Ecology of Anopheline (Diptera, Culicidae),
malaria vectors around the Serra da Mesa
R e s e r v o i r, State of Goiás, Brazil.
1 – Frequency and climatic factors
Ecologia de Anophelinae (Diptera, Culicidae),
v e t o res de malária em áreas da Usina Hidre l é t r i c a
de Serra da Mesa, Estado de Goiás, Brasil.
1 – Freqüência e fatores climáticos
1 La b o ratório de Di p t e ra , De p a rtamento de En t o m o l o g i a , Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Rio de Ja n e i ro, Bra s i l .
C o r re s p o n d e n c e Anthony Érico Gu i m a r ã e s La b o ratório de Di p t e ra , De p a rtamento de En t o m o l o g i a , Instituto Oswaldo Cruz, Fundação Oswaldo Cruz. Av. Brasil 4365, Rio de Ja n e i ro, RJ 2 1 0 4 5 - 9 0 0 , Bra s i l . a n t h o n y @ i o c . f i o c r u z . b r
Anthony Érico Guimarães 1
Ca rla Gentile 1
Je ronimo Alencar 1
Catarina Macedo Lopes 1
Rubens Pinto de Mello 1
A b s t r a c t
The ecology of anopheline species (Di p t e ra , Culicidae) was studied in the vicinity of the Se r ra da Mesa Re s e rvo i r, State of Go i á s , Bra z i l . Climatic factors and frequency of anopheline populations were analyze d . Bimonthly hum a n -bait and Shannon trap captures were conduct-ed for 36 consecutive months ( Ja n u a ry 1997 t h rough December 1999). A total of 5,205 a d u l t anophelines belonging to five species were
col-l e c t e d .Anopheles darlingiwas the most
fre-quently collected anopheline (61.4%), f o l l ow e d by An. albitarsis s. l .( 3 5 . 4 % ) ,An. tri a n n u l a t u s. ( 2 . 5 % ) ,An. oswaldoi( 0 . 4 % ) , and An. eva n s a e ( 0 . 2 % ) . The water level and vegetation along the banks of the re s e rvoir were crucial to the f requency of the various anopheline species. Climatic factors had a secondary influence. The re s e rvo i r ’s water- l e vel stability, i n c re a s e d f requency of An. darlingi, and the arrival of gold prospectors were responsible for the in-c rease in malaria in-cases.
Ma l a r i a ; Vectors Ecology ;E c o l o gy
I n t ro d u c t i o n
Human intrusion in natural ecosystems and the resulting environmental changes modify established niches and create conditions for new ecological configura t i o n s. Such changes p rovide opportunities for the establishment of mosquito vector populations and tra n s m i s s i o n of the re s p e c t i ve ve c t o r- b o rne diseases.
A prime example of radical human inter-vention in the environment is the constru c t i o n of hyd ro e l e c t ric power plants, with major eco-logical impacts on vector population dynam-i c s. The rdynam-isk of epdynam-idemdynam-ics has been shown to i n c rease as the result of deforestation, con-s t ruction of hyd ro e l e c t ric damcon-s, and the intro-duction of human population groups where in-sect ve c t o r- b o rne diseases are endemic.
In the present study, we observed the p ro c e s s of human intrusion →e n v i ronmental change
Material and methods
The Se r ra da Mesa Re s e rvoir is located in the Upper Tocantins River Basin, nort h e rn Go i á s State (13o50’ S, 48o18’ W ). The dam, 1,500 m long, 154 m high, and 460 m above sea level, is located on the main channel of the To c a n t i n s R i ver (Municipality of Minaçu) 1,790km fro m its mouth (Fi g u re 1). The Se r ra da Mesa Re s e r-voir is the largest in Brazil in terms of water volume flow. Du ring maximum flow the re s e r-voir contains 54.4 billion m3, measures 1,784 k m2, and extends to the limits of five main t owns: Ba r ro Alto, Ca m p i n o rt e, Minaçu, Ni q u e-lândia, and Uru a ç u .
The re s e rvoir is located in the c e r ra d o( s a-vannah) ecosystem, which in all occupies some two million km2of Bra z i l’s terri t o ry. The Bra z i l-ian c e r ra d ois occupied by an extensive p l a t e a u , b e t ween 300 and 600m high, extending into the States of Amazo n a s, Rondônia, Pará, Ma ran h ã o, Piauí, To c a n t i n s, Go i á s, Mato Gro s s o, Mato Gro s-so do Sul, Bahia, Minas Ge ra i s, and São Pa u l o and the Fe d e ral Di s t ri c t .
