Abstract
It has been proposed recently that labile state variables (e.g. energy reserves) can have a key role in the development and maintenance of consistent between-individual behavioural variation (i.e. animal personality) within population. In male Carpetan rock lizards (Iberolacerta cyreni), the provitamin D3 component of femoral gland secretion acts as an honest signal in sexual communication. Further, vitamin D3 has many important metabolic functions in reptiles. Therefore, by employing a factorial experiment with food (high vs. low) and vitamin D3 (supplemented vs. control) treatments in wild-caught reproductive male I. cyreni, we tested whether changing labile components of individual state affected (i) behavioural consistency (the degree of between-individual difference) and (ii) behavioural type (mean behaviour). Animal personality in activity was present in all treatments; however, personality was present only in the high food × vitamin D3 supplementation treatment in shelter use and it was present in all but the low food × placebo treatment in risk taking. Lizards (i) decreased activity in the high food treatment, (ii) increased shelter use in the vitamin D3 supplementation treatment and (iii) increased risk taking in the low food × vitamin D3 supplementation treatment. We conclude that short-term changes in individual state affect both behavioural consistency and behavioural type of reproductive male I. cyreni. Unfavourable conditions resulted in decreased behavioural consistency, while high-state individuals became less active in general. Individuals with high specific (vitamin D3) but low general (energy reserves) state took higher risk. We discuss several evolutionary explanations for the reported patterns.
Significance statement
The evolutionary and developmental mechanisms resulting in consistent between-individual behavioural differences across time and situations (i.e. animal personality) are of high scientific interest. It has been recently proposed that links between individual state (e.g. how well-fed the individual is) and behaviour can maintain such between-individual differences even on an evolutionarily timescale. However, whether short-term state changes are able to affect animal personality in adults is an open question. In a manipulative experiment, we found that the amount of food and vitamin D3 (known to increase physiological quality and attractiveness of male Carpetan rock lizards, I. cyreni) affected the expression of animal personality and the actual behavioural types of reproductive male Carpetan rock lizards. Therefore, we provide evidence that short-term environmental variation does induce or suppress animal personality, and it also affects individual behaviour.
Similar content being viewed by others
Reference
Allen ME, Bush M, Oftedal OT, Rosscoe R, Walsh T, Holick MF (1994) Update on vitamin D and ultraviolet light in basking lizards. Proc Am Assoc Zoo Vet 25:314–316
Aragón P, López P, Martín J (2001) Discrimination of femoral gland secretions from familiar and unfamiliar conspecifics by male Iberian rock-lizards, Lacerta monticola. J Herpetol 35:346–350
Bajer K, Horváth G, Molnár O, Török J, Garamszegi LZ, Herczeg G (2015) European green lizard (Lacerta viridis) personalities: linking behavioural types to ecologically relevant traits at different ontogenetic stages. Behav Process 111:67–74
Bajer K, Molnár O, Török J, Herczeg G (2012) Temperature, but not available energy, affects the expression of a sexually selected ultraviolet (UV) colour trait in male European green lizards. PLoS One 7:e34359
Bartoń K (2016) MuMIn: multi-model inference, R package version 1.15.6, https://CRAN.R-project.org/package=MuMIn
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Beckmann C, Biro PA (2013) On the validity of a single (boldness) assay in personality research. Ethology 119:937–9477
Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783
Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834
Biro PA (2012) Do rapid assays predict repeatability in labile (behavioural) traits? Anim Behav 83:1295–1300
Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368
Brommer JE, Karell P, Ahola K, Karstinen T (2014) Residual correlations, and not individual properties, determine a nest defense boldness syndrome. Behav Ecol 25:802–812
Candolin U (2000) Increased signalling effort when survival prospects decrease: male-male competition ensures honesty. Anim Behav 60:417–422
