Seção de Parasitologia, Instituto Evandro Chagas/Funasa, Av. Almirante Barroso 492, 66090-000 Belém, PA,
Brasil *Walter Reed Army Institute of Research, Washington, DC, USA **Pathogen Molecular Biology and
Biochemistry Unit, Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical
Medicine, London, UK
We conducted a survey to determine the vectors of malaria in six localities of Serra do Navio munici-
pality, State of Amapá, from 1990 to 1991. Malaria infection rates of 29.3%, 6.2% and 20.4% were
detected by human blood smears in Colônia Água Branca, Porto Terezinha and Arrependido, respec-
tively. There was no malaria infection detected in Serra do Navio. Fifteen species were identified among
3,053 anopheline mosquitoes collected by human bait and 64.4% were identified as Anopheles albitarsis
s.l., 16.7% An. braziliensis, 9.5% An. nuneztovari and 5.8% An. triannulatus. An. darlingi, the main
vector of malaria in the Amazon region of Brazil, was scare. Using enzyme-linked immunosorbent assay
(ELISA), a total positive rate of 0.8% (23/2876) was found for six species: fifteen An. albitarsis s.l., four
An. nuneztovari, and one of each: An. braziliensis, An. triannulatus, An. oswaldoi and An. rangeli. Nine
of 23 positive mosquitoes were infected with Plasmodium malariae, eight with P. vivax VK210, three
with P. vivax VK247 and three with P. falciparum. Since An. albitarsis s.l. was collected feeding on
humans, was present in the highest density and was positive by ELISA for malaria sporozoites, it prob-
ably plays an important role in malaria transmission in this area.
Key words: mosquito - Anopheles - malaria vector - Plasmodium - Brazil
Since the 80’s, several studies on malaria trans-
mission have been carried out in different parts of
the Brazilian Amazon and, based on dissections,
enzyme-linked immunosorbent assays (ELISA)
and anthropophilic behavior, Anopheles darlingi
Root, 1926 was found to be the main vector. Other
species such as An. albitarsis s.l. Lynch-
Arribalzaga, 1878, An. deaneorum Rosa-Freitas,
1989, An. oswaldoi (Peryassú, 1922), An.
mediopunctatus s.l. Theobald, 1903 (now a com-
plex of three species – Sallum et al. 1999) and An.
triannulatus (Neiva and Pinto, 1922) are consid-
ered to be potentially regional vectors (Arruda et
al. 1986, Tadei et al. 1988, Deane 1988, Lourenço-
de-Oliveira et al. 1989, Klein et al. 1991,
Branquinho et al. 1996) and, more recently, An.
marajoara Galvão and Damasceno, 1942 has been
determined to be a new emerging malaria vector
near Macapá, State of Amapá (Segura 1998). De-
spite the high prevalence and wide distribution of
human malaria in Brazil, there are areas or states
such as Amapá where little information about abun-
dance and identification of anopheline mosquitoes,
or their vector status is available.
The present study was conducted to identify
anopheline mosquitoes and to determine their role
as potential vectors in each of six localities in the
Serra do Navio (SNV) municipality, in Amapá.
MATERIALS AND METHODS
Study site - The study area is the municipality
of SNV (0o57’00”S, 52o00’49”W; elevation 380
m) located 146 km north of Macapá, the capital of
Amapá. The climate is that of a tropical rainforest
with a rainy season in which 85% of the precipita-
tion generally occurs, and a dry season. From De-
cember to March it rains several times every day
with high intensity but short duration; from April
to June the rain is continuous and heavy; and from
July to November (the dry season) the rain is less
frequent and of lower intensity. The mean rainfall
for 1990 was 293.6 mm (January-June) and 129.1
This study received financial support from the UNDP/
World Bank Special Programme for Research and
Training in Tropical Disease (grant ID 870284) and
from the Instituto Evandro Chagas/Funasa, Ministry
of Health, Brazil.
