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The power of the seasons: rainfall triggers parental care in poison frogs

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Abstract

The quality of breeding sites is of great importance for the reproductive success and accordingly the fitness of many animal species. Hence, individuals should decide carefully where to rear their offspring. Often parents have to account for multiple characteristics of habitat quality at once, which in turn might change over time. Specimens confronted with such variability may evolve the ability to display context-dependant decision plasticity. Anuran amphibians breeding in ephemeral pools largely face two risks for their offspring: desiccation and predation. The Neotropical poison frog Ranitomeya variabilis deposits both eggs and tadpoles in phytotelmata. These small tadpole nurseries lower the risk of offspring predation. However, because most poison frog tadpoles are cannibalistic, even these pools need to be surveyed for predators, and parents tend to avoid deposition with conspecifics. We tested if this avoidance behaviour does change in parental R. variabilis depending on seasonal circumstances. Over several months we provided the frogs the option to deposit their eggs or tadpoles in pools that did and did not contain chemical cues of cannibalistic conspecifics, respectively. During the rainy season, frogs strongly avoided conspecific cues for both eggs and tadpoles. Anyway, with the change to the dry season, parental preferences changed such that parent frogs were more likely to deposit tadpoles (but not eggs) in pools containing cues of conspecific tadpoles. We suggest that R. variabilis, a species that typically isolates its cannibalistic offspring, has evolved a plastic feeding behaviour with regard to the risk of phytotelmata desiccation. We interpret that parents provide older tadpoles with younger ‘trophic’ tadpoles in order to accelerate their development and save them from impending desiccation.

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References

  • Abrunhosa PA, Wogel H, Pombal JP (2006) Anuran temporal occupancy in a temporary pond from the Atlantic Rain Forest, South-Eastern Brazil. Herpetol J 16:115–122

    Google Scholar 

  • Aichinger M (1987) Annual activity patterns of anurans in a seasonal neotropical environment. Oecologia 71:583–592

    Article  Google Scholar 

  • Aichinger M (1991) Tadpole transport in relation to rainfall, fecundity and body size in five species of poison-dart frogs from Amazonian Peru. Amphib Reptil 12:49–55

    Article  Google Scholar 

  • Aspbury AS, Juliano SA (1998) Negative effects of habitat drying and prior exploitation on the detritus resource in an ephemeral aquatic habitat. Oecologia 115:137–148

    Article  Google Scholar 

  • Badyaev AV (1993) Breeding biology of the gold-fronted serin (Serinus pusillus) in conditions of subalpine bush zone of the Phansky Mountains. Biol Sci 348:89–99

    Google Scholar 

  • Badyaev AV (1994) Breeding biology of white-winged grosbeak (Mycerobas carnipes) in conditions of subalpine bush zone of the Phansky Mountains. Bull MOIP 99:20–28

    Google Scholar 

  • Balshine-Earn S, Earn DJD (1997) An evolutionary model of parental care in St. Peter’s fish. J Theor Biol 184:423–431

    Article  Google Scholar 

  • Bertoluci J, Rodrigues MT (2002) Seasonal patterns of breeding activity of Atlantic Rainforest anurans at Boraceia, Southeastern Brazil. Amphib Reptil 23:161–167

    Article  Google Scholar 

  • Bevier CR (1997) Breeding activity and chorus tenure of two neotropical hylid frogs. Herpetologica 53:297–311

    Google Scholar 

  • Binckley CA, Resetarits WJ (2002) Reproductive decisions under threat of predation: squirrel treefrog (Hyla squirella) responses to banded sunfish (Enneacanthus obesus). Oecologia 130:157–161

    Google Scholar 

  • Bouskila A, Robertson IC, Robinson ME, Roitberg BD, Tenhumberg B, Tyre AJ, vanRanden E (1995) Submaximal oviposition rates in a mymarid parasitoid: choosiness should not be ignored. Ecology 76:1990–1993

    Article  Google Scholar 

  • Brodsky BE, Darkhovsky BS (1993) Nonparametric methods in change-point problems, vol 243. Kluwer, Dordrecht

