Larval aggression is independent of food limitation in nurseries of a poison frog

Abstract

Aggression between nurserymates is common in animals and often hypothesized to result from proximate resource limitation. In numerous terrestrial frogs, larvae develop in phytotelmata, tiny water bodies where resources are scarce and competition, aggression, and cannibalism are all common between individuals sharing these nurseries. In some species, mothers provision phytotelm-bound young with trophic eggs, a strategy that compensates for low nutrient availability and could allow mothers to reduce costly aggression and cannibalism among nurserymates. We tested this hypothesis using strawberry poison frog (Oophaga pumilio) tadpoles, staging secondary depositions in arenas occupied by residents that had either been food deprived or fed ad libitum. Resident tadpoles were nearly all aggressive and most killed intruders, but aggression was unrelated to resident food deprivation. Unlike most related frogs studied, O. pumilio residents did not cannibalize their victims. This result supports the hypothesis that proximate food limitation and aggression can be independent.

Significance statement

Aggression and cannibalism are common in the resource-limited nurseries in which many young animals develop. An intuitive hypothesis for this is that individuals are aggressive because they are hungry. Although this hypothesis has usually been supported in birds, we found no support for it in a test we conducted in a terrestrial frog that feeds its young with trophic eggs. Resident tadpoles fed ad libitum were just as aggressive to staged intruders as those that were food-deprived, and were just as likely to kill intruders. Residents did not cannibalize their victims. These results suggest that hunger-independent aggression in young animals is taxonomically widespread, and demonstrates an important ecological constraint on parents: they cannot prevent fatal aggression, they cannot “feed” tadpoles to older siblings, and thus, they cannot use occupied rearing sites.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Brown JL, Morales V, Summers K (2009) Tactical reproductive parasitism via larval cannibalism in Peruvian poison frogs. Biol Lett 5:148–151

    Article  PubMed  Google Scholar 

  2. 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 

  3. Brust DG (1990) Maternal brood care by Dedrobates pumilio: a frog that feeds its young. PhD dissertation, Cornell University, Ithaca, NY

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

    Article  Google Scholar 

  5. 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 

  6. Crespi BJ (1992) Cannibalism and trophic eggs in subsocial and eusocial insects. In: Crespi BJ (ed) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, Oxford, pp 176–213

    Google Scholar 

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

    Article  Google Scholar 

  8. Drummond H (2001) The control and function of agonism in avian broodmates. Adv Stud Behav 30:261–360

    Article  Google Scholar 

  9. Drummond H (2002) Begging versus aggression in avian broodmate competition. In: Wright J, Leonard M (eds) The evolution of begging. Kluwer Academic Publishers, Dordrecht, NL, pp 337–360

    Google Scholar 

  10. Dugas MB, Richards-Zawacki CL (2016) Conspicuous and cryptic morphs of a polytypic poison frog differ in reproductive output because of differences in tadpole performance, not parental effort. Ethol Ecol Evol (published online, doi:10.1080/03949370.2015.1076527)

  11. Dugas MB, Wamelink CN, Richards-Zawacki CL (2015) Both sexes pay a cost of reproduction in a frog with biparental care. Biol J Linn Soc 115:211–218

    Article  Google Scholar 

  12. Dugas MB, Wamelink CL, Killius AM, Richards-Zawacki CL (2016) Parental care is beneficial for offspring, costly for mothers, and limited by family size in an egg-feeding frog. Behav Ecol 27:476–483

    Article  Google Scholar 

  13. Forbes LS (1990) Insurance offspring and the evolution of avian clutch size. J Theor Biol 147:345–359

    Article  Google Scholar 

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

    Google Scholar 

  15. Gray HM, Summers K, Ibáñez RD (2009) Kin discrimination in cannibalistic tadpoles of the green poison frog, Dendrobates auratus (Anura, Dendrobatidae). Phyllomedusa 8:41–50

    Article  Google Scholar 

  16. Haase A, Prohl H (2002) Female activity patterns and aggressiveness in the strawberry poison frog Dendrobates pumilio (Anura: Dendrobatidae). Amphibia-Reptilia 23:129–140

    Article  Google Scholar 

  17. Lessels CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121

    Article  Google Scholar 

  18. Maple MM (2002) Maternal effects on offspring fitness in Dendrobates pumilio, the strawberry poison frog. PhD dissertation, University of Kentucky, Lexington, KY

  19. Mock DW (1985) Siblicidal brood reduction: the prey size hypothesis. Am Nat 125:327–343

    Article  Google Scholar 

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

    Google Scholar 

  21. Mock DW, Lamey TC, Ploger BJ (1987) Proximate and ultimate roles of food amount in regulating egret sibling aggression. Ecology 68:1760–1722

