This article is one of thousands of articles on the web describing Chimpanzees being used in experiments to benefit humans. Is it worth the suffering that might be caused in some of the experiments?
Background
In humans, traumatic experiences are sometimes followed by psychiatric disorders.
In chimpanzees, studies have demonstrated an association between traumatic events and the emergence of behavioral disturbances resembling posttraumatic stress disorder (PTSD) and depression.
We addressed the following central question:
Do chimpanzees develop post traumatic symptoms, in the form of abnormal behaviors, which cluster into syndromes similar to those described in human mood and anxiety disorders?
Methodology/Principal Findings
In phase 1 of this study, we accessed case reports of chimpanzees who had been reportedly subjected to traumatic events, such as maternal separation, social isolation, experimentation, or similar experiences. We applied and tested DSM-IV criteria for PTSD and major depression to published case reports of 20 chimpanzees identified through PrimateLit.Additionally, using the DSM-IV criteria and ethograms as guides, we developed behaviorally anchored alternative criteria that were applied to the case reports. A small number of chimpanzees in the case studies met DSM-IV criteria for PTSD and depression. Measures of inter-rater reliability, including Fleiss' kappa and percentage agreement, were higher with use of the alternative criteria for PTSD and depression. In phase 2, the alternative criteria were applied to chimpanzees living in wild sites in Africa (n = 196) and chimpanzees living in sanctuaries with prior histories of experimentation, orphanage, illegal seizure, or violent human conflict (n = 168). In phase 2, 58% of chimpanzees living in sanctuaries met the set of alternative criteria for depression, compared with 3% of chimpanzees in the wild (p = 0.04), and 44% of chimpanzees in sanctuaries met the set of alternative criteria for PTSD, compared with 0.5% of chimpanzees in the wild (p = 0.04).
Conclusions/Significance
Chimpanzees display behavioral clusters similar to PTSD and depression in their key diagnostic criteria, underscoring the importance of ethical considerations regarding the use of chimpanzees in experimentation and other captive settings.
Citation: Ferdowsian HR, Durham DL, Kimwele C, Kranendonk G, Otali E, et al. (2011) Signs of Mood and Anxiety Disorders in Chimpanzees. PLoS ONE 6(6): e19855. doi:10.1371/journal.pone.0019855
Editor: Patrick Callaerts, VIB & Katholieke Universiteit Leuven, Belgium
Received: January 3, 2011; Accepted: April 4, 2011; Published: June 16, 2011
Copyright: © 2011 Ferdowsian et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The Arcus Foundation provided financial support for the study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: HRF and DLD are employed by Physicians Committee for Responsible Medicine, which is a non-governmental organization that promotes higher ethical standards in research and alternatives to the use of animals in research, education, and training. JBM is employed by Chimpanzee Sanctuary Northwest, which provides lifetime quality care for formerly abused or exploited chimpanzees, while advocating for great apes through education and collaboration. GK is employed by AAP Sanctuary for Exotic Animals, which promotes the replacement of the use in apes in invasive research. CK is a consultant to the World Society for the Protection of Animals and Chairman of the Board of Directors and Scientific Advisor to the Africa Network for Animal Welfare. LA is employed by Chimpanzee Sanctuary & Wildlife Conservation Trust, which promotes the conservation of chimpanzees and their habitats. EO CMJ and TA declare no conflicts of interest. All of the organizations mentioned are nonprofit organizations, and all authors adhere to the PLoS ONE policies on sharing data and materials.
* E-mail: hferdowsian@pcrm.org
The association of pathological behaviors with captivity in nonhuman primates has been noted for decades [1]–[9]. In fact, the relationships between captivity and adverse physical, social and psychological effects have been the foundation for many attempts to develop “models” of human psychopathology, especially following from the early work of Harry Harlow [10].
For example, it is widely recognized that premature separation from mothers reliably leads to a range of adverse behavioral and social effects in chimpanzee infants [11], [12].
Likewise, other unfavorable rearing conditions, social isolation, prolonged captivity, sensory deprivation, and use in laboratory experimentation have been reported to be contributors to behavioral pathology in nonhuman primates [13]–[16].
Several authors have demonstrated the prevalence of abnormal behaviors, ranging from whole-body stereotypies to self-injurious behaviors, in chimpanzees and other nonhuman primates in captivity [6], [15], [17], [18].
Brain structures and neuroendocrine mechanisms associated with mood and anxiety disorders are shared across a wide range of vertebrates [19]–[24]. An evolutionary psychiatry framework, as described by Brüne [25], Stevens and Price [26], Fabrega [27], and others, also predicts similarities across species in genetic, developmental, and environmental risk and protective factors for psychopathology. Similarly, changes, disruption, or dysfunction of common neuropsychiatric systems can result in similar patterns of symptom expression.
