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

Koolhaas, Jaap M.; Korte, S. Mechiel; Boer, Sietse F. de; Vegt, Bea J. van der; Reenen, C.G. van; Hopster, H.; Jong, I.C. de; Ruis, M.A.W.; Blokhuis, H.J.

doi:10.1016/s0149-7634(99)00026-3

Cited by 2,419 publications

(2,217 citation statements)

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“…Our results find support in results showing how the impact of stress on cardiovascular and psychiatric diseases is modulated by a passive or reactive coping style in response to stressful situations (Koolhaas et al., 1999). Consistently, subordinate male mice, corresponding to subjects characterized by high aggression received and low aggression exhibited, manifested HPA axis upregulation that is one of the common markers of chronic stress and allostatic load (McEwen, 1998; Seeman et al., 1997), which might set the stage for metabolic disease thus compromising healthspan.…”

Section: Discussionmentioning

confidence: 99%

Social stress shortens lifespan in mice

et al. 2018

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SummaryStress and low socioeconomic status in humans confer increased vulnerability to morbidity and mortality. However, this association is not mechanistically understood nor has its causation been explored in animal models thus far. Recently, cellular senescence has been suggested as a potential mechanism linking lifelong stress to age‐related diseases and shorter life expectancy in humans. Here, we established a causal role for lifelong social stress on shortening lifespan and increasing the risk of cardiovascular disease in mice. Specifically, we developed a lifelong chronic psychosocial stress model in which male mouse aggressive behavior is used to study the impact of negative social confrontations on healthspan and lifespan. C57BL/6J mice identified through unbiased cluster analysis for receiving high while exhibiting low aggression, or identified as subordinate based on an ethologic criterion, had lower median and maximal lifespan, and developed earlier onset of several organ pathologies in the presence of a cellular senescence signature. Critically, subordinate mice developed spontaneous early‐stage atherosclerotic lesions of the aortic sinuses characterized by significant immune cells infiltration and sporadic rupture and calcification, none of which was found in dominant subjects. In conclusion, we present here the first rodent model to study and mechanistically dissect the impact of chronic stress on lifespan and disease of aging. These data highlight a conserved role for social stress and low social status on shortening lifespan and increasing the risk of cardiovascular disease in mammals and identify a potential mechanistic link for this complex phenomenon.

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Section: Discussionmentioning

confidence: 99%

Social stress shortens lifespan in mice

et al. 2018

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“…Proactivity has been shown to be repeatable over time (reviewed by Réale et al., 2007) and there are consistent individual differences in parental behavior (Budaev, Zworykin, & Mochek, 1999; Fairbanks, 1996; Maestripieri, 1993; Schwagmeyer & Mock, 2003), affiliative behavior (Seyfarth, Silk, & Cheney, 2012; Webb, Franks, Romero, Higgins, & de Waal, 2014), and alloparental behavior in cooperative breeders (Carter, English, & Clutton‐Brock, 2014; English, Nakagawa, & Clutton‐Brock, 2010). Furthermore, individual differences in measures of HPA‐axis activity exist (Baugh, van Oers, Dingemanse, & Hau, 2014; Ellis, Jackson, & Boyce, 2006; Fletcher, Dantzer, & Boonstra, 2015) and has been observed to co‐vary with different behavioral types (Carere et al., 2010; Cockrem, 2007; Koolhaas et al., 1999; Korte, Koolhaas, Wingfield, & McEwen, 2005). In this review, we focus on the potential for these individual differences in HPA‐axis activity to cause the individual variation across the range of social behaviors (Figure 1), though we recognize that much of this work is correlative.…”

Section: Diversity Of Social Behaviormentioning

confidence: 99%

“…The proximate mechanisms underlying animal personalities or individual‐variation in behavior have already been reviewed to some extent (Carere et al., 2010; Hau et al., 2016; Koolhaas et al., 1999, 2010; Packard, Egan, & Ulrich‐Lai, 2016; Sapolsky, 1990; Sih, 2011). However, the predominant focus of these previous studies has been on repeatable differences in personality traits such as aggression, activity, or docility (reviewed by Bell, Hankison, & Laskowski, 2009).…”

Section: Introductionmentioning

confidence: 99%

Associations between glucocorticoids and sociality across a continuum of vertebrate social behavior

