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Malaria in macaques

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Abstract

Seven species of malaria naturally infect eight species of macaques in southwestern India, Sri Lanka, and Southeast Asia. Within malarious areas, the frequency of infections in infected species of macaques varies from 9 to 61%. Natural malarial infections in macaques are relatively benign. The proved or probable vectors of macaque malaria are seven species of mosquitoes that belong to the Leucosphyrus Group of the genus Anopheles. The geographic distribution of macaque malaria apparently is determined by the distribution of the Leucosphyrus Group of mosquitoes, which in turn apparently is determined by the distribution of tropical evergreen rain forest. Experimental infections with three species of macaque malaria frequently are lethal to populations or species of macaques that inhabit areas outside the geographic ranges of the parasites. In populations or species of macaques that are sympatric with experimentally virulent species of malaria, partial resistance probably evolved as a consequence of natural selection acting on favorable mutations.

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References

  • Actams, J. H., Hudson, D. E., Torli, M., Ward, G. E., Wellems, T. E., Aikawa, M., and Miller, L. H. (1990). The Duffy receptor family ofPlasmodium knowlesi is located within the micronemes of invasive malaria merozoites.Cell 63: 141–153.

    Article  Google Scholar 

  • Aikawa, M., Brown, A., Smith, C. D., Tegoshi, T., Howard, R. J., Hasler, T. H., Ito, Y., Perry, G., Collins, W. E., and Webster, K. (1992). A primate model for human cerebral malaria:Plasmodium coatneyi-infected rhesus monkeys.Am. J. Trop. Med. Hyg. 46: 391–397.

    PubMed  CAS  Google Scholar 

  • Anderson, R. M., and May, R. M. (1982). Coevolution of hosts and parasites.Parasitology 85: 411–426.

    Article  PubMed  Google Scholar 

  • Baimai, V., Andre, R. G., Harrison, B. A., Kijchalao, U., and Panthusiri, L. (1987). Crossing and chromosomal evidence for two additional sibling species within the taxonAnopheles dirus Peyton and Harrison (Diptera: Culicidae) in Thailand.Proc. Entomol. Soc. Wash. 89: 157–166.

    Google Scholar 

  • Baimai, V., Harbach, R. E., and Kijchalao, U. (1988a). Cytogenetic evidence for a fifth species within the taxonAnopheles dirus in Thailand.J. Am. Mosq. Control Assoc. 4: 333–338.

    PubMed  CAS  Google Scholar 

  • Baimai, V., Harbach, R. E., and Sukowati, S. (1988b). Cytogenetic evidence for two species within the current concept of the malaria vectorAnopheles leucosphyrus in Southeast Asia.J. Am. Mosq. Control Assoc. 4: 44–50.

    PubMed  CAS  Google Scholar 

  • Bennet, G. F., and Warren, M. (1965). Transmission of a new strain ofPlasmodium cynomolgi to man.J. Parasitol. 51: 79–80.

    Article  Google Scholar 

  • Bray, R. S. (1963). Malaria infections in primates and their importance to man.Ergeb. Mikrob. Immun. Exp. Ther. 36: 168–213.

    Google Scholar 

  • Brug, S. L. (1934). Observations on monkey malaria.Riv. Malarial. 13: 121–142.

    Google Scholar 

  • Chasen, F. N. (1940). A handlist of Malaysian mammals.Bull. Raffles Mus., 15: i-xx, 1–209.

    Google Scholar 

  • Cheong, W. H., Warren, M., Omar, A. H., and Mahadevan, S. (1965).Anopheles balabacensis balabacensis identified as vector of simian malaria in Malaysia.Science 150: 1314–1315.

    Article  PubMed  CAS  Google Scholar 

  • Chin, W., Contacos, P. G., Coatney, C. R., and Kimball, H. R. (1965). A naturally acquired quotidian-type malaria in man transferable to monkeys.Science 149: 865.

