Coping styles in animals: current status in behavior and stress-physiology
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This paper summarizes the current views on coping styles as a useful concept in understanding individual adaptive capacity and vulnerability to stress-related disease. Studies in feral populations indicate the existence of a proactive and a reactive coping style. These coping styles seem to play a role in the population ecology of the species. Despite domestication, genetic selection and inbreeding, the same coping styles can, to some extent, also be observed in laboratory and farm animals. Coping styles are characterized by consistent behavioral and neuroendocrine characteristics, some of which seem to be causally linked to each other. Evidence is accumulating that the two coping styles might explain a differential vulnerability to stress mediated disease due to the differential adaptive value of the two coping styles and the accompanying neuroendocrine differentiation.
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Dingemanse, N. J., Both, C., Drent, P. J., & Tinbergen, J. M. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2004.2680 · Cited by 911 · see citing works
“These individual differences in behaviour often arise early in life (Kagan et al. 1988; Verbeek et al. 1994), have substantial additive (Boissy 1995; Koolhaas et al. 1999; Dingemanse et al. 2002; Drent et al. 2003) and non-additive genetic components (Bouchard & Loehlin 2001; Van Oers et al. 2004)…”
BackgroundInfluentialNatural selection and animal personality
Dingemanse, N. J., & Réale, D. J. F. (2005) · Behaviour · doi:10.1163/156853905774539445 · Cited by 915 · see citing works
“…of animal personality (e.g., aggressiveness) are moderately heritable and relatively stable over the entire life of the individual (Boissy, 1995; Koolhaas et al., 1999; Bouchard & Loehlin, 2001) and that phenotypic correlations between components of personality (e.g., between aggressiveness and…”
BackgroundInfluentialEnergy metabolism and animal personality
Careau, V., Thomas, D. W., Humphries, M. M., & Réale, D. J. F. (2008) · Oikos · doi:10.1111/j.0030-1299.2008.16513.x · Cited by 888 · see citing works
“Proactive and reactive individuals have been shown to differ in HPA axis reactivity, sympathetic and parasympathetic reactivity, as well as testosterone activity (Koolhaas et al. 1999).”
BackgroundInfluentialNeuroendocrinology of coping styles: Towards understanding the biology of individual variation
Koolhaas, J. M., de Boer, S. F., Coppens, C. M., & Buwalda, B. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.04.001 · Cited by 883 · see citing works
Self-citationCurrent issues in fish welfare
Huntingford, F. A., Adams, C. E., Braithwaite, V. A., Kadri, S., Pottinger, T. G., Sandøe, P., & Turnbull, J. F. (2006) · Journal of Fish Biology · doi:10.1111/j.0022-1112.2006.001046.x · Cited by 873 · see citing works
Do baseline glucocorticoids predict fitness?
Bonier, F., Martin, P. R., Moore, I. T., & Wingfield, J. C. (2009) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2009.04.013 · Cited by 789 · see citing works
“For example, we find two patterns of cort secretion associated with two distinct, heritable coping styles (proactive and reactive) in several species, suggesting selective maintenance of variation in cort secretion patterns within populations [ 18 ,19].”
The biology of fear- and anxiety-related behaviors
Steimer, T. J. (2002) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2002.4.3/tsteimer · Cited by 796 · see citing works
“These coping styles are characterized by consistent behavioral and neuroendocrine patterns, and may explain individual differences in vulnerability to stressinduced diseases.(26) Differences in coping styles have also been found between various strains of mice,(27) or between genetically selected rat lines,(28) which…”
BackgroundSex differences in stress-related psychiatric disorders: neurobiological perspectives
Bangasser, D. A., & Valentino, R. J. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.03.008 · Cited by 737 · see citing works
Exposure to predation generates personality in threespined sticklebacks ( Gasterosteus aculeatus )
Bell, A. M., & Sih, A. (2007) · Ecology Letters · doi:10.1111/j.1461-0248.2007.01081.x · Cited by 716 · see citing works
“There is increasing evidence for covariance among behavioural responses [reviewed in Koolhaas et al. (1999), Gosling (2001), Sih et al. (2004b), Dingemanse & Reale (2005) and Bell (2007)].”