Corresponding author. Fax: +55-91-211.4417. E-mail:
*Present address: Division of Parasitic Diseases, CDC,
4770 Buford Highway, NE Atlanta GA 30341-3724,
Received 15 May 2000
Accepted 27 September 2000
SNV was created in 1947, when Icomi
(Indústria e Comércio SA) received a license to
explore mineral resources in this area for a period
of 50 years (Gusmão 1991). From 1954 to 1960,
the company constructed an industrial park and a
residential village to accommodate a population
of about 2,000-2,500 inhabitants. The administra-
tive, industrial and residential areas (SNV treated
area) were completely isolated from one another.
Facilities included a water purification plant, a sew-
age treatment plant, rain water drainage, a rubbish
incinerator and a hospital. A disease control pro-
gram was initiated, aimed mainly at malaria and
leishmaniasis, that consisted of water purification,
houses with window and door screening, biannual
residual insecticide (DDT) spraying, domestic ani-
mal control and administration of chloroquinised
salt to every inhabitant. The three localities (CAB:
Colônia Água Branca, PT: Porto Terezinha, and
ARR: Arrependido) are small villages which have
a standard of living in marked contrast with that of
the population of SNV (the treated area). The
houses in these villages are made of wood with
roofs of zinc panels, strong plastic or dry palm
leaves, and there has been no vector control to re-
duce parasite transmission.
Mosquito collection - Anopheline mosquito
collections were carried out four times, twice in
each year, for about 20 days during each of the
wet and dry seasons. Different collection sites were
chosen within each locality. These included SNV
(the treated area), SNV the forest, and SNV
Carpintaria, as well as CAB, PT and ARR.
Carpintaria was separated from SNV because, al-
though people from SNV work there during the
day, no one stays there at the time of peak biting
activity of anophelines. The forested area was part
of SNV, located between SNV and CAB, PT and
ARR. It was not treated. Each sampling site was
visited for at least three days during each trip, by a
protozoologist and three entomological techni-
cians. Human bait catches were made peridomes-
tically (indoors and outdoors) in the residential
areas and light traps (Shannon and CDC) were used
in the forest. Collection periods were 18-22 h and
in addition, at least one 12 h collection was con-
ducted in each locality. Mosquitoes were collected
by pairs of collectors and a rotating catch time-
table was used to prevent a bias due to personal
differences in attraction and skill. The mosquitoes
were separated at the time of collection into glass
tubes. The identification of adult anophelines was
carried out using taxonomic keys (Forattini 1962,
Faran & Linthicum 1981).
Detection of sporozoites - All anophelines from
light traps and human bait captures were tested for
the Plasmodium circumsporozoite protein (CSP)
by ELISA (Wirtz et al. 1987). Specimens were
identified, placed in capped vials and kept in plas-
tic bags containing silica gel. In the laboratory at
Evandro Chagas Institute, Belém, specimens were
stored at -20oC until tested. The head and thorax
of each specimen was triturated prior to use in the
test. Positive controls for each Plasmodium spe-
cies were placed in two wells of each test plate.
Negative controls (uninfected mosquito homo-
genates) were placed in four wells and blocking
buffer in four wells. The same batches of capture
monoclonals, peroxidase-labelled mono-clonals
and positive controls were used in all tests. Posi-
tivity was determined by both visual reading and
at 405-414 nm using an ELISA reader 30 min af-
ter the substrate had been added. The cut-off was
selected as twice the mean of negative controls
(Wirtz et al. 1987).
Collection parameters - Ninety-five mosquito
collections were made during four trips (two each
in the dry and rainy seasons). The usual capture
time was 4 h a day (from 18 to 22 h) based on the
peak activity of the species in all localities as de-
termined by the 12 h collections. The range of tem-
perature during collections was 23oC to 31oC for
both wet and dry seasons and the relative humid-
ity ranged from 78 to 100% in the wet season and
from 62 to 100% in the dry season with means of
96% and 80.3%, respectively. Collections were
carried out during all four phases of the moon, on
days with or without rain and wind. The number
of bites/man/hour for each area during dry and
rainy seasons is shown in Table I, with the highest
index obtained in the dry season.