    Article  PubMed  CAS  Google Scholar 

  • Choudhury, D. S., Mohan, B. N., Satya Prakash, and Ramakrishnan, S. P. (1963a). Experimental susceptibility of anopheline mosquitoes to simian malaria in the Nilgiris, Madras State, South India.Indian J. Malarial. 17: 237–242.

    CAS  Google Scholar 

  • Choudhury, D. S., Wattal, B. L., and Ramakrishnan, S. P. (1963b). Incrimination ofAnopheles elegans James (1903) as a natural vector of simian malaria in the Nilgiris, Madras State, South India.Indian J. Malarial. 17: 243–247.

    CAS  Google Scholar 

  • Coatney, G. R., Collins, W. E., Warren, M., and Contacos, P. G. (1971).The Primate Malarias, U.S. Government Printing Office, Washington, D.C.

    Google Scholar 

  • Colless, D. H. (1956). TheAnopheles leucosphyrus group.Trans. R. Entomol. Soc. Lond. 108: 37–116.

    Google Scholar 

  • Colless, D. H. (1957). Further notes on the systematics and distribution of theAnopheles leucosphyrus group (Diptera: Culicidae).Proc. R. Entomol. Soc. Lond. 26: 131–139.

    Google Scholar 

  • Collins, W. E. (1988). Major animal models in malaria research: Simian. In Wernsdorfer, W. H., and McGregor, I. (eds.),Malaria: Principles and Practice of Malariology, Churchill Livingstone, Edinburgh, pp. 1473–1501.

    Google Scholar 

  • Corbet, G. B., and Hill, J. E. (1992).The Mammals of the Indomalayan Region: A Systematic Review, Oxford University Press, Oxford.

    Google Scholar 

  • Davis, T. M. E., Brown, A. E., and Smith, C. D. (1993). Metabolic disturbances inPlasmodium coatneyi-infected rhesus monkeys.Int. J. Parasitol. 23: 557–563.

    Article  PubMed  CAS  Google Scholar 

  • Desowitz, R. S., Miller, L. H., Buchanan, R. D., Yuthasastrkosol, V., and Permpanich, B. (1967). Comparative studies on the pathology and host physiology of malarias. I.Plasmodium coatneyi. Ann. Trop. Med. Parasitol. 61: 365–374.

    CAS  Google Scholar 

  • Desowitz, R. S., Miller, L. H., Buchanan, R. D., and Permpanich, B. (1968). Comparative studies on the pathology and host physiology of malarias. VI.Plasmodium inui. Ann. Trop. Med Parasitol. 62: 233–237.

    CAS  Google Scholar 

  • Dissanaike, A. S. (1963).Plasmodium infection in Ceylon monkeys.Trans. R. Soc. Trop. Med. Hyg. 57: 488–489.

    Article  Google Scholar 

  • Dissanaike, A. S. (1965). Simian malaria parasites of Ceylon.Bull. WHO 32: 593–597.

    PubMed  CAS  Google Scholar 

  • Dissanaike, A. S., Nelson, P., and Garnham, P. C. C. (1965a). Two new malaria parasites,Plasmodium cynomolgi ceylonensis subsp. nov. andPlasmodium fragile sp. nov., from onkeys in Ceylon.Ceylon J. Med. Sci. (D) 14: 1–9.

    Google Scholar 

  • Dissanaike, A. S., Nelson, P., and Garnham, P. C. C. (1965b).Plasmodium simiovale sp. nov., a new simian malaria parasite from Ceylon.Ceylon J. Med. Sci. (D) 14: 27–32.

    Google Scholar 

  • Donovan, C. (1920). Malaria of monkeys at the foot of the Nilgiris during the months of May and June, 1919.Indian J. Med. Res. 7: 717–721.

    Google Scholar 

  • Donovan, J. C., Stokes, W. S., Montrey, R. D., and Rozmiarek, H. (1983). Hematologic characterization of naturally occurring malaria(Plasmodium inui) in cynomolgus monkeys(Macaca fascicularis).Lab. Anim. Sci. 33: 86–89.