Qualities exhibited by chimpanzees demonstrate that they have perceptual abilities, memory, cognition, and emotions, all of which have varying levels of importance for the development of psychiatric disorders. Like human children, young chimpanzees inspect and manipulate objects that do not function as expected in a familiar task, reflecting a foundation of causative understanding [28]. When adequate information about causation is apparent in problem-solving tests, young, wild-born chimpanzees ignore irrelevant information and improvise solutions [29]. Chimpanzees' understanding of causal relationships in the environment is further illustrated by varied, sophisticated use of tools, and dozens of tool use have been described in wild chimpanzee adults [4], [30], [31].
Chimpanzees demonstrate self-awareness in standard mirror tests [32], even in infancy [33]. As adults, chimpanzees have demonstrated joint attention (gaze following with a similar focus of attention) [34], selective cooperation [29], and deception [35], each reflecting an awareness of what others know. Learning and memory develop rapidly during the first 2 years of life [36], and young chimpanzees can outperform adult humans on complex short-term memory tests [37]. Moreover, chimpanzees are capable of remembering objects [38] and place [4] following intervals of years or even decades since prior exposure.
Despite the many similarities between humans and nonhuman primates, it is uncommon to study psychopathology in nonhuman primates using the terms and tools of human psychiatry. Moreover, pathological behaviors in these individuals are often described in isolation without being distilled into recognizable syndromes. Still, such behaviors are widely recognized as abnormal [39], in that they are not typically present in wild populations [4], [40].
There is empirical support for using psychiatric diagnostic criteria for nonhuman primates. Complex PTSD, depression, and other psychiatric conditions have been diagnosed in other species, including chimpanzees [14], [22], [23], [41]–[46], although it is unclear how appropriate the DSM-IV (Diagnostic and Statistical Manual of Mental Disorders, 4th Ed.) criteria [47] or other traditional methods of assessing psychopathology are for use in species other than humans.
Efforts to estimate the prevalence of psychiatric disorders in chimpanzees and other animals encounter special challenges. Diagnostic criteria for mood and anxiety disorders typically require verbal descriptions from subjects of their experiences and internal states. The inability of nonhuman primates to report symptoms presents obstacles similar to those in pediatrics, psychiatry, and geriatrics, often requiring special investigative methods, including gathering information from relevant third parties [48]–[52]. As in the care of humans, the reports of specialized observers, such as technicians and staff, have been used successfully to assess and study well-being [53]–[55] and personality in chimpanzees [56]–[59] and other primates [2] for decades.
Here, we describe an investigation to apply formal diagnostic criteria for mood and anxiety disorders to chimpanzees in which we address two fundamental questions: (a) Do traumatized chimpanzees develop posttraumatic symptoms expressed in the form of psychiatric disorders? (b) If they do, are DSM-IV diagnostic criteria for these disorders adequate to describe posttraumatic disorders in chimpanzees?
In the first part of the study, we hypothesized that behavioral disorders in chimpanzees would fit one of three mutually exclusive possibilities: (a) a number of traumatized chimpanzees would reliably meet DSM-IV criteria for PTSD or depression; (b) traumatized chimpanzees would manifest few or only transient symptoms; (c) traumatized chimpanzees would develop many of the symptoms of psychiatric disorders, but would not reliably meet DSM-IV criteria.
If hypothesis (a) was supported, we would conclude that PTSD and depression occur in chimpanzees in forms similar to those described in human adults.
If hypothesis (b) was supported, we would conclude that the disorders of interest do not occur in chimpanzees.
Finally, if hypothesis (c) was supported by our findings, we would conclude that disorders similar to those occurring in humans occur in chimpanzees, but that the diagnostic criteria and perhaps the definitions of syndromes need revising to be appropriate for this species.
For the second part of the study, we hypothesized that there would be differences between the wild and sanctuary populations in the prevalence of constellations (clusters) of abnormal behavior.
The significant differences we found in phase 2 between the wild and sanctuary populations in the percentage of chimpanzees who met a set of alternative diagnostic criteria for PTSD and depression suggest that syndromes similar to PTSD and depression are identifiable in previously traumatized chimpanzees. We propose that these diagnostic terms be used, when applicable, in chimpanzees and offer criteria for their use.
