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Do antipredator responses of Euphlyctis cyanophlyctis tadpoles depend on the intensity of predation risk?

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Abstract

Successful coexistence with predators depends on the ability of prey to strike a balance between the costs of predator avoidance and the benefits of foraging and reproducing as there is a trade-off between these activities. Prey animals can balance this trade-off by responding to predation risk in a manner that matches the intensity of risk posed by the predator, which is known as the threat-sensitive predator avoidance hypothesis. To test this hypothesis, we exposed larval Indian skipper frogs (Euphlyctis cyanophlyctis) to different intensities of predation risk by increasing the number of predators and the amount of biomass consumed and recorded their behaviour, morphology, and metamorphic traits. We also quantified the whole-body corticosterone to assess the physiological basis of alterations in morphology, behaviour, and life-history traits. The results indicate that behavioural responses of larval skipper frogs increased with the intensity of risk conforming to the predictions of the threat-sensitivity hypothesis. However, the morphological responses did not vary with the intensity of risk and hence did not support the predictions of the hypothesis. Interestingly, tadpoles facing a higher level of predation risk metamorphosed at the largest size, but with increased larval duration. At the physiological level, corticosterone levels increased with increases in the intensity of risk. Thus, our results suggest that certain antipredator responses may vary with the intensity of risk while others may not. Further, the results of our study also show an association between physiological and behavioural responses of larval E. cyanophlyctis to predation risk. More importantly, we show that larval skipper frogs can assess the intensity of predation risk through threat-sensitive learning by associating conspecific alarm cues with odours of dragonfly nymphs.

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References

  • Amo L, Lopez P, Martin J (2004) Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges. Anim Behav 67:647–653

    Google Scholar 

  • Arendt J (2010) Morphological correlates of sprint swimming speed in five species of spadefoot toad tadpoles: comparison of morphometric methods. J Morphol 271:1044–1052

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673

    Google Scholar 

  • Bennett AM, Pereira D, Murray DL (2013) Investment into defensive traits by anuran prey (Lithobates pipiens) is mediated by the starvation-predation risk trade-off. PLoS ONE 8:e82344

    PubMed  PubMed Central  Google Scholar 

  • Bennett AM, Longhi JN, Chin EH, Burness G, Kerr LR, Murray DL (2016) Acute changes in whole body corticosterone in response to perceived predation risk: a mechanism for anti-predator behavior in anurans? Gen Comp Endocrinol 229:62–66

    CAS  PubMed  Google Scholar 

  • Bourdeau PE (2010) Cue reliability, risk sensitivity and inducible morphological defense in a marine snail. Oecologia 162:987–994

    PubMed  Google Scholar 

  • Bourdeau PE, Johansson F (2012) Predator-induced morphological defenses as by-products of prey behaviour: a review and prospectus. Oikos 121:1175–1190

    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, Elvidge CK, Ramnarine I, Chivers DP (2013) Phenotypically plastic neophobia: a response to variable predation risk. Proc R Soc Lond B 280:20122712

    Google Scholar 

  • Buchanan AL, Hermann SL, Lund M, Szendrei Z (2017) A meta-analysis of non-consumptive predator effects in arthropods: the influence of organismal and environmental characteristics. Oikos 126:1233–1240

    Google Scholar 

  • Burraco P, Duarte LJ, Gomez-Mestre I (2013) Predator-induced physiological responses in tadpoles challenged with herbicide pollution. Curr Zool 59:475–484

    CAS  Google Scholar 

  • Cabrera-Guzmán E, Crossland MR, Brown GP, Shine R (2013) Larger body size at metamorphosis enhances survival, growth and performance of young cane toads (Rhinella marina). PLoS ONE 8:e70121

    PubMed  PubMed Central  Google Scholar 

  • Capellan E, Nicieza AG (2007) Non-equivalence of growth arrest induced by predation risk or food limitation: context-dependent compensatory growth in anuran tadpoles. J Anim Ecol 76:1026–1035

    CAS  PubMed  Google Scholar 

  • Chivers DP, Smith RJF (1998) Chemical alarm signaling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5:338–352

    Google Scholar 

  • Chivers DP, Mirza RS, Bryer PJ, Kiesecker JM (2001) Threat-sensitive predator avoidance by slimy sculpins: understanding the importance of visual versus chemical information. Can J Zool 79:867–873

    Google Scholar 

  • Crespi EJ, Williams TD, Jessop TS, Delehanty B (2013) Life-history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? Funct Ecol 27:93–106

    Google Scholar 

  • Daniels RJR (2005) In: Gadgil M (ed) India a lifescape amphibians of peninsular India. Universities press, India, pp 179–182

    Google Scholar 

  • Davenport JM, Hossack BR, Lowe WH (2014) Partitioning the non-consumptive effects of predators on prey with complex life histories. Oecologia 176:149–155

