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Space use and phenotypic plasticity in tadpoles under predation risk

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Abstract

Food acquisition by most organisms is a complex ecological process that involves benefits and risks, affecting organism development and interspecific interactions. The evaluation of habitat selection, food consumption, and predator avoidance is pivotal for understanding the ecological process affecting life history traits and the role of species on communities and ecosystems. In a microcosm experiment, we evaluated if Rhinella diptycha tadpoles actively choose to forage in habitats with high resource (food) availability and if they avoid such habitats when predators are positively correlated with resource distribution. We also evaluated if behavioral changes under predation risk were associated with specific morphological phenotypes. We observed that tadpoles chose, although not intensely, habitats with high resource availability when predator cues were absent, but they avoided the same habitats when predation cues were present. We also observed an increase in swimming activity and morphological changes in tadpoles exposed to predation risk, especially related to body and tail morphology, which translates into rapid development. Our results suggest that tadpoles assess habitat quality through resource availability and predation risk. Moreover, our results suggest that tadpoles seem to exhibit functionally independent co-specialization of defensive strategies, due to the expression of specific behavioral and morphological phenotypes.

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References

  • Abrahams, M. & L. Dill, 1989. A determination of the energetic equivalence of the risk of predation. Ecology 70: 999–1007.

    Article  Google Scholar 

  • Alonzo, S. H., 2002. State-dependent habitat selection games between predators and prey: the importance of behavioural interactions and expected lifetime reproductive success. Evolutionary Ecology Research 4: 759–778.

    Google Scholar 

  • Anderson, R. B. & S. P. Lawler, 2016. Behavioral changes in tadpoles after multigenerational exposure to an invasive intraguild predator. Behavioral Ecology 27: 1790–1796.

    Article  Google Scholar 

  • Appleton, R. D. & R. A. Palmer, 1988. Water-borne stimuli released by predator crabs and damage prey induce more predator-resistant shells in a marine gastropod. Proceedings of the National Academy of Sciences 85: 4387–4391.

    Article  CAS  Google Scholar 

  • Bernot, R. J. & A. M. Turner, 2001. Predator identity and trait-mediated indirect effects in a littoral food web. Oecologia 129: 139–146.

    Article  PubMed  Google Scholar 

  • Bookstein, F. L., 1997. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge.

    Google Scholar 

  • Boyce, M. S., C. J. Johnson, E. H. Merrill, S. E. Nielsen, E. J. Solberg & B. Moorter, 2016. Can habitat selection predict abundance? Journal of Animal Ecology 85: 11–20.

    Article  PubMed  Google Scholar 

  • Brown, J. S., B. P. Kotler & A. Bouskila, 2001. Ecology of fear: foraging games between predators and prey with pulsed resources. Annales Zoologici Fennici 38: 71–87.

    Google Scholar 

  • Caldwell, G. S., 1986. Predation as a selective force on foraging herons: effects of plumage color and flocking. The Auk 103: 494–505.

    Google Scholar 

  • Chivers, D. P. & R. J. F. Smith, 1998. Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5: 338–352.

    Article  Google Scholar 

  • Costello, D. M. & M. J. Michel, 2013. Predator-induced defenses in tadpoles confound body stoichiometry predictions of the general stress paradigm. Ecology 94: 2229–2236.

    Article  PubMed  Google Scholar 

  • Crossland, M. R. & C. Azevedo-Ramos, 1999. Effects of Bufo (Anura: bufonidae) toxin on tadpoles from native and exotic Bufo habitats. Herpetologica 55: 192–199.

    Google Scholar 

  • Davies, G. M. & A. Gray, 2015. Don’t let spurious accusations of pseudoreplication limit our ability to learn from natural experiments (and other messy kinds of ecological monitoring). Ecology and Evolution 5: 5295–5304.

    Article  PubMed  PubMed Central  Google Scholar 

  • DeWitt, T. J. & R. B. Langerhans, 2003. Multiple prey traits, multiple predators: keys to understanding complex community dynamics. Journal of Sea Research 49: 143–145.

    Article  Google Scholar 

  • DeWitt, T. J., B. W. Robinson & D. S. Wilson, 2000. Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evolutionary Ecology Research 2: 129–148.

    Google Scholar 

  • Edelaar, P., A. M. Siepielski & J. Clobert, 2008. Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution 62: 2462–2472.

    Article  PubMed  Google Scholar 

  • Eklöv, P. & R. Svanbak, 2006. Predation risk influences adaptive morphological variation in fish populations. The American Naturalist 167: 440–452.

    Article  PubMed  Google Scholar 

  • Ferguson, S. H., A. T. Bergerud & R. Ferguson, 1988. Predation risk and habitat selection in the persistence of a remnant caribou population. Oecologia 76: 236–245.