    PubMed  CAS  Google Scholar 

  • Dutta, G. P., Singh, P. P., and Banyal, H. S. (1978).Macaca assamensis as a new host for experimentalPlasmodium knowlesi infection.Indian J. Med. Res. 68: 923–926.

    PubMed  CAS  Google Scholar 

  • Edeson, J. F. B., and Davey, D. G. (1953). Isolation of a virulent strain ofPlasmodium knowlesi Sinton and Mulligan, 1932.Trans. R. Soc. Trop. Med. Hyg. 47: 259–260.

    Article  Google Scholar 

  • Ewald, P. W. (1983). Host-parasite relations, vectors, and the evolution of disease severity.Annu. Rev. Ecol. Syst. 14: 465–485.

    Article  Google Scholar 

  • Eyles, D. E. (1963). The species of simian malaria: taxonomy, morphology, life cycle, and geographical distribution of the monkey species.J. Parasitol. 49: 866–887.

    Article  PubMed  CAS  Google Scholar 

  • Eyles, D. E., and Warren, M. (1962).Plasmodium inui in Sulawesi.J. Parasitol. 48: 739.

    Article  Google Scholar 

  • Eyles, D. E., Laing, A. B. G., and Dobrovolny, C. G. (1962a). The malaria parasites of the pig-tailed macaque,Macaca nemestrina nemestrina (Linnaeus), in Malaya.Indian J. Malariol. 16: 285–298.

    Google Scholar 

  • Eyles, D. E., Laing, A. B. G., and Yap, L. F. (1962b).Plasmodium fieldi sp. nov., a new species of malaria parasite from the pig-tailed macaque in Malaya.Ann. Trop. Med Parasitol. 56: 242–247.

    PubMed  CAS  Google Scholar 

  • Eyles, D. E., Yap, L. F., Warren, M., Guinn, E., Sandosham, A. A., and Wharton, R. H. (1962c).Plasmodium coatneyi, a new species of primate malaria from Malaya.Am. J. Trop. Med. Hyg. 11: 597–604.

    Google Scholar 

  • Eyles, D. E., Dunn, F. L., Warren, M., and Guinn, E. (1963a).Plasmodium coatneyi from the Philippines.J. Parasitol. 49: 1038.

    Article  PubMed  CAS  Google Scholar 

  • Eyles, D. E., Warren, M., Guinn, E., Wharton, R. H., and Ramachandran, C. P. (1963b). Identification ofAnopheles balabacensis introlatus as a vector of monkey malaria in Malaya.Bull. WHO 28: 134–135.

    PubMed  CAS  Google Scholar 

  • Eyles, D. E., Wharton, R. H., Cheong, W. H., and Warren, M. (1964). Studies on malaria andAnopheles balabacensis in Cambodia.Bull. WHO 30: 7–21.

    PubMed  CAS  Google Scholar 

  • Flint, J., Hill, A. V. S., Bowden, D. K., Oppenheimer, S. J., Sill, P. R., Serjeantson, S. W., Bana-Koiri, J., Bhatia, K., Alpers, M. P., Boyce, A. J., Weatherall, D. J., and Clegg, J. B. (1986). High frequencies of a-thalassaemia are the result of natural selection by malaria.Nature 321: 744–750.

    Article  PubMed  CAS  Google Scholar 

  • Fooden, J. (1969). Taxonomy and evolution of the monkeys of Celebes.Bibl. Primatol. 20: 1–148.

    Google Scholar 

  • Fooden, J. (1971). Report on primates collected in western Thailand January-April, 1967.Fieldiana Zool. 59: 1–62.

    Google Scholar 

  • Fooden, J. (1975a). Taxonomy and evolution of liontail and pigtail macaques (Primates: Cercopithecidae).Fieldiana Zool. 67: 1–169.