    PubMed  Google Scholar 

  • Denver RJ (2009) Stress hormones mediate environment genotype interactions during amphibian development. Gen Comp Endocrinol 164:13–20

    Google Scholar 

  • Dijk B, Laurila A, Orizaola G, Johansson F (2016) Is one defense enough? Disentangling the relative importance of morphological and behavioural predator-induced defenses. Behav Ecol Sociobiol 70:237–246

    Google Scholar 

  • Eklöv P, Werner EE (2000) Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae. Oikos 88:250–258

    Google Scholar 

  • Epp KJ (2013) Threat sensitivity in the San Marcos salamander: effects of predator diet and prey experience. Behaviour 150:617–634

    Google Scholar 

  • Ferrari MCO, Trowell JJ, Brown GE, Chivers DP (2005) The role of learning in the development of threat-sensitive predator avoidance by fathead minnows. Anim Behav 70:777–784

    Google Scholar 

  • Ferrari MCO, Capitania-Kwok T, Chivers DP (2006) The role of learning in the acquisition of threat-sensitive responses to predator odours. Behav Ecol Sociobiol 60:522–527

    Google Scholar 

  • Ferrari MCO, Messier F, Chivers DP (2008) Threat sensitive learning of predators by larval mosquitoes Culex restuans. Behav Ecol Sociobiol 62:1079–1083

    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

    Google Scholar 

  • Flynn AM, Smee DL (2010) Behavioural plasticity of the soft-shell clam, Mya arenaria (L.), in the presence of predators increases survival in the field. J Exp Mar Biol Ecol 383:32–38

    Google Scholar 

  • Fonner CW, Woodley SK (2015) Testing the predation stress hypothesis: behavioural and hormonal responses to predator cues in Allegheny Mountain dusky salamanders. Behaviour 152:797–819

    Google Scholar 

  • Fraker ME, Hu F, Cuddapah V, McCollum SA, Relyea RA, Hempel J, Denver RJ (2009) Characterization of an alarm pheromone secreted by amphibian tadpoles that induces behavioural inhibition and suppression of the neuroendocrine stress axis. Horm Behav 55:520–529

    CAS  PubMed  Google Scholar 

  • Gazzola A, Brandalise F, Rubolini D, Rossi P, Galeotti P (2015) Fear is the mother of invention: anuran embryos exposed to predator cues alter life-history traits, post-hatching behaviour and neuronal activity patterns. J Exp Biol 218:3919–3930

    PubMed  Google Scholar 

  • Glennemeier KA, Denver RJ (2002) Small changes in whole-body corticosterone content affect larval Rana pipiens fitness components. Gen Comp Endocrinol 127:16–25

    CAS  PubMed  Google Scholar 

  • Golub JL, Brown GE (2003) Are all signals the same? Ontogenetic change in the response to conspecific and heterospecific chemical alarm signals by juvenile green sunfish (Lepomis cyanellus). Behav Ecol Sociobiol 54:113–118

    Google Scholar 

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

    Google Scholar 

  • Harvell CD (1990) The ecology and evolution of inducible defenses. Q Rev Biol 65:323–340

    CAS  PubMed  Google Scholar 

  • Helfman GS (1989) Threat-sensitive predator avoidance in damselfish-trumpet fish interactions. Behav Ecol Sociobiol 24:47–58

    Google Scholar 

  • Holomuzki JR, Short TM (1990) Ontogenetic shifts in habitat use and activity in a stream-dwelling isopod. Ecography 13:300–307

    Google Scholar 

  • Hossie T, Landolt K, Murray DL (2017) Determinants and co-expression of anti-predator responses in amphibian tadpoles: a meta-analysis. Oikos 126:173–184

    Google Scholar 

  • Joshi AM, Wadekar NV, Gramapurohit NP (2017) Does corticosterone mediate predator-induced responses of larval Hylarana indica? Gen Comp Endocrinol 251:30–37

    CAS  PubMed  Google Scholar 

  • Kiesecker JM, Chivers DP, Anderson M, Blaustein AR (2002) Effect of predator diet on life-history shifts of red-legged frogs, Rana aurora. J Chem Ecol 28:1007–1015

    CAS  PubMed  Google Scholar 

  • Kishida O, Nishimura K (2004) Bulgy tadpoles: inducible defense morph. Oecologia 140:414–421

    PubMed  Google Scholar 

  • Kulkarni PS, Gramapurohit NP (2017) Effect of corticosterone on larval growth, antipredator behaviour and metamorphosis of Hylarana indica. Gen Comp Endocrinol 251:21–29

