Journal of Biosciences

, Volume 42, Issue 3, pp 459–468 | Cite as

Can embryonic skipper frogs (Euphlyctis cyanophlyctis) learn to recognise kairomones in the absence of a nervous system?

  • Swapnil C Supekar
  • Narahari P GramapurohitEmail author


In this study, we used larval Euphlyctis cyanophlyctis to determine the predator recognition mechanism. We conducted a series of experiments to determine if larval E. cyanophlyctis have the innate ability to recognise predatory odour (kairomones) as a threat or if they learn to do so during ontogeny. In the case of learning, we wanted to determine the developmental window during which learning is accomplished. Further, we tested the antipredator response of predator-naïve as well as predator-experienced tadpoles to chemical cues of different origins in order to assess if they exhibit differential responses. Our results clearly indicate that predator-naïve tadpoles of E. cyanophlyctis do not reduce their activity against predatory cues of dragonfly nymphs, suggesting that they lack the innate ability to recognise kairomones. However, they could learn to do so when trained to perceive kairomones simultaneously along with alarm cues. Surprisingly, larval E. cyanophlyctis could learn to recognise kairomones through association during embryonic stages even before the development of a nervous system. Although larval E. cyanophlyctis lack the innate ability to recognise kairomones, they were able to recognise conspecific alarm cues on the first encounter, indicating that they have the innate ability to recognise alarm cues as a potential threat.


Alarm cues associative learning E. cyanophlyctis embryonic learning kairomones predator recognition 



This work was supported by UGC-CAS Phase III and DRDP to Department of Zoology, Savitribai Phule Pune University. SCS is grateful to Savitribai Phule Pune University for a research fellowship. Thanks are also due to Neelesh Dhahanukar for his help in statistical analysis. This study was carried out following the guidelines of Departmental Committee for Animal Ethics (In India, animals other than mammals do not come under the purview of the institutional committee for animal ethics, No. 538/CPCSEA).