Raulo

Dantzer

2018

Ecology and Evolution

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The causes and consequences of individual differences in animal behavior and stress physiology are increasingly studied in wild animals, yet the possibility that stress physiology underlies individual variation in social behavior has received less attention. In this review, we bring together these study areas and focus on understanding how the activity of the vertebrate neuroendocrine stress axis (HPA‐axis) may underlie individual differences in social behavior in wild animals. We first describe a continuum of vertebrate social behaviors spanning from initial social tendencies (proactive behavior) to social behavior occurring in reproductive contexts (parental care, sexual pair‐bonding) and lastly to social behavior occurring in nonreproductive contexts (nonsexual bonding, group‐level cooperation). We then perform a qualitative review of existing literature to address the correlative and causal association between measures of HPA‐axis activity (glucocorticoid levels or GCs) and each of these types of social behavior. As expected, elevated HPA‐axis activity can inhibit social behavior associated with initial social tendencies (approaching conspecifics) and reproduction. However, elevated HPA‐axis activity may also enhance more elaborate social behavior outside of reproductive contexts, such as alloparental care behavior. In addition, the effect of GCs on social behavior can depend upon the sociality of the stressor (cause of increase in GCs) and the severity of stress (extent of increase in GCs). Our review shows that the while the associations between stress responses and sociality are diverse, the role of HPA‐axis activity behind social behavior may shift toward more facilitating and less inhibiting in more social species, providing insight into how stress physiology and social systems may co‐evolve.

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“…In animals kept for production, both environmental challenges and social isolation are recognised as stressors, which could negatively affect the fear and anxiety levels of the animals (Forkman et al, 2007) and thus their physiology and immune reaction (Koolhaas et al, 1999). Specific tests are used to measure fear levels in several species (Forkman et al, 2007), but few experimental data are available for rabbits (Verga et al, 2007): the tonic immobility test has been used to evaluate rabbit fear towards humans (Ferrante et al, 1992;Trocino et al, 2004 andVerwer et al, 2009), and the open-field test has been used to obtain information on the fear of rabbits when exposed to an unknown environment (Meijsser et al, 1989;Ferrante et al, 1992;Xiccato et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Housing of growing rabbits in individual, bicellular and collective cages: fear level and behavioural patterns

Trocino

Majolini

Tazzoli

et al. 2013

Animal

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During growth (27 to 75 days of age), a total of 384 rabbits were kept in 72 individual cages, 48 bicellular cages (2 rabbits/cage) and 24 collective cages (9 rabbits/cage). To evaluate the effects of the housing system on the fear level and behavioural patterns of rabbits at the two ages (39 to 45 days and 66 to 73 days), a tonic immobility test and an open-field test were conducted and their behaviour was video recorded. In the tonic immobility test, the number of attempts to induce immobility (1.38) was lower, and the duration of immobility (47.8 s) was higher (0.05 , P , 0.01) in the rabbits housed in individual cages than in those kept in bicellular (1.72 attempts and 25.0 s of immobility) and collective cages (1.99 attempts and 25.0 s of immobility). During the open-field test, the rabbits from individual and bicellular cages showed higher latency (38.8 and 40.3 v. 27.0 s), a lower number of total (73.3 and 81.7 v. 91.9) and central displacements (3.6 and 2.8 v. 5.4) and a shorter running time (11.8 and 13.6 s v. 17.7 s) and the time biting the pen (5.5 and 9.1 s v. 28.2 s) compared with the rabbits kept in collective cages (0.05 , P , 0.001). During the 24-h video recording, the rabbits in individual and bicellular cages spent less time allogrooming (0.34% and 0.19% v. 1.44%), moving (0.74% and 0.60% v. 1.32%) and running (0.08% and 0.03% v. 0.21%) than the rabbits in the collective cages (0.01 , P , 0.001). The lowest numbers of alerts and hops were observed in the rabbits kept in bicellular cages. With increasing age, a lower number of rabbits were sensitive to the immobility test and more rabbits entered the pen spontaneously during the open-field test (P , 0.001). In conclusion, the rabbits in individual cages exhibited the highest fear level and incomplete behavioural patterns; the rabbits housed in collective cages showed the lowest fear levels and had the possibility of expressing a wider range of behaviour; and the rabbits in bicellular cages exhibited an inconsistent pattern of fear in the tonic immobility and open-field tests. Probably, these rabbits were in a less stressful condition compared with animals in individual cages because social contacts were allowed, even if freedom of movement was more limited.Keywords: housing system, fear level, behaviour, growing rabbits ImplicationsPeople are concerned about the welfare status of rabbits reared for meat production in small cages. This paper demonstrates that housing rabbits in individual or bicellular cages threatens their welfare by increasing their fear level and by limiting their possibility of expressing normal behaviour. In collective cages (9 rabbits/cage), social contacts and movements are permitted, and both fear response and behavioural patterns improve. The tonic immobility and the open-field tests can be used to compare the fear level of rabbits in different housing systems.

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

Cited by 2,419 publications

References 65 publications

Social stress shortens lifespan in mice

Social stress shortens lifespan in mice

Associations between glucocorticoids and sociality across a continuum of vertebrate social behavior

Housing of growing rabbits in individual, bicellular and collective cages: fear level and behavioural patterns

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