BackgroundNatal dispersal and personalities in great tits (Parus major)
Dingemanse, N. J., Both, C., van Noordwijk, A. J., Rutten, A. L., & Drent, P. J. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2300 · Cited by 688 · see citing works
Côté, J., Clobert, J., Brodin, T., et al. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0176 · Cited by 682 · see citing works
“Furthermore, Krawczak et al. (2005) showed that a polymorphism in the promoter region of the serotonin transporter creates differences in age-dependent reproductive success, which in turn is likely to affect age at natal dispersal (Trefilov et al.”
BackgroundBehavioural responses to human‐induced environmental change
Tuomainen, U., & Candolin, U. (2010) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2010.00164.x · Cited by 677 · see citing works
“Individuals differ in traits such as boldness and temperament, that is, in personality, which can influence their responses to human disturbance (Koolhaas et al., 1999; Minderman et al., 2009).”
BackgroundSensory Processing Sensitivity: A Review in the Light of the Evolution of Biological Responsivity
Aron, E. N., Aron, A., & Jagiellowicz, J. (2012) · Personality and Social Psychology Review · doi:10.1177/1088868311434213 · Cited by 645 · see citing works
The evolutionary genetics of personality
Penke, L., Denissen, J. J. A., & Miller, G. F. (2007) · European Journal of Personality · doi:10.1002/per.629 · Cited by 610 · see citing works
Coping styles and behavioural flexibility: towards underlying mechanisms
Coppens, C. M., de Boer, S. F., & Koolhaas, J. M. (2010) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2010.0217 · Cited by 610 · see citing works
“Rodent research distinguishes between proactive and reactive coping (Koolhaas et al. 1999) and researchers of fish and birds often use the terms shyness and boldness (Wilson et al.”
BackgroundSelf-citationCorticosteroids in relation to fear, anxiety and psychopathology
Korte, S. M. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00002-1 · Cited by 607 · see citing works
Self-citationNon-invasive measurement of glucocorticoids: Advances and problems
Palme, R. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.11.021 · Cited by 614 · see citing works
Chapter 5 Insights for Behavioral Ecology from Behavioral Syndromes
Sih, A., & Bell, A. M. (2008) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)00005-3 · Cited by 596 · see citing works
“Coping styles have been studied in some detail in a range of animals including laboratory rodents (Benus et al., 1987, 1991; Koolhaas et al., 1999), farm animals (Hessing et al.”
BackgroundInfluentialRealized heritability of personalities in the great tit ( Parus major )
Drent, P. J., van Oers, K., & van Noordwijk, A. J. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2002.2168 · Cited by 576 · see citing works
“Individuals on the extremes of the main axes can be characterized as having different strategies or coping styles (review, Koolhaas et al. 1999 ).”
BackgroundEvolutionary and ecological approaches to the study of personality
Réale, D. J. F., Dingemanse, N. J., Kazem, A. J. N., & WRIGHT, J. M. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0222 · Cited by 574 · see citing works
Recent models for adaptive personality differences: a review
Dingemanse, N. J., & Wolf, M. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0221 · Cited by 574 · see citing works
“aggressive types are less plastic than non-aggressive ones (Koolhaas et al. 1999).”
BackgroundInfluentialAvian personalities: characterization and epigenesis
Groothuis, T. G. G., & Carere, C. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.06.010 · Cited by 567 · see citing works
“These larger species facilitate physiological research, and based on both behavioral and physiological studies it has been argued that in these two species similar coping strategies exist as in the house mice [7,8,47,48].”
BackgroundFuture directions in behavioural syndromes research
Bell, A. M. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.0199 · Cited by 560 · see citing works
“1993, 1994; Coleman & Wilson 1998) and the proactive–reactive axis (Koolhaas et al. 1999), as well as individual differences in ‘aggressiveness’ (Huntingford 1976; Benus et al.”
BackgroundInfluentialAn explanatory framework for adaptive personality differences
Wolf, M., & Weissing, F. J. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0215 · Cited by 557 · see citing works
“2009) and stress response systems (Koolhaas et al. 1999; Schjolden & Winberg 2007) and their associated physiological morphology, structural differences in the organization of the brain (e.”