    Article  CAS  PubMed  Google Scholar 

  • Godin, J. & M. Keenleyside, 1984. Foraging on on patchily distributed prey by a cichlid fish (Teleosteicichlidae): a test of the ideal free distribution theory. Animal Behaviour 32: 120–131.

    Article  Google Scholar 

  • Gosner, K. L., 1960. A simplified table for staging anuran embryos larvae with notes on identification. Herpetologica 16: 183–190.

    Google Scholar 

  • Gotceitas, V., 1990. Foraging and predator avoidance: a test of a patch choice model with juvenile bluegill sunfish. Oecologia 83: 346–351.

    Article  PubMed  Google Scholar 

  • Guariento, R. D., B. Luttbeg, T. Mehner & F. A. Esteves, 2014. The effect of predation pressure and predator adaptive foraging on the relative importance of consumptive and non-consumptive predator net effects in a freshwater model system. Oikos 123: 705–713.

    Article  Google Scholar 

  • Guariento, R. D., B. Luttbeg, L. S. Carneiro & A. Caliman, 2018. Prey adaptive behaviour under predation risk modify stoichiometry predictions of predator-induced stress paradigms. Functional Ecology 32: 1631–1643.

    Article  Google Scholar 

  • Guariento, R. D., L. S. Carneiro, F. A. Esteves, J. S. Jorge & A. Caliman, 2015. Conspecific density affects predator-induced prey phenotypic plasticity. Ecosphere 6: 1–12.

    Article  Google Scholar 

  • Gunzburger, M. S. & J. Travis, 2004. Evaluating predation pressure on green treefrog larvae across a habitat gradient. Oecologia 140: 422–429.

    Article  PubMed  Google Scholar 

  • Hammill, E. & A. P. Beckerman, 2010. Reciprocity in predator-prey interactions: exposure to defended prey and predation risk affects intermediate predator life history and morphology. Oecologia 163: 193–202.

    Article  PubMed  Google Scholar 

  • Hammond, J. I., B. Luttbeg & A. Sih, 2007. Predator and prey space use: dragonflies and tadpoles in an interactive game. Ecology 88: 1525–1535.

    Article  PubMed  Google Scholar 

  • Hanski, I. & O. Ovaskainen, 2000. The metapopulation capacity of a fragmented landscape. Nature 404: 755.

    Article  CAS  PubMed  Google Scholar 

  • Heithaus, M. R. & L. M. Dill, 2002. Food availability and tiger shark predation risk. Ecology 83: 480–491.

    Article  Google Scholar 

  • Hero, J. M., W. E. Magnusson, C. F. Rocha & C. P. Catterall, 2001. Antipredator defenses influence the distribution of amphibian prey species in the central Amazon rain forest. Biotropica 33: 131–141.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Howe, N. R. & Y. M. Sheikh, 1975. Anthopleurine: a sea anemone alarm pheromone. Science 189: 386–388.

    Article  CAS  PubMed  Google Scholar 

  • Jara, F. G. & M. G. Perotti, 2010. Risk of predation and behavioural response in three anuran species: influence of tadpole size and predator type. Hydrobiologia 644: 313–324.

    Article  Google Scholar 

  • Kacelnik, A., J. R. Krebs & C. Bernstein, 1992. The ideal free distribution and predator-prey populations. Trends in Ecology & Evolution 7: 50–55.

    Article  CAS  Google Scholar 

  • Kerfoot, W. C., 1987. Translocation experiments: bosmina responses to copepod predation. Ecology 68: 596–610.

    Article  Google Scholar 

  • Kotler, B. P. & L. Blaustein, 1995. Titrating food and safety in a heterogenous environment: when are the risky and safety patches of equal value? Oikos 74: 251–258.

    Article  Google Scholar 

  • Krivan, V., 1997. Dynamic ideal free distribution: effects of optimal patch choice on predator-prey dynamics. The American Naturalist 149: 164–178.

    Article  Google Scholar 

  • Krivan, V., 2003. Ideal free distributions when resources undergo population dynamics. Theoretical Population Biology 64: 25–38.

    Article  PubMed  Google Scholar 

  • Lima, S. L., 1998. Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Advances in the Study of Behavior 27: 215–290.

    Article  Google Scholar 

  • Lima, S. L. & L. M. Dill, 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68: 619–640.

    Article  Google Scholar 

  • Lima, S. L. & P. A. Bednekoff, 1999. Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. The American Naturalist 153: 649–659.

    Article  PubMed  Google Scholar 

  • Luttbeg, B., J. I. Hammond & A. Sih, 2008. Dragonfly larvae and tadpole frog space use games in varied light conditions. Behavioral Ecology 20: 13–21.