The study has important limitations. Chimpanzees cannot clearly articulate their thoughts, feelings, and experiences to humans, although a few have learned to communicate using sign language. In phase 1, ratings of psychopathology were made from published studies and case reports. These reports may have contained biases that could have influenced the raters. It is also possible that these reports did not include sufficient information for raters to accurately assess the cases for evidence of mood and anxiety disorders. The low measures of inter-rater reliability observed for some of the items composing the alternative criteria for depression and PTSD merits further exploration. However, the optimal sets of alternative criteria for PTSD and depression were tested and selected based on multiple factors, including the frequency with which items were reported in the case studies, each items' face validity and reliability coefficients, and consultation with experts. It is likely that reliability would have improved further with more training of raters. It was reassuring that there was 100 percent agreement (K = 1.0) among raters for the diagnosis of PTSD, when testing the set of alternative criteria in phase 1. Since there is no gold standard for the assessment of mood and anxiety disorders in chimpanzees, it is not possible to establish the external validity of the alternative criteria we developed.
In phase 2, the design was not longitudinal and therefore did not allow for full assessment of the duration of symptoms and impeded the assessment of severity. The study was not designed to capture simultaneous observations, therefore making it difficult to assess inter-rater reliability. Observers were asked to recall specific behaviors over differing time periods (the time in which they knew the chimpanzees). A question might arise about the comparability of data collection in the wild and sanctuary chimpanzees. Therefore, it is important to note that chimpanzees at the wild sites are typically observed for five days per week from dawn to dusk as part of systematic behavioral study. The raters at the sites have job duties which require them to observe and record very detailed features of behavior on a daily basis. The chimpanzees are recognized by unique features, such as scars, freckles, and other facial and body features that require clear view. When animals are not in close physical proximity, raters from the wild sites use high-quality binoculars to view them to ensure proper individual identification and detailed behavioral data. In our review of ethograms, we noted that some of the wild chimpanzee behaviors recorded included facial expressions and fine motor tasks. Additionally, chimpanzees at some of the sanctuaries can roam freely outdoors and out of view of the raters, sometimes comparable to distances from raters in the wild. However, given the extensive work that the raters have with the chimpanzees, there were sufficient opportunities to view the detailed study behaviors in wild and captive settings. It is likely that the prevalence of behaviors such as physiological reactions (e.g. heavy or irregular breathing) would be underestimated, rather than overestimated, at the wild and sanctuary sites.
Possible refinements for future studies include greater attention to behavioral duration and severity, respondent experience, and incorporation of other abnormal behaviors specific to chimpanzees, such as self-mutilation, smearing of feces, urophagia, and regurgitation and reingestion. In terms of the present study, it is important to note that the approach taken does not account for disorders that may occur in chimpanzees but not in humans, or for the assessment of more global dysfunction that may be measured using instruments such as surveys on subjective well-being [54], among others. Symptoms of mood and anxiety disorders can be disabling, even when full diagnostic criteria for specific psychiatric disorders are not met, as is often the case in human children and adolescents [71].
Strengths of the current study include a robust sample size in phase 2 representing a wide age range of both sexes, as well as reports of trained observers, the broad spectrum of behaviors assessed, and the ability for caregivers to report observations in a relatively unrestricted but structured setting. The clusters of symptoms, as revised, had face validity, in that they were similar to symptoms for PTSD and depression listed in the DSM-IV.
Future research may include further tests for validity and reliability, along with the evaluation of correlates for specific items and diagnoses using the alternative criteria described in our study. Additionally, longitudinal follow-up would be helpful for the interpretation of this study's findings.
Our study's findings underscore the association between psychopathology and conditions that include captivity, confinement, physical harm, loss of social bonds, and isolation. Mood and anxiety disorders such as PTSD and depression are commonly diagnosed among humans exposed to significant acute, recurrent, or persistent trauma [72]–[76]. This study suggests that chimpanzees can exhibit syndromes similar to PTSD and depression as a result of potentially traumatic experiences.
Editor: Patrick Callaerts, VIB & Katholieke Universiteit Leuven, Belgium
Received: January 3, 2011; Accepted: April 4, 2011; Published: June 16, 2011
Copyright: © 2011 Ferdowsian et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The Arcus Foundation provided financial support for the study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: HRF and DLD are employed by Physicians Committee for Responsible Medicine, which is a non-governmental organization that promotes higher ethical standards in research and alternatives to the use of animals in research, education, and training. JBM is employed by Chimpanzee Sanctuary Northwest, which provides lifetime quality care for formerly abused or exploited chimpanzees, while advocating for great apes through education and collaboration. GK is employed by AAP Sanctuary for Exotic Animals, which promotes the replacement of the use in apes in invasive research. CK is a consultant to the World Society for the Protection of Animals and Chairman of the Board of Directors and Scientific Advisor to the Africa Network for Animal Welfare. LA is employed by Chimpanzee Sanctuary & Wildlife Conservation Trust, which promotes the conservation of chimpanzees and their habitats. EO CMJ and TA declare no conflicts of interest. All of the organizations mentioned are nonprofit organizations, and all authors adhere to the PLoS ONE policies on sharing data and materials.
