Relation between the level of self-mutilation and theconcentration of fecal metabolites of glucocorticoids incaptive chimpanzees (Pan troglodytes)

Relação do grau de automutilação com as concentrações de metabólitos fecais de glicocorticoides em chimpanzés (Pan troglodytes)

Cristiane S. Pizzutto Manuela G.F.G. Sgai Danielle A. Lopes Cecília Pessutti Adauto Nunes Priscila V. Furtado Cláudio A. de Oliveira Marcelo A.B.V. Guimarães About the authors

Abstracts

The influence of stress in an environment, according with the behavioral and endocrine variables of primates, are increasingly being studied by a diversity of authors, and have shown that abnormal behaviors associated with increased glucocorticoids may be directly related with the impairment of their well-being. In this work were used 22 adult chimpanzees (Pan troglodytes), 11 males and 11 females, kept in captivity in three different institutions. All animals had their behavior registered by focal session using a 30 seconds sample interval, during six months, totaling 4,800 registries per each animal. During this period, fecal samples were collected 3 times a week for the extraction and measurement of the concentration of fecal metabolites of glucocorticoid by radioimmunoassay. Of the total observed, stereotypical behaviors represented 13,45±2.76%, and among them, self-mutilation represented 38.28±3.98 %. The animals were classified into three different scores, according with the percentage of body surface with alopecia due to self-mutilation. It was found a positive correlation of high intensity between the scores of alopecia due to the observed mutilation and the average concentrations of fecal metabolites of glucocorticoids. This result strongly suggests that this measurement of self-mutilation in a chimpanzee can be used as an important auxiliary tool to evaluate de conditions of adaptation of an animal in captivity, functioning as a direct indicator of the presence of chronic stress.

Chimpanzee; Pan troglodytes; self-mutilation; glucocorticoid fecal metabolites; captivity.


A influência do estresse de um ambiente nas variáveis endócrino-comportamentais de primatas vem sendo cada vez mais estudada por diversos autores, e mostram que comportamentos anormais associados a aumentos de glicocorticóides podem estar diretamente relacionados ao comprometimento do bem-estar. Neste trabalho foram utilizados 22 chimpanzés (Pan troglodytes) adultos, sendo 11 machos e 11 fêmeas mantidos em cativeiro de três instituições diferentes. Todos os animais tiveram seus comportamentos registrados pelo método de amostragem focal por intervalo de tempo, durante seis meses, totalizando 4800 registros para cada animal. Amostras fecais foram coletadas três vezes por semana, durante este período, para extração e dosagem de metabólitos fecais de glicocorticoides por radioimunoensaio. Os comportamentos estereotipados representaram 13,45+2,76% do total observado, sendo que dentre estes comportamentos a automutilação representou 38,28+3,98%. Os animais foram classificados em três graus diferentes, de acordo com o percentual da superfície corpórea com alopecia decorrente da automutilação. Foi encontrada uma correlação positiva de intensidade forte entre os graus de alopecia decorrentes de mutilação observados e as médias de concentrações de metabólitos fecais de glicocorticoides. Este resultado sugere fortemente que esta graduação de automutilação de um chimpanzé possa ser utilizada como uma ferramenta auxiliar importante nas avaliações das condições de adaptação do animal ao cativeiro, atuando como um indicador indireto da presença de estresse crônico.

Chimpanzé; Pan troglodytes; automutilação; metabólitos fecais de glicocorticóides; cativeiro.


Introduction

For decades the concern about the effects of the interaction between the environment and the organisms has held the attention of researchers Worldwide. The question of how to define and quantify animal welfare is still under constant debate.

Typically, for vertebrates, the habitats are not static and the animals have to adapt to situations predicted by physiological, morphological and behavioral changes. Components that are not predictable promote the so-called "state of emergency", which results in changes in the endocrine and metabolic parameters of an organism (Möstl & Palme 2002Möstl E. & Palme R.2002. Hormones as indicators of stress. Domest. Anim. Endocrinol. 23:67-74.).

