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Clutch identity and predator-induced hatching affect behavior and development in a leaf-breeding treefrog

  • Behavioral ecology - Original research
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Abstract

For species with complex life cycles, transitions between life stages result in niche shifts that are often associated with evolutionary trade-offs. When conditions across life stages are unpredictable, plasticity in niche shift timing may be adaptive; however, factors associated with clutch identity (e.g., genetic or maternal) may influence the effects of such plasticity. The red-eyed treefrog (Agalychnis callidryas) is an ideal organism for investigating the effects of genetics and life stage switch point timing because embryos exhibit adaptive phenotypic plasticity in hatching time. In this study, we evaluated the effects of experimentally manipulated hatching time and clutch identity on antipredator behavior of tadpoles and on developmental traits of metamorphs, including larval period, mass, SVL, and jumping ability. We found that in the presence of dragonfly nymph predator cues at 21 days post-oviposition, tadpoles reduced both their activity level and height in the water column. Furthermore, early-hatched tadpoles were less active than late-hatched tadpoles of the same age. This difference in behavior patterns of early- and late-hatched tadpoles may represent an adaptive response due to a longer period of susceptibility to odonate predators for early-hatched tadpoles, or it may be a carry-over effect mediated by early exposure to an environmental stressor (i.e., induction of early hatching). We also found that hatching time affected both behavioral traits and developmental traits, but its effect on developmental traits varied significantly among clutches. This study shows that a single early-life event may influence a suite of factors during subsequent life stages and that some of these effects appear to be dependent on clutch identity. This interaction may represent an evolutionary response to a complex life cycle and unpredictable environments, regardless of whether the clutch differences are due to additive genetic variance or maternal effects.

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References

  • Abjornsson K, Hansson LA, Bronmark C (2004) Responses of prey from habitats with different predator regimes: local adaptation and heritability. Ecology 85:1859–1866

    Article  Google Scholar 

  • Alvarez D, Nicieza AG (2002) Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131:186–195. doi:10.1007/s00442-002-0876-x

    Article  Google Scholar 

  • Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234

    Article  Google Scholar 

  • Barlow GW (1991) Nature–nurture and the debates surrounding ethology and sociobiology. Am Zool 31:286–296

    Google Scholar 

  • Beck CW, Congdon JD (2000) Effects of age and size at metamorphosis on performance and metabolic rates of Southern Toad, Bufo terrestris, metamorphs. Funct Ecol 14:32–38

    Article  Google Scholar 

  • Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673. doi:10.1146/annurev.ecolsys.35.021004.112426

    Article  Google Scholar 

  • Blouin MS (1992) Genetic correlations among morphometric traits and rates of growth and differentiation in the green tree frog, Hyla cinerea. Evolution 46:735–744

    Article  Google Scholar 

  • Boake CRB et al (2002) Genetic tools for studying adaptation and the evolution of behavior. Am Nat 160:S143–S159

    Article  PubMed  Google Scholar 

  • Brown C, Burgess F, Braithwaite VA (2007) Heritable and experiential effects on boldness in a tropical poeciliid. Behav Ecol Sociobiol 62:237–243. doi:10.1007/s00265-007-0458-3

    Article  Google Scholar 

  • Buckley CR, Metcalf KA, Warkentin KM (2002) Egg development affects the foraging strategy of wasps preying on red-eyed tree frog eggs. Integr Comp Biol 42:1203

    Google Scholar 

  • Chelgren ND, Rosenberg DK, Heppell SS, Gitelman AI (2006) Carryover aquatic effects on survival of metamorphic frogs during pond emigration. Ecol Appl 16:250–261

    Article  PubMed  Google Scholar 

  • Crump ML (1981) Variation in propagule size as a function of environmental uncertainty for tree frogs. Am Nat 117:724–737

    Article  Google Scholar 

  • Denver RJ (2009) Stress hormones mediate environment-genotype interactions during amphibian development. Gen Comp Endocrinol 164:20–31

    Google Scholar 

  • Duellman WE (1970) The hylid frogs of middle America. Monograph of the Museum of Natural History University of Kansas 1:1–753

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

    Article  Google Scholar 

  • Falconer DS (1989) Introduction to quantitative genetics, 3rd edn. Longman, London

    Google Scholar 

  • Ficetola GF, De Bernardi F (2006) Trade-off between larval development rate and post-metamorphic traits in the frog Rana latastei. Evol Ecol 20:143–158. doi:10.1007/s10682-005-5508-6

