J Med Primatol doi:10.1111/jmp.12129
CASE REPORT
Facial dysplasia in wild chimpanzees rard Couly4,5 & Giovanni Levi5 Sabrina Krief1,2, Jean-Michel Krief2, Andrew Seguya3, Ge 1 2 3 4 5
UMR 7206 CNRS/MNHN/P7, Ecoathropologie et ethnobiologie, CP 135, Museum national d’histoire naturelle, Paris, France Projet pour la conservation des grands singes (PCGS), UWA Sebitoli Station, Kibale National Park, Fort Portal, Uganda Uganda Wildlife Authority, Kampala, Uganda Paris Descartes, Institut de la Bouche et du Visage de l’Enfant, Ho ^pital Universitaire Necker 149, Paris, France Universite gulations endocriniennes, Museum national d’histoire naturelle, Paris, France UMR 7221 CNRS/MNHN, Evolution des re
Keywords chimpanzee – congenital malformation – nasal defect Correspondence Sabrina Krief, UMR 7206 CNRS/MNHN/P7, Ecoathropologie et ethnobiologie, CP 135, Museum national d’histoire naturelle, 57 rue Cuvier, 75231 Paris Cedex 5, France. Tel.: +33 1 40 79 53 37; fax: +33 688 24 15 96; e-mail: [email protected]
Abstract At least 10% of the Sebitoli chimpanzee community of the Kibale National Park (Uganda) present a characteristic facial phenotype with flattened nose, reduced nostrils, and concave mid-face. Affected individuals do not present skin lesions, and also young infants are affected. We suggest, therefore, a congenital origin of this defect.
Accepted April 23, 2014.
Case report In the northern area of the Kibale National Park (Uganda) known as the ‘Sebitoli’ region, a wild chimpanzee (Pan troglodytes schweinfurthii) community has been undergoing a habituation program for 4 years. Approval for fieldwork has been obtained from Uganda Wildlife Authority and Uganda National Council for Science and Technology, and the research adheres to national and international ethics, protocols, and legal requirements. At least nine of the 80 identified individuals of this community share a characteristic facial phenotype. Their nose is flattened with reduced or absent nostrils and their mid-face is concave. None of them have facial scars, wounds, ulcers, or other skin lesions evoking yaws disease. One individual seems to present exophthalmos. The incidence of the facial phenotype is thus high with about 10% of the community affected. This unusual phenotype is present in male and female individuals of any class of age and sex: 1-year-old infants, juveniles, subadults, and young adults. The oldest affected individual has an estimated age of 16 years. The three mothers of younger affected individuals (two juveniles and two infants) do not present nasal
280
dysplasia. Two of the affected chimpanzees were born from the same mother, which has a normal-looking face and body except for a very light fur color. The older affected individual is entirely missing his left foot, resulting most likely from being caught in a snare (Table 1; Fig. 1). According to our monitoring, aside from facial abnormalities, all affected individuals appeared in good health and did not present other deformities. Individuals with flat face and reduced nose seem to maintain a normal respiratory function. The cause of the nasal defect present in the Sebitoli chimpanzees is unknown; however, its high incidence in a restricted population and its presence in a young infant suggest a congenital origin. To understand the possible etiology of this phenotype, we reviewed other reported malformations in wild primates. Limbs deformities, common in wild nonhuman primates (NHP), are usually the result of fight, falls, or consequences of being caught in snares set by poachers [14, 17]. The prevalence of congenital limb malformations is, however, normally less than 1% between both humans and NHP [1]; the only known exceptions are constituted by two food-provisioned colonies of semi-wild macaques in Hong Kong and in Japan, where the incidence can reach 17.1% of the total
J Med Primatol 43 (2014) 280–283 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Krief et al.