Captive environments show commonly restricted and invariant stimuli (Paquette & Prescott 1988Paquette D. & Prescott J. 1988. Use of novel objects to enhance environments of captive chimpanzees. Zoo Biol. 7:15-23.) and are largely responsible for the development of chronic stress (characterized by prolonged periods of high concentrations of glucocorticoids) or intermittent (Carlstead et al. 1992Carlstead K., Brown J.L., Monfort S.L., Killens R. & Wildt D.E. 1992. Validation of a urinary cortisol radioimmunoassay for non-invasive monitoring of adrenal activity in domestic and non-domestic fields. Zoo Biol. 11:165-176.). This condition can have high costs for the animals, such as decreased individual fitness by immune suppression and tissue atrophy, decreased reproductive function (Gronli et al. 2005Gould E. & Bress M. 1986. Regurgitation and reingestion in captive gorilla: description and intervention. Zoo Biol. 5:241-250., Peel et al. 2005Palme R.2005b. Measuring fecal steroids - Guidelines for practical application. Ann.N.Y. Acad. Sci. 1046:75-80.) and promote behavioral changes, also known as stereotypies (Mason 1991Mason G.J.1991. Stereotypies: a critical review. Anim. Behav. 41:1015-1037., Carlstead et al. 1992Carlstead K., Brown J.L., Monfort S.L., Killens R. & Wildt D.E. 1992. Validation of a urinary cortisol radioimmunoassay for non-invasive monitoring of adrenal activity in domestic and non-domestic fields. Zoo Biol. 11:165-176., McBride & Cuddelford 2001McBride S.D. & Cuddelford D. 2001. The putative welfare reducing effects of preventing equine stereotypic behavior. Anim. Welf. 10:173-189.).

Several aspects may predispose stereotypic behavior, such as a genetic component (Schoenecker & Heller 2000Pizzutto C.S., Sgai M.G.F.G., Viau P., Chelini M.O.M., Oliveira C.A. & Guimarães M.A.B. 2008. Validação laboratorial e fisiológica de conjunto comercial para a quantificação de corticóides fecais em chimpanzé (Pan troglodytes) e orangotango (Pongo pygmaeus), cativos e submetidos a enriquecimentos ambientais. Braz. J. Vet. Res. Anim. Sci. 45(1):104-110., Schwaibold & Pillay 2001Schoenecker B. & Heller K.E. 2000. Indication of a genetic basis of stereo- typies in laboratory-bred bank voles (Clethrionomys glareolus). Appl. Anim. Behav. Sci. 68:339-347.) and separation or inadequate maternal care (Lutz et al. 2003Latham N.R. & Mason G.J. 2008. Maternal deprivation and the development of stereotypic behaviour. Appl. Anim. Behav. Sci. 110:84-108., Novak 2003Novak M. A.2003. Self-injurious behavior in rhesus monkeys: new insights into its etiology, physiology, and treatment. Am. J. Primatol. 59:3-19., Novak et al. 2006Novak M. A.2003. Self-injurious behavior in rhesus monkeys: new insights into its etiology, physiology, and treatment. Am. J. Primatol. 59:3-19., Latham & Mason 2008Ferdowsian H.R., Durham D.L., Kimwele C., Kranendonk G., Otali E., Akugizibwe T., Akugizibwe T., Mulcahy J.B., Ajarova L. & Johnson C.M. 2011. Signs of mood and anxiety disorders in chimpanzees. PLoS One 6(6):e19855.). The most commonly cited etiology is associated with the type of enclosure (Marriner & Drickmer 1994Mallapur A. & Chellam R. 2002. Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in Southern India. Zoo Biol. 21:585-595., Nash, Fritz & Alford 1999Murray C.M., Heintz M.R., Lonsdorf E.V., Parr L.A. & Santymire R.M. 2013. Validation of a Field Technique and Characterization of Fecal Glucocorticoid Metabolite Analysis in Wild Chimpanzees (Pan troglodytes). Am. J. Primatol. 75:57-64., Mallapur & Chellan 2002Mallapur A. & Chellam R. 2002. Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in Southern India. Zoo Biol. 21:585-595.), such as the size and complexity of the environment (Macedonia 1987Lyons J., Young R.J. & Deag J.M. 1997. The effects of physical characteristics of the environment and feeding regime on the behavior of captive felids. Zoo Biol. 16:71-83., Lyons, Young & Deag 1997Lutz C.K., Well A. & Novak M. 2003. Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience. Am. J. Primatol. 60:1-15.), lack of stimuli (Meehan, Garner & Mench 2004McBride S.D. & Cuddelford D. 2001. The putative welfare reducing effects of preventing equine stereotypic behavior. Anim. Welf. 10:173-189., Swaisgood & Shepherdson 2006Sgai M.G.F.G., Pizzutto C.S.& Guimarães M.A.B. V.2010. Estresse, estereotipias e enriquecimento ambiental em animais selvagens cativos: revisão. Clín. Vet. 88:88-98.) or lack of proper socialization (Bellanca & Crockett 2002Bellanca R.U. & Crockett C.M. 2002. Factors predicting increased incidence of abnormal behavior in male pigtailed macaques. Am. J. Primatol. 58:57-69., Lutz et al. 2003Latham N.R. & Mason G.J. 2008. Maternal deprivation and the development of stereotypic behaviour. Appl. Anim. Behav. Sci. 110:84-108., Novak 2003Nash L.T., Fritz J., Alford P.A. & Brent L. 1999. Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes). Am. J. Primatol. 48:15-29.).

