Larval skipper frogs recognise kairomones of certain predators innately

Article

Abstract

Recognising potential predators is critical for the survival and reproduction of prey animals. However, prey animals may possess an innate ability to recognise the signature odours (kairomones) of only certain native, sympatric predators, while requiring learning to recognise others. Our observations have shown that larval skipper frogs (Euphlyctis cyanophlyctis) fail to recognise kairomones of dragonfly nymph, a common predator of amphibian tadpoles with a cosmopolitan distribution. Hence, we wanted to determine if larval skipper frogs totally lack an innate mechanism to recognise kairomones of all aquatic predators, or have an innate ability to recognise kairomones of only certain predators. In a series of experiments, we tested the antipredator response of larval skipper frogs to kairomones of dragonfly nymph (Bradinopyga geminata); walking catfish (Clarias batrachus); Mozambique tilapia (Oreochromis mossambicus); two species of predatory tadpoles, Indian bullfrog (Hoplobatrachus tigerinus) and Jerdon’s bullfrog (Hoplobatrachus crassus); and the checkered keel back snake (Xenochrophis piscator). The results clearly indicate that larval skipper frogs have the innate ability to recognise kairomones of the walking catfish, both species of larval bullfrog and checkered keel back snake. However, they lack the innate ability to recognise kairomones of dragonfly nymph and Mozambique tilapia. Prey choice of the Mozambique tilapia and gape-limitation of dragonfly nymphs could be responsible for the lack of innate responses of larval skipper frogs to them. The study provides empirical evidence for the notion that prey can innately recognise certain predators.

Keywords

Antipredator response Euphlyctis cyanophlyctis Innate predator recognition Signature odour Non-native predator 

Notes

Acknowledgements

This research was supported by UGC-CAS Phase III and DRDP to the Department of Zoology, Savitribai Phule Pune University. S. C. S. is grateful to Savitribai Phule Pune University for a research fellowship. We are thankful to two anonymous referees for their critical comments on the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no potential conflicts of interest.

Ethical approval

This study was carried out in accordance with the guidelines of the 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). No animals were sacrificed during the study and all the animals used for the study were released back into nature.