Facial dysplasia in wild chimpanzees
Table 1 Cases of facial dysplasia observed in Sebitoli chimpanzees, Kibale National Park, Uganda Chimpanzee code name
Sex
Mother
Estimated age
AG
M
Unknown
16
SA KB GA KR LV
F M M M M
Unknown KT KT KL LS
13 7 1,5 8 3
KW Unnamed #1
M F
KE Unknown
5 9
Unnamed #2
M
Unknown
8
Description of the defect Concave mid-face profile, flat nose, nostrils absent, concave shape of the area of nasal spine, 3 deep notches, asymmetry of the nasal fossa, missing left foot Concave mid-face profile, flat nose, the absence of nasal wings Flat nose Flat nose Flat nose Asymmetrical and reduced nostrils, three median notches on the nose, swollen areas both sides of the nose Flat nose Flat nose, absence of nasal wings, asymmetry of the fossa, swollen area both sides of the nose Absence of nasal wings and round fossa of nose, exophthalmos
Fig. 1 Photographs of chimpanzees with facial dysplasia and normal phenotype, Kibale National Park, Uganda: (1) immature individuals (1A) LV (immature); (1B) Unnamed #1 (immature); (1C) Unnamed #2 (immature); (1D) an infant chimpanzee with a normal phenotype. (2) adult individuals (2A) AG (adult); (2B) an adult chimpanzee with a normal phenotype. J Med Primatol 43 (2014) 280–283 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
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Facial dysplasia in wild chimpanzees
population [2, 7, 16, 18]. In great apes, such deformities are rarely reported [4, 13, 17]. Only two cases of facial congenital deformities have been so far reported in wild NHP: an adult female baboon symmetrically missing most of her upper jaw and nose; a case of acrocephalo-dactylism in an infant chimpanzee [13, 15]. Deformations caused by the infectious yaws disease may spread in wild great apes populations. Treponema bacteria transmitted via flies through wounds can cause total necrosis of the nose and lips [5]. In the population of gorillas of Lokoue in the Republic of Congo, 17% of the 377 identified gorillas had skin lesions generally localized on the face. The seriously handicapped individuals experienced difficulties in chewing and breathing [5]. The phenotypic features observed in Sebitoli chimpanzees have never been described in NHP but are reminiscent of those presented by humans suffering from the congenital Binder’s syndrome: hypoplastic mid-face profile, flattened nose, nostrils atypically crescent of semilunar in shape due to the short columella, reduced or absent nasal spine, convex upper lip, and sometimes malformations of cervical vertebrae and prognathism [3]. Binder’s syndrome seems to occur sporadically, but some familial cases have also been reported [8–10]. The etiology of this condition is connected with a disturbance of the prosencephalic induction in the third month of the intrauterine life when the nasal bone is formed [9]. The survey of the literature did not contradict the possibility of a genetic etiology. It is also proposed that such failure of development may be caused by prenatal exposure to agents that cause vitamin K deficiency such as lithium, ethanol, warfarin, or phenytoin. Several other human syndromes result in nasal defects (Johanson-Blizzard; Apert; Pfeiffer; trichorhinophalangeal syndromes), but they are often associated with other deformities and often not compatible with survival. Transplacentally acquired syphilis (Treponema pallidum) may cause collapse of the bony part of nose (called ‘saddle nose’) in infants. These infants also frequently suffer from pathological conditions to their bones, teeth, eyes, ears, and brain. In Japan, the macaque limb deformities were first reported only 3 years after the food provisioning was started there (T. Matsuzawa, personal communication). This suggests that the presence of pesticides in food may be an origin for these defects. In Kowloon, fuel emission was one of the teratogenic agents suspected to explain monkey deformities [2]. In investigating the origin of the Sebitoli malformations, there are several hypotheses that should be considered. First, as chimpanzees are male-philopatric, a mutation impacting the development of nasal structures
282
Krief et al.
