined effect of elevated CO2 and temperature on behavioural lateralization in a coral reef fish. PLoS ONE 9, e87969 (2014).

    ADS  PubMed  PubMed Central  Google Scholar 

  20. Nilsson, G. E. et al. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat. Clim. Change 2, 201–204 (2012).

    ADS  CAS  Google Scholar 

  21. Ferrari, M. C. O. et al. Effects of ocean acidification on visual risk assessment in coral reef fishes. Funct. Ecol. 26, 553–558 (2012).

    Google Scholar 

  22. Chung, W. S., Marshall, N. J., Watson, S.-A., Munday, P. L. & Nilsson, G. E. Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors. J. Exp. Biol. 217, 323–326 (2014).

    CAS  PubMed  Google Scholar 

  23. Welch, M. & Munday, P. L Raw Data for Olfactory Response of Acanthochromis polyacanthus in a Y-maze Flume (dataset). https://doi.org/10.4225/28/5add60af3a267 (James Cook University, 2018).

  24. Schunter, C. et al. Molecular signatures of transgenerational response to ocean acidification in a species of reef fish. Nat. Clim. Change 6, 1014–1018 (2016).

    ADS  CAS  Google Scholar 

  25. Allan, B. J. M., Miller, G. M., McCormick, M. I., Domenici, P. & Munday, P. L. Parental effects improve escape performance of juvenile reef fish in a high-CO2 world. Proc. R. Soc. Lond. B 281, 20132179 (2014).

    Google Scholar 

  26. Welch, M. J. & Munday, P. L. Heritability of behavioural tolerance to high CO2 in a coral reef fish is masked by nonadaptive phenotypic plasticity. Evol. Appl. 10, 682–693 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Stiasny, M. H. et al. Ocean acidification effects on Atlantic cod larval survival and recruitment to the fished population. PLoS ONE 11, e0155448 (2016).

    PubMed  PubMed Central  Google Scholar 

  28. Murray, C. S., Wiley, D. & Baumann, H. High sensitivity of a keystone forage fish to elevated CO2 and temperature. Conserv. Physiol. 7, coz084 (2019).

    PubMed  PubMed Central  Google Scholar 

  29. Munday, P. L. et al. Elevated CO2 affects the behavior of an ecologically and economically important coral reef fish. Mar. Biol. 160, 2137–2144 (2013).

    CAS  Google Scholar 

  30. Allan, B. J. M., Domenici, P., McCormick, M. I., Watson, S.-A. & Munday, P. L. Elevated CO2 affects predator–prey interactions through altered performance. PLoS ONE 8, e58520 (2013).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  31. Benítez, S. et al. Intertidal pool fish Girella laevifrons (Kyphosidae) shown strong physiological homeostasis but shy personality: the cost of living in hypercapnic habitats. Mar. Pollut. Bull. 118, 57–63 (2017).

    PubMed  Google Scholar 

  32. Borges, F. O. et al. Ocean warming and acidification may challenge the riverward migration of glass eels. Biol. Lett. 15, 20180627 (2019).

    PubMed  PubMed Central  Google Scholar 

  33. Castro, J. M. et al. Painted goby larvae under high-CO2 fail to recognize reef sounds. PLoS ONE 12, e0170838 (2017).

    PubMed  PubMed Central  Google Scholar 

  34. Chivers, D. P. et al. Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference. Glob. Change Biol. 20, 515–522 (2014).

    ADS  Google Scholar 

  35. Ferrari, M. C. O. et al. Putting prey and predator into the CO2 equation—qualitative and quantitative effects of ocean acidification on predator–prey interactions. Ecol. Lett. 14, 1143–1148 (2011).

    PubMed  Google Scholar 

  36. Forsgren, E., Dupont, S., Jutfelt, F. & Amundsen, T. Elevated CO2 affects embryonic development and larval phototaxis in a temperate marine fish. Ecol. Evol. 3, 3637–3646 (2013).

    PubMed  PubMed Central  Google Scholar 

  37. Goldenberg, S. U. et al. Ecological complexity buffers the impacts of future climate on marine consumers. Nat. Clim. Change 8, 229–233 (2018).

    ADS  Google Scholar 

  38. Green, L. & Jutfelt, F. Elevated carbon dioxide alters the plasma composition and behaviour of a shark. Biol. Lett. 10, 20140538 (2014).

    PubMed  PubMed Central  Google Scholar 

  39. Hamilton, T. J., Holcombe, A. & Tresguerres, M. CO2-induced ocean acidification increases anxiety in rockfish via alteration of GABAA receptor functioning. Proc. R. Soc. B 281, 20132509 (2014).

