Behavioral Ecology and Sociobiology

, Volume 63, Issue 2, pp 241–250 | Cite as

Ancient behaviors of larval amphibians in response to an emerging fungal pathogen, Batrachochytrium dendrobatidis

  • Barbara A. Han
  • Paul W. Bradley
  • Andrew R. Blaustein
Original Paper


Behaviors have evolved in response to various selection pressures over evolutionary time. However, not all behaviors are adaptive. Some presumably “ancient” behaviors, persistent for millions of years, may be detrimental in the face of novel selection pressures in modern times. These pressures include a multitude of emerging infectious diseases which may be stimulated by environmental changes. We examined how a globally emerging amphibian pathogen, Batrachochytrium dendrobatidis (BD), affected two key evolutionarily persistent behaviors displayed by amphibian larvae: aggregation and thermoregulation. Larval aggregation behavior is often essential for foraging, thermoregulation, and antipredator defense, but varies among species. Thermoregulatory behavior speeds larval development in ephemeral habitats. Specifically, we examined whether aggregation and thermoregulatory behaviors changed when exposed to the BD pathogen in two species (Bufo boreas and Rana cascadae) whose larvae aggregate in nature. In laboratory choice tests, larvae of neither species avoided infected conspecifics. BD-exposed B. boreas larvae aggregated, while unexposed R. cascadae larvae associated more frequently with BD-exposed conspecifics. There was no evidence of behavioral fever or altered thermoregulation in larvae of four species we examined (Pseudacris regilla, Rana aurora, B. boreas, R. cascadae). The absence of behavioral fever may suggest an inability of the larvae of some host species to mediate infection risk by this pathogen. Thermoregulatory behaviors may exhibit a high degree of evolutionary inertia in amphibian hosts because they are linked with host physiology and developmental rates, while altered aggregation behaviors could potentially elevate pathogen transmission rates, leading to increased infection risk in social amphibian species.


Tadpoles Aggregation Schooling Thermoregulation Chytridiomycosis 



We thank J Ng, H Lee, S Smith, R LeMaster, M Westphal, BW Patton, J Takishita, J Romansic, R Hill, T Young, J Hubbard, B Moore, S Yi, K Bryant and P House for assistance. B Bancroft and N Baker constructed thermal gradients. J Kerby ran supplemental PCR analyses and provided insightful discussion to improve this manuscript. Training by JE Longcore and LB Kats made this work possible. Authors were funded by the Budweiser Conservation Scholarship (BAH), the Howard Hughes Medical Institute grant for undergraduate research (PWB), and the National Science Foundation Integrated Research Challenges in Environmental Biology (NSF IRCEB) Program (DEB0213851 and IBN9977063). All aspects of this study comply with US laws and adhere to standards of the Institutional Animal Care and Use Committee at Oregon State University.


