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«Item type Thesis or dissertation Authors Davis, Nicolas Citation Davis, N., Schaffner, C. M., & Smith, T. E. (2005). Evidence that zoo visitors ...»

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In contrast, the neuroendocrine system, which confers another biological response to stress, can have a broad and long lasting effect on the body. During periods of stress the HPA axis is stimulated, initially to produce corticotrophin releasing hormone (CRH) and vasopressin (AVP) from the hypothalamus. This in turn stimulates the release of adrenocorticotrophic hormone (ACTH) from the anterior pituitary gland, which leads to the production of glucocorticoids (GCs) (cortisol and corticosterone) from the adrenal cortex (Mormede, et al., 2007). They are responsible for nearly all the biological functions affected by stress, such as changes in the immune system, reproduction, metabolism and behaviour (Matteri, Caroll, & Dyer, 2000). Other endocrinological responses to stress include the secretion of prolactin, growth hormone, thyroid stimulating hormone and gonadotrophins. Finally, the immune system also responds directly to a stress response, and although this has yet to be fully understood, it provides a potentially powerful alternative tool to evaluate an animal’s response to stress (Honess, et al., 2005; Moberg, 2000).

The stress response can be considered adaptive, enabling animals to escape from or cope with a threat (Wiepkema & Koolhaas, 1993). Together, these biological responses are essential for surviving the regular exposure of various stressors (Sapolsky, 2004). Providing there are sufficient biological reserves to deal with the cost then there are no biological consequences of the stress response. If there are insufficient reserves to deal with the biological cost then the consequences are that resources will be shifted away from essential biological functions, and the animal will be left in what has been referred to as a prepathological state.

1.4.3 Distress and eustress Only when the stress response threatens the animal’s wellbeing does it experience ‘distress’. This term helps to differentiate between a non-threatening stress response and a biological state when the stressor starts having a negative impact on the individual’s welfare (Moberg, 2000).

While care should be taken to avoid unnecessary stressors in animals kept and managed in a captive environment some forms of stress are unavoidable, although not necessarily detrimental (Chamove & Moodie, 1990). Indeed, an animal living within its natural environment is often exposed to a variety of serious and potentially life threatening stressors (Sapolsky, 2000). These include hunger, thirst, injury through conspecific aggression or attempted predation and a variety of social stressors (Veasey, et al., 1996b). Animals maintained by human beings, whether as a pet, in a farm, laboratory or a zoo setting, normally benefit from regular provision of food, water, shelter and veterinary aid, factors that can reduce stress.

Not all stressors that evoke a stress response are detrimental to an individual.

A stress response can provide stimulation that is beneficial to the animal by optimising vigilance (Wiepkema & Koolhaas, 1993), facilitating the activation of reproduction (G. M. Barrett, Shimizu, Bardi, Asaba, & Mori, 2002; Engh, et al., 2006), enhancing learning, increasing alertness and exploration (Chamove & Anderson, 1989; Chamove & Moodie, 1990), and even improving immune responses in the short term (Ellard, Castle, & Mian, 2001). This ‘good stress’ may even be perceived as pleasurable, and as a concept has been described as ‘eustress’ (Selye, 1974). The difference between distress and eustress is biological cost. An animal has evolved to be able to cope with a short term stressor, such as an attack by a predator, providing the animal has enough reserve to cover the cost of the stressor (Sapolsky, 2000).

1.4.4 Acute and chronic stressors Generally the effects of chronic stress are more likely to have an impact on an animal’s welfare than acute stress (Lane, 2006). For example, chronic stress can make an animal more prone to infections due to suppression of the immune system, whereas an acute stressor actually enhances the immune function leading to a short term protection against disease (Lane, 2006).

