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Experience window influences development and retention of memory to recognize predators in the larval skipper frogs
Learning and memory are critical for predator recognition as they allow prey species to develop an adaptive response to a novel situation, thus increasing their chances of survival. In prey species that lack innate predator recognition, alarm cues play a crucial role in learning by their association with novel predator odour. Perception of novel predator odours along with alarm cues allows the prey to learn to detect predatory odours alone in their future encounters. A single event of exposure is considered to be sufficient for the prey to associate predatory cues with alarm cues. However, the minimum time required for learning and memorizing information about predator identity is unknown. Hence we used the tadpoles of Euphlyctis cyanophlyctis to determine the association between the experience window and memory development and its retention. We conditioned tadpoles with a mixture of dragonfly nymph odours and alarm cues for 1, 3, 6, 12 and 24 h, and subsequently assessed their antipredator behaviour at different intervals. Our results show that the minimum duration required for associative learning is ~6 h. Interestingly, the intensity of antipredator response was proportional to the duration of conditioning. Moreover, retention of memory increased with an increase in the duration of conditioning. Hence, we show the significance of conditioning duration in learning. We also show an association between the duration of conditioning and retention of memory. In aquatic ecosystems, where the prey encounters a wide array of predatory cues, our findings open a new avenue for understanding the complexities associated with learning and the development of memory.
Keywords
Associative learning, experience window, Euphlyctis cyanophlyctis, memory retention, predator and prey.
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- Křivan, V. and Sirot, E., Do short-term behavioural responses of consumers in tri-trophic food chains persist at the population timescale?. Evol. Ecol. Res., 2004, 6(7), 1063–1081.
- Ferrari, M. C., Wisenden, B. D. and Chivers, D. P., Chemical ecology of predator–prey interactions in aquatic ecosystems: a review and prospectus. Can. J. Zool., 2010, 88(7), 698–724.
- Ferrari, M. C., Short-term environmental variation in predation risk leads to differential performance in predation-related cognitive function. Anim. Behav., 2014, 95, 9–14.
- Mogali, S., Shanbhag, B. and Saidapur, S., Experience of predacious cues and accessibility to refuge minimize mortality of Hylarana temporalis tadpoles. Acta Herpetol., 2019, 14(1), 15–19.
- Lima, S. L., Stress and decision-making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv. Study Behav., 1998, 27(8), 215–290.
- Preisser, E. L., Bolnick, D. I. and Benard, M. F., Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology, 2005, 86(2), 501–509.
- Kats, L. B. and Dill, L. M., The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience, 1998, 5(3), 361–394.
- Supekar, S. C. and Gramapurohit, N. P., Larval skipper frogs recognise kairomones of certain predators innately. J. Ethol., 2018, 36(2), 143–149.
- McCoy, M. W., Touchon, J. C., Landberg, T., Warkentin, K. M. and Vonesh, J. R., Prey responses to predator chemical cues: disentangling the importance of the number and biomass of prey consumed. PLoS ONE, 2012, 7(10), e47495.
- Wisenden, B. D., Olfactory assessment of predation risk in the aquatic environment. Philos. Trans. R. Soc. London, Ser. B, 2000, 355(1401), 1205–1208.
- Chivers, D. P., Brown, G. E. and Smith, R. J. F., The evolution of chemical alarm signals: attracting predators benefits alarm signal senders. Am. Nat., 1996, 148(4), 649–659.
- Wisenden, B. D., Chemically mediated strategies to counter predation. In Sensory Processing in Aquatic Environments, Springer, New York, USA, 2003, pp. 236–251.
- Epp, K. J. and Gabor, C. R., Innate and learned predator recognition mediated by chemical signals in Eurycea nana. Ethology, 2008, 114(6), 607–615.
- Sharma, S. S., Veeranagoudar, D. K., Shanbhag, B. A. and Saidapur, S. K., Activity of Sphaerotheca breviceps tadpoles in response to chemical cues of the predaceous tadpoles Hoplobatrachus tigerinus. J. Ethol., 2008, 26(3), 303–307.
- Saidapur, S. K., Veeranagoudar, D. K., Hiragond, N. C. and Shanbhag, B. A., Mechanism of predator–prey detection and behavioral responses in some anuran tadpoles. Chemoecology, 2009, 19(1), 21–28.
