Naturwissenschaften

, Volume 101, Issue 4, pp 291–303

Frugal cannibals: how consuming conspecific tissues can provide conditional benefits to wood frog tadpoles (Lithobates sylvaticus)

  • Dale M. Jefferson
  • Keith A. Hobson
  • Brandon S. Demuth
  • Maud C. O. Ferrari
  • Douglas P. Chivers
Original Paper

Abstract

Tadpoles show considerable behavioral plasticity. When population densities become high, tadpoles often become cannibalistic, likely in response to intense competition. Conspecific tissues are potentially an ideal diet by composition and should greatly improve growth and development. However, the potential release of alarm cues from the tissues of injured conspecifics may act to deter potential cannibals from feeding. We conducted multiple feeding experiments to test the relative effects that a diet of conspecifics has on tadpole growth and development. Results indicate that while conspecific tissues represent a better alternative to starvation and provide some benefits over low-protein diets, such a diet can have detrimental effects to tadpole growth and/or development relative to diets of similar protein content. Additionally, tadpoles raised individually appear to avoid consuming conspecific tissues and may continue to do so until they suffer from the effects of starvation. However, tadpoles readily fed upon conspecific tissues immediately when raised with competitors. These results suggest that cannibalism may occur as a result of competition rather than the specific quality of available diets, unless such diets lead to starvation.

Keywords

Cannibalism Competition Density Diet Tadpole Lithobates sylvaticus 

Supplementary material

114_2014_1156_MOESM1_ESM.pdf (89 kb)
ESM 1(PDF 89 kb)
114_2014_1156_MOESM2_ESM.pdf (334 kb)
ESM 2(PDF 334 kb)

