R e v ista da Socied ad e B rasileira de M e dicina Tropical 24(1): 13-20, ja n -m a r, 1991
B IT IN G B E H AV IO R O F
A N O P H E L E SM O SQ UIT O ES IN C O ST A M A R Q U E S,
R O N D O N IA , BRAZIL
T e r r y A . K le in , J o s e B .P . L im a a n d A m a z o n ia T o d a T a n g
M o sq u ito c olle c tion s were m a d e in a n d n e a r C o sta M a r q u e s, R o n d o n ia , B ra zil, to d e te r m in e a n o p h e lin e a n th r o p o p h ilic /z o o p h ilic beha vior. C o lle c tio n s fr o m a n o n -illu m in a te d , b o v in e -b a ite d trap a n d in d o o r a n d o u td o o r h u m a n -b a it c o llec tio ns were c om pare d. Anopheles darlingi a n d Anopheles deaneorum were m o re a n th ro p o p h ilic th a n th e o th e r a n o p h e lin e s collected. T h e re m a in d e r o f th e Anopheles spe cies were c o llec te d m u c h m o re fr e q u e n tly in b o v in e -b a ite d trap s th a n in h u m a n -b a it c ollec tions. Anopheles darlingi a n d An. deaneorum were m o re fr e q u e n tly c olle c te d in sid e h o u se s th a n th e o th e r a n o p h e lin e species. B u t, w h en c ollec tio n s w ere m a d e in a h o use w ith n u m e ro u s o p e nin g s in th e w alls, the re were f e w d ifference s in th e p e r c e n ta g e s o f each sp e cie s b itin g m a n in d o o r s v ersu s o utdo ors. Anopheles darlingi w as th e p re d o m in a n t m o sq u ito collected, b o th in sid e a n d o u tsid e houses, a n d h a d the stro n g e st a n th ro p o p h ilic fe e d in g b e h a v io r o f the a n o p h e lin e s p re se nt.
Key-words: Anopheles sp. B ra zil, B e ha v io r, A n th r o p o p h ilic . Z o o p h ilic .
The incidence of malaria in the Amazon Basin ofBrazilhas steadily increased over the last ten years7. Marques1*^ outlined many of the problems associated with malaria control and environmental and social factors in Brazil which influenced the increasing malaria trends through 1989. But, in addition, vector behavior and feeding preference also affect the intensity of malaria by governing the human-vector contact12.
Feeding preferences and host behavior have an important influence on the local epidemiology of malaria. F or example, malaria prevalence may be less in communities where the principal malaria vector is not strictly anthropophilic and where cattle range between the villages and major breeding sites8. In some areas of Brazil, observations indicate that local populations of mosquito species are zoophilic, while in others they are anthropophilic^. It is now apparent that these differences are often species differences within species complexes^.
Departments of the Army and Defense of the United States. Instituto de Biologia do Exército, Rio de Janeiro, RJ, Brasil. Laboratório Central de Entomologia, Divisão de Malária, SUCAM/MS, Brasília, DF, Brasil.
This study was supported by the US Army Medical Research and Development Command, Grant DAMD17-84-6-4004 to the University of Brasilia, DF, Brazil.
Núcleo de Medicina Tropical e Nutrição, Universidade de Brasília, Brasília, DF, Brasil.
Address to: Major Terry A. Klein. Division of CD&I. W alter Reed Army Institute of Research, Washington, DC 20307-5100.
Recebido para publicação em 31/01/91.
In our studies, the host attraction of anophelines to bovines and man were compared to identify dif ferences in species behavior. Residences in the small frontier town (house 1) and in a rural area (house 5) 7 km from Costa Marques were sampled to evaluate the malaria vector potential in different environments?.
M A T E R IA L A N D M E T H O D S
Mosquitoes were collected on human-bait (inside and outside houses) and in a non-illuminated bovine- baited trap (Figure l)n e a r house 1 in the town of Costa Marques (12°26’S, 64°14’W ), Rondonia and near a corral at house 5, 7 km from town along road BR 429 leading to Presidente Medici. Detailed descriptions of the areas and houses were provided by Klein and Lima7. House 1 was made of wood construction with open eaves and unscreened windows and doors. House 5 was poorly constructed having numerous gaps >2.5 cm between the wall boards. Collections were con ducted alternately at house 1 (urban) and then house 5 (rural) for each collection period from April 1987 through September 1987. One volunteer conducted human-bait collections for 40 minutes at the beginning of each hour from 1800 to 0700 h by exposing their feet and lower legs to natural populations of mosquitoes. During the last 20 minutes of each collection hour, the collector aspirated mosquitoes from the non-illumi nated bovine-baited trap. All mosquitoes were collec ted with oral aspirators, transferred to screened 215 cm3 (pint) cartons, killed by freezing and identified as described by Klein and Lima7.
