Skip to main content
SpringerLink
Log in

Congenital malformations in Japanese macaques (Macaca fuscata) at Takasakiyama

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

From the late 1960s to the early 1970s, many congenitally malformed infants were born into provisioned Japanese macaque troops. Although the exact cause of this problem was not determined, the occurrence of malformations decreased thereafter. We examined possible factors such as total population size, number of adult females, birth rate, and volume of provisioned food. Agrichemicals attached to provisioned food are suspected as the main cause, as other factors were found to have no influence. Many more malformations were seen in males compared with females, in feet compared with hands, and in the fourth compared with other digits. We confirmed that the frequency of congenital malformation was high during the 1960s through to the mid-1970s when increased levels of provisioned food were given and that the incidence of congenital malformations was also elevated among wild macaques during this time.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ariyoshi S (1975) Fukugou Osen (Composite Pollution). Shinchosha, Tokyo (in Japanese)

  • Brignolo L, Tarara R, Peterson PE, Hendrickx AG (2002) Two cases of digital defects in Macaca mulatta infants and a survey of the literature. J Med Primatol 31:98–103

    Article  PubMed  CAS  Google Scholar 

  • Burton FD, Chan LKW (1989) Congenital limb malformations in the free-ranging macaques of Kowloon. J Med Primatol 18:397–403

    PubMed  CAS  Google Scholar 

  • Furuya Y (1958) Malformed infants of Japanese monkeys. Yaen (Wild Monkeys) 1:15–17 (in Japanese)

    Google Scholar 

  • Furuya Y (1966) On the malformation occurred in the Gagyusan troop of wild Japanese monkeys. Primates 7:488–492

    Article  Google Scholar 

  • Homma T (1980) Sequential pattern of limb anomalies in Japanese monkeys on Awajishima island. Primates 21:20–30

    Article  Google Scholar 

  • Itani J, Mizuhara H (1957) On the malformation seen in Japanese monkeys at Takasakiyama. Jikken Dobutsu (Experim Anim) 6:105–107 (in Japanese)

    Google Scholar 

  • Itani J, Tokuda K, Furuya Y, Kano K, Shin Y (1963) The social construction of natural troops of Japanese monkeys in Takasakiyama. Primates 4(3):1–42

    Article  Google Scholar 

  • Ito M, Ogawa K, Sonobe T, Nakaminami G, Ishida N, Watanabe N, Inagaki H, Nigi H (1988) Relation of the congenital limb-malformation in the Japanese monkeys and organochlorin pesticides. Primate Res 4:103–113 (in Japanese with English summary)

    Article  Google Scholar 

  • Iwamoto M (1967) Morphological observations on the congenital malformation of limbs in the Japanese monkey. Primates 8:247–270

    Article  Google Scholar 

  • Iwamoto M, Hirai M (1970) Case report on a Japanese monkey with congenital malformation on the limbs. Primates 11:395–398

    Article  Google Scholar 

  • JMAP (Japanese Monkey Abnormality Problem Research Group). 1979. Abnormal monkeys: research report from Wild Monkey Parks, Tokyo, Chobunsha (in Japanese)

  • Kristensen P, Irgens LM, Andersen A, Bye AS, Sundheim L (1997) Birth defects among offspring of Norwegian farmers, 1967–1991. Epidemiology 8:537–544

    Article  PubMed  CAS  Google Scholar 

  • Kurita H (2007) Comparison of artificial food intake between high and low ranking females among provisioned, free-ranging Japanese macaques (Macaca fuscata) at Takasakiyama: preliminary report. Primate Res 23:25–32 (in Japanese with English summary)

    Article  Google Scholar 

  • Kurita H, Sugiyama Y, Ohsawa H, Hamada Y, Watanabe T (2008) Changes in demographic parameters of Macaca fuscata at Takasakiyama in relation to decrease of provisioned foods. Int J Primatol 29:1189–1202

    Article  Google Scholar 

  • Masui K, Nishimura A, Ohsawa H, Sugiyama Y (1973) Population study of Japanese monkeys at Takasakiyama I. J Anthropol Soc Nippon 81:236–248

    Article  Google Scholar 

  • Merio GR, Paleari L, Mantero S, Genova F, Beverdam A, Palmisano GL, Barbien O, Levi G (2002) Mouse model of split hand/foot malformation type 1. Genesis 33:97–101

    Article  CAS  Google Scholar 

  • Minezawa M, Nozawa K, Gotoh S, Yoshihiro S, Hamada Y, Inagaki H, Nigi H (1990) A cytogenetic study on congenital limb malformation in the Japanese monkey (Macaca fuscata). Primates 31:571–577

    Article  Google Scholar 

  • Minezawa M, Matsui T, Nigi H (1992) Partial albinism in distal part of limbs observed in Takasakiyama Japanese monkey. Primate Res 8:33–47 (in Japanese with English summary)

    Article  Google Scholar 

  • Nakamichi M, Nobuhara H, Nobuhara T, Nakahashi M, Nigi H (1997) Birth rate and mortality rate of infants with congenital malformations of the limbs in the Awajishima free-ranging group of Japanese monkeys (Macaca fuscata). Am J Primatol 42:225–234

    Article  PubMed  CAS  Google Scholar 

  • Nigi H (1982) Japanese monkeys: physiology of sex. Tokyo, Dobutsu-sya (in Japanese)

  • Nozawa K (1975) Genetics of non-human primates. Rinsho Kagaku (Clinic Sci) 11: 880–892 (in Japanese)

  • Nozawa K (1979) On the survey of congenital limb malformation in Japanese macaques. In: Reports on environmental science research B23-S14-1, special research on developmental abnormality. Ministry of Science and Education, Japan, pp 28–30 (in Japanese)

