Advertisement

Oecologia

, Volume 189, Issue 3, pp 637–645 | Cite as

The role of predation risk in metamorphosis versus behavioural avoidance: a sex-specific study in a facultative paedomorphic amphibian

  • M. DenoëlEmail author
  • L. Drapeau
  • N. Oromi
  • L. Winandy
Behavioral ecology – original research

Abstract

Evolutionary theory predicts the evolution of metamorphosis over paedomorphosis (the retention of larval traits at the adult stage) in response to life in unfavourable habitats and to the benefits of dispersal. Although many organisms are canalised into obligatory complex or simple life cycles, some species of newts and salamanders can express both processes (facultative paedomorphosis). Previous research highlighted the detrimental effect of fish on both metamorphic and paedomorphic phenotypes, but it remains unknown whether predation risk could induce shifts from paedomorphosis to metamorphosis, whether behavioural avoidance could be an alternative strategy to metamorphosis and whether these responses could be sex-biased. Testing these hypotheses is important because metamorphosed paedomorphs are dispersal individuals which could favour the long-term persistence of the process by breeding subsequently in more favourable waters. Therefore, we quantified the spatial behaviour and timing of the metamorphosis of facultative paedomorphic palmate newts Lissotriton helveticus in response to predation risk. We found that fish induced both male and female paedomorphs to hide more often, but behavioural avoidance was not predictive of metamorphosis. Paedomorphs did not metamorphose more in the presence of fish, yet there was an interaction between sex and predation risk in metamorphosis timing. These results improve our understanding of the lower prevalence of paedomorphs in fish environments and of the female-biased sex ratios in natural populations of paedomorphic newts. Integrating sex-dependent payoffs of polyphenisms and dispersal across habitats is therefore essential to understand the evolution of these processes in response to environmental change.

Keywords

Behavioural avoidance Facultative paedomorphosis Invasive species Metamorphosis Polymorphism 

Notes

Acknowledgements

We wish to thank J.L. Soulié for allowing access to the pond and two anonymous reviewers for their constructive comments on our manuscript. MD is a Research Director at the Fonds de la Recherche Scientifique—FNRS, LW was a PhD fellow at FNRS and is now funded by a Fyssen Foundation post-doctoral fellowship and NO was a Marie Curie COFUND post-doctoral fellow. This study was funded by Fonds de la Recherche Scientifique—FNRS grant numbers J.008.13 and J.0112.16.

Author contribution statement

MD and LW conceived and supervised the study. MD, LD and NO collected newts in the field. LD carried out behavioural observations. LD, NO, LW, and MD participated to the logistics of the experiment. LW and MD carried out the statistical analyses. MD wrote the first draft of the manuscript, and MD, LW and NO contributed to the revisions. All authors agreed on the final version of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and national guidelines for the care and use of animals were followed. The capture permit was issued by DREAL Languedoc-Roussillon (decree 2013274-0001). All experiments were approved by the University of Liège’s animal ethical committee (authorization 1613).

Supplementary material

442_2019_4362_MOESM1_ESM.pdf (141 kb)
Supplementary material 1 (pdf 140 kb)