The stereotypical behaviors may manifest themselves differently depending on the species or the individual (Coleman & Maier 2010Coleman K. & Maier A. 2010. The use of positive reinforcement training to reduce stereotypic behavior in rhesus macaques. Appl. Anim. Behav. Sci. 124:142-148., Würbel et al. 2006Würbel H., Bergeron R. & Cabib S. 2006. The coping hypothesis of stereotypic behavior, p.14-15. In: Mason G.J.& Rushen J. (Eds), Stereotypic Animal Behaviour: fundamentals and applications to welfare. CABI,Oxfordshire.). Shepherdson (1998)Schwaibold U. & Pillay N. 2001. Stereotypic behaviour is genetically transmitted in the African striped mouse Rhabdomys pumilio. Appl. Anim. Behav. Sci. 74:273-280. stated that stereotypies can be quantitative, such as hyperactivity, or qualitative. As examples, one can cite the behaviors that the individual would not show in nature, such as walking aimless, false chewing, drinking water excessively, foraging even after feeding (Mason 1991Mason G.J.1991. Stereotypies: a critical review. Anim. Behav. 41:1015-1037.), masturbation, food regurgitation followed by re-ingestion (Gould & Bress 1986Dickie L. 1998. Environmental enrichment for old world primates with references to the primate collection at Edinburgh zoo. Int. Zoo Yearb. 36:131-139., Dickie 1998Dickie L. 1998. Environmental enrichment for old world primates with references to the primate collection at Edinburgh zoo. Int. Zoo Yearb. 36:131-139.), coprophagy (Akers & Schildkraut 1985Akers J.S. & Schildkraut D.S. 1985. Regurgitation/reingestion and copraphagy in captive gorillas, Zoo Biol. 4:99-109.), pacing (Boorer 1972Boorer M.K. 1972. Some aspects of stereotyped patterns of movement exhibited by zoo animals. Int. Zoo Yearbook 12:164-168.) and self-addressed, such as self-mutilation.

