Advertisement

Oecologia

, Volume 171, Issue 1, pp 115–127 | Cite as

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study

  • Ana L. NunesEmail author
  • Alex Richter-Boix
  • Anssi Laurila
  • Rui Rebelo
Behavioral ecology - Original research

Abstract

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.

Keywords

Tadpole Activity level Spatial avoidance Behavioural plasticity Exotic predator 

Notes

Acknowledgments

We thank Pedro Andrade, Erika Almeida, Susana Alves and Cátia Guerreiro for their invaluable help in the field and experimental work, Hélder Duarte for providing data on species phylogeny and Jesús Díaz-Rodríguez for providing an insight on the Pelodytes taxonomy. Permits were provided by the Portuguese Instituto da Conservação da Natureza e da Biodiversidade (ICNB). This research was funded by the FCT Project POCI/BIA-BDE/56100/2004, FCT grant SFRH/BD/29068/2006 and by Stiftelsen för Zoologisk Forskning.

Supplementary material

442_2012_2389_MOESM1_ESM.doc (74 kb)
Supplementary material 1 (DOC 73 kb)

References

  1. Abouheif E (1999) A method to test the assumption of phylogenetic independence in comparative data. Evol Ecol Res 1:895–909Google Scholar
  2. Almaça C (1991) L’ecrevisse a pieds blancs, Astacus pallipes Lereboullet 1858, au Portugal. L’Astaciculteur de France 28:11–16Google Scholar
  3. Aquiloni L, Ilhéu M, Gherardi F (2005) Habitat use and dispersal of the invasive crayfish Procambarus clarkii in ephemeral water bodies of Portugal. Mar Freshw Behav Physiol 38:225–236CrossRefGoogle Scholar
  4. Blackburn TM, Pettorelli N, Katzner T, Gompper ME, Mock K, Garner TWJ, Altwegg R, Redpath S, Gordon IJ (2010) Dying for conservation: eradicating invasive alien species in the face of opposition. Anim Conserv 13:227–228CrossRefGoogle Scholar
  5. Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. Ecoscience 5:338–352Google Scholar
  6. Cox JG, Lima SL (2006) Naiveté and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680PubMedCrossRefGoogle Scholar
  7. Cruz MJ, Rebelo R (2005) Vulnerability of southwest Iberian amphibians to an introduced crayfish, Procambarus clarkii. Amphibia-Reptilia 26:293–303CrossRefGoogle Scholar
  8. Cruz MJ, Rebelo R (2007) Colonization of freshwater habitats by an introduced crayfish, Procambarus clarkii, in Southwest Iberian Peninsula. Hydrobiologia 575:191–201CrossRefGoogle Scholar
  9. Duarte H, Tejedo M, Katzenberger M, Marangoni F, Baldo D, Beltrán JF, Martí DA, Richter-Boix A, Gonzalez-Voyer A (2012) Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities. Global Change Biol 18:412–421CrossRefGoogle Scholar
  10. Eklöv P, Werner EE (2000) Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae. Oikos 88:250–258CrossRefGoogle Scholar
  11. Ferrari MCO, Wisenden BD, Chivers DP (2010) Chemical ecology of predator-prey interactions in aquatic ecosystems: a review and prospectus. Can J Zool 88:698–724CrossRefGoogle Scholar
  12. Fraker M, Hu E, Cuddapah V, McCollum S, Relyea R, Hempel H, Denver R (2009) Characterization of an alarm pheromone secreted by amphibian tadpoles that induces behavioral inhibition and suppression of the neuroendocrine stress axis. Horm Behav 55:520–529PubMedCrossRefGoogle Scholar
  13. Gall BG, Mathis A (2010) Innate predator recognition and the problem of introduced trout. Ethology 116:47–58CrossRefGoogle Scholar
  14. Gamradt SC, Kats LB (1996) Effect of introduced crayfish and mosquitofish on California newts. Conserv Biol 10:1155–1162CrossRefGoogle Scholar
  15. Gasc JP, Cabela A, Crnobrnja-Isailovic J, Dolmen D, Grossenbacher K, Haffner P, Lescure J, Martens H, Martínez Rica JP, Maurin H, Oliveira ME, Sofianidou TS, Veith M, Zuiderwijk A (1997) Atlas of amphibians and reptiles in Europe, Collection Patrimoines Naturels, 29. SPN/IEGB/MNHN, Paris 496 ppGoogle Scholar