- Mogali, S. M., Saidapur, S. K. and Shanbhag, B. A., Levels of predation modulate antipredator defense behavior and metamorphic traits in the toad Bufo melanostictus. J. Herpetol., 2011, 45(4), 428–431.
- Mezrai, N., Arduini, L., Dickel, L., Chiao, C. C. and Darmaillacq, A. S., Awareness of danger inside the egg: evidence of innate and learned predator recognition in cuttlefish embryos. Learn. Behav., 2020, 48(4), 401–410.
- Supekar, S. C. and Gramapurohit, N. P., Can embryonic skipper frogs (Euphlyctis cyanophlyctis) learn to recognise kairomones in the absence of a nervous system?. J. Biosci., 2017, 42(3), 459–468.
- Brown, G. E., Ferrari, M. C., Elvidge, C. K., Ramnarine, I. and Chivers, D. P., Phenotypically plastic neophobia: a response to variable predation risk. Proc. R. Soc. London, Ser. B, 2013, 280(1756), 20122712.
- Pearce, J. M. and Bouton, M. E., Theories of associative learning in animals. Annu. Rev. Psychol., 2001, 52(1), 111–139.
- Mathis, A., Ferrari, M. C., Windel, N., Messier, F. and Chivers, D. P., Learning by embryos and the ghost of predation future. Proc. R. Soc. London, Ser. B, 2008, 275(1651), 2603–2607.
- Ferrari, M. C. and Chivers, D. P., Sophisticated early life lessons: threat-sensitive generalization of predator recognition by embryonic amphibians. Behav. Ecol., 2009, 20(6), 1295–1298.
- Ferrari, M. C., Horn, M. E. and Chivers, D. P., Cognitive resonance: when information carry‐over constrains cognitive plasticity. Funct. Ecol., 2019, 33(4), 703–711.
- Ferrari, M. C., Trowell, J. J., Brown, G. E. and Chivers, D. P., The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. Anim. Behav., 2005, 70(4), 777–784.
- Mogali, S. M., Saidapur, S. K. and Shanbhag, B. A., Tadpoles of the bronze frog (Rana temporalis) assess predation risk before evoking antipredator defense behavior. J. Ethol., 2012, 30(3), 379–386.
- Supekar, S. C. and Gramapurohit, N. P., Does temporal variation in predation risk affect antipredator responses of larval Indian skipper frogs (Euphlyctis cyanophlyctis)?. Can. J. Zool., 2020, 98(3), 202–209.
- Supekar, S. C. and Gramapurohit, N. P., Do antipredator responses of Euphlyctis cyanophlyctis tadpoles depend on the intensity of predation risk?. Aquat. Ecol., 2020, 54(3), 823–837.
- Shettleworth, S. J., Cognition, Evolution and Behavior, Oxford University Press, Oxford, UK, 1998.
- Mirza, R. S. and Chivers, D. P., Predator-recognition training enhances survival of brook trout: evidence from laboratory and fieldenclosure studies. Can. J. Zool., 2000, 78(12), 2198–2208.
- Gonzalo, A., López, P. and Martín, J., Learning, memorizing and apparent forgetting of chemical cues from new predators by Iberian green frog tadpoles. Anim. Cogn., 2009, 12(5), 745–750.
- Malka, P. H., Chivers, D. P., Ferrari, M. C., Brown, G. E. and Jackson, C. D., Differential retention of predator recognition by juvenile rainbow trout. Behaviour, 2010, 147(13–14), 1791–1802.
- Dall, S. R., Giraldeau, L. A., Olsson, O., McNamara, J. M. and Stephens, D. W., Information and its use by animals in evolutionary ecology. Trends Ecol. Evol., 2005, 20(4), 187–193.
- Chivers, D. P. and Ferrari, M. C., Tadpole antipredator responses change over time: what is the role of learning and generalization?. Behav. Ecol., 2013, 24(5), 1114–1121.
- Ferrari, M. C., Brown, G. E., Bortolotti, G. R. and Chivers, D. P., Linking predator risk and uncertainty to adaptive forgetting: a theoretical framework and empirical test using tadpoles. Proc. R. Soc. London, Ser. B, 2010, 277(1691), 2205–2210.