References

  1. Andrews JH (2017) Comparative ecology of microorganisms and macroorganisms. Springer, New York.  https://doi.org/10.1007/978-1-4939-6897-8_6 CrossRefGoogle Scholar
  2. Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35:651–673.  https://doi.org/10.1146/annurev.ecolsys.35.021004.112426 CrossRefGoogle Scholar
  3. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135.  https://doi.org/10.1016/j.tree.2008.10.008 CrossRefGoogle Scholar
  4. Bonett RM, Blair AL (2017) Evidence for complex life cycle constraints on salamander body form diversification. Proc Natl Acad Sci USA 114:9936–9941.  https://doi.org/10.1073/pnas.1703877114 CrossRefGoogle Scholar
  5. Bonett RM, Steffen MA, Lambert SM, Wiens JJ, Chippindale PT (2014) Evolution of paedomorphosis in plethodontid salamanders: ecological correlates and re-evolution of metamorphosis. Evolution 68:466–482.  https://doi.org/10.1111/evo.12274 CrossRefGoogle Scholar
  6. Bucciarelli GM, Blaustein AR, Garcia TS, Kats LB (2014) Invasion complexities: the diverse impacts of nonnative species on amphibians. Copeia 2014:611–632.  https://doi.org/10.1643/OT-14-014 CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  8. Chiocchio A, Bisconti R, Zampiglia M, Nascetti G, Canestrelli D (2017) Quaternary history, population genetic structure and diversity of the cold-adapted Alpine newt Ichthyosaura alpestris in peninsular Italy. Sci Rep 7:2955.  https://doi.org/10.1038/s41598-017-03116-x CrossRefGoogle Scholar
  9. Contreras V, Martinez-Meyer E, Valiente E, Zambrano L (2009) Recent decline and potential distribution in the last remnant area of the microendemic Mexican axolotl (Ambystoma mexicanum). Biol Conserv 142:2881–2885.  https://doi.org/10.1016/j.biocon.2009.07.008 CrossRefGoogle Scholar
  10. Davis DR, Gabor CR (2015) Behavioral and physiological antipredator responses of the San Marcos salamander, Eurycea nana. Phys Behav 139:145–149.  https://doi.org/10.1016/j.physbeh.2014.11.013 CrossRefGoogle Scholar
  11. Denoël M (2003) How do paedomorphic newts cope with lake drying? Ecography 26:405–410.  https://doi.org/10.1034/j.1600-0587.2003.03366.x CrossRefGoogle Scholar
  12. Denoël M (2017) On the identification of paedomorphic and overwintering larval newts based on cloacal shape: review and guidelines. Curr Zool 63:165–173.  https://doi.org/10.1093/cz/zow054 Google Scholar
  13. Denoël M, Ficetola GF (2014) Heterochrony in a complex world: disentangling environmental processes of facultative paedomorphosis in an amphibian. J Anim Ecol 83:606–615.  https://doi.org/10.1111/1365-2656.12173 CrossRefGoogle Scholar
  14. Denoël M, Ficetola GF (2015) Using kernels and ecological niche modeling to delineate conservation areas in an endangered patch-breeding phenotype. Ecol Appl 25:1922–1931.  https://doi.org/10.1890/14-1041.1 CrossRefGoogle Scholar
  15. Denoël M, Winandy L (2015) The importance of phenotype diversity in conservation: resilience of palmate newt morphotypes after fish removal in Larzac ponds (France). Biol Conserv 192:402–408.  https://doi.org/10.1016/j.biocon.2015.10.018 CrossRefGoogle Scholar
  16. Denoël M, Džukić G, Kalezić ML (2005a) Effect of widespread fish introductions on paedomorphic newts in Europe. Conserv Biol 19:162–170.  https://doi.org/10.1111/j.1523-1739.2005.00001.x CrossRefGoogle Scholar
  17. Denoël M, Whiteman HH, Joly P (2005b) Evolutionary ecology of facultative paedomorphosis in newts and salamanders. Biol Rev 80:663–671.  https://doi.org/10.1017/S1464793105006858 CrossRefGoogle Scholar
  18. Denoël M, Lena JP, Joly P (2007) Morph switching in a dimorphic population of Triturus alpestris (Amphibia, Caudata). Evol Ecol 21:325–335.  https://doi.org/10.1007/s10682-006-9103-2 CrossRefGoogle Scholar
  19. Denoël M, Ficetola GF, Ćirović R, Radović D, Džukić G, Kalezić ML, Vukov TD (2009) A multi-scale approach to facultative padomorphosis of European newts in the Montenegrin karst: distribution pattern, environmental variables and conservation. Biol Conserv 142:509–517.  https://doi.org/10.1016/j.biocon.2008.11.008 CrossRefGoogle Scholar
  20. Denoël M, Scime P, Zambelli N (2016) Newt life after fish introduction: extirpation of paedomorphosis in a mountain fish lake and newt use of satellite pools. Curr Zool 62:61–69.  https://doi.org/10.1093/cz/zov003 CrossRefGoogle Scholar
