Skip to main content
SpringerLink
Log in

Offering offspring as food to cannibals: oviposition strategies of Amazonian poison frogs (Dendrobates ventrimaculatus)

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Species utilizing distinct resources for offspring production often show plasticity in reproductive strategies as a function of resource quality. For species using ephemeral pools, strategies are mainly shaped by a time constraint related to pool stability, resource availability and the colonizing community. We studied reproductive strategies in Amazonian poison frogs (Dendrobates ventrimaculatus) that are characterized by oviposition in distinct, small and resource-limited water bodies in leaf axils of plants and the transport of newly hatched tadpoles on the back of males to similar water bodies. Cannibalism of eggs by tadpoles was found to be the main cause of egg mortality. Typically, at the end of the rainy season new clutches of eggs were deposited in water bodies already containing a tadpole. Manipulation of the available number of water bodies showed that this observation did not result from resource limitation. We conclude that D. ventrimaculatus has a plastic reproductive strategy that includes provisioning its tadpoles with fertilized eggs as a function of desiccation risk of water bodies housing its offspring. Provisioning behavior is expected to increase developmental rate and, therefore, chances of metamorphosis for tadpoles that hatched towards the end of the rainy season. The plastic food provisioning strategy may be an important evolutionary link to bi-parental and female care with development of obligate unfertilized egg provisioning in the genus Dendrobates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alford RA (1999) Ecology. In: McDiarmid RW, Altig R (eds) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, Illinois, USA, pp 240–278

    Google Scholar 

  • van Alphen JJM, Visser ME (1990) Superparasitism as an adaptive strategy for insect parastoids. Annu Rev Entomol 35:59–79

    Article  PubMed  Google Scholar 

  • Álvarez D, Nicieza AG (2002) Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion. Oecologia 131:186–195

    Article  Google Scholar 

  • Altwegg R, Reyer HU (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882

    Article  PubMed  Google Scholar 

  • Bechter R, Lescure J (1982) Dendrobates quinquevittatus, Fortpflanzungsverhalten im Terrarium und Vielgestaltigkeit der Art (Teil 1). Herpetofauna 4:26–30

    Google Scholar 

  • Bourne GR, Collins AC, Holder AM, McCarthy CL (2001) Vocal communication and reproductive behavior of the frog Colostethus beebei in Guyana. J Herpetol 35:272–281

    Article  Google Scholar 

  • Brodeur J, Geervliet JBF, Vet LEM (1998) Effects of Pieris host species on life history parameters in a solitary specialist and gregarious generalist parasitoid (Cotesia species). Entomol Exp Appl 86:145–152

    Article  Google Scholar 

  • Brown JL, Schulte R, Summers K (2006) A new species of Dendrobates (Anura: Dendrobatidae) from the Amazonian lowlands in Peru. Zootaxa 1152:45–48

    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 (1997) Pair bonding in spotted poison frogs. Nature 385:211

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Crawley MJ (1993) GLIM for ecologists. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Crump ML (1983) Opportunistic cannibalism by amphibian larvae in temporary aquatic environments. Am Nat 121:281–287

    Article  Google Scholar 

  • Donnelly MA (1989a) Effects of reproductive resource supplementation on space-use patterns in Dendrobates pumilio. Oecologia 81:212–218

    Google Scholar 

  • Donnelly MA (1989b) Demographic effects of reproductive resource supplementation in a territorial frog, Dendrobates pumilio. Ecol Monogr 59:207–221

    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 behavior. Herpetol J 11:91–100

    Google Scholar 

  • Ekbom B, Popov SYA (2004) Host plant affects pollen beetle (Meligethes aeneus) egg size. Physiol Entomol 29:118–122

    Article  Google Scholar 

  • Fincke OM (1994) Population regulation of a tropical damselfly in the larval stage by food limitation, cannibalism, intraguild predation and habitat drying. Oecologia 100:118–127