    Article  Google Scholar 

  • Gibbons ME, Ferguson AM, Lee DR (2005) Both learning and heritability affect foraging behaviour of red-backed salamanders, Plethodon cinereus. Anim Behav 69:721–732. doi:10.1016/j.anbehav.2004.06.021

    Article  Google Scholar 

  • Gomez-Mestre I, Wiens JJ, Warkentin KM (2008) Evolution of adaptive plasticity: risk-sensitive hatching in neotropical leaf-breeding treefrogs. Ecol Monograph 78:205–224

    Article  Google Scholar 

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

    Google Scholar 

  • Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352. doi:10.1016/j.neubiorev.2004.12.002

    Article  PubMed  CAS  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 

  • Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204

    PubMed  CAS  Google Scholar 

  • Husak JF (2006) Do female collared lizards change field use of maximal sprint speed capacity when gravid? Oecologia 150:339–343. doi:10.1007/s00442-006-0513-1

    Article  PubMed  Google Scholar 

  • Iwami T, Kishida O, Nishimura K (2007) Direct and indirect induction of a compensatory phenotype that alleviates the costs of an inducible defense. PLoS ONE 2:e1084. doi:10.1371/journal.pone.0001084

    Article  PubMed  Google Scholar 

  • King RB, Milstead WB, Gibbs HL, Prosser MR, Burghardt GM, McCracken GF (2001) Application of microsatellite DNA markers to discriminate between maternal and genetic effects on scalation and behavior in multiply-sired garter snake litters. Can J Zool 79:121–128

    Article  CAS  Google Scholar 

  • Lancaster LT, McAdam AG, Wingfield JC, Sinervo BR (2007) Adaptive social and maternal induction of antipredator dorsal patterns in a lizard with alternative social strategies. Ecol Lett 10:798–808. doi:10.1111/j.1461-0248.2007.01069.x

    Article  PubMed  Google Scholar 

  • Laugen AT, Kruuk LEB, Laurila A, Rasanen K, Stone J, Merila J (2005) Quantitative genetics of larval life-history traits in Rana temporaria in different environmental conditions. Genet Res 86:161–170. doi:10.1017/S0016672305007810

    Article  PubMed  CAS  Google Scholar 

  • Laurila A, Jarvi-Laturi M, Pakkasmaa S, Merila J (2004) Temporal variation in predation risk: stage-dependency, graded responses and fitness costs in tadpole antipredator defences. Oikos 107:90–99

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lindstrom J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  • McDade LA, Hartshorn GS (1994) La Selva Biological Station. In: McDade LA, Bana KS, Hespenheide HA, Hartshorn GS (eds) La Selva: ecology and natural history of a neotropical rain forest. The University of Chicago Press, Chicago, pp 6–14

    Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

  • Moran NA (1994) Adaptation and constraint in the complex life-cycles of animals. Annu Rev Ecol Syst 25:573–600

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  PubMed  CAS  Google Scholar 

  • Newman RA (1992) Adaptive plasticity in amphibian metamorphosis. Bioscience 42:671–678

    Article  Google Scholar 

  • Newman RA (1994) Genetic variation for phenotypic plasticity in the larval life history of spadefoot toads (Scaphiopus couchii). Evolution 48:1773–1785

    Article  Google Scholar 

  • Pakkasmaa S, Merila J, O’Hara RB (2003) Genetic and maternal effect influences on viability of common frog tadpoles under different environmental conditions. Heredity 91:117–124

    Article  PubMed  CAS  Google Scholar 

  • Plaistow SJ, Lapsley CT, Benton TG (2006) Context-dependent intergenerational effects: the interaction between past and present environments and its effect on population dynamics. Am Nat 167:206–215

    Article  PubMed  Google Scholar 

  • Postma E, van Noordwijk AJ (2005) Genetic variation for clutch size in natural populations of birds from a reaction norm perspective. Ecology 86:2344–2357

    Article  Google Scholar 

  • Price T, Schluter D (1991) On the low heritability of life-history traits. Evolution 45:853–861

    Article  Google Scholar 

  • Relyea RA (2001) The relationship between predation risk and antipredator responses in larval anurans. Ecology 82:541–554

    Article  Google Scholar 

  • Relyea RA (2005) The heritability of inducible defenses in tadpoles. J Evol Biol 18:856–866. doi:10.1111/j.1420-9101.2005.00882.x

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Richardson JML, Anholt BR (1995) Ontogenetic behaviour changes in larvae of the damselfly Ischnura verticalis (Odonata: Coenagrionidae). Ethology 101:308–334

    Article  Google Scholar 

  • Robert KA, Thompson MB (2007) Is basking opportunity in the viviparous lizard, Eulamprus tympanum, compromised by the presence of a predator scent? J Herpetol 41:287–293

