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Simian Malaria at Two Sites in the Brazilian Amazon. I-The Infection Rates of Plasrnodium brasilianum in Non-human Primates Ricardo Lourenco-de-Oliveira, Leonidas M Deane+ Laboratorio de Transmissores de Hematozoanos, Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, R J, Brasil
Code Number: OC95066
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The parasite that causes sintian nullaria in the Brazilian Antazon, Plasmodium brasilianum, is infective to man. In this region, where humans live within and in close proximity to the forest, it was suspected that this parasite could be the cause of a zoonosis. A study was performed in the areas surrounding two hydroelectric plants in the Amazon, Balbina and Santuel, aiming at determining the zoonotic potential of this parasite. P. brasilianum was detected in, respectively, 15.8% and 9.9% of 126 and 252 primates belonging to seven and eight species examined from Balbina and Santuel. The highest nullaria infection rates were found among the red-howler monkey Alouatta seniculus straminea (32.3 %), the bearded-saki Chiropotes satanas chiropotes (50%) and the spider-monkey Ateles paniscus pamscus (2[1+])front Balbina and in the squirrel-monkey Saimiri ustus (21%) and the blackfaced-spider-monkey Ateles paniscus chamek (28. 6%)front Santuel. Key words: simian malaria - Plasmodium brasilianum - Plasmodium simium - Primates - Cebiadae -Callitluicidae Simian malaria parasites have been described since the first decade of this century, when the practice of importing exotic animals, including primates, to be exhibited in circus and zoos in Europe was in vogue. The first New World's simian plasmodium, Plasmodiunt brasilianum Gonder and Berenberg-Gossler, 1908, was described from the blood of a bald-uakari (Cacajao calvus) acquired in the Brazilian Amazon. The other neotropical non-human malaria parasite, P. simium Fonseca, 1951, was identified from southem Brazil, in a howler-monkey (Alouatta fusca). These two simian parasites are very different, but both are infective to man. P. brasilianum is a quartan malaria parasite, practically indistinguishable from the human P. malariae (Garnham et al. 1963, Collins et al. 1969b, Cochrane et al. 1985, Lal et al. 1988), of which it may be synonimous (Coatney et al. 1972). P. simium is a tertian plasmodium, similar to P. vivax and P. ovale (Garnham 1966, Collins et al. 1969a). Goldman et al. (1993) argued that P. simium might be a strain of P. vivax. P. brasilianum is widely distributed among the simians (46 species) from Panama, Colombia, Peru, Venezuela and Brazil, while P. simium is restricted to two monkey species from southern and southeastern Brazil. There has been early evidence that some simian malaria parasites could experimentally infect man. In 1960, humans were accidentally infected at a laboratory, by anopheline bite, with a strain of P. cynomolgi, an Asian malaria of M. irus (Eyles et al. 1960). Nevertheless, two episodes occured in nature, with two distinct simian para- sites: one person infected in Malaysia, by P. knowlesi, a parasite of M. irus and M. nentestrina (Chin et al. 1965) and another in southeastem Brazil, by P. sinium (Deane et al. 1966a). On other occasions, human infections by simian malaria were suspected (Coatney 1971, Sulzer et al. 1975, Kalra 1980). No other human malaria cases of proved simian origin has been reported in Malaysia and southeastern Brazil. There was no evidence that monkey malaria demonstrated epidemiological importance to the indigenous population in those places since the simian and human malarias cycles are aparently independent (Warren & Wharton 1963, Deane et al. 1966b, Deane 1969, 1976, Warren et al. 1970, Coatney et al. 1972). The place where that Brazilian episode of human infection of simian malaria was contracted, Cantareira forest, is highly enzootic (about 60% of howler-monkeys are infected with Plasmodium). The patient was a forest guard who used to conduct most of the anopheline captures at the malaria in this area, where the guard was born and lived all of his life. This was an isolated event, like the Asian one, which occurred under special conditions, when a human introduced himself into the habitat of both mosquito and simian hosts of the malaria parasites. Why did the individual living in a holoenzootic area acquire monkey malaria in that particular episode? The simian malaria vector in Cantareira forest well as in other areas in south- eastem Brasil is Anopheles cruzi, an acrodendrophilic anopheline (99% collected at the tree canopy) (Deane 1967, Deane et al. 1970). This marked preference of An. cruzi for the upper forest canopy is certainly the barrier that restricts the malaria infection to monkeys in