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Sink or swim: a test of tadpole behavioral responses to predator cues and potential alarm pheromones from skin secretions

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Abstract

Chemical signaling is a vital mode of communication for most organisms, including larval amphibians. However, few studies have determined the identity or source of chemical compounds signaling amphibian defensive behaviors, in particular, whether alarm pheromones can be actively secreted from tadpoles signaling danger to conspecifics. Here we exposed tadpoles of the common toad Bufo bufo and common frog Rana temporaria to known cues signaling predation risk and to potential alarm pheromones. In both species, an immediate reduction in swimming activity extending over an hour was caused by chemical cues from the predator Aeshna cyanea (dragonfly larvae) that had been feeding on conspecific tadpoles. However, B. bufo tadpoles did not detectably alter their behavior upon exposure to potential alarm pheromones, neither to their own skin secretions, nor to the abundant predator-defense peptide bradykinin. Thus, chemicals signaling active predation had a stronger effect than general alarm secretions of other common toad tadpoles. This species may invest in a defensive strategy alternative to communication by alarm pheromones, given that Bufonidae are toxic to some predators and not known to produce defensive skin peptides. Comparative behavioral physiology of amphibian alarm responses may elucidate functional trade-offs in pheromone production and the evolution of chemical communication.

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References

  • Apponyi MA, Pukala TL, Brinkworth CS, Maselli VM, Bowie JH, Tyler MJ, Booker GW, Wallace JC, Carver JA, Separovic F, Doyle J, Llewellyn LE (2004) Host-defence peptides of Australian anurans: structure, mechanism of action and evolutionary significance. Peptides 25:1035–1054

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Che Q, Wang X, Li J, Yang H, Li D, Zhang K, Lai R (2010) Cloning and characterization of the first amphibian bradykinin gene. Biochimie 92:226–231

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Chivers DP, Wisenden BD, Hindman CJ et al (2007) Epidermal ‘alarm substance’ cells of fishes maintained by non-alarm functions: possible defense against pathogens, parasites and UVB radiation. Proc R Soc Lond B 274:2611–2619

    Article  Google Scholar 

  • Conlon JM (1999) Bradykinin and its receptors in non-mammalian vertebrates. Regul Pept 79:71–81

    Article  PubMed  CAS  Google Scholar 

  • Conlon JM, Aronsson U (1997) Multiple bradykinin-related peptides from the skin of the frog, Rana temporaria. Peptides 18:361–365

    Article  PubMed  CAS  Google Scholar 

  • Conlon JM, Iwamuro S, King JD (2009) Dermal cytolytic peptides and the system of innate immunity in anurans. Ann NY Acad Sci 1163:75–82

    Article  PubMed  CAS  Google Scholar 

  • Daly J (1998) Thirty years of discovering arthropod alkaloids in amphibian skin. J Nat Prod 61:162–172

    Article  PubMed  CAS  Google Scholar 

  • Erspamer V (1994) Bioactive secretions of the amphibian integument. In: Heatwole G, Barthalmus T, Heatwole AT (eds) Amphibian Biology, vol 1. Surrey Beatty and Sons, Chipping Norton, pp 178–350

    Google Scholar 

  • Ferland-Raymond B, March RE, Metcalfe CD, Murray DL (2010) Prey detection of aquatic predators: assessing the identity of chemical cues eliciting prey behavioral plasticity. Biochem Syst Ecol 38:169–177

    Article  CAS  Google Scholar 

  • Flier J, Edwards MW, Daly JW, Myers CW (1980) Widespread occurrence in frogs and toads of skin compounds interacting with the ouabain site of Na + , K + ,-ATPase. Science 208:503–505

    Article  PubMed  CAS  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 behavioral inhibition and suppression of the neuroendocrine stress axis. Horm Behav 55:520–529

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Griffiths RA, Denton J (1992) Interspecific associations in tadpoles. Anim Behav 44:1153–1157

    Article  Google Scholar 

  • Hagman M, Shine R (2009) Larval alarm pheromones as a potential control for invasive cane toads (Bufo marinus) in tropical Australia. Chemoecology 19:211–217

    Article  CAS  Google Scholar 

  • Hettyey A, Zsarnóczai S, Vincze K, Hoi H, Laurila A (2010) Interactions between the information content of different chemical cues affect induced defences in tadpoles. Oikos 119:1814–1822

