Coping styles and behavioural flexibility: towards underlying mechanisms
Open accessAbstract
A coping style (also termed behavioural syndrome or personality) is defined as a correlated set of individual behavioural and physiological characteristics that is consistent over time and across situations. This relatively stable trait is a fundamental and adaptively significant phenomenon in the biology of a broad range of species, i.e. it confers differential fitness consequences under divergent environmental conditions. Behavioural flexibility appears to be an important underlying attribute or feature of the coping style that might explain consistency across situations. Proactive coping is characterized by low flexibility expressed as rather rigid, routine-like behavioural tendencies and reduced impulse control (behavioural inhibition) in operant conditioning paradigms. This article summarizes some of the evidence that individual differentiation in behavioural flexibility emerges as a function of underlying variability in the activation of a brain circuitry that includes the prefrontal cortex and its key neurochemical signalling pathways (e.g. dopaminergic and serotonergic input). We argue that the multidimensional nature of animal personality and the terminology used for the various dimensions should reflect the differential pattern of activation of the underlying neuronal network and the behavioural control function of its components. Accordingly, unravelling the molecular mechanisms that give rise to individual differences in the coping style will be an important topic in biobehavioural neurosciences, ecology and evolutionary biology.
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“[32]), and neural pathways between the prefrontal cortex and the hippocampus play a role in the ability to inhibit behaviour [53].”
Homberg, J. R., Schubert, D., Asan, E., & Aron, E. N. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.029 · Cited by 121 · see citing works
Neural plasticity and stress coping in teleost fishes
Sørensen, C., Johansen, I. B., & Øverli, Ø. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.12.003 · Cited by 120 · see citing works
Age, sex and reproductive status affect boldness in dogs
Starling, M. J., Branson, N., Thomson, P. C., et al. (2013) · The Veterinary Journal · doi:10.1016/j.tvjl.2013.05.019 · Cited by 116 · see citing works
Mazza, V., Eccard, J. A., Zaccaroni, M., Jacob, J., & Dammhahn, M. (2018) · Animal Behaviour · doi:10.1016/j.anbehav.2018.01.011 · Cited by 114 · see citing works
Fetal programming by maternal stress: Insights from a conflict perspective
Giudice, M. D. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.05.014 · Cited by 112 · see citing works
“However, there are reasons to believe that emotional reactivity and HPA responsivity increase postnatal plasticity in many different organisms (Coppens et al., 2010).”
Guillette, L. M., Hahn, A. H., Hoeschele, M., et al. (2014) · Animal Cognition · doi:10.1007/s10071-014-0787-3 · Cited by 108 · see citing works
Jolles, J. W., Briggs, H. D., Araya‐Ajoy, Y. G., & Boogert, N. J. (2019) · Animal Behaviour · doi:10.1016/j.anbehav.2019.06.022 · Cited by 109 · see citing works
Interacting personalities: behavioural ecology meets quantitative genetics
Dingemanse, N. J., & Araya‐Ajoy, Y. G. (2014) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2014.12.002 · Cited by 104 · see citing works
Personality predicts foraging site fidelity and trip repeatability in a marine predator
Harris, S. M., Descamps, S., Sneddon, L. U., Bertrand, P., Chastel, O., & Patrick, S. C. (2019) · Journal of Animal Ecology · doi:10.1111/1365-2656.13106 · Cited by 104 · see citing works
“While shy animals typically exhibit flexibility in response to environmental fluctuations, bolder animals are instead thought to rely upon routines when navigating (Benus et al., 1990; Coppens et al., 2010; Marchetti & Drent, 2000).”
BackgroundPersonality predicts behavioral flexibility in a fluctuating, natural environment
Herborn, K. A., Heidinger, B. J., Alexander, L. G., et al. (2014) · Behavioral Ecology · doi:10.1093/beheco/aru131 · Cited by 102 · see citing works
“Our findings with the neophobia trait fit the expectation from captive studies that slow types should be behaviorally flexible (Coppens et al. 2010).”
ResultInfluentialLearning and personality types are related in cavies (Cavia aperea).
