Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal

mystery of yawning 





mise à jour du
1 septembre 2015
Zoo Biology
Perception of Available Space During Chimpanzee Introductions: Number of Accessible Areas Is More Important Than Enclosure Size
Elizabeth S. Herrelko, Hannah M.
Buchanan-Smith, and Sarah-Jane Vick
Psychology, School of Natural Sciences, University of Stirling
Stirling, Scotland


Maintenance behavior - Comportement substitutif
Restricting animals to different areas of their enclosure, for both brief and extended durations, is a key element of animal management practices. With such restrictions, available space decreases and the choices the animals can make are more limited, particularly in relation to social dynamics. When unfamiliar individuals are introduced to each other, group dynamics can be unpredictable and understanding space usage is important to facilitate successful introductions.
We studied the behavioral, welfare-related responses of two groups of zoo-housed chimpanzees (n = 22) as they were introduced to each other and experienced a variety of enclosure restrictions and group composition changes. Our analysis of available space while controlling for chimpanzee density, found that arousal-related scratching and yawning decreased as the number of enclosure areas (separate rooms) available increased, whereas only yawning decreased as the amount of available space (m2) increased.
Allogrooming, rubbing, and regurgitation/reingestion rates remained constant as both the number of enclosure areas and amount of space changed. Enclosure space is important to zoo-housed chimpanzees, but during introductions, a decrease in arousal-related scratching indicates that the number of accessible areas is more important than the total amount of space available, suggesting that it is important to provide modular enclosures that provide choice and flexible usage, to minimize the welfare impact of short- and long-term husbandry needs.
An important element in the captive management of animals is safely moving groups between enclosure areas to allow care staff to provide for the animals' needs [Hosey et ah, 2009]. Husbandry requirements may temporarily limit animals to off-exhibit areas for cleaning or maintenance purposes [e.g., Ross et ah, 2010] and sections of enclosures might be closed off on a long-term basis for major events such as animal introductions [e.g., Schel et ah, 2013]. Additionally, zoos in temperate climates have to deal with the challenges of temperature fluctuations and inclement weather, prompting animal care staff to occasionally limit animal access to indoor areas (e.g., when moats freeze over [de Waal, 1982]). Even when access is permitted during inclement weather, animals may choose to stay indoors [Ross et ah, 2011]. As a result, the space (m ) and number of available enclosure areas (separate rooms) often change.
This may lead to shifts in behavioral and social opportunities, making it important to understand the impact of short- and long-term spatial restrictions on animal welfare. Individuals often indicate strong location preferences; however, suggest¬ing that having a choice of locations may be more important for optimal welfare than overall space availability [Ross et ah, 2011].
Crowding and space availability impact social relationships with an increased likelihood of social conflict under higher density conditions [Judge, 2000]. Primates are known to employ different strategies to mediate the stressors of high-density situations: The conflict-avoidance model describes when social interactions decrease during short-term conflict management [Judge and de Waal, 1993]. The tension-reduction model occurs when affiliative behaviors are increased and aggressive behaviors are decreased during long-term conflict management [de Waal, 1989]. With many captive habitats consisting of two or three separate areas (e.g., one outdoor enclosure and one indoor enclosure, often with an indoor, off-exhibit area), restricted access decreases the degree of choice animals have regarding location and interactions [Ross et ah, 2011]. This can lead to an increase in negative behaviors, such as stereotypies and aggression (e.g., giant pandas [Owen et ah, 2005]; great apes [Ross et ah, 2010]).
Although social contact is essential for gregarious species, if social interaction only fills 10% of a chimpanzee's day in the wild [Pruetz and McGrew, 2002], is it desirable to encourage captive situations in which interactions are unavoidable [Schapiro, 2003]? Over the past few decades, we have increased our awareness of the importance of enclosure design, group density, and the ability to form subgroups on the behavior of chimpanzees (Design&emdash;usage [Traylor-Holzer and Fritz, 1985]; Design&emdash;differences within facilities [Ross and Lukas, 2006; Ross et ah, 2010]; differences between facilities [Jensvold et al., 2001; Ross et ah, 2009]; Density [Nieuwenhuijsen and de Waal, 1982; Aureli and de Waal, 1997; Videan and Fritz, 2007]; Fission-fusion [Bloomsmith and Barker, 2001; Amici et ah, 2008; Clark, 2011]), providing helpful background information for facility design and renovation. The impact of enclosure size is of particular concern as it is often limited due to practical as well as financial constraints.