* E-mail: hferdowsian@pcrm.org
Introduction
Since nonhuman animals, including chimpanzees, are frequently used in research, there is an ethical imperative to understand the potentially adverse effects of captivity and their use in research.The association of pathological behaviors with captivity in nonhuman primates has been noted for decades [1]–[9]. In fact, the relationships between captivity and adverse physical, social and psychological effects have been the foundation for many attempts to develop “models” of human psychopathology, especially following from the early work of Harry Harlow [10].
For example, it is widely recognized that premature separation from mothers reliably leads to a range of adverse behavioral and social effects in chimpanzee infants [11], [12].
Likewise, other unfavorable rearing conditions, social isolation, prolonged captivity, sensory deprivation, and use in laboratory experimentation have been reported to be contributors to behavioral pathology in nonhuman primates [13]–[16].
Several authors have demonstrated the prevalence of abnormal behaviors, ranging from whole-body stereotypies to self-injurious behaviors, in chimpanzees and other nonhuman primates in captivity [6], [15], [17], [18].
In humans, anxiety disorders, such as posttraumatic stress disorder (PTSD), and mood disorders, such as major depressive disorder, are commonly diagnosed after acute, repeated, or chronic trauma. These types of stressors can sometimes overwhelm normal physiological responses, which can cause persistent physiological and structural changes [19], [20].
Brain structures and neuroendocrine mechanisms associated with mood and anxiety disorders are shared across a wide range of vertebrates [19]–[24]. An evolutionary psychiatry framework, as described by Brüne [25], Stevens and Price [26], Fabrega [27], and others, also predicts similarities across species in genetic, developmental, and environmental risk and protective factors for psychopathology. Similarly, changes, disruption, or dysfunction of common neuropsychiatric systems can result in similar patterns of symptom expression.
The hippocampus, found in all mammals, is a brain structure involved in memory storage and retrieval. In humans, PTSD has been associated with reductions in hippocampal volume or activity, perhaps because of recurrently and chronically elevated levels of cortisol, followed by down-regulation of the hypothalamic-pituitary-adrenal axis. Abnormalities of this axis have been described in animals subjected to confinement, restraint, isolation, or surgical procedures [22], [23].
Qualities exhibited by chimpanzees demonstrate that they have perceptual abilities, memory, cognition, and emotions, all of which have varying levels of importance for the development of psychiatric disorders. Like human children, young chimpanzees inspect and manipulate objects that do not function as expected in a familiar task, reflecting a foundation of causative understanding [28]. When adequate information about causation is apparent in problem-solving tests, young, wild-born chimpanzees ignore irrelevant information and improvise solutions [29]. Chimpanzees' understanding of causal relationships in the environment is further illustrated by varied, sophisticated use of tools, and dozens of tool use have been described in wild chimpanzee adults [4], [30], [31].
Chimpanzees demonstrate self-awareness in standard mirror tests [32], even in infancy [33]. As adults, chimpanzees have demonstrated joint attention (gaze following with a similar focus of attention) [34], selective cooperation [29], and deception [35], each reflecting an awareness of what others know. Learning and memory develop rapidly during the first 2 years of life [36], and young chimpanzees can outperform adult humans on complex short-term memory tests [37]. Moreover, chimpanzees are capable of remembering objects [38] and place [4] following intervals of years or even decades since prior exposure.
Despite the many similarities between humans and nonhuman primates, it is uncommon to study psychopathology in nonhuman primates using the terms and tools of human psychiatry. Moreover, pathological behaviors in these individuals are often described in isolation without being distilled into recognizable syndromes. Still, such behaviors are widely recognized as abnormal [39], in that they are not typically present in wild populations [4], [40].
There is empirical support for using psychiatric diagnostic criteria for nonhuman primates. Complex PTSD, depression, and other psychiatric conditions have been diagnosed in other species, including chimpanzees [14], [22], [23], [41]–[46], although it is unclear how appropriate the DSM-IV (Diagnostic and Statistical Manual of Mental Disorders, 4th Ed.) criteria [47] or other traditional methods of assessing psychopathology are for use in species other than humans.
Efforts to estimate the prevalence of psychiatric disorders in chimpanzees and other animals encounter special challenges. Diagnostic criteria for mood and anxiety disorders typically require verbal descriptions from subjects of their experiences and internal states. The inability of nonhuman primates to report symptoms presents obstacles similar to those in pediatrics, psychiatry, and geriatrics, often requiring special investigative methods, including gathering information from relevant third parties [48]–[52]. As in the care of humans, the reports of specialized observers, such as technicians and staff, have been used successfully to assess and study well-being [53]–[55] and personality in chimpanzees [56]–[59] and other primates [2] for decades.