Guenther, A., Brust, V., Dersen, M., & Trillmich, F. (2013) · Journal of comparative psychology · doi:10.1037/a0033678 · Cited by 101 · see citing works
Kotrschal, A., Lievens, E., Dahlbom, J., Bundsen, A., Semenova, S. A., Sundvik, M., Maklakov, A. A., Winberg, S., Panula, P., & Kolm, N. (2013) · Evolution · doi:10.1111/evo.12341 · Cited by 96 · see citing works
“Finally, to investigate behavioral flexibility, which generally decreases with increased proactivity (Coppens et al. 2010), we 1 1 4 0 EVOLUTION APRIL 2014 quantified the response to a change in a familiar task, represented by a novel food source.”
BackgroundInfluentialThe ontogeny of personality in the wild guinea pig
Guenther, A., Finkemeier, M., & Trillmich, F. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2014.01.032 · Cited by 95 · see citing works
Personalities influence spatial responses to environmental fluctuations in wild fish
Villegas‐Ríos, D., Réale, D. J. F., Freitas, C., Moland, E., & Olsen, E. M. (2018) · Journal of Animal Ecology · doi:10.1111/1365-2656.12872 · Cited by 94 · see citing works
Why personality differences matter for social functioning and social structure
Wolf, M., & Krause, J. (2014) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2014.03.008 · Cited by 91 · see citing works
Common marmosets show social plasticity and group-level similarity in personality
Koski, S. E., & Burkart, J. M. (2015) · Scientific Reports · doi:10.1038/srep08878 · Cited by 91 · see citing works
Yu, R. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00019 · Cited by 98 · see citing works
“Identifying determinates of such resilience to stress can also aid in engineering training regimens that better equip individuals to meet the challenges in the modern society (Coppens et al., 2010; Koolhaas et al., 2010; van den Bos et al., 2013b).”
BackgroundAgustín‐Pavón, C., Braesicke, K., Shiba, Y., Santangelo, A. M., Mikheenko, Y., Cockroft, G., Asma, F., Clarke, H. F., Man, M., & Roberts, A. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.03.007 · Cited by 90 · see citing works
Dunn, J. C., Cole, E. F., & Quinn, J. L. (2011) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-011-1156-8 · Cited by 89 · see citing works
“This is also likely to be confounded by the strong association between physiological and behavioural traits (Koolhaas 2008; Coppens et al. 2010).”
BackgroundHaas, E. N. D., & van der Eijk, J. A. J. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.07.007 · Cited by 92 · see citing works
Behavioral flexibility of a generalist carnivore
Daniels, S. E., Fanelli, R. E., Gilbert, A. T., & Benson‐Amram, S. (2019) · Animal Cognition · doi:10.1007/s10071-019-01252-7 · Cited by 85 · see citing works
Niemelä, P. T., Vainikka, A., Forsman, J. T., Loukola, O., & Kortet, R. (2012) · Ecology and Evolution · doi:10.1002/ece3.451 · Cited by 83 · see citing works
“Also serotonin and dopamine levels may affect the level of behavioral flexibility (Coppens et al. 2010), implying that some individuals may have more direct stimulus – response chain to environmental cues compared with others leading some to being guided by the environment while others being guided by routines (Coppen…”
BackgroundBiologging reveals individual variation in behavioural predictability in the wild
Hertel, A. G., Royauté, R., Zedrosser, A., & Mueller, T. (2020) · Journal of Animal Ecology · doi:10.1111/1365-2656.13406 · Cited by 82 · see citing works
“…a neuroendocrinological perspective, bolder and more proactive individuals seem to have less inhibitory control and are hence more predictable in their behavioural responses, whereas shyer, reactive individuals are more flexible to adjust their behaviour to the environment (Coppens et al., 2010).”
BackgroundSquibb, K., Griffin, K., Favier, R., et al. (2018) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2018.02.003 · Cited by 80 · see citing works
“However, interpreting behaviour may be confounded by individual differences in stress response (Coppens et al., 2010; Ijichi et al., 2014; Lush and Ijichi, Accepted).”
BackgroundBasic functional trade-offs in cognition: An integrative framework
Giudice, M. D., & Crespi, B. J. (2018) · Cognition · doi:10.1016/j.cognition.2018.06.008 · Cited by 80 · see citing works
“…contribute to broader individual differences in behavior, which in the animal literature are captured by the distinction between proactive and reactive coping styles (defined as stable patterns of behavioral and physiological responses to challenges; see Coppens et al., 2010; Del Giudice, 2015).”