  16. Gherardi F (2006) Crayfish invading Europe: the case study of Procambarus clarkii. Mar Freshw Behav Physiol 39:175–191CrossRefGoogle Scholar
  17. Gómez VI, Kehr AI (2011) Morphological and developmental responses of anuran larvae (Physalaemus albonotatus) to chemical cues from the predators Moenkhausia dichoroura (Characiformes: Characidae) and Belostoma elongatum (Hemiptera: Belostomatidae). Z. Zool Stud 50:203–210Google Scholar
  18. Gomez-Mestre I, Díaz-Paniagua C (2011) Invasive predatory crayfish do not trigger inducible defences in tadpoles. Proc Royal Soc Lond B 278:3364–3370CrossRefGoogle Scholar
  19. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  20. Habsburgo-Lorena AS (1983) Socioeconomic aspects of the crawfish industry in Spain. Freshw Crayfish 5:552–554Google Scholar
  21. Hagman M (2008) Behavioral responses by tadpoles of six Australian species to chemical cues from other tadpoles. Herpetol Conserv Biol 3:239–246Google Scholar
  22. Hettyey A, Zsarnóczai S, Vincze K, Hoi H, Laurila A (2010) Interactions between the information content of different chemical cues affect induced defences in tadpoles. Oikos 119:1814–1822CrossRefGoogle Scholar
  23. Hobbs HH, Jass JP, Huner JV (1989) A review of global crayfish introductions with particular emphasis on two North-American species (Decapoda, Cambaridae). Crustaceana 56:299–316CrossRefGoogle Scholar
  24. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  25. Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110CrossRefGoogle Scholar
  26. Knapp RA (2005) Effects of nonnative fish and habitat characteristics on lentic herpetofauna in Yosemite National Park, USA. Biol Conserv 121:265–279CrossRefGoogle Scholar
  27. Larson ER, Olden JD (2010) Latent extinction and invasion risk of crayfishes in the southeastern United States. Conserv Biol 24:1099–1110PubMedCrossRefGoogle Scholar
  28. Laurila A, Kujasalo J, Ranta E (1997) Different antipredator behaviour in two anuran tadpoles: effects of predator diet. Behav Ecol and Sociobiol 40:329–336CrossRefGoogle Scholar
  29. Laurila A, Kujasalo J, Ranta E (1998) Predator-induced changes in life-history in two anuran tadpoles: effects of predator diet. Oikos 83:307–317CrossRefGoogle Scholar
  30. Laurila A, Järvi-Laturi M, Pakkasmaa S, Merilä J (2004) Temporal variation in predation risk: stage-dependency, graded responses and fitness costs in tadpole antipredator defences. Oikos 107:90–99CrossRefGoogle Scholar
  31. Lima SL (1998) Nonlethal effects in the ecology of predator–prey interactions: what are the ecological effects of anti-predator decision-making? Bioscience 48:25–34CrossRefGoogle Scholar
  32. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640CrossRefGoogle Scholar
  33. Lodge DM, Stein RA, Brown KM, Covich AP, Bronmark C, Garvey JE, Klosiewski SP (1998) Predicting impact of freshwater exotic species on native biodiversity: challenges in spatial scaling. Aust J Ecol 23:53–67CrossRefGoogle Scholar
  34. Loureiro A, Ferrand de Almeida N, Carretero MA, Paulo OS (eds) (2008) Atlas dos Anfíbios e Répteis de Portugal. Instituto da Conservação da Natureza e da Biodiversidade, Lisboa 257 ppGoogle Scholar
  35. Magurran AE (1990) The adaptive significance of schooling as an anti-predator defence in fish. Ann Zool Fennici 27:3–18Google Scholar
  36. Marquis O, Saglio P, Neveu A (2004) Effects of predators and conspecific chemical cues on the swimming activity of Rana temporaria and Bufo bufo tadpoles. Arch Hydrobiol 160:153–170CrossRefGoogle Scholar
  37. Nicieza AG, Álvarez DA, Atienza EMS (2006) Delayed effects of larval predation risk and food quality on anuran juvenile performance. J Evol Biol 19:1092–1103PubMedCrossRefGoogle Scholar
  38. Pearl CA, Adams MJ, Schuytema GS, Nebeker AV (2003) Behavioral responses of anuran larvae to chemical cues of native and introduced predators in the Pacific Northwestern United States. J Herpetol 37:572–576CrossRefGoogle Scholar
