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Ganswindt, A., Palme, R., Heistermann, M., Borragan, S., & Hodges, J. K. (2003). Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen Comp Endocrinol, 134(2), 156–166.
Abstract: Adult male elephants periodically show the phenomenon of musth, a condition associated with increased aggressiveness, restlessness, significant weight reduction and markedly elevated androgen levels. It has been suggested that musth-related behaviours are costly and that therefore musth may represent a form of physiological stress. In order to provide data on this largely unanswered question, the first aim of this study was to evaluate different assays for non-invasive assessment of adrenocortical function in the male African elephant by (i) characterizing the metabolism and excretion of [3H]cortisol (3H-C) and [14C]testosterone (14C-T) and (ii) using this information to evaluate the specificity of four antibodies for determination of excreted cortisol metabolites, particularly with respect to possible cross-reactions with androgen metabolites, and to assess their biological validity using an ACTH challenge test. Based on the methodology established, the second objective was to provide data on fecal cortisol metabolite concentrations in bulls during the musth and non-musth condition. 3H-C (1 mCi) and 14C-T (100 microCi) were injected simultaneously into a 16 year old male and all urine and feces collected for 30 and 86 h, respectively. The majority (82%) of cortisol metabolites was excreted into the urine, whereas testosterone metabolites were mainly (57%) excreted into the feces. Almost all radioactive metabolites recovered from urine were conjugated (86% 3H-C and 97% 14C-T). In contrast, 86% and >99% of the 3H-C and 14C-T metabolites recovered from feces consisted of unconjugated forms. HPLC separations indicated the presence of various metabolites of cortisol in both urine and feces, with cortisol being abundant in hydrolysed urine, but virtually absent in feces. Although all antibodies measured substantial amounts of immunoreactivity after HPLC separation of peak radioactive samples and detected an increase in glucocorticoid output following the ACTH challenge, only two (in feces against 3alpha,11-oxo-cortisol metabolites, measured by an 11-oxo-etiocholanolone-EIA and in urine against cortisol, measured by a cortisol-EIA) did not show substantial cross-reactivity with excreted 14C-T metabolites and could provide an acceptable degree of specificity for reliable assessment of glucocorticoid output from urine and feces. Based on these findings, concentrations of immunoreactive 3alpha,11-oxo-cortisol metabolites were determined in weekly fecal samples collected from four adult bulls over periods of 11-20 months to examine whether musth is associated with increased adrenal activity. Results showed that in each male levels of these cortisol metabolites were not elevated during periods of musth, suggesting that in the African elephant musth is generally not associated with marked elevations in glucocorticoid output. Given the complex nature of musth and the variety of factors that are likely to influence its manifestation, it is clear, however, that further studies, particularly on free-ranging animals, are needed before a possible relationship between musth and adrenal function can be resolved. This study also clearly illustrates the potential problems associated with cross-reacting metabolites of gonadal steroids in EIAs measuring glucocorticoid metabolites. This has to be taken into account when selecting assays and interpreting results of glucocorticoid metabolite analysis, not only for studies in the elephant but also in other species.
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Zhang, T. - Y., Parent, C., Weaver, I., & Meaney, M. J. (2004). Maternal programming of individual differences in defensive responses in the rat. Ann N Y Acad Sci, 1032, 85–103.
Abstract: This paper describes the results of a series of studies showing that variations in mother-pup interactions program the development of individual differences in behavioral and endocrine stress responses in the rat. These effects are associated with altered expression of genes in brain regions, such as the amygdala, hippocampus, and hypothalamus, that regulate the expression of stress responses. Studies from evolutionary biology suggest that such “maternal effects” are common and often associated with variations in the quality of the maternal environment. Together these findings suggest an epigenetic process whereby the experience of the mother alters the nature of the parent-offspring interactions and thus the phenotype of the offspring.
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Detmer, D. (1992). Response: of pigs and primitive notions. Between Species, 8(4), 203–208.
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Graham, M., & Letz, R. (1979). Within-species variation in the development of ultrasonic signaling of preweanling rats. Dev Psychobiol, 12(2), 129–136.
Abstract: The development of litter and individual differences in the rate of ultrasonic signaling of neonatal rats was studied. Systematic variations among litters and individuals emerged, without differential treatment. These differences were not correlated with variations in general development as indexed by body weight. Two experiments using a cross-fostering design showed that litter differences developed independently of variations in postnatal environment. These results indicate that the variations among litters in ultrasound rate have a prenatal, possibly genetic, etiology and may represent reliable indicants of response to environmental stress.
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Reimers, M., Schwarzenberger, F., & Preuschoft, S. (2007). Rehabilitation of research chimpanzees: stress and coping after long-term isolation. Horm Behav, 51(3), 428–435.