BackgroundInfluentialIndividual Differences in Environmental Sensitivity
Pluess, M. (2015) · Child Development Perspectives · doi:10.1111/cdep.12120 · Cited by 556 · see citing works
“These two prototypical behavioral types have been described as hawks and doves, reflecting two different behavioral strategies—proactive versus reactive coping (2)—that evolved over time, each characterized by specific advantages and disad-”
BackgroundSexual selection and animal personality
Schuett, W., Tregenza, T., & Dall, S. R. X. (2009) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2009.00101.x · Cited by 549 · see citing works
“Nevertheless, individuals often show very limited behavioural plasticity which can be manifest in consistent individual differences in behaviour (e.g. Benus et al., 1991; Boissy, 1995; Gosling & John, 1999; Koolhaas et al., 1999; Gosling, 2001; Groothuis & Carere, 2005; Réale et al., 2007), also known as personality d…”
BackgroundInfluentialEvolutionary emergence of responsive and unresponsive personalities
Wolf, M., van Doorn, G. S., & Weissing, F. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805473105 · Cited by 544 · see citing works
“Empirical evidence suggests that individuals that are responsive to environmental stimuli at one point in time and in one context tend to be responsive at later points in time and in different contexts as well (6, 7).”
BackgroundAttachment and the regulation of the right brain
Schore, A. N. (2000) · Attachment & Human Development · doi:10.1080/146167300361309 · Cited by 527 · see citing works
“Basic research in stress physiology shows that the behavioral and physiological response of an individual to a speci c stressor is consistent over time (Koolhaas et al., 1999).”
BackgroundBehavioural syndromes in fishes: a review with implications for ecology and fisheries management
Conrad, J. L., Weinersmith, K. L., Brodin, T., Saltz, J. B., & Sih, A. (2011) · Journal of Fish Biology · doi:10.1111/j.1095-8649.2010.02874.x · Cited by 525 · see citing works
Edaravone ameliorates depressive and anxiety-like behaviors via Sirt1/Nrf2/HO-1/Gpx4 pathway
Dang, R., Wang, M., Li, X., Wang, H., Liu, L., Wu, Q., Zhao, J., Ji, P., Zhong, L., Licinio, J., et al. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02400-6 · Cited by 538 · see citing works
“Next, mice, exposed to an inescapable aversive environment TST and FST, initially violent escape but then transition to a passive coping (PC) state [46].”
BackgroundThe use of pigs in neuroscience: Modeling brain disorders
Lind, N. M., Moustgaard, A., Jelsing, J., Vajta, G., Cumming, P. D., & Hansen, A. K. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.02.003 · Cited by 515 · see citing works
“In most of these studies, the possible characterization of pigs was according to their inclinations to respond either actively (proactive) or passively (reactive) to different situations, which is a well-known phenomenon in many animal species (for review, Koolhaas et al., 1999).”
BackgroundRegulation of the Hypothalamic‐Pituitary‐Adrenocortical Stress Response
Herman, J. P., McKlveen, J. M., Ghosal, S., Kopp, B., Wulsin, A. C., Makinson, R. A., Scheimann, J. R., & Myers, B. (2016) · Comprehensive physiology · doi:10.1002/j.2040-4603.2016.tb00694.x · Cited by 541 · see citing works
“Repeated defeat can produce groups of animals that will largely avoid interaction with the resident (variably referred to as “passive copers” or “stress susceptible”) and groups that will reengage the resident [variably referred to as “active copers” or “stress resistant”) (35,95)].”
Animal personality due to social niche specialisation
Bergmüller, R., & Michael Taborsky, A. (2010) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2010.06.012 · Cited by 494 · see citing works
Øyvind Øverli, A., Sørensen, C., Pulman, K. G. T., Pottinger, T. G., Korzan, W. J., Summers, C. H., & Nilsson, G. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.10.006 · Cited by 503 · see citing works
“Behavioral responses to stress have been described with a variety of terminologies (see e.g. Koolhaas et al., 1999; Wingfield, 2003).”
BackgroundInfluentialAn evolutionary ecology of individual differences
Dall, S. R. X., Bell, A. M., Bolnick, D. I., & Ratnieks, F. L. W. (2012) · Ecology Letters · doi:10.1111/j.1461-0248.2012.01846.x · Cited by 490 · see citing works
“…populations across the animal kingdom (Sih et al. 2004a; Reale et al. 2007; Smith & Blumstein 2008) and is variously referred to as ‘animal personality’ (Dall et al. 2004), ‘behavioural syndromes’ (Sih et al. 2004b), ‘temperament’ (Reale et al. 2007) and ‘coping styles’ (Koolhaas et al. 1999).”
