Coping styles in animals: current status in behavior and stress-physiology

“Many authors consider that this assumption of ecological and evolutionary significance is valid (Boissy, 1995; Koolhaas et al., 1999).”

“These different ‘coping styles’ are thought to represent alternative, coherent, adaptive strategies [ 2 ].”

“…doi:10.1016/j.anbehav.2008.12.022 syndromes (Sih et al. 2004a), temperament (Reale et al. 2007), personality (Gosling 2001) and coping styles (Koolhaas et al. 1999), all of which generally refer to behavioural consistency through time and across situations, repeatability is more restrictive…”

“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)].”

“These effects were particularly severe in the aggressive wild-type strain of rats compared to non-aggressive Wistars [30,436,437].”

“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)…”

“…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…”

“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).”

“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].”

“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…”

“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)].”

“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.”

“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).”

“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.”

“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.”

“Individuals on the extremes of the main axes can be characterized as having different strategies or coping styles (review, Koolhaas et al. 1999 ).”

“aggressive types are less plastic than non-aggressive ones (Koolhaas et al. 1999).”

“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].”

“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.”

“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.”

“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-”

“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…”

“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).”

“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).”

“Next, mice, exposed to an inescapable aversive environment TST and FST, initially violent escape but then transition to a passive coping (PC) state [46].”

“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).”

“Behavioral responses to stress have been described with a variety of terminologies (see e.g. Koolhaas et al., 1999; Wingfield, 2003).”

“…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).”

“Such differences in coping styles have been associated with differences in glucocorticoid concentrations and allostatic load (Koolhaas et al. 1999; Sapolsky 2002).”

“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).”

“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).”

“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).”

“, (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).”

“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].”

“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.”

“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).”

“This particular strain is known for its wide variation in levels of aggressive behavior (De Boer et al., 2000; Koolhaas et al., 1999).”

“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).”

“…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).”

“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…”

“…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).”

“…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).”

“…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…”

“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.”

“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…”

“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).”

“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).”

“…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…”

“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).”

“…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).”

“…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).”

“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).”

“Individual coping strategies (13) are particularly relevant to resilience and can be classified into two categories.”

“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…”

“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).”

“[6] Koolhaas JM, Korte SM, de Boer SF, Van der Vegt BJ, Van Reenen CG, Hopster H, et al.”

“At the animal level investigators have generally distinguished between active and passive coping styles (Koolhaas et al., 1999).”

“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).”

“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…”

“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).”

“An aggression–boldness syndrome has been found in numerous animals (see review by Koolhaas et al. 1999).”

“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.”

“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…”

“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 ).”