Associations between glucocorticoids and sociality across a continuum of vertebrate social behavior
Raulo, A., & Dantzer, B. (2018) · Ecology and Evolution · doi:10.1002/ece3.4059 · Cited by 78 · see citing works
Consumer and motor innovation in the common myna: the role of motivation and emotional responses
Sol, D., Griffin, A. S., & Bartomeus, Í. (2011) · Animal Behaviour · doi:10.1016/j.anbehav.2011.10.024 · Cited by 77 · see citing works
“These findings again contradict the view that proactive coping styles, here measured in terms of lower neophobic responses, are characterized by low behavioural flexibility (Coppens et al. 2010).”
InfluentialThermal physiology: A new dimension of the pace‐of‐life syndrome
Goulet, C. T., Thompson, M. B., Michelangeli, M., et al. (2017) · Journal of Animal Ecology · doi:10.1111/1365-2656.12718 · Cited by 77 · see citing works
Developmental constraints on behavioural flexibility
Holekamp, K. E., Swanson, E. M., & Meter, P. E. V. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0350 · Cited by 77 · see citing works
Behavioural Flexibility and Personality in Zebra Finches
Brust, V., Würz, Y., & Krüger, O. (2013) · Ethology · doi:10.1111/eth.12095 · Cited by 76 · see citing works
Cell-type-specific role for nucleus accumbens neuroligin-2 in depression and stress susceptibility
Heshmati, M., Aleyasin, H., Menard, C., Christoffel, D. J., Flanigan, M. E., Pfau, M. L., Hodes, G. E., Lepack, A. E., Bicks, L. K., Takahashi, A., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1719014115 · Cited by 75 · see citing works
A comparison of problem-solving success between urban and rural house sparrows
Papp, S., Vincze, E., Preiszner, B., Liker, A., & Bókony, V. (2014) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-014-1859-8 · Cited by 75 · see citing works
“Behavioural flexibility is the ability of an organism to directly respond and adjust its behaviour to environmental circumstances (Coppens et al. 2010; Wright et al. 2010), which provides animals with a crucial tool for adapting to changing environments (Sol and Lefebvre 2000; Reader and Laland 2003).”
BackgroundSex differences in risk-taking and associative learning in rats
Jolles, J. W., Boogert, N. J., & van den Bos, R. (2015) · Royal Society Open Science · doi:10.1098/rsos.150485 · Cited by 75 · see citing works
“It is interesting to note that similar effects as we describe here at the level of the sexes have been documented extensively at the individual level (‘coping styles’) [72,76].”
BackgroundUrbanization erodes niche segregation in Darwin's finches
León, L. D. D., Sharpe, D., Gotanda, K., Raeymaekers, J., Chaves, J., Hendry, A., & Podos, J. (2018) · Evolutionary Applications · doi:10.1111/eva.12721 · Cited by 51 · see citing works
Rebolo‐Ifrán, N., Carrete, M., Sanz‐Aguilar, A., et al. (2015) · Scientific Reports · doi:10.1038/srep13723 · Cited by 74 · see citing works
Interacting with the enemy: indirect effects of personality on conspecific aggression in crickets
Santostefano, F., Wilson, A. J., Araya‐Ajoy, Y. G., & Dingemanse, N. J. (2016) · Behavioral Ecology · doi:10.1093/beheco/arw037 · Cited by 74 · see citing works
Sources of intraspecific variation in sleep behaviour of wild great tits
Stuber, E. F., Dingemanse, N. J., Kempenaers, B., & Mueller, J. C. (2015) · Animal Behaviour · doi:10.1016/j.anbehav.2015.05.025 · Cited by 72 · see citing works
Costantini, D., Ferrari, C., Pasquaretta, C., Cavallone, E., Carere, C., von Hardenberg, A., & Réale, D. J. F. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.062034 · Cited by 72 · see citing works
“According to previous results on the relationship between glucocorticoids and coping styles (Koolhaas et al., 1999; Koolhaas et al., 2010; Øverli et al., 2007; Coppens et al., 2010), we predicted that proactive individuals should show both a lower baseline level of CORT and a lower production of CORT under restraint t…”
BackgroundResultInfluentialMultidimensionality in parasite-induced phenotypic alterations: ultimate versus proximate aspects
Cézilly, F., Favrat, A., & Perrot‐Minnot, M. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.074005 · Cited by 73 · see citing works
“…that multidimensionality in personality syndromes could reflect differential patterns of activation of some key neurochemical signalling pathways (Coppens et al., 2010), such that a disruption of such pathways caused by parasitic infection may simultaneously affect several personality traits in…”
BackgroundKrupıć, D., & Corr, P. J. (2017) · Psihologijske teme · doi:10.31820/pt.26.1.2 · Cited by 72 · see citing works
“, 2008), self-control (Carver, Johnson, & Joormann, 2014; Ranade, Pi, & Kepecs, 2014), and cognitive flexibility (Coppens et al., 2010), while in rats, serotonin participates in control of impulsive behaviour (Bizot, Le Bihan, Puech, Hamon, & Thiébot, 1999).”