may have originated from an adult male to his descendants. Secondly, inbreeding can also be suspected. In Bossou (Guinea), a male chimpanzee was born with six fingers in a small community of 12 individuals, and this community appears to be isolated from neighboring communities [6]. Third, the disturbance of nasal development may rather be acquired, considering the high rate of the phenotype. The mothers of the affected individuals may have been exposed during gestation either to a bacteria (such as a Treponema) that infected them, or to teratogenic agents when crop raiding for maize or guava, ingesting water, soil, or plants contaminated by chemical sprayed on tea growing around their home range. Additionally, in the 1970s during logging exploitation, their territory was treated with arboricides (Finopal DT, also called Agent Orange, a mixture of butyl esters of 2,4-D et 2,4,5-T, dissolved in heavy diesel oil; Agent Orange). Environmental pollutions (such as soil rich in heavy metals, most notably selenium) are well documented to produce malformations in several animal species including fish, birds, and mammals [11] and coal combustion waste in a large proportion of bullfrogs [12]. The home range of this chimpanzee community, the northern area of the Kibale National Park, is surrounded by human settlements and is crossed by a heavily trafficked tarmac road. It is very likely that the Sebitoli chimpanzees are also exposed to pollution from combustion exhaust gases and to lead in this exhaust. Further multidisciplinary studies are needed to better understand the extent of facial dysplasia of the Sebitoli chimpanzees described in this case report. Future research is needed to further identify the possible genetic relationship of these individuals, and/or to investigate the ecotoxicological context of the Sebitoli area to evaluate the possible impact these external pollutants have on this primate population. Acknowledgments Data have been collected in the context of a scientific agreement signed between National Museum of Natural History, Uganda Wildlife Authority and Makerere University. We are grateful to Uganda Wildlife Authority and Uganda National Council for Science and Technology for authorization to conduct research and to the National Museum of Natural History/ATM 16, ANR JC-JC SAFAPE, Projet pour la Conservation des Grands Singes for supporting and funding the project. We are particularly grateful to Ugandan assistants for their fieldwork. We are thankful to the anonymous reviewer for his/her valuable comments and edits of the manuscript.
J Med Primatol 43 (2014) 280–283 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Krief et al.
Facial dysplasia in wild chimpanzees
References 1 Brignolo L, Tarara R, Peterson PE, Hendrickx AG: Two cases of digital defects in Macaca mulatta infants and a survey of the literature. J Med Primatol 2002; 80:98–103. 2 Burton FD, Kin WaiChan LK: Congenital Limb Malformations in the free-tanging Macaques of Kowloon. J Med Primatol 1989; 18:397–403. 3 Dyer FMV, Wilmot DR: Maxillo-nasal dysplasia, Binder’s syndrome: review of the literature and case report. J Orthod 2002; 29: 15–21. 4 Kano T: Observations of physical abnormalities among the wild bonobos (Pan paniscus) of Wamba, Zaire. Am J Phys Anthropol 1984; 63:1–11. 5 Levrero F, Gatti S, Gautier-Hion A, Menard N: Yaws disease in a wild gorilla population and its impact on the reproductive status of males. Am J Phys Anthropol 2007; 132:568–75. 6 Matsuzawa T, Humle T, Sugiyama Y (Eds): The Chimpanzees of Bossou and Nimba. Japan: Springer. Doi: 10.1007/978-4-43153921-6. 7 Minezawa M, Nozawa K, Gotoh S, Yoshihiro S, Hamada Y, Inagaki H, Nigi H: A cytogenetic study on