Self-mutilation has been widely studied as an abnormal behavior in chimpanzees (Birkett & Fisher-Newton 2011Birkett L.P. & Fisher-Newton N.E. 2011. How abnormal is the behaviour of captive, zoo-living chimpanzees? PLoS ONE 6(6):e20101., Ferdowsian 2011Gronli J., Murison R., Fiske E., Bjorvatn B., Sorensen E., Portas C.M. & Ursin R. 2005. Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol. Behav. 84:571-577.) and quantitative studies of these behaviors can demonstrate the effects of captivity among this specie (Birkett & Fisher-Newton 2011Birkett L.P. & Fisher-Newton N.E. 2011. How abnormal is the behaviour of captive, zoo-living chimpanzees? PLoS ONE 6(6):e20101.).

The association of behavioral and endocrine methods of study enables greater efficiency for the evaluation of stress intensity (Sgai et al. 2010Shepherdson D.J. 1998. Tracing the path of environmental enrichment in zoos, p.1-12. In:, Shepherdson D.J. Mellen J.D. & Hutchins M. (Eds), Second Nature: environmental enrichment for captive animals. Smithsonian Institution Press, Washington, DC.). The concentration of glucocorticoids in plasma is widely used as one indicator of the presence of stressors. In light of the fact that blood sampling may also be dangerous or even impossible in some zoo and wildlife species, noninvasive methods for measuring glucocorticoids or their metabolites seem desirable for assessing adrenocortical function in animals (Palme 2005aPalme R., Rettenbacher S., Touma C., El-Bahr S.M. & Mostl E.2005a. Stress hormones in mammals and birds: Comparative aspects regarding metabolism, excretion and non- invasive measurement in fecal samples. Ann. N. Y. Acad. Sci. 1040:162-171.) and has been used with primates (Bahr et al. 2000Bahr N.I., Palme R., Möhle U., Hodges J.K. & Heistermann M. 2000. Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates. Gen. Comp. Endocrinol. 117:427-438., Murray et al. 2013Möstl E. & Palme R.2002. Hormones as indicators of stress. Domest. Anim. Endocrinol. 23:67-74.).

Noninvasive methods of measuring fecal steroid metabolites to assess an animal's endocrine status are now widely used to investigate hormone-behavior relationships, as well as questions in the fields of reproduction, animal welfare, ecology, conservation biology, and biomedicine (Palme 2005bPalme R., Rettenbacher S., Touma C., El-Bahr S.M. & Mostl E.2005a. Stress hormones in mammals and birds: Comparative aspects regarding metabolism, excretion and non- invasive measurement in fecal samples. Ann. N. Y. Acad. Sci. 1040:162-171.).

This way, the objective of this study was to analyze a possible relation between the level of self-mutilation and the concentration of fecal metabolites of glucocorticoids in captive chimpanzees.

Materials and Methods

In this study 22 adult chimpanzees (Pan troglodytes) were used, 11 males and 11 females, kept in captivity, They came from three different institutions, two zoos and one private facility, the environmental enrichment program of which was not followed in the routine management of the animals. At the zoos the animals were kept in pairs, in areas of about 100m2, and at the private facility, they were kept in individual enclosures, with areas of 25m2. The diet at those three institutions was based on fruits, vegetables and protein items, offered twice a day, every day.

All chimpanzees had their behaviors recorded by focal session using a 30 seconds intersample interval (Altmann 1974Altmann J. 1974. Observation study of behavior: sampling methods. Behaviour 49:227-267., Martin & Bateson 1993Marriner L.M. & Drickamer L.C. 1994. Factors influencing stereotyped behavior of primates in a zoo.Zoo Biol. 13:267-275.), with recordings every 30 seconds in 30-minute sessions, in the morning (8:00 - 11:00 a.m.), time of greatest activity of the animals (determinated by implementation of peak activity), totalizing 40 hours for each animal with 4,800 records during six months. All recordings were made in spreadsheets by a single observer, during exposure of the animal to the public, three times a week.