    Article  Google Scholar 

  • Luttbeg, B. & A. Sih, 2004. Predator and prey habitat selection games: the effects of how prey balance foraging and predation risk. Israel Journal of Zoology 50: 233–254.

    Article  Google Scholar 

  • McCollum, S. A. & J. D. Leimberger, 1997. Predator-induced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109: 615–621.

    Article  CAS  PubMed  Google Scholar 

  • McCoy, M. W., B. M. Bolker, C. W. Osenberg, B. G. Miner & J. R. Vonesh, 2006. Size correction: comparing morphological traits among populations and environments. Oecologia 148: 547–554.

    Article  PubMed  Google Scholar 

  • McDiarmid, R. W. & R. Altig, 1999. Tadpoles: The Biology of Anuran Larvae. The University of Chicago Press, Chicago.

    Google Scholar 

  • McIvor, C. C. & W. E. Odum, 1988. Food, predation risk, and microhabitat selection in a marsh fish assemblage. Ecology 69: 1341–1351.

    Article  Google Scholar 

  • Nomura, F., V. H. M. Prado, F. R. Silva, R. E. Borges, N. Y. N. Dias & D. D. C. Rossa-Feres, 2011. Are you experienced? Predator type and predator experience trade-offs in relation to tadpole mortality rates. Journal of Zoology 284: 144–150.

    Article  Google Scholar 

  • Pease, C. M., R. Lande & J. J. Bull, 1989. A model of population growth, dispersal and evolution in a changing environment. Ecology 70: 1657–1664.

    Article  Google Scholar 

  • Peckarsky, B. L., 1982. Aquatic insect predator-prey relations. BioScience 32: 261–266.

    Article  Google Scholar 

  • Perotti, M. G., L. A. Fitzgerald, L. Moreno & M. Pueta, 2006. Behavioral responses of Bufo arenarum tadpoles to odonate naiad predation. Herpetological Conservation and Biolology 1: 117–120.

    Google Scholar 

  • Peterson, C. H. & G. A. Skilleter, 1994. Control of foraging behavior of individuals within an ecosystem context: the clam Macoma balthica, flow environment, and siphon-cropping fishes. Oecologia 100: 256–267.

    Article  PubMed  Google Scholar 

  • Pigliucci, M., 2003. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecology Letters 6: 265–272.

    Article  Google Scholar 

  • Pigliucci, M., 2005. Evolution of phenotypic plasticity: where are we going now? Trends in Ecology and Evolution 20: 481–486.

    Article  PubMed  Google Scholar 

  • Prevedello, J. A., G. Forero-Medina & M. V. Vieira, 2010. Movement behaviour within and beyond perceptual ranges in three small mammals: effects of matrix type and body mass. Journal of Animal Ecology 79: 1315–1323.

    Article  PubMed  Google Scholar 

  • R Development Core Team, 2016. R: a langauge and environment for statistical coumputing. R Foundation for Statistical Computing, Vienna, Austria. http://R-project.org.

  • Ravigné, V., U. Dieckmann & I. Olivieri, 2009. Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. The American Naturalist 174: E141–E169.

    Article  PubMed  Google Scholar 

  • Relyea, R. A., 2001. Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82: 523–540.

    Article  Google Scholar 

  • Relyea, R. A. & J. T. Hoverman, 2003. The impact of larval predators and competitors on the morphology and fitness of juvenile treefrogs. Oecologia 134: 596–604.

    Article  PubMed  Google Scholar 

  • Repka, S. & K. Pihlajamaa, 1996. Predator-induced phenotypic plasticity in Daphnia pulex: uncoupling morphological defenses and life history shifts. Hydrobiologia 339: 67–71.

    Article  Google Scholar 

  • Rodrigues, M. E. & F. O. Roque, 2017. Checklist de Odonata do estado de Mato Grosso do Sul, Brasil. Iheringia Série Zoologia 107: e2017117.

    Article  Google Scholar 

  • Schmidt, K. A., J. M. Earnhardt, J. S. Brown & R. D. Holt, 2000. Habitat selection under temporal heterogeneity: exorcizing the ghost of competition past. Ecology 81: 2622–2630.

    Article  Google Scholar 

  • Scrimgeour, G. J., J. M. Culp & F. J. Wrona, 1994. Feeding while avoiding predators: evidence for a size-specific trade-off by a lotic mayfly. Journal of the North American Benthological Society 13: 368–378.

    Article  Google Scholar 

  • Seebacher, F., C. R. White & C. E. Franklin, 2015. Physiological plasticity increases resilience of ectothermic animals to climate change. Nature Climate Change 5: 61–66.

