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Near-future CO2 levels impair the olfactory system of a marine fish

Nature Climate Change volume 8, pages 737–743 (2018)Cite this article

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Abstract

Survival of marine fishes that are exposed to elevated near-future CO2 levels is threatened by their altered responses to sensory cues. Here we demonstrate a physiological and molecular mechanism in the olfactory system that helps to explain altered behaviour under elevated CO2. We combine electrophysiology measurements and transcriptomics with behavioural experiments to investigate how elevated CO2 affects the olfactory system of European sea bass (Dicentrarchus labrax). When exposed to elevated CO2 (approximately 1,000 µatm), fish must be up to 42% closer to an odour source for detection, compared with current CO2 levels (around 400 µatm), decreasing their chances of detecting food or predators. Compromised olfaction correlated with the suppression of the transcription of genes involved in synaptic strength, cell excitability and wiring of the olfactory system in response to sustained exposure to elevated CO2 levels. Our findings complement the previously proposed impairment of γ-aminobutyric acid receptors, and indicate that both the olfactory system and central brain function are compromised by elevated CO2 levels.

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Fig. 1: Behaviour responses of European sea bass (D. labrax) to a 5-min exposure to a predator odour (monkfish bile).
Fig. 2: Elevated CO2 decreases the olfactory sensitivity of European sea bass to amino acids, bile acids and body fluids.
Fig. 3: Acute exposure of European seabass to elevated CO2 (around 1,000 µatm) decreases the amplitude of the olfactory response and increases the detection threshold of several odorants tested.
Fig. 4: Differential regulation of genes in the olfactory epithelium and olfactory lobe of European sea bass exposed to control and high CO2.
Fig. 5: Proposed mechanism of action of CO2-induced ocean acidification on fish behaviour via the olfactory pathway.

References

  1. Velez, Z. et al. Identification, release and olfactory detection of bile salts in the intestinal fluid of the Senegalese sole (Solea senegalensis). J. Comp. Physiol. A 195, 691–698 (2009).

    Google Scholar 

  2. Yacoob, S. Y. & Browman, H. I. Olfactory and gustatory sensitivity to some feed-related chemicals in the Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 263, 303–309 (2007).

    CAS  Google Scholar 

  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).

    CAS  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).

    CAS  Google Scholar 

  5. Yambe, H. et al. L-kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon. Proc. Natl Acad. Sci. USA 103, 15370–15374 (2006).

    CAS  Google Scholar 

  6. Arvedlund, M., McCormick, M. I., Fautin, D. G. & Bildsøe, M. Host recognition and possible imprinting in the anemonefish Amphiprion melanopus (Pisces: Pomacentridae). Mar. Ecol. Prog. Ser. 188, 207–218 (1999).

    Google Scholar 

  7. Arvedlund, M. & Takemura, A. The importance of chemical environmental cues for juvenile Lethrinus nebulosus Forsskål (Lethrinidae, Teleostei) when settling into their first benthic habitat. J. Exp. Mar. Biol. Ecol. 338, 112–122 (2006).

    CAS  Google Scholar 

  8. Atema, J., Kingsford, M. J. & Gerlach, G. Larval reef fish could use odour for detection, retention and orientation to reefs. Mar. Ecol. Prog. Ser. 241, 151–160 (2002).

    Google Scholar 

  9. Gerlach, G., Atema, J., Kingsford, M. J., Black, K. P. & Miller-Sims, V. Smelling home can prevent dispersal of reef fish larvae. Proc. Natl Acad. Sci. USA 104, 858–863 (2007).

    CAS  Google Scholar 

  10. Vrieze, L. A. & Sorensen, P. W. Laboratory assessment of the role of a larval pheromone and natural stream odor in spawning stream localization by migratory sea lamprey (Petromyzon marinus). Can. J. Fish. Aquat. Sci. 58, 2374–2385 (2001).

    Google Scholar 

  11. 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).

    Google Scholar 

  12. 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).

