Abstract
Due to the high variability in predation risk through space and time, prey have to continuously update information about the risk level posed by predators. Despite numerous studies focusing on temporal risk assessment, we know very little about how individuals deal with information regarding changes in risk level of a given predator through time. In this study, we conditioned tadpoles to recognize a predator as a high or low risk twice 2 weeks apart, in a 2 × 2 design. We tested the responses of the tadpoles 1 and 11 days after each conditioning event. Prey showed responses to the predator 1 day after the first conditioning, but the low-risk group failed to respond to the predator after 11 days. However, we found that information learned during the first conditioning affected the response to the predator after the second conditioning, indicating that prey do not ‘forget’ old information, but simply ignore it. Moreover, tadpoles were able to assess their change in vulnerability over the 2-week period and further extrapolate the risk level of the predator through time to display adaptive threat-sensitive antipredator responses. Our study highlights the complex decision-making that prey use to assess temporal fluctuation in predation risk.
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References
Bernays EA, Wcislo WT (1994) Sensory capabilities, information processing, and resource specialization. Q Rev Biol 69:187–204
Blumstein DT (2010) Flush early and avoid the rush: a general rule of antipredator behavior? Behav Ecol 21(3):440–442. doi:10.1093/beheco/arq030
Blumstein DT, Barrow L, Luterra M (2008) Olfactory predator discrimination in yellow-bellied marmots. Ethology 114(11):1135–1143. doi:10.1111/j.1439-0310.2008.01563.x
Brown GE, Dreier VM (2002) Predator inspection behaviour and attack cone avoidance in a characin fish: the effects of predator diet and prey experience. Anim Behav 63:1175–1181. doi:10.1006/anbe.2002.3024
Brown GE, Magnavacca G (2003) Predator inspection behaviour in a characin fish: an interaction between chemical and visual information? Ethology 109(9):739–750
Brown GE, Ferrari MCO, Malka PH, Oligny M-A, Romano M, Chivers DP (2011) Growth rate and retention of learned predator cues in juvenile rainbow trout: faster growing fish forget sooner. Behav Ecol Sociobiol 65:1267–1276
Caldwell RL (1992) Recognition, signaling and reduced aggression between former mates in a stomatopod. Anim Behav 44(1):11–19. doi:10.1016/s0003-3472(05)80749-3
Chivers DP, Mirza RS (2001) Importance of predator diet cues in responses of larval wood frogs to fish and invertebrate predators. J Chem Ecol 27(1):45–51
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(3):597–606
Chivers DP, Zhao XX, Brown GE, Marchant TA, Ferrari MCO (2008) Predator-induced changes in morphology of a prey fish: the effects of food level and temporal frequency of predation risk. Evol Ecol 22(4):561–574. doi:10.1007/s10682-007-9182-8
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(4):187–193. doi:10.1016/j.tree.2005.01.010
Dugatkin LA (2009) Principles of animal behavior. W. W Norton, New York
Ferrari MCO, Chivers DP (2006) Learning threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information? Anim Behav 71:19–26. doi:10.1016/j.anbehav.2005.02.016
Ferrari MCO, Chivers DP (2008) Cultural learning of predator recognition in mixed-species assemblages of frogs: the effect of tutor-to-observer ratio. Anim Behav 75:1921–1925. doi:10.1016/j.anbehav.2007.10.037
Ferrari MCO, Chivers DP (2009) Temporal variability, threat sensitivity and conflicting information about the nature of risk: understanding the dynamics of tadpole antipredator behaviour. Anim Behav 78(1):11–16. doi:10.1016/j.anbehav.2009.03.016
Ferrari MCO, Chivers DP (2010) The ghost of predation future: threat-sensitive and temporal assessment of risk by embryonic woodfrogs. Behav Ecol Sociobiol 64(4):549–555. doi:10.1007/s00265-009-0870-y
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. doi:10.1016/j.anbehav.2005.01.009
Ferrari MCO, Messier F, Chivers DP (2007) First documentation of cultural transmission of predator recognition by larval amphibians. Ethology 113(6):621–627. doi:10.1111/j.1439-0310.2007.01362.x
Ferrari MCO, Messier F, Chivers DP (2008) Threat-sensitive learning of predators by larval mosquitoes Culex restuans. Behav Ecol Sociobiol 62(7):1079–1083. doi:10.1007/s00265-007-0535-7
Ferrari MCO, Brown GE, Messier F, Chivers DP (2009a) Threat-sensitive generalization of predator recognition by larval amphibians. Behav Ecol Sociobiol 63(9):1369–1375. doi:10.1007/s00265-009-0779-5
Ferrari MCO, Sih A, Chivers DP (2009b) The paradox of risk allocation: a review and prospectus. Anim Behav 78(3):579–585. doi:10.1016/j.anbehav.2009.05.034
Ferrari MCO, Brown GE, Bortolotti GR, Chivers DP (2010a) Linking predator risk and uncertainty to adaptive forgetting: a theoretical framework and empirical test using tadpoles. Proc R Soc B Biol Sci 277(1691):2205–2210. doi:10.1098/rspb.2009.2117
Ferrari MCO, Brown GE, Jackson CD, Malka PH, Chivers DP (2010b) Differential retention of predator recognition by juvenile rainbow trout. Behaviour 147:1791–1802
Ferrari MCO, Wisenden BD, Chivers DP (2010c) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724