This region features abundant metamor-phic rock from the lower Pro t e rozoic peri o d and major natural deposits of asbestos in the municipality of Minaçu and nickel in the mu-nicipalities of Niquelândia and Barro Alto. Sm a l l g ranite outcroppings in the shape of re s i d u a l peaks are occasionally observed. The Se r ra da Mesa Dam was built on the Goiano plateau consisting of a dome called the “Granito Se r ra da Me s a” and circled by deformed metamor-phic rocks (e.g., para g n e i s s, quart z i t e, and mi-caschist).
The re g i o n’s vegetation, influenced by the Se r ra da Mesa Re s e rvo i r, consists of sparse and re l a t i vely short trees that ra rely reach a height of 10m, numerous bushes, and a lower layer of g rassy plants. The trees often have large and rough leave s, with twisted thick-barked tru n k s and bra n c h e s. These features are associated with high levels of aluminum in the soil ra t h e r than the lack of water. The twisting of tru n k s and branches is related to the frequent fore s t f i res that result in the loss of the main shoots, stimulating the sprouting of surrounding buds, thus forming irregular and twisted bra n c h e s. Even in the driest period these woody plants g u a rantee access to water through their long roots that can reach 20m below the surf a c e.
Ga l l e ry forests extend non-continuously along the ri ver banks and in wet terra i n s, form-ing irregular patches of forest. The study are a’s climate is hot and tropical sub-humid. Ave ra g e annual rainfall ranges from 1,500 to 2,000mm, with more than 70% of precipitation occurri n g
f rom October through Ap ril (Fi g u re 2). In the p e riod of heavy rainfall the re l a t i ve humidity f requently exceeds 90% and tempera t u re highs a re often above 40oC. May through Se p t e m b e r is an extended intensely dry period with re l a-t i ve humidia-ty levels ofa-ten below 15% and infre-quent light rains (e.g., 20 mm per month in 4 or 5 days of rain and dry periods that may last for as long as 50 consecutive days). The dry peri o d is also the coolest, but tempera t u res ra re l y d rop below 10oC. Te m p e ra t u res above 25oC are not uncommon, with the mean monthly tem-p e ra t u res during this tem-period above 18oC. T h i s climatic profile is chara c t e ristic in regions that a re distant from the coast and subject to stro n g continental effects.
Mosquito surveillance was conducted at f i ve sites (Fi g u re 1) in the area surrounding the Se r-ra da Mesa Re s e rvoir for three consecutive ye a r s, f rom Ja n u a ry 1997 to December 1999. Each site has unique environmental chara c t e ri s t i c s. • Site 1: Municipality of Minaçu: the sam-pling point is located in the construction are a of the Se r ra da Mesa Dam, between 13o4 9 ’ 2 6 . 9 ’’ S and 48o18’ 56.5’’ W, next to the eastern bank of the Tocantins Rive r, near the secondary re s e rvoir (“Re s e rvoir II”) and 5km north of the p ri m a ry re s e rvoir (Fi g u re 1). This area is char-a c t e ri zed by dense woods or c e r ra d ã o( l i t e ra l l y “big sava n n a h”), with 6 meter-high tre e s, the c rowns of which limit the penetration of light to the lower underg rowth laye r s, resulting in a thick layer of organic matter. The gallery fore s t s reach the edges of the re s e rvo i r, forming shad-owy creeks in the many tri b u t a ri e s.
• Site 2: Municipality of Ca m p i n o rte: the s a m-pling point is located at 14o05’ 38.5’’ S and 48o
59’ 51.3’’ W, by the we s t e rn bank of the To c a n-tins Rive r, in a farming pro p e rty known as Planeta Água, 18 km from the secondary access road to the town of Je rusalém, next to the BR-153 highway (Fi g u re 1). Collections we re con-ducted along the banks of a creek that dra i n s into the re s e rvo i r. The site is chara c t e ri zed by f e rtile soil and typical gallery forest ve g e t a t i o n , f o rming dense, mainly arboreal woods, with bushes in the lower underg rowth. Hu m i d i t y and water from the drainage system sustain plant growth throughout the ye a r, providing a habitat that does not suffer the intense climat-ic adversities of the dry peri o d .
