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White Monkey Syndrome and Presumptive Copper Deficiency in Wild Savannah Baboons

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White Monkey Syndrome and Presumptive Copper Deficiency in Wild Savannah Baboons American Journal of Primatology 73:1160–1168 (2011) RESEARCH ARTICLE White Monkey Syndrome and Presumptive Copper Deficiency in Wild Savannah Baboons A. CATHERINE MARKHAM1Ã, LAURENCE R. GESQUIERE1, JEAN-PHILIPPE BELLENGER2,3, SUSAN C. ALBERTS4,5, 1,5 AND JEANNE ALTMANN 1Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey 2Department of Geosciences, Princeton Environmental Institute, Princeton University, Princeton, New Jersey 3De´partement de Chimie, Universite´ de Sherbrooke, Sherbrooke, Que´bec, Canada 4Biology Department, Duke University, Durham, North Carolina 5Institute for Primate Research, National Museums of Kenya, Nairobi, Kenya In immature wild savannah baboons (Papio cynocephalus), we observed symptoms consistent with copper (Cu) deficiency and, more specifically, with a disorder referred to as white monkey syndrome (WMS) in laboratory primates. The objectives of this study were to characterize this pathology, and test three hypotheses that (1) Cu deficiency may have been induced by zinc (Zn) toxicity, (2) it may have been induced by molybdenum (Mo) toxicity, and (3) cumulative rainfall during the perinatal period and particularly during gestation is an ecological factor distinguishing infants afflicted with WMS from non- WMS infants. During 2001–2009, we observed 22 instances of WMS out of a total 377 live births in the study population. Visible symptoms exhibited by WMS infants included whitening of the animal’s fur and/or impaired mobility characterized by an apparent ‘‘stiffening’’ of the hindlimbs. Occurrence of WMS did not vary significantly by gender. However, among individuals that survived at least 180 days, WMS males had a significantly lower survivorship probability than non-WMS males. Zn/Cu ratios assessed from hair samples of adult female baboons were higher in females who had produced at least one WMS offspring relative to females who had not had a WMS offspring. This was true even when the hair sample was collected long after the birth of the female’s afflicted infant. We consider this potentially indicative of a robust tendency for low Cu levels induced by elevated Zn intake in some individuals. No significant differences of Mo/Cu ratios were observed. Cumulative rainfall during gestation (179 days) was 50% lower for WMS infants relative to non-WMS infants. In contrast, rainfall for the two classes of infants did not differ in the 180 days before conception or in the 180 days following birth. This finding highlights the importance of prenatal ecological conditions in healthy fetal development with regard to WMS. Am. J. Primatol. 73:1160–1168, 2011. r 2011 Wiley Periodicals, Inc. Key words: Amboseli; copper deficiency; Papio cynocephalus; white monkey syndrome; wild baboons; zinc toxicity INTRODUCTION lower limb parathesias, and failure to thrive [reviewed in Culotta & Gitlin, 2000]. Trace minerals are naturally occurring elements Both genetic and environmental factors can lead essential in minute concentrations for optimal to Cu deficiency. For example, Menkes disease is an growth and development of living organisms. Dele- x-linked recessive disorder in humans resulting from terious effects are often observed with either excessive or deficient intake, and imbalances are considered risk factors for several diseases in a wide Contract grant sponsors: American Society of Primatologists; range of species. In particular, extensive research on Animal Behavior Society; International Primatological Society; NIA; Contract grant numbers: R01AG034513-01; Contract grant human and nonhuman subjects has focused on the sponsor: NSF; Contract grant numbers: IBN-0322613; IOS- causes and consequences of deficiencies in the trace 0919200; BCS-0851750; Contract grant sponsor: Sigma Xi. element copper (Cu). Cu is required for numerous ÃCorrespondence to: A. Catherine Markham, Department of cellular processes, including mitochondrial respira- Ecology and Evolutionary Biology, Princeton University, Guyot tion, antioxidant defense, neurotransmitter synth- Hall, Washington Road, Princeton, NJ 08544. E-mail: [email protected] esis, connective tissue formation, and tissue Received 19 January 2011; revised 4 June 2011; revision pigmentation [reviewed in Culotta & Gitlin, 2000]. accepted 19 June 2011 Cu deficiencies are associated with symptoms, DOI 10.1002/ajp.20983 including immune system dysfunction, anemia, Published online 6 September 2011 in Wiley Online Library (wiley pigmentation loss in the skin and hair, gait difficulty, onlinelibrary.com). r 2011 Wiley Periodicals, Inc. Baboon White Monkey Syndrome / 1161 disruptions to the body’s pathways for Cu absorption ratio in the same hair samples. For