that area, even though simian malaria parasites are infectire to man. The forest guard was infected only when he entered the holoenzootic upper forest canopy. It seems that the acrodendrophilic behaviour of An. cruzi does not allow for transmission of simian malaria to humans. If that behavioral barrier were surmountable, i.e., in case the vector attacked frequently in both environments - near the ground and at the tree canopy, could the simian malaria be transmitted to humans in Brazil? P. brasilianum is widely disseminated in the Amazon Basin, where An. cruzi is absent and the vector remains unknown (Deane et al. 1968a, 1971, Almeida & Deane 1970, Ferreira Neto et al. 1970, Deane & Ferreira Neto 1973, Deane 1976). In the Amazon, where indians, miners, wood-choppers, rubber-gatherers and fishermen live in close proximity to or within the forest, it was suspected that P. brasilianum could be the cause of a zoonosis. This is dependent upon the simian malaria vector behavior, whether it activly feeds on monkeys, at the tree canopy, and also people on the ground. These assumptions were emphasized when Arruda et al. (1989) verified that a high proportion of indians, miners and immigrants in the Amazon had antibodies against sporozoites and blood stages of P. brasiliaum/malariae, although corresponding parasites were not detected in their blood films. Besides, Anuda et al. (1989) observed that all pets and wild monkeys examined in some of those tribes had antibodies against blood stages of P. brasilianum/malariae. Examining 755 An. darlingi Root, 1926 collected in some of the tribes, the same authors found three specimens positive for P. brasilianum/malariae circumsporozoite antigens. Based in this information it was speculated that An- darlingi is the vector of both the human and the simian quartan malarias in those settlements. Nevertheless, it is necessary to determine the zoonotic potential of P. brasilianum in the Amazon, i.e mainly its sylvan cycle, (2) identify the vector, (3) determin vector blood feeding behaviour of biting regularly infected monkeys and humans inside the jungle or in the surrounding areas, (4) know the epidemiological importance of human transmission of this parasite and its threat to the anti-malaria campaigns and public health. A study was performed in areas around two hydroelectric plants in the Brazilian Amazon aiming at to detennine the potential for transmission of simian malaria caused by P. brasilianum to humans, based primarily on parasitological surveys among monkeys and on the distribution and behavior of the anopheline vectors. The study comprised three phases: (1) determine malaria prevalence among the non-human primates in each area, (2) conduct mosquito captures and observations on the ecology and behavior of the potential vectors and (3) examine the caught anophelines for detection of natural infection of the quartan malaria parasites. The present paper consists of the description of the studied areas and the search for simian malaria parasite infections. The anopheline survey will appear elsewhere. METHODOLOGY
Studied areas - The study was carried out near two hydroelectric plants constructed on two rivers, on each side of the Amazon Basin: Balbins, on the Uatuma River, a tributary of the left margin of the Amazonas River, State of Amazonas (1^o 55'S 59028'W) and Samuel, on the Jaman River, an affluent of the Madeira river, which flows into the right margin of the Amazonas River, State of Rondonia (8^o 10'S 62^o 29'W), Brazil (Fig. 1). After the construction of the hydroelectric plants, a proportion of the jungle around each reservoir was selected as a forest reservation, where nearly all observations reported here and in the following papers on both the simian malaria and the anophelines, were performed. The Balbina dam was built at a site where formerly there was a waterfall (Cachoeira Balbina), surrounded by dense forest. Only one person lived permanently at Cachoeira Balbina, while six rubber-tree tapers and nut collectors used to settle temporarily at the margins of Uatuma River nearby. During the construction these settlers were moved down-river (Chagas et al. 1982), while thousands of workers were settled a few kilometers from the dam site, starting the city of Balbina (9,300 inhabitants, 1985). Balbina is at a low elevation: the dam and the city are located at 34m and 170m above sea level, respectively. The local relief is slightly undulated and the land is extremely poor, not favorable for agriculture. The Uatuma river and its tributaries are black water rivers, i.e. acidic and nutrient poor. The climate is tropical, warm and humid (annual rainfall near 2,262mm: mean temperatureranges from 22 C to 36 C; mean monthly RH around 82%) (Eletronote 1989, 1992).