    Article  Google Scholar 

  • Shrader, A. M., G. I. H. Kerley, J. S. Brown & B. P. Kotler, 2012. Patch use in free-ranging goats: does a large mammalian herbivore forage like other central place foragers? Ethology 118: 967–974.

    Article  Google Scholar 

  • Skelly, D. K. & E. E. Werner, 1990. Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71: 2313–2322.

    Article  Google Scholar 

  • Souza, F. L., C. P. A. Prado, J. L. M. M. Sugai, V. L. Ferreira, C. Aoki, P. Landgref-Filho, C. Strüssmann, R. W. Ávila, D. J. Rodrigues, N. R. Albuquerque, J. Terra, M. Uetanabaro, A. F. Béda, L. Piatti, R. A. Kawashita-Ribeiro, M. Delatorre, G. F. Faggioni, S. D. B. Demczuk & S. Duleba, 2017. Diversidade de anfíbios do Estado de Mato Grosso do Sul, Brasil. Iheringia Série Zoologia 107: e2017152.

    Article  Google Scholar 

  • Stav, G., B. P. Kotler & L. Blaustein, 2007. Direct and indirect effects of dragonfly (Anax imperator) nymphs on green toad (Bufo viridis) tadpoles. Hydrobiologia 579: 85–93.

    Article  Google Scholar 

  • Takahara, T., H. Doi, Y. Kohmatsu & R. Yamaoka, 2013. Different chemical cues originating from a shared predator induce common defense responses in two prey species. Animal Cognition 16: 147–153.

    Article  PubMed  Google Scholar 

  • Turkia, T., E. Korpimäki, A. Villers & V. Selonen, 2018. Predation risk landscape modifies flying and red squirrel nest site occupancy independently of habitat amount. PLoS ONE 13: e0194624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Baalen, M. & M. W. Sabelis, 1993. Coevolution of patch selection strategies of predator and prey and the consequences for ecological stability. The American Naturalist 142: 646–670.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Van Buskirk, J., A. Krügel, J. Kunz, F. Miss & A. Stamm, 2014. The rate of degradation of chemical cues indicating predation risk: an experiment and review. Ethology 120: 942–949.

    Article  Google Scholar 

  • Wassersug, R. J., 1971. On the comparative palatability of some dry-season tadpoles from costa Rica. American Midland Naturalist 86: 101–109.

    Article  Google Scholar 

  • Wells, K. D., 2010. The Ecology and Behavior of Amphibians. University of Chicago Press, Chicago.

    Google Scholar 

  • Werner, E. E., J. F. Gilliam, D. J. Hall & G. G. Mittelbach, 1983. An experimental test of the effects of predation risk on habitat use in fish. Ecology 64: 1540–1548.

    Article  Google Scholar 

  • Winandy, L., P. Legrand & M. Denoël, 2017. Habitat selection and reproduction of newts in networks of fish and fishless aquatic patches. Animal Behaviour 123: 107–115.

    Article  Google Scholar 

  • Wong, B. B. M. & U. Candolin, 2015. Behavioral responses to changing environments. Behavioral Ecology 26: 665–673.

    Article  Google Scholar 

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Acknowledgements

We are grateful to Jefferson Medina, Nathalia Mangini, and Beatriz Carneiro for their support in field work and the montage of the experiment. We thank the Use Animal Ethics Committee from Federal University of Mato Grosso do Sul by the approval of this project (protocol#732/2015). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. DJS thanks CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for his research fellowship (311492/2017-7). We also thank Dr. Luiz Gustavo de Oliveira-Santos for the helpful suggestions along the study.

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  1. Laboratório de Ecologia, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul Campo Grande, Cidade Universitária, 79002-970, Campo Grande, Mato Grosso do Sul, Brazil

    Eduardo Oliveira Pacheco, Mauricio Almeida-Gomes & Rafael Dettogni Guariento

  2. Laboratório de Zoologia, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul Campo Grande, Cidade Universitária, 79002-970, Campo Grande, Mato Grosso do Sul, Brazil

    Diego José Santana

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  1. Eduardo Oliveira Pacheco
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  2. Mauricio Almeida-Gomes
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Comparison of morphological characters between risk and control treatments. Online Resource 1 (DOCX 42 kb)

10750_2019_3962_MOESM2_ESM.docx

Temporal tendency of tadpoles to occupy the high resources patches in absence of predators. Online Resource 2 (DOCX 58 kb)

Morphometric measures of Rhinella diptycha in risk and control treatments. Online Resource 3 (DOCX 17 kb)

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Pacheco, E.O., Almeida-Gomes, M., Santana, D.J. et al. Space use and phenotypic plasticity in tadpoles under predation risk. Hydrobiologia 837, 77–86 (2019). https://doi.org/10.1007/s10750-019-3962-3

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