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Larval skipper frogs recognise kairomones of certain predators innately

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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.

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References

  • 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 39:701–710

    Article  PubMed  Google Scholar 

  • 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 34–54

    Google Scholar 

  • 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 81:1249–1256

    Article  Google Scholar 

  • 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 280:20122712

    Article  Google Scholar 

  • 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 120:942–949

    Article  Google Scholar 

  • Chivers DP, Brown GE, Smith RJF (1996) The evolution of chemical alarm signals: attracting predator’s benefits alarm signal senders. Am Nat 148:649–659

    Article  Google Scholar 

  • Daniels RJR (2005) Amphibians of peninsular India. In: Gadgil M (ed) India - a life scape, Universities Press, India, pp 179–182

    Google Scholar 

  • Davis DR, Epp KJ, Gabor CR (2012) Predator generalization decreases the effect of introduced predators in the San Marcos salamander, Eurycea nana. Ethology 118:1191–1197

    Article  Google Scholar 

  • Day T, Abrams PA, Chase JM (2002) The role of size-specific predation in the evolution and diversification of prey life histories. Evolution 56:877–887

    Article  PubMed  Google Scholar 

  • DeAngelis DL, Kitchell JA, Post WM (1985) The influence of naticid predation on evolutionary strategies of bivalve prey: conclusions from a model. Am Nat 126:817–842

    Article  Google Scholar 

  • DeSantis DL, Davis DR, Gabor CR (2013) Chemically mediated predator avoidance in the Barton Springs salamander (Eurycea sosorum). Herpetologica 69:291–297

    Article  Google Scholar 

  • 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 13:268–282

    Article  Google Scholar 

  • Epp KJ, Gabor CR (2008) Innate and learned predator recognition mediated by chemical signals in Eurycea nana. Ethology 114:607–615

    Article  Google Scholar 

  • Ferrari MCO, Chivers DP (2013) Temporal dynamics of information use in learning and retention of predator-related information in tadpoles. Anim Cogn 16:667–676

    Article  PubMed  Google Scholar 

  • 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 274:1853–1859

    Article  PubMed  Google Scholar 

  • Ferrari MCO, Brown GE, Messier F, Chivers DP (2009) Threat-sensitive generalization of predator recognition by larval amphibians. Behav Ecol Sociobiol 63:1369–1375

    Article  Google Scholar 

  • Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724

    Article  Google Scholar 

  • Gall BG, Mathis A (2010) Innate predator recognition and the problem of introduced trout. Ethology 116:47–58

    Article  Google Scholar 

  • Gallardo B, Clavero M, Sanchez MI, Vila M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol 22:151–163

    Article  Google Scholar 

  • 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 57:376–383

    Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • 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 81:171–181

    Article  Google Scholar 

  • Hossain MdL (2016) Food habits of checkered keelback, Xenochrophis piscator (schneider, 1799), in Bangladesh. Bangl J Zool 44:153–161

    Article  Google Scholar 

  • 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 4:157–169

    Google Scholar 

  • International Union for Conservation of Nature (2009) IUCN Red List of Threatened Species version 2016-3. http://www.iucnredlist.org. Accessed 14 Dec 2008

  • Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110

    Article  Google Scholar 

  • Khan MS (1996) The oropharyngeal morphology and feeding habits of tadpole of tiger frog Rana tigerina Daudin. Russ J Herpetol 3:163–171

    Google Scholar 

  • 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 57:1295–1300

    Article  CAS  PubMed  Google Scholar 

  • Kumar AB (2000) Exotic fishes and freshwater fish diversity. Zoos Print J 15:363–367

    Article  Google Scholar 

  • Laurila A (2000) Behavioural responses to predator chemical cues and local variation in antipredator performance in Rana temporaria tadpoles. Oikos 88:159–168

    Article  CAS  Google Scholar 

  • 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 46:645–656

    Article  Google Scholar 

  • 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 110:635–647

    Article  Google Scholar 

  • 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 179:319–323

    Article  CAS  PubMed  Google Scholar 

  • 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 42:263–271

    Article  Google Scholar 

  • Polo-Cavia N, Gomez-Mestre I (2014) Learned recognition of introduced predators determines survival of tadpole prey. Funct Ecol 28:432–439

    Article  Google Scholar 

  • Pringle R (2011) Nile Perch. In: Simberloff D, Rejmanek M (eds) Encyclopedia of biological invasions. University of California Press, Berkeley, p 484

    Google Scholar 

  • Saidapur SK, Veeranagoudar DK, Hiragond NC, Shanbhag BA (2009) Mechanism of predator–prey detection and behavioural responses in some anuran tadpoles. Chemoecology 19:21–28

    Article  Google Scholar 

  • Sakhare VB, Jetithor SG (2016) Food and feeding behaviour of Mozambique tilapia (Oreochromis mossambicus Peters) from Borna Reservoir of Maharashtra, India. J Fish 4:431–434

    Article  Google Scholar 

  • Schmidt BR, Amézquita A (2001) Predator-induced behavioural responses: tadpoles of the Neotropical frog Phyllomedusa tarsius do not respond to all predators. Herpetol J 11:9–16

    Google Scholar 

  • Schoeppner NM, Relyea RA (2005) Damage, digestion, and defense: the roles of alarm cues and kairomones for inducing prey defenses. Ecol Lett 8:505–512

    Article  PubMed  Google Scholar 

  • 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 26:303–307

    Article  Google Scholar 

  • Supekar SC, Gramapurohit NP (2017) Can embryonic skipper frogs (Euphlyctis cyanophlyctis) learn to recognise kairomones in the absence of a nervous system? J Biosci 42:459–468

    Article  CAS  PubMed  Google Scholar 

  • 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 23:863–868

    Article  Google Scholar 

  • Urban MC (2007) The growth-predation risk trade of under a growing gape-limited predation threat. Ecology 88:2587–2597

    Article  PubMed  Google Scholar 

  • Wisenden BD (2000) Olfactory assessment of predation risk in the aquatic environment. Philos Trans R Soc Lond B Biol Sci 355:1205–1208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wisenden BD (2003) Chemically mediated strategies to counter predation. In: Collin S, Marshall NJ (eds) Sensory processing in aquatic environments. Springer, New York, pp 236–251

    Chapter  Google Scholar 

  • Wisenden BD, Chivers DP, Smith RJF (1995) Early warning in the predation sequence: a disturbance pheromone in Iowa Darters (Etheostoma exile). J Chem Ecol 21:1469–1480

    Article  CAS  PubMed  Google Scholar 

  • Wissinger SA (1992) Niche overlap and the potential for competition and intraguild predation between size-structured populations. Ecology 73:1431–1444

    Article  Google Scholar 

  • 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 112:4531–4540

    Article  CAS  PubMed  Google Scholar 

Download references

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.

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  1. Department of Zoology, Savitribai Phule Pune University, Ganeshkhind, Pune, 411007, India

    Swapnil C. Supekar & Narahari P. Gramapurohit

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  1. Swapnil C. Supekar
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  2. Narahari P. Gramapurohit
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Correspondence to Narahari P. Gramapurohit.

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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.

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Supekar, S.C., Gramapurohit, N.P. Larval skipper frogs recognise kairomones of certain predators innately. J Ethol 36, 143–149 (2018). https://doi.org/10.1007/s10164-018-0545-0

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