Skip to main content
Log in

Behavioural consistency and life history of Rana dalmatina tadpoles

  • Special Topic: Individual-level niche specialization
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The focus of evolutionary behavioural ecologists has recently turned towards understanding the causes and consequences of behavioural consistency, manifesting either as animal personality (consistency in a single behaviour) or behavioural syndrome (consistency across more behaviours). Behavioural type (mean individual behaviour) has been linked to life-history strategies, leading to the emergence of the integrated pace-of-life syndrome (POLS) theory. Using Rana dalmatina tadpoles as models, we tested if behavioural consistency and POLS could be detected during the early ontogenesis of this amphibian. We targeted two ontogenetic stages and measured activity, exploration and risk-taking in a common garden experiment, assessing both individual behavioural type and intra-individual behavioural variation. We observed that activity was consistent in all tadpoles, exploration only became consistent with advancing age and risk-taking only became consistent in tadpoles that had been tested, and thus disturbed, earlier. Only previously tested tadpoles showed trends indicative of behavioural syndromes. We found an activity—age at metamorphosis POLS in the previously untested tadpoles irrespective of age. Relative growth rate correlated positively with the intra-individual variation of activity of the previously untested older tadpoles. In previously tested older tadpoles, intra-individual variation of exploration correlated negatively and intra-individual variation of risk-taking correlated positively with relative growth rate. We provide evidence for behavioural consistency and POLS in predator- and conspecific-naive tadpoles. Intra-individual behavioural variation was also correlated to life history, suggesting its relevance for the POLS theory. The strong effect of moderate disturbance related to standard behavioural testing on later behaviour draws attention to the pitfalls embedded in repeated testing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adriaenssens B, Johnsson JI (2013) Natural selection, plasticity and the emergence of a behavioural syndrome in the wild. Ecol Lett 16:47–55

    Article  PubMed  Google Scholar 

  • Andersson MÅ, Höglund E (2012) Linking personality to larval energy reserves in rainbow trout (Oncorhynchus mykiss). PLoS One 7(11):e49247

    Article  PubMed Central  PubMed  Google Scholar 

  • American Public Health Association (APHA) (1985) Standard methods for the examination of water and wastewater, 16th edn. APHA, Washington DC

    Google Scholar 

  • Becker WA (1985) Manual of quantitative genetics. Academic Enterprises, Washington State University, Pullman

    Google Scholar 

  • Bell AM (2007) Future directions in behavioural syndromes research. Proc R Soc B 274:755–761

    Article  PubMed Central  PubMed  Google Scholar 

  • Bell AM, Sih A (2007) Exposure to predation generates personality in three-spined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834

    Article  PubMed  Google Scholar 

  • Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783

    Article  PubMed Central  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300

    Google Scholar 

  • Biro PA, Abrahams MV, Post JR, Parkinson EA (2006) Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates. J Anim Ecol 75:1165–1171

    Article  PubMed  Google Scholar 

  • Butler MW, Toomey MB, McGraw KJ, Rowe M (2012) Ontogenetic immune challenges shape adult personality in mallard ducks. Proc R Soc B 279:326–333

    Article  PubMed Central  PubMed  Google Scholar 

  • Careau V, Garland T Jr (2012) Performance, personality, and energetics: correlation, causation, and mechanism. Physiol Biochem Zool 85:543

    Article  PubMed  Google Scholar 

  • Careau V, Thomas D, Pelletier F, Turki L, Landry F, Garant D, Réale D (2011) Genetic correlation between resting metabolic rate and exploratory behaviour in deer mice (Peromyscus maniculatus). J Evol Biol 24:2153–2163

    Article  CAS  PubMed  Google Scholar 

  • Carter AJ, Feeney WE, Marshall HH, Cowlishaw G, Heinsohn R (2013) Animal personality: what are behavioural ecologists measuring? Biol Rev 88:465–475

    Article  PubMed  Google Scholar 

  • Cohen J (1988) Statistical power analysis for the behavioral sciences 2nd edn. Academic Press, San Diego Press

  • Coppens CM, de Boer SF, Koolhaas JM (2010) Coping styles and behavioural flexibility: towards underlying mechanisms. Philos Trans R Soc B Biol Sci 365:4021–4028

    Article  Google Scholar 

  • David M, Auclair Y, Giraldeau LA, Cezilly F (2012) Personality and body condition have additive effects on motivation to feed in Zebra Finches Taeniopygia guttata. Ibis 154:372–378

    Article  Google Scholar 

  • Dingemanse NJ, Kazem AJN, Reale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89

