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.
Similar content being viewed by others
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.
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.
Anderson, R. M., and May, R. M. (1982). Coevolution of hosts and parasites.Parasitology 85: 411–426.
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.
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.
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.
Bennet, G. F., and Warren, M. (1965). Transmission of a new strain ofPlasmodium cynomolgi to man.J. Parasitol. 51: 79–80.
Bray, R. S. (1963). Malaria infections in primates and their importance to man.Ergeb. Mikrob. Immun. Exp. Ther. 36: 168–213.
Brug, S. L. (1934). Observations on monkey malaria.Riv. Malarial. 13: 121–142.
Chasen, F. N. (1940). A handlist of Malaysian mammals.Bull. Raffles Mus., 15: i-xx, 1–209.
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.
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.
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.
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.
Coatney, G. R., Collins, W. E., Warren, M., and Contacos, P. G. (1971).The Primate Malarias, U.S. Government Printing Office, Washington, D.C.
Colless, D. H. (1956). TheAnopheles leucosphyrus group.Trans. R. Entomol. Soc. Lond. 108: 37–116.
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.
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.
Corbet, G. B., and Hill, J. E. (1992).The Mammals of the Indomalayan Region: A Systematic Review, Oxford University Press, Oxford.
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.
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.
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.
Dissanaike, A. S. (1963).Plasmodium infection in Ceylon monkeys.Trans. R. Soc. Trop. Med. Hyg. 57: 488–489.
Dissanaike, A. S. (1965). Simian malaria parasites of Ceylon.Bull. WHO 32: 593–597.
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.
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.
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.
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.
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.
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.
Ewald, P. W. (1983). Host-parasite relations, vectors, and the evolution of disease severity.Annu. Rev. Ecol. Syst. 14: 465–485.
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.
Eyles, D. E., and Warren, M. (1962).Plasmodium inui in Sulawesi.J. Parasitol. 48: 739.
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.
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.
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.
Eyles, D. E., Dunn, F. L., Warren, M., and Guinn, E. (1963a).Plasmodium coatneyi from the Philippines.J. Parasitol. 49: 1038.
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.
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.
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.
Fooden, J. (1969). Taxonomy and evolution of the monkeys of Celebes.Bibl. Primatol. 20: 1–148.
Fooden, J. (1971). Report on primates collected in western Thailand January-April, 1967.Fieldiana Zool. 59: 1–62.
Fooden, J. (1975a). Taxonomy and evolution of liontail and pigtail macaques (Primates: Cercopithecidae).Fieldiana Zool. 67: 1–169.
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.)
Fooden, J. (1982). Ecogeographic segregation of macaque species.Primates 23: 574–579.
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.
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.
Garnham, P. C. C. (1966).Malaria Parasites and Other Haemosporidia, Blackwell, Oxford.
Garnham, P. C. C. (1973a). Second roundtable discussion on taxonomic problems relating to malaria parasites.J. Protozool 20:37–42.
Garnham, P. C. C. (1973b). Distribution of malaria parasites in primates, insectivores and bats.Symp. Zool. Soc. Lond. 33: 377–404.
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.
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).
Green, R. (1932). A malarial parasite of Malayan monkeys and its development in anopheline mosquitoes.Trans. R. Soc. Trop. Med. Hyg. 25: 455–477.
Halberstaedter, L., and von Prowazek, S. (1907). Untersuchungen üüber die Malariaparasiten der Affen.Arb. K. Gesundh. -Amte (Berl.) 26: 37–43.
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).]
Herre, E. A. (1993). Population structure and the evolution of virulence in nematode parasites of fig wasps.Science 259: 1442–1445.
Hodgkin, E. P. (1950). TheAnopheles umbrosus group (Diptera: Culicidae). II. Biology and transmission of malaria.Trans. R. Entomol. Soc. London. 101: 319–334.
Howard, L. M., and Cabrera, B. D. (1961). Simian malaria in the Philippines.Science 134: 555–556.
Hsieh, H.-C. (1960). Malaria parasites of the Taiwan monkey.Formosan Sci. 14: 477–487.
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).
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.
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.
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.