    CAS  Google Scholar 

  13. Ferrari, M. C. O. et al. Effects of ocean acidification on learning in coral reef fishes. PLoS ONE 7, e31478 (2012).

    CAS  Google Scholar 

  14. Dixson, D. L., Jennings, A. R., Atema, J. & Munday, P. L. Odor tracking in sharks is reduced under future ocean acidification conditions. Glob. Change Biol. 21, 1454–1462 (2015).

    Google Scholar 

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

    Google Scholar 

  16. 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).

    CAS  Google Scholar 

  17. 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 (2013).

    Google Scholar 

  18. Watson, S.-A. et al. Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels. Proc. R. Soc. B 281, 20132377 (2014).

    Google Scholar 

  19. 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).

    CAS  Google Scholar 

  20. Leduc, A. O. H. C., Munday, P. L., Brown, G. E. & Ferrari, M. C. O. Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis. Phil. Trans. R. Soc. B 368, 20120447 (2013).

    Google Scholar 

  21. Fariña, A. C. et al. Lophius in the world: a synthesis on the common features and life strategies. ICES J. Mar. Sci. 65, 1272–1280 (2008).

    Google Scholar 

  22. Hara, T. The diversity of chemical stimulation in fish olfaction and gustation. Rev. Fish Biol. Fish. 4, 1–35 (1994).

    Google Scholar 

  23. Buchinger, T. J., Li, W. & Johnson, N. S. Bile salts as semiochemicals in fish. Chem. Senses 39, 647–654 (2014).

  24. Leduc, A. O. H. C. et al. Ambient pH and the response to chemical alarm cues in juvenile Atlantic salmon: mechanisms of reduced behavioral responses. Trans. Am. Fish. Soc. 139, 117–128 (2010).

    CAS  Google Scholar 

  25. Lönnstedt, O. M. & McCormick, M. I. Chemical alarm cues inform prey of predation threat: the importance of ontogeny and concentration in a coral reef fish. Anim. Behav. 82, 213–218 (2011).

    Google Scholar 

  26. Frade, P., Hubbard, P. C., Barata, E. N. & Canario, A. V. M. Olfactory sensitivity of the Mozambique tilapia to conspecific odours. J. Fish Biol. 61, 1239–1254 (2002).

    Google Scholar 

  27. Hubbard, P. C., Barata, E. N. & Canário, A. V. M. Olfactory sensitivity of the gilthead seabream (Sparus auratus L) to conspecific body fluids. J. Chem. Ecol. 29, 2481–2498 (2003).

    CAS  Google Scholar 

  28. Haas, B. J. et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494–1512 (2013).

    CAS  Google Scholar 

  29. Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011).

    CAS  Google Scholar 

  30. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).

    CAS  Google Scholar 

  31. Malenka, R. C. & Nicoll, A. R. Long-term potentiation--a decade of progress? Science 285, 1870–1874 (1999).

    CAS  Google Scholar 

  32. Zhang, J. J., Okutani, F., Inoue, S. & Kaba, H. Activation of the mitogen-activated protein kinase/extracellular signal-regulated kinase signaling pathway leading to cyclic AMP response element-binding protein phosphorylation is required for the long-term facilitation process of aversive olfactory learning in young rats. Neuroscience 121, 9–16 (2003).

    CAS  Google Scholar 

  33. Deigweiher, K., Koschnick, N., Pörtner, H.-O. & Lucassen, M. Acclimation of ion regulatory capacities in gills of marine fish under environmental hypercapnia. Am. J. Physiol. 295, R1660–R1670 (2008).

    CAS  Google Scholar 

  34. Hashiguchi, Y., Furuta, Y. & Nishida, M. Evolutionary patterns and selective pressures of odorant/pheromone receptor gene families in teleost fishes. PLoS ONE 3, e4083 (2008).

    Google Scholar 

  35. Dubacq, C., Fouquet, C. & Trembleau, A. Making scent of the presence and local translation of odorant receptor mRNAs in olfactory axons. Dev. Neurobiol. 74, 259–268 (2014).

    CAS  Google Scholar 

  36. Benhaïm, D. et al. Early life behavioural differences in wild caught and domesticated sea bass (Dicentrarchus labrax). Appl. Anim. Behav. Sci. 141, 79–90 (2012).