    Article  Google Scholar 

  • Savage JM (2002) The amphibians and reptiles of Costa Rica: a herpetofauna between two continents, between two seas. The University of Chicago Press, Chicago

    Google Scholar 

  • Semlitsch RD (2002) Critical elements for biologically based recovery plans of aquatic-breeding amphibians. Conserv Biol 16:619–629

    Article  Google Scholar 

  • Skelly DK, Werner EE (1990) Behavioral and life-historical responses of larval American toads to an odonate predator. Ecology 71:2313–2322

    Article  Google Scholar 

  • Smith DC (1983) Factors controlling tadpole populations of the chorus frog (Pseudacris triseriata) on Isle Royale, Michigan. Ecology 64:501–510

    Article  Google Scholar 

  • SPSS Inc. (2006) SPSS for Windows. Version 15.0 edn. SPSS Inc., Chicago

  • Stirling DG, Reale D, Roff DA (2002) Selection, structure and the heritability of behaviour. J Evol Biol 15:277–289

    Article  Google Scholar 

  • Touchon JC, Warkentin KM (2010) Short- and long-term effects of the abiotic egg environment on viability, development and vulnerability to predators of a Neotropical anuran. Funct Ecol 24:566–575

    Article  Google Scholar 

  • Van Buskirk J, Saxer G (2001) Delayed costs of an induced defense in tadpoles? Morphology, hopping, and development rate at metamorphosis. Evolution 55:821–829

    Article  PubMed  Google Scholar 

  • Van Damme N, Van Dooren TJM (1999) Absolute versus per unit body length speed of prey as an estimator of vulnerability to predation. Anim Behav 57:347–352

    Article  Google Scholar 

  • Via S (1984) The quantitative genetics of polyphagy in an insect herbivore.2. Genetic correlations in larval performance within and among host plants. Evolution 38:896–905

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Walsh PT (2010) Anuran life history plasticity: variable practice in determining the end-point of larval development. Amphibia-Reptilia 31:157–167

    Article  Google Scholar 

  • Warkentin KM (1995) Adaptive plasticity in hatching age: a response to predation risk trade-offs. Proc Natl Acad Sci USA 92:3507–3510

    Article  PubMed  CAS  Google Scholar 

  • Warkentin KM (1999a) The development of behavioral defenses: a mechanistic analysis of vulnerability in red-eyed tree frog hatchlings. Behav Ecol 10:251–262

    Article  Google Scholar 

  • Warkentin KM (1999b) Effects of hatching age on development and hatchling morphology in the red-eyed treefrog, Agalychnis callidryas. Biol J Linnean Soc 68:443–470

    Google Scholar 

  • Warkentin KM, Buckley CR, Metcalf KA (2006a) Development of red-eyed treefrog eggs affects efficiency and choices of egg-foraging wasps. Anim Behav 71:417–425. doi:10.1016/j.anbehav.2005.06.007

    Article  Google Scholar 

  • Warkentin KM, Caldwell MS, McDaniel JG (2006b) Temporal pattern cues in vibrational risk assessment by embryos of the red-eyed treefrog, Agalychnis callidryas. J Exp Biol 209:1376–1384. doi:10.1242/jeb.02150

    Article  PubMed  Google Scholar 

  • Watkins TB, McPeek MA (2006) Growth and predation risk in green frog tadpoles (Rana clamitans): a quantitative genetic analysis. Copeia 2006(3):478–488

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structured populations. Annu Rev Ecol Syst 15:393–425

    Article  Google Scholar 

  • Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93

    Article  Google Scholar 

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Acknowledgments

We thank K.M. Warkentin, S.J. Arnold, and their research groups for guidance and advice, E. Day for helping with data collection, Birmingham-Southern College for sabbatical release time, and La Selva Biological Station for support and use of their field sites and facilities. We also thank R.G. Jaeger, P.A. Van Zandt, J.R. Vonesh, and K.M. Warkentin for comments on earlier drafts. This study was conducted under Costa Rican MINAE permit 01570.

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  1. Department of Biology, Birmingham-Southern College, Birmingham, AL, 35254, USA

    Megan E. Gibbons & M. Patricia George

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  1. Megan E. Gibbons
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  2. M. Patricia George
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Correspondence to Megan E. Gibbons.

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Communicated by Raoul Van Damme.

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Gibbons, M.E., Patricia George, M. Clutch identity and predator-induced hatching affect behavior and development in a leaf-breeding treefrog. Oecologia 171, 831–843 (2013). https://doi.org/10.1007/s00442-012-2443-4

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