8
9
10
11
12
13
14
congenital limb malformations in the Japanese monkey (Macaca fuscata). Primates 1990; 31:571–7. Mulhern D: Probable case of Binder syndrome in a skeleton from Quarai, New Mexico. Am J Phys Anthropol 2002; 118:371–7. Nedev P: The Binder syndrome: review of the literature and case report. Scripta Scientifica Medica 2008; 40:153–6. Olow-Norderam M, Radberg CT: Maxillonasal dysplasia (Binder syndrome) and associated malformations of the cervical spine. Acta Radiol Diagn (Stockh) 1984; 25:353–60. Rousseaux CG, Politis MJ, Keiner J: The effects of sodium selenite and selenomethionine on murine limb development in culture. Environ Toxicol Chem 1993; 12:1283–90. Rowe CL, Kinney OM, Congdon JD: Oral deformities in tadpoles of the bullfrog (Rana catesbeiana) caused by conditions in a polluted habitat. Copeia 1998; 244–6. Schultz AH: Acrocephalo-oligodactylism in a wild chimpanzee. J Anat 1958; 92:568–79. Stokes EJ, Byrne RW: The effect of snare injuries on the fig-feeding behaviour of chimpanzees of the Budongo Forest, Uganda:
J Med Primatol 43 (2014) 280–283 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
15
16
17
18
behavioural adaptations and longterm implications. In: The Primates of Western Uganda. Newton-Fisher, Notman, Paterson & Reynolds (eds). Chicago: SpringerVerlag, 2006; 281–97. Struhsaker TT, Chapman CA, Pope TR, Marcus JR: Healthy baboon with no upper jaw or nose: an extreme case of adaptability in the Kibale National Park, Uganda. Primates 2011; 52:15–8. Turner SE, Fedigan LM, Nobuhara H, Nobuhara T, Matthews HD, Nakamichi M: Monkeys with disabilities: prevalence and severity of congenital limb malformations in Macaca fuscata on Awaji Island. Primates 2008; 49:223–6. Waller JC, Reynolds V: Limb injuries resulting from snares and traps in chimpanzees (Pan troglodytes schweinfurthii) at the Budongo Forest, Uganda. Primates 2001; 42:135–9. Yoshihiro S, Goto S, Minezawa M, Muramatsu M, Saito Y, Sugita H, Nigi H: Frequency of occurrence, morphology, and causes of congenital malformation of limbs in the Japanese monkey. Ecotoxicol Environ Saf 1979; 3:458–70.
283
CASE REPORT
Facial dysplasia in wild chimpanzees rard Couly4,5 & Giovanni Levi5 Sabrina Krief1,2, Jean-Michel Krief2, Andrew Seguya3, Ge 1 2 3 4 5
UMR 7206 CNRS/MNHN/P7, Ecoathropologie et ethnobiologie, CP 135, Museum national d’histoire naturelle, Paris, France Projet pour la conservation des grands singes (PCGS), UWA Sebitoli Station, Kibale National Park, Fort Portal, Uganda Uganda Wildlife Authority, Kampala, Uganda Paris Descartes, Institut de la Bouche et du Visage de l’Enfant, Ho ^pital Universitaire Necker 149, Paris, France Universite gulations endocriniennes, Museum national d’histoire naturelle, Paris, France UMR 7221 CNRS/MNHN, Evolution des re
Keywords chimpanzee – congenital malformation – nasal defect Correspondence Sabrina Krief, UMR 7206 CNRS/MNHN/P7, Ecoathropologie et ethnobiologie, CP 135, Museum national d’histoire naturelle, 57 rue Cuvier, 75231 Paris Cedex 5, France. Tel.: +33 1 40 79 53 37; fax: +33 688 24 15 96; e-mail: [email protected]
Abstract At least 10% of the Sebitoli chimpanzee community of the Kibale National Park (Uganda) present a characteristic facial phenotype with flattened nose, reduced nostrils, and concave mid-face. Affected individuals do not present skin lesions, and also young infants are affected. We suggest, therefore, a congenital origin of this defect.
Accepted April 23, 2014.