Here, we describe an investigation to apply formal diagnostic criteria for mood and anxiety disorders to chimpanzees in which we address two fundamental questions: (a) Do traumatized chimpanzees develop posttraumatic symptoms expressed in the form of psychiatric disorders? (b) If they do, are DSM-IV diagnostic criteria for these disorders adequate to describe posttraumatic disorders in chimpanzees?
In the first part of the study, we hypothesized that behavioral disorders in chimpanzees would fit one of three mutually exclusive possibilities: (a) a number of traumatized chimpanzees would reliably meet DSM-IV criteria for PTSD or depression; (b) traumatized chimpanzees would manifest few or only transient symptoms; (c) traumatized chimpanzees would develop many of the symptoms of psychiatric disorders, but would not reliably meet DSM-IV criteria.
If hypothesis (a) was supported, we would conclude that PTSD and depression occur in chimpanzees in forms similar to those described in human adults.
If hypothesis (b) was supported, we would conclude that the disorders of interest do not occur in chimpanzees.
Finally, if hypothesis (c) was supported by our findings, we would conclude that disorders similar to those occurring in humans occur in chimpanzees, but that the diagnostic criteria and perhaps the definitions of syndromes need revising to be appropriate for this species.
For the second part of the study, we hypothesized that there would be differences between the wild and sanctuary populations in the prevalence of constellations (clusters) of abnormal behavior.
Methods ..........
Discussion Top
Our study shows that previously traumatized chimpanzees demonstrate persistent abnormal objective symptoms and that these symptoms cluster into syndromes that are similar to PTSD and depression. We began this investigation with three mutually exclusive hypotheses. The first hypothesis, that a number of traumatized chimpanzees would reliably meet DSM-IV criteria for PTSD or depression, was not wholly supported in phase 1. Although a number of chimpanzees met DSM-IV criteria for PTSD and depression in this phase, measures of inter-rater reliability were low. The second hypothesis, that chimpanzees would manifest few, if any, criteria for PTSD or depression, was also not supported. In both phase 1 and phase 2, multiple signs of abnormal chimpanzee behaviors similar to the criteria for PTSD and depression were reported. The third hypothesis, that chimpanzees would display clusters of symptoms that are similar to disorders such as PTSD and depression, was supported. Measures of reliability were greater among raters when testing the alternative criteria. This is likely partly attributable to attempts to reduce the need to make inferences about thoughts or feelings.The significant differences we found in phase 2 between the wild and sanctuary populations in the percentage of chimpanzees who met a set of alternative diagnostic criteria for PTSD and depression suggest that syndromes similar to PTSD and depression are identifiable in previously traumatized chimpanzees. We propose that these diagnostic terms be used, when applicable, in chimpanzees and offer criteria for their use.
The study has important limitations. Chimpanzees cannot clearly articulate their thoughts, feelings, and experiences to humans, although a few have learned to communicate using sign language. In phase 1, ratings of psychopathology were made from published studies and case reports. These reports may have contained biases that could have influenced the raters. It is also possible that these reports did not include sufficient information for raters to accurately assess the cases for evidence of mood and anxiety disorders. The low measures of inter-rater reliability observed for some of the items composing the alternative criteria for depression and PTSD merits further exploration. However, the optimal sets of alternative criteria for PTSD and depression were tested and selected based on multiple factors, including the frequency with which items were reported in the case studies, each items' face validity and reliability coefficients, and consultation with experts. It is likely that reliability would have improved further with more training of raters. It was reassuring that there was 100 percent agreement (K = 1.0) among raters for the diagnosis of PTSD, when testing the set of alternative criteria in phase 1. Since there is no gold standard for the assessment of mood and anxiety disorders in chimpanzees, it is not possible to establish the external validity of the alternative criteria we developed.
In phase 2, the design was not longitudinal and therefore did not allow for full assessment of the duration of symptoms and impeded the assessment of severity. The study was not designed to capture simultaneous observations, therefore making it difficult to assess inter-rater reliability. Observers were asked to recall specific behaviors over differing time periods (the time in which they knew the chimpanzees). A question might arise about the comparability of data collection in the wild and sanctuary chimpanzees. Therefore, it is important to note that chimpanzees at the wild sites are typically observed for five days per week from dawn to dusk as part of systematic behavioral study. The raters at the sites have job duties which require them to observe and record very detailed features of behavior on a daily basis. The chimpanzees are recognized by unique features, such as scars, freckles, and other facial and body features that require clear view. When animals are not in close physical proximity, raters from the wild sites use high-quality binoculars to view them to ensure proper individual identification and detailed behavioral data. In our review of ethograms, we noted that some of the wild chimpanzee behaviors recorded included facial expressions and fine motor tasks. Additionally, chimpanzees at some of the sanctuaries can roam freely outdoors and out of view of the raters, sometimes comparable to distances from raters in the wild. However, given the extensive work that the raters have with the chimpanzees, there were sufficient opportunities to view the detailed study behaviors in wild and captive settings. It is likely that the prevalence of behaviors such as physiological reactions (e.g. heavy or irregular breathing) would be underestimated, rather than overestimated, at the wild and sanctuary sites.