Distribution of mosquito species - Fifteen
anopheline species were identified among 3,053
mosquitoes collected in the four localities. The most
frequent species and their distribution by locality
and season are shown in Table II. The majority
(96.4%) of mosquitoes caught consisted of four spe-
cies, An. albitarsis s.l. (64.4%), An. braziliensis
(Chagas, 1907) (16.7%), An. nuneztovari Galbadon,
1940 (9.5%) and An. triannulatus (5.8%). The re-
maining 11 species [An. oswaldoi, An. darlingi, An.
peryassui Dyar and Knab, 1908, An. minor Costa
Lima, 1929 , An. neivai Howard, Dyar and Knab,
1903, An. intermedius (Chagas, 1908), An.
mediopunctatus s.l., An. rangeli Galbadon, Cova-
Garcia & Lopes, 1940, An. evansae (Berthes, 1926),
An. argyritarsis Robineau-Desvoidy, 1827 and
Chagasia bonneae Root, 1927] were uncommon
(3.6%). Most mosquitoes (77.2%) were collected
during the dry season.
Sporozoite rate by salivary gland dissection -
We carried out 88 dissections of mosquitoes col-
lected from human bait, of four species: 35 An.
albitarsis s.l., 20 An. braziliensis, 15 An.
nuneztovari, 10 An. triannulatus and 8 An.
oswaldoi, of which 46 (52.2%) mosquitoes were
parous. Of those, three had sporozoites in the sali-
vary glands (one each of An. albitarsis s.l., An.
braziliensis and An. nuneztovari) and four had oo-
cysts on the stomach wall (two were the same speci-
mens that had sporozoites – An. braziliensis and
An. nuneztovari – and two An. oswaldoi). The over-
all infection rate for the salivary glands was 3.4%
and for stomachs 4.5%.
Infection with malaria parasites - The positive
rate of the total number of mosquitoes tested by
ELISA performed with CSP antigen for P.
falciparum, P. vivax VK210, P. vivax VK247 and
P. malariae, was 0.8 (23/2876) belonging to six
mosquito species: 15 An. albitarsis s.l., four An.
nuneztovari and one of each: An. braziliensis, An.
triannulatus, An. oswaldoi and An. rangeli. Nine
were positive for P. malariae (five An. albitarsis
s.l., and one of each An. braziliensis, An.
nuneztovari, An. triannulatus and An. rangeli),
eight for P. vivax VK210 (seven An. albitarsis s.l.
Number of bites/man/hour for all areas in which anophelines were collected, during the dry and rainy seasons
(February and August 1990 and April and September 1991)
Study areaDry season Rainy season
Serra do Navio (SNV)-treated area
Serra do Navio forest
Serra do Navio Carpintariac
Colonia Água Branca
a: P>0.05, Chi-square test; b: P< 0.05, Chi-square test; c: locality 3 km from SNV (the treated area), at the foot of
Number of each Anopheles species collected during 1990-1991 in study areas Serra do Navio (SNV), Colonia
Água Branca (CAB), Porto Terezinha (PT) and Arrependido (ARR), by season
An. albitarsis s.l.
Total 221/195 75/140142/189 259/1832697/2356 3053
a: consists of mosquitoes collected in the forest and Carpintaria (none was collected in the treated area); b: other
Anopheles mosquitoes collected in low numbers included: An. intermedius, An. mediopunctatus, An. rangeli, An.
evansae, An. neivai, An. argyritarsis and Chagasia bonneae; W: wet season; D: dry season; ( ): percentages
determined in relation to the total number of mosquitoes collected by locality.
and one An. nuneztovari), three for P. falciparum
(two An. albitarsis s.l. and one An. oswaldoi) and
three for P. vivax VK 247 (one An. albitarsis s.l.
and two An. nuneztovari) as shown in Table III.
Abdomens of all positive specimens were also re-
tested by ELISA and only the An. triannulatus was
negative for this second test.
No mosquitoes were collected in the residen-
tial and administrative part of the treated area
P. malariae, found in some mosquitoes col-
lected in the SNV-forest, could be P. brasilianum
Gonder and Berenberg-Gossler, 1908 which is a
monkey parasite (Deane 1992) that are indistin-
guishable by morphological techniques from P.
malariae (Lal et al. 1988) and had already been
detected in monkeys captured in these localities
(Deane 1969, Deane & Ferreira Neto 1969, Deane
et al. 1971).