References

  1. Altig R, Whiles MR, Taylor CL (2007) What do tadpoles really eat? Assessing the trophic status of an understudied and imperilled group of consumers in freshwater habitats. Freshw Biol 52:386–395CrossRefGoogle Scholar
  2. Audo MC, Mann TM, Polk TL, Loudenslager CM, Diehl WJ, Altig R (1995) Food deprivation during different periods of tadpole (Hyla chysoscelis) ontogeny affects metamorphic performance differently. Oecologia 103:518–522CrossRefGoogle Scholar
  3. Babbitt KJ, Meshaka WE Jr (2000) Benefits of eating conspecifics: effects of background diet on survival and metamorphosis in the Cuban treefrog (Osteopilus septentrionalis). Copeia 2000:469–474CrossRefGoogle Scholar
  4. Biesterfield JM, Petranka JW, Sherbondy S (1993) Prevalence of chemical interference competition in natural populations of wood frogs, Rana sylvatica. Copeia 1993:688–695CrossRefGoogle Scholar
  5. Bleakney S (1958) Cannibalism in Rana sylvatica tadpoles: a well-known phenomenon. Herpetologica 14:34Google Scholar
  6. Bolker BM, de Castro F, Storfer A, Mech S, Harvey E, Collins JP (2008) Disease as a selective force precluding widespread cannibalism: a case study of an iridovirus of tiger salamanders, Ambystoma tigrinum. Evol Ecol Res 10:105–128Google Scholar
  7. Bridges CM (2002) Tadpoles balance foraging and predator avoidance: effects of predation, pond drying, and hunger. J Herpetol 36:627–634Google Scholar
  8. Caldwell JP, Araújo MC (1998) Cannibalistic interactions resulting from indiscriminate predatory behavior in tadpoles of poison frogs (Anura: Dendrobatidae). Biotropica 30:92–103CrossRefGoogle Scholar
  9. Collins JP, Cheek JE (1983) Effect of food and density on development of typical and cannibalistic salamander larvae in Ambystoma tigrinum nebulosum. Am Zool 23:77–84Google Scholar
  10. Costa CS, Pereyra MC, Alcalde L, Herrera R, Trudeau VL, Natale GS (2014) Underwater sound emission as part of an antipredator mechanism in Ceratophrys cranwelli tadpoles. Acta Zool–StockholmGoogle Scholar
  11. Crespi EJ, Denver RJ (2005) Roles of stress hormones in food intake regulation in anuran amphibians throughout the life cycle. Comp Biochem Physiol A 141:381–390CrossRefGoogle Scholar
  12. Crossland MR, Hearnden MN, Pizzatto L, Alford RA, Shine R (2011) Why be a cannibal? The benefits of cane toad, Rhinella marina [=Bufo marinus] tadpoles of consuming conspecific eggs. Anim Behav 82:775–782CrossRefGoogle Scholar
  13. Crump ML (1986) Cannibalism by younger tadpoles: another hazard of metamorphosis. Copeia 1986:1007–1009CrossRefGoogle Scholar
  14. Dickman M (1968) The effect of grazing by tadpoles on the structure of a periphyton community. Ecology 49:1188–1190CrossRefGoogle Scholar
  15. Duellman WE, Trueb L (1986) Biology of amphibians. McGraw-Hill, New YorkGoogle Scholar
  16. Fox LR (1975) Cannibalism in natural populations. Ann Rev Ecol Syst 6:87–106CrossRefGoogle Scholar
  17. Gannes LZ, O’Brien DM, del Rio CM (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78:1271–1276CrossRefGoogle Scholar
  18. Gosner ML (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 1960:183–190Google Scholar
  19. 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 153:338–347CrossRefGoogle Scholar
  20. Holbrook CT, Petranka JW, Douglas ME (2004) Ecological interactions between Rana sylvatica and Ambystoma maculatum: evidence of interspecific competition and facultative intraguild predation. Copeia 2004:932–939CrossRefGoogle Scholar
  21. Horat P, Semlitsch RD (1994) Effects of predation risk and hunger on the behaviour of two species of tadpoles. Behav Ecol Sociobiol 34:393–401Google Scholar
  22. Jefferson DM, Russell RW (2008) Ontogenetic and fertilizer effects on stable isotopes in the green frog (Rana clamitans). Appl Herpetol 5:189–196CrossRefGoogle Scholar
  23. Jefferson DM, Hobson KA, Chivers DP (2013) Understanding the information value of repeated exposure to chemical alarm cues: what can growth patterns tell us? Ann Zool Fenn 50:237–246CrossRefGoogle Scholar
  24. Jefferson DM, Hobson KA, Chivers DP (2014) Time to feed: how diet, competition, and experience may influence the feeding behaviour and cannibalism of wood frog tadpoles (Lithobates sylvaticus). Curr ZoolGoogle Scholar
  25. Kiesecker JM, Skelly DK, Beard KH, Preisser E (1999) Behavioral reduction of infection risk. Proc Natl Acad Sci U S A 96:9165–9168PubMedCentralPubMedCrossRefGoogle Scholar
  26. Kupferberg SJ (1997) The role of larval diet in anuran metamorphosis. Amer Zool 37:146–159Google Scholar