  1. Ball P 2008 Cellular memory hints at the origins of intelligence. Nature 451 385CrossRefPubMedGoogle Scholar
  2. Batabyal A, Gosavi SM and Gramapurohit NP 2014 Determining sensitive stages for learning to recognise predators in larval bronzed frogs: importance of alarm cues in learning. J. Biosci. 39 701–710CrossRefPubMedGoogle Scholar
  3. Biju SD, Garg S, Mahony S, Wijayathilaka N, Senevirathne G and Meegaskumbura M 2014 DNA barcoding, phylogeny and systematics of Golden-backed frogs (Hylarana, Ranidae) of the Western Ghats-Sri Lanka biodiversity hotspot, with the description of seven new species. Contrib. Zool. 83 269–335 Google Scholar
  4. 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 34–53Google Scholar
  5. Brown GE, Ferrari MCO, Elvidge CK, Ramnarine I and Chivers DP 2013 Phenotypically plastic neophobia: a response to variable predation risk. Proc. R. Soc. B 280 20122712CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chivers DP, Brown GE and Smith RJF 1996 The evolution of chemical alarm signals: attracting predator’s benefits alarm signal senders. Am. Nat. 148 649–659CrossRefGoogle Scholar
  7. Chivers DP and Mirza RS 2001 Predator diet cues and the assessment of predation risk by aquatic vertebrates: a review and prospectus. In: Chemical signals in vertebrates (eds) DA Marchlewska, JJ Lepri and D Muller-Schwarze (New York: Plenum Press) pp 277–284Google Scholar
  8. Chivers DP and Smith RJF 1998 Chemical alarm signaling in aquatic predator/prey interactions: a review and prospectus. Ecoscience 5 338–352CrossRefGoogle Scholar
  9. Chivers DP, Wildy EL, Kiesecker JM and Blaustein AR 2001 Avoidance response of juvenile Pacific tree frogs to chemical cues of introduced predatory bullfrogs. J. Chem. Ecol. 27 1667–1676CrossRefPubMedGoogle Scholar
  10. Dalesman S, Rundle SD and Cotton PA 2007 Predator regime influences innate anti-predator behaviour in the freshwater gastropod Lymnaea stagnalis. Freshw. Biol. 52 2134–2140CrossRefGoogle Scholar
  11. Daniels RJR 2005 India a Lifescape Amphibians of Peninsular India (ed) M Gadgil (India: Universities Press) pp 179–182Google Scholar
  12. Dodson SI, Crowl TA, Peckarsky BL, Kats LB, Covich AP and Culp JM 1994 Non-visual communication in freshwater benthos: an overview. J. N. Am. Benthol. Soc. 13 268–282CrossRefGoogle Scholar
  13. Eklöv P 2000 Chemical cues from multiple predator–prey interactions induce changes in behavior and growth of anuran larvae. Oecologia 123 192–199CrossRefPubMedGoogle Scholar
  14. Epp KJ 2013 Threat sensitivity in the San Marcos salamander: effects of predator diet and prey experience. Behaviour 150 617–634CrossRefGoogle Scholar
  15. Epp KJ and Gabor CR 2008 Innate and learned predator recognition mediated by chemical signals in Eurycea nana. Ethology 114 607–615CrossRefGoogle Scholar
  16. Ferrari MCO and Chivers DP 2008 Cultural learning of predator recognition in mixed-species assemblages of frogs: the effect of tutor-to-observer ratio. Anim. Behav. 75 1921–1925CrossRefGoogle Scholar
  17. Ferrari MCO and Chivers DP 2009 Latent inhibition of predator recognition by embryonic amphibians. Biol. Lett. 5 160–162CrossRefPubMedGoogle Scholar
  18. Ferrari MCO, Manek AK and Chivers DP 2009 Temporal learning of predation risk by embryonic amphibians. Biol. Lett. 6 308–310CrossRefPubMedCentralGoogle Scholar
  19. Ferrari MCO, Messier F and Chivers DP 2008 Threat-sensitive learning of predators by larval mosquitoes Culex restuans. Behav. Ecol. Sociobiol. 62 1079–1083CrossRefGoogle Scholar
  20. Ferrari MCO, Wisenden BD and Chivers DP 2010 Chemical ecology of predator prey interactions in aquatic ecosystems: a review and prospectus. Can. J. Zool. 88 698–724CrossRefGoogle Scholar
  21. Ferrer RP and Zimmer RK 2007 The scent of danger: arginine as an olfactory cue of reduced predation risk. J. Exp. Biol. 210 1768–1775CrossRefPubMedGoogle Scholar
  22. Gall BG and Mathis A 2010 Innate predator recognition and the problem of introduced trout. Ethology 116 47–58CrossRefGoogle Scholar
  23. Gallie JA, Mumme RL and Wissinger SA 2001 Experience has no effect on the development of chemosensory recognition of predators by tadpoles of the American Toad, Bufo americanus. Herpetologica 57 376–383Google Scholar
  24. Gonzalo A, Lopez P and Martin J 2007 Iberian green frog tadpoles may learn to recognise novel predators from chemical alarm cues of conspecifics. Anim. Behav. 74 447–453CrossRefGoogle Scholar
  25. Gosner KL 1960 A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16 183–190Google Scholar
  26. Griffin AS 2004 Social learning about predators: a review and prospectus. Learn. Behav. 32 131–140CrossRefPubMedGoogle Scholar
  27. Griffiths RA, Schley L, Sharp PE, Dennis JL and Roman A 1998 Behavioural responses of Mallorcan midwife toad tadpoles to natural and unnatural snake predators. Anim. Behav. 55 207–214CrossRefPubMedGoogle Scholar