    CAS  PubMed  Google Scholar 

  • Kusch RC, Mirza RS, Chivers DP (2004) Making sense of the predator scents: investigating the sophistication of predator assessment abilities of fathead minnows. Behav Ecol Sociobiol 55:551–555

    Google Scholar 

  • Lardner B (2000) Morphological and life-history responses to predators in larvae of seven anurans. Oikos 88:169–180

    Google Scholar 

  • Large S, Smee D, Trussell G (2011) Environmental conditions influence the frequency of prey responses to predation risk. Mar Ecol Prog Ser 422:41–49

    Google Scholar 

  • Lent EM, Babbitt KJ (2020) The effects of hydroperiod and predator density on growth, development, and morphology of wood frogs (Rana sylvatica). Aquat Ecol. https://doi.org/10.1007/s10452-020-09748-y

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Google Scholar 

  • Maher JM, Werner EE, Denver RJ (2013) Stress hormones mediate predator-induced phenotypic plasticity in amphibian tadpoles. Proc R Soc Lond B 280:20123075

    Google Scholar 

  • Marcus J, Brown GE (2003) Response of pumpkinseed sunfish to conspecific chemical alarm cues: an interaction between ontogeny and stimulus concentration. Can J Zool 81:1671–1677

    Google Scholar 

  • Mathis A, 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

    CAS  Google Scholar 

  • McCollum SA, Leimberger JD (1997) Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109:615–621

    CAS  PubMed  Google Scholar 

  • McCoy MW (2007) Conspecific density determines the magnitude and character of predator-induced phenotype. Oecologia 153:871–878

    PubMed  Google Scholar 

  • McCoy MW, Bolker BM (2008) Trait-mediated interactions: influence of prey size, density and experience. J Anim Ecol 77:478–486

    PubMed  Google Scholar 

  • McCoy MW, Bolker BM, Osenberg CW, Miner BG, Vonesh JR (2006) Size correction: comparing morphological traits among populations and environments. Oecologia 148:547–554

    PubMed  Google Scholar 

  • McCoy MW, Bolker BM, Warkentin KM, Vonesh JR (2011) Predicting predation through prey ontogeny using size-dependent functional response models. Am Nat 177:752–766

    PubMed  Google Scholar 

  • McCoy MW, Touchon JC, Landberg T, Warkentin KM, Vonesh JR (2012) Prey responses to predator chemical cues: disentangling the importance of the number and biomass of prey consumed. PLoS ONE 7:1–5

    Google Scholar 

  • McMahon TA, Halstead NT, Johnson S, Raffel TR, Romansic JM, Crumrine PW, Boughton RK, Martin LB, Bohr JR (2011) The fungicide chlorothalonil is nonlinearly associated with corticosterone levels, immunity, and mortality in amphibians. Environ Health Perspect 119:1098–1103

    PubMed  PubMed Central  Google Scholar 

  • Mikolajewski DJ, Scharnweber K, Jiang B, Leicht S, Mauersberger R, Johansson F (2016) Changing the habitat: the evolution of intercorrelated traits to escape from predators. J Evol Biol 29:1394–1405

    CAS  PubMed  Google Scholar 

  • Mitchell MD, Bairos-Novak KR, Ferrari MCO (2017) Mechanisms underlying the control of responses to predator odours in aquatic prey. J Exp Biol 220:1937–1946

    PubMed  Google Scholar 

  • Munoz NE, Blumstein DT (2012) Multisensory perception in uncertain environments. Behav Ecol 23:457–462

    Google Scholar 

  • Orchinik M (1998) Glucocorticoids, stress, and behaviour: shifting the time frame. Horm Behav 152:48–56

    Google Scholar 

  • Pacheco EO, Almeida-Gomes M, Santana DJ, Guariento RD (2019) Space use and phenotypic plasticity in tadpoles under predation risk. Hydrobiologia 837:77–86

    Google Scholar 

  • Pechenik JA (2006) Larval experience and latent effects-metamorphosis is not a new beginning. Integr Comp Biol 46:323–333

    PubMed  Google Scholar 

  • Preisser EL, Orrock JL, Schmitz OJ (2007) Predator hunting mode and habitat domain alter non consumptive effects in predator–prey interactions. Ecology 88:2744–2751

    PubMed  Google Scholar 

  • Reeder DM, Kramer KM (2005) Stress in free-ranging mammals: integrating physiology, ecology and natural history. J Mammal 86:225–235

    Google Scholar 

  • Relyea RA (2000) Trait-mediated indirect effects in larval anurans: reversing competition with the threat of predation. Ecology 81:2278–2289

    Google Scholar 

  • Relyea RA (2001a) Morphological and behavioural plasticity of larval anurans in response to divergent predators. Ecology 82:523–540

    Google Scholar 

  • Relyea RA (2001b) The lasting effects of adaptive plasticity: predator-induced tadpoles become long-legged frogs. Ecology 82:1947–1955