  21. Denoël M, Dalleur S, Langrand E, Besnard A, Cayuela H (2018) Dispersal and alternative pond fidelity strategies in an amphibian. Ecography 41:1543–1555.  https://doi.org/10.1111/ecog.03296 CrossRefGoogle Scholar
  22. Denoël M, Ficetola GF, Sillero N, Džukić G, Kalezić ML, Vukov TD, Muhovic I, Ikovic V, Lejeune B (2019) Traditionally managed landscapes do not prevent amphibian decline and the extinction of paedomorphosis. Ecol Monogr.  https://doi.org/10.1002/ecm.1347 Google Scholar
  23. Denver RJ, Glennemeier KS, Boorse GC (2002) Endocrinology of complex life cycles: Amphibians. In: Pfaff D, Arnold A, Etgen A, Fahrbach S, Rubin R (eds) Hormones, brain and behaviour. Academic Press, London, pp 469–513CrossRefGoogle Scholar
  24. Ficetola GF, Siesa ME, Manenti R, Bottoni L, De Bernardi F, Padoa-Schioppa E (2011) Early assessment of the impact of alien species: differential consequences of an invasive crayfish on adult and larval amphibians. Divers Distrib 17:1141–1151.  https://doi.org/10.1111/j.1472-4642.2011.00797.x CrossRefGoogle Scholar
  25. Figiel CR, Semlitsch RD (1990) Population variation in survival and metamorphosis of larval salamanders (Ambystoma maculatum) in the presence and absence of fish predation. Copeia 1990:818–826.  https://doi.org/10.2307/1446447 CrossRefGoogle Scholar
  26. Gabrion J (1976) La néoténie chez Triturus helveticus Raz. Etude morphofonctionnelle de la fonction thyroidienne. PhD thesis, Université des Sciences et Techniques du Languedoc, Montpellier, FranceGoogle Scholar
  27. Gould SJ (1977) Ontogeny and phylogeny. Harvard University Press, CambridgeGoogle Scholar
  28. Grayson KL, Wilbur HM (2009) Sex- and context-dependent migration in a pond-breeding amphibian. Ecology 90:306–312.  https://doi.org/10.1890/08-0935.1 CrossRefGoogle Scholar
  29. Hairston NG (1980) Species packing in the salamander genus Desmognathus: what are the interspecific interactions involved? Am Nat 115:354–366.  https://doi.org/10.1086/283566 CrossRefGoogle Scholar
  30. Huang C, Sih A (1990) Experimental studies on behaviorally mediated, indirect interactions through a shared predator. Ecology 71:1515–1522.  https://doi.org/10.2307/1938288 CrossRefGoogle Scholar
  31. Istock CA (1967) The evolution of complex life cycle phenomena: an ecological perspective. Evolution 21:592–605.  https://doi.org/10.1111/j.1558-5646.1967.tb03414.x CrossRefGoogle Scholar
  32. Jackson ME, Semlitsch RD (1993) Paedomorphosis in the salamander Ambystoma talpoideum: effects of a fish predator. Ecology 74:342–350.  https://doi.org/10.2307/1939297 CrossRefGoogle Scholar
  33. Kalezić ML, Džukić G (1985) Ecological aspects of the smooth newt (Triturus vulgaris) paedomorphosis from Montenegro. Ark Biol Nauka 37:43–50Google Scholar
  34. Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110.  https://doi.org/10.1046/j.1472-4642.2003.00013.x CrossRefGoogle Scholar
  35. Keinath MC, Voss SR, Tsonis PA, Smith JJ (2017) A linkage map for the newt Notophthalmus viridescens: insights in vertebrate genome and chromosome evolution. Dev Biol 426:211–218.  https://doi.org/10.1016/j.ydbio.2016.05.027 CrossRefGoogle Scholar
  36. Knapp RA, Matthews KR (2000) Non-native fish introductions and the decline of the mountain yellow-legged frog from within protected areas. Conserv Biol 14:428–438.  https://doi.org/10.1046/j.1523-1739.2000.99099.x CrossRefGoogle Scholar
  37. Knapp RA, Matthews KR, Sarnelle O (2001) Resistance and resilience of alpine lake fauna to fish introductions. Ecol Monogr 71:401–421.  https://doi.org/10.1890/0012-9615(2001)071%5b0401:RAROAL%5d2.0.CO;2 CrossRefGoogle Scholar
  38. Laudet V (2011) The origins and evolution of vertebrate metamorphosis. Curr Biol 21:R726–R737.  https://doi.org/10.1016/j.cub.2011.07.030 CrossRefGoogle Scholar
  39. Laurila A, Kujasalo J (1999) Habitat duration, predation risk and phenotypic plasticity in common frog (Rana temporaria) tadpoles. J Anim Ecol 68:1123–1132.  https://doi.org/10.1046/j.1365-2656.1999.00354.x CrossRefGoogle Scholar