References

  1. Batabyal A, Gosavi SM, 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
  2. Brown GE, Chivers DP (2005) Learning as an adaptive response to predation. In: Barbosa P, Castellanos I (eds) Ecology of predator/prey interactions. Oxford University Press, Oxford, pp 34–54Google Scholar
  3. Brown GE, Ferrari MCO, Malka PH, Russo S, Tressider M, Chivers DP (2011) Generalization of predators and non-predators by juvenile rainbow trout: learning what is and is not a threat. Anim Behav 81:1249–1256CrossRefGoogle Scholar
  4. Brown GE, Ferrari MCO, Elvidge CK, Ramnarine I, Chivers DP (2013) Phenotypically plastic neophobia: a response to variable predation risk. Proc R Soc Lond B 280:20122712CrossRefGoogle Scholar
  5. Buskirk JV, Krugel A, Kunz J, Miss F, Stamm A (2014) The rate of degradation of chemical cues indicating predation risk: an experiment and review. Ethology 120:942–949CrossRefGoogle Scholar
  6. Chivers DP, Brown GE, Smith RJF (1996) The evolution of chemical alarm signals: attracting predator’s benefits alarm signal senders. Am Nat 148:649–659CrossRefGoogle Scholar
  7. Daniels RJR (2005) Amphibians of peninsular India. In: Gadgil M (ed) India - a life scape, Universities Press, India, pp 179–182Google Scholar
  8. Davis DR, Epp KJ, Gabor CR (2012) Predator generalization decreases the effect of introduced predators in the San Marcos salamander, Eurycea nana. Ethology 118:1191–1197CrossRefGoogle Scholar
  9. Day T, Abrams PA, Chase JM (2002) The role of size-specific predation in the evolution and diversification of prey life histories. Evolution 56:877–887CrossRefPubMedGoogle Scholar
  10. DeAngelis DL, Kitchell JA, Post WM (1985) The influence of naticid predation on evolutionary strategies of bivalve prey: conclusions from a model. Am Nat 126:817–842CrossRefGoogle Scholar
  11. DeSantis DL, Davis DR, Gabor CR (2013) Chemically mediated predator avoidance in the Barton Springs salamander (Eurycea sosorum). Herpetologica 69:291–297CrossRefGoogle Scholar
  12. Dodson SI, Crowl TA, Peckarsky BL, Kats LB, Covich AP, Culp JM (1994) Non-visual communication in freshwater benthos: an overview. J N Am benthol Soc 13:268–282CrossRefGoogle Scholar
  13. Epp KJ, Gabor CR (2008) Innate and learned predator recognition mediated by chemical signals in Eurycea nana. Ethology 114:607–615CrossRefGoogle Scholar
  14. Ferrari MCO, Chivers DP (2013) Temporal dynamics of information use in learning and retention of predator-related information in tadpoles. Anim Cogn 16:667–676CrossRefPubMedGoogle Scholar
  15. Ferrari MCO, Gonzalo A, Messier F, Chivers DP (2007) Generalization of learned predator recognition: an experimental test and framework for future studies. Proc R Soc B 274:1853–1859CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ferrari MCO, Brown GE, Messier F, Chivers DP (2009) Threat-sensitive generalization of predator recognition by larval amphibians. Behav Ecol Sociobiol 63:1369–1375CrossRefGoogle Scholar
  17. Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724CrossRefGoogle Scholar
  18. Gall BG, Mathis A (2010) Innate predator recognition and the problem of introduced trout. Ethology 116:47–58CrossRefGoogle Scholar
  19. Gallardo B, Clavero M, Sanchez MI, Vila M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol 22:151–163CrossRefGoogle Scholar
  20. Gallie JA, Mumme RL, 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
  21. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  22. Grosjean S, Vences M, Dubois A (2004) Evolutionary significance of oral morphology in the carnivorous tadpoles of tiger frogs, genus Hoplobatrachus (Ranidae). Biol J Linnean Soc 81:171–181CrossRefGoogle Scholar
  23. Hossain MdL (2016) Food habits of checkered keelback, Xenochrophis piscator (schneider, 1799), in Bangladesh. Bangl J Zool 44:153–161CrossRefGoogle Scholar
  24. Indira R, Prabhu Arachi JMA, Varadharajan D (2013) Food and feeding habits of tilapiine cichlid fish Oreochromis mossambicus (Peters) from Pichavaram Mangrove, South East Coast of India. Int J Pharm Biol Arch 4:157–169Google Scholar
  25. International Union for Conservation of Nature (2009) IUCN Red List of Threatened Species version 2016-3. http://www.iucnredlist.org. Accessed 14 Dec 2008
  26. Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110CrossRefGoogle Scholar
  27. Khan MS (1996) The oropharyngeal morphology and feeding habits of tadpole of tiger frog Rana tigerina Daudin. Russ J Herpetol 3:163–171Google Scholar
