Behavioral syndrome persists over metamorphosis in a pond-breeding amphibian

  • Adam M. Koenig
  • Brittany H. OusterhoutEmail author
Original Article


In recent years, behavioral ecology has shifted from assuming animal behavior is infinitely plastic and situation specific to recognizing that behavior can be limited in its plasticity and correlated across different ecological situations. At the center of this new framework are behavioral syndromes or consistent individual differences in behavioral tendencies. Over the past decade, numerous studies have identified the evolutionary mechanisms and ecological implications of behavioral syndromes. However, the persistence of behavioral syndromes over ontogeny remains an open question. Species with complex life cycles present an interesting system in which to test the persistence of behavioral syndromes, because such life histories are thought to evolve when correlations between life stages are costly. In this study, we tested the hypothesis that behavioral tendencies of species with complex life histories are consistent within a life stage (before or after metamorphosis) but not between life stages. We experimentally assayed the activity, boldness, and exploration of spotted salamanders (Ambystoma maculatum) before and after metamorphosis. We found most behaviors to be at least moderately repeatable. Additionally, there was support for a behavioral syndrome within the larval stage as well as between larval behaviors and juvenile boldness. Our results reject the adaptive decoupling hypothesis and instead suggest that behavioral syndromes in species with complex life cycles can be maintained over metamorphosis.

Significance statement

A central prediction of behavioral syndromes is that individual behavioral consistency should be maintained over the life of an organism. However, in species with complex life cycles, evolution is thought to act independently on each stage, leading to the prediction that behavioral syndromes should not persist over metamorphosis. We tested for behavioral correlations over metamorphosis by assaying salamander activity, boldness, and exploration in larval and juvenile salamanders. We found support for behavioral syndromes within and between life stages. These findings contradict the predictions of complex life cycle evolution and instead suggest that behavioral syndromes may span metamorphosis. However, because support for the persistence of syndromes over metamorphosis varies between taxa, we caution researchers against extrapolating inferences from the larval stage to the juvenile stage.


Ambystoma maculatum Boldness Complex life history Personality Temperament 



We thank L. Weiskopf, D. Westfall, C. Kimball, and E. Wedekind for monitoring pond mesocosms and J. Burkhart for assisting with animal care. This manuscript was greatly improved by comments from the Semlitsch lab, Rex Cocroft, and two anonymous reviewers.


This work was funded by the US Department of Defense SERDP (RC-2155 and RC-2703), National Science Foundation (DEB-0943941 to BHO and DEB-1620046). AMK was supported by the University of Missouri Undergraduate Mentoring in Research Program, and BHO was supported by a University of Missouri Life Sciences Fellowship and Trans World Airline Scholarship.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the University of Missouri Animal Care and Use Committee (8402) and collected under Missouri Department of Conservation permit no. 16463.

Supplementary material

265_2018_2595_MOESM1_ESM.docx (196 kb)
Fig. S1 (DOCX 195 kb)