BackgroundAllostatic load, social status and stress hormones: the costs of social status matter
Goymann, W., & Wingfield, J. C. (2004) · Animal Behaviour · doi:10.1016/j.anbehav.2003.08.007 · Cited by 482 · see citing works
“Such differences in coping styles have been associated with differences in glucocorticoid concentrations and allostatic load (Koolhaas et al. 1999; Sapolsky 2002).”
BackgroundStress, corticosterone responses and avian personalities
Cockrem, J. F. (2007) · Journal of Ornithology · doi:10.1007/s10336-007-0175-8 · Cited by 478 · see citing works
“Fast and slow personalities in great tits are equivalent to the proactive (active) and reactive (passive) coping styles or personalities identified in mammals (Koolhaas et al. 1999).”
BackgroundInfluentialHuizink, A. C., Mulder, E. J. H., & Buitelaar, J. K. (2004) · Psychological Bulletin · doi:10.1037/0033-2909.130.1.115 · Cited by 473 · see citing works
Behavioural indicators of welfare in farmed fish
Martins, C. I. M., Galhardo, L., Chris, N., Damsgård, B., Spedicato, M. T., Zupa, W., Beauchaud, M., Kulczykowska, E., Massabuau, J., Carter, T., et al. (2011) · Fish Physiology and Biochemistry · doi:10.1007/s10695-011-9518-8 · Cited by 469 · see citing works
“Physiologically, the proactive coping style is characterised by low production of corticosteroid hormones in response to stress production, but high sympathetic reactivity, while the opposite is true for the reactive coping style (Koolhaas et al. 1999; Pottinger and Carrick 2001a; Øverli et al. 2007).”
BackgroundBOARD-INVITED REVIEW: Using behavior to predict and identify ill health in animals1
Weary, D. M., Huzzey, J. M., & von Keyserlingk, M. A. G. (2008) · Journal of Animal Science · doi:10.2527/jas.2008-1297 · Cited by 460 · see citing works
Between-individual differences in behavioural plasticity within populations: causes and consequences
Dingemanse, N. J., & Wolf, M. (2013) · Animal Behaviour · doi:10.1016/j.anbehav.2012.12.032 · Cited by 458 · see citing works
Engelmann, M., Landgraf, R., & Wotjak, C. T. (2004) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2004.09.001 · Cited by 450 · see citing works
Realized heritability and repeatability of risk-taking behaviour in relation to avian personalities
van Oers, K., Drent, P. J., de Goede, P., & van Noordwijk, A. J. (2004) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2003.2518 · Cited by 447 · see citing works
“These differences in a range of correlated behavioural traits have been labelled as temperament, coping strategies, styles or syndromes (Wechsler 1995; Boissy 1995; Koolhaas et al. 1999), comparable with human personalities (Eysenck & Eysenck 1985; Zuckerman 1991).”
BackgroundStress: An inevitable component of animal translocation
Dickens, M. J., Delehanty, D. J., & Romero, L. M. (2010) · Biological Conservation · doi:10.1016/j.biocon.2010.02.032 · Cited by 443 · see citing works
“, (1999), individuals in a population may have different coping strategies, or in the case of wild avian species, different ‘‘personality” types (Carere and Van Oers, 2004; Groothuis and Carere, 2005), that make them more or less susceptible to stress-related pathology (Cohen et al., 2006; Koolhaas et al., 1999).”
BackgroundGarland, T., Schutz, H., Chappell, M. A., Keeney, B. K., Meek, T. H., Copes, L. E., Acosta, W., Drenowatz, C., Maciel, R. C., van Dijk, G., et al. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.048397 · Cited by 444 · see citing works
Koolhaas, J. M., de Boer, S. F., Buwalda, B., & van Reenen, K. (2007) · Brain Behavior and Evolution · doi:10.1159/000105485 · Cited by 440 · see citing works
“Various terms are used to categorize the extremes of the individual variation such as shy versus bold, active versus passive or proactive versus reactive [Koolhaas et al., 1999].”