    Google Scholar 

  • Fooden, J. (1975b). Primates obtained in peninsular Thailand June-July, 1973, with notes on the distribution of continental Southeast Asian leaf-monkeys(Presbytis).Primates 17: 95–118. (For date of publication, see back cover.)

    Article  Google Scholar 

  • Fooden, J. (1982). Ecogeographic segregation of macaque species.Primates 23: 574–579.

    Article  Google Scholar 

  • Fooden, J. (1991). New perspectives on macaque evolution. In Ehara, A., Kiraura, T., Takenaka, O., and Iwamoto, I. (eds.),Primatology Today, Elsevier, Amsterdam, pp. 1–7.

    Google Scholar 

  • Fooden, J., Mahabal, A., and Saha, S. S. (1981). Redefinition of rhesus macaque-bonnet macaque boundary in peninsular India (Primates:Macaca mulatto, M. radiata).J. Bombay Nat. Hist. Soc. 78: 463–474.

    Google Scholar 

  • Garnham, P. C. C. (1966).Malaria Parasites and Other Haemosporidia, Blackwell, Oxford.

    Google Scholar 

  • Garnham, P. C. C. (1973a). Second roundtable discussion on taxonomic problems relating to malaria parasites.J. Protozool 20:37–42.

    PubMed  CAS  Google Scholar 

  • Garnham, P. C. C. (1973b). Distribution of malaria parasites in primates, insectivores and bats.Symp. Zool. Soc. Lond. 33: 377–404.

    Google Scholar 

  • Garnham, P. C. C. (1980). Malaria in its various vertebrate hosts. In Krier, J. P. (ed.),Malaria: Vol. 1. Epidemiology, Chemotherapy, Morphology, and Metabolism, Academic Press, New York, pp. 95–144.

    Google Scholar 

  • Goldman, I. F., Collins, W. E., Parekh, K. H., and Lal, A. A. (1992). Circumsporite protein gene ofPlasmodium fieldi andPlasmodium coatneyi, two monkey malaria parasites.Am. J. Trop. Med. Hyg. 47(4, suppl.): 109 (abstract only).

    Google Scholar 

  • Green, R. (1932). A malarial parasite of Malayan monkeys and its development in anopheline mosquitoes.Trans. R. Soc. Trop. Med. Hyg. 25: 455–477.

    Article  Google Scholar 

  • Halberstaedter, L., and von Prowazek, S. (1907). Untersuchungen üüber die Malariaparasiten der Affen.Arb. K. Gesundh. -Amte (Berl.) 26: 37–43.

    Google Scholar 

  • Harrison, B. A. Rattanarithikul, R., Peyton, E. L., and Mongkolpanya, K. (1991). Taxonomic changes, revised occurrence records and notes on the Culicidae of Thailand and neighboring countries.Mosq. Syst. 22: 196–227. [For date of publication, seeMosq. Syst. 24: 217 (1992).]

    Google Scholar 

  • Herre, E. A. (1993). Population structure and the evolution of virulence in nematode parasites of fig wasps.Science 259: 1442–1445.

    Article  PubMed  Google Scholar 

  • Hodgkin, E. P. (1950). TheAnopheles umbrosus group (Diptera: Culicidae). II. Biology and transmission of malaria.Trans. R. Entomol. Soc. London. 101: 319–334.

    Google Scholar 

  • Howard, L. M., and Cabrera, B. D. (1961). Simian malaria in the Philippines.Science 134: 555–556.

    Article  PubMed  CAS  Google Scholar 

  • Hsieh, H.-C. (1960). Malaria parasites of the Taiwan monkey.Formosan Sci. 14: 477–487.

    Google Scholar 

  • Hu Xiaosu, Hu Anqi, Lin Fangqing, Yan Heping, Zhu Shenghua, and Deng Anxiao (1982). On the infection ofMacaca thibetanus withPlasmodium knowlesi Acta Zool. Sinica 28: 200–201 (in Chinese).