    Article  Google Scholar 

  22. Morandini V, Ferrer M (2015) Sibling aggression and brood reduction: a review. Ethol Ecol Evol 27:2–16

    Article  Google Scholar 

  23. Muralidhar P, De Sá FP, Haddad CFB, Zamudio KR (2014) Kin-bias, breeding site selection and female fitness in a cannibalistic Neotropical frog. Mol Ecol 23:423–463

    Article  Google Scholar 

  24. Osorno JL, Drummond H (2003) Is obligate siblicidal aggression food sensitive? Behav Ecol Sociobiol 54:547–554

    Article  Google Scholar 

  25. Perry JC, Roitberg BD (2006) Trophic egg laying: hypotheses and tests. Oikos 112:706–714

    Article  Google Scholar 

  26. Pexton JJ, Meyhew PJ (2002) Siblicide and life-history evolution in parasitiods. Behav Ecol 13:690–695

    Article  Google Scholar 

  27. 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 

  28. Prӧhl H, Berke O (2001) Spatial distributions of male and female strawberry poison frogs and their relation to female reproductive resources. Oecologia 21:215–227

    Google Scholar 

  29. Reynolds JD, Goodwin NB, Freckleton RP (2002) Evolutionary transitions in parental care and live bearing in vertebrates. Philos T Roy Soc B 357:269–281

    Article  Google Scholar 

  30. Rojas B (2014) Strange parental decisions: fathers of the dyeing poison frog deposit their tadpoles in pools occupied by large cannibals. Behav Ecol Sociobiol 68:551–559

    Article  Google Scholar 

  31. Schulte LM, Lӧtters S (2013) The power of the seasons: rainfall triggers parental care in poison frogs. Evol Ecol 27:711–723

    Article  Google Scholar 

  32. Simmons RE (1988) Offspring quality and the evolution of Cainism. Ibis 130:339–356

    Article  Google Scholar 

  33. Stynoski JL (2009) Discrimination of offspring by indirect recognition in an egg-feeding dendrobatid frog, Oophaga pumilio. Anim Behav 78:1351–1356

    Article  Google Scholar 

  34. Stynoski JL (2012) Behavioural ecology of parental care in a dendrobatid frog (Oophaga pumilio). PhD dissertation, University of Miami, Miami, FL

  35. Stynoski JL, Torres–Mendoza Y, Sasa–Marin M, Saporito RA (2014) Evidence of maternal provisioning of alkaloid–based chemical defences in the strawberry poison frog Oophaga pumilio. Ecology 95:587–593

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  37. 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 

  38. Summers K, McKeon CS, Heying H, Hall J, Patrick W (2007) Social and environmental influences on egg size evolution in frogs. J Zool 271:225–232

    Article  Google Scholar 

  39. Tarvin RD, Santos JC, O’Connell LA, Zakon HH, Cannatella DC (2016) Convergent substitutions in a sodium channel suggest multiple origins of toxin resistance in poison frogs. Mol Biol Evol 33:1068–1081

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  41. Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chicago

    Google Scholar 

Download references

Acknowledgments

We thank Corinne Richards-Zawacki and the LaSelva Biological Station for support during this project. This work was funded by a grant from the Louisiana Board of Regents to MBD (LEQSF-EPS(2013)-PFUND-332). MBD was supported on a grant from the National Science foundation (Award 1146370). David Pfennig and two anonymous reviewers provided insightful comments that greatly improved the quality of this manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Matthew B. Dugas.

Ethics declarations

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures involving live animals were approved by Tulane University’s Institutional Animal Care and Use Committee (R0382-R1). The Ministerio de Ambiente, Energía y Telecomunicaciones of Costa Rica approved all methods and issued the appropriate permit (053-2013-SINAC).

Additional information

Communicated by D. W. Pfennig

Electronic supplementary material

Below is the link to the electronic supplementary material.

(MPG 7872 kb)

(MPG 6744 kb)

(MPG 8016 kb)

ESM 4

(PDF 72 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dugas, M.B., Stynoski, J. & Strickler, S.A. Larval aggression is independent of food limitation in nurseries of a poison frog. Behav Ecol Sociobiol 70, 1389–1395 (2016). https://doi.org/10.1007/s00265-016-2148-5

Download citation

Keywords

  • Aggression
  • Cannibalism
  • Food amount
  • Hypothesis
  • Parental care
  • Trophic egg