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Risk-induced neophobia: does sensory modality matter?

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Abstract

Recent studies have documented that exposure to high levels of background risk can induce neophobic predator avoidance in prey animals, whereby they respond to any novel cue with an anti-predator response. Such phenotypically plastic predator avoidance may allow prey to maximize anti-predator benefits in variable risk environments. It remains poorly understood whether risk assessment information from different sensory modalities can be integrated to induce generalized, cross-sensory system neophobic responses. Here, we directly test this hypothesis by exposing juvenile convict cichlids (Amatitlania nigrofasciata) to high- versus low-risk environments using either conspecific alarm cue (chemosensory risk) or a model avian predator (visual/mechanical risk) and testing their response to a novel chemosensory cue (Experiment 1) or visual cue (Experiment 2). Our results suggest that regardless of the sensory modality used to increased perceived risk, cichlids pre-exposed to high-risk conditions exhibited increased predator avoidance in response to any novel visual or chemical cue. As expected, cichlids pre-exposed to low-risk conditions did not display any neophobic responses. Our results suggest that induced neophobia is not cue specific; rather, it may function as a generalized response to perceived predation risk.

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References

  • Allouche S, Gaudin P (2001) Effects of avian predation threat, water flow and cover on growth and habitat use by chub, Leuciscus cephalus, in an experimental stream. Oikos 94:481–4920

    Article  Google Scholar 

  • Amo L, López P, Martín J (2004) Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges. Anim Behav 67:647–653. doi:10.1016/j.anbehav.2003.08.005

    Article  Google Scholar 

  • Botham MS, Kerfoot CH, Louca V, Krause J (2006) The effects of different predator species on antipredator behavior in the Trinidadian guppy, Poecilia reticulata. Naturwissenschaften 93:431–439. doi:10.1007/s00114-006-0131-0

    Article  CAS  PubMed  Google Scholar 

  • Brown GE, Bongiorno T, Dicapua DM, Ivan LI, Roh E (2006) Effects of group size on the threat-sensitive response to varying concentrations of chemical alarm cues by juvenile convict cichlids. Can J Zool 84:1–8. doi:10.1139/Z05-166

    Article  Google Scholar 

  • Brown GE, Ferrari MCO, Chivers DP (2011) Learning about danger: chemical alarm cues and threat-sensitive assessment of predation risk by fishes. In: Brown C, Laland K, Krause J (eds) Fish cognition and behaviour, 2nd edn. Wiley-Blackwell, Chichester, pp 59–80

    Chapter  Google Scholar 

  • Brown GE, Ferrari MCO, Elvidge CK, Ramnarine I, Chivers DP (2013) Phenotypically-plastic neophobia: a response to variable predation risk. Proc R Soc Lond B 280:20122712. doi:10.1098/rspb.2012.2712

    Article  Google Scholar 

  • Brown GE, Elvidge CK, Ramnarine I, Chivers DP, Ferrari MCO (2014a) Personality and the response to predation risk: effects of information quantity and quality. Anim Cogn 17:1063–1069. doi:10.1007/s10071-014-0738-z

    Article  PubMed  Google Scholar 

  • Brown GE, Ferrari MCO, Elvidge CK, Jackson CD, Chivers DP (2014b) Background level of risk determines the intensity of predator neophobia in cichlids. Behav Ecol Sociobiol 68:127–133. doi:10.1007/s00265-013-1629-z

    Article  Google Scholar 

  • Brown GE, Elvidge CK, Ramnarine I, Ferrari MCO, Chivers DP (2015) Background risk and recent experience influence retention of neophobic responses to predators. Behav Ecol Sociobiol 69:737–745. doi:10.1007/s00265-015-1888-y

    Article  Google Scholar 

  • Chivers DP, McCormick MI, Mitchell MD, Ramasamy RA, Ferrari MCO (2014) Background level of risk determines how prey categorize predators and non-predators. Proc R Soc Lond B 281:20140355. doi:10.1098/rspb.2014.0355

    Article  Google Scholar 

  • Dall SRX, Giraldeau L-A, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193. doi:10.1016/j.treee.2005.01.010

