Animal Cognition

, Volume 21, Issue 3, pp 419–424 | Cite as

A cross-modal effect of noise: the disappearance of the alarm reaction of a freshwater fish

  • Md Robiul Hasan
  • Adam L. Crane
  • Maud C. O. Ferrari
  • Douglas P. Chivers
Original Paper

Abstract

Anthropogenic noise pollution is recognized as a major global stressor of animals. While many studies have assessed the unimodal impacts of noise pollution with a focus on intraspecific acoustic communication, little is known about noise pollution on the perception of visual and chemical information. The ‘distracted prey hypothesis’ posits that processing noise interferes with processing other information in the brain. Here, we found evidence for such a cross-modal effect of noise on the antipredator behaviour of a freshwater prey fish, the fathead minnow, Pimephales promelas. In laboratory trials, exposure to noise from a motorboat caused the total absence of the classical fright reaction of minnows to conspecific alarm cues, whereas an ambient noise control had no such impact. In natural habitats, the impairment of such antipredator behaviour due to noise pollution could have major fitness consequences. We discuss how our findings translate to animal ecology and the need for future studies that target specific management decisions regarding noise pollution.

Keywords

Alarm cues Anthropogenic noise Antipredator behaviour Boat noise Predation risk 

Notes

Acknowledgements

This research was funded by the Natural Science and Engineering Research Council of Canada to MCOF and DPC. We thank Reid Bryshun for operating the boat.

Supplementary material

10071_2018_1179_MOESM1_ESM.xlsx (13 kb)
Supplementary material 1 (XLSX 13 kb)