    Book  Google Scholar 

  • Brown JL, Morales V, Summers K (2008a) Divergence in parental care, habitat selection and larval life history between two species of Peruvian poison frogs: an experimental analysis. J Evol Biol 21:1534–1543

    Article  PubMed  CAS  Google Scholar 

  • Brown JL, Twomey E, Morales V, Summers K (2008b) Phytotelm size in relation to parental care and mating strategies in two species of Peruvian poison frogs. Behaviour 145:1139–1165

    Article  Google Scholar 

  • Brown JL, Morales V, Summers K (2009) Home range size and location in relation to reproductive resources in poison frogs (Dendrobatidae): a Monte Carlo approach using GIS data. Anim Behav 77:547–554

    Article  Google Scholar 

  • Brown JL, Morales V, Summers K (2010) A key ecological trait drove the evolution of biparental care and monogamy in an amphibian. Am Nat 175:436–446

    Article  PubMed  Google Scholar 

  • Brown JL, Twomey E, Amézquita A, Barbosa de Souza M, Caldwell JP, Lötters S, von May R, Melo-Sampaio PR, Mejía-Vargas D, Perez-Peña P, Pepper M, Poelman EH, Sanchez-Rodriguez M, Summers K (2011) A taxonomic revision of the Neotropical poison frog genus Ranitomeya (Amphibia: Dendrobatidae). Zootaxa 3083:1–120

    Google Scholar 

  • Brust DG (1993) Maternal brood care by Dendrobates pumilio: a frog that feeds its young. J Herpetol 27:96–98

    Article  Google Scholar 

  • Caldwell JP, de Araújo MC (1998) Cannibalistic interactions resulting from indiscriminate predatory behavior in tadpoles of poison frogs (Anura: Dendrobatidae). Biotropica 30:92–103

    Article  Google Scholar 

  • Caldwell J, de Oliveira V (1999) Determinants of biparental care in the spotted poison frog, Dendrobates vanzolinii (Anura: Dendrobatidae). Copeia 1999:565–575

  • Clutton-Brock TH, Vincent ACJ (1991) The evolution of parental care. Princeton University Press, Oxford

    Google Scholar 

  • Crump ML (1990) Possible enhancement of growth in tadpoles through cannibalism. Copeia 1990:560–564

  • Crump ML (1991) Choice of oviposition site and egg load assessment by a treefrog. Herpetologica 47:308–315

    Google Scholar 

  • Dillon ME, Fiaño J (2000) Oviposition site selection by the túngara frog (Physalaemus pustulosus). Copeia 2000:883–885

  • Donnelly MA, Guyer C (1994) Patterns of reproduction and habitat use in an assemblage of Neotropical hylid frogs. Oecologia 98:291–302

    Article  Google Scholar 

  • Downie JR, Livingstone SR, Cormack JR (2001) Selection of tadpole deposition sites by male Trinidadian stream frogs, Mannophryne trinitatis (Dendrobatidae): an example of anti-predator behaviour. Herpetol J 11:91–100

    Google Scholar 

  • Duellman WE, Trueb L (1986) Biology of amphibians. Johns Hopkins University Press, New York

    Google Scholar 

  • Edgerly JS, McFarland M, Morgan P, Livdahl T (1998) A seasonal shift in egg-laying behaviour in response to cues of future competition in a treehole mosquito. J Anim Ecol 67:805–818

    Article  Google Scholar 

  • Engelbrecht BMJ, Dalling JW, Pearson TRH, Wolf RL, Galvez DA, Koehler T, Tyree MT, Kursar TA (2006) Short dry spells in the wet season increase mortality of tropical pioneer seedlings. Oecologia 148:258–269

    Article  PubMed  Google Scholar 

  • Fisher RA (1922) On the interpretation of Χ2 from contingency tables, and the calculation of P. J Roy Stat Soc Ser A (Stat Soc) 85:87–94

    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 

  • Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. Sinauer, Sunderland

    Google Scholar 

  • Gottsberger B, Gruber E (2004) Temporal partitioning of reproductive activity in a neotropical anuran community. J Trop Ecol 20:271–280