    Article  PubMed  Google Scholar 

  • Elmasri OL, Moreno MS, Neumann CA, Blumstein DT (2012) Response of brown anoles Anolis sagrei to multimodal signals from a native and novel predator. Curr Zool 58:791–796. doi:10.1093/czoolo/58.6.791

    Article  Google Scholar 

  • Elson PF (1962) Predator-prey relationships between fish-eating birds and Atlantic salmon. Fish Res Board Can Bull 133:1–87

    Google Scholar 

  • Elvidge CK, MacNaughton CJ, Brown GE (2013) Sensory complementation and antipredator behaivoural compensation in acid-impacted juvenile Atlantic salmon. Oecologia 172:69–78. doi:10.1007/s00442-012-2478-6

    Article  CAS  PubMed  Google Scholar 

  • Ferrari MCO (2014) Short-term environmental variation in predation risk leads to differential performance in predation-related cognitive function. Anim Behav 95:9–14. doi:10.1016/j.anbehav.2014.06.001

    Article  Google Scholar 

  • Ferrari MCO, Gonzalo A, Messier F, Chivers DP (2007) Generalization of learned predator recognition: an experimental test and framework for future studies. Proc R Soc Lond B 274:1853–1859. doi:10.1098/rspb.2015.2197

    Article  Google Scholar 

  • Ferrari MCO, Rive AC, MacNaughton CJ, Brown GE, Chivers DP (2008a) Fixed vs. random temporal predictability of predation risk: an extension of the risk allocation hypothesis. Ethology 114:238–244. doi:10.1111/j.1439-0310.2007.01468.x

    Article  Google Scholar 

  • Ferrari MCO, Vavrek MA, Elvidge CK, Fridman B, Chivers DP, Brown GE (2008b) Sensory complementation and the acquisition of predator recognition by salmonid fishes. Behav Ecol Sociobiol 63:113–121. doi:10.1007/s00265-008-0641-1

    Article  Google Scholar 

  • Ferrari MCO, Sih A, Chivers DP (2009) The paradox of risk allocation: a review and prospectus. Anim Behav 78:579–585. doi:10.1016/j.anbehav.2009.05.034

    Article  Google Scholar 

  • Ferrari MCO, Crane AL, Brown GE, Chivers DP (2015a) Getting ready for invasions: can background level of risk predict the ability of naïve prey to survive novel predators? Sci Rep 5:8309. doi:10.1038/srep08309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrari MCO, McCormick MI, Meekan MG, Chivers DP (2015b) Background level of risk and the survival of predator-naïve prey: can neophobia compensate for predator naivety in juvenile coral reef fishes? Proc Roy Soc Lond B 282:20142197

    Article  Google Scholar 

  • Foam PE, Harvey MC, Mirza RS, Brown GE (2005) Heads up: juvenile convict cichlids switch to threat-sensitive foraging tactics based on chemosensory information. Anim Behav 70:601–607. doi:10.1016/j.anbehav.2004.12.011

    Article  Google Scholar 

  • Goodale E, Beauchamp G, Magrath RD, Neih JC, Ruxton GD (2010) Interspecific information transfer influences animal community structure. Trends Ecol Evol 25:354–361. doi:10.1016/j.tree.2010.01.002

    Article  PubMed  Google Scholar 

  • Grant JWA, Girard IL, Breau C, Weir LK (2002) Influence of food abundance on competitive aggression in juvenile convict cichlids. Anim Behav 63:323–330. doi:10.1006/j.anbe.2001.1891

    Article  Google Scholar 

  • Joyce BJ, Demers EEM, Chivers DP, Ferrari MCO, Brown GE (2016) Risk-induced neophobia is constrained by ontogeny in juvenile convict cichlids. Anim Behav 114:37–43. doi:10.1016/j.anbehav.2016.01.007

    Article  Google Scholar 

  • Kim J-W, Brown GE, Dolinsek IJ, Brodeur NN, Leduc AOHC, Grant JWA (2009) Combined effects of chemical and visual information in eliciting antipredator behaviour in juvenile Atlantic salmon, Salmo salar. J Fish Biol 74:1280–1290. doi:10.1111/j.1095-8649.2009.02199.x

