Abstract
Variable environments can select for behavioral plasticity. Yet, along environmental gradients, personalities (consistent differences in behavior) and behavioral syndromes (associations between behavioral traits) can arise both across and within populations, which point to limits in behavioral plasticity. To date, little is known on how behavioral plasticity and animal personalities are associated along geographical gradients. Hereto, we subjected colonies of the ant Temnothorax longispinosus from populations along a natural climatic gradient to temperature manipulations and behavioral experiments. We asked whether personalities and behavioral syndromes stem from local adaptations or are plastic responses and whether the extent of behavioral plasticity differs between populations from warmer versus colder habitats. Our results reveal that colonies responded to warmer temperatures with increased explorative and brood care behavior. Interestingly, these behavioral traits shifted in the same direction as a syndrome previously found along this climatic gradient, where colonies from warmer environments displayed more exploration and brood care. Additionally, colonies that exhibited lower aggression but more exploration prior to temperature manipulations showed the highest behavioral plasticity. Moreover, only in one behavioral trait, exploration, colonies from colder sites exhibited higher plasticity than those from warmer sites. This suggests that ant behaviors are influenced mostly by prevailing conditions with a limited influence of past experience on behavioral plasticity. Our study proposes that associations between behavioral traits can be modified by climatic conditions, thus providing insights into the complex ways animals respond to current and past environments.
Significance statement
Behavioral plasticity and animal personalities could be linked to climate. Yet few studies have investigated behavioral associations along geographical gradients. Hence, we still lack an understanding of how current and past environmental conditions affect such behavioral associations along gradients. Here, we asked whether the extent of behavioral plasticity differs between populations from warmer versus colder sites along a climatic gradient and whether animal personalities stem from local adaptations or plastic responses. We demonstrate in a social insect that associations between behavioral traits can be modified by temperature. Specifically, in response to temperature changes, behavioral traits shifted in a direction consistent with variation in a syndrome across a climatic gradient. This study provides unique empirical support linking animal personalities and phenotypic plasticity across populations along climatic gradients, thus offering new insights into the complex ways animals respond to current conditions and past experience.
Similar content being viewed by others
References
Alcalay Y, Scharf I, Ovadia O (2015) Foraging syndromes and trait variation in antlions along a climatic gradient. Oecologia 178:1093–1103
Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford Univ Press, New York
Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc R Soc B Biol Sci 277:503–511
Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834
Bengston SE, Dornhaus A (2014) Be meek or be bold? A colony-level behavioural syndrome in ants. Proc R Soc B Biol Sci 281:20140518
Bengston SE, Jandt JM (2014) The development of collective personality: the ontogenetic drivers of behavioral variation across groups. Front Ecol Evol 2
Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659
Biro PA, Beckmann C, Stamps JA (2010) Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proc R Soc B Biol Sci 277:71–77
Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28
Bonte D, Bossuyt B, Lens L (2007) Aerial dispersal plasticity under different wind velocities in a salt marsh wolf spider. Behav Ecol 18:438–443
Briffa M, Rundle SD, Fryer A (2008) Comparing the strength of behavioural plasticity and consistency across situations: animal personalities in the hermit crab Pagurus bernhardus. Proc R Soc B Biol Sci 275:1305–1311
Briffa M, Bridger D, Biro PA (2013) How does temperature affect behaviour? Multilevel analysis of plasticity, personality and predictability in hermit crabs. Anim Behav 86:47–54
Brodie ED, Russell NH (1999) The consistency of individual differences in behaviour: temperature effects on antipredator behaviour in garter snakes. Anim Behav 57:445–451
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789
Careau V, Thomas D, Humphries MM, Reale D (2008) Energy metabolism and animal personality. Oikos 117:641–653
Chiba S, Arnott SA, Conover DO (2007) Coevolution of foraging behavior with intrinsic growth rate: risk-taking in naturally and artificially selected growth genotypes of Menidia menidia. Oecologia 154:237–246
Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905
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
Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739
DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81
Dingemanse NJ, Wolf M (2013) Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav 85:1031–1039
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
Dingemanse NJ, Kazem AJN, Reale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89
Dingemanse NJ, Bouwman KM, van de Pol M, van Overveld T, Patrick SC, Matthysen E, Quinn JL (2012) Variation in personality and behavioural plasticity across four populations of the great tit Parus major. J Anim Ecol 81:116–126
Foitzik S, Heinze J (1998) Nest site limitation and colony takeover in the ant Leptothorax nylanderi. Behav Ecol 9:367–375
Foster SA, Endler JA (1999) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press
Garamszegi LZ, Moller AP (2017) Partitioning within-species variance in behaviour to within- and between-population components for understanding evolution. Ecol Lett 20:599–608
