Abstract
Successful survival and reproduction of prey organisms depend on their ability to detect their potential predators accurately and respond effectively with suitable defences. Predator detection can be innate or can be acquired through learning. We studied prey–predator interactions in the larval bronzed frogs (Sylvirana temporalis), which have the innate ability to detect certain predators. We conducted a series of experiments to determine if the larval S. temporalis rely solely on innate predator detection mechanisms or can also learn to use more specific cues such as conspecific alarm cues for the purpose. The results of our study clearly indicate that larval S. temporalis use both innate and learned mechanisms for predator detection. Predator-naïve tadpoles could detect kairomones alone as a potential threat and responded by reducing activity, suggesting an innate predator detection mechanism. Surprisingly, predator-naïve tadpoles failed to detect conspecific alarm cues as a potential threat, but learned to do so through experience. After acquiring the ability to detect conspecific alarm cues, they could associate novel predator cues with conspecific alarm cues. Further, post feeding stages of larval S. temporalis are sensitive for learning to detect conspecific alarm cues to label novel predators.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amo L, López P and 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
Boothby KM and Roberts A 1995 Effects of site of tactile stimulation on the escape swimming responses of hatchling Xenopus laevis embryos. J. Zool. 235 113–125
Brown GE and Chivers DP 2005 Learning as an adaptive response to predation; in Ecology of predator-prey interactions (eds) P Barbosa and P Castellanos (New York: Oxford University Press) pp 34–53
Cabido C, Gonzalo A, Galán P, Martín J and López P 2004 Chemosensory predator recognition induces defensive behavior in the slow-worm (Anguis fragilis). Can. J. Zool. 82 510–515
Chivers DP and Mirza RS 2001 Importance of predator diet cues in responses of larval wood frogs to fish and invertebrate predators. J. Chem. Ecol. 27 45–51
Chivers DP and Smith RJF 1998 Chemical alarm signaling in aquatic predator-prey systems: a review and prospectus. Écoscience 5 338–352
Chivers DP, Kiesecker JM, Anderson MT, Wildy EL and Blaustein AR 1996 Avoidance response of a terrestrial salamander (Ambystoma macrodactylum) to chemical alarm cues. J. Chem. Ecol. 22 1709–1716
Epp KJ and Gabor CR 2008 Innate and learned predator recognition mediated by chemical signals in Eurycea nana. Ethology 114 607–615
Ferrari MCO, Wisenden BD and Chivers DP 2010 Chemical ecology of predator prey interactions in aquatic ecosystems: a review and prospectus. Can. J. Zool. 88 698–724
Ferrer RP and Zimmer RK 2007 The scent of danger: Arginine as an olfactory cue of reduced predation risk. J. Exp. Biol. 210 1768–1775
Gonzalo A, Lopez P and Martin J 2007 Iberian green frog tadpoles may learn to recognize novel predators from chemical alarm cues of conspecifics. Anim. Behav. 74 447–453
Gosner KL 1960 A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16 183–190
Griffiths RA, Schley L, Sharp PE, Dennis JL and Roman A 1998 Behavioral responses of Mallorcan midwife toad tadpoles to natural and unnatural snake predators. Anim. Behav. 55 207–214
Kats LB and Dill LM 1998 The scent of death: chemosensory assessment of predation by prey animals. Écoscience 5 361–394
Lima SL and Dill LM 1990 Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68 619–640
Mandrillon AL and Saglio P 2005 Prior exposure to conspecific chemical cues affects predator recognition in larval common toad (Bufo bufo). Arch. Hydrobiol. 164 1–12
Mathis A, Ferrari MCO, Windel N, Messier F and Chivers DP 2008 Learning by embryos and the ghost of predation future. Proc. R. Soc. B. 275 2603–2607
Mathis A and Smith RJF 1993 Fathead minnows, Pimephales promelas, learn to recognise northern pike, Esox lucius, as predators on the basis of chemical stimuli from minnows in the pike’s diet. Anim. Behav. 46 645–656
Mathis A and Vincent F 2000 Differential use of visual and chemical cues in predator recognition and threat sensitive predator-avoidance responses by larval newts (Notophthalmus viridescens). Can. J. Zool. 78 1646–1652
Mathis A, Murray KL and Hickman CR 2003 Do experience and body size play a role in responses of larval ringed salamanders, Ambystoma annulatum, to predator kairomones? Laboratory and field assays. Ethology 109 159–170
Mirza RS and Chivers DP 2001 Learned recognition of heterospecific alarm signals: the importance of a mixed predator diet. Ethology 107 1007–1018
Mogali SM, Saidapur SK and Shanbhag BA 2012 Tadpoles of the bronze frog (Rana temporalis) assess predation risk before evoking antipredator defense behavior. J. Ethol. 30 379–386
Parker DA and Shulman DA 1986 Avoiding predation: alarm responses of Caribbean Sea urchins to simulated predation on conspecific and heterospecific Sea urchins. Mari. Biol. 93 201–208
Petranka JW, Kats LB and Sih A 1987 Predatoreprey interactions among fish and larval amphibians: use of chemical cues to detect predatory fish. Anim. Behav. 35 420–425
Raymond BF and Murray DL 2008 Predator diet and prey adaptive responses: can tadpoles distinguish between predators feeding on congeneric vs. conspecific prey? Can. J. Zool. 86 1329–1336
Schoeppner NM and Relyea RA 2005 Damage, digestion and defence: the role of alarm cues and kairomones for inducing prey defences. Ecol. Lett. 8 505–512
Sullivan AM, Madison DM and Rohr JR 2003 Behavioural responses by Red- backed salamander to conspecific and heterospecific cues. Behaviour 140 553–564
Tollrian R and Harvell CD 1999 The ecology and evolution of inducible defenses (New Jersey: Princeton University Press, Princeton)
Wildy AL and Blaustein AR 2001 Learned recognition of intraspecific predators in the larval long-toed salamanders Ambystoma macrodactylaum. Ethology 107 479–493
Wisenden BD 2003 Chemically mediated strategies to counter predation; in Sensory processing in aquatic environments (eds) SP Collin and NJ Marshall (New York: Springer Verlag) pp 236–251
Woody DR and Mathis A 1998 Acquired recognition of chemical stimuli from an unfamiliar predator: Associative learning by adult newts Notophthalmus viridescens. Copeia 1 1027–1031
Acknowledgements
The research work was supported from grants from the University Grants Commission [F. 37-467/2009 (SR)] and UGC-CAS Phase II, Department of Zoology, University of Pune. SMG is grateful to UGC for a research fellowship. Thanks are due to Ms Richa Sharma, Department of Statistics, University of Pune, for her help in statistical analyses of the data.
Author information
Authors and Affiliations
Corresponding author
Additional information
Corresponding editor: Renee M Borges
[Batabyal A, Gosavi SM and Gramapurohit NP 2014 Determining sensitive stages for learning to detect predators in larval bronzed frogs: Importance of alarm cues in learning. J. Biosci. 39 1–10] DOI 10.1007/s12038-014-9455-7
Rights and permissions
About this article
Cite this article
Batabyal, A., Gosavi, S.M. & Gramapurohit, N.P. Determining sensitive stages for learning to detect predators in larval bronzed frogs: Importance of alarm cues in learning. J Biosci 39, 701–710 (2014). https://doi.org/10.1007/s12038-014-9455-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12038-014-9455-7