    Google Scholar 

  • Inoki, S., Okuno, Y., and Aoyama, A. (1951). On the length of the asexual life cycle ofPlasmodium inui var.cyclopis. Med. J. Osaka Univ. 2: 37–43.

    Google Scholar 

  • Jayewardene, L. G. (1963). Morphology of the erythrocytic stage ofPlasmodium inui Halberstadter and Prowazek, 1907, in the toque monkey,Macaca sinica from Ceylon.Indian J. Malariol 17: 365–372.

    PubMed  CAS  Google Scholar 

  • Kalra, N. L. (1980). Emergence of malaria zoonosis of simian origin as natural phenomenon in Greater Nicobars, Andaman & Nicobar Islands—A preliminary note.J. Commun. Dis. 12: 49–54.

    PubMed  CAS  Google Scholar 

  • Kawai, S., Aikawa, M., Kano, S., and Suzuki, M. (1993). A primate model for severe human malaria with cerebral involvement:Plasmodium coatneyi-infectedMacaco fuscata.Am. J. Trop. Med. Hyg. 48: 630–636.

    PubMed  CAS  Google Scholar 

  • Keymer, A. E., and Read, A. F. (1991). Behavioural ecology: The impact of parasitism. In Toft, C. A., Aeschlimann, A., and Bolis, L. (eds.),Parasite-Host Associations: Coexistence or Conflict?, Oxford University Press, Oxford, pp. 37–61.

    Google Scholar 

  • Klein, T. A., Harrison, B. A., Dixon, S. V., and Burge, J. R. (1991). Comparative susceptibility of Southeast AsianAnopheles mosquitoes to the simian malaria parasitePlasmodium cynomolgi.J. Am. Mosq. Control Assoc. 7: 481–487.

    PubMed  CAS  Google Scholar 

  • Küchler, A. W. (1978). Natural vegetation. In Espenshade, E. B., Jr., and Morrison, J. L. (eds.),Goode’s World Atlas, 15th ed., Rand McNally, Chicago, pp. 16–17.

    Google Scholar 

  • Kurup, G. U. (1974). Mammals of Assam and the mammal-geography of India. In Mani, M. S. (ed.),Ecology and Biogeography in India, Dr. W. Junk, The Hague, pp. 585–613.

    Google Scholar 

  • Lambrecht, F. L., Dunn, F. L., and Eyles, D. E. (1961). Isolation ofPlasmodium knowlesi from Philippine macaques.Nature 191: 1117–1118.

    Article  PubMed  CAS  Google Scholar 

  • Le Bras, J., Larouze, B., Geniteau, M., Andrieu, B., Dazza, M.-C., and Rodhain, F. (1984). Malaria, arbovirus and hepatic infections inMacaca fascicularis from Malaysia.Lab. Anim. 18: 61–64.

    Article  PubMed  CAS  Google Scholar 

  • Markell, E. K., Voge, M., and John, D. T. (1992).Medical Parasitology, 7th ed., W. B. Saunders, Philadelphia.

    Google Scholar 

  • Mason, S. J., Miller, L. H., Shiroishi, T., Dvorak, J. A., and McGinnis, M. H. (1977). The Duffy blood group determinants: their role in the susceptibility of human and animal erythrocytes toPlasmodium knowlesi malaria.Br. J. Haematol. 36: 327–335.

    PubMed  CAS  Google Scholar 

  • Mathis, C., and Leger, M. (1911).Plasmodium des macaques du Tonkin.Ann. Inst. Past. 25: 593–600.

    Google Scholar 

  • Matsubayashi, K., and Sajuthi, D. (1981). Microbiological and clinical examinations of cynomolgus monkeys in Indonesia.Kyoto Univ. Overseas Rep. Stud. Indones. Mac. 1: 47–56.

    Google Scholar 

  • Mayer, M. (1907). Ueber Malaria beim Affen.Med. Klin. Berl. 3: 579–580.