  1. Aguirre JD, Blows MW, Marshall DJ (2014) The genetic covariance between life cycle stages separated by metamorphosis. Proc R Soc B 281:20141091CrossRefGoogle Scholar
  2. Alcalay Y, Ovadia O, Scharf I (2014) Behavioral repeatability and personality in pit-building antlion larvae under differing environmental contexts. Behav Ecol Sociobiol 68:1985–1993. CrossRefGoogle Scholar
  3. Altwegg R, Reyer H-U (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882CrossRefGoogle Scholar
  4. Anderson BB, Scott A, Dukas R (2015) Social behavior and activity are decoupled in larval and adult fruit flies. Behav Ecol 27:820–828. CrossRefGoogle Scholar
  5. Austin CC, Shaffer HB (2010) Short-, medium-, and long-term repeatability of locomotor performance in the tiger salamander Ambystoma californiense. Funt Ecol 6:145–153CrossRefGoogle Scholar
  6. Baguette M, Van Dyck H (2007) Landscape connectivity and animal behavior: functional grain as a key determinant for dispersal. Landsc Ecol 22:1117–1129. CrossRefGoogle Scholar
  7. Barbasch T, Benard MF (2011) Past and present risk: exposure to predator chemical cues before and after metamorphosis influences juvenile wood frog behavior. Ethology 117:367–373. CrossRefGoogle Scholar
  8. Beckmann C, Biro PA (2013) On the validity of a single (boldness) assay in personality research. Ethology 119:937–947. CrossRefGoogle Scholar
  9. Bell AM (2013) Randomized or fixed order for studies of behavioral syndromes? Behav Ecol 24:16–20. CrossRefPubMedGoogle Scholar
  10. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834. CrossRefPubMedGoogle Scholar
  11. Bell AM, Stamps JA (2004) Development of behavioural differences between individuals and populations of sticklebacks, Gasterosteus aculeatus. Anim Behav 68:1339–1348. CrossRefGoogle Scholar
  12. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Blouin MS (1992) Genetic correlations among metamorphic traits and rates of growth and differentiation in the green tree frog, Hyla cinerea. Evolution 46:735–744CrossRefGoogle Scholar
  14. Brodin T (2009) Behavioral syndrome over the boundaries of life—carryovers from larvae to adult damselfly. Behav Ecol 20:30–37. CrossRefGoogle Scholar
  15. Brodin T, Drotz MK (2011) Larval behavioral syndrome does not affect emergence behavior in a damselfly (Lestes congener). J Ethol 29:107–113. CrossRefGoogle Scholar
  16. Brodin T, Lind MI, Wiberg MK, Johansson F (2013) Personality trait differences between mainland and island populations in the common frog (Rana temporaria). Behav Ecol Sociobiol 67:135–143. CrossRefGoogle Scholar
  17. Brodman R, Jaskula J (2002) Activity and microhabitat use during interactions among five species of pond-breeding salamander larvae. Herpetologica 58:346–354CrossRefGoogle Scholar
  18. Buchanan BW (1993) Effects of enhanced lighting on the behavior of nocturnal frogs. Anim Behav 45:893–899CrossRefGoogle Scholar
  19. Careau V, Biro PA, Bonneaud C, Fokam EB, Herrel A (2014) Individual variation in thermal performance curves: swimming burst speed and jumping endurance in wild-caught tropical clawed frogs. Oecologia 175:471–480. CrossRefPubMedGoogle Scholar
  20. Carere C, Gherardi F (2013) Animal personalities matter for biological invasions. Trends Ecol Evol 28:5–6. CrossRefPubMedGoogle Scholar
  21. Carlson BE, Langkilde T (2013) Personality traits are expressed in bullfrog tadpoles during open-field trials. J Herpetol 47:378–383. CrossRefGoogle Scholar
  22. Conrad JL, Weinersmith KL, Brodin T, Saltz JB, Sih A (2011) Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. J Fish Biol 78:395–435. CrossRefPubMedGoogle Scholar
  23. Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Google Scholar
  24. Cote J, Fogarty S, Weinersmith K, Brodin T, Sih A (2010) Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc R Soc Lond B 277:1571–1579. CrossRefGoogle Scholar
  25. Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739. CrossRefGoogle Scholar
  26. Dall SRX, Bell AM, Bolnick DI, Ratnieks FLW (2012) An evolutionary ecology of individual differences. Ecol Lett 15:1189–1198. CrossRefPubMedPubMedCentralGoogle Scholar
  27. DeSantis DL, Davis DR, Gabor CR (2013) Chemically mediated predator avoidance in the Barton Springs salamander (Eurycea sosorum). Herpetologica 69:291–297. CrossRefGoogle Scholar
  28. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54. CrossRefPubMedGoogle Scholar
  29. Dingemanse NJ, Réale D (2005) Natural selection and animal personality. Behaviour 142:1159–1184. CrossRefGoogle Scholar
  30. Ducatez S, Legrand D, Chaput-Bardy A, Stevens VM, Fréville H, Baguette M (2012) Inter-individual variation in movement: is there a mobility syndrome in the large white butterfly Pieris brassicae? Ecol Entomol 37:377–385. CrossRefGoogle Scholar
  31. Duckworth RA (2006) Aggressive behaviour affects selection on morphology by influencing settlement patterns in a passerine bird. Proc R Soc Lond B 273:1789–1795. CrossRefGoogle Scholar