  40. Lejeune B, Sturaro N, Lepoint G, Denoël M (2018) Facultative paedomorphosis as a mechanism promoting intraspecific niche differentiation. Oikos 127:427–439.  https://doi.org/10.1111/oik.04714 CrossRefGoogle Scholar
  41. Luiselli L, Filippi E, Capula M (2005) Geographic variation in diet composition of the grass snake (Natrix natrix) along the mainland and an island of Italy: the effects of habitat type and interference with potential competitors. Herpetol J 15:221–230Google Scholar
  42. Mathiron AGE, Lena J-P, Baouch S, Denoël M (2017) The ‘male escape hypothesis’: sex-biased metamorphosis in response to climatic drivers in a facultatively paedomorphic amphibian. Proc R Soc B 284:20170176.  https://doi.org/10.1098/rspb.2017.0176 CrossRefGoogle Scholar
  43. McKinney ML, McNamara KJ (1991) Heterochrony. The evolution of ontogeny. Plenum Press, New YorkGoogle Scholar
  44. McNamara JM (2012) Heterochrony: the evolution of development. Evol Educ Outreach 5:203–218CrossRefGoogle Scholar
  45. Monello RJ, Wright RG (2001) Predation by goldfish (Carassius auratus) on eggs and larvae of the eastern long-toed salamander (Ambystoma macrodactylum columbianum). J Herpetol 35:350–353CrossRefGoogle Scholar
  46. Orizaola G, Braña F (2003) Response of predator-naive newt larvae to food and predator presence. Can J Zool 81:1845–1850.  https://doi.org/10.1139/z03-160 CrossRefGoogle Scholar
  47. Orizaola G, Braña F (2005) Plasticity in newt metamorphosis: the effect of predation at embryonic and larval stages. Freshw Biol 50:438–446.  https://doi.org/10.1111/j.1365-2427.2005.01332.x CrossRefGoogle Scholar
  48. Orizaola G, Braña F (2006) Effect of salmonid introduction and other environmental characteristics on amphibian distribution and abundance in mountain lakes of northern Spain. Anim Cons 9:171–178.  https://doi.org/10.1111/j.1469-1795.2006.00023.x CrossRefGoogle Scholar
  49. Oromi N, Michaux J, Denoël M (2016) High gene flow between alternative morphs and the evolutionary persistence of facultative paedomorphosis. Sci Rep 6:32046.  https://doi.org/10.1038/srep32046 CrossRefGoogle Scholar
  50. Oromi N, Valbuena-Ureña E, Soler-Membrives A, Amat F, Camarasa S, Carranza S, Sanuy D, Denoël M (2019) Genetic structure of lake and stream populations in a Pyrenean amphibian (Calotriton asper) reveals evolutionary significant units associated with paedomorphosis. J Zool Res Evol Syst.  https://doi.org/10.1111/jzs.12250 Google Scholar
  51. Page RB, Boley MA, Kump DK, Voss SR (2013) Genomics of a metamorphic timing QTL: Met1 maps to a unique genomic position and regulates morph and species-specific patterns of brain transcription. Genome Biol Evol 5:1716–1730.  https://doi.org/10.1093/gbe/evt123 CrossRefGoogle Scholar
  52. Pinheiro P, Bates D (2000) Mixed-effect models in S and S-Plus. Springer, New YorkCrossRefGoogle Scholar
  53. Relyea RA (2007) Getting out alive: how predators affect the decision to metamorphose. Oecologia 152:389–400.  https://doi.org/10.1007/s00442-007-0675-5 CrossRefGoogle Scholar
  54. Roček Z (1995) Heterochrony: response of amphibia to cooling events. Geolines, Praha 3:55–58Google Scholar
  55. Semlitsch RD (1987) Paedomorphosis in Ambystoma talpoideum: effects of density, food, and pond drying. Ecology 68:994–1002.  https://doi.org/10.2307/1938370 CrossRefGoogle Scholar
  56. Semlitsch RD, Wilbur HM (1989) Artificial selection for paedomorphosis in the salamander Ambystoma talpoideum. Evolution 43:105–112.  https://doi.org/10.1111/j.1558-5646.1989.tb04210.x CrossRefGoogle Scholar
  57. Shaffer HB (1984) Evolution in a paedomorphic lineage. I. An electrophoretic analysis of the Mexican ambystomatid salamanders. Evolution 38:1194–1206.  https://doi.org/10.1111/j.1558-5646.1984.tb05643.x CrossRefGoogle Scholar
  58. Sih A, Crowley P, McPeek M, Petranka J, Strohmeier K (1985) Predation, competition, and prey communities: a review of field experiments. Annu Rev Ecol Syst 16:269–311.  https://doi.org/10.1146/annurev.es.16.110185.001413 CrossRefGoogle Scholar
  59. Sprules WG (1974) The adaptive significance of paedogenesis in North American species of Ambystoma (Amphibia: Caudata): an hypothesis. Can J Zool 52:393–400.  https://doi.org/10.1139/z74-047 CrossRefGoogle Scholar