Individual ethograms were prepared, however for this work, just information related to self-mutilation were used. The degree of self-mutilation was classified into three scores, according to the percentage of alopecia along the body surface, ranging from 0 to 2 (Fig.1):

Fig.1:
Schematic figure showing different levels of self-mutilation (Score 0 = Absence of areas without hair; Score1 = Areas with alopecia in up to approximately 30% of body surface, reaching upper limbs, scapular region and lower limbs; Score 2 = Areas with alopecia in more than 30% of body surface, reaching upper limbs, scapular region, lower limbs, chest, dorsum, cervical area and head) of chimpanzees (Pan troglodytes), front and dorsal view.

- Score 0: Absence of areas without hair;

- Score1: Areas with alopecia in up to approximately 30% of body surface, reaching upper limbs, scapular region and lower limbs;

- Score 2: Areas with alopecia in more than 30% of body surface, reaching upper limbs, scapular region, lower limbs, chest, dorsum, cervical area and head.

All chimpanzees had fecal samples collected during six months. The samples were collected three times a week, in early morning (between 8:00 and 10:00 am), homogenized and packed in plastic bags like "Ziploc". After identification with date and time of harvesting, samples were then kept in a freezer at -20°C until processed at the Laboratory of Hormonal Dosages of the Department of Animal Reproduction, Faculty of Veterinary Medicine, University of São Paulo.

The extraction of metabolites was performed according to the recommended technique by Whitten et al. (1998)Swaisgood R. & Shepherdson D. 2006. Environmental enrichment as a strategy for mitigating stereotypies in zoo animals: a literature review and meta-analysis, p.256-285. In: Mason G.J.& Rushen J. (Eds), Stereotypic Animal Behaviour: fundamentals and applications to welfare. CABI, Oxfordshire. for chimpanzees (Pan troglodytes) feces. For the dosing of the glucocorticoids metabolites, it was used the commercial kit for measurement of corticosterone of double antibody (Corticosterone(r) MP Biomedical - New York), previously validated by Pizzutto et al. (2008)Peel A.J., Vogelnest L., Finnigan M., Grossfeldt L. & O'Brien J.K. 2005. Non-invasive fecal hormone analysis and behavioral observations for monitoring stress responses in captive western lowland gorillas (Gorilla gorilla gorilla). Zoo Biol. 24:431-445..

Statistical analysis

The frequency of occurrence (%) of self-mutilation behavior was calculated in relation to the total number of behavioral records for each animal, as well as the frequencies for each degree of self-mutilation. There were calculated the means and the standard deviations of the concentration of fecal glucocorticoid metabolites of all animals within each degree of mutilation. The results were tested for normality using the method of Kolmogorov-Smirnov, and for homogeneity of variances using the method of Bartlett, in order to characterize them as parametric. Means were then compared by the ANOVA test, complemented by Tukey Test, both with p<0.05. The concentrations of the hormone metabolites were correlated with the degree of mutilation using the Pearson's correlation test, with p<0.05.

The present study was approved by the Bioethics Commission of the School of Veterinary Medicine and Animal Science, São Paulo University (FMVZ-USP), Brazil under procedure number 413/2004.

Results

From the 4,800 behavioral records for each chimpansee, a repertoire was obtained of 19 different behaviors. The abnormal behaviors observed had a frequency of occurrence of 13.45±2.76%, and among them, self-mutilation represented 38.28±3.98% of those abnormal behaviors.

From the 22 chimpanzees studied, 20 presented some level of self-mutilation and were classified as: 2 animals with score 0; 15 animals with score 1; and 5 animals with score 2.

The quality control of the assays performed to measure the concentrations of glucocorticoid fecal metabolites showed the following results: coefficients of variation inter-assay: 12.75%, intra-assay: 2.21% and minimum sensitivity detected: 2.55ng/dl.

Mean concentrations of glucocorticoid fecal metabolites found in three different scores of self-mutilation were: 34.65±9.35, 90.34±29.08 and 138.82±38.45ng/g of dry feces for scores 0, 1 and 2 respectively, showing significant differences (Fig.2).