both hypotheses, and transport; severity of symptoms varies among we predicted that mineral ratios would be higher in patients and can include hypopigmentation, anemia, individuals associated with WMS (reflecting high Zn neurological defects, connective tissue defects, and or Mo concentration relative to the concentration of distinctively brittle hair [reviewed in de Bie et al., Cu) compared with the ratios in individuals with no 2007; Cox et al., 2002; Vonk et al., 2008]. Cu WMS association. Finally, because (1) rain in the deficiency may also be acquired owing to environ- semi-arid Amboseli ecosystem is a key environmen- mental factors, either (1) directly as a result of tal variable influencing the nutritional and repro- inadequacies in an organism’s habitat and/or nutri- ductive status of baboons [e.g. Alberts et al., 2005; tion or (2) indirectly as a result of Cu’s susceptibility Beehner et al., 2006] and (2) gestation is a vulnerable to transport or bioavailability interference from time to mineral imbalances [e.g. Adogwa et al., 1999; other trace elements, notably zinc (Zn) and molyb- Barone et al., 1998; Gambling & McArdle, 2004], we denum (Mo) in the circumstances of this study tested the hypothesis that rainfall in the perinatal [reviewed in McDowell, 2003]. Consequently, ele- period contributes to WMS. Specifically, we predicted vated levels of one or more of these other elements that infants afflicted with WMS experienced lower may result in a secondary Cu deficiency. rainfall regimes during gestation than did non-WMS In nonhuman primates, acquired Cu deficiency infants. induced by Zn toxicity has been associated with a disorder known as white monkey syndrome (WMS). In documented cases of Zn/Cu imbalances in rhesus METHODS macaques (Macaca mulatta) [Obeck, 1978] and All project protocols complied with regulations baboons (Papio spp.) [Frost et al., 2004], afflicted in Kenya (Republic of Kenya Research Permits individuals were juveniles characterized by alopecia, NCST/5/002/R/776 to J.A. and NCST/5/002/R/777 to dehydration, emaciation, cachexia, dermatitis, diar- S.C.A.) and in the United States (Princeton Uni- rhea, and whitening of hair, skin, and mucous versity IACUC 1649), and adhered to the American membranes. Researchers attributed the occurrence Society of Primatologists Principles for the Ethical of these symptoms to elevated Zn intake originating Treatment of Nonhuman Primates. from the galvanized cages in which the animals were We observed a population of wild savannah housed. Prolonged, untreated exposure to the toxic baboons living in the Amboseli basin, a semi-arid Zn levels resulted in death; symptoms were occa- short grass savannah located in east Africa at the sionally reversible if animals were relocated to northwestern base of Mt. Kilimanjaro. Alberts et al. nontoxic enclosures. Similar pigmentation loss in [2005] provide a thorough description of the Ambo- hair was also observed in a population of captive seli study site and the broader ecological region. squirrel monkeys (Saimiri sciureus) housed in out- Review of the area’s volcanic geochemistry and clay door pens with galvanized metal fencing and roofs at mineralogy are described by Hay et al. [1995] and the Sabana Seca Field Station of the Caribbean Stoessell and Hay [1978]. Maskall and Thornton Primate Research Center, University of Puerto Rico. [1996] provide an overview of the trace mineral However, no tests were performed to confirm the content of soils in Amboseli; elevated Mo concentra- conditions were directly attributable to Zn/Cu im- tion is of particular relevance. balances [Matthew Kessler, personal communica- Savannah baboons are a highly social species tion, February 3, 2011]. obligated to group living. Many aspects of their Here, we report the occurrence of symptoms sociality have been studied extensively, including consistent with WMS and, more broadly, with Cu patterns characteristic of typical infant care and deficiency in wild savannah baboons (Papio cynoce- development [e.g. Altmann, 1980; Altmann et al., phalus). Using long-term observational data avail- 1981; Rhine et al., 1985]. The species is omnivorous able through the Amboseli Baboon Research Project but seasonally available seeds, leaves, pods, and (ABRP), we offer novel documentation and insight fruits comprise the bulk of their diet [e.g. Alberts into the characterization of this pathology in wild et al., 2005; Altmann, 1998; Norton et al., 1987]. primates. Specifically, we tested two hypotheses All baboons within the study population were regarding the probable source of this pathology. individually identifiable by ABRP field researchers, First, we evaluated whether Cu deficiency was and each of the five social groups monitored by induced by Zn toxicity [as reported by Frost et al., ABRP was the focus of detailed observations several 2004; Obeck,
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