Chronic stress is caused either by repeated exposure to the same stressor, or by simultaneous exposure to several active stressors, both of which must persist over a long period of time and whose accumulative biological cost initially forces the animal into sub clinical stress (Moberg, 2000). Under these conditions, although biological functions may not be affected, they make the animal more vulnerable to distress when exposed to a further stressor. Long-term chronic stress should be thought of as a series of repeated exposures to acute stressors, rather than a constant and unvarying condition (Ladewig, 2000). This has particular relevance for an animal that is kept in sub optimal conditions, such as inappropriate housing environments or social contexts leaving them more susceptible to another, normally innocuous stressor. Although long-term chronic stress is a more likely cause of distress, depending on its severity and timing, an acute stressor can also cause a major welfare problem (Lane, 2006; Moberg, 2000).

Acute stressors are short term and normally associated with an initial behavioural response of orientation, alarm and vigilance. Often they are easier to cope with as the animal may be successful in avoiding the stressor by simply removing itself from the threat (Moberg, 2000). Such a response will not be appropriate for all stressors or if the animal finds itself in a position where such behavioural options are restricted (Ladewig, 2000). Even when a behavioural response does not alleviate the stressor, a component of it may still be a part of the stress response and thus provide a potential clue to distress (Rushen, 2000).

However, insufficient understanding of the behaviour of animals during stress limits the value of using behaviour as a means of predicting distress.

All animals in captivity should have their stress levels managed, just as their nutrition or reproduction is managed (Moberg 1992, 1993). The strategy should be to minimise the biological costs of stress at all times and never allow it to rise above subclinical levels.

1.4.5 Social stressors While social groups provide the advantage of support and co-operation, there are also disadvantages of increased conflict and competition (Goymann & Wingfield, 2004; Kikusui, Winslow, & Mori, 2006). Research in non-human primates has shown that social stress is especially effective in producing chronic changes in the function of the HPA axis, although the effect is influenced by the species’ social organisation and an individual’s position within it (Engh, et al., 2006; Smith & French, 1997b; Ziegler, Scheffler, & Snowdon, 1995). For example, social instability, unnatural isolation, dominance, introductions and separations all demonstrate behavioural and physiological impacts on stress responses (Honess & Marin, 2006; Paker, Collins, Sindimwo, & Goodall, 1995; Sapolsky, 2005), although the responses differ widely across various species (Setchell, Smith, Wicking, & Knapp, 2008).

1.4.6 Environmental stressors Animals have adapted a variety of behavioural and physiological responses to deal with the diverse challenges that natural surroundings can offer (Morgan & Tromborg, 2007). When animals are kept in captivity their ability to deal with stressors can be affected if they are not allowed to or are unable to carry out these responses. The lack of complexity, restricted movement, lack of retreat space, forced proximity to humans, routine husbandry and restricted foraging have all been identified as potential environmental stressors for captive animals (Morgan & Tromborg, 2007).

A variety of studies examined various environmental features and their impact on animals in captivity. For example, the provision of appropriate substrates stimulates more natural foraging behaviour patterns (Beisner & Isbell, 2008;

Chamove, Anderson, Morgan-Jones, & Jones, 1982; Dawkins, 1983; Lutz & Novak, 1995). Studies assessing enclosure size (Clubb & Mason, 2007; Crockett, et al., 1995), environmental enrichment (Carlstead & Shepherdson, 2000; Schapiro, Bloomsmith, Kessel, & Shively, 1993), novelty (T. E. Smith, et al., 1998) and husbandry procedures and routines (Bassett & Buchanan-Smith, 2007; Line, Morgan, Markowitz, & Strong, 1989) have demonstrated that these also impact on the physiology and behaviour of captive animals. The prevention or interference by the captive environment on an animal’s ability to perform certain species-specific behaviours, for which animals may have a behavioural need, can also cause a stress response (Morgan & Tromborg, 2007).

Captive environments are generally less complex than natural habitats and consequently animals have a reduced amount of environmental control and an increased amount of predictability (Carlstead, 1996). It is this lack of control and variations in predictability that are potentially the greatest stressors for animals in captivity (Bassett & Buchanan-Smith, 2007; Sambrook & Buchanan-Smith, 1997;

Wiepkema & Koolhaas, 1993). The importance of predictability and control has been demonstrated in a classic study on rats (Rattus norvegicus) (Weiss, 1972). When two rats were subjected to a series of identical electric shocks, but one was able to predict and control the shock by means of a warning light and the use of an adjustable wheel, its GC response was significantly reduced.