BackgroundSelf-citationImplications of domestication and rearing conditions for the behaviour of cultivated fishes
Huntingford, F. A. (2004) · Journal of Fish Biology · doi:10.1111/j.0022-1112.2004.00562.x · Cited by 438 · see citing works
Contribution of genetics to the study of animal personalities: a review of case studies
Drent, P. J., van Noordwijk, A. J., van Oers, K., de Jong, G., & Kempenaers, B. (2005) · Behaviour · doi:10.1163/156853905774539364 · Cited by 427 · see citing works
“These results show that despite a strong genetic correlation in one environment (van Oers et al., 2004b), and a possibly rigid underlying physiological mechanism (Koolhaas et al., 1999), phenotypic correlations between personality traits depend on the context in which they are measured.”
BackgroundInfluentialDetermining the fitness consequences of antipredation behavior
Lind, J., & Cresswell, W. R. (2005) · Behavioral Ecology · doi:10.1093/beheco/ari075 · Cited by 390 · see citing works
“These approaches can also be more fruitful because it has become well established that individuals differ consistently in how they cope with a variety of circumstances (reviewed in Koolhaas et al., 1999).”
BackgroundDefensive burying in rodents: ethology, neurobiology and psychopharmacology
de Boer, S. F., & Koolhaas, J. M. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01278-0 · Cited by 391 · see citing works
“This particular strain is known for its wide variation in levels of aggressive behavior (De Boer et al., 2000; Koolhaas et al., 1999).”
BackgroundSelf-citationResilience in farm animals: biology, management, breeding and implications for animal welfare
Colditz, I. G., & Hine, B. C. (2016) · Animal Production Science · doi:10.1071/an15297 · Cited by 390 · see citing works
“Social conflict has been used in tests of coping style in farm animals (Koolhaas et al. 1999; Lee et al. 2014) and in animal models of human resilience (Russo et al. 2012; Wu et al. 2013).”
BackgroundMethodAtwell, J. W., Cardoso, G. C., Whittaker, D. J., et al. (2012) · Behavioral Ecology · doi:10.1093/beheco/ars059 · Cited by 386 · see citing works
“…expected to contribute to differences in boldness among individuals (van Oers, Drent, de Jong, et al. 2004; van Oers et al. 2005), especially since the allelic variation at SNP830 only explained 4.5–6.0% of the variation in behavior in the P. major study (Fidler et al. 2007; Korsten et al. 2010).”
BackgroundResultInfluentialSex differences in anxiety and emotional behavior
Donner, N. C., & Lowry, C. A. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1271-7 · Cited by 379 · see citing works
“normal 25 % protein content) increases openarm exploration of female offspring tested on the EPM (an anxiolytic effect), but significantly decreases social exploration in both sexes in the SI test due to increased rearing behavior, possibly indicative of increased explorative escape behavior, vigilance, and impulsivit…”
BackgroundSTRESS AND THE CITY: URBANIZATION AND ITS EFFECTS ON THE STRESS PHYSIOLOGY IN EUROPEAN BLACKBIRDS
Partecke, J., Schwabl, I., & Gwinner, E. (2006) · Ecology · doi:10.1890/0012-9658(2006)87[1945:satcua]2.0.co;2 · Cited by 376 · see citing works
“…of changes in behavior (e.g., increased tameness) and stress physiology in urbanized European Blackbirds raises the possibility that urbanization of wild species favors coping styles different from those of their non-urban congeners, enhancing prospects of survival in a city (Koolhaas et al. 1999).”
BackgroundTemperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus
Martin, J. G. A., & Réale, D. (2007) · Animal Behaviour · doi:10.1016/j.anbehav.2007.05.026 · Cited by 374 · see citing works
“…and ecological implications of temperament, personality, or coping style have recently experienced a growing interest (Wilson et al. 1994; Wilson 1998; Koolhass et al. 1999; Dingemanse et al. 2003; Réale & Festa-Bianchet 2003; Dall et al. 2004; Sih et al. 2004; Bell 2005; Carere et al. 2005).”