The territory of one indian tribe, WaimiriAtroari, is located within the area of influence of the Balbina reservoir. Three settlements of these indians were visited in this survey: Cacau, Mare and Curiuau, and the descriptions and data on malaria will appear elsewhere. The Samuel hydroelectric plant was built on the rapids on the Jamari river, at the village of Cachoeira Samuel, whose inhabitants were subsequently moved 50km west. As opposed to Balbina, neither borough nor city was settled near the dam. The Jamari valley elevations ranges between 80-200m above sea level. The land being very propitious for agriculture. The water of the Jamari river and its affluents is nutrient rich, carries a high sediment and has a neutral pH. In Samuel, the climate is equatorial, warm and humid, like Balbina. The annual rainfall ranges from 2,000mm to 2,900mm; the temperature usually varies from 20 C to 32 C and RH ranges from 74% to 90% (Lisboa 1990, Eletronorte 1990). Almost 70% of the area around Balbina and Samuel are covered by a dense and tall humid forest, called "terra firme" forest. It is constituted mostly of medium-sized and tall leafy trees, with canopies at 5-15m and 25-30m, respectively.
Capture and examination of non-human primates - After the constructuion of both dams, primates were captured in the forests of the dam reservoir flooded plains and transferred to dry portions of the bordering jungle, i.e., to the forest reservations. Blood samples were obtained from some of these primates before their resettlement (from May 16 to 20 and September 6 to 30, 1988, in Balbina, and from February 17 to March, 28, 1989, in Samuel). In 1989, some of the squirrel- monkeys captured in both areas were transported to the Oswaldo Cruz Foundation, in Rio de Janeiro, for breeding purposes, where they were subsequently examined. Blood was obtained from a slight incision performed at the primates' ear and the exam carried out through Giemsa stained thick and thin blood smears. At least one whole thick blood film was examined before considering the animal negative. Parasitemia was not measured. The nomenclature and systematics of the primates used here are those adopted by Coimbra Filho (1990), Hershkovitz (1983, 1984, 1985, 1987, 1988), Vivo (1985) and Konstant et al. (1985). RESULTS Primates from Balbina - A total of 1,919 nonhuman primates belonging to eight species were captured in Balbina. The most common species was the red-howler-monkey A.s. straminea (69.7%), followed by far by the bearded saki C.s. chiropotes (9.3%), the capuchin Cebus apella apella (7.6%), the white-faced-saki Pithecia pithecia pithecia (6%), and the squirrel-monkey Saimiri sciureus'sciureus (4%) (Fig. 2a). The search for Plasmodium included 126 primates belonging to seven out of the eight species detected in Balbina (Table I; Fig. 2b). The squirrel-monkey S.s. sciureus and the redhowlermonkey A.s. straminea were the most frequently examined, respectively, 48% and 24.6% of the total. P. brasilianum was the only malaria parasite found infecting 20 monkeys (15.8%) distributed among five species (Table I). All infections were among Cebidae monkeys and high infection rates were obtained in A.s. straminea (32.3%), A. p. paniscus and C.s. chiropotes (50%). Only and 12.5% of the squirrel-monkeys and sakis were positive, respectively. Primates from Samuel - In Samuel, 1,806 non-human primates were captured. The most common species were the squirrel-monkey S. ustus (27.7%), the saki P. irrorata irrorata (20.4%), the titi Callicebus brunneus (19.3%) and the capuchin C.a. apella (11.5%). Four other species were caught less frequently at Samuel (Fig. 3a).
Fig. 3: percentage of primate species captured (a) in Samuel, and Co) examined for simian malaria parasites. Percentage of primates species examined positive for Plasmodium brasilianum in parenthesis.