    Google Scholar 

  • Mayer, M. (1908). Über Malariaparasiten bei Affen.Arch. Protistenk. 12: 314–321.

    Google Scholar 

  • Miller, L. H., Mason, S. J., Dvorak, J. A., McGinnis, M. H., and Rothman, I. K. (1975). Erythrocyte receptors for(Plasmodium knowlesi) malaria: Duffy blood group determinants.Science 189: 561–563.

    Article  PubMed  CAS  Google Scholar 

  • Mulligan, H. W. (1935). Description of two species of monkeyPlasmodium isolated fromSilenus bus.Arch. Protistenk. 84: 285–314.

    Google Scholar 

  • Mulligan, H. W., and Swaminath, C. S. (1940). Natural infection withPlasmodium inui inSilenus sinicus from South India.J. Malaria Inst. India 3: 603–604.

    Google Scholar 

  • Nelson, P., Jayasuriya, J. M. R., and Bandarawatte, B. V. P. C. (1971). The establishment ofAnopheles elegans as the natural vector of simian malaria in Ceylon.Ceyl. J. Med. Sci. 20: 46–51.

    Google Scholar 

  • Notananda, V., Nilubol, S., and Swasdiwongphorn, P. (1961). A preliminary note on the discovery of simian malaria in Chiengmai.Minuten Nadeln 1: 27.

    Google Scholar 

  • Osgood, W. H. (1932). Mammals of the Kelley-Roosevelts and Delacour Asiatic expeditions.Field Mus. Nat. Hist. Publ. 312 Zool. Ser. 18: 193–339.

    Google Scholar 

  • Otsuru, M., and Sekikawa, H. (1979). Surveys of simian malaria in Japan.Zbl. Bakt. Hyg. I. Abt. Orig. A 244: 345–350.

    Google Scholar 

  • Pattanayak, S. (1963). A note on natural simian malaria infection in Kerala State, India.Indian J. Malariol. 17: 293–294.

    PubMed  CAS  Google Scholar 

  • Peyton, E. L. (1990). A new classification for the Leucosphyrus Group ofAnopheles (Cellia).Mosq. Syst. 21: 197–205. [For date of publication, seeJ. Am. Mosq. Control Assoc. 6: 481 (1990).]

    Google Scholar 

  • Peyton, E. L., and Harrison, B. A. (1979).Anopheles (Cellia) dirus, a new species of the Leucosphyrus Group from Thailand (Diptera: Culicidae).Mosq. Syst. 11: 40–49.

    Google Scholar 

  • Peyton, E. L., and Harrison, B. A. (1980).Anopheles (Cellia) takasagoensis Morishita 1946, an additional species in the Balabacensis Complex of Southeast Asia (Diptera: Culicidae).Mosq. Syst. 12: 335–347.

    Google Scholar 

  • Peyton, E. L., and Ramalingam, S. (1988).Anopheles (Cellia) nemophilous, a new species of the Leucosphyrus Group from peninsular Malaysia and Thailand (Diptera: Culicidae).Mosq. Syst. 20: 272–299.

    Google Scholar 

  • Pocock, R. I. (1932). The rhesus macaques(Macaca mulatto).J. Bombay Nat. Hist Soc. 35: 530–551.

    Google Scholar 

  • Pocock, R. I. (1939).The Fauna of British India, including Ceylon and Burma. Mammalia. Vol. 1. Primates and Carnivora (in Part). Taylor and Francis, London.

    Google Scholar 

  • Rain, A. N., Mak, J., and Zamri, R. (1993). Simian malaria infection in wild caughtMacaca fascicularis andPresbytis spp. in Malaysia.Southeast Asian J. Trop. Med Publ. Health 24: 386–387.