Migratory movement has played an important
role in the spread of malaria in Brazil (Marques
1986), since the exodus in Brazil has been from
town to rural areas and within the rural areas in the
Amazon region. This was initially a result of a Fed-
eral government program for populating and de-
veloping the Amazon region based on a belief that
in the Amazon region everyone was entitled to land
in order to facilitate economic development. This
resulted in a major migration of people from all
parts of Brazil to become farmers, goldminers or
hydroelectric workers (Alecrim 1992). Deforesta-
tion and burning were carried out to provide space
for settlements, resulting in drastic changes in the
ecology of this region (Marques 1987). Those
changes and the growth of settlements without pro-
vision for infrastructure, are thought to have con-
tributed to the spread of malaria throughout the
Amazon region by the formation of new breeding
sites for Anopheles mosquitoes (Marques 1986).
In the 60’s, companies such as Icomi estab-
lished projects which created new residential lo-
calities and new jobs and this subsequently in-
creased migration. Even companies that had made
extensive preparations faced problems of morbid-
ity and mortality from tropical diseases, mainly
malaria and leishmaniasis. This was the stimulus
for Icomi to establish a program for the control of
malaria, the most important disease in the area
The prevalence of malaria infections in the lo-
calities (CAB, PT and ARR) during the period of
this study (1990-1991) was 29.3%, 6.2% and
20.4%, respectively, and there were no malaria
infections in SNV-treated area (Póvoa 1993). Data
Positive rate by enzyme-linked immunosorbent assay of Anopheles species collected in the localities [Serra do
Navioa (SNV), Colonia Água Branca (CAB), Porto Terezinha (PT) and Arrependido (ARR)]
PF PV1 PV2PM TIM/TTM
SNV CAB PT ARR SNV CAB PT ARR SNV CAB PT ARR SNV CAB PT ARR
a: consists of mosquitoes collected in the forest and in Carpintaria; b: An. darlingi, An. peryassui and An. minor
were all negative; c: one of each of these mosquitoes was also positive by dissection (sporozoite); d: other Anopheles
mosquitoes collected in low number included: An. intermedius, An. mediopunctatus, An. rangeli, An. evansae, An.
argyritarsis and Chagasia bonneae; e: An. rangeli; f: total tested including negative specimens; PF: Plasmodium
falciparum; PV1: P. vivax VK210; PV2: P. vivaxVK247; PM: P. malariae; TIM: total of infected mosquitoes;
TTM: total of tested mosquitoes; -: negative; ( ): percentages determined in relation to infected mosquito by the
total number of collected mosquito.
from 1961 (prior to the control measures) show
malaria infection in SNV (47.1%), then a sharp
decrease in the rate to 4.3% immediately after the
establishment of the daily intake of chloroquinised
salt in 1963 as part of the malaria control program
established by Icomi until 1993. Therefore, in the
treated area at SNV, it was not surprising to find
no evidence of malaria infection.
Unpublished records of the Anopheles species
distribution in the SNV area obtained by Icomi
malaria control program, show that in the 60’s An.
darlingi was found close to the SNV residential
areas. After the implementation of their control
program, this species disappeared from SNV as
confirmed by Deane and Ferreira Neto (1969), and
has only been occasionally reported from SNV
Carpintaria (the present study).
Our findings support the Icomi data since we
collected An. darlingi (n=16) from all localities
except SNV (the treated area). In the forest con-
necting SNV residential and administrative areas
to the other three localities, the Anopheles species
collected during our study are those considered
predominantly zoophilic (e.g. An. triannulatus, An.
rangeli and An. evansae) (Consoli & Oliveira
Our results demonstrate that the number of
bites/man/hour is significantly higher at SNV-
Carpintaria during the dry season, possibly sup-
porting the observation that most malaria transmis-
sion in the Amazon Basin occurs at this time (Deane
1988). However, in all other localities, no seasonal
differentiation was observed. The locality ARR had
significantly higher (Chi-square test, P < 0.05)
bites/man/hour in both seasons compared with all
other localities except Carpintaria and also a high
malaria infection rate (20.4%). Because 14/23 of
the mosquitoes positive by ELISA were collected
at ARR, and only 4/23 at CAB (in spite of a ma-
laria infection rate of 29.3%), we suggest that the
highest risk for malaria transmission was for the
inhabitants of ARR.