• Site 3: Municipality of Uruaçu: the sam-pling point is located at 14o32’ 04.4’’ S and 49o
re c reational activities associated with the re s e r-vo i r. The wooded areas consist mostly of s h ru b s with few trees taller than 3m. The lower laye r consists of small bushes and leaf-cove red soil. The vegetation does not extend to the edges of the re s e rvo i r, where there are clear signs of de-f o restation. In the dry season, the de-few shadow y c reeks are exposed to the sun and the banks become ari d .
• Site 4: Municipality of Ba r ro Alto: the sam-pling point is located at 14o39’ 47.9’’ S and 48o
57’ 35.2’’ W, on the we s t e rn bank of the To c a n-tins ri ver and in mining areas and is 27 km f rom the secondary access road in the distri c t of Placa, via the BR-080 highway (Fi g u re 1). This area has been heavily altered by extensive mining activity. Human settlements are con-c e n t rated in con-crowded shacon-cks. T h e re is heavy t raffic from tra n s p o rtation of people and min-ing equipment and materi a l s, resultmin-ing in ero-sion of the road and surrounding area. The ve g-etation is chara c t e ri zed as c e r ra d ã o, dominat-ed by shrubs with occasional tre e s. The soil l a c k s o rganic matter, with frequent sandy patches exposed to intense sunlight. The sluggish wa-ters of the Ma ranhão River form areas of sparse vegetation along the shady banks.
• Site 5: Municipality of Niquelândia: the sampling point is located at 14o26’ 51.0’’ S and 4 8o57’ 34.6’’ W, on the eastern bank, in areas of the Córrego Dantas Fa rm, 9km from the sec-o n d a ry access rsec-oad beginning at the Pa rada da Vendinha village, via the GO-237 highway (Fi g-u re 1). This region is chara c t e ristic of the Bra z i l-ian c e r ra d ã o. Located between tow n s, the are a consists of extensive plantations and cattle f a rms and small settlements where the local residents live off basic subsistence activities. The local population mostly lives in simple houses near the Re s e rvo i r, with eve ryday activ-ities related to fishing. The environment has been extensively modified by deforestation and f a rming and livestock activities. Near the Re s e r-voir there are dense stretches of shrubs with soil cove red by grassy plants.
Mosquito captures we re conducted bi-m o n t h l y, always beginning at sunset (18:00h to 21:00h). Previous studies and random sam-pling around the re s e rvoir showed that sunset and early evening hours we re the most favo r-able periods for presence of anophelines. Fro m October to Fe b ru a ry, during daylight savings t i m e, captures we re conducted between 19:00 and 22:00h.
Mosquitoes we re simultaneously collected using human bait and Shannon light tra p s, with 100-candle gas lamps. Two members of the re s e a rch team collected anophelines that
landed on the Shannon traps or on themselve s with a mouth aspira t o r. The Shannon trap was located 150m from the human-bait capture s.
Ca p t u red anophelines we re killed with c h l o-ro f o rm and placed in small boxes containing p a ra f o rm a l d e h yd e. The specimens we re tra n s-p o rted to the labora t o ry and mounted on s- pa-per triangles and labeled with a number and re f e rence data.
All specimens we re added to the collection of the Entomology De p a rtment of the Os w a l d o Cruz In s t i t u t e, Fi o c ruz, under the name “Se r ra da Mesa Co l l e c t i o n”. Anopheles albitarsiss p e c i-mens we re considered sensu lato.
The relationship between the flooding s t a g e of the re s e rvoir and presence of anophelines was determined by the Williams mean test ( Xw). The level of significance between the
fre-F i g u re 1
Location of the Serra da Mesa Hydroelectric Dam in Brazil and the State of Goiás, featuring anopheline collection sites 1, 2, 3, 4, and 5.
0
original scale 1:500,000
5 10 15 20 25km
Niquelândia
Barro Alto Uruaçu
Campinorte
Minaçu
Tocantins River
Tocantinzinho River
Bagagem River Maranhão River
4 3
5 2
1
BR-080 GO-237 GO-241 BR-153
quency of anophelines and diagnosed malari a cases was established using the linear corre l a-tion coefficient. Data on malaria cases aro u n d the re s e rvoir we re obtained from the Goiás of-fice of the Brazilian National Health Fo u n d a-tion (FUNASA).