    PubMed  PubMed Central  Google Scholar 

  40. Heuer, R. M., Welch, M. J., Rummer, J. L., Munday, P. L. & Grosell, M. Altered brain ion gradients following compensation for elevated CO2 are linked to behavioural alterations in a coral reef fish. Sci. Rep. 6, 33216 (2016).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hurst, T. P. et al. Elevated CO2 alters behavior, growth, and lipid composition of Pacific cod larvae. Mar. Environ. Res. 145, 52–65 (2019).

    CAS  PubMed  Google Scholar 

  42. Jiahuan, R. et al. Ocean acidification impairs foraging behavior by interfering with olfactory neural signal transduction in black sea bream, Acanthopagrus schlegelii. Front. Physiol. 9, 1592 (2018).

    PubMed  PubMed Central  Google Scholar 

  43. Jutfelt, F., Bresolin de Souza, K., Vuylsteke, A. & Sturve, J. Behavioural disturbances in a temperate fish exposed to sustained high-CO2 levels. PLoS ONE 8, e65825 (2013).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  44. Lai, F., Jutfelt, F. & Nilsson, G. E. Altered neurotransmitter function in CO2-exposed stickleback (Gasterosteus aculeatus): a temperate model species for ocean acidification research. Conserv. Physiol. 3, cov018 (2015).

    PubMed  PubMed Central  Google Scholar 

  45. Laubenstein, T. D., Rummer, J. L., McCormick, M. I. & Munday, P. L. A negative correlation between behavioural and physiological performance under ocean acidification and warming. Sci. Rep. 9, 4265 (2019).

    ADS  PubMed  PubMed Central  Google Scholar 

  46. Lopes, A. F. et al. Behavioural lateralization and shoaling cohesion of fish larvae altered under ocean acidification. Mar. Biol. 163, 243 (2016).

    Google Scholar 

  47. Maulvault, A. L. et al. Differential behavioural responses to venlafaxine exposure route, warming and acidification in juvenile fish (Argyrosomus regius). Sci. Total Environ. 634, 1136–1147 (2018).

    ADS  CAS  PubMed  Google Scholar 

  48. McCormick, M. I., Watson, S.-A. & Munday, P. L. Ocean acidification reverses competition for space as habitats degrade. Sci. Rep. 3, 3280 (2013).

    PubMed  PubMed Central  Google Scholar 

  49. Munday, P. L. et al. Selective mortality associated with variation in CO2 tolerance in a marine fish. Ocean Acidif. 1, 1–5 (2012).

    Google Scholar 

  50. Nadler, L. E., Killen, S. S., McCormick, M. I., Watson, S.-A. & Munday, P. L. Effect of elevated carbon dioxide on shoal familiarity and metabolism in a coral reef fish. Conserv. Physiol. 4, cow052 (2016).

    PubMed  PubMed Central  Google Scholar 

  51. Näslund, J., Lindstrom, E., Lai, F. & Jutfelt, F. Behavioural responses to simulated bird attacks in marine three-spined sticklebacks after exposure to high CO2 levels. Mar. Freshw. Res. 66, 877–885 (2015).

    Google Scholar 

  52. Ou, M. et al. Responses of pink salmon to CO2-induced aquatic acidification. Nat. Clim. Change 5, 950–955 (2015).

    ADS  CAS  Google Scholar 

  53. Paula, J. R. et al. Neurobiological and behavioural responses of cleaning mutualisms to ocean warming and acidification. Sci. Rep. 9, 12728 (2019).

    ADS  PubMed  PubMed Central  Google Scholar 

  54. Paula, J. R. et al. The past, present and future of cleaner fish cognitive performance as a function of CO2 levels. Biol. Lett. 15, 20190618 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Porteus, C. S. et al. Near-future CO2 levels impair the olfactory system of a marine fish. Nat. Clim. Change 8, 737–743 (2018).

    ADS  CAS  Google Scholar 

  56. Pistevos, J. C. A., Nagelkerken, I., Rossi, T., Olmos, M. & Connell, S. D. Ocean acidification and global warming impair shark hunting behaviour and growth. Sci. Rep. 5, 16293 (2015).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  57. Regan, M. D. et al. Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels. J. Exp. Biol. 219, 109–118 (2016).

    PubMed  Google Scholar 

  58. Rossi, T., Nagelkerken, I., Pistevos, J. C. A. & Connell, S. D. Lost at sea: ocean acidification undermines larval fish orientation via altered hearing and marine soundscape modification. Biol. Lett. 12, 20150937 (2016).

    PubMed  PubMed Central  Google Scholar 

  59. Rossi, T., Pistevos, J. C. A., Connell, S. D. & Nagelkerken, I. On the wrong track: ocean acidification attracts larval fish to irrelevant environmental cues. Sci. Rep. 8, 5840 (2018).