  32. Ebenman B (1992) Evolution in organisms that change their niches during the life cycle. Am Nat 139:990–1021CrossRefGoogle Scholar
  33. Edelsparre AH, Vesterberg A, Lim JH, Anwari M, Fitzpatrick MJ (2014) Alleles underlying larval foraging behaviour influence adult dispersal in nature. Ecol Lett 17:333–339. CrossRefPubMedGoogle Scholar
  34. Favati A, Zidar J, Thorpe H, Jensen P, Løvlie H (2016) The ontogeny of personality traits in the red junglefowl, Gallus gallus. Behav Ecol 27:484–493. CrossRefGoogle Scholar
  35. Fournier D, Skaug H, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielsen A, Sibert J (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249CrossRefGoogle Scholar
  36. Fox J, Weisberg S (2011) An R companion to applied regression. Sage, Thousand Oaks, CAGoogle Scholar
  37. Gifford ME, Clay TA, Careau V (2014) Individual (co)variation in standard metabolic rate, feeding rate, and exploratory behavior in wild-caught semiaquatic salamanders. Physiol Biochem Zool 87:384–396. CrossRefPubMedGoogle Scholar
  38. González-Bernal E, Brown GP, Shine R (2014) Invasive cane toads: social facilitation depends upon an individual’s personality. PLoS One 9:e102880. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Grim T, Samaš P, Hauber ME (2014) The repeatability of avian egg ejection behaviors across different temporal scales, breeding stages, female ages and experiences. Behav Ecol Sociobiol 68:749–759. CrossRefGoogle Scholar
  40. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22CrossRefGoogle Scholar
  41. Hedrick AV, Kortet R (2012) Sex differences in the repeatability of boldness over metamorphosis. Behav Ecol Sociobiol 66:407–412. CrossRefGoogle Scholar
  42. Hickman CR, Stone MD, Mathis A (2004) Priority use of chemical over visual cues for detection of predators by graybelly salamanders, Eurycea multiplicata griseogaster. Herpetologica 60:203–210CrossRefGoogle Scholar
  43. Hocking DJ, Rittenhouse TAG, Rothermel BB, Johnson JR, Conner CA, Harper EB, Semlitsch RD (2008) Breeding and recruitment phenology of amphibians in Missouri oak-hickory forests. Am Midl Nat 160:41–60. CrossRefGoogle Scholar
  44. Johansson F, Lederer B, Lind MI (2010) Trait performance correlations across life stages under environmental stress conditions in the common frog, Rana temporaria. PLoS One 5:e11680. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Johnson JC, Sih A (2005) Precopulatory sexual cannibalism in fishing spiders (Dolomedes triton): a role for behavioral syndromes. Behav Ecol Sociobiol 58:390–396. CrossRefGoogle Scholar
  46. Kats LB, Petranka JW, Sih A (1988) Antipredator defenses and the persistence of amphibian larvae with fishes. Ecology 69:1865–1870CrossRefGoogle Scholar
  47. Koprivnikar J, Gibson CH, Redfern JC (2012) Infectious personalities: behavioural syndromes and disease risk in larval amphibians. Proc R Soc Lond B 279:1544–1550. CrossRefGoogle Scholar
  48. Moran NA (1994) Adaptation and constraint in the complex life cycles of animals. Annu Rev Ecol Syst 25:573–600CrossRefGoogle Scholar
  49. Müller T, Müller C (2015) Behavioural phenotypes over the lifetime of a holometabolous insect. Front Zool 12:S8. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956. CrossRefPubMedGoogle Scholar
  51. Nannini MA, Parkos J, Wahl DH (2012) Do behavioral syndromes affect foraging strategy and risk-taking in a juvenile fish predator? Trans Am Fish Soc 141:26–33. CrossRefGoogle Scholar
  52. Niemelä PT, Vainikka A, Hedrick AV, Kortet R (2012a) Integrating behaviour with life history: boldness of the field cricket, Gryllus integer, during ontogeny. Funct Ecol 26:450–456. CrossRefGoogle Scholar
  53. Niemelä PT, DiRienzo N, Hedrick AV (2012b) Predator-induced changes in the boldness of naïve field crickets, Gryllus integer, depends on behavioural type. Anim Behav 84:129–135. CrossRefGoogle Scholar
  54. Ousterhout BH, Anderson TL, Drake DL, Peterman WE, Semlitsch RD (2015) Habitat traits and species interactions differentially affect abundance and body size in pond-breeding amphibians. J Anim Ecol 84:914–924. CrossRefPubMedGoogle Scholar
  55. Peterman WE, Anderson TL, Drake DL, Ousterhout BH, Semlitsch RD (2014) Maximizing pond biodiversity across the landscape: a case study of larval ambystomatid salamanders. Anim Conserv 2014:275–285. CrossRefGoogle Scholar
  56. Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, DCGoogle Scholar
  57. Phillips PC (1998) Genetic constraints at the metamorphic boundary: morphological development in the wood frog, Rana sylvatica. J Evol Biol 11:453–463. CrossRefGoogle Scholar
  58. Phillips BL, Brown GP, Shine R (2010) Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads. J Evol Biol 23:2595–2601. CrossRefPubMedGoogle Scholar