K le in TA, L im a JBP, T a n g A T. B itin g b ehavior o f Anopheles m osquitoes in C osta M arques, R ondonia, B r a z il R e vista d a òocieaaae B ra sile ira d e M e dic in a T ropical 2 4 :1 3 -2 0 , ja n -m a r, 1991
F ig u r e 1 - S c h e m a tic d r a w in g o f th e n o n - illu m in a te d b o v in e -b a ite d trap. A n o p h e lin e c olle c tion s f r o m th e b o v in e -b a ite d tra p were c o m p a re d to th o s e f r o m h u m a n -b a it c olle c tio n s in sid e a n d o u tsid e houses.
T a b le 1 - Anopheles c o m p o sitio n a n d p re fe re n c e f o r h u m a n -o r b o v in e -b a it f r o m A p r il th rou gh S e pte m be r, 1 9 87 , C osta M a rq u e s.
Anopheles
Number mosquitoes collected
Urban1 Rural1
House 1 House 5
Bovine Human Human Bovine Human Human
(out) (in) (out) (in)
S u b g e n u s (N y s so rh y n c h u s )
a lb ita rs is 6 0 2 933 150 71
b r a zilie n s is 1 0 0 0 0 0
d a rlin g i 768 2,440 364 518 1,762 507
d e a n e o ru m 153 516 98 107 65 39
n u n e z to v a r i 0 0 0 5 0 0
o s w a ld o i 17 10 1 192 27 14
ro n d o n i 2 0 0 0 0 0
tria n n u la tu s 10 12 1 34 9 3
Subgenus {A no p h e le s)
m a tto g ro sse n sis 20 3 0 7 0 0
m e d io p u n c ta tu s 2 0 0 2 0 0
m in o r 0 0 0 0 0 1
p e r y a ss u i 0 0 0 2 0 0
Total 384 2,981 466 1,796
K le in TA, L im a J B P , T a n g A T . B itin g be havior o f Anopheles m osquitoes in C osta M arques, R ondonia, B razil. R e vista da S ocieda de B rasileira de M e dic in a Tropical 2 4 :1 4 -2 0 , ja n -m ar, 1991
RESULTS
In the Costa Marques area, 12 species of adult anophelines were collected from bovine - and human- bait (Table 1). Species diversity was much greater in the rural environment than within the town o f Costa Marques. A n o p h e le s d a r lin g i was the most frequently collected anopheline from human-bait inside and outside houses (81%) in Costa Marques and at house 5(86%), 7 km from Costa Marques (Figures 2 and 3).
A n o p h e le s d e a n e o r u m was the second most abundant anopheline collected in the town of Costa Marques
( 1 8 % ) and together with A n . d a r l i n g i comprised >99% of the total anophelines collected on human- bait at house 1. Three species,,4«. d a r lin g i (85%), A n . a l b i t a r s i s ( 10%) and/1«, d e a n e o r u m (4%) comprised 98% of the anophelines collected in human-bait at house 5. Large differences in the average number of
A n . d e a n e o r u m and A n . a lb ita r s is were observed between house 1 and house 5 (Figure 2). Comparisons
betwfeen house 1 and house 5 were only made for A n.
d a r l i n g i a n d A n . d e a n e o r u m because other anopheline species were infrequently collected in either bovine or human-bait captures in the town of Costa Marques.
In bovine-bait collections in the town of Costa
Marques, 77% of the anophelines collected were A n .
d a r lin g i while 15% were ,4«. d e a n e o r u m . There was only a slight increase in the percent of the remaining species of anophelines collected on bovine-bait. A t house 1, there was little difference in the percentage of
A n . d a r lin g i a n d A n . d e a n e o r u m collected on human- andbovine-bait (Figure 2). However, 7 km from Costa Marques (house 5), where the diversity of anophelines
was much greater, A n . d a r lin g i only comprised 29%
while A n . a lb ita r s is comprised 52% of the anophelines from bovine-bait collections (Figures 2 and 3).