Case report In the northern area of the Kibale National Park (Uganda) known as the ‘Sebitoli’ region, a wild chimpanzee (Pan troglodytes schweinfurthii) community has been undergoing a habituation program for 4 years. Approval for fieldwork has been obtained from Uganda Wildlife Authority and Uganda National Council for Science and Technology, and the research adheres to national and international ethics, protocols, and legal requirements. At least nine of the 80 identified individuals of this community share a characteristic facial phenotype. Their nose is flattened with reduced or absent nostrils and their mid-face is concave. None of them have facial scars, wounds, ulcers, or other skin lesions evoking yaws disease. One individual seems to present exophthalmos. The incidence of the facial phenotype is thus high with about 10% of the community affected. This unusual phenotype is present in male and female individuals of any class of age and sex: 1-year-old infants, juveniles, subadults, and young adults. The oldest affected individual has an estimated age of 16 years. The three mothers of younger affected individuals (two juveniles and two infants) do not present nasal
280
dysplasia. Two of the affected chimpanzees were born from the same mother, which has a normal-looking face and body except for a very light fur color. The older affected individual is entirely missing his left foot, resulting most likely from being caught in a snare (Table 1; Fig. 1). According to our monitoring, aside from facial abnormalities, all affected individuals appeared in good health and did not present other deformities. Individuals with flat face and reduced nose seem to maintain a normal respiratory function. The cause of the nasal defect present in the Sebitoli chimpanzees is unknown; however, its high incidence in a restricted population and its presence in a young infant suggest a congenital origin. To understand the possible etiology of this phenotype, we reviewed other reported malformations in wild primates. Limbs deformities, common in wild nonhuman primates (NHP), are usually the result of fight, falls, or consequences of being caught in snares set by poachers [14, 17]. The prevalence of congenital limb malformations is, however, normally less than 1% between both humans and NHP [1]; the only known exceptions are constituted by two food-provisioned colonies of semi-wild macaques in Hong Kong and in Japan, where the incidence can reach 17.1% of the total
J Med Primatol 43 (2014) 280–283 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Krief et al.
Facial dysplasia in wild chimpanzees
Table 1 Cases of facial dysplasia observed in Sebitoli chimpanzees, Kibale National Park, Uganda Chimpanzee code name
Sex
Mother
Estimated age
AG
M
Unknown
16
SA KB GA KR LV
F M M M M
Unknown KT KT KL LS
13 7 1,5 8 3
KW Unnamed #1
M F
KE Unknown
5 9
Unnamed #2
M
Unknown
8
Description of the defect Concave mid-face profile, flat nose, nostrils absent, concave shape of the area of nasal spine, 3 deep notches, asymmetry of the nasal fossa, missing left foot Concave mid-face profile, flat nose, the absence of nasal wings Flat nose Flat nose Flat nose Asymmetrical and reduced nostrils, three median notches on the nose, swollen areas both sides of the nose Flat nose Flat nose, absence of nasal wings, asymmetry of the fossa, swollen area both sides of the nose Absence of nasal wings and round fossa of nose, exophthalmos
Fig. 1 Photographs of chimpanzees with facial dysplasia and normal phenotype, Kibale National Park, Uganda: (1) immature individuals (1A) LV (immature); (1B) Unnamed #1 (immature); (1C) Unnamed #2 (immature); (1D) an infant chimpanzee with a normal phenotype. (2) adult individuals (2A) AG (adult); (2B) an adult chimpanzee with a normal phenotype. J Med Primatol 43 (2014) 280–283 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
281
Facial dysplasia in wild chimpanzees
population [2, 7, 16, 18]. In great apes, such deformities are rarely reported [4, 13, 17]. Only two cases of facial congenital deformities have been so far reported in wild NHP: an adult female baboon symmetrically missing most of her upper jaw and nose; a case of acrocephalo-dactylism in an infant chimpanzee [13, 15]. Deformations caused by the infectious yaws disease may spread in wild great apes populations. Treponema bacteria transmitted via flies through wounds can cause total necrosis of the nose and lips [5]. In the population of gorillas of Lokoue in the Republic of Congo, 17% of the 377 identified gorillas had skin lesions generally localized on the face. The seriously handicapped individuals experienced