Fig.2:
Means and SD of concentrations of fecal metabolites of glucocorticoids in different scores of self-mutilation in captive chimpanzees (Pan troglodytes). (*Different superscript letters denote significancy at P<0,05).

It was found a positive correlation of high intensity (0.82), p<0,0001 between the means of glucocorticoid fecal metabolites concentrations and the different scores of self-mutilation.

Discussion

Self-mutilation presented the highest frequency of occurrence of abnormal behaviors (mean 38.28% ± 3.98), in contrast with the findings of Ferdowsian (2011)Gronli J., Murison R., Fiske E., Bjorvatn B., Sorensen E., Portas C.M. & Ursin R. 2005. Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol. Behav. 84:571-577., in which coprophagy was the abnormal behavior with a higher prevalence. The frequency of occurrence of abnormal behaviors (13.45% ±2.76), can also be considered higher comparing to the findings by Bloomsmith and Lambet (1995)Bloomsmith M.A. & Lambeth S.P. 1995. Effects of predictable versus unpredictable feeding schedules on chimpanzee behaviour. Appl. Anim. Behav. Sci. 44:65-74. and Ferdowsian (2011)Gronli J., Murison R., Fiske E., Bjorvatn B., Sorensen E., Portas C.M. & Ursin R. 2005. Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol. Behav. 84:571-577. however, no work had previously related the occurrence of abnormal behaviors with concentrations of glucocorticoids. The high positive correlation found between the means of concentrations of glucocorticoid fecal metabolites and the different scores of self-mutilation, suggested that this kind of lesion can be associated to a chronic stress situation and consequent dysfunctional behavior. These results showed that chimpanzees subjected to captive environments with poor quality stimuli may develop a pattern of qualitative stereotypical behavior as described by Swaisgood and Shepherdson (2006)Sgai M.G.F.G., Pizzutto C.S.& Guimarães M.A.B. V.2010. Estresse, estereotipias e enriquecimento ambiental em animais selvagens cativos: revisão. Clín. Vet. 88:88-98. and this can be directly related to the endocrine-physiological response of the animal against a condition of difficult adaptation. It could represent the specie adaptive-biological-cost due to the conditions of captivity.

In this study, it was not compared the different levels of mutilation according to age, sex or animal individual history, based in Birkett & Fisher-Newton (2011)Birkett L.P. & Fisher-Newton N.E. 2011. How abnormal is the behaviour of captive, zoo-living chimpanzees? PLoS ONE 6(6):e20101. when he found no difference between these variables for the study of abnormal behaviors in chimpanzees. To our knowledge, this is the first study establishing a relationship between cutaneous lesions, stereotypical behavior and concentrations of glucocorticoid fecal metabolites in chimpanzees, suggesting a chronic stress captive related situation.

Conclusions

In this study was found a relationship between the means of concentrations of glucocorticoid fecal metabolites and the different scores of self-mutilation.

These results strongly suggest that the level of self-mutilation can be used as a tool to help important evaluations of the conditions for animal adaptation in captivity, acting as an indicator of chronic stress in chimpanzees.

Acknowledgements

The Foundation for Research Support of São Paulo State (FAPESP) for the financial support given to the project.