Previous research has identified few behavioral changes in relation to differences in enclosure size, suggesting that we should focus our resources on other enclosure elements (e.g., opportunities for enrichment, foraging, and socialization) rather than enclosure size alone [Line et ah, 1991]. For example, although aggression was higher in an indoor enclosure than a larger outdoor enclosure, the increase was not proportionate to the difference in spatial density in these two areas [Nieuwenhuijsen and de Waal, 1982]. Chimpanzees may use strategies to avoid conflict by reducing social interaction when space is restricted on a short-term basis [Judge and de Waal, 1993; Aureli and de Waal, 1997; Videan and Fritz, 2007]. They may use other coping strategies to reduce aggression at higher spatial densities for longer durations (e.g., increase affiliative behavior and decrease aggressive behaviors [de Waal, 1989]; increase of self-directed (e.g., scratching) or abnormal behaviors
Although the internal states of animals are difficult to assess, we can look to specific behavioral indicators as a means to evaluate their well-being, particularly self-directed behaviors (SDBs: scratch, rub, and yawn) and the abnormal behavior, regurgitation/reingestion (R/R). Known as dis¬placement behaviors, SDBs are considered to be a redirection of behavior when the animal is uncertain about how to behave [Maestripieri et ah, 1992]. Scratching, in particular, has been well studied and increased rates are linked to social changes that have the potential to produce negative outcomes, such as proximity of other groups [Aureli and de Waal, 1997; Baker and Aureli, 1997]. Regurgitation/ reingestion, on the other hand, is considered to be an abnormal undesirable behavior and was exhibited by the individuals in one of the two groups included in this study. Although R/R has been well studied [e.g., Baker and Easley, 1996; Lukas, 1999; Hill, 2007; Struck et ah, 2007], there are several suggestions regarding its etiology (e.g., to cure boredom, to taste an enjoyable food again, as a coping mechanism, etc.), making it difficult to eradicate. The functional significance of allogrooming is widely known as more than simple hygiene [Dunbar, 1991] and has been linked to the development of relationships and group formation, as it has shown to reduce negative outcomes [Baker and Aureli, 2000]. Given that these behaviors may serve as coping mechanisms, variations in frequency and duration may indicate a change in welfare conditions.
When managing animal introductions or other social issues (e.g., separating individuals to create a bachelor group), sustained restrictions on social groupings and available enclosure space are inevitable [e.g., McDonald, 1994; Brent et ah, 1997; Fritz and Howell, 2001; Seres et ah, 2001]. Despite the best efforts of care staff to minimize the impact of social upheavals and provide active and enriched lives for those going through the introduction process, these changes have a substantial impact on their physical and social opportunities. This study examines the impact of changes in available space and enclosure areas (number of separate rooms) for chimpanzees as two groups merged. Group mergers can prove acutely challenging for individuals and require careful monitoring, as many group size and enclosure availability changes take place during the process. We examined chimpanzee self-directed behaviors, and regurgitation/reingestion in varying combinations of enclosure number, size, and group density situations, to assess how these factors might impact upon welfare.
When considering available space in captivity, density studies are often at the forefront; however, the results of this study do not directly translate to previous group density research in terms of group size. While group composition frequently changed as a result of the introduction process, group composition in previous research remained constant [e.g., Nieuwenhuijsen and de Waal, 1982; Aureli and de Waal, 1997; Videan and Fritz, 2007]. Thinking of density in terms of low versus high amounts of space in addition to the number of individuals provides a broader understanding of how enclosure size and design relate to behavior.
Although the available space in terms of the number of areas and the m available varied during the introduction process, an analysis of group density across the number of available areas indicates that density alone does not explain our findings. Group density decreased from one to two areas, but remained comparable when comparing two to three areas, while behavioral changes (scratching and yawning) were only seen in the latter comparison, suggesting that those changes were a product of the number of accessible areas rather than absolute space available or density. Although high density situations can increase social tension [Aureli and de Waal, 1997] and the likelihood of social conflict [Judge, 2000], having an increased choice of different locations ameliorates the impact of social density and suggests that location preferences for social groupings may be a result of their visual proximity to other individuals.
We would expect allogrooming, an affiliative behav¬ior, to fluctuate in accordance with a known coping strategy to manage social density changes [e.g., de Waal, 1989]. Given the relative stability of density across the number of areas, however, the consistency of allogrooming shown in this study is fitting. As a result, we looked to known indicators of anxiety or uncertainty (SDBs) and an abnormal behavior (R/R) to identify the perception of available space in terms of the number of areas versus size of the accessible
While scratching and yawning decreased as the number of accessible enclosure areas increased (from two to three areas), scratching did not decrease as available space increased. This contradicts previous density research where both yawning and scratching increased when less space (high density) was available [Aureli and de Waal, 1997]. Since scratching did not decrease as available space (m ) increased and the observed behaviors did not increase or decrease over the introduction phases in a way that clearly reflected desensitization or sensitization to the introduction process, it suggests that having the choice of where to be or who to be with (particularly when three options are provided) is more important than the amount of space available or total density.