1.4.7 Inter-individual variability Inter-individual variability to the stress response is well documented with different disease patterns resulting across animals experiencing the same stressor (Boccia, Laudenslager, & Reite, 1995; Moberg, 1985, 2000; Mormede, et al., 2007).

This variation is consistent and stable over time, and a given stress response style may remain characteristic to an individual over its lifetime (Pottinger, 2000). A number of factors that may contribute to this individual variation have been highlighted (Mormede, et al., 2007). They include: past experiences (Kikusui, et al., 2006; W. A. Mason, 2000), age (Honess & Marin, 2006a), social status (McGlone, et al., 1993), genetics (Pottinger, 2000), reproductive state (Cavigelli & Pereira, 2000;

Ziegler, Scheffler, & Snowdon, 1995), temperament (A. S. Clarke & Boinski, 1995;

Maestripieri, 2000), rearing history, (Boccia, Laudenslager, & Reite, 1995; Dettling, Feldon, & Pryce, 2002) and even time of year (Carlstead & Seidensticker, 1991).

While it may be possible to monitor individuals under carefully controlled laboratory conditions, even to the advantage of learning more about how the stress response is affected, it can be more difficult to know the past experience, social relationships or genetic predisposition to a stress response in a less controlled environment, such as a farm or a wild population (Mormede, et al., 2007).

Due to the high degree of individual variation to stressors it is better to use animals as their own control using repeated measures design (Honess & Marin, 2006a). As acute and chronic stress can both lead to negative effects on welfare the key to the use of GCs for assessment must lie in repeated sampling as a stand alone measure of GC can be misleading (Lane, 2006).

1.4.8 Measurement of the stress response While there are a variety of physiological and behavioural indicators that can be used for measuring an individual’s response to stress it is important to determine which methods are the most reliable, accurate and appropriate. It is therefore not expected that any particular indicator of stress will be appropriate for all types of stressors (Moberg, 2000). To complicate the matter further these systems can also often have similar responses to both harmful and innocuous stimuli.

Behavioural indices of stress are attractive as they are relatively easy, non invasive and inexpensive to obtain when compared to physiological measures.

Behaviour has also been considered to more accurately reflect the animals underlying dispositional state than physiological measures (Dawkins, 2004, 2006). Displacement behaviours, which are activities that are characterised by their apparent irrelevance to ongoing activities (Tinbergen, 1952), can also be used as indicators of an individual animal’s emotional state (Maestripieri, Schino, Aureli, & Troisi, 1992). In non human primates such behaviours include yawning, scratching, auto grooming and body shaking (O. N. Fraser, Stahl, & Aureli, 2008; Maestripieri, et al., 1992). The exhibition of these behaviours is consistently accompanied by physiological changes such as increases in heart rate, blood pressure and GCs, which are associated with a stress response. Pharmacological validation of displacement behaviour by using anxiety inducing and reducing drugs leads to corresponding increases and decreases in the rate of displacement behaviours, respectively (Barros, et al., 2007; Gabriele Schino, 1996). Further investigation is also required to associate the various behaviours and emotional states (Maestripieri, et al., 1992).

There are also a number of normally rare and distinctive behaviours whose presence is associated with extreme levels of stress in primates. These include selfmutilation and stereotypies and many studies have used them as indicators of high stress levels (Honess & Marin, 2006a). Another approach includes quantitative and qualitative changes in the overall behaviour repertoire (Rushen, 2000). However, the control of behaviour in response to stress is complex. Until the underlying causal mechanisms of behaviour during stress are fully understood they are difficult to interpret as a means of identifying stress. There is also no general behavioural stress response shown by an animal during stress, rather the behavioural response is specific to the stressor (Rushen, 2000). In non-human primates there is also evidence that increased locomotion may be part of a generalized stress response in some species (T. E. Smith, et al., 1998).

More invasive procedures are often used within laboratory settings. For example, the monitoring of autonomic stress responses, such as changes in heart rate or blood pressure, has been used in non human primates (Boccia, et al., 1995; S.

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