  27. Marcus R, Peritz E, Gabriel KR (1976) On closed testing procedures with special reference to ordered analysis of variance. Biometrika 63:655–660CrossRefGoogle Scholar
  28. McCallum ML, Trauth SE (2002) Performance of wood frog (Rana sylvatica) tadpoles on three soybean meal–cornmeal rations. Podarcis 3:78–85Google Scholar
  29. McCue MD (2007) Western diamondback rattlesnakes demonstrate physiological and biochemical strategies for tolerating prolonged starvation. Physiol Biochem Zool 80:25–34PubMedCrossRefGoogle Scholar
  30. Meffe GK, Crump ML (1987) Possible growth and reproductive benefits of cannibalism in the mosquito fish. Am Nat 129:203–212CrossRefGoogle Scholar
  31. Newman RA (1987) Density and predation on Scaphiopus couchii tadpoles in desert ponds. Oecologia 71:301–307CrossRefGoogle Scholar
  32. Peacor SD, Pfister CA (2006) Experimental and model analyses of the effects of competition on individual size variation in wood frog (Rana sylvatica) tadpoles. J Anim Ecol 75:990–999PubMedCrossRefGoogle Scholar
  33. Petranka JW, Thomas DG (1995) Explosive breeding reduces egg and tadpole cannibalism in the wood frog, Rana sylvatica. Anim Behav 50:731–739CrossRefGoogle Scholar
  34. Petranka JW, Rushlow AW, Hopey ME (1998) Predation by tadpoles of Rana sylvatica on Ambystoma maculatum: implication of ecological role reversals by Rana (predator) and Ambystoma (prey). Herpetologica 54:1–13Google Scholar
  35. Pfennig DW, Ho SG, Hoffman EA (1998) Pathogen transmission as a selective force against cannibalism. Anim Behav 55:1255–1261PubMedCrossRefGoogle Scholar
  36. R Development Core Team (2010) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna.— cran.r-project.org/doc/manuals/refman.pdfGoogle Scholar
  37. Reeve E, Ndriantsoa SH, Strauβ A, Randrianiaina R-D, Hiobiarilanto TR, Glaw F, Glos J, Vences M (2011) Acoustic underwater signals with a probable function during competitive feeding in a tadpole. Naturwissenschaften 98:135–143PubMedCrossRefGoogle Scholar
  38. Relyea RA (2002) Competitor-induced plasticity in tadpoles: consequences, cues, and connections to predator-induced plasticity. Ecol Monogr 72:523–540CrossRefGoogle Scholar
  39. Relyea RA (2004) Fine-tuned phenotypes: tadpole plasticity under 16 combinations of predators and competitors. Ecology 82:172–179CrossRefGoogle Scholar
  40. Richter-Boix A, Llorente GA, Montori A, Garcia J (2007) Tadpole diet selection varies with the ecological context in predictable ways. Basic Appl Ecol 8:464–474CrossRefGoogle Scholar
  41. Schiesari L, Werner EE, Kling GW (2009) Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology. Freshw Biol 54:572–586CrossRefGoogle Scholar
  42. Secco EM, De Stéfani MV, Vidotti RM (2005) Apparent digestibility of different ingredients in diets for bullfrog Rana catesbeiana tadpoles. J World Aquacult Soc 36:135–140CrossRefGoogle Scholar
  43. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New YorkGoogle Scholar
  44. Steinwascher K, Travis J (1983) Influence of food quality and quantity on early larval growth of two anurans.  Copeia 1983:238–242Google Scholar
  45. Sterner RW, Elser JJ (2002) Ecology of stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  46. Trakimas G, Jardine TD, Barisevičiūtė R, Garbaras A, Skipitytė R, Remeikis V (2011) Ontogenetic dietary shifts in European common frog (Rana temporaria) revealed by stable isotopes. Hydrobiologia 675:87–95CrossRefGoogle Scholar
  47. Venesky MD, Wilcoxen TE, Rensel MA, Rollins-Smith L, Kerby JL, Parris MJ (2012) Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles. Oecologia 169:23–31PubMedCrossRefGoogle Scholar
  48. Waldman B (1985) Olfactory basis of kin recognition in toad tadpoles. J Comp Physiol A 156:564–577CrossRefGoogle Scholar
  49. Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363CrossRefGoogle Scholar
  50. Wildy EL, Chivers DP, Kiesecker JM, Blaustein AR (2001) The effects of food level and conspecific density on biting and cannibalism in larval long-toed salamanders, Ambystoma macrodactylum. Oecologia 128:202–209CrossRefGoogle Scholar
  51. Wilkinson L (1998) Systat, the system for statistics. Systat Inc., EvanstonGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Dale M. Jefferson
    • 1
  • Keith A. Hobson
    • 2
  • Brandon S. Demuth
    • 1
  • Maud C. O. Ferrari
    • 3
  • Douglas P. Chivers
    • 1
  1. 1.Department of BiologyUniversity of SaskatchewanSaskatoonCanada
  2. 2.Environment CanadaSaskatoonCanada
  3. 3.Department of Biomedical Sciences WCVMUniversity of SaskatchewanSaskatoonCanada

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