References

  1. Blumstein DT, Fernández-Juricic E (2010) A primer of conservation behavior. Sinauer Associates, SunderlandGoogle Scholar
  2. Bracciali C, Campobello D, Giacoma C, Sara G (2012) Effects of nautical traffic and noise on foraging patterns of Mediterranean damselfish (Chromis chromis). PLoS ONE 7:e40582CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bruintjes R, Radford AN (2013) Context-dependent impacts of anthropogenic noise on individual and social behaviour in a cooperatively breeding fish. Anim Behav 85:1343–1349CrossRefGoogle Scholar
  4. Brumm H (2013) Animal communication and noise, vol 2. Springer, BerlinGoogle Scholar
  5. Chan A, Giraldo-Perez P, Smith S, Blumstein DT (2010) Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis. Biol Lett 6:458–461CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chivers DP, Smith RJF (1993) The role of olfaction in chemosensory-based predator recognition in the fathead minnow, Pimephales promelas. J Chem Ecol 19:623–633CrossRefPubMedGoogle Scholar
  7. Chivers DP, Smith RJF (1994) Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish. Anim Behav 48:597–605CrossRefGoogle Scholar
  8. Chivers DP, Smith RJF (1995) Fathead minnows (Pimephales promelas) learn to recognize chemical stimuli from high-risk habitats by the presence of alarm substance. Behav Ecol 6:155–158CrossRefGoogle Scholar
  9. Cui B, Wu M, She X, Liu H (2012) Impulse noise exposure in rats causes cognitive deficits and changes in hippocampal neurotransmitter signaling and tau phosphorylation. Brain Res 1427:35–43CrossRefPubMedGoogle Scholar
  10. Cunnington GM, Fahrig L (2010) Plasticity in the vocalizations of anurans in response to traffic noise. Acta Oecol 36:463–470CrossRefGoogle Scholar
  11. Ferrari MCO, Trowell JJ, Brown GE, Chivers DP (2005) The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. Anim Behav 70:777–784CrossRefGoogle Scholar
  12. Ferrari MCO, Sih A, Chivers DP (2009) The paradox of risk allocation: a review and prospectus. Anim Behav 78:579–585CrossRefGoogle Scholar
  13. Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724CrossRefGoogle Scholar
  14. Graham AL, Cooke SJ (2008) The effects of noise disturbance from various recreational boating activities common to inland waters on the cardiac physiology of a freshwater fish, the largemouth bass (Micropterus salmoides). Aquat Conserv 18:1315–1324CrossRefGoogle Scholar
  15. Halfwerk W, Slabbekoorn H (2009) A behavioural mechanism explaining noise-dependent frequency use in urban birdsong. Anim Behav 78:1301–1307CrossRefGoogle Scholar
  16. Halfwerk W, Slabbekoorn H (2015) Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance. Biol Lett 11:20141051CrossRefPubMedPubMedCentralGoogle Scholar
  17. Haren AM (2007) Reducing noise pollution from commercial shipping in the Channel Islands National Marine Sanctuary: a case study in marine protected area management of underwater noise. J Int Wildl Law Policy 10:153–173CrossRefGoogle Scholar
  18. Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58CrossRefGoogle Scholar
  19. Hildebrand JA (2009) Anthropogenic and natural sources of ambient noise in the ocean. Mar Ecol Prog Ser 395:5–20CrossRefGoogle Scholar
  20. Kunc HP, Lyons GN, Sigwart JD, McLaughlin KE, Houghton JD (2014) Anthropogenic noise affects behavior across sensory modalities. Am Nat 184:E93–E100CrossRefPubMedGoogle Scholar
  21. Leaper R, Renilson M (2012) A review of practical methods for reducing underwater noise pollution from large commercial vessels. Int J Marit Eng 154:A79–A88Google Scholar
  22. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  23. Mathis A, Crane AL (2017) Chemoreception. In: Call J (ed) APA handbook of comparative psychology, vol 2. APA Books, Washington, DC, pp 69–87Google Scholar
  24. McDonald MA, Hildebrand JA, Wiggins SM (2006) Increases in deep ocean ambient noise in the Northeast Pacific west of San Nicolas Island, California. J Acoust Soc Am 120:711–718CrossRefPubMedGoogle Scholar
  25. Morris-Drake A, Kern JM, Radford AN (2016) Cross-modal impacts of anthropogenic noise on information use. Curr Biol 26:R911–R912CrossRefPubMedGoogle Scholar
  26. Northcutt RG (2006) Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J Comp Neurol 494:903–943CrossRefPubMedGoogle Scholar
  27. Olson CL (1976) On choosing a test statistic in multivariate analysis of variance. Psychol Bull 83:579CrossRefGoogle Scholar
  28. Pijanowski BC, Farina A, Gage SH, Dumyahn SL, Krause BL (2011) What is soundscape ecology? An introduction and overview of an emerging new science. Landsc Ecol 26:1213–1232CrossRefGoogle Scholar
  29. Purser J, Radford AN (2011) Acoustic noise induces attention shifts and reduces foraging performance in three-spined sticklebacks (Gasterosteus aculeatus). PLoS ONE 6:e17478CrossRefPubMedPubMedCentralGoogle Scholar
  30. Relyea RA (2002) Local population differences in phenotypic plasticity: predator-induced changes in wood frog tadpoles. Ecol Monogr 72:77–93CrossRefGoogle Scholar
  31. Rogers PH, Hawkins AD, Popper AN, Fay RR, Gray MD (2016) Parvulescu revisited: small Tank acoustics for bioacousticians. In: Popper AN, Hawkins A (eds) The effects of noise on aquatic life II. Advances in experimental medicine and biology, vol 875. Springer, New York, pp 933–941Google Scholar
  32. Sarà G et al (2007) Effect of boat noise on the behaviour of bluefin tuna Thunnus thynnus in the Mediterranean Sea. Mar Ecol Prog Ser 331:243–253CrossRefGoogle Scholar
  33. Scholik AR, Yan HY (2002) Effects of boat engine noise on the auditory sensitivity of the fathead minnow, Pimephales promelas. Environ Biol Fishes 63:203–209CrossRefGoogle Scholar
  34. Sebastianutto L, Picciulin M, Costantini M, Ferrero EA (2011) How boat noise affects an ecologically crucial behaviour: the case of territoriality in Gobius cruentatus (Gobiidae). Environ Biol Fishes 92:207–215CrossRefGoogle Scholar
  35. Shannon G et al (2016) A synthesis of two decades of research documenting the effects of noise on wildlife. Biol Rev 91:982–1005CrossRefPubMedGoogle Scholar
  36. Simpson SD, Purser J, Radford AN (2015) Anthropogenic noise compromises antipredator behaviour in European eels. Global Change Biol 21:586–593CrossRefGoogle Scholar
  37. Simpson SD, Radford AN, Holles S, Ferarri MC, Chivers DP, McCormick MI, Meekan MG (2016a) Small-boat noise impacts natural settlement behavior of coral reef fish larvae. In: Popper AN, Hawkins A (eds) The effects of noise on aquatic life II. Advances in experimental medicine and biology, vol 875. Springer, New York, pp 1041–1048Google Scholar
  38. Simpson SD, Radford AN, Nedelec SL, Ferrari MC, Chivers DP, McCormick MI, Meekan MG (2016b) Anthropogenic noise increases fish mortality by predation. Nat Commun 7:10544CrossRefPubMedPubMedCentralGoogle Scholar
  39. Smith RJF (1992) Alarm signals in fishes. Rev Fish Biol Fisher 2:33–63CrossRefGoogle Scholar
  40. Templeton CN, Zollinger SA, Brumm H (2016) Traffic noise drowns out great tit alarm calls. Curr Biol 26:R1173–R1174CrossRefPubMedGoogle Scholar
  41. Voellmy IK, Purser J, Simpson SD, Radford AN (2014) Increased noise levels have different impacts on the anti-predator behaviour of two sympatric fish species. PLoS ONE 9:e102946CrossRefPubMedPubMedCentralGoogle Scholar
  42. von Frisch K (1938) Zur psychologie des fisch-schwarmes. Naturwissenschaften 26:601–606CrossRefGoogle Scholar
  43. Wisenden BD, Pogatshnik J, Gibson D, Bonacci L, Schumacher A, Willett A (2008) Sound the alarm: learned association of predation risk with novel auditory stimuli by fathead minnows (Pimephales promelas) and glowlight tetras (Hemigrammus erythrozonus) after single simultaneous pairings with conspecific chemical alarm cues. Environ Biol Fishes 81:141–147CrossRefGoogle Scholar
  44. Würsig B, Greene C, Jefferson T (2000) Development of an air bubble curtain to reduce underwater noise of percussive piling. Mar Environ Res 49:79–93CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyUniversity of SaskatchewanSaskatoonCanada
  2. 2.Department of Biomedical Sciences, WCVMUniversity of SaskatchewanSaskatoonCanada

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