  60. Stoks R, Cordoba-Aguilar A (2012) Evolutionary ecology of Odonata: a complex life cycle perspective. Annu Rev Entomol 57:249–265.  https://doi.org/10.1146/annurev-ento-120710-100557 CrossRefGoogle Scholar
  61. Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:357–374.  https://doi.org/10.1111/j.1461-0248.2005.00874.x CrossRefGoogle Scholar
  62. Teplitsky C, Plénet S, Joly P (2003) Tadpoles’ responses to risk of fish introduction. Oecologia 134:270–277.  https://doi.org/10.1007/s00442-002-1106-2 CrossRefGoogle Scholar
  63. Therneau TM (2017) Package ‘survival’. Version 2.41-2Google Scholar
  64. Van Buskirk J, Schmidt BR (2000) Predator-induced phenotypic plasticity in larval newts: trade-offs, selection, and variation in nature. Ecology 81:3009–3028.  https://doi.org/10.1890/0012-9658(2000)081%5b3009:PIPPIL%5d2.0.CO;2 CrossRefGoogle Scholar
  65. Voss SR, Shaffer HB (2000) Evolutionary genetics of metamorphic failure using wild-caught vs. laboratory axolotls (Ambystoma mexicanum). Mol Ecol 9:1401–1407.  https://doi.org/10.1046/j.1365-294X.2000.01025.x CrossRefGoogle Scholar
  66. Voss SR, Smith JJ (2005) Evolution of salamander life cycles: a major-effect quantitative trait locus contributes to discrete and continuous variation for metamorphosis timing. Genetics 170:275–281.  https://doi.org/10.1534/genetics.104.038273 CrossRefGoogle Scholar
  67. Wells KD (2007) The ecology and behavior of amphibians. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  68. Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341.  https://doi.org/10.1086/284565 CrossRefGoogle Scholar
  69. Whiteman HH (1994) Evolution of facultative paedomorphosis in salamanders. Q Rev Biol 69:205–221.  https://doi.org/10.1086/418540 CrossRefGoogle Scholar
  70. Whiteman HH (1997) Maintenance of polymorphism promoted by sex-specific fitness payoffs. Evolution 51:2039–2044.  https://doi.org/10.1111/j.1558-5646.1997.tb05127.x CrossRefGoogle Scholar
  71. Whiteman HH, Howard RD (1998) Conserving alternative amphibian phenotypes: is there anybody out there? In: Lannoo MJ (ed) The Status and conservation of midwestern amphibians. Iowa University Press, Iowa City, pp 317–324CrossRefGoogle Scholar
  72. Whiteman HH, Wissinger S, Denoël M, Mecklin C, Gerlanc N, Gutrich J (2012) Larval growth in polyphenic salamanders: making the best of a bad lot. Oecologia 168:109–118.  https://doi.org/10.1007/s00442-011-2076-z CrossRefGoogle Scholar
  73. Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Syst 11:67–93.  https://doi.org/10.1146/annurev.es.11.110180.000435 CrossRefGoogle Scholar
  74. Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182:1305–1314.  https://doi.org/10.1126/science.182.4119.1305 CrossRefGoogle Scholar
  75. Winandy L, Denoël M (2013a) Cues from introduced fish alter shelter use and feeding behaviour in adult alpine newts. Ethology 119:121–129.  https://doi.org/10.1111/eth.12043 CrossRefGoogle Scholar
  76. Winandy L, Denoël M (2013b) Introduced goldfish affect amphibians through inhibition of sexual behaviour in risky habitats: an experimental approach. PLoS One 8:e82736.  https://doi.org/10.1371/journal.pone.0082736 CrossRefGoogle Scholar
  77. Winandy L, Denoël M (2015) The aggressive personality of an introduced fish affects foraging behavior in a polymorphic newt. Behav Ecol 26:1528–1536.  https://doi.org/10.1093/beheco/arv101 CrossRefGoogle Scholar
  78. Winandy L, Colin M, Denoël M (2016) Temporal habitat shift of a polymorphic newt species under predation risk. Behav Ecol 27:1025–1032.  https://doi.org/10.1093/beheco/arw008 CrossRefGoogle Scholar
  79. Winandy L, Legrand P, Denoël M (2017) Habitat selection and reproduction of newts in networks of fish and fishless aquatic patches. Anim Behav 123:107–115.  https://doi.org/10.1016/j.anbehav.2016.10.027 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Behavioural Biology Group, Laboratory of Fish and Amphibian Ethology, Freshwater and OCeanic science Unit of reSearch (FOCUS)University of Liège (ULiège)LiègeBelgium
  2. 2.Laboratoire Evolution et Diversité Biologique, CNRS, UMR 5174Université Paul SabatierToulouseFrance
  3. 3.Station d’Ecologie Théorique et ExpérimentaleCNRS UMR 5321MoulisFrance

Personalised recommendations