difficulties in chewing and breathing [5]. The phenotypic features observed in Sebitoli chimpanzees have never been described in NHP but are reminiscent of those presented by humans suffering from the congenital Binder’s syndrome: hypoplastic mid-face profile, flattened nose, nostrils atypically crescent of semilunar in shape due to the short columella, reduced or absent nasal spine, convex upper lip, and sometimes malformations of cervical vertebrae and prognathism [3]. Binder’s syndrome seems to occur sporadically, but some familial cases have also been reported [8–10]. The etiology of this condition is connected with a disturbance of the prosencephalic induction in the third month of the intrauterine life when the nasal bone is formed [9]. The survey of the literature did not contradict the possibility of a genetic etiology. It is also proposed that such failure of development may be caused by prenatal exposure to agents that cause vitamin K deficiency such as lithium, ethanol, warfarin, or phenytoin. Several other human syndromes result in nasal defects (Johanson-Blizzard; Apert; Pfeiffer; trichorhinophalangeal syndromes), but they are often associated with other deformities and often not compatible with survival. Transplacentally acquired syphilis (Treponema pallidum) may cause collapse of the bony part of nose (called ‘saddle nose’) in infants. These infants also frequently suffer from pathological conditions to their bones, teeth, eyes, ears, and brain. In Japan, the macaque limb deformities were first reported only 3 years after the food provisioning was started there (T. Matsuzawa, personal communication). This suggests that the presence of pesticides in food may be an origin for these defects. In Kowloon, fuel emission was one of the teratogenic agents suspected to explain monkey deformities [2]. In investigating the origin of the Sebitoli malformations, there are several hypotheses that should be considered. First, as chimpanzees are male-philopatric, a mutation impacting the development of nasal structures
282
Krief et al.
may have originated from an adult male to his descendants. Secondly, inbreeding can also be suspected. In Bossou (Guinea), a male chimpanzee was born with six fingers in a small community of 12 individuals, and this community appears to be isolated from neighboring communities [6]. Third, the disturbance of nasal development may rather be acquired, considering the high rate of the phenotype. The mothers of the affected individuals may have been exposed during gestation either to a bacteria (such as a Treponema) that infected them, or to teratogenic agents when crop raiding for maize or guava, ingesting water, soil, or plants contaminated by chemical sprayed on tea growing around their home range. Additionally, in the 1970s during logging exploitation, their territory was treated with arboricides (Finopal DT, also called Agent Orange, a mixture of butyl esters of 2,4-D et 2,4,5-T, dissolved in heavy diesel oil; Agent Orange). Environmental pollutions (such as soil rich in heavy metals, most notably selenium) are well documented to produce malformations in several animal species including fish, birds, and mammals [11] and coal combustion waste in a large proportion of bullfrogs [12]. The home range of this chimpanzee community, the northern area of the Kibale National Park, is surrounded by human settlements and is crossed by a heavily trafficked tarmac road. It is very likely that the Sebitoli chimpanzees are also exposed to pollution from combustion exhaust gases and to lead in this exhaust. Further multidisciplinary studies are needed to better understand the extent of facial dysplasia of the Sebitoli chimpanzees described in this case report. Future research is needed to further identify the possible genetic relationship of these individuals, and/or to investigate the ecotoxicological context of the Sebitoli area to evaluate the possible impact these external pollutants have on this primate population. Acknowledgments Data have been collected in the context of a scientific agreement signed between National Museum of Natural History, Uganda Wildlife Authority and Makerere University. We are grateful to Uganda Wildlife Authority and Uganda National Council for Science and Technology for authorization to conduct research and to the National Museum of Natural History/ATM 16, ANR JC-JC SAFAPE, Projet pour la Conservation des Grands Singes for supporting and funding the project. We are particularly grateful to Ugandan assistants for their fieldwork. We are thankful to the anonymous reviewer for his/her valuable comments and edits of the manuscript.