  1. Altig R (2007) Comments on the descriptions and evaluations of tadpole mouthpart anomalies. Herpetol Conserv Biol 2:1–4CrossRefGoogle Scholar
  2. Altizer S, Harvell D, Friedle E (2003a) Rapid evolutionary dynamics and disease threats to biodiversity. TREE 18:589–596Google Scholar
  3. Altizer S, Nunn CL, Thrall PH, Gittleman JL, Antonovics J, Cunningham AA, Dobson AP, Ezenwa V, Jones KE, Pedersen AB, Poss M, Pulliam JRC (2003b) Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu Rev Ecol Evol Syst 34:517–547 doi: 10.1146/annurev.ecolsys.34.030102.151725 CrossRefGoogle Scholar
  4. Bancroft BA, Baker NJ, Searle CL, Garcia TS, Blaustein AR (2008) Larval amphibians seek warm temperatures and do not avoid harmful UVB radiation. Behav Ecol 19(4):879–886CrossRefGoogle Scholar
  5. Battin J (2004) When good animals love bad habits: ecological traps and the conservation of animal populations. Conserv Biol 16:1482–1491CrossRefGoogle Scholar
  6. Behringer DC, Butler MJ, Shields JD (2006) Avoidance of disease by social lobsters. Nature 441:421 doi: 10.1038/441421 PubMedCrossRefGoogle Scholar
  7. Beiswenger RE (1977) Diel patterns of aggregative behavior in tadpole of Bufo americanus, in relation to light and temperature. Ecology 58:98–108CrossRefGoogle Scholar
  8. Berger L, Speare R, Hyatt AD (1999) Chytrid fungi and amphibian declines: overview, implications and future directions. In: Campbell A (ed) Declines and disappearances of Australian frogs. Environment Australia, Canberra, pp 23–33Google Scholar
  9. Berger L, Hyatt AD, Speare R, Longcore JE (2005) Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Dis Aquat Org 68:51–63PubMedCrossRefGoogle Scholar
  10. Blaustein AR, Bancroft BA (2007) Amphibian population declines: evolutionary considerations. BioScience 57:437–444 doi: 10.1641/B570517 CrossRefGoogle Scholar
  11. Blaustein AR, Romansic JM, Scheessele EA, Han BA, Pessier AP, Longcore JE (2005) Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conserv Biol 19:1460–1468CrossRefGoogle Scholar
  12. Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Org 60:141–148PubMedCrossRefGoogle Scholar
  13. Brattstrom BH (1962) Thermal control of aggregation behavior in tadpoles. Herpetologica 18:38–46Google Scholar
  14. Brattstrom BH (1963) A preliminary review of the thermal requirements of amphibians. Ecology 44:238–255CrossRefGoogle Scholar
  15. Crump ML (1983) Opportunistic cannibalism by amphibian larvae of temporary aquatic environments. Am Nat 121:281–289CrossRefGoogle Scholar
  16. Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9:141–150CrossRefGoogle Scholar
  17. de Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecol Lett 8:117–126CrossRefGoogle Scholar
  18. Dugatkin LA, FitzGerald GJ, Lavoie J (1994) Juvenile three-spined sticklebacks avoid parasitized conspecifics. Environ Biol Fishes 39:215–218CrossRefGoogle Scholar
  19. Dupré RK, Petranka JW (1985) Ontogeny of temperature selection in larval amphibians. Copeia 1985:462–467CrossRefGoogle Scholar
  20. Freeland WJ (1976) Pathogens and the evolution of primate sociality. Biotropica 8:12–24CrossRefGoogle Scholar
  21. Garcia TS, Romansic JM, Blaustein AR (2006) Survival of three species of anuran metamorphs exposed to UV-B radiation and the pathogenic fungus Batrachochytrium dendrobatidis. Dis Aquat Org 72:163–169PubMedCrossRefGoogle Scholar
  22. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  23. Griffiths RA, Foster JP (1998) The effect of social interactions on tadpole activity and growth in the British anuran amphibians (Bufo bufo, B. calamita, and Rana temporaria). J Zool Lond 245:431–437CrossRefGoogle Scholar
  24. 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
  25. Hoff KVS, Blaustein AR, McDiarmid RW, Altig R (1999) Behavior: interactions and their consequences. In: McDiarmid RW, Altig R (eds) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago London, pp 215–239Google Scholar
  26. Huey RB (1982) Temperature, physiology, and the ecology of reptiles. In: Gans C, Pough FH (eds) Biology of the Reptilia. Academic, New York, pp 25–74Google Scholar
  27. Huey RB, Hertz PE, Sinervo B (2003) Behavioral drive versus behavioral inertia in evolution: a null model approach. Am Nat 161:357–366 doi: 10.1086/346135 PubMedCrossRefGoogle Scholar
  28. Kavaliers M, Colwell DD (1992) Aversive responses of female mice to the odors of parasitized males: neuromodulatory mechanisms and implications for mate choice. Ethology 95:202–212CrossRefGoogle Scholar
  29. Kavaliers M, Colwell DD (1995) Discrimination by female mice between the odours of parasitized and non-parasitized males. Proc R Soc Lond Ser B 261:31–35CrossRefGoogle Scholar
  30. Kermack WO, McKendrick AG (1927) A contribution to the mathematical theory of epidemics. Proc R Soc Lond Ser A 115:700–721CrossRefGoogle Scholar
  31. Kiesecker JM, Skelly DK, Beard KH, Preisser E (1999) Behavioral reduction of infection risk. Proc Natl Acad Sci U S A 96:9165–6198PubMedCrossRefGoogle Scholar
  32. Kluger MJ, Kozak W, Conn CA, Leon LR, Soszynski D (1998) Role of fever in disease. Ann N Y Acad Sci 856:224–233PubMedCrossRefGoogle Scholar
  33. Koko H, Sutherland WJ (2001) Ecological traps in changing environments: ecological and evolutionary consequences of a behaviourally mediated Allee effect. Evol Ecol Res 3:537–551Google Scholar
  34. Kriger KM, Hero J-M (2007) The chytrid fungus Batrachochytrium dendrobatidis in non-randomly distributed across amphibian breeding habitats. Divers Distrib 13:781–788CrossRefGoogle Scholar