Careau V, Garland T (2012) Performance, personality, and energetics: correlation, causation, and mechanism. Physiol Biochem Zool 85:543–571
Carere C, Maestripieri D (2013) Animal personalities: who cares and why? In: Carere C, Masterpieri D (eds) Animal personalities. Behaviour, physiology and evolution. The University of Chicago Press, Chicago, pp 1–25
Clark CW (1994) Antipredator behavior and the asset-protection principle. Behav Ecol 5:159–170
Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123:212–229
Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739
David M, Auclair Y, Giraldeau LA, Cézilly F (2012) Personality and body condition have additive effects on motivation to feed in zebra finches Taeniopygia guttata. Ibis 154:372–378
Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond B 278:847–852
Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54
Dingemanse NJ, Dochtermann NA, Nakagawa S (2012) Defining behavioural syndromes and the role of “syndrome deviation” in understanding their evolution. Behav Ecol Sociobiol 66:1543–1548
Dingemanse NJ, Kazem AJN, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89
Dingemanse NJ, Wolf M (2010) Recent models for adaptive personality differences: a review. Philos T Roy Soc B 365:3947–3958
Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138
DiRienzo N, Montiglio PO (2016) The contribution of developmental experience vs. condition to life history, trait variation and individual differences. J Anim Ecol 85:915–926
Di Rienzo N, Niemelä PT, Hedrick AV, Kortet R (2016) Adult bacterial exposure increases behavioral variation and drives higher repeatability in field crickets. Behav Ecol Sociobiol. doi:10.1007/s00265-016-2200-5
DiRienzo N, Niemelä PT, Skog A, Vainikka A, Kortet R (2015) Juvenile pathogen exposure affects the presence of personality in adult field crickets. Front Ecol Evol 3:36
DiRienzo N, Pruitt JN, Hedrick AV (2012) Juvenile exposure to acoustic sexual signals from conspecifics alters growth trajectory and an adult personality trait. Anim Behav 84:861–868
Dochtermann NA, Dingemanse NJ (2013) Behavioral syndromes as evolutionary constraints. Behav Ecol 24:806–811
Dosmann AJ, Brooks KC, Mateo JM (2014) Within-individual correlations reveal link between a behavioral syndrome, condition, and cortisol in free-ranging Belding’s ground squirrels. Ethology 120:1–10
Engqvist L, Cordes N, Reinhold K (2015) Evolution of risk-taking during conspicuous mating displays. Evolution 69:395–406
Garamszegi LZ, Markó G, Herczeg G (2012a) 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
Garamszegi LZ, Rosivall B, Rettenbacher S, Markó G, Zsebők S, Szöllősi E, Eens M, Potti J, Török J (2012b) Corticosterone, avoidance of novelty, risk-taking and aggression in a wild bird: no evidence for pleiotropic effects. Ethology 118:621–635
Garamszegi LZ, Markó G, Szász E, Zsebők S, Azcárate M, Herczeg G, Török J (2015) Among-year variation in the repeatability, within- and between-individual, and phenotypic correlations of behaviors in a natural population. Behav Ecol Sociobiol 69:2005–2017
González-Tokman D, González-Santoyo I, Munguía-Steyer R, Córdoba-Aguilar A (2013) Effect of juvenile hormone on senescence in males with terminal investment. J Evol Biol 26:2458–2466
Griffin MD, Xing N, Kumar R (2003) Vitamin D and its analogs as regulators of immune activation and antigen presentation. Annu Rev Nutr 23:117–145
Hammond-Tooke C, Nakagawa S, Poulin R (2012) Parasitism and behavioural syndromes in the fish Gobiomorphus cotidianus. Behaviour 149:601–622
Harcourt JL, Ang TZ, Sweetman G, Johnstone RA, Manica A (2009) Social feedback and the emergence of leaders and followers. Curr Biol 19:248–252
Hayes CE, Nashold FE, Spach KM, Pedersen LB (2003) The immunological functions of the vitamin D endocrine system. Cell Mol Biol 49:277–300
Herczeg G, Gonda A, Saarikivi J, Merilä J (2006) Experimental support for the cost-benefit model of lizard thermoregulation. Behav Ecol Sociobiol 60:405–414
Herczeg G, Herrero A, Saarikivi J, Gonda A, Jäntti M, Merilä J (2008) Experimental support for the cost-benefit model of lizard thermoregulation: the effects of predation risk and food supply. Oecologia 155:1–10
Horváth G, Martín J, López P, Garamszegi LZ, Bertók P, Herczeg G (2016) Blood parasite infection intensity covaries with risk-taking personality in male Carpetan rock lizards (Iberolacerta cyreni). Ethology. doi:10.1111/eth.12475
Houston AI, McNamara JM (1999) Models of adaptive behaviour: an approach based on state. Cambridge University Press, Cambridge