    CAS  Google Scholar 

  • Ramakrishnan, S. P., and Mohan, B. N. (1962). An enzootic focus of simian malaria inMacaca radiata radiata Geoffroy of Nilgiris, Madras State, India.Indian J. Malariol. 16: 87–94.

    PubMed  CAS  Google Scholar 

  • Read, A. F., and Harvey, P. H. (1993). The evolution of virulence.Nature 362: 500–501.

    Article  PubMed  CAS  Google Scholar 

  • Reid, J. A. (1968). Anopheline mosquitoes of Malaya and Borneo.Stud. Inst. Med. Res. Malaysia 31: 1–520.

    Google Scholar 

  • Rosenberg, R., and Maheswary, N. P. (1982). Forest malaria in Bangladesh. I. Parasitology.Am. J. Trop. Med. Hyg. 31: 175–182.

    PubMed  CAS  Google Scholar 

  • Satya Prakash and Chakrabarti, S. C. (1962). The isolation and description ofPlasmodium cynomolgi (Mayer, 1907) andPlasmodium inui (Halberstadter and Prowazek, 1907) from naturally occurring mixed infections inMacaca radiata radiata monkeys of the Nilgiris, Madras State, India.Indian J. Malariol. 16: 303–311.

    Google Scholar 

  • Sawadipanich, Y., Baimai, V., and Harrison, B. A. (1990).Anopheles drus species E: Chromosomal and crossing evidence for another member of the Dirus Complex.J. Am. Mosq. Control Assoc. 6: 477–481.

    PubMed  CAS  Google Scholar 

  • Schmidt, L. H. (1972). Problems and opportunities of breeding primates. In Beveridge, W. I. B. (ed.),Breeding Primates, S. Karger, Basel, pp. 1–22.

    Google Scholar 

  • Schmidt, L. H., Greenland, R., Rossan, R., and Genther, C. (1961). Natural occurrence of malaria in rhesus monkeys.Science 133:753.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, L. H., Cramer, D. V., Rossan, R. N., and Harrison, J. (1977a). The characteristics ofPlasmodium cynomolgi infections in various Old World primates.Am. J. Trop. Med. Hyg. 26: 356–372.

    PubMed  CAS  Google Scholar 

  • Schmidt, L. H., Fradkin, R., Harrison, J., and Rossan, R. N. (1977b). Differences in the virulence ofPlasmodium knowlesi forMacaca irus (fascicularis) of Philippine and Malayan origins.Am. J. Trop. Med. Hyg. 26: 612–622.

    PubMed  CAS  Google Scholar 

  • Schmidt, L. H., Fradkin, R., Harrison, J., Rossan, R. N., and Squires, W. (1980). The course of untreatedPlasmodium inui infections in the rhesus monkeyMacaca mulatta.Am. J. Trop. Med. Hyg. 29: 158–169.

    PubMed  CAS  Google Scholar 

  • Shortt, H. E., Rao, G., Qadri, S. S., and Abraham, R. (1961).Plasmodium osmaniae, a malaria parasite of an Indian monkeyMacaca radiata.J. Trop. Med. Hyg. 64: 140–143.

    Google Scholar 

  • Sinha, S., and Dasgupta, R. (1989). A note on the malaria parasite of crab-eating monkey of Nicobar Islands.J. Bengal Nat. Hist. Soc. (N.S.) 8: 63–66.

    Google Scholar 

  • Sinha, S., and Gajanana, A. (1984). First report of a natural infection with quartan malaria parasitePlasmodium shortti inMacaca fascicularis umbrosa (=irus) of Nicobar Islands.Trans. R. Soc. Trop. Med. Hyg. 78: 567.

    Article  PubMed  CAS  Google Scholar 

  • Sinton, J. A. (1934). A quartan malaria parasite of the lower Oriental monkey,Silenus irus (Macacus cynomolgus).Rec. Malaria Surv. India 4: 379–410.