    Article  PubMed  Google Scholar 

  • Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54

    Article  PubMed  Google Scholar 

  • Dingemanse NJ, Van der Plas F, Wright J, Réale D, Schrama M, Roff DA, Van der Zee E, Barber I (2009) Individual experience and evolutionary history of predation affects expression of heritable variation in fish personality and morphology. Proc R Soc B 276:1285–1293

    Article  PubMed Central  PubMed  Google Scholar 

  • Dochtermann NA, Dingemanse NJ (2013) Behavioural syndromes as evolutionary constraints. Behav Ecol 24:806–811

    Article  Google Scholar 

  • Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971

    Article  Google Scholar 

  • Le Galliard JF, Paquet M, Cisel M, Montes-Poloni L (2013) Personality and the pace-of-life syndrome: variation and selection on exploration, metabolism and locomotor performances. Funct Ecol 27:136–144

    Article  Google Scholar 

  • Garamszegi LZ, Herczeg G (2012) Behavioural syndromes, syndrome deviation and the within-and between-individual components of phenotypic correlations: when reality does not meet statistics. Behav Ecol Sociobiol 66:1651–1658

    Article  Google Scholar 

  • Garamszegi LZ, Markó G, Herczeg G (2012) A meta-analysis of correlated behaviours with implications for behavioural syndromes: mean effect size, publication bias, phylogenetic effects and the role of mediator variables. Evol Ecol 26:1213–1235

    Article  Google Scholar 

  • Garamszegi LZ, Markó G, Herczeg G (2013) A meta-analysis of correlated behaviors with implications for behavioral syndromes: relationships between particular behavioral traits. Behav Ecol 24:1068–1080

    Article  Google Scholar 

  • García LV (2004) Escaping the Bonferroni iron claw in ecological studies. Oikos 105:657–663

    Article  Google Scholar 

  • Gienapp P, Teplitsky C, Alho JS, Mills JA, Merilä J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178

    Article  CAS  PubMed  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Groothuis TGG, Trillmich F (2011) Unfolding personalities: the importance of studying ontogeny. Dev Psychobiol 53:641–655

    Article  PubMed  Google Scholar 

  • Grafen A, Hails R (2002) Modern statistics for the life sciences. Oxford University Press, Oxford

    Google Scholar 

  • Hegyi G, Garamszegi LZ (2011) Using information theory as a substitute for stepwise regression in ecology and behavior. Behav Ecol Sociobiol 65:69–76

    Article  Google Scholar 

  • Herczeg G, Garamszegi LZ (2012) Individual deviation from behavioural correlations: a simple approach to study the evolution of behavioural syndromes. Behav Ecol Sociobiol 66:161–169

    Article  Google Scholar 

  • Herczeg G, Gonda A, Merilä J (2009) Predation mediated population divergence in complex behaviour of nine-spined stickleback (Pungitius pungitius). J Evol Biol 22(544):552

    Google Scholar 

  • Jandt JM, Bengston S, Pinter-Wollman N, Pruitt JN, Raine NE, Dornhaus A, Sih A (2014) Behavioural syndromes and social insects: personality at multiple levels. Biol Rev 89:48–67

    Article  PubMed  Google Scholar 

  • Kaplan RH (1998) Maternal effect, developmental plasticity, and life history evolution: an amphibian model. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, New York, pp 244–260

    Google Scholar 

  • Kortet R, Hedrick AV, Vainikka A (2010) Parasitism, predation and the evolution of animal personalities. Ecol Lett 13(12):1449–1458

    Article  PubMed  Google Scholar 

  • Kuparinen A, Merilä J (2007) Detecting and managing fisheries-induced evolution. Trends Ecol Evol 22:652–659

    Article  PubMed  Google Scholar 

  • Laugen AT, Laurila A, Merilä J (2002) Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits. Biol J Linn Soc 76:61–70

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Niemelä PT, Vainikka A, Forsman JT, Loukola OJ, Kortet R (2012b) How does variation in the environment and individual cognition explain the existence of consistent behavioral differences? Ecol Evol 3:457–464

    Article  PubMed Central  PubMed  Google Scholar 

  • Merilä J (2009) Genetic constraints on adaptation? Science 325:1212–1213

    Article  PubMed  Google Scholar 

  • Murtaugh PA (2009) Performance of several variable-selection methods applied to real ecological data. Ecol Lett 12:1061–1068

    Article  PubMed  Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    Article  PubMed  Google Scholar 

  • Réale D, Garant D, Humphries MM, Bergeron P, Careau V, Montiglio PO (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc B: Biol Sci 365:4051–4063