  28. Kiesecker JM, Chivers DP, Marco A, Quilchano C, Anderson MT, Blaustein AR (1999) Identification of a disturbance signal in larval red-legged frogs, Rana aurora. Anim Behav 57:1295–1300CrossRefPubMedGoogle Scholar
  29. Kumar AB (2000) Exotic fishes and freshwater fish diversity. Zoos Print J 15:363–367CrossRefGoogle Scholar
  30. Laurila A (2000) Behavioural responses to predator chemical cues and local variation in antipredator performance in Rana temporaria tadpoles. Oikos 88:159–168CrossRefGoogle Scholar
  31. Mathis A, 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
  32. Murray DL, Roth JD, Wirsing AJ (2004) Predation risk avoidance by terrestrial amphibians: the role of prey experience and vulnerability to native and exotic predators. Ethology 110:635–647CrossRefGoogle Scholar
  33. Pereira RT, Leutz JACM, Valença-Silva G, Barcellos LJG, Barreto RE (2017) Ventilation responses to predator odors and conspecific chemical alarm cues in the frillfin goby. Physiol Behav 179:319–323CrossRefPubMedGoogle Scholar
  34. Petranka J, Hayes L (1998) Chemically mediated avoidance of a predatory odonate (Anax junius) by American toad (Bufo americanus) and wood frog (Rana sylvatica) tadpoles. Behav Ecol Sociobiol 42:263–271CrossRefGoogle Scholar
  35. Polo-Cavia N, Gomez-Mestre I (2014) Learned recognition of introduced predators determines survival of tadpole prey. Funct Ecol 28:432–439CrossRefGoogle Scholar
  36. Pringle R (2011) Nile Perch. In: Simberloff D, Rejmanek M (eds) Encyclopedia of biological invasions. University of California Press, Berkeley, p 484Google Scholar
  37. Saidapur SK, Veeranagoudar DK, Hiragond NC, Shanbhag BA (2009) Mechanism of predator–prey detection and behavioural responses in some anuran tadpoles. Chemoecology 19:21–28CrossRefGoogle Scholar
  38. Sakhare VB, Jetithor SG (2016) Food and feeding behaviour of Mozambique tilapia (Oreochromis mossambicus Peters) from Borna Reservoir of Maharashtra, India. J Fish 4:431–434CrossRefGoogle Scholar
  39. Schmidt BR, Amézquita A (2001) Predator-induced behavioural responses: tadpoles of the Neotropical frog Phyllomedusa tarsius do not respond to all predators. Herpetol J 11:9–16Google Scholar
  40. Schoeppner NM, Relyea RA (2005) Damage, digestion, and defense: the roles of alarm cues and kairomones for inducing prey defenses. Ecol Lett 8:505–512CrossRefPubMedGoogle Scholar
  41. Sharma SS, Veeranagoudar DK, Shanbhag BA, Saidapur SK (2008) Activity of Sphaerotheca breviceps tadpoles in response to chemical cues of the predaceous Hoplobatrachus tigerinus tadpoles. J Ethol 26:303–307CrossRefGoogle Scholar
  42. Supekar SC, Gramapurohit NP (2017) Can embryonic skipper frogs (Euphlyctis cyanophlyctis) learn to recognise kairomones in the absence of a nervous system? J Biosci 42:459–468CrossRefPubMedGoogle Scholar
  43. Takahara T, Kohmatsu Y, Maruyama A, Doi H, Yamanaka H, Yamaoka R (2012) Inducible defense behavior of an anuran tadpole: cue-detection range and cue types used against predator. Behav Ecol 23:863–868CrossRefGoogle Scholar
  44. Urban MC (2007) The growth-predation risk trade of under a growing gape-limited predation threat. Ecology 88:2587–2597CrossRefPubMedGoogle Scholar
  45. Wisenden BD (2000) Olfactory assessment of predation risk in the aquatic environment. Philos Trans R Soc Lond B Biol Sci 355:1205–1208CrossRefPubMedPubMedCentralGoogle Scholar
  46. Wisenden BD (2003) Chemically mediated strategies to counter predation. In: Collin S, Marshall NJ (eds) Sensory processing in aquatic environments. Springer, New York, pp 236–251CrossRefGoogle Scholar
  47. Wisenden BD, Chivers DP, Smith RJF (1995) Early warning in the predation sequence: a disturbance pheromone in Iowa Darters (Etheostoma exile). J Chem Ecol 21:1469–1480CrossRefPubMedGoogle Scholar
  48. Wissinger SA (1992) Niche overlap and the potential for competition and intraguild predation between size-structured populations. Ecology 73:1431–1444CrossRefGoogle Scholar
  49. Woinarski JC, Burbidge AA, Harrison PL (2015) Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement. Proc Natl Acad Sci 112:4531–4540CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Japan Ethological Society and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Swapnil C. Supekar
    • 1
  • Narahari P. Gramapurohit
    • 1
  1. 1.Department of ZoologySavitribai Phule Pune UniversityPuneIndia

Personalised recommendations