Simian malaria in non-human primates captured in Balbina, State of Amazonas, in May and September, 1988. Number of primates examined and positive for Plasmodium brasilianum,
-----------------------------------------------------
Primate species
-----------------------------------------------------
Cebidae
Alouatta seniculus straminea (Humboldt, 1812)
Ateles paniscus paniscus (Linnaeus, 1758)
Cebus apella apella (Linnaeus, 1758)
Chiropotes satanas chiropotes (Humboldt, 1811 )
Pithecia pithecia pithecia (Linnaeus, 1766)
Saimiri sciureus sciureus (Linnaeus, 1758)
Callifluicidae
Saguinus midas midas (Linnaeus, 1758)
--------------------------------------------------------------
Number primates Percent
Common name examined (positive) positive
--------------------------------------------------------------
Red-howler-monkey 31 (10) 32.3
Spider-monkey 2 (1) 50
Capuehin 8 -
Bearded-saki 6 (3) 50
White-faced-saki 8 (1) 12.5
Squirrel-monkey 61 (5) 8.2
Tamarin 10 -
-------------------------------------------------------------
Total 126 (20) 15.8
-------------------------------------------------------------
The number of primates examined at Samuel was twice that of Balbina, i.e., 232 animals belonging to all eight species found in the local forest. S. ustus, C. brunneus and P.i. irrorata were the most frequently examined (Fig. 3b). A total of 25 animals (9.9%) belonging to five species was found to be infected with P. brasilianum at Samuel (Table II). The parasite was most frequently detected in two species: A. P. chamek (26.6%) and S. ustus (21%) (Fig. 3b). Only 6% of the local titis, 5.3% of the sakis and 3% of the capuchins were infected. All examined tamam and marmosets - Saguinus fuscicollis weddelli and Callithrix emiliae - and night'monkeys, provisionally called Aotus nigriceps (Pieckzarka et al. 1993) were negative. DISCUSSION According to Deane (1992) simian malaria in Brazil is present or more frequent in primary tall, humid forests, populated of susceptible Cebidae monkeys, especially those belonging to genera Alouatta and Ateles, while it is infrequently observed in drier, bushy regions, with secondary or low and little dense vegetation, propitious mostly to Callitrichidae and less susceptible Cebidae species. An example of the first situation is da Cantareira, Sao Paulo, where more than 60% of the local primates are infected, thus making it a holoenzootic area. On the contrary, simian malaria was not found in numerous primates examined in the northeast States and southeast State of Minas Gerais, which are in the second situation. In intermediate situations, which may represent the majority, the infection rate is moderate or low, depending mostly on the constitution of the primate fauna and the existence of an efficient vector. If the primate fauna of such an area includes the susceptible species of genera Alouatta or Ateles besides the less susceptible ones, simian malaria should be more common there, and vice versa. Besides susceptibility, the considerable body weight and the group size in spider and howler-monkeys seem to favor their contact with the vectors (Davies et al. 1991). More than 30% of the primates have malaria in Guaa, Joinvile, Santa Leopoldina, Altos das Ouaribas and Cabeceira Grande, where species of Alouatta are abundant. As the proportion of howler and spider-monkeys decreases, the prevalence of simian malaria diminishes, as in Barreifinha, Porto Maua, near the Manaus- Itacoatiara road, Sao Jose, Sooretama (Deane et al. 1969, Deane 1976), Balbina and Samuel. The percentage of infected monkeys in Balbina (15.8%) is slightly above the average previously observed for Brazilian Amazon primates (9.7%, Deane 1976; 10.1%, Deane 1992). But it practically coincides with the rates found by the same author in State of Amazonas, i.e. 15-16%. The red-howler-monkey A.s. stratainca has been frequently found infected with P. brasilianum in the Brazilian Amazon (Deane & Almeida 1967, DeaWe et al. 1969, Deane & Ferreira-Neto 1969). But only one specimen was de- tected with P. brasilianum outside Brazil: Serrano (1967) examined four howlers from Venezuela, detecting the parasite in the blood of one animal. Our data demonstrate a higher percentage of simian malaria than observed by Deane (1992) in this Alouatta species and in the two Ateles species from both Balbina and Samuel. The spider-monkeys were among the most commonly malaria- infected primates in the two studied areas. Other authors have also detected high infection rates in A.p. paniscus and A.p. TABLE II Simian malaria in non-human primates captured in Samuel, State of Rondonia, in February and March, 1989. Number of primates examined and positive for Plastnodium brasilianum
------------------------------------------------------------
Primate species
------------------------------------------------------------
Cebidae
Aotus nigriceps (Dollman, 1909)
Ateles paniscus chamek (Humboldt, 1812)
Callicebus brunneus (Wagner, 1842)
Cebus apella apella (Linnaeus, 1758)
Pithecia irrorata irrorata (Gray, 1842)
Saimiri ustus (Geoffroy, 1843)
Callithficidae
Callithnx etniliae (Thomas, 1820)
Saguinusfuscicollis weddelli (Deville, 1849)
------------------------------------------------------------
Number primates Percent
Common name examined (positive) positive
------------------------------------------------------------
Night-monkey 22 -
Black-faced-spider- 7 (2) 28.6
monkey
Titi 50 (3) 6
Capuchin 31 (1) 3.2
Saki 38 (2) 5.3
Squirrel-monkey 81 (17) 21
Marmoset 4 -
Tamann 19 -
-------------------------------------------------------------
Total 252 (25) 9.9
-------------------------------------------------------------
TABLE IIINeotropical primates naturally infected with Plasmodium brasilianum and Plasmodium simium, by country (BR: Brazil, CO: Colombia, PA: Panama, PE: Peru, VE: Venezuela) ------------------------------------------------------------- Plasmodia/Primates BR CO PA PE VE ------------------------------------------------------------- Plasmodium brasilianum Cebidae Alouatta belzebuth belzebuth + Alouatta belzebuth nigerrima + Alouatta caraya + Alouatta fusca clamitans + Alouattafuscafusca + Alouatta seniculus seniculus + Alouatta seniculusstraminea + + Alouatta villosapalliata + Alouatta villosa villosa + Aotus vociferans + Ateles belzebuth belzebuth (?)^b + Ateles fuscipes robustus + + Ateles geoffroyi grisescens + Ateles geoffroyi panamettsis + Ateles geoffroyi spp.c + Atelespaniscus chatnek + Ateles paniscus paniscus + Brachiteles arachinoides + Cacajao calvus + Cacajao rubicundus rubicundus + Callicebus brunneus + Callicebus moloch + Callicebus cupreus ornatus + Callicebus torquatus torquatus + Cebus albifrons + Cebus apella apella + + Cebus apella macrocephalus + Cebus capucinus capucinus + + Cebus capucinus imitator + Chiropoles albinasus + Chiropotes satanas chiropotes + Chiropotes satanas satanas + Lagothrix lagothrichia cana + Lagothrix lagothrichia lagothrichia + + + Lagothrix lagothrichia poeppigii + Pithecia irrorata irrorata + Pithecia monachus spp.(?)^e + Pithecia pithecia pithecia + Saimiri sciureus albigena + Saimiri sciureus macrodon (?)^f + Saimiri sciureus sciureus + Saimiri sciureus spp.(?)^g + Saimiri boliviensis peruviensis + + Saimiri ustus + Callithricidae Saguinus geoffroyi + Saguinus midas niger + Plasmodium simium Alouattafusca clamitans + Brachiteles arachinoides + -------------------------------------------------------------a: apud Dunn and Lambrecht (1963); b: Atelespaniscus and Ateles variegatus of Dunn and Lambrecht(1963); c: Ateles geoffroyi d:apud Marinkelle and Grose (1968); e: Pithecia monachus of Deane (1976); f:Saimiri sciura of Dunn and Lambrecht (1963); g: Saimiri sciureus of Marinkelle and Grose (1968).
-------------------------------------------------------------
Plasmodia/Primates References
-----------------------------------------------------------
--
Plasmodium brasilianum
Cebidae
Alouatta belzebuth belzebuth Ferreira Nero et al.