Kekäläinen J, Lai Y T, Vainikka A, Sirkka I, Kortet R (2014) Do brain parasites alter host personality?—experimental study in minnows. Behav Ecol Sociobiol 68:197–204
Komers PE (1997) Behavioural plasticity in variable environments. Can J Zool 75:161–169
Koolhaas JM, Korte SM, de Boer SF, van der Vegt BJ, van Reenen CG, Hopster H, de Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress—physiology. Neurosci Biobehav Rev 23:925–935
Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effcts models, R package version 2.0–33, https://CRAN.R-project.org/package=lmerTest
Laing CJ, Fraser DR (1999) The vitamin D system in iguanian lizards. Comp Biochem Physiol B 123:373–379
Lee VE, Head ML, Carter MJ, Royle NJ (2014) Effects of age and experience on contest behavior in the burying beetle, Nicrophorus vespilloides. Behav Ecol 25:172–179
Lichtenstein JLL, DiRienzo N, Knutson K et al (2016) Prolonged food restriction decreases body condition and reduces repeatability in personality traits in web-building spiders. Behav Ecol Sociobiol. doi:10.1007/s00265-016-2184-1
López P, Amo L, Martín J (2006) Reliable signaling by chemical cues of male traits and health state in male lizards, Lacerta monticola. J Chem Ecol 32:473–488
López P, Aragón P, Martín J (2003) Responses of female lizards, Lacerta monticola, to males’ chemical cues reflect their mating preference for older males. Behav Ecol Sociobiol 55:73–79
López P, Martín J (2002) Chemical rival recognition decreases aggression levels in male Iberian wall lizards, Podarcis hispanica. Behav Ecol Sociobiol 51:461–465
López P, Martín J (2005) Chemical compounds from femoral gland secretions of male Iberian rock lizards, Lacerta monticola cyreni. Z Naturforsch C 60:632–636
López P, Martín J (2011) Male Iberian rock lizards may reduce the costs of fighting by scent matching of the resource holders. Behav Ecol Sociobiol 65:1891–1898
Luttbeg B, Sih A (2010) Risk, resources and state-dependent adaptive behavioural syndromes. Philos T Roy Soc B 365:3977–3990
Martín J, López P (2006a) Links between male quality, male chemical signals, and female mate choice in Iberian rock lizards. Funct Ecol 20:1087–1096
Martín J, López P (2006b) Vitamin D supplementation increases the attractiveness of males’ scent for female Iberian rock lizards. Proc R Soc Lond B 273:2619–2624
Martín J, López P (2008) Female sensory bias may allow honest chemical signaling by male Iberian rock lizards. Behav Ecol Sociobiol 62:1927–1934
Martín J, López P (2010) Pheromones and reproduction in reptiles. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates, Vol. 3—reptiles. Academic Press, San Diego, pp 141–167
Martín J, López P (2012) Supplementation of male pheromone on rock substrates attracts female rock lizards to the territories of males: a field experiment. PLoS One 7:e30108
Martín J, López P (2013) Responses of female rock lizards to multiple scent marks of males: effects of male age, male density and scent over-marking. Behav Process 94:109–114
Martín J, Salvador A (1992) Tail loss consequences on habitat use by the Iberian rock lizard, Lacerta monticola. Oikos 65:328–333
Martín J, Salvador A (1993) Tail loss and foraging tactics of Iberian rock-lizards, Lacerta monticola. Oikos 66:318–324
Mason RT, Parker MR (2010) Social behavior and pheromonal communication in reptiles. J Comp Physiol A 196:729–749
Massot M, Clobert J, Montes-Poloni L, Haussy C, Cubo J, Meylan S (2011) An integrative study of ageing in a wild population of common lizards. Funct Ecol 25:848–858
Mather JA, Logue DM (2013) The bold and the spineless: invertebrate personalities. In: Carere C, Maestripieri D (eds) Animal Personalities Behavior, Physiology, and Evolution, The University of Chicago Press, Chicago, pp 13–35
Mathot KJ, Dingemanse NJ (2015) Energetics and behavior: unrequited needs and new directions. Trends Ecol Evol 30:99–106
Mathot KJ, Nicolaus M, Araya-Ajoy YG, Dingemanse NJ, Kampenaers B (2014) Does metabolic rate predict risk-taking behaviour? A field experiment in a wild passerine bird. Funct Ecol 29:239–249
Mathot KJ, Wright J, Kempenaers B, Dingemanse NJ (2012) Adaptive strategies for managing uncertainty may explain personality-related differences in behavioural plasticity. Oikos 121:1009–1020
McElreath R, Luttbeg B, Fogarty SP, Brodin T, Sih A (2007) Evolution of animal personalities. Nature 450:E5 discussion E5–E6