A n o p h e le s d a r lin g i a n d A n . d e a n e o r u m demonstrate a preference for feeding on humans and were collected in houses more frequently than the other anopheline species .A n o p h e l e s a lb ita r s is collected on bovine-bait was 7X greater than those collected on human-bait (Figure 4). The percentage of A n . o s w a ld o i and A n . t r i a n n u l a t u s collected in bovine-baited traps was also greater for the bovine-baited trap.
D ISCUSSION
A n o p h e le s d a r l i n g i and A n . d e a n e o r u m are likely the most important malaria vectors in Costa Marques based on their seasonal distribution, fre quency, endophilic and anthropophilic behavior and
susceptibility to malaria parasites7 8 9 However, A n .
d e a n e o r u m is only seasonally abundant during the late rainy to early dry season and therefore only augments malaria transmission from May through September in
Costa Marques7. Since A n o p h e le s a lb ita r s is is zoo- philic, not susceptible to P . f a l c i p a r u m and less susceptible to oocyst infection by P. v iv a x than A n . d a r l i n g f i 9, we feel that this species is likely a secondary vector. A n o p h e l e s m e d io p u n c ta tu s is
equally susceptible to sporozoite infection by P.
f a l c i p a r u m but is less susceptible to oocyst infection by P. v iv a x th a n A n . d a r lin g i and is only collected in forested areas and is also seasonal (unpublished data). This species may be seasonally important for malaria transmission for persons frequenting or living in forest habitats.
While A n . d a r l i n g i and A n . d e a n e o r u m were both more anthropophilic than other anophelines collected in Costa Marques, a large proportion were collected in the bovine-baited trap (Table 1). In areas where mosquito biting activity is crepuscular and present control measures are not effective, zoopro- phylaxis, or a technique to divert mosquitoes seeking a blood meal away from man, may be effective in reducing human malaria. This must be thoroughly investigated since the degree of anthropophilic behavior, location in relation to breeding sites of the animal bait and potential increase in mosquito density by increased success of blood-feeding also affects the frequency of mosquito bites on man and the infection rate of malaria14. S c h u l t z 1 2 demonstrated that people
received approximately 40% fewer bites outdoors from A n . f l a v i r o s t r i s and A n . a n n u l a r i s when the animal bait was placed between the human population and larval habitats or adult resting sites. However, the
frequency of mosquitoes collected indoors for A n .
f l a v i r o s t r i s a n d A n . a n n u l a r i s increased by 1.5X and 11.8X, respectively, when cattle were placed near houses. White and Rosen15 further demonstrated that
there was no difference in the vectorial capacity o i A n .
g a m b i a e and A n . a r a b ie n s is when cattle were not present In the presence of cattle, the vectorial capacity of A n . a r a b ie n s is was much lower than A n. g a m b i a e
because of its zoophilic feeding preference15. Ho wever, Sota and Mogi14 suggest that by introducing cattle, anopheline population densities may increase through greater success of blood-feeding. This may have an adverse affect by increasing the frequency of mosquito bites on man and the infection rate of malaria.
The vectorial capacity o f A n . a lb ita r s is as well as other species may be reduced dramatically when cattle are present due to their exophilic behavior and its preference for cattle as hosts. In the absence of alternate domestic hosts or high population densities,
A n . a lb ita r s is may become an important vector of
P l a s m o d i u m v iv a x in rural areas of Costa M arques^11 • Evidence also indicates that in the absence of
alternate domestic hosts, A n . t r i a n n u l a t u s and A n .
K l e i n TA , L i m a J B P , T a n g A T . B iti n g b e h a v io r o f Anopheles m o sq u ito e s in C o sta M a rq u e s, R o n d o n ia , B r a z i l R e v is ta d a S o c ie d a d e B ra sile ir a d e M e d ic in a T ro p ic a l 2 4 : ja n - m a r , 1 9 9 1
K le in TA, L im a JBP, T a n g A T . B itin g be havior o f Anopheles m osquitoe s in C osta M arques, R ondonia, B razil. R e v ista da S ocieda de B rasileira de M e dicina Tropical 24: 13-20, ja n -m a r, 1991
o s w a ld o i readily bite man. However, their importance in malaria transmission is probably much less because sporozoites were rarely found in the salivary glands of dissected mosquitoes in malaria susceptibility tests** 9.