(1970), Deane (976),
Arruda (1985)
Alouatta belzebuth nigerrima Deane (1976), Arruda
(1985)
Alouatta caraya Deane (1976)
Alouatta fusca clamitans Deane (1976)
Alouatta fusca fusca Deane (1976)
Alouatta seniculus seniculus Ferreira Nero and
Deane (1973), Arruda
(1985)
Alouatta seniculusstraminea Serrano (1967),
Deane (1976),
Lourenqo-de-
Oliveira (1988)
Alouatta villosapalliata Clark (1931)
Alouatta villosa villosa Galindoa, Porter et
al. (1966)
Aotus vociferans Collins et al.
(1985)
Ateles belzebuth belzebuth Dunn and Lambrecht (1963)
Atelesfuscipes rob,stus Clark(1931), Porter
et al. (1966), Marinkelle
and Grose (1968)
Ateles geoffroyi grisescens Galincloa
Ateles geoffroyi panamettsis Clark (1931), Porter
et al. (1966)
Ateles geoffroyi spp.c Galindoa
Ateles paniscus chatnek Deane (1976), Deane
et al. (1989)
Ateles paniscus paiscus Deane (1976),
Lourenqo-de- Oliveira (in
this paper)
Brachiteles arachinoides Deane et al. (1968c)
Cacajao calvus Gonder and
Berenberg-
Gossler(1908), Alineida and
Deane(1970)
Cacajao rubicundus rubicundus Ferreira Neto and
Deane (1973)
Callicebus brunneus Deane et al. (1989)
Callicebus moloch Deane (1976), Arruda
(1985) Callicebus cupreus ornatus Renjifo and
Peidrah ta (1949)
Callicebus torquatus torquatus Deane (1976)
Cebus albifrons Dunn and Lambreel,
(1963), Marinkelle and
Grose (1968), Ayala
(1978)
Cebus apella apella Dunn and
Lambrecht(1963),
Marinkelle and Grose
(1968), Deane (1976), Deane
et al. (1989)
Cebus apella macrocephalus Deane (1976)
Cebus capucinus capucinus Clark (1931), Porter
et al.(1966),
Marinkelle and Grose
(1968)
Cebus capucinus imitator Clark (1931),
Galindoa
Chiropotes albitasus Deane (1976)
Chiropotes satanas chiropotes Deane (1976),
Lourenqo-de- Oliveira (in
this paper)
Chiropotes satanas satanas Deane (1976), Arruda
(1985)
Lagothrix lagothrichia cana Deane (1967)
Lagothrix lagothrichia lagothirichia Dunn and Lambrecht
(1963), Garnham et
al. (1963), Deane
(1976) Marinkelle
and Grose (1968)
Lagothrix lagothrichia poeppigii Ferreira Nero and
Deane (1973)
Pithecia irrorata irrorata Lourenqo-de-Oliveira
(in this paper)
Pithecia monachus spp.(?)^e Deane (1976)
Pithecia pithecia pithecia Lourenco-de-Oliveira
(1988)
Saimiri sciureus albigena Renjifo et al.
(1952), Garnham et
al. (1963)
Saimiri sciurells macrodon (?)^f Dunn and Lambrecht
(1963)
Saimiri sciureus sciureus Deane (1976), Arruda
(1985), Lourenqo-de-
liveira (1988)
Saimiri sciureus spp.(?)^g Marinkelle and Grose
(1968)
Saimiri boliviensis peruviensis Ferreira Nero and
Deane (1973), Deane
(1976),
Collins et al. (1990)
Saimiri ustus Deane el al. (1989)
Callithricidae
Saguinus geoffroyi Baerg (1971)
Saguinus midas niger Arruda (1985)
Plasmodium simium
Alouatta fusca clamitans Fortseca (1951),
Garnharn (1966), Deane
(1976) Brachiteles arachinoides Deane et al.