Abstract: We report on the permanent retirement of chimpanzees from biomedical research and on resocialization after long-term social isolation. Our aim was to investigate to what extent behavioral and endocrine measures of stress in deprived laboratory chimpanzees can be improved by a more species-typical social life style. Personality in terms of novelty responses, social dominance after resocialization and hormonal stress susceptibility were affected by the onset of maternal separation of infant chimpanzees and duration of deprivation. Chimpanzees, who were separated from their mothers at a younger age and kept in isolation for more years appeared to be more timid personalities, less socially active, less dominant and more susceptible to stress, as compared to chimpanzees with a less severe deprivation history. However, permanent retirement from biomedical research in combination with therapeutic resocialization maximizing chimpanzees' situation control resulted in reduced fecal cortisol metabolite levels. Our results indicate that chimpanzees can recover from severe social deprivation, and may experience resocialization as less stressful than solitary housing.
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Overli, O., Korzan, W. J., Hoglund, E., Winberg, S., Bollig, H., Watt, M., et al. (2004). Stress coping style predicts aggression and social dominance in rainbow trout. Horm Behav, 45(4), 235–241.
Abstract: Social stress is frequently used as a model for studying the neuroendocrine mechanisms underlying stress-induced behavioral inhibition, depression, and fear conditioning. It has previously been shown that social subordination may result in increased glucocorticoid release and changes in brain signaling systems. However, it is still an open question which neuroendocrine and behavioral differences are causes, and which are consequences of social status. Using juvenile rainbow trout of similar size and with no apparent differences in social history, we demonstrate that the ability to win fights for social dominance can be predicted from the duration of a behavioral response to stress, in this case appetite inhibition after transfer to a new environment. Moreover, stress responsiveness in terms of confinement-induced changes in plasma cortisol was negatively correlated to aggressive behavior. Fish that exhibited lower cortisol responses to a standardized confinement test were markedly more aggressive when being placed in a dominant social position later in the study. These findings support the view that distinct behavioral-physiological stress coping styles are present in teleost fish, and these coping characteristics influence both social rank and levels of aggression.
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Abeyesinghe, S. M., Nicol, C. J., Wathes. C.M., & Randall, J. M. (2001). Development of a raceway method to assess aversion of domestic fowl to concurrent stressors. Behav. Process., 56(3), 175–194.
Abstract: The requirement for assessing the effects of stressor combinations in improving the welfare of animals has not been widely recognised. Knowledge of the effects of concurrent stressors is needed to improve environments such as transport, where animals are presented with many simultaneous challenges. However, no method for measuring the effects of different stressors with a common unit is currently available. A locomotor passive avoidance method was developed as a common currency measure of the aversion of domestic fowl to concurrent stressors, using vibrational and thermal stressors as an exemplar. Juvenile fowl, fasted overnight, were trained to run a raceway into a goal-box for small food rewards (FR1). When running consistently, the reinforcement schedule was superimposed with a FR5 treatment schedule (60 min confinement in the goal-box with either a control of no other stressors [N] or concurrent vibration and thermal stressors [VT]). Subsequent latency to return to the goal-box was recorded as a measure of aversion. The factors affecting bird response were addressed in a series of experiments to optimise the method and clarify interpretation of results. Pre-feeding (20% ration 2 h prior to testing) did not affect response, but increasing the number of treatment presentations facilitated learning and increased method sensitivity. Treatment responses were consistent across experiments; overall VT was avoided (P<0.001), but N was not. However, there was large individual variation in response to VT. A final experiment indicated that, given a visual discriminatory cue, birds were capable of learning the required association between entering the goal-box and receiving the treatment, suggesting that the delay responses were due to aversion rather than the immediate impact of treatment on ability to respond. Further work is required to test the singular stressors, but the method retains common currency potential for assessing aversion to multiple stressors.
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Aureli, F., & de Waal, F. B. (1997). Inhibition of social behavior in chimpanzees under high-density conditions. Am. J. Primatol., 41(3), 213–228.
Abstract: This is the first study to investigate the short-term effects of high population density on captive chimpanzees (Pan troglodytes). Subjects of the study were 45 chimpanzees living in five different groups at the Yerkes Regional Primate Research Center. The groups were observed under two conditions: 1) when they had access to both the indoor and outdoor sections of their enclosures; 2) during cold days when they were locked into the indoor runs, which reduced the available space by more than half. Under the high-density condition, allogrooming and submissive greetings decreased, but juvenile play increased. Remarkably, the rate of various forms of agonistic behavior, such as aggression, bluff charge, bluff display, and hooting, occurred less frequently under the high-density condition. This general decrease in adult social activity, including agonistic behavior, can be interpreted as an inhibition strategy to reduce opportunities for conflict when interindividual distances are reduced. This strategy is probably effective only in the short run, however. Behavioral indicators of anxiety, such as rough scratching and yawning, showed elevated rates, suggesting increased social tension under the high-density condition.