    Google Scholar 

  • Sinton, J. A., and Mulligan, H. W. (1933). Mixed infections in the malaria of the lower monkeys. II. The probable occurrence of mixed infections in some of the older records of monkey malaria.Rec. Malaria Surv. India 3: 769–808.

    Google Scholar 

  • Suzuki, J., and Varavudhi, P. (1989). Somatometric data of crab eating macaques in Thailand.Kyoto Univ. Overseas Res. Rep. Stud. Asian Non-Hum. Prim. 7: 110–116.

    Google Scholar 

  • Toft, C. A. and Aeschlimann, A. (1991). Introduction: Coexistence or conflict? In Toft, C. A., Aeschlimann, A., and Bolis, L. (eds.),Parasite-Host Associations: Coexistence or Conflict? Oxford University Press, Oxford, pp. 1–12.

    Google Scholar 

  • Tsukamoto, M., Miyata, A., and Miyagi, I. (1978). Surveys on simian malaria parasites and their vector in Palawan Island, the Philippines.Trop. Med. 20: 39–50.

    Google Scholar 

  • Warren, M. (1966). Observations on the fauna of Pulau Tioman and Pulau Tulai. 12. Primate malaria.Bull. Nat. Mus. Singapore 34: 150–158.

    Google Scholar 

  • Warren, M., and Wharton, R. H. (1963). The vectors of simian malaria: Identity, biology, and geographical distribution.J. Parasitol. 49: 892–904.

    Article  PubMed  CAS  Google Scholar 

  • Warren, M., Ali, K., Bennett, G., and Sandosham, A. A. (1964). Morphology ofPlasmodium fieldi in different species of the genusMacaca.Med. J. Malaya 19: 31.

    PubMed  CAS  Google Scholar 

  • Warren, M., Cheong, W. H., Fredericks, H. K., and Coatney, G. R. (1970). Cycles of jungle malaria in West Malaysia.Am. J. Trop. Med. Hyg. 19: 383–393.

    PubMed  CAS  Google Scholar 

  • Waters, A. P., Higgins, D. G., and McCutchan, T. F. (1993). Evolutionary relatedness of some primate models ofPlasmodium.Mol. Biol. Evol. 10: 914–923.

    PubMed  CAS  Google Scholar 

  • Wharton, R. H., Eyles, D. E., Warren, M., and Moorhouse, D. E. (1962).Anopheles leucosphyrus identified as a vector of monkey malaria in Malaya.Science 137: 758.

    Article  PubMed  CAS  Google Scholar 

  • Wharton, R. H., Eyles, D. E., Warren, M., and Cheong, W. H. (1964). Studies to determine the vectors of monkey malaria in Malaya.Ann. Trop. Med. Parasitol. 58: 56–77.

    PubMed  CAS  Google Scholar 

  • Wheatley, B. P. (1980). Malaria as a possible selective factor in the speciation of macaques.J. Mammal. 61: 307–311.

    Article  PubMed  CAS  Google Scholar 

  • Yap, L. F., Lim, B. L., de Witt, G. F., Krishnasamy, M., Sivanadam, S., and Foong, P. Y. K. (1977). Protozoan and helminth parasites of small wild mammals in a new Felda settlement Jenderak Utara, central Pahang, peninsular Malaysia.SE Asian J. Trop. Med. Pub. Hlth. 8: 345–353. (For surname of first author, see p. 353 of cited article.)

    Google Scholar 

  • Zhang Jiaxun, Huang Zaisong, Zheng Shancheng, Yang Bailin, and Ye Xiuyu (1980). On identification of a species of malaria parasite from monkeys.Acta Zool. Sinica 26: 140–145 (in Chinese with English summary).

    Google Scholar 

  • Zimmermann, E. A. W. (1780).Geographische Geschichte des Menschen und der vierfüssigen Thiere, Weygandische Buchhandlung, Leipzig.

    Google Scholar 

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Fooden, J. Malaria in macaques. Int J Primatol 15, 573–596 (1994). https://doi.org/10.1007/BF02735972

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