Vaz-Serrano, J., Ruiz‐Gómez, M. D. L., Gjøen, H. M., Skov, P. V., Huntingford, F. A., Øyvind Øverli, A., & Höglund, E. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.02.025 · Cited by 73 · see citing works
“Reactive individuals, on the other hand, show a freeze–hide cortisol dominated response to a challenge, social subordination, behavioural flexibility and a more shy behaviour [2,7,8].”
Individual differences in the effects of prenatal stress exposure in rodents
Boersma, G. J., & Tamashiro, K. L. (2014) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.10.006 · Cited by 71 · see citing works
“Proactive stresscoping individuals tend to show more aggression and impulsivity and are less behaviorally flexible than passive stress-copers (Coppens et al., 2010).”
BackgroundSant’Anna, A. C., & da Costa, M. J. R. P. (2013) · Livestock Science · doi:10.1016/j.livsci.2013.08.004 · Cited by 71 · see citing works
“the aim of understanding its physiological basis (Coppens et al., 2010; Koolhaas et al., 2010) and the effects of cattle temperament on animal's health (Burdick et al.”
BackgroundThe neurobiology of offensive aggression: Revealing a modular view
de Boer, S. F., Olivier, B., Veening, J., & Koolhaas, J. M. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.04.040 · Cited by 70 · see citing works
Self-citationLaredo, S. A., Steinman, M. Q., Robles, C. F., Ferrer, E., Ragen, B. J., & Trainor, B. C. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12824 · Cited by 75 · see citing works
“Coping strategies during times of rapid change can be traced back to an individual’s propensity to demonstrate behavioral flexibility under environmental stress (Coppens et al., 2010).”
BackgroundSoares, M. C., Gerlai, R. T., & Maximino, C. (2018) · Journal of Fish Biology · doi:10.1111/jfb.13757 · Cited by 69 · see citing works
Mazza, V., Jacob, J., Dammhahn, M., Zaccaroni, M., & Eccard, J. A. (2019) · Scientific Reports · doi:10.1038/s41598-019-46582-1 · Cited by 68 · see citing works
LeBlanc, S., Höglund, E., Gilmour, K. M., & Currie, S. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00196.2011 · Cited by 67 · see citing works
“In the HR/LR trout model (47), as well as in rats (8), such differences have been demonstrated using feeding behavior.”
BackgroundSocial stress models in rodents: Towards enhanced validity
Koolhaas, J. M., de Boer, S. F., Buwalda, B., & Meerlo, P. (2016) · Neurobiology of Stress · doi:10.1016/j.ynstr.2016.09.003 · Cited by 68 · see citing works
“It is rigid and makes much more mistakes than a reactive coping individual (Benus et al., 1990; Bolhuis et al., 2004; Coppens et al., 2010).”
Self-citationFavati, A., Leimar, O., Radesäter, T., et al. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.2531 · Cited by 66 · see citing works
“Third (and partially overlapping with the previous), behaviour and social position can have a common underlying cause [13,21].”
BackgroundMesa‐Gresa, P., Pérez‐Martinez, A., & Redolat, R. (2013) · Aggressive Behavior · doi:10.1002/ab.21481 · Cited by 66 · see citing works
Environmental and genetic determinants of innovativeness in a natural population of birds
Quinn, J. L., Cole, E. F., Reed, T. E., & Morand‐Ferron, J. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0184 · Cited by 65 · see citing works
The relationship between learning speed and personality is age- and task-dependent in red junglefowl
Zidar, J., Balogh, A., Favati, A., Jensen, P., Leimar, O., Sorato, E., & Løvlie, H. (2018) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-018-2579-2 · Cited by 66 · see citing works
Social support in pigs with different coping styles
Reimert, I., Bolhuis, J. E., Kemp, B., & Rodenburg, T. B. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.02.059 · Cited by 65 · see citing works
“16,48, this study] which indicates that the relationship between coping style and these systems is not yet clear [10,11].”