- Daniels, R. R., Amphibians of peninsular India – India a Life Scape, Universities Press, Hyderabad, India, 2005, pp. 179–182.
- Gosner, K. L., A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 1960, 16(3), 183–190.
- Brown, G. E. and Chivers, D. P., Learning as an adaptive response to predation. In Ecology of Predator–Prey Interactions, Oxford University Press, Oxford, UK, 2005, pp. 34–54.
- Kawecki, T. J., Evolutionary ecology of learning: insights from fruit flies. Popul. Ecol., 2010, 52(1), 15–25.
- Ferrari, M. C., Messier, F. and Chivers, D. P., Threat-sensitive learning of predators by larval mosquitoes Culex restuans. Behav Ecol. Sociobiol., 2008, 62(7), 1079–1083.
- Ferrari, M. C., Rive, A. C., MacNaughton, C. J., Brown, G. E. and Chivers, D. P., Fixed vs random temporal predictability of predation risk: an extension of the risk allocation hypothesis. Ethology,
- , 114(3), 238–244.
- Helfman, G. S., Threat-sensitive predator avoidance in damselfish–trumpetfish interactions. Behav. Ecol. Sociobiol., 1989, 24(1), 47–58.
- Ferrari, M. C., Brown, G. E. and Chivers, D. P., Temperaturemediated changes in rates of predator forgetting in woodfrog tadpoles. PLoS ONE, 2012, 7(12), e51143.
- Ferrari, M. C. and Chivers, D. P., Learning threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information?. Anim. Behav., 2006, 71(1), 19–26.
- Vilhunen, S., Repeated antipredator conditioning: a pathway to habituation or to better avoidance?. J. Fish Biol., 2006, 68(1), 25–43.
- Ferrari, M. C., Vrtělová, J., Brown, G. E. and Chivers, D. P., Understanding the role of uncertainty on learning and retention of predator information. Anim. Cogn., 2012, 15(5), 807–813.
- Brown, G. E. and Smith, R. J. F., Acquired predator recognition in juvenile rainbow trout (Oncorhynchus mykiss): conditioning hatchery-reared fish to recognize chemical cues of a predator. Can. J. Fish. Aquat. Sci., 1998, 55(3), 611–617.
- Hazlett, B. A., Acquistapace, P. and Gherardi, F., Differences in memory capabilities in invasive and native crayfish. J. Crust. Biol., 2002, 22(2), 439–448.
- Berejikian, B. A., Smith, R. J. F., Tezak, E. P., Schroder, S. L. and Knudsen, C. M., Chemical alarm signals and complex hatchery rearing habitats affect antipredator behavior and survival of chinook salmon (Oncorhynchus tshawytscha) juveniles. Can. J. Fish. Aquat. Sci., 1999, 56(5), 830–838.
- Brown, G. E., Ferrari, M. C., Malka, P. H., Oligny, M. A., Romano, M. and Chivers, D. P., Growth rate and retention of learned predator cues by juvenile rainbow trout: faster-growing fish forget sooner.
- Behav. Ecol. Sociobiol., 2011, 65(6), 1267–1276.
- Plotkin, H. C. and Oakley, D. A., Backward conditioning in the rabbit (Oryctolagus cuniculus). J. Comp. Physiol. Psychol., 1975, 88(2), 586.
- Matzel, L. D., Collin, C. and Alkon, D. L., Biophysical and behavioral correlates of memory storage, degradation, and reactivation. Behav. Neurosci., 1992, 106(6), 954.
- Monk, C. S., Gunderson, V. M., Grant, K. S. and Mechling, J. L., A demonstration of the memory savings effect in infant monkeys. Dev. Psychol., 1996, 32(6), 1051–1055.
- Nicholson, D. A., Sweet, J. A. and Freeman Jr, J. H., Long-term retention of the classically conditioned eyeblink response in rats. Behav. Neurosci., 2003, 117(4), 871.
- Philips, G. T., Tzvetkova, E. I., Marinesco, S. and Carew, T. J., Latent memory for sensitization in Aplysia. Learn. Mem., 2006, 13(2), 224–229.
- Gonzalo, A., López, P. and Martín, J., Iberian green frog tadpoles may learn to recognize novel predators from chemical alarm cues of conspecifics. Anim. Behav., 2007, 74(3), 447–453.
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