    Article  PubMed  Google Scholar 

  • Leduc AOHC, Kim J-W, MacNaughton CJ, Brown GE (2010) The sensory complement model helps predict diel alarm response patterns in juvenile Atlantic salmon (Salmo salar) under natural conditions. Can J Zool 88:398–403. doi:10.1139/Z10.016

    Article  Google Scholar 

  • Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659

    Article  Google Scholar 

  • Meuthen D, Baldauf SA, Bakker TCM, Thuken T (2016) Predator-induced neophobia in juvenile cichlids. Oecologia 181:947–958. doi:10.1007/s00442-15-2478-0

    Article  PubMed  Google Scholar 

  • Mikheev VN, Wanzenbock J, Pasternak AF (2006) Effects of predator-induced visual and olfactory cues on 0 + perch (Perca fluviatilis L.) foraging behaviour. Ecol Freshw Fish 15:111–117. doi:10.1111/j.1600-0633.2006.00140.x

    Article  Google Scholar 

  • Munoz NE, Blumstein DT (2012) Multisensory perception in uncertain environments. Behav Ecol 23:457–462

    Article  Google Scholar 

  • Schmidt KA, Dall SRX, van Gils JA (2010) The ecology of information: an overview on the ecological significance of making informed decisions. Oikos 119:304–316. doi:10.1111/j.1600-0706.2009.17573.x

    Article  Google Scholar 

  • Seppänen J-T, Forsman JT, Mönkkönen M, Thomson RL (2007) Social information use is a process across time, space, and ecology, reaching heterospecifics. Ecology 88:1622–1633

    Article  PubMed  Google Scholar 

  • Sih A, Ziemba R, Harding KC (2000) New insights on how temporal variation in predation risk shapes prey behavior. Trends Ecol Evol 15:3–4

    Article  PubMed  Google Scholar 

  • Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc Lond B 272:2627–2634. doi:10.1098/rspb.2005.3251

    Article  Google Scholar 

  • Vavrek MA, Brown GE (2009) Threat-sensitive responses to disturbance cues in juvenile convict cichlids and rainbow trout. Ann Zool Fenn 46:171–180

    Article  Google Scholar 

  • Weissburg M, Smee DL, Ferner MC (2014) The sensory ecology of nonconsumptive predator effects. Am Nat 184:141–157. doi:10.1086/676644

    Article  PubMed  Google Scholar 

  • Wisenden BD, Sargent RC (1997) Antipredator behavior and suppressed aggression by convict cichlids in response to injury-released chemical cues of conspecifics but not to those of an allopatric heterospecific. Ethology 103:282–291

    Google Scholar 

  • Wisenden BD, Chivers DP, Smith RJF (1995) Early warning in the predation sequence—a disturbance pheromone in Iowa darters (Etheostoma exile). J Chem Ecol 21:1469–1480

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Ebony E. Demers, Laurence Feyten and Amanda Jeanson for assistance in the laboratory. All work reported herein was conducted in accordance with Concordia University Animal Research Ethics protocol # AREC-BROW-2011 and # 30000255. Financial support was provided by Concordia University and the Natural Sciences and Engineering Research Council of Canada (NSERC) to G.E.B. and the University of Saskatchewan and NSERC to D.P.C. and M.C.O.F.

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Authors and Affiliations

  1. Department of Biology, Concordia University, 7141 Sherbrooke St. West, Montreal, QC, H4B 1R6, Canada

    Grant E. Brown, Christopher D. Jackson & Brendan J. Joyce

  2. Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N 5E2, Canada

    Douglas P. Chivers

  3. Department of Biomedical Sciences, WCVM, University of Saskatchewan, 52 Campus Drive, Saskatoon, SK, S7N 5B4, Canada

    Maud C. O. Ferrari

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  1. Grant E. Brown
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  5. Maud C. O. Ferrari
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Correspondence to Grant E. Brown.

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Brown, G.E., Jackson, C.D., Joyce, B.J. et al. Risk-induced neophobia: does sensory modality matter?. Anim Cogn 19, 1143–1150 (2016). https://doi.org/10.1007/s10071-016-1021-2

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  • DOI: https://doi.org/10.1007/s10071-016-1021-2

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