Possible refinements for future studies include greater attention to behavioral duration and severity, respondent experience, and incorporation of other abnormal behaviors specific to chimpanzees, such as self-mutilation, smearing of feces, urophagia, and regurgitation and reingestion. In terms of the present study, it is important to note that the approach taken does not account for disorders that may occur in chimpanzees but not in humans, or for the assessment of more global dysfunction that may be measured using instruments such as surveys on subjective well-being [54], among others. Symptoms of mood and anxiety disorders can be disabling, even when full diagnostic criteria for specific psychiatric disorders are not met, as is often the case in human children and adolescents [71].
Strengths of the current study include a robust sample size in phase 2 representing a wide age range of both sexes, as well as reports of trained observers, the broad spectrum of behaviors assessed, and the ability for caregivers to report observations in a relatively unrestricted but structured setting. The clusters of symptoms, as revised, had face validity, in that they were similar to symptoms for PTSD and depression listed in the DSM-IV.
Future research may include further tests for validity and reliability, along with the evaluation of correlates for specific items and diagnoses using the alternative criteria described in our study. Additionally, longitudinal follow-up would be helpful for the interpretation of this study's findings.
Our study's findings underscore the association between psychopathology and conditions that include captivity, confinement, physical harm, loss of social bonds, and isolation. Mood and anxiety disorders such as PTSD and depression are commonly diagnosed among humans exposed to significant acute, recurrent, or persistent trauma [72]–[76]. This study suggests that chimpanzees can exhibit syndromes similar to PTSD and depression as a result of potentially traumatic experiences.
Acknowledgments Top
We thank all the participating sites for their help and support throughout the project, especially during data collection. Specifically, we thank David Maina, Dr. Martin Mulama, Dr. Martin Müller, E.P. Schippers, AAP Sanctuary for Exotic Animals, Chimpanzee Sanctuary and Wildlife Conservation Trust, Chimpanzee Sanctuary Northwest, Chimpanzee Sanctuary Uto, Kibale Chimpanzee Project, Ol Pejeta Conservancy and Sweetwaters Chimpanzee Sanctuary, and all of the sanctuary and wild site staff. Uganda National Council for Science and Technology, the Uganda Wildlife Authority, and the National Council of Science and technology under the ministry of Higher Education, Science and Technology in the Republic of Kenya gave approval to the project, for which we are grateful. We also thank Greg Mazur for assistance with data management, and the guidance and comments offered by an anonymous reviewer.Author Contributions Top
Conceived and designed the experiments: HRF DLD. Analyzed the data: HRF CMJ DLD. Contributed reagents/materials/analysis tools: HRF DLD CMJ. Wrote the paper: HRF DLD. Assisted with data acquisition or interpretation of data: HRF DLD CK GK EO TA JBM LA CMJ. Critically reviewed or revised article: HRF DLD CK GK EO TA JBM LA CMJ. Provided final approval for the article to be published: HRF DLD CK EO TA JBM LA CMJ.References Top
- (1989) The effects of single caging on chimpanzee behavior. Lab Anim Sci 39: 345–346. Find this article online
- (1986) Behavioral pathology. In: Erwin MJ, editor. Comparative primate biology, volume 2, part A. Behavior, conservation, and ecology. New York: Alan R. Liss. pp. 411–454.
- (1970) Differential rearing of the chimpanzee. In: Bourne GH, editor. The chimpanzee, volume 3: Immunology, infection, hormones, anatomy, and behavior. Baltimore: University Park Press. pp. 337–360.
- (1986) The chimpanzees of the Gombe: Patterns of behavior. Boston: Harvard University Press. 673 p.
- (1965) Total social isolation in monkeys. Proc Natl Acad Sci U S A 54: 90–97. Find this article online
- (1999) Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes). Am J Primatol 48: 15–29. Find this article online
- (1982) Stereotypy in monkeys and humans. Psychol Med 12: 61–72. Find this article online
- (1928) The self-mutilation of a male Macacus rhesus monkey. J Mammal 9: 293–300. Find this article online
- (1943) Chimpanzees. A laboratory colony. New Haven: Yale University Press. 321 p.
- (1986) From learning to love: The selected papers of H.F. Harlow. In: Harlow CM, editor. editor. New York: Praeger Publishers. 328 p.