    Article  Google Scholar 

  • Godfray HCJ (1987) The evolution of clutch size in parasitic wasps. Am Nat 129:221–233

    Article  Google Scholar 

  • Godfray HCJ (1994) Parasitoids: behavior and evolutionary ecology. Princeton University Press, Princeton

    Google Scholar 

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

    Article  Google Scholar 

  • Heying HE (2001) Social and reproductive behaviour in the Madagascan poison frog, Mantella laevigata, with comparisons to the dendrobatids. Anim Behav 61:567–577

    Article  Google Scholar 

  • Hopkins R. J., Ekbom B. (1999) The pollen beetle Meligethes aeneus changes egg production rate to match host quality. Oecologia 120:274–278

    Google Scholar 

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

    Google Scholar 

  • Lehtinen RM (2004) Tests for competition, cannibalism, and priority effects in two phytotelm dwelling tadpoles from Madagascar. Herpetologica 60:1–13

    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 

  • Mattiacci L, Dicke M (1995) The parasitoid Cotesia glomerata (Hymenoptera: Braconidae) discriminates between first and fifth larval instar of its host Pieris brassicae, on the basis of contact cues from frass, silk, and herbivore-damaged leaf tissue. J Insect Behav 8:485–498

    Article  Google Scholar 

  • Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428

    Article  Google Scholar 

  • Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, Oxford

    Google Scholar 

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

    Article  Google Scholar 

  • Myers CW, Daly JW (1983) Dart-poison frogs. Sci Am 248:120–133

    Article  PubMed  CAS  Google Scholar 

  • Myers CW, Paolillo AO, Daly JW (1991) Discovery of a defensively malodorous and nocturnal frog in the family Dendrobatidae: phylogenetic significance of a new genus and species from the Venezuelan Andes. Am Mus Novit 3002:1–33

    Google Scholar 

  • Noonan BP, Wray KP (2006) Neotropical diversification: the effects of a complex history on diversity within the poison frog genus Dendrobates. J Biogeogr 33:1007–1020

    Article  Google Scholar 

  • Nufio CR, Papaj DR (2004) Superparasitism of larval hosts by the walnut fly, Rhagoletis juglandis, and its implications for female and offspring performance. Oecologia 141:460–467

    Article  PubMed  Google Scholar 

  • Pramuk JB, Hiler BI (1999) An investigation of obligate oophagy of Dendrobates pumilio tadpoles. Herpetol Rev 30:219–221

    Google Scholar 

  • Resetarits WJ, Wilbur HM (1989) Choice of oviposition site by Hyla chrysoscelis: role of predators and competitors. Ecology 70:220–228

    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 

  • Sarthou C (2001) Plant communities on a granitic outcrop. In: Bongers F, Charles-Dominique P, Forget PM, Théry M (eds) Nouragues Dynamics and plant-animal interactions in a neotropical rainforest. Kluwer Academic Publisher, Dordrecht, The Netherlands, pp 65–78

    Google Scholar 

  • Scheirs J, De Bruyn L, Verhagen R (2000) Optimization of adult performance determines host choice in a grass miner. Proc R Soc Lond B 267:2065–2069

    Article  CAS  Google Scholar 

  • Sherman PW, Reeve HK, Pfennig DW (1997) Recognition systems. In: Krebs JR, Davies NB (eds) Behavioural ecology, 4th edn. Blackwell Scientific Press, Oxford, pp 69–96

    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 

  • Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton

    Google Scholar 

  • Summers K (1989) Sexual selection and intra-female competition in the green dart-poison frog, Dendrobates auratus. Anim Behav 37:797–805

    Article  Google Scholar 

  • Summers K (1992) Mating strategies in two species of dart-poison frogs: a comparative study. Anim Behav 43:907–919

    Article  Google Scholar 

  • 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 analysis of reproductive strategies in the Amazonian dart-poison frogs, Dendrobates ventrimaculatus. Behav Ecol 8:260–267