  39. Petranka JW, Hayes LJ (1998) Chemically mediated avoidance of a predatory odonate (Anax junius) by American toad (Bufo americanus) and wood frog (Rana sylvatica) tadpoles. B. Behav Ecol Sociobiol 42:263–271CrossRefGoogle Scholar
  40. Reeve J, Abouheif E (2003) Phylogenetic Independence. Version 2.0. Computer ProgramGoogle Scholar
  41. Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540CrossRefGoogle Scholar
  42. Relyea RA (2003) Predators come and predators go: the reversibility of predator-induced traits. Ecology 84:1840–1848CrossRefGoogle Scholar
  43. Richardson JML (2001) A comparative study of activity levels in larval anurans and response to the presence of different predators. Behav Ecol 12:51–58CrossRefGoogle Scholar
  44. Richter-Boix A, Llorente GA, Montori A (2007) A comparative study of predator-induced phenotype in tadpoles across a pond permanency gradient. Hydrobiologia 583:43–56CrossRefGoogle Scholar
  45. Schoeppner NM, Relyea RA (2005) Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett 8:505–512PubMedCrossRefGoogle Scholar
  46. Schoeppner NM, Relyea RA (2009) Interpreting the smells of predation: how alarm cues and kairomones induce different prey defences. Funct Ecol 23:1114–1121CrossRefGoogle Scholar
  47. Semlitsch RD, Gavasso S (1992) Behavioural responses of Bufo bufo and Bufo calamita tadpoles to chemical cues of vertebrate and invertebrate predators. Ethol Ecol Evol 4:165–173CrossRefGoogle Scholar
  48. Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator-prey naiveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621CrossRefGoogle Scholar
  49. Slusarczk M (1999) Predator-induced diapause in Daphnia magna may require two chemical cues. Oecologia 119:159–165CrossRefGoogle Scholar
  50. Smith GR, Awan AR (2009) The roles of predator identity and group size in the antipredator responses of American toad (Bufo americanus) and bullfrog (Rana catesbeiana) tadpoles. Behaviour 146:225–243CrossRefGoogle Scholar
  51. Steiner UK (2007) Investment in defense and cost of predator-induced defense along a resource gradient. Oecologia 152:201–210PubMedCrossRefGoogle Scholar
  52. Stirling G (1995) Daphnia behavior as a bioassay of fish presence or predation. Funct Ecol 9:778–784CrossRefGoogle Scholar
  53. Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:354–371CrossRefGoogle Scholar
  54. Tejedo M (1993) Size-dependent vulnerability and behavioral responses of tadpoles of two anuran species to beetle larvae predators. Herpetologica 49:287–294Google Scholar
  55. Van Buskirk J (2002) A comparative test of the adaptive plasticity hypothesis: relationships between habitat and phenotype in anuran larvae. Am Nat 160:87–102PubMedCrossRefGoogle Scholar
  56. Van Buskirk J, Arioli M (2002) Dosage response of an induced defense: how sensitive are tadpoles to predation risk? Ecology 83:1580–1585CrossRefGoogle Scholar
  57. Wellborn GA, Skelly DK, Werner EE (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annu Rev Ecol Syst 27:337–363CrossRefGoogle Scholar
  58. Werner EE, Anholt BR (1996) Predator-induced behavioral indirect effects: consequences to competitive interactions in anuran larvae. Ecology 77:157–169CrossRefGoogle Scholar
  59. Witte F, Goldschmidt T, Wanink J, Van Oijen M, Goudswaard K, Witte-Maas E, Bouton N (1992) The destruction of an endemic species flock: quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environ Biol Fishes 34:1–28CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Ana L. Nunes
    • 1
    • 2
    Email author
  • Alex Richter-Boix
    • 2
  • Anssi Laurila
    • 2
  • Rui Rebelo
    • 1
  1. 1.Departamento de Biologia Animal, Centro de Biologia AmbientalFaculdade de Ciências da Universidade de LisboaLisbonPortugal
  2. 2.Population and Conservation Biology/Department of Ecology and Genetics, Evolutionary Biology CentreUppsala UniversityUppsalaSweden

Personalised recommendations