R e s u l t s
From Ja n u a ry 1997 to November 1999, 5,205 anophelines we re collected at the five study ar-e a s. Fi var-e spar-eciar-es war-e rar-e collar-ectar-ed: Anopheles dar-l i n g i , An .a dar-l b i t a r s i s , An .t r i a n n u dar-l a t u s , An .o s w a dar- l-d o i, andAn .e va n s a e(Table 1).
T h roughout the thre e - year study peri o d , An .d a rl i n g iwas the most frequently capture d s p e c i e s, comprising > 50% of the specimens c a p t u red at each sampling site. Ove rall, An . d a rl i n g ire p resented 61.4% of all anophelines c a p t u red. Calculation of the mean fre q u e n c y c o n f i rmed the abundance of this anopheline t h roughout the area. An .a l b i t a r s i swas the sec-ond most common species in all the sampling s i t e s, with 35.4% of all the anophelines collect-ed. An.triannulatus, An.oswaldoi, andAn. e va n-s a ewe re captured much less fre q u e n t l y.
En v i ronmental va riations during the study resulted in va riations in the anopheline fauna d u ring filling of the re s e rvo i r. From 1997 to 1999 there was a drop in anopheline fre q u e n c y f rom Xw= 169.1 in 1997 to Xw= 115.2 in 1998 (a
d e c rease of 32%) and Xw= 20.8 in 1999 (a de-c rease of 82%), or a total redude-ction of 88% in the anopheline population (Fi g u re 3).
The gradual reduction was common to all f i ve species over time, that is, An . d a rl i n g iw a s always the most common, followed by An .a l-b i t a r s i s , An .t r i a n n u l a t u s , An .o s w a l d o i, andAn . e vansae ( Fi g u re 3). The pro p o rtions of the two most frequently captured species, An .d a rl i n g i and An .a l b i t a r s i s, remained more or less con-stant. In 1997 they re p resented 56% and 39% of all the anophelines, re s p e c t i ve l y, with an ave r-age frequency of Xw= 95.4 and Xw= 66.4. T h e y re p resented 60% and 38% of all the anophe-lines in 1998 and 64% and 30% in 1999.
The frequency curve of the anophelines showed two peaks during the filling of the re s e r-vo i r. The first peak occurred from July 1997 to Ma rch 1998, with means va rying from Xw= 64.0 to Xw= 155.0. The second occurred in Ma rc h 1999 (Xw= 61.4) (Fi g u re 3).
This pattern was observed for four of the s p e c i e s. The only exception was An . e va n s a e, which was not captured during the second peak. Small annual va riations occurred in the first larger population peak for the less com-monly collected species: An .t r i a n n u l a t u s , An . o s w a l d o i, and An .e va n s a e( Fi g u re 3).
Va riations in anopheline frequency are be-l i e ved to be directbe-ly rebe-lated to interventions in the environment around the Se r ra da Me s a Re s e rvo i r. Among the most important eve n t s
F i g u re 2
Te m p e r a t u re, relative humidity, and rainfall measurements and monthly averages, verified during sampling a round the Serra da Mesa Reservoir, State of Goiás, Brazil, from January 1997 to December 1999.
oC 22 23 24 25 26 27 28 29 30 31 32
40 % 45 50 55 60 65 70 75 80 85 90
relative humidity (%) temperature (oC)
nov sep jul may mar jan nov sep jul may mar jan nov sep jul may mar jan
1997 1998 1999
mm 0 50 100 150 200 250 300 350 400 450
we re the closing of the bypass tunnels and fill-ing of the re s e rvo i r.
In October 1996 the bypass tunnels we re closed, and in Ja n u a ry 1997 the re s e rvoir began to form. The re s e rvoir was filled continuously un-til 1997. From the closing of the bypass tunnels until the end of the rainy season, the water leve l i n c reased from 340m to 431m above sea leve l .
Va riation in precipitation between the months of maximum and minimum ra i n f a l l was consistent with the re g i o n’s climatic pro-f i l e. Howe ve r, the dry season was extre m e l y long, and even with the beginning of rains in November 1997, there was no significant in-c rease in the re s e rvo i r’s water level. Rainfall w a s a p p roximately half that observed in the pre v i-ous ye a r. Te m p e ra t u re and re l a t i ve humidity remained at the expected levels (Fi g u re 2).
Until Ma rch 1998, rainfall was less than pected, and the region suffered another ex-t remely dry period from May ex-to Se p ex-t e m b e r 1998. Resumption of the rainy season, fro m October 1998 to May 1999, once again fell short of the expected level. Ave rage tempera t u re and re l a t i ve humidity did not reach the levels of p revious ye a r s.