(1968c)
-------------------------------------------------------------
a: apud Dunn and Lambrecht (1963); b: Atelespaniscus
and Ateles variegatus of Dunn and Lambrecht(1963);
c: Ateles geoffroyi d:apud Marinkelle and Grose (1968);
e: Pithecia monachus of Deane (1976); f:Saimiri sciura of Dunn
and Lambrecht (1963); g: Saimiri sciureus of Marinkelle and
Grose (1968).
chameck in Brazil, generally ranging from 25-30% (Deane 1967, 1976, 1992, Deane et al. 1969, Deane & Ferreira-Neto 1969). In Samuel, A.p. chameck was mainly observed in dense and nonflooded portions of the forest, on flat or slightly undulated terrain, i.e. "tetra firme". On the other hand, the titis, C. brunneus, were most frequently seen in secondary forests, with natural felling of trees and tangled growth of lianas in Samuel. Only 6% of them had malaria (Table II), a percentage close to that found by Deane (1992) for titis in Brazil. Actually most of the titis examined in Latin America have been consistently negative or poorly positive (Marinkelle & Grose 1968, Deane et al. 1969, Arruda 1985). Almost nothing is known on the susceptibility of this primate species to the Old World simian and human plasmodia. Meanwhile, some Aotus species are very susceptible to the New World simian malarias and to the human ones (WHO 1987, Collins 1992). But they have always been negative in monkey malaria surveys, except for one exemplar of A. vociferans (Spix, 1823), from Peru, from which Collins et al. (1985) isolated the Peruvian I/CDC strain of P. brasilianum. All marmosets and tamarins examined in the present study were negative for the malaria parasite (Tables I, II), similar to the finding of other authors. Malaria infection has been detected in only five out of more than 2,000 specimens ex- amined in the Americas: one Saguinus geoffroyi, from Panama and four Saguinus midas niger, Brazil, all infected with P. brasilianum (Porter et al. 1966, Baerg 1971, Arruda 1985). These findings seem to be exceptions, since 15 species of Callithrichidae have been examined in Brazil always with negative results (Deane 1976, 1992, Lourenqo-de-Oliveira 1990). However, it is known that some tamarins and marmosets are experimentally susceptible to P. simium and to some of the human malarias (Deane 1967). The shelters used ovemight for these animals, their low body weight and their small group size apparently do not favor their contact with the vectors (Davies et al. 1991). High infection rate (50%) was observed in the bearded sakis C.s. chiropotes from Balbina (Table i). The geographical distribution of the genus Chiropotes includes the three Guianas and the Brazilian and Venezuelan Amazon Regions. However, this genus has only been examined in Brazil for malaria infection. Three out of the four bearded saki species or subspecies (Herskovitz 1985) have previously been found infected with P. brasilianum in Brazil: C. albinasus (33.3%, Deane 1976) and C.s. satanas (11.8%, Arruda 1985) and C.s. chiropoles (18.2%, Deane 1967 and 13.3%, Deane 1976, 1992). Adding our results to the findings of Deane (1992), the malaria infection rate in C.s. chiropotes in Brazil increases by 19.4%. According to Deane (1992), the prevalence of malaria among the sakis, genus Pithecia, is generally low (2.4%), similar to that verified in P.p. irrorata from Samuel (5.3%), but less than in P. p. pilhecia from Balbina (12.5%). The distribution of genus Pithecia includes other countries in the Northwestern and Westem Amazon, but it has not been examined for malaria outside of Brazil. Squirrel-monkeys are among the most utilized primates in malaria research, mainly because of their susceptibility to human and simian malaria parasites (Deane et al. 1966d, Collins et al. 1985, Gysin 1991). The percentage of Saimiri infected with Plasmodium in Brazil is low, i.e. 6.9% (Deane 1992), and is similar to our findings in S. s. sciureus from Balbina (Table i). Deane (1967) examined 110 S.s. sciureus from localities in the States of Amazonas and Para, with negative results, while Almeida and Deane (1970) and Arruda (1985) found 26.1% and 1.3% malaria positive rates, respectively, in the above mentioned States. However, the infection rate in the squirrelmonkeys from Samuel, S. ustus (21%), was higher than those observed by Deane (1992) in S. boliviensis peruviensis (=S. sciureus boliviensis of Deane 1976, 1992) and S.s. sciureus.
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