  • Altmann J. 1974. Observation study of behavior: sampling methods. Behaviour 49:227-267.
  • Akers J.S. & Schildkraut D.S. 1985. Regurgitation/reingestion and copraphagy in captive gorillas, Zoo Biol. 4:99-109.
  • Bahr N.I., Palme R., Möhle U., Hodges J.K. & Heistermann M. 2000. Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates. Gen. Comp. Endocrinol. 117:427-438.
  • Bellanca R.U. & Crockett C.M. 2002. Factors predicting increased incidence of abnormal behavior in male pigtailed macaques. Am. J. Primatol. 58:57-69.
  • Birkett L.P. & Fisher-Newton N.E. 2011. How abnormal is the behaviour of captive, zoo-living chimpanzees? PLoS ONE 6(6):e20101.
  • Bloomsmith M.A. & Lambeth S.P. 1995. Effects of predictable versus unpredictable feeding schedules on chimpanzee behaviour. Appl. Anim. Behav. Sci. 44:65-74.
  • Boorer M.K. 1972. Some aspects of stereotyped patterns of movement exhibited by zoo animals. Int. Zoo Yearbook 12:164-168.
  • Carlstead K., Brown J.L., Monfort S.L., Killens R. & Wildt D.E. 1992. Validation of a urinary cortisol radioimmunoassay for non-invasive monitoring of adrenal activity in domestic and non-domestic fields. Zoo Biol. 11:165-176.
  • Coleman K. & Maier A. 2010. The use of positive reinforcement training to reduce stereotypic behavior in rhesus macaques. Appl. Anim. Behav. Sci. 124:142-148.
  • Dickie L. 1998. Environmental enrichment for old world primates with references to the primate collection at Edinburgh zoo. Int. Zoo Yearb. 36:131-139.
  • Gould E. & Bress M. 1986. Regurgitation and reingestion in captive gorilla: description and intervention. Zoo Biol. 5:241-250.
  • Gronli J., Murison R., Fiske E., Bjorvatn B., Sorensen E., Portas C.M. & Ursin R. 2005. Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol. Behav. 84:571-577.
  • Ferdowsian H.R., Durham D.L., Kimwele C., Kranendonk G., Otali E., Akugizibwe T., Akugizibwe T., Mulcahy J.B., Ajarova L. & Johnson C.M. 2011. Signs of mood and anxiety disorders in chimpanzees. PLoS One 6(6):e19855.
  • Latham N.R. & Mason G.J. 2008. Maternal deprivation and the development of stereotypic behaviour. Appl. Anim. Behav. Sci. 110:84-108.
  • Lutz C.K., Well A. & Novak M. 2003. Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience. Am. J. Primatol. 60:1-15.
  • Lyons J., Young R.J. & Deag J.M. 1997. The effects of physical characteristics of the environment and feeding regime on the behavior of captive felids. Zoo Biol. 16:71-83.
  • Macedonia J.M. 1987. Effects of housing differences upon activity budgets in captive sifakas (Propithecus verreauxi). Zoo Biol. 6: 55-67.
  • Mallapur A. & Chellam R. 2002. Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in Southern India. Zoo Biol. 21:585-595.
  • Marriner L.M. & Drickamer L.C. 1994. Factors influencing stereotyped behavior of primates in a zoo.Zoo Biol. 13:267-275.
  • Martin P. & Bateson P. 1993. Measuring behaviour: an introductory guide. 2nd ed. Cambridge University Press, Cambridge. 222p.
  • Mason G.J.1991. Stereotypies: a critical review. Anim. Behav. 41:1015-1037.
  • McBride S.D. & Cuddelford D. 2001. The putative welfare reducing effects of preventing equine stereotypic behavior. Anim. Welf. 10:173-189.
  • Meehan C.L., Garner J.P. & Mench J.A. 2004. Environmental enrichment and development of cage stereotypy in Orange-winged Amazon par- rots (Amazona amazonica). Dev. Psychobiol. 44:209-218.
  • Möstl E. & Palme R.2002. Hormones as indicators of stress. Domest. Anim. Endocrinol. 23:67-74.