It is difficult to make generalizations from one location to another because of current taxonomic problems with anophelines in the Amazon region2 7. D ata in the literature are often contradictory. F or example, F aran .and Linthicum4 and Charlwood and Wilkes1 report that A n . t r i a n n u l a t u s is zoophilic, rarely enters houses, but readily feeds on man outdoors, while Gabaldon5 reports that this specie primarily bites indoors. In our study, A n . tr ia n n u l a t u s rarely entered houses, but was frequently collected in human- bait collections in forested areas and along river margins. A larger percentage of A n . t r i a n n u l a t u s was collected in a bovine-baited trap, indicating a zoophilic preference.
Faran and Linthicum4 report th a t A n . o s w a ld o i
adults are largely restricted to the forest, and are exophilic and zoophilic. In other studies, populations of A n . o s w a ld o i were generally restricted to forest habitats and these mosquitoes readily bite man during the early evening and daytime when the sky was overcast (Klein and Lima, unpublished data).
Shannon and D a v i s 1 3 indicated that A n. a lb
i-ta r s is s e n s u la to did not, as a rule, enter houses as frequently as A n . d a r lin g i, but it will invade houses in
relatively large numbers. In Costa Marques, A n .
d e a n e o r u m readily enters houses, is anthropophilic, and is a vector of both P. f a l c i p a r u m and P. v iv a x . In contrast, A n . a lb ita r s is in Costa Marques is zoophilic, but will also bite man and enter poorly constructed houses with large spaces in the walls6.
In summary, zooprophylaxis may reduce the vectorial capacity of anopheline human malaria vec tors in some areas of Brazil. However, the endophilic/ exophilic and anthropophilic/zoophilic behavior of potential vector populations need to be evaluated more closely to determine the effectiveness of this method against malaria. With a strongly anthropophilic species like A n . d a r lin g i, alternate host availability may have little effect in reducing the incidence of malaria. Additionally, behavioral studies frequently lead to recognition of taxonomic problems and identification of potential vector populations/species. Resolving vector systematic problems ultimately results in a more effective malaria control program by allowing specific vector species to be identified and targeted.
R E S U M O
P a ra d e te r m in a r o c o m p o r ta m e n to a n tro p o filic o e zo o filic o d o s a n ofe lino s, f o r a m c a p tu ra d o s m o s q u ito s n a p e r ife ria e n a z o n a u rb a n a d e C o s ta M a rq u e s , R o n d ô n ia ,
B r a sil. F o r a m c o m p a ra d a s a s c a p tu ra s f e ita s à noite, c om isc as b o vin as e h u m a n a s, dentro e fo r a de casa. O Anopheles darlingi e o Anopheles deaneorumfo r a m m a is a n tro p o jilic o s
d o q u e o s o u tro s a n o fe lin o s ca p tu ra d os. O re sta n te d a s e spé cies a n o fe lin a s f o i c a p tu ra d o m a is fr e q ü e n te m e n te nas isc a s b o v in a s d o q u e n a s h u m a n a s. Anopheles darlingi e
Anopheles deaneorumf o r a m c a p tu ra d o s d en tro d e c a sa com m a is fr e q ü ê n c ia d o q u e a s o u tra s espécies an ofe lina s. P orém , q u a n d o a c a p tu ra f o i fe ita e m c a sa s c om m u ita s a b e rtu ra s n a s p a r e d e s h o u v e p o u c a d ife re n ça n a s p o rc e n ta g e n s d e c a da e spéc ie sug a d o ra d e h u m a n o s d en tro e fo r a d e casa. Anopheles darlingi f o i o m o sq u ito c a p tu ra d o com m a is fr e q ü ê n c ia , d e n tro e f o r a d e casa, e a p re sen ta v a m a io r a n tro p o filia e m re la ção a o s o utro s a n o fe lin o s p re sentes.
Palavras-chaves: Anopheles sp. B ra sil. C o m p o rta m en to . A n tr o p o filic o . Z o o filic o .
A C K N O W LED G M EN TS
W e gratefully appreciate Luis Gil, Jose Rodri gues and M aria Fatim a Barros for their technical support. We thank the following colleagues Stephen Hembree, USAMRU-Brazil, Aluizio R. Prata, Va- nize Macedo and Mauro S. Tada, University of Brasilia, Brasilia, and Lyman Roberts, W alter Reed Army Institute of Research for their support.
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