  • Nozawa K (1991) Population genetics of non-human primates. Primate Res 7:23–62 (in Japanese with English Summary)

    Article  Google Scholar 

  • Nozawa K, Shotake T, Minezawa M, Kawamoto Y, Hayasaka K, Kawamoto Y (1996) Population-genetic studies of the Japanese macaque, Macaca fuscata. In: Shotake T, Wada K (eds) Variations in the Asian macaques. Tokai University Press, Tokyo, pp 1–36

    Google Scholar 

  • Sackett GP (2008) Developmental disabilities and primate models defined. In: Burbacher TM, Sackett GP, Grant KS (eds) Primate models of children’s health and developmental disabilities. Academic Press, Amsterdam, pp 1–18

    Chapter  Google Scholar 

  • Schecter A, Dai LC, Thuy LT, Quyuh HT, Minh DQ, Can HD, Phiet PH, Ngyen NT, Constable JD, Baughman R (1995) Agent Orange and Vietnamese: the persistence of elevated dioxin levels in human tissues. Am J Pub Health 85:516–522

    Article  CAS  Google Scholar 

  • Schultz AH (1944) Age changes and variability in gibbons. Am J Phys Anthropol 2:1–159

    Article  Google Scholar 

  • Shidei T, Nigi H, Nozawa K, Gotoh S (1981) Studies on congenital limb malformation of Japanese macaques and its cause. Rep Res Fund Ministry Sci Edu, Jpn, 1958–1959. Inuyama, Japan Monkey Centre (in Japanese)

  • Sokal RR, Rohlf JF (1995) Biometry. Freeman, New York

    Google Scholar 

  • Soumah AG, Yokota N (1991) Female rank and feeding strategies in a free-ranging provisioned troop of Japanese macaques. Folia Primatol 57:191–200

    Article  Google Scholar 

  • SPSS Inc (1995). SPSS Exact Tests ™ 6.1 for Windows ™. Chicago, SPSS Inc

  • SPSS Inc (2001). SPSS Base 11.0J user’s guide. Chicago, SPSS Inc

  • Sugiyama Y, Iwamoto T, Ono Y (1995) Population control of artificially fed Japanese macaques. Primate Res 11:197–207 (in Japanese with English summary)

    Article  Google Scholar 

  • Turner SE, Gould K, Duffus DA (2005) Maternal behavior and infant congenital limb malformation in a free-ranging group of Macaca fuscata on Awaji Island, Japan. Int J Primatol 26:1435–1457

    Article  Google Scholar 

  • Turner S, Fedigan L, Nobuhara H, Nobuhara T, Matthews H, Nakamichi M (2008) Monkeys with disabilities: prevalence and severity of congenital limb malformations in Macaca fuscata on Awaji Island. Primates 49:223–226

    Article  PubMed  Google Scholar 

  • Tuyet LTN, Johansson A (2001) Impact of chemical warfare with agent orange on women’s reproductive lives in Vietnam: a pilot study. Reprod Health Matters 9:156–164

    Article  Google Scholar 

  • Yoshihiro S, Goto S, Minezawa M, Muramatsu M, Saito Y, Sugita H, Nigi H (1979) Frequency of occurrence, morphology, and causes of congenital malformation of limbs in the Japanese monkey. Ecotoxicol Environ Safe 3:458–470

    Article  CAS  Google Scholar 

  • Yoshimura J, Fujiki T, Kawai T, Amagai H (2003) How supplemental food may induce abnormality in wild Japanese macaque populations. Evol Ecol Res 5:1103–1109

    Google Scholar 

  • Zguricas J, Bakker WF, Heus H, Lindhout D, Heutink P, Hovius SER (1998) Genetics and limb development and congenital hand malformations. Plast Reconstr Surg 101:1126–1135

    Article  PubMed  CAS  Google Scholar 

  • Zhou E, Grimes P, Favor J, Koeboerlein B, Pretsch W, Newhauser-Klaus A, Sidjain D, Stambolian D (1997) Genetic mapping of a mouse ocular malformation locus, Tcm, to chromosome 4. Mam Genome 8:178–181

    Article  CAS  Google Scholar 

  • Zuniga A, Zeller R, Probst S (2012) The molecular basis of human congenital limb malformations. WIREs Dev Biol 1:803–822

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Basic records of malformation seen in newborn Japanese macaques at Takasakiyama were collected by many Takasakiyama Natural Park staff, and population surveys were carried out by staff and students of Kyoto University Primate Research Institute and Takasakiyama. The managers of the Takasakiyama Natural Zoo allowed us to use yearly records. Drs. Vanessa Hayes and Yoshi Kawamoto kindly commented and revised our earlier drafts. We are grateful to all these persons.

Author information

Authors and Affiliations

  1. Kyoto University Primate Research Institute, Inuyama, Japan

    Yukimaru Sugiyama

  2. Board of Education, Oita, Oita, Japan

    Hiroyuki Kurita

  3. Takasakiyama Natural Zoo, Oita, Japan

    Takeshi Matsui, Satoshi Kimoto & Junko Egawa

  4. Kitabesso 23-3, Inuyama, 484-0081, Japan

    Yukimaru Sugiyama

Authors
  1. Yukimaru Sugiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroyuki Kurita
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takeshi Matsui
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Satoshi Kimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junko Egawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yukimaru Sugiyama.

About this article

Cite this article

Sugiyama, Y., Kurita, H., Matsui, T. et al. Congenital malformations in Japanese macaques (Macaca fuscata) at Takasakiyama. Primates 55, 303–311 (2014). https://doi.org/10.1007/s10329-014-0405-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-014-0405-7

Keywords

Search

Navigation