    Article  Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98

    Article  PubMed  CAS  Google Scholar 

  • Haddad CFB, Pombal JP Jr (1998) Redescription of Physalaemus spiniger (Anura: Leptodactylidae) and description of two new reproductive modes. J Herpetol 32:557–565

    Article  Google Scholar 

  • Haddad CFB, Prado CPA (2005) Reproductive modes in frogs and their unexpected diversity in the Atlantic Forest of Brazil. Bioscience 55:207–217

    Article  Google Scholar 

  • Halloy M, Fiaño JM (2000) Oviposition site selection in Pleurodema borellii (Anura: Leptodactylidae) may be influenced by tadpole presence. Copeia 2000:606–609

  • Heard SB (1994) Imperfect oviposition decisions by the pitcher plant mosquito (Wyeomyia smithii). Evol Ecol 8:493–502

    Article  Google Scholar 

  • Heimpel GE, Rosenheim JA, Mangel M (1996) Egg limitation, host quality, and dynamic behavior by a parasitoid in the field. Ecology 77:2410–2420

    Article  Google Scholar 

  • Heinen JT, Abdella JA (2005) On the advantages of putative cannibalism in American toad tadpoles (Bufo a. americanus): is it active or passive and why? Am Midl Nat 153:338–347

    Article  Google Scholar 

  • Iwai N, Kagaya T, Isamu O (2007) Choice of oviposition site by Rana japonica: role of the developmental stage of conspecific eggs. Herpetologica 63:31–34

    Article  Google Scholar 

  • Johnson LS, Brubaker JL, Ostlind E, Balenger SL (2007) Effect of altitude on male parental expenditure in mountain bluebirds (Sialia currucoides): are higher-altitude males more attentive fathers? J Ornitol 148:9–16

    Article  Google Scholar 

  • Johnson O, Sejdinovic D, Cruise J, Ganesh A, Piechocki R (2011) Non-parametric change-point detection using string matching algorithms. http://arxiv.org/abs/1106.5714

  • Kam YC, Su YJ, Liu JL, Lin YS (2001) Intraspecific interactions among oophagous tadpoles (Chirixalus eiffingeri: Rhacophoridae) living in bamboo stumps in Taiwan. J Zool 255:519–524

    Article  Google Scholar 

  • Killick R, Eckley IA (2011a) Changepoint: an R package for changepoint analysis. www.lancs.ac.uk/~killick/Pub/KillickEckley2011.pdf

  • Killick R, Eckley IA (2011b) An R package for changepoint analysis. (R package)

  • Kitching RL (2000) Foodwebs and container habitats: the natural history and ecology of phytotelmata. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Lehtinen RM, Lannoo MJ, Wassersug RJ (2004) Phytotelm-breeding anurans: past, present, and future research. Misc Publ Mus Zool Univ Mich 193:1–10

    Google Scholar 

  • Lin YS, Kam YC (2008) Nest choice and breeding phenology of an arboreal-breeding frog, Kurixalus eiffingeri (Rhacophoridae), in a bamboo forest. Zool Stud 47:129–137

    Google Scholar 

  • Lin YS, Lehtinen RM, Kam YC (2008) Time-and context-dependent oviposition site selection of a phytotelm-breeding frog in relation to habitat characteristics and conspecific cues. Herpetologica 64:413–421

    Article  Google Scholar 

  • Lötters S, Jungfer K-H, Henkel F-W, Schmidt W (2007) Poison frogs: biology, species and captive husbandry. Chimaira, Frankfurt

    Google Scholar 

  • Mangel M (1989) An evolutionary interpretation of the “motivation to oviposit”. J Evol Biol 2:157–172

    Article  Google Scholar 

  • Marsh DM, Borrell BJ (2001) Flexible oviposition strategies in túngara frogs and their implications for tadpole spatial distributions. Oikos 93:101–109

    Article  Google Scholar 

  • Martins M, Pombal JP, Haddad CFB (1998) Escalated aggressive behaviour and facultative parental care in the nest building gladiator frog, Hyla faber. Amphib Reptil 19:65–73