J Med Primatol 43 (2014) 280–283 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Krief et al.
Facial dysplasia in wild chimpanzees
References 1 Brignolo L, Tarara R, Peterson PE, Hendrickx AG: Two cases of digital defects in Macaca mulatta infants and a survey of the literature. J Med Primatol 2002; 80:98–103. 2 Burton FD, Kin WaiChan LK: Congenital Limb Malformations in the free-tanging Macaques of Kowloon. J Med Primatol 1989; 18:397–403. 3 Dyer FMV, Wilmot DR: Maxillo-nasal dysplasia, Binder’s syndrome: review of the literature and case report. J Orthod 2002; 29: 15–21. 4 Kano T: Observations of physical abnormalities among the wild bonobos (Pan paniscus) of Wamba, Zaire. Am J Phys Anthropol 1984; 63:1–11. 5 Levrero F, Gatti S, Gautier-Hion A, Menard N: Yaws disease in a wild gorilla population and its impact on the reproductive status of males. Am J Phys Anthropol 2007; 132:568–75. 6 Matsuzawa T, Humle T, Sugiyama Y (Eds): The Chimpanzees of Bossou and Nimba. Japan: Springer. Doi: 10.1007/978-4-43153921-6. 7 Minezawa M, Nozawa K, Gotoh S, Yoshihiro S, Hamada Y, Inagaki H, Nigi H: A cytogenetic study on
8
9
10
11
12
13
14
congenital limb malformations in the Japanese monkey (Macaca fuscata). Primates 1990; 31:571–7. Mulhern D: Probable case of Binder syndrome in a skeleton from Quarai, New Mexico. Am J Phys Anthropol 2002; 118:371–7. Nedev P: The Binder syndrome: review of the literature and case report. Scripta Scientifica Medica 2008; 40:153–6. Olow-Norderam M, Radberg CT: Maxillonasal dysplasia (Binder syndrome) and associated malformations of the cervical spine. Acta Radiol Diagn (Stockh) 1984; 25:353–60. Rousseaux CG, Politis MJ, Keiner J: The effects of sodium selenite and selenomethionine on murine limb development in culture. Environ Toxicol Chem 1993; 12:1283–90. Rowe CL, Kinney OM, Congdon JD: Oral deformities in tadpoles of the bullfrog (Rana catesbeiana) caused by conditions in a polluted habitat. Copeia 1998; 244–6. Schultz AH: Acrocephalo-oligodactylism in a wild chimpanzee. J Anat 1958; 92:568–79. Stokes EJ, Byrne RW: The effect of snare injuries on the fig-feeding behaviour of chimpanzees of the Budongo Forest, Uganda:
J Med Primatol 43 (2014) 280–283 © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
15
16
17
18
behavioural adaptations and longterm implications. In: The Primates of Western Uganda. Newton-Fisher, Notman, Paterson & Reynolds (eds). Chicago: SpringerVerlag, 2006; 281–97. Struhsaker TT, Chapman CA, Pope TR, Marcus JR: Healthy baboon with no upper jaw or nose: an extreme case of adaptability in the Kibale National Park, Uganda. Primates 2011; 52:15–8. Turner SE, Fedigan LM, Nobuhara H, Nobuhara T, Matthews HD, Nakamichi M: Monkeys with disabilities: prevalence and severity of congenital limb malformations in Macaca fuscata on Awaji Island. Primates 2008; 49:223–6. Waller JC, Reynolds V: Limb injuries resulting from snares and traps in chimpanzees (Pan troglodytes schweinfurthii) at the Budongo Forest, Uganda. Primates 2001; 42:135–9. Yoshihiro S, Goto S, Minezawa M, Muramatsu M, Saito Y, Sugita H, Nigi H: Frequency of occurrence, morphology, and causes of congenital malformation of limbs in the Japanese monkey. Ecotoxicol Environ Saf 1979; 3:458–70.
283