BackgroundRisk, resources and state-dependent adaptive behavioural syndromes
Luttbeg, B., & Sih, A. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0207 · Cited by 373 · see citing works
“…exhibit behavioural consistency has emphasized proximate constraints: neuroendocrine profiles that can have a genetic basis (Capitanio et al. 1998; Koolhaas et al. 1999, 2007; Bell et al. 2007), or metabolic differences associated with variation in metabolic organ size (Biro & Stamps 2008; Careau…”
BackgroundIndividual variation in glucocorticoid stress responses in animals
Cockrem, J. F. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.11.025 · Cited by 365 · see citing works
Ellis, T., Yıldız, H. Y., López‐Olmeda, J. F., Spedicato, M. T., Tort, L., Øverli, Ø., & Martins, C. I. M. (2011) · Fish Physiology and Biochemistry · doi:10.1007/s10695-011-9568-y · Cited by 365 · see citing works
“ioural trait correlations that are consistent over time and across situation (Koolhaas et al. 1999; Øverli et al. 2007; Silva et al. 2010), or • are due to different environmental conditions (e.”
BackgroundPlasticity in animal personality traits: does prior experience alter the degree of boldness?
Frost, A. J., Winrow-Giffen, A., Ashley, P. J., et al. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3751 · Cited by 351 · see citing works
“Studies have shown that the degree of boldness displayed by an individual is consistently expressed across a range of behavioural tests with bold individuals being more active, taking more risks, learning more quickly (Sneddon 2003), and higher aggression compared with shy individuals performing who show relatively li…”
BackgroundResultInfluentialØverli, Ø. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.3.463 · Cited by 348 · see citing works
“A distinction is often made between proactive (active coping, or ‘‘fight or flight’’) and reactive (passive coping, or ‘‘conservation-withdrawal’’) responses (Engel and Schmale, 1972; Henry and Stephens, 1977; Benus et al., 1991a; Henry, 1993; Koolhaas et al., 1999).”
BackgroundInfluentialLionetti, F., Aron, A. P., Aron, E. N., Burns, G. L., Jagiellowicz, J., & Pluess, M. (2018) · Translational Psychiatry · doi:10.1038/s41398-017-0090-6 · Cited by 357 · see citing works
The mesoaccumbens dopamine in coping with stress
Cabib, S., & Puglisi-Allegra, S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.04.012 · Cited by 329 · see citing works
The mix matters: behavioural types and group dynamics in water striders
Watters, J. V., & Sih, A. (2005) · Behaviour · doi:10.1163/156853905774539454 · Cited by 341 · see citing works
“For example, some individuals might be more active, aggressive or bold than others in various contexts, such as feeding, antipredator, contests, mating and/or dispersal (Huntingford, 1976; Verbeek et al., 1996; Koolhaas et al., 1999).”
Bell, A. M., & Stamps, J. A. (2004) · Animal Behaviour · doi:10.1016/j.anbehav.2004.05.007 · Cited by 340 · see citing works
“…behavioural syndromes (Sih et al. 2003, 2004a, b), temperament (Reale et al. 2000; Reale & Festa-Bianchet 2003), coping styles (Benus et al. 1991; Koolhaas et al. 1999), personality (Gosling 2001) and behavioural strategies (Verbeek et al. 1994; Dingemanse et al. 2003; Drent et al. 2003), the…”
BackgroundLatham, N., & Mason, G. J. (2004) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2004.02.006 · Cited by 338 · see citing works
“Two extremes can be bred from feral mice in the laboratory: aggressive animals, exhibiting short attack latencies (SAL), and less aggressive ones exhibiting long attack latencies (LAL—van Zeegeren, 1980; Benus et al., 1991; Koolhaas et al., 1999).”
BackgroundMcDougall, P. T., Réale, D., Sol, D., & Reader, S. M. (2006) · Animal Conservation · doi:10.1111/j.1469-1795.2005.00004.x · Cited by 341 · see citing works
“…and even populations – differ in their behaviour in a consistent manner (animal science: Boissy, 1995; Grandin, 1998; psychology: Gosling, 2001; behavioural sciences: Clark & Ehlinger, 1987; Koolhaas et al., 1999; evolutionary ecology: Stamps, 1991; Wilson et al., 1994; Sih, Bell & Johnson, 2004).”
