Abstract
In communities of high biodiversity, the ability to distinguish predators from non-predators is crucial for prey success. Learning often plays a vital role in the ability to distinguish species that are threatening from those that are not. Many prey animals learn to recognise predators based on a single conditioning event whereby they are exposed to the unknown predator at the same time as alarm cues released from injured conspecifics. The remarkable efficiency of such learning means that recognition mistakes may occur if prey inadvertently learn that a species is a predator when it is not. Latent inhibition is a means by which prey that are pre-exposed to an unknown species in the absence of negative reinforcement can learn that the unknown animal is likely not a threat. Learning through latent inhibition should be conservative because mistakenly identifying predators as non-predators can have fatal consequences. In this study, we demonstrated that a common coral reef fish, lemon damselfish, Pomacentrus moluccensis can learn to recognise a predator as non-threatening through latent inhibition. Furthermore, we showed that we could override the latent inhibition effect by conditioning the prey to recognise the predator numerous times. Our results highlight the ability of prey fish to continually update the information regarding the threat posed by other fishes in their vicinity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acquistapace P, Hazlett BA, Gherardi F (2003) Unsuccessful predation and learning of predators cues by crayfish. J Crust Biol 23:364–370. doi:10.1651/0278-0372(2003)023[0364:UPALOP]2.0.CO;2
Beukers J, Jones GP (1997) Habitat complexitymodifies the impact of piscivores on a coral reef fish population. Oecologia 114:50–59
Chivers DP, Smith RFJ (1994) Fathead minnows, Pimephales promelas, acquire predator recognition when alarm substance is associated with the sight of unfamiliar fish. Anim Behav 48:597–605. doi:10.1006/anbe.1994.1279
Chivers DP, Smith RFJ (1998) Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5:338–352
Davey G (1989) The biological function of Pavlovian conditioning. In: Davey G (ed) Ecological learning theory. Routledge, London, pp 171–199
Dixon DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75. doi:10.1111/j.1461-0248.2009.01400.x
Ferrari MCO, Chivers DP (2006a) The role of latent inhibition in acquired predator recognition by fathead minnows. Can J Zool 84:505–509. doi:10.1139/Z06-027
Ferrari MCO, Chivers DP (2006b) Learning threat-sensitive predator avoidance: how do fathead minows incorporate conflicting information? Anim Behav 71:19–26. doi:10.1016/j.anbehav.2005.02.016
Ferrari MCO, Chivers DP (2009) Latent inhibition of predator recognition by embryonic amphibians. Biol Lett 5:160–162. doi:10.1098/rsbl.2008.0641
Ferrari MCO, Chivers DP (2011) Learning about non-predators and safe places: the forgotten elements of risk assessment. Anim Cogn. doi:10.1007/s10071-010-0363-4
Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool Invit Rev 88:698–724. doi:10.1139/Z10-029
George CJ (1981) The fishes of the adirondack park. New York State Department of Environmental Conservation Special Publication, New York
Hazlett BA (1999) Responses to multiple chemical cues by the crayfish Orconectes virilis. Behaviour 163:161–177
Holmes TH, McCormick MI (2010) Smell, learn and live: the role of chemical alarm cues in predator learning during early life history in a marine fish. Behav Process 83:299–305
Kaplan O, Lubow RE (2001) Context and reminder effects in a visual search analogue of latent inhibition. Learn Motiv 32:137–153. doi:10.1006/lmot.2000.1077
Kelly JL, Magurran AE (2003) Learned predator recognition and antipredator responses in fishes. Fish Fish 4:216–226. doi:10.1046/j.1467-2979.2003.00126.x
Larson JK, McCormick MI (2005) The role of chemical alarm signals in facilitating learned recognition of novel chemical cues in coral reef fish. Anim Behav 69:51–57. doi:10.1016/j.anbehav.2004.04.005
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659. doi:10.1086/303202
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation—a review and prospectus. Can J Zool 68:619–640
Lubow RE, Moore AU (1959) Latent inhibition: the effect of non-reinforced pre-exposure to the conditional stimulus. J Comp Physiol Psychol 52:415–419
Manzur T, Barahona M, Navarrete SA (2010) Ontogenetic changes in habitat use and diet of the sea-star Heliaster helianthus on the coast of central Chile. Mar Ecol Prog Ser 401:245–258. doi:10.1017/S0025315409990786
Meekan MG, Wilson SG, Halford A, Retzel A (2001) A comparison of catches of fishes and invertebrates by two light trap designs, in tropical NW Australia. Mar Biol 139:373–381. doi:10.1007/s002270100577
Messmer V, van Herwerden L, Munday PL, Jones GP (2005) Phylogeography of colour polymorphism in the coral reef fish Pseudochromis fuscus, from Papua New Guinea and the Great Barrier Reef. Coral Reefs 24:392–402. doi:10.1007/s00338-005-0001-9
Mirza RS, Chivers DP (2003) Response of juvenile rainbow trout to varying concentrations of chemical alarm cue: response thresholds and survival during encounters with predators. Can J Zool 81:88–95. doi:10.1139/Z02-216
Mitchell MD, McCormick MI, Ferrari MCO, Chivers DP (2011) Coral reef fish rapidly learn to identify multiple unknown predators upon recruitment to the reef. PLoS One 6:e15764. doi:10.1371/journal.pone.0015764
Mumby PJ, Edwards AJ, Arias-Gonzalez JE, Lindeman KC, Blackwell PG, Gall A, Gorczynska MI, Harborne AR, Pescod CL, Renken H, Wabnitz CCC, Llewellyn G (2004) Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427:533–536. doi:10.1038/nature02286
Shettleworth SJ (1998) Simple recognition learning. In: Shettleworth SJ (ed) Cognition, evolution, and behaviour. Oxford University Press, New York, pp 139–182
Vail A (2009) Non-leathal influence of predators on juvenile fishes. BSc Honours Thesis, James Cook University, Townsville
Wellington GM, Victor BC (1989) Planktonic larval duration of one hundred species of Pacific and Atlantic damselfishes (Pomacentridae). Mar Biol 101:557–567. doi:10.1007/BF00541659
Acknowledgments
We thank M. Meekan, O. Lönnstedt, W. Feeney, S. Leahy, C. Neligh, T. Kath, B. Devine and D. Dixon for assisting in the collection of the fish used in this study. We thank the staff at the Lizard Island Research Station (Australian Museum) for logistic support. Research was carried out under approval from the Great Barrier Reef Marine Park Authority and under James Cook University ethics guidelines. Funding was provided by the Australian Research Council (MIM, MCOF, DPC), the ARC Centre of Excellence for Coral Reef Studies (MIM) and the Natural Sciences and Engineering Council of Canada (MCOF, DPC).
Ethics statement
This research was undertaken with approval of the James Cook University Animal Ethics Committee (permit: A1067) and according to the University’s Animal Ethics Guidelines.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
10071_2011_405_MOESM1_ESM.eps
Supplementary Fig. 1 Diagram showing the combined conditioning regime used to test for both latent inhibition and latent inhibition reversal. Both the latent inhibition and latent inhibition reversal experiments were run simultaneously to allow comparison between the different treatments and control for any temporal or recruitment pulse effects. Numbers indicate the number of times individuals were exposed or conditioned with the relevant odour (EPS 318 kb)
Rights and permissions
About this article
Cite this article
Mitchell, M.D., McCormick, M.I., Ferrari, M.C.O. et al. Friend or foe? The role of latent inhibition in predator and non-predator labelling by coral reef fishes. Anim Cogn 14, 707–714 (2011). https://doi.org/10.1007/s10071-011-0405-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10071-011-0405-6