- (2007) IPS international guidelines for the acquisition, care and breeding of nonhuman primates. Available: http://www.internationalprimatologicalso ciety.org/docs/IPS_International_Guideli nes_for_the_Acquisition_Care_and_Breedin g_of_Nonhuman_Primates_Second_Edition_2007.pdf. Accessed 2010 Nov 5.
- (2005) Enrichment for nonhuman primates: chimpanzees. Washington, DC: Department of Health and Human Services. NIH Publication No. 05–5748. Available: http://grants.nih.gov/grants/olaw/Chimpanzees.pdf. Accessed 2010 Nov 5.
- (2002) Factors predicting increased incidence of abnormal behavior in male pigtailed macaques. Am J Primatol 58: 57–69. Find this article online
- (2008) Building an inner sanctuary: complex PTSD in chimpanzees. J Trauma Dissociation 9: 9–34. Find this article online
- (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. Find this article online
- (2003) Self-injurious behavior in rhesus monkeys: new insights into its etiology, physiology, and treatment. Am J Primatol 59: 3–19. Find this article online
- (2002) Inter-group variation in abnormal behavior in chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). Appl Anim Behav Sci 76: 165–176. Find this article online
- (2009) Risk factors and remediation of self-injurious and self-abuse behavior in rhesus macaques. J Appl Anim Welf Sci 12: 61–72. Find this article online
- (1997) Possible mechanisms for atrophy of the human hippocampus. Mol Psychiatry 2: 255–262. Find this article online
- (2000) Allostasis and allostatic load: implications for neuropsychopharmacology. Neuropsychopharmacology 22: 108–124. Find this article online
- (2005) Comparative vertebrate neuroanatomy: Evolution and adaptation. Hoboken, NJ: John Wiley & Sons, Inc. 744 p.
- (2005) Mental health and well-being in animals. Oxford: Blackwell Publishing Professional. 301 p.
- (2004) Physiology and behavior of animal suffering. Oxford: Blackwell Science. 268 p.
- (2003) Implications of natural selection in shaping 99.4% nonsynonymous DNA identity between humans and chimpanzees: enlarging genus Homo. Proc Natl Acad Sci U S A 100: 7181–7188. Find this article online
- (2008) Textbook of evolutionary psychiatry: The origins of psychopathology. Oxford: Oxford University Press. 380 p.
- (2000) Evolutionary psychiatry: A new beginning. Second edition. London: Biddles Ltd. 310 p.
- (2004) Psychiatric conditions in an evolutionary context. Psychopathology 37: 290–298. Find this article online
- (2001) Do chimpanzees seek explanations? Preliminary comparative investigations. Can J Exp Psychol 55: 185–193. Find this article online
- (2005) Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens). Anim Cogn 8: 164–181. Find this article online
- (1992) Material culture in chimpanzees. Cambridge: Cambridge University Press. 277 p.
- (1999) Cultures in chimpanzees. Nature 399: 682–685. Find this article online
- (2006) Self-Awareness in animals and humans: Developmental perspectives. Cambridge, UK: Cambridge University Press. 464 p.
- (2006) Cognitive development in chimpanzees. Tokyo: Springer. 522 p.
- (1996) Chimpanzees: joint visual attention. Psychol Sci 7: 129–135. Find this article online
- (2006) Chimpanzees deceive a human competitor by hiding. Cognition 101: 495–514. Find this article online
- (2006) Development of chimpanzee social cognition in the first two years of life. In: Matsuzawa T, Tomonaga M, Tanaka M, editors. Cognitive development in chimpanzees. Tokyo: Springer. pp. 182–200.
- (2007) Working memory of numerals in chimpanzees. Curr Biol 17: R1004–R1005. Find this article online
- (2000) A chimpanzee's (Pan troglodytes) long-term retention of lexigrams. Anim Learn Behav 28: 201–207. Find this article online
- (1996) Guide for the care and use of laboratory animals. Washington, DC: National Academy Press. 140 p.
- (2006) Psychopathology in great apes: concepts, treatment options and possible homologies to human psychiatric disorders. Neurosci Biobehav Rev 30: 1246–1259. Find this article online
- (2006) Mirror, mirror. Am Scientist 94: 487–489. Find this article online
- (2007) How elephants are opening doors: developmental neuroethology, attachment and social context. Ethology 113: 426–436. Find this article online
- (2007) Elephant breakdown. Nature 433: 807. Find this article online
- (2007) Avian neuroanatomy revisited: from clinical principles to avian cognition. Vet Clin North Am Exot Anim Pract 10: 775–802.vi Find this article online
- (2000) Natural animal models of human psychiatric conditions: assessment of mechanism and validity. Prog Neuropsychopharmacol Biol Psychiatry 24: 727–776. Find this article online
- (1989) Animal models of depression. New York: Springer-Verlag. 300 p.