    Article  Google Scholar 

  • Summers K, Earn DJD (1999) The cost of polygyny and the evolution of female care in poison frogs. Biol J Linn Soc 66:515–538

    Article  Google Scholar 

  • Summers K, Symula R (2001) Cannibalism and kin discrimination in tadpoles of the Amazonian poison frog, Dendrobates ventrimaculatus, in the field. Herpetol J 11:17–21

    Google Scholar 

  • Summers K, McKeon CS (2004) The evolutionary ecology of phytotelmata use in neotropical poison frogs. In: Lehtinen RM (ed) Ecology and evolution of phytotelm-breeding anurans. Misc. Publ. Mus. Zool. Univ., Michigan 193, pp 55–73

    Google Scholar 

  • Symula R, Schulte R, Summers K (2003) Molecular systematics and phylogeography of Amazonian poison frogs of the genus Dendrobates. Mol Phyl Evol 26:452–475

    Article  CAS  Google Scholar 

  • Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14

    Article  Google Scholar 

  • Vet LEM, Datema A, van Welzen K, Snellen H (1993) Clutch size in a larval-pupal endoparasitoid 1. Variation across and within host species. Oecologia 95:410–415

    Article  Google Scholar 

  • Visser ME (1993) Adaptive self superparasitism and conspecific superparasitism in the solitary parasitoid Leptopilina heterotoma (Hymenoptera, Eucoilidae). Behav Ecol 4:22–28

    Article  Google Scholar 

  • Waage JK, Godfray HCL (1985) Reproductive strategies and population ecology of insect parasitoids. In: Sibly RM, Smith RH (eds) Behavioural ecology. Blackwell scientific publications, Oxford, pp 449–470

    Google Scholar 

  • Weisser WW, Houston AI, Völkl W (1994) Foraging strategies in solitary parasitoids: the trade-off between female and offspring mortality risks. Evol Ecol 8:587–597

    Article  Google Scholar 

  • Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Ann Rev Ecol Syst 27:337–363

    Article  Google Scholar 

  • Wells KD (1981) Parental behavior of male and female frogs. In: Alexander RD, Tinkle DW (eds) Natural selection and social behavior. Chiron Press, New York, pp 184–198

    Google Scholar 

  • Weygoldt P (1980) Complex brood care and reproductive behavior in captive poison-arrow frogs, Dendrobates pumilio O. Schmidt. Behav Ecol Sociobiol 7:329–332

    Article  Google Scholar 

  • Weygoldt P (1987) Evolution of parental care in dart poison frogs (Amphibia: Dendrobatidae). Z Zool Syst Evolutionsforsch 25:51–67

    Article  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New␣York

    Google Scholar 

  • Wilbur HM (1997) Experimental ecology of food webs: complex systems in temporary ponds. Ecology 78:2279–2302

    Article  Google Scholar 

  • van Zandt PA, Agrawal AA (2004) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629

    Google Scholar 

Download references

Acknowledgements

We thank Kyle Summers, Jason Brown, Kees van Oers and two anonymous referees for valuable comments on an earlier version of this manuscript, Marga Born for advice on research and camp site equipment as well as valuable up-front information on the study area, Pierre Charles-Dominique (CNRS) for logistics and research permission to work at Nouragues field station, Patrick Chatelet for collecting weather data and the Wageningen Universiteitsfonds for financial support to EHP.

Author information

Authors and Affiliations

  1. Laboratory of Entomology, Wageningen University, PO Box 8031, 6700 EH, Wageningen, the Netherlands

    Erik H. Poelman & Marcel Dicke

Authors
  1. Erik H. Poelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marcel Dicke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Erik H. Poelman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Poelman, E.H., Dicke, M. Offering offspring as food to cannibals: oviposition strategies of Amazonian poison frogs (Dendrobates ventrimaculatus). Evol Ecol 21, 215–227 (2007). https://doi.org/10.1007/s10682-006-9000-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-006-9000-8

Keywords

Search

Navigation