    Google Scholar 

  37. 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).

    Google Scholar 

  38. Cripps, I. L., Munday, P. L. & McCormick, M. I. Ocean acidification affects prey detection by a predatory reef fish. PLoS ONE 6, e22736 (2011).

    CAS  Google Scholar 

  39. Duteil M. et al. European sea bass show behavioural resilience to near-future ocean acidification. R. Soc. Open Sci. 3, 160656 (2016).

    CAS  Google Scholar 

  40. 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 

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

    CAS  Google Scholar 

  42. 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).

    Google Scholar 

  43. 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).

    CAS  Google Scholar 

  44. Brauner, C. J. et al. Limited extracellular but complete intracellular acid–base regulation during short-term environmental hypercapnia in the armoured catfish, Liposarcus pardalis. J. Exp. Biol. 207, 3381–3390 (2004).

    CAS  Google Scholar 

  45. Esbaugh, A., Heuer, R. & Grosell, M. Impacts of ocean acidification on respiratory gas exchange and acid–base balance in a marine teleost, Opsanus beta. J. Comp. Physiol. B 182, 921–934 (2012).

    CAS  Google Scholar 

  46. 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).

    CAS  Google Scholar 

  47. 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).

    CAS  Google Scholar 

  48. Poulton, D. A., Porteus, C. S. & Simpson, S. D. Combined impacts of elevated CO2 and anthropogenic noise on European sea bass (Dicentrarchus labrax). ICES J. Mar. Sci. 74, 1230–1236 (2017).

    Google Scholar 

  49. Chivers, D., Puttlitz, M. & Blaustein, A. Chemical alarm signaling by reticulate sculpins, Cottus perplexus. Environ. Biol. Fish. 57, 347–352 (2000).

    Google Scholar 

  50. Field, D. et al. Open software for biologists: from famine to feast. Nat. Biotechnol. 24, 801–803 (2006).

    CAS  Google Scholar 

  51. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    CAS  Google Scholar 

  52. Crusoe, M. R. et al. The khmer software package: enabling efficient nucleotide sequence analysis. F1000Research 4, 900 (2015).

    Google Scholar 

  53. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    CAS  Google Scholar 

  54. Yates, A. et al. Ensembl 2016. Nucleic Acids Res. 44, D710–D716 (2016).

    CAS  Google Scholar 

  55. Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Methods 12, 59–60 (2015).

    CAS  Google Scholar 

  56. Huson, D. H., Mitra, S., Ruscheweyh, H.-J., Weber, N. & Schuster, S. C. Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21, 1552–1560 (2011).

    CAS  Google Scholar 

  57. Huang, D. W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57 (2008).

    Google Scholar 

  58. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45 (2001).

    CAS  Google Scholar 

  59. Filby, A. L. & Tyler, C. R. Appropriate ‘housekeeping’ genes for use in expression profiling the effects of environmental estrogens in fish. BMC Mol. Biol. 8, 10 (2007).

    Google Scholar 

  60. Hagey, L. R., Møller, P. R., Hofmann, A. F. & Krasowski, M. D. Diversity of bile salts in fish and amphibians: evolution of a complex biochemical pathway. Physiol. Biochem. Zool. 83, 308–321 (2010).

    CAS  Google Scholar 

  61. Ballantyne, J. S. Jaws: the inside story. The metabolism of elasmobranch fishes. Comp. Biochem. Physiol.B 118, 703–742 (1997).

    Google Scholar 

  62. Huertas, M. et al. Olfactory sensitivity to bile fluid and bile salts in the European eel (Anguilla anguilla), goldfish (Carassius auratus) and Mozambique tilapia (Oreochromis mossambicus) suggests a ‘broad range’ sensitivity not confined to those produced by conspecifics alone. J. Exp. Biol. 213, 308–317 (2010).

    CAS  Google Scholar 

  63. Zhang, C., Brown, S. & Hara, T. Biochemical and physiological evidence that bile acids produced and released by lake char (Salvelinus namaycush) function as chemical signals. J. Comp. Physiol. B 171, 161–171 (2001).