Choice and control are important aspects of animals' lives [Sambrook and Buchanan-Smith, 1997; Badihi, 2006; Meehan and Mench, 2007; Buchanan-Smith, 2010]. Previous research suggests that great apes avoid open spaces [Traylor-Holzer and Fritz, 1985; Ogden et ah, 1993; Stoinski et ah, 2002; Ross et ah, 2011] and exhibit preferences for enclosure elements that provide: oppor¬tunities to escape from conspecifics (doorways, even if they were closed), security (corners), or interaction with keepers (mesh walls [Ross and Lukas, 2006]). When individuals were allowed to choose to be together or in different areas, we saw a reduction in SDBs. Access to three areas, regardless of overall space, provided the greatest decrease in these behaviors suggesting that the ability to exhibit choice and preferences when it comes to their physical location plays an important role in the welfare of captive chimpanzees [e.g., Ross et ah, 2011].
Zoos are often restricted when it comes to the amount of space available for animal enclosures, but by working with what is available (or when designing new exhibits) and incorporating separate areas or perhaps visual barriers into enclosures, the concept of choice can be provided, potentially without the cost of a larger enclosure. While the impact of visual barriers was not specifically isolated in this study, they provide similar opportunities as separate areas (e.g., hide, reduce eye contact, etc.) and could be a low-cost option for alleviating the social pressure of space restrictions [e.g., Chamove et al., 1984; Reinhardt and Reinhardt, 1991; Westergaard et al., 1999; Stoinski et al., 2004; Coe et al., 2009]. This is not to suggest that the overall amount of space is irrelevant. While usable space should always be a consideration for the physical and psychological well-being of the species being housed [e.g., Ross andLukas, 2006; USDA and APHIS, 1991a,b], the number of separate areas within the enclosure during the introduction process also seems to be important for the psychological health of the animal.
With regards to R/R, no changes were seen in relation to the number of areas or available space. It is important to note that for the Beekse Bergen group (the only individuals in this study who exhibited R/R) nearly every aspect of their daily lives had recently changed and they were continually getting used to an unfamiliar environment, with both unfamiliar staff and chimpanzees. Although other behaviors were influenced by enclosure access, this might suggest that for this group of chimpanzees, space restrictions or coping mechanisms [Lukas, 1999] were not the underlying reasons behind their performance of R/R.
The variety of enclosure areas within Budongo Trail exhibit offered the residents many choices. The Beekse Bergen group could often be found in the smaller, off-exhibit area; their previous experiences in a laboratory environment likely determined their spatial decisions in the new enclosure [e.g., Novak et al., 1992; Duncan et al., 2013]. The freedom to choose to be in this preferred area might have assisted in their adjustment to life in the new enclosure and in the larger, integrated group. However, it can be difficult to disentangle additional influences such as the strengthening of existing close bonds within the original Beekse Bergen group [Schel et al., 2013] and preferences for different location characteristics (e.g., off-exhibit versus on-exhibit, small and enclosed versus large and open, concrete floors versus biofloors, etc.).
One challenging aspect of the choice concept is striking a balance between what is best for the animal, for example, tending to the animals' need for physical exercise and to benefit from being outdoors in nice weather (e.g., vitamin D from the sun) with their need to "feel safe" indoors in smaller areas. Although data measuring the impact of different life histories in relation to choice are lacking, there has been a recent focus on the long-term outcomes for chimpanzees with atypical life histories (e.g., former entertainment or pet chimpanzees [Ross and Vreeman, 2013]; former biomedical laboratory chimpanzees [Kalcher-Sommersguter et al., 2013]). The question of providing optimal levels of choice without compromising welfare is likely to be an on-going discussion and challenge for zoos and sanctuaries, particularly in relation to animals with atypical life histories. However, despite strong preferences for specific locations, there is no evidence suggesting that smaller enclosures could improve welfare [Ross et al., 2011].
1. Enclosure space is important to chimpanzees [Ross and Lukas, 2006; Ross et al., 2009], but the number of different areas is more important than the total amount of space during chimpanzee introductions.
2. When designing orrefitting enclosures, multiple areas should be provided to allow chimpanzees to exercise choice [Markowitz, 1982] over where they are and to whom they are near, particularly during animal management scenarios that involve space restrictions.
3. Increased flexibility, in terms of the potential configurations of access to multiple areas, is important for reducing the negative welfare impact of both short- and long-term animal management decisions.
4. While increased flexibility in enclosure choice might be an expected result for fission-fusion species like chimpanzees, given that captivity and the introduction process reduces social choices so greatly for most species, it is likely to be important for many other animals in captive environments.
Inhibition of social behavior in chimpanzees under high-density conditions
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