    ADS  PubMed  PubMed Central  Google Scholar 

  60. Schmidt, M. et al. Impact of ocean warming and acidification on the behaviour of two co-occurring gadid species, Boreogadus saida and Gadus morhua, from Svalbard. Mar. Ecol. Prog. Ser. 571, 183–191 (2017).

    ADS  CAS  Google Scholar 

  61. Schunter, C. et al. An interplay between plasticity and parental phenotype determines impacts of ocean acidification on a reef fish. Nat. Ecol. Evol. 2, 334–342 (2018).

    PubMed  Google Scholar 

  62. Simpson, S. D. et al. Ocean acidification erodes crucial auditory behaviour in a marine fish. Biol. Lett. 7, 917–920 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Sundin, J. & Jutfelt, F. 9–28 d of exposure to elevated pCO2 reduces avoidance of predator odour but had no effect on behavioural lateralization or swimming activity in a temperate wrasse (Ctenolabrus rupestris). ICES J. Mar. Sci. 73, 620–632 (2016).

    Google Scholar 

  64. Sundin, J. & Jutfelt, F. Effects of elevated carbon dioxide on male and female behavioural lateralization in a temperate goby. R. Soc. Open Sci. 5, 171550 (2018).

    ADS  PubMed  PubMed Central  Google Scholar 

  65. Devine, B. M. & Munday, P. L. Habitat preferences of coral-associated fishes are altered by short-term exposure to elevated CO2. Mar. Biol. 160, 1955–1962 (2013).

    CAS  Google Scholar 

  66. Velez, Z., Roggatz, C. C., Benoit, D. M., Hardege, J. D. & Hubbard, P. C. Short- and medium-term exposure to ocean acidification reduces olfactory sensitivity in gilthead seabream. Front. Physiol. 10, 731 (2019).

    PubMed  PubMed Central  Google Scholar 

  67. Williams, C. R. et al. Elevated CO2 impairs olfactory-mediated neural and behavioral responses and gene expression in ocean-phase coho salmon (Oncorhynchus kisutch). Glob. Change Biol. 25, 963–977 (2019).

    ADS  Google Scholar 

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Author information

Authors and Affiliations

  1. Australian Research Council Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland, Australia

    Philip L. Munday, Megan J. Welch, Geoffrey P. Jones, Mark I. McCormick & Sue-Ann Watson

  2. School of Marine Science and Policy, University of Delaware, Lewes, DE, USA

    Danielle L. Dixson

  3. Department of Biology, University of Saskatchewan, Saskatoon, Saskatchewan, Canada

    Douglas P. Chivers

  4. Istituto per lo studio degli impatti Antropici e Sostenibilità in ambiente marino, Consiglio Nazionale delle Ricerche, IAS-CNR, Oristano, Italy

    Paolo Domenici

  5. Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL, USA

    Martin Grosell & Rachael M. Heuer

  6. College of Science and Engineering, James Cook University, Townsville, Queensland, Australia

    Geoffrey P. Jones

  7. Australian Institute of Marine Science, IOMRC, Crawley, Western Australia, Australia

    Mark Meekan

  8. Section for Physiology and Cell Biology, Department of Biosciences, University of Oslo, Oslo, Norway

    Göran E. Nilsson

  9. Marine Climate Change Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan

    Timothy Ravasi

  10. Biodiversity and Geosciences Program, Museum of Tropical Queensland, Queensland Museum, Townsville, Queensland, Australia

    Sue-Ann Watson

Authors
  1. Philip L. Munday
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  2. Danielle L. Dixson
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Contributions

P.L.M. wrote the first version with input from D.L.D. and P.D. All authors edited and contributed to the final version.

Corresponding author

Correspondence to Philip L. Munday.

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Supplementary information

Supplementary Table 1

| Published studies testing the effects of elevated CO2 on fish behaviour to end of 2019 Studies are scored as showing significant effects (YES) or not (NO). YES/NO indicates that a significant effect of elevated CO2 was detected for one or more behaviour(s), but not one or more other behaviour(s), or that significant effects of elevated CO2 on a behaviour were absent when another ecological factor (e.g. predation risk, habitat type, parental or developmental effects, diel CO2 cycles) was cross-factored with elevated CO2. The study number matches reference numbers (in parentheses) in Figure 1. Highlighted section indicates papers by authors of Clark et al. 2020.

Supplementary Information

This file contains Supplementary information about the experimental control of elevated CO2, including minimum, maximum and within-day range of pCO2 (µatm) in the experiments conducted by Clark et al. 2020 at Lizard Island Research Station in 2016; and Supplementary Table 2: Inadequate control of elevated CO2 treatments in Clark et al. 2020.

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Munday, P.L., Dixson, D.L., Welch, M.J. et al. Methods matter in repeating ocean acidification studies. Nature 586, E20–E24 (2020). https://doi.org/10.1038/s41586-020-2803-x

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