Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Blumstein DT, Fernández-Juricic E (2010) A primer of conservation behavior. Sinauer Associates, Sunderland

    Google Scholar 

  • 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:e40582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bruintjes R, Radford AN (2013) Context-dependent impacts of anthropogenic noise on individual and social behaviour in a cooperatively breeding fish. Anim Behav 85:1343–1349

    Article  Google Scholar 

  • Brumm H (2013) Animal communication and noise, vol 2. Springer, Berlin

    Google Scholar 

  • Chan A, Giraldo-Perez P, Smith S, Blumstein DT (2010) Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis. Biol Lett 6:458–461

    Article  PubMed  PubMed Central  Google Scholar 

  • Chivers DP, Smith RJF (1993) The role of olfaction in chemosensory-based predator recognition in the fathead minnow, Pimephales promelas. J Chem Ecol 19:623–633

    Article  CAS  PubMed  Google Scholar 

  • 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 48:597–605

    Article  Google Scholar 

  • 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 6:155–158

    Article  Google Scholar 

  • 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 1427:35–43

    Article  CAS  PubMed  Google Scholar 

  • Cunnington GM, Fahrig L (2010) Plasticity in the vocalizations of anurans in response to traffic noise. Acta Oecol 36:463–470

    Article  Google Scholar 

  • 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 70:777–784

    Article  Google Scholar 

  • Ferrari MCO, Sih A, Chivers DP (2009) The paradox of risk allocation: a review and prospectus. Anim Behav 78:579–585

    Article  Google Scholar 

  • Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724

    Article  Google Scholar 

  • 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 18:1315–1324

    Article  Google Scholar 

  • Halfwerk W, Slabbekoorn H (2009) A behavioural mechanism explaining noise-dependent frequency use in urban birdsong. Anim Behav 78:1301–1307

    Article  Google Scholar 

  • Halfwerk W, Slabbekoorn H (2015) Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance. Biol Lett 11:20141051

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 10:153–173

    Article  Google Scholar 

  • Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58

    Article  Google Scholar 

  • Hildebrand JA (2009) Anthropogenic and natural sources of ambient noise in the ocean. Mar Ecol Prog Ser 395:5–20

    Article  Google Scholar 

  • Kunc HP, Lyons GN, Sigwart JD, McLaughlin KE, Houghton JD (2014) Anthropogenic noise affects behavior across sensory modalities. Am Nat 184:E93–E100

    Article  PubMed  Google Scholar 

  • 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–A88

    Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Mathis A, Crane AL (2017) Chemoreception. In: Call J (ed) APA handbook of comparative psychology, vol 2. APA Books, Washington, DC, pp 69–87

    Google Scholar 

  • 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 120:711–718

    Article  PubMed  Google Scholar 

  • Morris-Drake A, Kern JM, Radford AN (2016) Cross-modal impacts of anthropogenic noise on information use. Curr Biol 26:R911–R912

    Article  CAS  PubMed  Google Scholar 

  • Northcutt RG (2006) Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J Comp Neurol 494:903–943

    Article  PubMed  Google Scholar 

  • Olson CL (1976) On choosing a test statistic in multivariate analysis of variance. Psychol Bull 83:579

    Article  Google Scholar 

  • 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 26:1213–1232

    Article  Google Scholar 

  • Purser J, Radford AN (2011) Acoustic noise induces attention shifts and reduces foraging performance in three-spined sticklebacks (Gasterosteus aculeatus). PLoS ONE 6:e17478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Relyea RA (2002) Local population differences in phenotypic plasticity: predator-induced changes in wood frog tadpoles. Ecol Monogr 72:77–93

    Article  Google Scholar 

  • 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 933–941

    Google Scholar 

  • 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 331:243–253

    Article  Google Scholar 

  • Scholik AR, Yan HY (2002) Effects of boat engine noise on the auditory sensitivity of the fathead minnow, Pimephales promelas. Environ Biol Fishes 63:203–209

    Article  Google Scholar 

  • 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 92:207–215

    Article  Google Scholar 

  • Shannon G et al (2016) A synthesis of two decades of research documenting the effects of noise on wildlife. Biol Rev 91:982–1005

    Article  PubMed  Google Scholar 

  • Simpson SD, Purser J, Radford AN (2015) Anthropogenic noise compromises antipredator behaviour in European eels. Global Change Biol 21:586–593

    Article  Google Scholar 

  • 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 1041–1048

    Google Scholar 

  • Simpson SD, Radford AN, Nedelec SL, Ferrari MC, Chivers DP, McCormick MI, Meekan MG (2016b) Anthropogenic noise increases fish mortality by predation. Nat Commun 7:10544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith RJF (1992) Alarm signals in fishes. Rev Fish Biol Fisher 2:33–63

    Article  Google Scholar 

  • Templeton CN, Zollinger SA, Brumm H (2016) Traffic noise drowns out great tit alarm calls. Curr Biol 26:R1173–R1174

    Article  CAS  PubMed  Google Scholar 

  • 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:e102946

    Article  PubMed  PubMed Central  Google Scholar 

  • von Frisch K (1938) Zur psychologie des fisch-schwarmes. Naturwissenschaften 26:601–606

    Article  Google Scholar 

  • 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 81:141–147

    Article  Google Scholar 

  • Würsig B, Greene C, Jefferson T (2000) Development of an air bubble curtain to reduce underwater noise of percussive piling. Mar Environ Res 49:79–93

    Article  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Biology, University of Saskatchewan, Saskatoon, SK, Canada

    Md Robiul Hasan, Adam L. Crane & Douglas P. Chivers

  2. Department of Biomedical Sciences, WCVM, University of Saskatchewan, Saskatoon, SK, Canada

    Maud C. O. Ferrari

Authors
  1. Md Robiul Hasan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adam L. Crane
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maud C. O. Ferrari
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Douglas P. Chivers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adam L. Crane.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hasan, M.R., Crane, A.L., Ferrari, M.C.O. et al. A cross-modal effect of noise: the disappearance of the alarm reaction of a freshwater fish. Anim Cogn 21, 419–424 (2018). https://doi.org/10.1007/s10071-018-1179-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-018-1179-x

Keywords

Search

Navigation