  59. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318. CrossRefPubMedGoogle Scholar
  60. Rodrigues AS, Botina L, Nascimento CP, Gontijo LM, Torres JB, Guedes RNC (2016) Ontogenic behavioral consistency, individual variation and fitness consequences among lady beetles. Behav Process 131:32–39. CrossRefGoogle Scholar
  61. Schielzeth H, Stoffel M, Nakagawa S (2016) rptR: repeatability estimation for gaussian and non-gaussian data.
  62. Scott DE (1994) The effect of larval density on adult demographic traits in Ambystoma opacum. Ecology 75:1383–1396CrossRefGoogle Scholar
  63. Shaffer HB, Austin CC, Huey RB (1991) The consequences of metamorphosis on salamander (Ambystoma) locomotor performance. Physiol Zool 64:212–231CrossRefGoogle Scholar
  64. Sih A, Kats LB, Maurer EF (2003) Behavioural correlations across situations and the evolution of antipredator behaviour in a sunfish–salamander system. Anim Behav 65:29–44. CrossRefGoogle Scholar
  65. Sih A, Bell AM, Johnson JC (2004a) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378. CrossRefPubMedGoogle Scholar
  66. Sih A, Bell AM, Johnson JC, Ziemba RE (2004b) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277. CrossRefPubMedGoogle Scholar
  67. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289. CrossRefPubMedGoogle Scholar
  68. Sih A, Mathot KJ, Moirón M, Montiglio PO, Wolf M, Dingemanse NJ (2015) Animal personality and state-behaviour feedbacks: a review and guide for empiricists. Trends Ecol Evol 30:50–60. CrossRefPubMedGoogle Scholar
  69. Stamps JA (2007) Growth-mortality tradeoffs and “personality traits” in animals. Ecol Lett 10:355–363. CrossRefPubMedGoogle Scholar
  70. Stamps JA (2016) Individual differences in behavioural plasticities. Biol Rev 91:534–567. CrossRefPubMedGoogle Scholar
  71. Stamps JA, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325. CrossRefPubMedGoogle Scholar
  72. Urban MC (2007a) The growth-predation risk trade-off under a growing gape-limited predation threat. Ecology 88:2587–2597CrossRefGoogle Scholar
  73. Urban MC (2007b) Risky prey behavior evolves in risky habitats. P Natl Acad Sci USA 104:14377–14382. CrossRefGoogle Scholar
  74. Urszán TJ, Török J, Hettyey A, Garamszegi LZ, Herczeg G (2015) Behavioural consistency and life history of Rana dalmatina tadpoles. Oecologia 178:129–140. CrossRefPubMedGoogle Scholar
  75. van Overveld T, Adriaensen F, Matthysen E (2014) No evidence for correlational selection on exploratory behaviour and natal dispersal in the great tit. Evol Ecol 29:137–156. CrossRefGoogle Scholar
  76. Verbeek MEM, Drent PJ, Wiepkema PR (1994) Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 48:1113–1121. CrossRefGoogle Scholar
  77. Videlier M, Bonneaud C, Cornette R, Herrel A (2014) Exploration syndromes in the frog Xenopus (Silurana) tropicalis: correlations with morphology and performance? J Zool 294:206–213. CrossRefGoogle Scholar
  78. Watkins TB (1997) The effect of metamorphosis on the repeatability of maximal locomotor performance in the Pacific tree frog Hyla regilla. J Exp Biol 200:2663–2668PubMedGoogle Scholar
  79. Watkins TB (2001) A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the Pacific tree frog, Hyla regilla. Evolution 55:1668–1677CrossRefGoogle Scholar
  80. Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  81. Werner EE (1986) Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am Nat 128:319–341CrossRefGoogle Scholar
  82. Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425. CrossRefGoogle Scholar
  83. Wexler Y, Subach A, Pruitt JN, Scharf I (2016) Behavioral repeatability of flour beetles before and after metamorphosis and throughout aging. Behav Ecol Sociobiol 70:745–753. CrossRefGoogle Scholar
  84. Wilbur HM (1980) Complex life cycles. Annu Rev Ecol Evol S 11:67–93CrossRefGoogle Scholar
  85. Wilson ADM, Krause J (2012a) Metamorphosis and animal personality: a neglected opportunity. Trends Ecol Evol 27:529–531. CrossRefPubMedGoogle Scholar
  86. Wilson ADM, Krause J (2012b) Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav Ecol 23:1316–1323. CrossRefGoogle Scholar
  87. Wirth O, Slaven J, Taylor MA (2014) Interval sampling methods and measurement error: a computer simulation. J Appl Behav Anal 47:83–100. CrossRefPubMedGoogle Scholar
  88. Wolak ME, Fairbairn DJ, Paulsen YR (2012) Guidelines for estimating repeatability. Methods Ecol Evol 3:129–137. CrossRefGoogle Scholar
  89. Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461. CrossRefPubMedGoogle Scholar
  90. Wuerz Y, Krüger O (2015) Personality over ontogeny in zebra finches: long-term repeatable traits but unstable behavioural syndromes. Front Zool 12:S9. CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Division of Biological SciencesUniversity of MissouriColumbiaUSA
  2. 2.National Great Rivers Research and Education CenterEast AltonUSA

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