Ferrari MCO, Brown GE, Bortolotti GR, Chivers DP (2011) Prey behaviour across antipredator adaptation types: how does growth trajectory influence learning of predators? Anim Cogn 14:809–816
Gonzalo A, Lopez P, Martin J (2009) Learning, memorizing and apparent forgetting of chemical cues from new predators by Iberian green frog tadpoles. Anim Cogn 12(5):745–750. doi:10.1007/s10071-009-0232-1
Guilford T, Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42(1):1–14
Hammond JI, Luttbeg B, Sih A (2007) Predator and prey space use: dragonflies and tadpoles in an interactive game. Ecology 88(6):1525–1535
Hartman EJ, Abrahams MV (2000) Sensory compensation and the detection of predators: the interaction between chemical and visual information. Proc R Soc B Biol Sci 267(1443):571–575
Hazlett BA, Acquistapace P, Gherardi F (2002) Differences in memory capabilities in invasive and native crayfish. J Crustac Biol 22(2):439–448
Healy S (1992) Optimal memory—toward an evolutionary ecology of animal cognition. Trends Ecol Evol 7(12):399–400
Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24(1):47–58
Hirvonen H, Ranta E, Rita H, Peuhkuri N (1999) Significance of memory properties in prey choice decisions. Ecol Model 115:177–189
Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hübener M (2008) Experience leaves a lasting structural trace in cortical circuits. Nature 457(7227):313–317
Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33(3):121–129
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5(3):361–394
Kawecki TJ (2010) Evolutionary ecology of learning: insights from fruit flies. Popul Ecol 52(1):15–25
Killeen P (1981) Averaging theory. Quant Steady State Operant Behav: 21–34
Kohn NR, Deitloff JM, Dartez SF, Wilcox MM, Jaeger RG (2013) Memory of conspecifics in male salamanders Plethodon cinereus: Implications for territorial defense. Current Zoology (in press)
Kraemer PJ, Golding JM (1997) Adaptive forgetting in animals. Psychon Bull Rev 4:480–491
Lima SL (1998a) Nonlethal effects in the ecology of predator-prey interactions—What are the ecological effects of anti-predator decision-making? Bioscience 48(1):25–34
Lima SL (1998b) Stress and decision making under the risk of predation: Recent developments from behavioral, reproductive, and ecological perspectives. In: Stress and Behavior, vol 27. Advances in the study of behavior. pp 215–290
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153(6):649–659
Lima SL, Dill LM (1990) Behavioral decision made under the risk of predation—a review and prospectus. Can J Zool 68(4):619–640
Luttbeg B, Sih A (2004) Predator and prey habitat selection games: the effects of how prey balance foraging and predation risk. Isr J Zool 50(2–3):233–254
McNamara JM, Houston AI (1987) Memory and the efficient use of information. J Theor Biol 125:385–395
Mery F, Kawecki TJ (2005) A cost of long-term memory in Drosophilia. Science 308:1148
Mirza RS, Chivers DP (2000) Predator-recognition training enhances survival of brook trout: evidence from laboratory and field-enclosure studies. Can J Zool 78(12):2198–2208
Mirza RS, Ferrari MCO, Kiesecker JM, Chivers DP (2006) Responses of American toad tadpoles to predation cues: behavioural response thresholds, threat-sensitivity and acquired predation recognition. Behaviour 143:877–889
Ryan MJ, Akre KL, Kirkpatrick M (2009) Cognitive mate choice. In: Dukas R, Ratcliffe JM (eds) Cognitive ecology II. Chicago University Press, Chicago, pp 137–155
Shoup DE, Wahl DH (2009) The effects of turbidity on prey selection by piscivorous largemouth bass. Trans Am Fish Soc 138:1018–1027
Werner EE, Gilliam JF, Hall DJ, Mittelbach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64(6):1540–1548. doi:10.2307/1937508
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford
Wisenden BD, Harter KR (2001) Motion, not shape, facilitates association of predation risk with novel objects by fathead minnows (Pimephales promelas). Ethology 107(4):357–364
Wisenden BD, Rugg ML, Korpi NL, Fuselier LC (2009) Lab and field estimates of active time of chemical alarm cues of a cyprinid fish and an amphipod crustacean. Behaviour 146:1423–1442. doi:10.1163/156853909x440998
Zentall TR, Roper KL, Sherburne LM (1995) Most directed forgetting in pigeons can be attributed to the absence of reinforcement on forget trials during training or to other procedural artifacts. J Exp Anal Behav 63(2):127–137. doi:10.1901/jeab.1995.63-127
Zhao XX, Ferrari MCO, Chivers DP (2006) Threat-sensitive learning of predator odours by a prey fish. Behaviour 143:1103–1121
Acknowledgments
All work reported herein was performed in accordance with the UCACS Animal Care Protocol 20060014. Funding was provided by NSERC of Canada to DPC and MCOF. A big thanks to Jean and Glen for letting us play in the ponds, to Jana Vrtelova for field assistance and Oliver and Harold for their invaluable moral support during our never-ending observations in mosquito-infected field sites.
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Ferrari, M.C.O., Chivers, D.P. Temporal dynamics of information use in learning and retention of predator-related information in tadpoles. Anim Cogn 16, 667–676 (2013). https://doi.org/10.1007/s10071-013-0602-6
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DOI: https://doi.org/10.1007/s10071-013-0602-6