    Article  Google Scholar 

  • Matsushima N, Kawata M (2005) The choice of oviposition site and the effects of density and oviposition timing on survivorship in Rana japonica. Ecol Res 20:81–86

    Article  Google Scholar 

  • Mokany A, Shine R (2003) Oviposition site selection by mosquitoes is affected by cues from conspecific larvae and anuran tadpoles. Austral Ecol 28:33–37

    Article  Google Scholar 

  • Murphy PJ (2003a) Context-dependent reproductive site choice in a Neotropical frog. Behav Ecol 14:626–633

    Article  Google Scholar 

  • Murphy PJ (2003b) Does reproductive site choice in a Neotropical frog mirror variable risks facing offspring? Ecol Monogr 73:45–67

    Article  Google Scholar 

  • Muths E, Campbell DH, Corn PS (2003) Hatching success in salamanders and chorus frogs at two sites in Colorado, USA: effects of acidic deposition and climate. Amphib Reptil 24:27–36

    Article  Google Scholar 

  • Newman RA (1988) Adaptive plasticity in development of Scaphiopus couchii tadpoles in desert ponds. Evolution 42:774–783

    Article  Google Scholar 

  • Page ES (1954) Continuous inspection schemes. Biometrika 41:100–115

    Google Scholar 

  • Petranka JW, Hopey ME, Jennings BT, Baird SD, Boone SJ (1994) Breeding habitat segregation of wood frogs and American toads: the role of interspecific tadpole predation and adult choice. Copeia 1994:691–697

  • Poelman EH, Dicke M (2007) Offering offspring as food to cannibals: oviposition strategies of Amazonian poison frogs (Dendrobates ventrimaculatus). Evol Ecol 21:215–227

    Article  Google Scholar 

  • Pröhl H, Hödl W (1999) Parental investment, potential reproductive rates, and mating system in the strawberry dart-poison frog, Dendrobates pumilio. Behav Ecol Sociobiol 46:215–220

    Article  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/

  • Refsnider J, Janzen F (2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Ann Rev Ecol Evol Syst 41:39–57

    Article  Google Scholar 

  • Rieger JF, Binckley CA, Resetarits WJ Jr (2004) Larval performance and oviposition site preference along a predation gradient. Ecology 85:2094–2099

    Article  Google Scholar 

  • Roitberg BD, Mangel M, Lalonde RG, Roitberg CA, van Alphen JJM, Vet L (1992) Seasonal dynamic shifts in patch exploitation by parasitic wasps. Behav Ecol 3:156–165

    Article  Google Scholar 

  • Rudolf VHW, Rödel MO (2005) Oviposition site selection in a complex and variable environment: the role of habitat quality and conspecific cues. Oecologia 142:316–325

    Article  PubMed  Google Scholar 

  • Sachs L (1974) Angewandte statistik: planung und auswertung—methoden und modelle. Springer, Berlin

    Book  Google Scholar 

  • Sanuy D, Joly P (2009) Olfactory cues and breeding habitat selection in the natterjack toad, Bufo calamita. Amphib Reptil 30:555–559

    Article  Google Scholar 

  • Schulte LM, Rödder D, Schulte R, Lötters S (2010) Preference and competition for breeding plants in coexisting Ranitomeya species (Dendrobatidae): does height play a role? Salamandra 46:180–184

    Google Scholar 

  • Schulte LM, Yeager J, Schulte R, Veith M, Werner P, Beck LA, Lötters S (2011) The smell of success: choice of larval rearing sites by means of chemical cues in a Peruvian poison frog. Anim Behav 81:1147–1154

    Article  Google Scholar 

  • Shine R, Harlow PS (1996) Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard. Ecology 77:1808–1817

    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 

  • Spieler M, Linsenmair KE (1997) Choice of optimal oviposition sites by Hoplobatrachus occipitalis (Anura: Ranidae) in an unpredictable and patchy environment. Oecologia 109:184–199