    Google Scholar 

  • Relyea RA (2004) Fined-tuned phenotypes: tadpole plasticity under 16 combinations of predators and competitors. Ecology 85:172–179

    Google Scholar 

  • Relyea RA (2007) Getting out alive: how predators affect the decision to metamorphose. Oecologia 152:389–400

    PubMed  Google Scholar 

  • Relyea RA, Werner EE (2000) Morphological plasticity of four larval anurans distributed along an environmental gradient. Copeia 2000:178–190

    Google Scholar 

  • Scherer AE, Smee DL (2016) A review of predator diet effects on prey defensive responses. Chemoecology 26:83–100

    CAS  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

    PubMed  Google Scholar 

  • Schoeppner NM, Relyea RA (2008) Detecting small environmental differences: risk-response curves for predator-induced behaviour and morphology. Oecologia 154:743–754

    PubMed  Google Scholar 

  • Schoeppner NM, Relyea RA (2009) Interpreting the smells of predation: how alarm cues and kairomones induce different prey defenses. Funct Ecol 23:1114–1121

    Google Scholar 

  • Semlitsch RD (1990) Effects of body size, sibship, and tail injury on the susceptibility of tadpoles to dragonfly predation. Can J Zool 68:1027–1030

    Google Scholar 

  • Sih A (1992) Prey uncertainty and the balancing of antipredator and feeding needs. Am Nat 139:1052–1069

    Google Scholar 

  • Sih A, Bell AM, Kerby JL (2004) Two stressors are far deadlier than one. Trends Ecol Evol 19:274–276

    PubMed  Google Scholar 

  • Smith DC, Van Buskirk J (1995) Phenotypic design, plasticity, and ecological performance in two tadpole species. Am Nat 145:211–233

    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

    CAS  PubMed  Google Scholar 

  • Supekar SC, Gramapurohit NP (2018) Larval skipper frogs recognize kairomones of certain predators innately. J Ethol 36:143–149

    Google Scholar 

  • Supekar SC, Gramapurohit NP (2020) Does temporal variation in predation risk affect antipredator responses of larval skipper frogs (Euphlyctis cyanophlyctis)? Can J Zool 98:202–209

    Google Scholar 

  • Urban MC (2007) Predator size and phenology shape prey survival in temporary ponds. Oecologia 154:571–580

    PubMed  Google Scholar 

  • Van Buskirk J, Arioli M (2002) Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83:1580–1585

    Google Scholar 

  • Van Buskirk J, Yurewicz K (1998) Effects of predators on prey growth rate: relative contributions of thinning and reduced activity. Oikos 82:20–28

    Google Scholar 

  • Van Buskirk J, Muller C, Portmann A, Surbeck M (2002) A test of the risk allocation hypothesis: tadpole responses to temporal change in predation risk. Behav Ecol 13:526–530

    Google Scholar 

  • Van Buskirk J, Anderwald P, Lüpold S, Reinhardt L, Schuler H (2003) The lure effect, tadpole tail shape, and the target of dragonfly strikes. J Herpetol 37:420–424

    Google Scholar 

  • Vonesh JR, Warkentin KM (2006) Opposite shifts in size at metamorphosis in response to larval and metamorph predators. Ecology 87:556–562

    PubMed  Google Scholar 

  • Wahle RA (1992) Body-size dependent anti-predator mechanisms of the American lobster. Oikos 65:52–60

    Google Scholar 

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

    CAS  Google Scholar 

  • Zhao X, Chivers DP (2005) Response of juvenile goldfish (Carassius auratus) to chemical cues: relationship between response intensity, response duration and the level of predation risk. In: Mason RT, Le-Master M, Muller-Scharze D (eds) Chemical signals in vertebrates. Plenum, New York, pp 334–341

    Google Scholar 

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Funding

This work was supported by SERB/F/1344/2016-17 awarded to NPG and DST-PURSE, UGC-CAS Phase III to Department of Zoology, and RUSA to Savitribai Phule Pune University. SCS is grateful to S. P. Pune University for a research fellowship.

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Supekar, S. C. designed the study, collected, analysed, interpreted the data and drafted the manuscript. Gramapurohit, N.P. conceptualized and designed the study, provided intellectual inputs in data collection, analyses, interpretation and drafted the manuscript in addition to providing all logistic support.

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Correspondence to Narahari P. Gramapurohit.

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This study was carried out following the guidelines of the Departmental committee for animal ethics (No. 538/CPCSEA).

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Supekar, S.C., Gramapurohit, N.P. Do antipredator responses of Euphlyctis cyanophlyctis tadpoles depend on the intensity of predation risk?. Aquat Ecol 54, 823–837 (2020). https://doi.org/10.1007/s10452-020-09780-y

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