    Article  Google Scholar 

  • Hews DK (1988) Alarm response in larval western toads, Bufo boreas: release of larval chemicals by a natural predator and its effect on predator capture efficiency. Anim Behav 36:125–133

    Article  Google Scholar 

  • Hews DK, Blaustein AR (1985) An investigation of the alarm response in Bufo boreas and Rana cascadae tadpoles. Behav Neural Biol 43:47–57

    Article  PubMed  CAS  Google Scholar 

  • Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394

    Google Scholar 

  • Kiesecker JM, Skelly DK, Beard KH, Preisser E (1999) Behavioral reduction of infection risk. Proc Natl Acad Sci USA 96:9165–9168

    Article  PubMed  CAS  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

    Article  Google Scholar 

  • Lutterschmidt WI, Marvin GA, Hutchison VH (1994) Alarm response by a plethodontid salamander (Desmognathus ochraphaeus): conspecific and heterospecific “schreckstoff”. J Chem Ecol 20:2751–2757

    Article  CAS  Google Scholar 

  • Manteifel YB, Kiseleva EI (2011) Ammonia as a pheromone in anuran tadpoles. Physiol Res 60:185–191

    Google Scholar 

  • Marquis O, Saglio P, Neveu A (2004) Effects of predators and conspecific chemical cues on the swimming activity of Rana temporaria and Bufo bufo tadpoles. Arch Hydrobiol 160:153–170

    Article  Google Scholar 

  • Nakajima T, Yasuhara T, Falconieri EG, Visser J (1979) Occurrence of Hyp3-bradykinin in methanol extracts of the skin of the South African lepodactylid frog Heleophryne purcelli. Experientia 35:1133–1134

    Article  PubMed  CAS  Google Scholar 

  • Pask J, Woodhams DC, Rollins-Smith LA (2012) The ebb and flow of antimicrobial skin peptides defends northern leopard frogs, Rana pipiens, against chytridiomycosis. Glob Change Biol 18:1231–1238

    Article  Google Scholar 

  • Petranka JW (1989) Response to toad tadpoles to conflicting chemical stimuli: predator avoidance versus “optimal” foraging. Herpetologica 45:283–292

    Google Scholar 

  • Pollard KA (2011) Making the most of alarm signals: the adaptive value of individual discrimination in an alarm context. Behav Ecol 22:93–100

    Article  Google Scholar 

  • Rollins-Smith LA, Woodhams DC (2012) Amphibian Immunity: staying in Tune with the Environment, chap 4. In: Demas GE, Nelson RJ (eds) Ecoimmunology. Oxford University Press, New York, pp 92–143

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Semlitsch RD, Gavasso S (1992) Behavioral responses of Bufo bufo and Bufo calamita tadpoles to chemical cues of vertebrate and invertebrate predators. Ethol Ecol Evol 4:165–173

    Article  Google Scholar 

  • Smith RJF (1992) Alarm signals in fishes. Rev Fish Biol Fisheries 2:33–63

    Article  Google Scholar 

  • Snyder NFR, Snyder HA (1970) Alarm response of Diadema antillarum. Science 168:276–278

    Article  PubMed  CAS  Google Scholar 

  • Stenzler D, Atema J (1977) Alarm response of the marine mud snail, Nassarius obsoletus: specificity and behavioral priority. J Chem Ecol 3:159–171

    Article  Google Scholar 

  • Van Buskirk J (2001) Specific induced responses to different predator species in anuran larvae. J Evol Biol 14:482–489

    Article  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

    Article  Google Scholar 

  • Werner EE, Anholt BR (1993) Ecological consequences of the tradeoff between growth and mortality rates mediated by foraging activity. Am Nat 142:242–272

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Woodley SK (2010) Pheromonal communication in amphibians. J Comp Physiol A 196:713–727

    Article  CAS  Google Scholar 

  • Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the Institute of Evolutionary Biology and Environmental Studies and the Swiss National Science Foundation (31-125099 to DCW). We would like to thank J. Van Buskirk and participants in the Advanced Ecology course at the University of Zurich for valuable input. Animal care and experimental procedures were approved by the Veterinary Authority for the canton of Zürich (74/2009) collection permits were provided by the Office of Landscape and Nature.

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Correspondence to Douglas C. Woodhams.

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Maag, N., Gehrer, L. & Woodhams, D.C. Sink or swim: a test of tadpole behavioral responses to predator cues and potential alarm pheromones from skin secretions. J Comp Physiol A 198, 841–846 (2012). https://doi.org/10.1007/s00359-012-0750-1

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