Reports on malaria vectors in Brazil are few.
Based on studies carried out in the 40’s and 50’s,
it was established that along the coast, malaria was
transmitted with a low level of endemicity by the
brackish-water breeder An. aquasalis and in all
other areas where malaria transmission occurred,
An. darlingi was the primary vector. However,
species of the subgenus Kerteszia were also im-
portant on the transmission of malaria in the south-
ern part of Brazil. Other species such as An.
albitarsis and An. braziliensis were sometimes of
secondary importance as malaria vectors (Deane
et al. 1946, 1948). In our study we determined spe-
cies carrying human malaria sporozoites detectable
by ELISA, were the same as those reported in past
studies in Brazil (Arruda et al. 1986, Tadei et al.
1988, Lourenço-de-Oliveira et al. 1989,
Branquinho et al. 1996), plus An. braziliensis and
An. rangeli. The latter was positive only for P.
malariae/brasilianum, but we do not believe that
this specie take role on the transmission of both,
human and simian malaria in the Brazilian Ama-
Because An. albitarsis s.l. was caught with hu-
man bait, presented the highest density over lo-
calities, was positive by ELISA for the four tested
species of Plasmodium and positive by salivary
glands dissection for malaria sporozoites, it prob-
ably plays an important role in the epidemiology
of malaria in these localities. It is also worth not-
ing the number of An. nuneztovari caught in CAB,
which, as in Venezuela (Gabaldón 1981, Rubio-
Palis & Curtis 1992) and in Suriname (Rozendal
1990), probably plays a role in local malaria trans-
All Anopheles mosquitoes positive for P.
malariae were collected in the forest area, where
on several occasions during the catches we saw
small monkeys. Since P. brasilianum (monkey
malaria parasite) is genetically and morphologi-
cally indistinguishable from P. malariae (Lal et
al. 1988), probably a sylvatic cycle of this parasite
occurs in this area. Our records did not show in-
fection in man caused by P. malariae and the SNV
hospital and Fundação Nacional de Saúde records
show a very low prevalence of this parasite, yet a
high positivity in mosquitoes was detected for P.
malariae in SNV. The maintenance of this Plas-
modium could therefore be through the monkeys.
Marques (1986, 1987) showed that the spread
of malaria in Brazil started in the 60’s with the
building of new roads followed in the 70’s with
the establishment of hydroelectric projects and in
80’s with the emergence of the gold prospecting
sites. He classified transmission areas of malaria
in Brazil as “stable malaria” (old transmission ar-
eas) and “frontier malaria” (recent transmission
areas). The Meeting of World Health Organiza-
tion (WHO) held in Amsterdam, in 1992, resulted
in a global malaria control strategy which suggested
that each country, based on its specific character-
istics of malaria transmission, had to identify local
problems and priorities in order to apply appropri-
ate interventions (WHO 1992). Based on the WHO
suggestions and considering the classification made
by Marques, our localities, CAB, PT and ARR have
the characteristics of areas of “stable malaria”.
The control measures used at SNV aimed at
decreasing the human/vector contact were very
effective (i.e., we collected very few mosquitoes
and they were primarily zoophilic, and no malaria
cases were detected by blood smears). In contrast,
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after the desativation of the control system at SNV,
human malaria cases were registered and we col-
lected infected mosquitoes within the residences.
Similar institutional programs are likely to dramati-
cally reduce malaria transmission in the Amazon
region of Brazil.
To assistance in field work by Raimundo Nivaldo
de Almeida and Orlando Vaz, the Icomi hospital techni-
cal personnel and the logistic support of Icomi. To Jan
Conn, Richard Wilkerson and Yasmin Rubio for com-
menting on the manuscript.
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