    CAS  Google Scholar 

  64. Hubbard, P., Barata, E. N., Ozório, R. A., Valente, L. P. & Canário, A. M. Olfactory sensitivity to amino acids in the blackspot sea bream (Pagellus bogaraveo): a comparison between olfactory receptor recording techniques in seawater. J. Comp. Physiol. A 197, 839–849 (2011).

    CAS  Google Scholar 

  65. Hubbard, P. C., Barata, E. N. & Canario, A. V. Olfactory sensitivity to changes in environmental [Ca2+] in the marine teleost Sparus aurata. J. Exp. Biol. 203, 3821–3829 (2000).

    CAS  Google Scholar 

  66. Velez, Z., Hubbard, P. C., Barata, E. N. & Canário, A. V. M. Olfactory transduction pathways in the Senegalese sole Solea senegalensis. J. Fish Biol. 83, 501–514 (2013).

    CAS  Google Scholar 

  67. Dickson, A. G., Sabine, C. L. & Christian, J. R. (eds) Guide to Best Practices for Ocean CO 2 Measurements PICES Special Publication 3 (North Pacific Marine Science Organization, 2007).

  68. Meredith, T. L., Caprio, J. & Kajiura, S. M. Sensitivity and specificity of the olfactory epithelia of two elasmobranch species to bile salts. J. Exp. Biol. 215, 2660–2667 (2012).

    CAS  Google Scholar 

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Acknowledgements

We thank L. Hagey and A. Hofmann (UCSD) for their gift of cyprinol sulfate and scymnol sulfate, the Aquatic Research Centre (ARC) staff at the University of Exeter for their assistance with fish husbandry and experimental setup, B. Verbruggen for helpful bioinformatics advice and L. Salisbury for help with tissue sampling. This study was supported by grants from Association of European Marine Biology Laboratories (227799), the Natural Environment Research Council (R.W.W.; NE/H017402/1), the Biotechnology and Biological Sciences Research Council (R.W.W.; BB/D005108/1), Fundação para a Ciência e Tecnologia (Portuguese Science Ministry) (UID/Multi/04326/2013) and a Royal Society Newton International Fellowship to C.S.P. C.S.P. is also a beneficiary of a Starting Grant from AXA.

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Authors and Affiliations

  1. Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, UK

    Cosima S. Porteus, Eduarda M. Santos & Rod W. Wilson

  2. Centro de Ciências do Mar, Campus de Gambelas, Universidade do Algarve, Faro, Portugal

    Peter C. Hubbard & Adelino V. M. Canário

  3. Biosciences, College of Science, Swansea University, Swansea, UK

    Tamsyn M. Uren Webster

  4. Centre for Environment, Fisheries and Aquaculture Science (Cefas), Weymouth, UK

    Ronny van Aerle

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  1. Cosima S. Porteus
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Contributions

C.S.P. and R.W.W. designed the behavioural experiments. C.S.P. performed the experiments and analysed those data; C.S.P., P.C.H., A.V.M.C. and R.W.W. designed the electrophysiology study, C.S.P. and P.C.H. performed the electrophysiology experiments. C.S.P., T.M.U.W., R.v.A. and E.M.S. designed the transcriptomics experiments, C.S.P. performed the experiments and constructed the libraries. C.S.P. performed the bioinformatics analysis and interpreted the results with help from T.M.U.W., R.v.A. and E.M.S. All authors contributed to and provided feedback on various drafts of the paper.

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Correspondence to Cosima S. Porteus or Rod W. Wilson.

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Supplementary Information

Supplementary figures 1–8, Supplementary tables 1–13, Supplementary References

Supplementary Data 1

Lists of differentially expressed genes in the olfactory epithelium and olfactory bulb at 2 and 7 days of exposure to control and high CO2

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Porteus, C.S., Hubbard, P.C., Uren Webster, T.M. et al. Near-future CO2 levels impair the olfactory system of a marine fish. Nature Clim Change 8, 737–743 (2018). https://doi.org/10.1038/s41558-018-0224-8

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