McEvoy J, While GM, Sinn DL, Carver S, Wapstra E (2015) Behavioural syndromes and structural and temporal consistency of behavioural traits in a social lizard. J Zool 296:58–66
Mell H, Josserand R, Decencière B, Artacho P, Meylan S, Le Galliard JF (2016) Do personalities co-vary with metabolic expenditure and glucocorticoid stress response in adult lizards? Behav Ecol Sociobiol. doi:10.1007/s00265-016-2117-z
Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142
Nielsen ML, Holman L (2012) Terminal investment in multiple sexual signals: immune-challenged males produce more attractive pheromones. Funct Ecol 26:20–28
Øverli Ø, Sørensen C, Pulman KGT, Pottinger TG, Korzan W, Summers CH, Nilsson GE (2007) Evolutionary background for stress-coping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci Biobehav Rev 31:396–412
R Developmental Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org/
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318
Salvador A, Díaz JA, Veiga JP, Bloor P, Brown RP (2008) Correlates of reproductive success in male lizards of the alpine species Iberolacerta cyreni. Behav Ecol 19:169–176
Seaman B, Briffa M (2015) Parasites and personality in periwinkles (Littorina littorea): infection status is associated with mean-level boldness but not repeatability. Behav Process 115:132–134
Sih A, Bell A, Johnson JC (2004a) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378
Sih A, Bell AM, Johnson JC, Ziemba RE (2004b) Behavioural syndromes: an integrative overview. Q Rev Biol 79:241–277
Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289
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
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
Sinn DL, Moltschaniwskyj NA (2005) Personality traits in dumpling squid (Euprymna tasmanica): context-specific traits and their correlation with biological characteristics. J Comp Psychol 119:99–110
Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455
Stahlschmidt ZR, Holcomb LM, Luoma RL (2016) Context-dependent effects of complex environments on behavioral plasticity. Behav Ecol 27:237–244
Stapley J (2006) Individual variation in preferred body temperature covaries with social behaviours and colour in male lizards. J Therm Biol 31:362–369
Urszán TJ, Garamszegi LZ, Nagy G, Hettyey A, Török J, Herczeg G (2015a) No personality without experience? A test on Rana dalmatina tadpoles. Ecol Evol 5:5847–5856
Urszán TJ, Török J, Hettyey A, Garamszegi LZ, Herczeg G (2015b) Behavioural consistency and life history of Rana dalmatina tadpoles. Oecologia 178:129–140
van Oers K, de Jong G, van Noordwijk AJ, Kempenaers B, Drent PJ (2005) Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142:1185–1206
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York
Wilson DS (1998) Adaptive individual differences within single populations. Philos T Roy Soc B 353:199–205
Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584
Wolf M, Weissing FJ (2010) An explanatory framework for adaptive personality differences. Philos T Roy Soc B 365:3959–3968
Acknowledgements
We are highly grateful for two anonymous reviewers whose comments and advice helped us to improve our manuscript. Our sincere thank goes to Roberto García-Roa for his assistance in noosing lizards. We thank ‘El Ventorrillo’ Field Station of Museo Nacional de Ciencias Naturales for use of their facilities. Our work was funded by the Hungarian Scientific Research Fund (# OTKA-K 105517 for GH). LZG was supported by funds from The Ministry of Economy and Competitiveness (Spain) (CGL2015-70639-P) and The National Research, Development and Innovation Office (Hungary) (K-115970). PL and JM were supported by the Ministerio de Economía y Competitividad project MINECO CGL2014-53523-P. The research also received support from the SYNTHESYS Project http://www.synthesys.info/, which is financed by European Community Research Infrastructure Action under the FP7 “Capacitie” Program.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The experiment was performed under licence (permit number: 10/024398.9/13) from the Environmental Agency of Madrid Government (“Consejería de Medio Ambiente de la Comunidad de Madrid”, Spain).
Additional information
Communicated by S. J. Downes
Rights and permissions
About this article
Cite this article
Horváth, G., Martín, J., López, P. et al. Food and vitamin D3 availability affects lizard personalities: an experiment. Behav Ecol Sociobiol 71, 27 (2017). https://doi.org/10.1007/s00265-016-2257-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-016-2257-1