    Article  Google Scholar 

  • Riechert SE, Hedrick AV (1993) A test for correlations among fitness-linked behavioural traits in the spider Agelenopsis aperta (Araneae, Agelenidae). Anim Behav 46:669–675

    Article  Google Scholar 

  • Rigterink A, Houpt K, Cho M, Eze O, Xu R, Horii T, Hatada I (2014) Genetics of canine behavior: a review. World J Med Genet 4:46–57

    Article  Google Scholar 

  • Rodel HG, Monclus R (2011) Long-term consequences of early development on personality traits: a study in European rabbits. Behav Ecol 22:1123–1130

    Article  Google Scholar 

  • Ruiz-Gomez MDL, Kittilsen S, Höglund E, Huntingford FA, Sørensen C, Pottinger TG, Bakken M, Winberg S, Korzan WJ, Øverli Ø (2008) Behavioral plasticity in rainbow trout (Oncorhynchus mykiss) with divergent coping styles: when doves become hawks. Horm Behav 54:534–538

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sih A, Bell A, Johnson JC (2004) Behavioural syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378

    Article  PubMed  Google Scholar 

  • Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289

    Article  PubMed  Google Scholar 

  • Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455

    Article  Google Scholar 

  • Stamps JA (2007) Growth-mortality tradeoffs and ‘personality traits’ in animals. Ecol Lett 10:355–363

    Article  PubMed  Google Scholar 

  • Stamps JA, Groothuis TG (2010) Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Philos Trans R Soc B: Biol Sci 365:4029–4041

    Article  Google Scholar 

  • Stamps JA, Briffa M, Biro PA (2012) Unpredictable animals: individual differences in intraindividual variability (IIV). Anim Behav 83:1325–1334

    Article  Google Scholar 

  • Sweeney K, Gadd RD, Hess ZL, McDermott DR, MacDonald L, Cotter P, Armagost F, Chen JZ, Berning AW, DiRienzo N, Pruitt JN (2013) Assessing the effects of rearing environment, natural selection, and developmental stage on the emergence of a behavioral syndrome. Ethology 119:436–447

    Article  Google Scholar 

  • Teplitsky C, Mills JA, Alho JS, Yarrall JW, Merilä J (2008) Bergmann’s rule and climate change revisited: disentangling environmental and genetic responses in a wild bird population. Proc Natl Acad Sci USA 105:13492–13496

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Trillmich F, Hudson R (2011) The emergence of personality in animals: the need for a developmental approach. Dev Psychobiol 53:505–509

    Article  PubMed  Google Scholar 

  • van der Waaij EH, Wilsson E, Strandberg E (2008) Genetic analysis of results of a Swedish behaviour test on German shepherd dogs and labrador retrievers. J Anim Sci 86:2853–2861

    Article  PubMed  Google Scholar 

  • Verhoeven KJ, Simonsen KL, McIntyre LM (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647

    Article  Google Scholar 

  • Wilson AD, Krause MJ (2012) Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav Ecol 23:1316–1323

    Article  Google Scholar 

  • Wolf M, Weissing FJ (2010) An explanatory framework for adaptive personality differences. Philos Trans R Soc B Biol Sci 365:3959–3968

    Article  Google Scholar 

  • Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27(8):452–461

    Article  PubMed  Google Scholar 

  • Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are highly indebted to Tibor Kovács, Gergely Nagy and Orsolya Molnár for their help during the fieldwork and the laboratory experiment. Our research was funded by the Hungarian State PhD Scholarship to (TJU), the Hungarian Scientific Research Fund (K-105517) and the János Bolyai Research Scholarship of the Hungarian Academy of Sciences (to GH), the FP7 Marie Curie Career Integration Grant (PCIG13-GA-2013-631722) and the “Lendület” programme of the Hungarian Academy of Sciences (MTA, LP2012-24/2012; to AH), and the Spanish government within the framework of the ‘‘Plan Nacional” program (ref. no. CGL2012- 38262 and CGL2012-40026-C02-01; to LZG). Our experiment was done under the permit of Middle-Danube Valley Inspectorate for Environmental Protection, Nature Conservation and Water Management (ref. no. 8464-2/2011) and followed the guidelines of the Hungarian Act of Animal Care and Experimentation (1998, XXVIII, Sect. 243/1998), which conforms to the regulation of animal experiments by the European Union.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tamás János Urszán.

Additional information

Communicated by Craig A. Layman.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 109 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Urszán, T.J., Török, J., Hettyey, A. et al. Behavioural consistency and life history of Rana dalmatina tadpoles. Oecologia 178, 129–140 (2015). https://doi.org/10.1007/s00442-014-3207-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-3207-0

Keywords

Navigation