Garamszegi LZ, Marko G, Szasz E, Zsebok S, Azcarate M, Herczeg G, Torok 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
Goulet CT, Thompson MB, Michelangeli M, Wong BBM, Chapple DG (2017) Thermal physiology: a new dimension of the pace-of-life syndrome. J Anim Ecol 86:1269–1280
Herbers JM (1986) Nest site limitation and facultative polygyny in the ant Leptothorax longispinosus. Behav Ecol Sociobiol 19:115–122
Hölldobler B, Wilson EO (1990) The ants. The Belknap Press of Harvard University Press, Cambridge
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 (Camb) 89:48–67
Jongepier E, Foitzik S (2016) Fitness costs of worker specialization for ant societies. Proc R Soc B Biol Sci 283:7
Kaspari M, Alonso L, O'Donnell S (2000) Three energy variables predict ant abundance at a geographical scale. Proc R Soc B Biol Sci 267:485–489
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
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
Maupin JL, Riechert SE (2001) Superfluous killing in spiders: a consequence of adaptation to food-limited environments. Behav Ecol 12:569–576
Mery F, Burns JG (2010) Behavioural plasticity: an interaction between evolution and experience. Evol Ecol 24:571–583
Mitchell DJ, Biro PA (2017) Is behavioural plasticity consistent across different environmental gradients and through time? Proc R Soc B Biol Sci 284:20170893
Modlmeier AP, Liebmann JE, Foitzik S (2012) Diverse societies are more productive: a lesson from ants. Proc R Soc B Biol Sci 279:2142–2150
Modlmeier AP, Keiser CN, Shearer TA, Pruitt JN (2014) Species-specific influence of group composition on collective behaviors in ants. Behav Ecol Sociobiol 68:1929–1937
Nicolaus M, Tinbergen JM, Ubels R, Both C, Dingemanse NJ (2016) Density fluctuations represent a key process maintaining personality variation in a wild passerine bird. Ecol Lett 19:478–486
Pinter-Wollman N, Gordon DM, Holmes S (2012) Nest site and weather affect the personality of harvester ant colonies. Behav Ecol 23:1022–1029
Pruitt JN, Goodnight CJ (2014) Site-specific group selection drives locally adapted group compositions. Nature 514:359–35+
Pruitt JN, Riechert SE, Iturralde G, Vega M, Fitzpatrick BM, Aviles L (2010) Population differences in behaviour are explained by shared within-population trait correlations. J Evol Biol 23:748–756
Pruitt JN, Demes KW, Dittrich-Reed DR (2011) Temperature mediates shifts in individual aggressiveness, activity level, and social behavior in a spider. Ethology 117:318–325
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
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
Segev U, Burkert L, Feldmeyer B, Foitzik S (2017) Pace-of-life in a social insect: behavioral syndromes in ants shift along a climatic gradient. Behav Ecol 28:1149–1159
Sih A, Bell A, Johnson JC (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378
Snell-Rood EC (2013) An overview of the evolutionary causes and consequences of behavioural plasticity. Anim Behav 85:1004–1011
Spiegel O, Leu ST, Bull CM, Sih A (2017) What’s your move? Movement as a link between personality and spatial dynamics in animal populations. Ecol Lett 20:3–18
Stamps JA (2016) Individual differences in behavioural plasticities. Biol Rev (Camb) 91:534–567
Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev (Camb) 85:301–325
Stearns SC (1992) The evolution of life histories. Oxford University Press, New York
Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116
Verbeek MEM, Drent PJ, Wiepkema PR (1994) Consistent individual differences in early exploratory behaviour of male great tits. Anim Behav 48:1113–1121
Wiersma P, Munoz-Garcia A, Walker A, Williams JB (2007) Tropical birds have a slow pace of life. Proc Natl Acad Sci U S A 104:9340–9345
Wilson DS (1998) Adaptive individual differences within single populations. Philos Trans R Soc B Biol Sci 353:199–205
Wolf M, Weissing FJ (2012) Animal personalities: consequences for ecology and evolution. Trends Ecol Evol 27:452–461
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, van Doorn GS, Weissing FJ (2008) Evolutionary emergence of responsive and unresponsive personalities. Proc Natl Acad Sci U S A 105:15825–15830
Wright CM, Lichtenstein JL, Doering GN, Pretorius J, Meunier J, Pruitt JN (2019) Collective personalities: present knowledge and new frontiers. Behav Ecol Sociobiol 73:31
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Inc., New Jersey
Zhao DP, Feng PS (2015) Temperature increase impacts personality traits in aquatic non-native species: implications for biological invasion under climate change. Curr Zool 61:966–971
Acknowledgements
We are grateful to Lars Burkert and Damaris Petermann for helping with conducting the behavioral experiments in the lab and to Omer Falik, Barbara Feldmeyer, Evelien Jongepier, and Isabelle Kleeberg for helping to collect the ant colonies. We also wish to thank Steffi Emmling, Marion Kever, and Heike Stypa for support in ant colony maintenance. We are thankful to Katharina Foerster and anonymous reviewers for valuable comments and suggestions. Collection permits were obtained from parks and reserves or we asked private landowners for permission to collect ants. Import and export licenses are not required for the transport of T. longispinosus. We obeyed the guidelines of the Study of Animal Behavior and the legal and institutional rules.
Funding
This study was funded in part by the Deutsche Forschungsgemeinschaft (Fo 298/9-1) and the E.N. Huyck Preserve, NY, USA.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Animal welfare note
The ant species used in this study, Temnothorax longispinosus, do not have specific legislation regulating welfare concerns.
Additional information
Communicated by W. Hughes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Segev, U., Foitzik, S. Ant personalities and behavioral plasticity along a climatic gradient. Behav Ecol Sociobiol 73, 84 (2019). https://doi.org/10.1007/s00265-019-2690-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-019-2690-z