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.
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.
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.
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.
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.
Lambrecht, F. L., Dunn, F. L., and Eyles, D. E. (1961). Isolation ofPlasmodium knowlesi from Philippine macaques.Nature 191: 1117–1118.
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.
Markell, E. K., Voge, M., and John, D. T. (1992).Medical Parasitology, 7th ed., W. B. Saunders, Philadelphia.
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.
Mathis, C., and Leger, M. (1911).Plasmodium des macaques du Tonkin.Ann. Inst. Past. 25: 593–600.
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.
Mayer, M. (1907). Ueber Malaria beim Affen.Med. Klin. Berl. 3: 579–580.
Mayer, M. (1908). Über Malariaparasiten bei Affen.Arch. Protistenk. 12: 314–321.
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.
Mulligan, H. W. (1935). Description of two species of monkeyPlasmodium isolated fromSilenus bus.Arch. Protistenk. 84: 285–314.
Mulligan, H. W., and Swaminath, C. S. (1940). Natural infection withPlasmodium inui inSilenus sinicus from South India.J. Malaria Inst. India 3: 603–604.
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.
Notananda, V., Nilubol, S., and Swasdiwongphorn, P. (1961). A preliminary note on the discovery of simian malaria in Chiengmai.Minuten Nadeln 1: 27.
Osgood, W. H. (1932). Mammals of the Kelley-Roosevelts and Delacour Asiatic expeditions.Field Mus. Nat. Hist. Publ. 312 Zool. Ser. 18: 193–339.
Otsuru, M., and Sekikawa, H. (1979). Surveys of simian malaria in Japan.Zbl. Bakt. Hyg. I. Abt. Orig. A 244: 345–350.
Pattanayak, S. (1963). A note on natural simian malaria infection in Kerala State, India.Indian J. Malariol. 17: 293–294.
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).]
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.
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.
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.
Pocock, R. I. (1932). The rhesus macaques(Macaca mulatto).J. Bombay Nat. Hist Soc. 35: 530–551.
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.
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.
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.
Read, A. F., and Harvey, P. H. (1993). The evolution of virulence.Nature 362: 500–501.
Reid, J. A. (1968). Anopheline mosquitoes of Malaya and Borneo.Stud. Inst. Med. Res. Malaysia 31: 1–520.
Rosenberg, R., and Maheswary, N. P. (1982). Forest malaria in Bangladesh. I. Parasitology.Am. J. Trop. Med. Hyg. 31: 175–182.
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.
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.
Schmidt, L. H. (1972). Problems and opportunities of breeding primates. In Beveridge, W. I. B. (ed.),Breeding Primates, S. Karger, Basel, pp. 1–22.
Schmidt, L. H., Greenland, R., Rossan, R., and Genther, C. (1961). Natural occurrence of malaria in rhesus monkeys.Science 133:753.
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.
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.
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.
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.
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.
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.
Sinton, J. A. (1934). A quartan malaria parasite of the lower Oriental monkey,Silenus irus (Macacus cynomolgus).Rec. Malaria Surv. India 4: 379–410.
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.
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.
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.
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.
Warren, M. (1966). Observations on the fauna of Pulau Tioman and Pulau Tulai. 12. Primate malaria.Bull. Nat. Mus. Singapore 34: 150–158.
Warren, M., and Wharton, R. H. (1963). The vectors of simian malaria: Identity, biology, and geographical distribution.J. Parasitol. 49: 892–904.
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.
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.
Waters, A. P., Higgins, D. G., and McCutchan, T. F. (1993). Evolutionary relatedness of some primate models ofPlasmodium.Mol. Biol. Evol. 10: 914–923.
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.
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.
Wheatley, B. P. (1980). Malaria as a possible selective factor in the speciation of macaques.J. Mammal. 61: 307–311.
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.)
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).
Zimmermann, E. A. W. (1780).Geographische Geschichte des Menschen und der vierfüssigen Thiere, Weygandische Buchhandlung, Leipzig.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Fooden, J. Malaria in macaques. Int J Primatol 15, 573–596 (1994). https://doi.org/10.1007/BF02735972
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02735972