BackgroundStress response during development predicts fitness in a wild, long lived vertebrate
Blas, J., Bortolotti, G. R., Tella, J. L., Baos, R., & Marchant, T. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700232104 · Cited by 327 · see citing works
Individual differences in behavioural plasticities
Stamps, J. A. (2015) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12186 · Cited by 329 · see citing works
“…correlations across individuals between specific personality traits (e.g. aggressiveness or exploratory behaviour) and flexibility, in the sense that term is used herein (Benus et al., 1987; Verbeek, Drent & Wiepkema, 1994; Koolhaas et al., 1999; Coppens et al., 2010, see also Section VI.2).”
BackgroundAcevedo, B. P., Aron, E. N., Aron, A. P., Sangster, M.-D. D., Collins, N. L., & Brown, L. L. (2014) · Brain and Behavior · doi:10.1002/brb3.242 · Cited by 329 · see citing works
“A functionally similar trait — termed responsivity, plasticity, or flexibility (Wolf et al. 2008) — has been observed in over 100 nonhuman species including pumpkinseed sunfish (Wilson et al. 1993), birds (Verbeek et al. 1994), rodents (Koolhaas et al. 1999), and rhesus macaques (Suomi 2006).”
Control of behavioural strategies for capricious environments
Wingfield, J. C. (2003) · Animal Behaviour · doi:10.1006/anbe.2003.2298 · Cited by 313 · see citing works
Neurobiology of Resilience: Interface Between Mind and Body
Cathomas, F., Murrough, J. W., Nestler, E. J., Han, M.-H., & Russo, S. J. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.011 · Cited by 296 · see citing works
“Individual coping strategies (13) are particularly relevant to resilience and can be classified into two categories.”
BackgroundDantzer, R., Cohen, S., Russo, S. J., & Dinan, T. G. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.08.010 · Cited by 313 · see citing works
Interaction between animal personality and animal cognition
Carere, C., & Locurto, C. (2011) · Current Zoology · doi:10.1093/czoolo/57.4.491 · Cited by 309 · see citing works
“For example, in birds, fish and rodents some individuals are more aggressive than others and the former differ from non aggressive individuals in many other respects like foraging behaviour or exploration of novel environments (for reviews and special issues; Wilson et al., 1994; Gosling and John, 1999; Koolhaas et al…”
BackgroundInfluentialThe relation between dominance and exploratory behavior is context-dependent in wild great tits
Dingemanse, N. J., & de Goede, P. (2004) · Behavioral Ecology · doi:10.1093/beheco/arh115 · Cited by 306 · see citing works
“Behavioral responses to different stimuli are further often correlated (Huntingford, 1976; Koolhaas et al., 1999; van Oers et al., 2004a) and are therefore commonly regarded as individual differences in temperament or personality (Gosling, 2001; Gosling and John, 1999).”
BackgroundLong-term effects of social stress on brain and behavior: a focus on hippocampal functioning
Buwalda, B., Kole, M. H. P., Veenema, A. H., Huininga, M., de Boer, S. F., Korte, S. M., & Koolhaas, J. M. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.05.005 · Cited by 304 · see citing works
“[6] Koolhaas JM, Korte SM, de Boer SF, Van der Vegt BJ, Van Reenen CG, Hopster H, et al.”
BackgroundSelf-citationRole of the medial prefrontal cortex in coping and resilience
Maier, S. F., & Watkins, L. R. (2010) · Brain Research · doi:10.1016/j.brainres.2010.08.039 · Cited by 292 · see citing works
“At the animal level investigators have generally distinguished between active and passive coping styles (Koolhaas et al., 1999).”
Coping style and immunity in animals: Making sense of individual variation
Koolhaas, J. M. (2008) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2007.11.006 · Cited by 300 · see citing works
“In our view, high levels of aggression are a reflection of a more general proactive coping style, whereas a low level of aggression reflects a reactive coping style (Koolhaas et al., 1999).”