  35. Lefcort H, Blaustein AR (1995) Disease, predator avoidance, and vulnerability to predation in tadpoles. Oikos 74:469–474CrossRefGoogle Scholar
  36. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Carey C, Livo L, Pessier AP, Collins JP (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci U S A 103:3165–3170 doi: 10.1073/pnas.0506889103 PubMedCrossRefGoogle Scholar
  37. Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227CrossRefGoogle Scholar
  38. Moore J (2002) Parasites and the behavior of animals. Oxford University Press, OxfordGoogle Scholar
  39. Morens DM, Folkers GK, Fauci AS (2004) The challenges of emerging and re-emerging infectious diseases. Nature 430:242–249PubMedCrossRefGoogle Scholar
  40. O’Hara RK (1981) Habitat selection behavior in three species of anuran larvae: environmental cues, ontogeny, and adaptive significance. PhD dissertation, Oregon State UniversityGoogle Scholar
  41. Ouedraogo RM, Cusson M, Goettel MS, Brodeur J (2003) Inhibition of fungal growth in thermoregulating locusts, Locusta migratoria, infected by the fungus Metarhizium anisopliae var acridum. J Invertebr Path 82:103–109 doi: 10.1016/S0022-2011(02)00185-4 CrossRefGoogle Scholar
  42. Parris MJ, Davis A, Collins JP (2004) Single-host pathogen effects on mortality and behavioral responses to predators in salamanders (Urodela: Ambystomatidae). Can J Zool 82:1477–1483CrossRefGoogle Scholar
  43. Parrish JK, Edelstein-Keshet L (1999) Complexity, pattern, and evolutionary trade-offs in animal aggregation. Science 284:99–101PubMedCrossRefGoogle Scholar
  44. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15CrossRefGoogle Scholar
  45. Pfennig DW, Ho SG, Hoffman EA (1998) Pathogen transmission as a selective force against cannibalism. Anim Behav 55:1255–1261PubMedCrossRefGoogle Scholar
  46. Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Sanchez-Azofeifa GA, Still CJ, Young BE (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167PubMedCrossRefGoogle Scholar
  47. Putnam RW, Bennett AF (1981) Thermal dependence of behavioural performance of anuran amphibians. Anim Behav 29:502–509CrossRefGoogle Scholar
  48. Rachowicz LJ, Knapp RA, Morgan JAT, Stice MJ, Vredenburg VT, Parker JM, Briggs CJ (2006) Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87:1671–1683PubMedCrossRefGoogle Scholar
  49. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. TREE 17:462–468Google Scholar
  50. Robertson BA, Hutto RL (2006) A framework for understanding ecological traps and an evaluation of existing evidence. Ecology 87:1075–1085PubMedCrossRefGoogle Scholar
  51. Rowley JJL, Alford RA (2007) Behaviour of Australian rainforest stream frogs may affect the transmission of chytridiomycosis. Dis Aquat Org 77:1–9 doi: 10.3354/dao01830 PubMedCrossRefGoogle Scholar
  52. Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu Rev Entomol 51:331–357 doi: 10.1146/annurev.ento.51.110104.150941 PubMedCrossRefGoogle Scholar
  53. Schlaepfer MA, Runge MC, Sherman PW (2002) Ecological and evolutionary traps. TREE 17:474–480Google Scholar
  54. Schlaepfer MA, Sherman PW, Blossey B, Runge MC (2005) Introduced species as evolutionary traps. Ecol Lett 8:241–246CrossRefGoogle Scholar
  55. Schlaepfer MA, Sredl MJ, Rosen PC, Ryan MJ (2007) High prevalence of Batrachochytrium dendrobatidis in wild populations of lowland leopard frogs Rana yavapaiensis in Arizona. EcoHealth 4:421–427CrossRefGoogle Scholar
  56. Schloegel LM, Hero JM, Berger L, Speare R, McDonald K, Daszak P (2006) The decline of the sharp-snouted day frog (Taudactylus acutirostris): the first documented case of extinction by infection in a free-ranging wildlife species? EcoHealth 3:35–40 doi: 10.1007/s10393-005-0012-6v CrossRefGoogle Scholar
  57. Sparrow FK (1968) Ecology of freshwater fungi. In: Gainsworth GC, Sussman AS (eds) The fungi. Academic, New York, pp 41–93Google Scholar
  58. Wassersug RJ (1973) Aspects of social behavior in anuran larvae. In: Vial JL, Blair WF, Bogart JP, Duellman WE, Estes R, Guttman SI, Lynch JD, Merrell DJ, Rabb GB, Reig OA, Salthe SN, Savage JM, Schiøtz A, Starrett PH, Straughan IR, Trueb L, Wassersug RJ (eds) Evolutionary biology of the anurans: contemporary research on major problems. University of Missouri Press, Columbia, MissouriGoogle Scholar
  59. Watt PJ, Nottingham SF, Young S (1997) Toad tadpole aggregation behaviour: evidence for a predator avoidance function. Anim Behav 54:865–872PubMedCrossRefGoogle Scholar
  60. Wcislo WT (1989) Behavioral environments and evolutionary change. Ann Rev Ecolog Syst 20:137–169CrossRefGoogle Scholar
  61. Weldon C, Du Preez LH (2006) Quantitative measurement of Batrachochytrium dendrobatidis in amphibian skin. Dis Aquat Org 72:153–161PubMedCrossRefGoogle Scholar
  62. West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Ann Rev Ecolog Syst 20:249–279CrossRefGoogle Scholar
  63. Woodhams DC, Alford RA, Marantelli G (2003) Emerging disease of amphibians cured by elevated body temperature. Dis Aquat Org 55:65–67PubMedCrossRefGoogle Scholar
  64. Yamakazi K, Sugiura S, Fukasawa Y (2004) Epizootics and behavioral alteration in the arctiid caterpillar Chionarctia nivea (Lepidoptera: Arctiidae) caused by an entomopathogenic fungus, Entomophaga aulicae (Zygomycetes: Entomophthorales). Entomol Sci 7:219–223CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Barbara A. Han
    • 1
  • Paul W. Bradley
    • 1
  • Andrew R. Blaustein
    • 1
  1. 1.Department of ZoologyOregon State UniversityCorvallisUSA

Personalised recommendations