BackgroundStamatakis, A., Diamantopoulou, A., Panagiotaropoulos, T. I., Raftogianni, A., & Stylianopoulou, F. (2013) · Frontiers in Endocrinology · doi:10.3389/fendo.2013.00178 · Cited by 65 · see citing works
Differences in stress reactivity between zebrafish with alternative stress coping styles
Wong, R. Y., French, J. A., & Russ, J. B. (2019) · Royal Society Open Science · doi:10.1098/rsos.181797 · Cited by 64 · see citing works
A proactive–reactive syndrome affects group success in an ant species
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On personality, energy metabolism and mtDNA introgression in bank voles
Šíchová, K., Koskela, E., Mappes, T., Lantová, P., & Boratyński, Z. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2014.04.011 · Cited by 64 · see citing works
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“In contrast, reactive animals are more driven by the environment and may exhibit immobility and anxiety-like behaviors in response to a novel environment (see Coppens et al., 2010 for review).”
BackgroundLinking Fearfulness and Coping Styles in Fish
Martins, C. I. M., Silva, P. I. M., Conceição, L. E. C., Costas, B., Höglund, E., Øyvind Øverli, A., & Schrama, J. W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028084 · Cited by 63 · see citing works
“flexible responses, when faced with changing environmental conditions, individuals of the same species or population show consistent responses in stressful and dangerous situations [2,3,4].”
BackgroundSocial modulation of decision-making: a cross-species review
van den Bos, R., Jolles, J. W., & Homberg, J. R. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00301 · Cited by 64 · see citing works
Song bout length is indicative of spatial learning in European starlings
Farrell, T. M., Weaver, K. H. A., An, Y., & MacDougall‐Shackleton, S. A. (2011) · Behavioral Ecology · doi:10.1093/beheco/arr162 · Cited by 61 · see citing works
“…onset and longer duration of stress in development had effects on neural and physiological de- velopment that altered physiological reactivity to novel objects and situations (Coppens et al. 2010) or 2) birds caught as juveniles represent a subpopulation of birds from our nestling population.”
BackgroundCarbonara, P., Alfonso, S., Zupa, W., et al. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112698 · Cited by 62 · see citing works
Reimert, I., Rodenburg, T. B., Ursinus, W., Kemp, B., & Bolhuis, J. E. (2013) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2013.11.015 · Cited by 61 · see citing works
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“Conversely, passive responders avoid threats, have a less aggressive phenotype, and respond actively only when it is absolutely necessary [24,25].”
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“Boldness” in the domestic dog differs among breeds and breed groups
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Individuality in movement: the role of animal personality
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“In many different animal species two extremes in coping style or personality have been described: proactive and reactive [91,92,93].”
BackgroundLuo, L., Reimert, I., Haas, E. N. D., Kemp, B., & Bolhuis, J. E. (2019) · Animal Cognition · doi:10.1007/s10071-019-01287-w · Cited by 58 · see citing works
- Authors
- Coppens, C. M., de Boer, S. F., & Koolhaas, J. M.
- Affiliations
- University of Groningen (NL)
- Department of Behavioural Physiology, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2010-12-27
- Volume
- 365
- Issue
- 1560
- Pages
- 4021-4028
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC2992750
- OpenAlex
- W2136361247
- Semantic Scholar
- a728963ac55bd0a912d799a48dfeb94690ee6746
- Cited by
- 610
- References
- 64
- Citations by year
- 2026: 23 · 2025: 38 · 2024: 39 · 2023: 48 · 2022: 38 · 2021: 32 · 2020: 52 · 2019: 43 · 2018: 44 · 2017: 41 · 2016: 43 · 2015: 46 · 2014: 40 · 2013: 35 · 2012: 24
- FWCI
- 27.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (submittedVersion)
- PubMed Central (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- coping styles, behavioral flexibility, animal personality, behavioral syndromes, proactive coping, behavioral inhibition, individual differences, prefrontal cortex, dopamine signaling, brain circuits
- MeSH terms
- Adaptation, Psychological, Animals, Behavior, Animal, Models, Neurological, Models, Psychological, Personality, Receptors, Dopamine, Reward, Prefrontal Cortex, Behavioral Research
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