  28. Hawkins LA, Magurran AE and Armstrong JD 2004 Innate predator recognition in newly-hatched Atlantic salmon. Behaviour 141 1249–1262CrossRefGoogle Scholar
  29. Hepper PG and Waldman B 1992 Embryonic olfactory learning in frogs. Q. J. Exp. Psychol. B 44 179–197PubMedGoogle Scholar
  30. Horat P and Semlitsch RD 1994 Effects of predation risk and hunger on the behaviour of two species of tadpoles. Behav. Ecol. Sociobiol. 34 393–401CrossRefGoogle Scholar
  31. Kats LB and Dill LM 1998 The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5 361–394CrossRefGoogle Scholar
  32. Kelley JL and Magurran AE 2003 Learned predator recognition and antipredator responses in fishes. Fish Fish. 4 216–226CrossRefGoogle Scholar
  33. Kiesecker JM, Chivers DP, Marco A, Quilchano C, Anderson MT and Blaustein AR 1999 Identification of a disturbance signal in larval red-legged frogs, Rana aurora. Anim. Behav. 57 1295–1300CrossRefPubMedGoogle Scholar
  34. Laurila A 2000 Behavioural responses to predator chemical cues and local variation in antipredator performance in Rana temporaria tadpoles. Oikos 88 159–168CrossRefGoogle Scholar
  35. Lima SL and Dill LM 1990 Behavioural decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68 619–640CrossRefGoogle Scholar
  36. 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 2603–2607CrossRefPubMedPubMedCentralGoogle Scholar
  37. 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. 46 645–656CrossRefGoogle Scholar
  38. Mirza RS and Chivers DP 2001 Learned recognition of heterospecific alarm signals: the importance of a mixed predator diet. Ethology 107 1007–1018CrossRefGoogle Scholar
  39. Mirza RS and Chivers DP 2003 Fathead minnows learn to recognise heterospecific alarm cues they detect in the diet of a known predator. Behaviour 140 1359–1369CrossRefGoogle Scholar
  40. Mirza RS, Ferrari MCO, Kiesecker JM and Chivers DP 2006 Responses of American toad tadpoles to predation cues: behavioural response thresholds, threat sensitivity and acquired predation recognition. Behaviour 143 877–889CrossRefGoogle Scholar
  41. 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 79–386CrossRefGoogle Scholar
  42. Ogurtsov SV and Bastakov AV 2001 Imprinting on native pond odour in the pool frog, Rana lessonae cam. In: Chemical signals in Vertebrates 9 (eds) A Marchlewska-Koj, JJ Lepri and D. Muller-Schwarze (New York: Kluwer Academic/Plenum Publishers) pp 433–438Google Scholar
  43. Parker DA and Shulman MJ 1986 Avoiding predation: alarm responses of Caribbean Sea urchins to simulated predation on conspecific and heterospecific sea urchins. Mar. Biol. 93 201–208CrossRefGoogle Scholar
  44. 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 1329–1336CrossRefGoogle Scholar
  45. Schoeppner NM and Relyea RA 2005 Damage, digestion and defence: the role of alarm cues and kairomones for inducing prey defences. Ecol. Lett. 8 505–512CrossRefPubMedGoogle Scholar
  46. Smith JJ, Leduc AOHC and Brown GE 2008 Chemically mediated learning in juvenile rainbow trout. Does predator odour pH influence intensity and retention of acquired predator recognition? J. Fish Biol. 72 1750–1760CrossRefGoogle Scholar
  47. Spaeti U 1978 Development of the sensory systems in the larval and metamorphosing European grass frog (Rana temporaria L.). J. Hirnforsch. 19 543–575PubMedGoogle Scholar
  48. Sullivan AM, Madison DM and Rohr JR 2003 Behavioural responses by red-backed salamander to conspecific and heterospecific cues. Behaviour 140 553–564CrossRefGoogle Scholar
  49. Vilhunen S and Hirvonen H 2003 Innate antipredator responses of Arctic charr (Salvelinus alpinus) depend on predator species and their diet. Behav. Ecol. Sociobiol. 55 1–10CrossRefGoogle Scholar
  50. Wilson DJ and Lefcort H 1993 The effect of predator diet on the alarm response of red-legged frog, Rana aurora tadpoles. Anim. Behav. 46 1017–1019CrossRefGoogle Scholar
  51. Wisenden BD 2000 Olfactory assessment of predation risk in the aquatic environment. Philos. Trans. R. Soc. Lond. B 355 1205–1208CrossRefGoogle Scholar
  52. Wisenden BD 2003 Chemically mediated strategies to counter predation. In: Sensory processing in aquatic environments (eds) SP Collin and NJ Marshall (New York: Springer) pp 236–251CrossRefGoogle Scholar
  53. Wisenden BD Chivers DP and Smith RJF 1995 Early warning in the predation sequence: a disturbance pheromone in Iowa Darters (Etheostoma exile). J. Chem. Ecol. 21 1469–1480CrossRefPubMedGoogle Scholar
  54. Woody DR and Mathis A 1998 Acquired recognition of chemical stimuli from an unfamiliar predator: associative learning by adult newts Notophthalmus viridescens. Copeia 4 1027–1031CrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2017

Authors and Affiliations

  1. 1.Department of ZoologySavitribai Phule Pune UniversityPuneIndia

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