  • Murray C.M., Heintz M.R., Lonsdorf E.V., Parr L.A. & Santymire R.M. 2013. Validation of a Field Technique and Characterization of Fecal Glucocorticoid Metabolite Analysis in Wild Chimpanzees (Pan troglodytes). Am. J. Primatol. 75:57-64.
  • Nash L.T., Fritz J., Alford P.A. & Brent L. 1999. Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes). Am. J. Primatol. 48:15-29.
  • Novak M. A.2003. Self-injurious behavior in rhesus monkeys: new insights into its etiology, physiology, and treatment. Am. J. Primatol. 59:3-19.
  • Novak M. A., Meyer J.S., Lutz C. & Tiefenbacher S. 2006. Deprived environments: developmental insights from primatology, p.153-189. In: Mason G. & Rushen J. (Eds), Stereotypic Animal Behavior: Fundamentals and Applications to Welfare. CABI, Oxfordshire.
  • Paquette D. & Prescott J. 1988. Use of novel objects to enhance environments of captive chimpanzees. Zoo Biol. 7:15-23.
  • Palme R., Rettenbacher S., Touma C., El-Bahr S.M. & Mostl E.2005a. Stress hormones in mammals and birds: Comparative aspects regarding metabolism, excretion and non- invasive measurement in fecal samples. Ann. N. Y. Acad. Sci. 1040:162-171.
  • Palme R.2005b. Measuring fecal steroids - Guidelines for practical application. Ann.N.Y. Acad. Sci. 1046:75-80.
  • Peel A.J., Vogelnest L., Finnigan M., Grossfeldt L. & O'Brien J.K. 2005. Non-invasive fecal hormone analysis and behavioral observations for monitoring stress responses in captive western lowland gorillas (Gorilla gorilla gorilla). Zoo Biol. 24:431-445.
  • Pizzutto C.S., Sgai M.G.F.G., Viau P., Chelini M.O.M., Oliveira C.A. & Guimarães M.A.B. 2008. Validação laboratorial e fisiológica de conjunto comercial para a quantificação de corticóides fecais em chimpanzé (Pan troglodytes) e orangotango (Pongo pygmaeus), cativos e submetidos a enriquecimentos ambientais. Braz. J. Vet. Res. Anim. Sci. 45(1):104-110.
  • Schoenecker B. & Heller K.E. 2000. Indication of a genetic basis of stereo- typies in laboratory-bred bank voles (Clethrionomys glareolus). Appl. Anim. Behav. Sci. 68:339-347.
  • Schwaibold U. & Pillay N. 2001. Stereotypic behaviour is genetically transmitted in the African striped mouse Rhabdomys pumilio. Appl. Anim. Behav. Sci. 74:273-280.
  • Shepherdson D.J. 1998. Tracing the path of environmental enrichment in zoos, p.1-12. In:, Shepherdson D.J. Mellen J.D. & Hutchins M. (Eds), Second Nature: environmental enrichment for captive animals. Smithsonian Institution Press, Washington, DC.
  • Sgai M.G.F.G., Pizzutto C.S.& Guimarães M.A.B. V.2010. Estresse, estereotipias e enriquecimento ambiental em animais selvagens cativos: revisão. Clín. Vet. 88:88-98.
  • Swaisgood R. & Shepherdson D. 2006. Environmental enrichment as a strategy for mitigating stereotypies in zoo animals: a literature review and meta-analysis, p.256-285. In: Mason G.J.& Rushen J. (Eds), Stereotypic Animal Behaviour: fundamentals and applications to welfare. CABI, Oxfordshire.
  • Whitten P.L., Stavisky R., Aureli F. & Russel E. 1998. Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). Am. J. Primatol. 44:57-69.
  • Würbel H., Bergeron R. & Cabib S. 2006. The coping hypothesis of stereotypic behavior, p.14-15. In: Mason G.J.& Rushen J. (Eds), Stereotypic Animal Behaviour: fundamentals and applications to welfare. CABI,Oxfordshire.

Publication Dates

  • Publication in this collection
    Jan 2015

History

  • Received
    04 Apr 2014
  • Accepted
    19 Dec 2014
Colégio Brasileiro de Patologia Animal - CBPA Pesquisa Veterinária Brasileira, Caixa Postal 74.591, 23890-000 Rio de Janeiro, RJ, Brasil, Tel./Fax: (55 21) 2682-1081 - Rio de Janeiro - RJ - Brazil
E-mail: pvb@pvb.com.br