BackgroundSelf-citationde la Mora, M. P., Gallegos-Cari, A., Arizmendi-García, Y., Marcellino, D., & Fuxe, K. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.10.010 · Cited by 296 · see citing works
“The same arguments can be used to differentiate between the avoidance to explore the open arms of the Elevated Plus-Maze and the immobility observed in the ShockProbe Burying test once the animals are electrically shocked which can be identified as passive coping responses (Rodgers, 1997; Koolhaas et al., 1999; De Boe…”
BackgroundA robust animal model of state anxiety: fear-potentiated behaviour in the elevated plus-maze
Korte, S. M., & de Boer, S. F. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01279-2 · Cited by 293 · see citing works
Self-citationBoon, A. K., Réale, D., & Boutin, S. A. (2007) · Ecology Letters · doi:10.1111/j.1461-0248.2007.01106.x · Cited by 288 · see citing works
Carere, C., & van Oers, K. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.07.009 · Cited by 288 · see citing works
“This expectation came from the fact that respiration, being likely under vagal control, can be considered controlled by the parasympathetic system which is supposed to be the dominating system in shy and “passive” animals (Koolhaas et al. 1999; Korte et al. 1999, see introduction).”
BackgroundInfluentialBehavioral syndromes and the evolution of correlated behavior in zebrafish
Moretz, J. A., Martins, E. P., & Robison, B. D. (2007) · Behavioral Ecology · doi:10.1093/beheco/arm011 · Cited by 287 · see citing works
“An aggression–boldness syndrome has been found in numerous animals (see review by Koolhaas et al. 1999).”
BackgroundCarere, C., Groothuis, T. G. G., Möstl, E., Daan, S., & Koolhaas, J. M. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00065-5 · Cited by 282 · see citing works
“Since a differential HPA axis (re)activity between the two strategies is suggested to underlie these difference (Koolhaas et al., 1999), we hypothesize that the slow line of the great tits would show higher CORT levels than the fast line in response to social stress.”
BackgroundSelf-citationPredicting Behavior During Interracial Interactions: A Stress and Coping Approach
Trawalter, S., Richeson, J. A., & Shelton, J. N. (2009) · Personality and Social Psychology Review · doi:10.1177/1088868309345850 · Cited by 280 · see citing works
“Bio-behavioral approaches have outlined broad categories of behavioral coping resp onses that are relevant to coping with stressful interpersonal interactions (e.g., Cannon, 1929, 1932; Engel & Schmale, 1972; Frijda, 1986; Gallup & Maser, 1977; Henry, 1992; Koolhaas et al., 1999; Marks, 1987; Taylor, Klein, Lewis, & G…”
InfluentialActive Avoidance Learning Requires Prefrontal Suppression of Amygdala-Mediated Defensive Reactions
Moscarello, J. M., & LeDoux, J. E. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2596-12.2013 · Cited by 277 · see citing works
High vs Low Anxiety-Related Behavior Rats: An Animal Model of Extremes in Trait Anxiety
Landgraf, R., & Wigger, A. (2002) · Behavior Genetics · doi:10.1023/a:1020258104318 · Cited by 274 · see citing works
“Under identical conditions, LAB rats showed increased locomotor activity and signs of aggressive behavior toward the resident, indicative of active coping ( Koolhaas et al., 1999 ).”
Background
- Authors
- Koolhaas, J. M., Korte, S. M., De Boer, S. F., Van Der Vegt, B. J., Van Reenen, C. G., Hopster, H., De Jong, I. C., Ruis, M. A. W., & Blokhuis, H. J.
- Affiliations
- University of Groningen (NL)
- Corresponding author
- Koolhaas, J.M
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 1999-11
- Volume
- 23
- Issue
- 7
- Pages
- 925-935
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2116707460
- Semantic Scholar
- 129169f853b1e71e05d97fe6ff733d7cd57b22d8
- Cited by
- 2,875
- References
- 97
- Citations by year
- 2026: 87 · 2025: 108 · 2024: 117 · 2023: 136 · 2022: 145 · 2021: 149 · 2020: 197 · 2019: 157 · 2018: 162 · 2017: 158 · 2016: 169 · 2015: 136 · 2014: 152 · 2013: 143 · 2012: 127
- FWCI
- 6.84
- Type
- journal article
- Language
- en
- Open access
- green
- research.wur.nl
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- coping styles, proactive coping, reactive coping, stress physiology, neuroendocrine system, stress-related disorders, feral populations, domestication, livestock, population ecology, behavioral consistency
- MeSH terms
- Adaptation, Psychological, Animals, Behavior, Animal, Stress, Psychological
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