- (2000) Diagnostic and statistical manual of mental disorders, fourth edition (text revision). Washington, DC: American Psychiatric Association. 943 p.
- (2006) Screening for preschool posttraumatic stress disorder with the Child Behavior Checklist. J Pediatr Psychol 31: 431–435. Find this article online
- (1995) Two approaches to the diagnosis of posttraumatic stress disorder in infancy and early childhood. J Am Acad Child Adolesc Psychiatry 34: 191–200. Find this article online
- (2003) New findings on alternative criteria for PTSD in preschool children. J Am Acad Child Adolesc Psychiatry 42: 561–570. Find this article online
- (1990) Brief report: validation of a reinforcer survey for use with geriatric patients. Behav Interventions 5: 129–136. Find this article online
- (1988) Cornell Scale for Depression in Dementia. Biol Psychiatry 23: 271–284. Find this article online
- (2001) Chimpanzee psychopathology and subjective well-being and social adjustment. In: Landau V, editor. ChimpanZoo 2000 conference proceedings. Tucson, AZ: ChimpanZoo: Research, Education and Enrichment Program. pp. 24–32.
- (2003) Can chimpanzee (Pan troglodytes) happiness be estimated by human raters? J Res Personality 37: 1–15. Find this article online
- (2006) Assessing the effects of private ownership on chimpanzees through personality testing. War of the worlds: Chimpanzee protection versus chimpanzee exploitation. Tucson: ChimpanZoo.
- (1997) The five-factor model plus dominance in chimpanzee personality. J Res Personality 31: 257–271. Find this article online
- (2003) Chimpanzee (Pan troglodytes) personality predicts behavior. J Res Personality 39: 534–549. Find this article online
- (2008) Aping humans: age and sex effects in chimpanzee (Pan troglodytes) and human (Homo sapiens) personality. J Comp Psychol 122: 418–427. Find this article online
- (1999) A preliminary investigation of the construct of psychopathic personality (psychopathy) in chimpanzees (Pan troglotydes). J Comp Psychol 113: 365–375. Find this article online
- (1969) The effect of early deprivation on the social behavior of adolescent chimpanzees. Am J Psychiatry 125: 1531–1536. Find this article online
- (1963) The effects of environmental restriction upon the chimpanzee's responsiveness to objects. J Comp Physiol Psychol 56: 78–85. Find this article online
- (1982) Behavioral effects of a change in the physical environment: a pilot study of captive chimpanzees. Zoo Biol 1: 371–380. Find this article online
- (2009) Developmental context effects on bicultural posttrauma self repair in chimpanzees. Dev Psychol 45: 1376–1388. Find this article online
- (2007) Combination therapy reduces self-injurious behavior in a chimpanzee (Pan Troglodytes Troglodytes): a case report. J Appl Anim Welf Sci 10: 123–140. Find this article online
- (1997) Treating chronic regurgitation behavior: a case study. Lab Anim 26: 30–33. Find this article online
- (2007) Attempting to reduce regurgitation and reingestion in a captive chimpanzee through increased feeding opportunities: a case study. Lab Anim (NY) 36: 35–38. Find this article online
- (1990) A case history of a decrement in maternal competence in a captive chimpanzee (Pan troglodytes). Brown University Lab Primate Newsletter 29: 3–6. Find this article online
- (1978) The resocialization of single-caged chimpanzees and the establishment of an island colony. J Med Primatol 7: 70–81. Find this article online
- (1991) Resocialization of a group of ex-laboratory chimpanzees, Pan troglodytes. J Med Primatol 20: 375–381. Find this article online
- (1988) A case of offspring desertion by a female chimpanzee and the behavioral changes of the abandoned offspring. Primates 29: 319–330. Find this article online
- (1995) Traumas and posttraumatic stress disorder in a community population of older adolescents. J Am Acad Child Adolesc Psychiatry 34: 1369–1380. Find this article online
- (2004) Assessing psychological trauma and PTSD. Second edition. New York: The Guilford Press. 668 p.
- (1995) Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 52: 1048–1060. Find this article online
- (2000) Comorbidity of psychiatric disorders and posttraumatic stress disorder. J Clin Psychiatry 61: suppl 722–32. Find this article online
- (1998) Epidemiology of trauma and posttraumatic stress disorder. In: Yehuda R, editor. Psychological trauma. Washington, DC: American Psychiatric Press. pp. 1–27.
- (2001) Reported trauma, post-traumatic stress disorder and major depression among primary care patients. Psychol Med 31: 1249–1257. Find this article online
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