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Rietmann, T. R., Stuart, A. E. A., Bernasconi, P., Stauffacher, M., Auer, J. A., & Weishaupt, M. A. (2004). Assessment of mental stress in warmblood horses: heart rate variability in comparison to heart rate and selected behavioural parameters. Appl. Anim. Behav. Sci., 88(1-2), 121–136.
Abstract: The aim of the study was to investigate whether heart rate variability (HRV) could assess alterations of the autonomic nervous system (ANS) at different levels of excitement. The behavioural and physiological responses of 20 warmblood horses to a challenging ground exercise task were studied. Prior to the experiment, the horses were evaluated at rest and during forward walking (FW). The horses were then forced to move backwards continuously during 3 min according to a standardised protocol (BW1). Subsequently, the horses were exposed to two training sessions, after which the backward walking (BW2) was re-evaluated. Heart rate (HR) and HRV-parameters such as the standard deviation of the beat-to-beat intervals (SDRR), the low (LF; sympathetic tone) and high frequency (HF) component of HRV (HF; parasympathetic tone) and their ratio (LF/HF; index representing the sympatho-vagal balance) were sampled at rest, and during FW, BW1 and BW2. Stress-related behaviour during BW1 and BW2 was determined from video recordings. The results of the different evaluations were compared to each other. Compared to rest and FW, the first backward experiment induced a significant rise in HR, LF and LF/HF and a significant decrease of HF. SDRR decreased from both FW and rest with only the latter reaching significance. In BW2 after the training sessions, HR and the parameters of the sympathetic branch of the ANS (LF, LF/HF) were decreased and the vagal tone (HF) increased compared to BW1; all changes were significant. The duration of stress indicating behavioural patterns revealed also a significant decrease of excitement after the training, when backward walking did not differ from forward walking in any parameter. Correlations between HRV-parameters and stress indicating behaviour as well as HR were found. We conclude that the HRV-parameters LF and HF are valuable measures to quantify sympatho-vagal balance, which allows a more precise assessment of the responses of HR and SDRR to mental stress during low intensity exercise.
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Mendl, M. (1999). Performing under pressure: stress and cognitive function. Appl. Anim. Behav. Sci., 65(3), 221–244.
Abstract: The way in which cognitive functioning is affected by stressors is an important area of research for applied ethologists because stress caused by captive conditions may disrupt cognitive processes and lead to welfare and husbandry problems. Such problems may be minimised through an understanding of the links between stress and cognition. The effects of stress on cognitive function have been studied in disciplines ranging from human perceptual psychology to animal neuroscience. The aim of this paper is to provide an introduction to this research, focusing on the effects of stressors on attention, memory formation and memory recall. Findings from such a diverse literature with little apparent inter-disciplinary communication are inevitably complex and often contradictory. Nevertheless, some generalities do emerge. The idea that an inverted U-shaped relationship exists between an individual's state of stress or arousal and its ability to perform a cognitive task effectively, the so-called Yerkes-Dodson law, is commonly encountered. The law has limited explanatory value because it is unlikely that different stressors act on cognitive function via the same intervening, non-specific state. Furthermore, the law only provides a very general description of the relationship between stress and cognitive function. Empirical research on attention and memory processes reveals more specific findings. Stressors appear to cause shifts, lapses and narrowing of attention, and can also influence decision speed. These processes may be viewed as serving an adaptive role helping the animal to search for and scrutinise a source of danger. There is conflicting evidence as to whether hormones involved in the hypothalamic-pituitary-adrenal stress response play a part in these processes. These hormones and those involved in the sympathetic-adrenomedullary stress response do appear to play an important role in memory formation. Low or moderate concentrations of circulating glucocorticoids and catecholamines can enhance memory formation, while excessively high or prolonged elevations of these hormones can lead to memory disruption. The effects of stressors on memory recall are less clear. There is evidence for disruptive effects, and for facilitatory effects indicating state-dependent memory recall; events experienced under conditions of high arousal may be best recalled under similar conditions. Applied ethologists have the opportunity to extend work in this area, which often involves studies of single stressors/stress hormones acting in isolation and limited measures of cognitive function, by focusing on real-life husbandry stressors encountered by captive animals. This will yield fundamental information which also has direct relevance to animal welfare and management issues.
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