    Article  Google Scholar 

  • SPSS Inc. (2009) PASW Statistics 18.0

  • Summers K (1999) The effects of cannibalism on Amazonian poison frog egg and tadpole deposition and survivorship in Heliconia axil pools. Oecologia 119:557–564

    Article  Google Scholar 

  • Summers K, Amos W (1997) Behavioral, ecological, and molecular genetic analyses of reproductive strategies in the Amazonian dart-poison frog, Dendrobates ventrimaculatus. Behav Ecol 8:260

    Article  Google Scholar 

  • Summers K, McKeon CS (2004) The evolutionary ecology of phytotelmata use in Neotropical poison frogs. Misc Publ Mus Zool Univ Mich 193:55–73

    Google Scholar 

  • Summers K, McKeon S (2006) The evolution of parental care and egg size: a comparative analysis in frogs. Proc R Soc Lond Ser B Biol Sci 273:687

    Google Scholar 

  • Székely T, Cuthill I (1999) Brood desertion in Kentish plover: the value of parental care. Behav Ecol 10:191–197

    Article  Google Scholar 

  • Székely T, Cuthill IC (2000) Trade-off between mating opportunities and parental care: brood desertion by female Kentish plovers. Proc R Soc Lond Ser B Biol Sci 267:2087–2092

    Article  Google Scholar 

  • Tarutis J, Lewis S, Dyke M (2005) Active parental care in a freshwater amphipod (Crustacea: Gammarus pseudolimnaeus): effects of environmental factors. Am Midl Nat 153:276–283

    Article  Google Scholar 

  • Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Ann Rev Entomol 36:65–89

    Article  Google Scholar 

  • Touchon JC, Warkentin KM (2009) Negative synergism of rainfall patterns and predators affects frog egg survival. J Anim Ecol 78:715–723

    Article  PubMed  Google Scholar 

  • Townend J (2002) Practical statistics for environmental and biological scientists. Wiley, Chichester

    Google Scholar 

  • van den Berghe EP (1990) Variable parental care in a labrid fish: how care might evolve. Ethology 84:319–333

    Article  Google Scholar 

  • Varga L (1928) Ein interessanter Biotop der Biocönose von Wasserorganismen. Biol Zentralbl 48:143–162

    Google Scholar 

  • Webb JN, Houston AI, McNamara JM, Székely T (1999) Multiple patterns of parental care. Anim Behav 58:983–993

    Article  PubMed  Google Scholar 

  • Williams DA (1976) Improved likelihood ratio tests for complete contingency tables. Biometrika 63:33

    Article  Google Scholar 

  • Woolf B (1957) The log likelihood ratio test (the G-test); methods and tables for tests of heterogeneity in contingency tables. Ann Hum Genet 21:397–409

    Article  PubMed  CAS  Google Scholar 

  • Yamamura N, Tsuji N (1993) Parental care as a game. J Evol Biol 6:103–127

    Article  Google Scholar 

  • Zimmermann H, Zimmermann E (1988) Etho-Taxonomie und zoogeographische Artengruppenbildung bei Pfeilgiftfröschen (Anura: Dendrobatidae). Salamandra 24:125–160

    Google Scholar 

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Acknowledgments

We thank Rebecca Killick and Ortwin Elle for help with the statistics and Michael Mayer, Elena Rudolf, Rainer Schulte and Evan Twomey for support in the field. Asociación de Productores de Ranas Venenosas, Progreso (ASPRAVEP), kindly allowed us to use their field station. Research permits were issued by the Ministry of Agriculture (DGFFS) in Lima (0200-2011-AG-DGFFS-DGFFS). This study was funded by the ‘Forschungsfonds’ of Trier University (to S. L.), the ‘Studienstiftung des deutschen Volkes’ (to L. M. S.) and the ‘Deutsche Forschungsgemeinschaft’, DFG (to S. L., M. Veith and W. Brack; LO 1681/1-1). We are most grateful to authorities, funders and collaborators.

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Schulte, L.M., Lötters, S. The power of the seasons: rainfall triggers parental care in poison frogs. Evol Ecol 27, 711–723 (2013). https://doi.org/10.1007/s10682-013-9637-z

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