D i s c u s s i o n
Obtaining entomological information by mon-i t o rmon-ing populatmon-ions of dmon-isease vectors has p roven to be a vital measure of disease risk as-sessment. T h e re f o re, detailed studies of ve c t o r population bionomics are re l e vant for deve l o p-ing and implementp-ing control pro g ra m s.
It has been shown that enviro n m e n t a l changes may alter the frequency of malari a
1 , 2 , 3 , 4 , 5 , 6Such changes are particularly re l e va n t in regions altered by human intrusion, includ-ing dam construction, mininclud-ing, and ru ral
settle-ment projects that provide increased opport u-nities for anthropophilic vector populations and where the environment favors the latter, t h e re by increasing the epidemiological ri s k s.
7 , 8 , 9 , 1 0 , 1 1 , 1 2
Intense and extensive deforestation, part i a l o b s t ruction of ri vers and cre e k s, highway e a rt h-w o rk h-without proper dra i n a g e, accumulation of water, and the formation of large manmade lakes are examples of environmental changes that can result in increased vector density, fa-vo ring ve c t o r- b o rne endemics.
In the current study we observed anophe-line population changes over time in areas un-der the influence of the Se r ra da Mesa Re s e r-vo i r, from the beginning of the filling of the re s e rvoir until months after the initial hyd ro-e l ro-e c t ric plant opro-eration. Thro-e fivro-e sitro-es wro-e rro-e sro-e- se-lected to provide a re p re s e n t a t i ve sample of the region. Mo n i t o ring populations over time was essential to assess environmental effects.
An .d a rl i n g iis endophilic and anthrop o p h i l i c and is captured using human bait both inside and outside re s i d e n c e s. It is also the pri m a ry human malaria vector species in much of Brazil, and even transmits malaria when the s p e c i e s’ density is low.2 , 5 , 1 3 , 1 4
The second most frequent species in our s u rve y, An . albitarsis sensu lato, also plays an i m p o rtant role in malaria epidemiology in Brazil. That is, although it is normally pre s e n t as a secondary ve c t o r, it may acquire gre a t e r significance where transmission by An .d a rl i n-g ia l ready occurs.1 3 , 1 5 , 1 6This species is an effi-cient colonizer of areas altered by human ac-t i v i ac-t y, and ac-the increase in iac-ts populaac-tion de-s e rvede-s attention due to itde-s vector efficiency.
1 2 , 1 7 , 1 8 , 1 9 , 2 0Wilkerson et al.2 1distinguished four genetically differentiated species from An . a
l-bitarsis sensu lato using random amplified
polymorphic DNA polymerase chain re a c t i o n
Table 1
Number (n), percentage (%), and Williams means (Xw) of anophelines captured by sampling site, Serra da Mesa Reservoir,
State of Goiás, Brazil, January 1997 to December 1999.
S p e c i e s Site 1 Site 2 Site 3 Site 4 Site 5 To t a l
n % X w n % X w n % X w n % X w n % X w n % X w
Anopheles darlingi 6 5 8 6 4 . 2 6 . 6 8 8 7 3 . 9 1 . 8 8 4 7 6 4 . 8 1 1 . 7 5 5 1 7 2 . 5 1 0 . 4 1 , 0 5 3 5 2 . 8 1 5 . 4 3 , 1 9 7 6 1 . 4 4 6 . 9
An. albitarsis s.l. 3 5 6 3 4 . 7 4 . 3 1 9 1 6 . 0 0 . 6 4 3 5 3 3 . 3 6 . 6 1 9 1 2 5 . 1 3 . 6 8 4 4 4 2 . 3 1 4 . 9 1 , 8 4 5 3 5 . 4 2 8 . 0
An. triannulatus 9 0 . 9 0 . 3 1 0 8 . 4 0 . 4 2 3 1 . 8 0 . 6 9 1 . 2 0 . 3 7 8 3 . 9 2 . 0 1 2 9 2 . 5 2 . 6
An. oswaldoi 2 0 . 2 0 . 1 2 1 . 7 0 . 1 3 0 . 2 0 . 1 5 0 . 7 0 . 2 1 1 0 . 6 0 . 4 2 3 0 . 4 0 . 6
An. evansae 0 0 . 0 0 . 0 0 0 . 0 0 . 0 0 0 . 0 0 . 0 4 0 . 5 0 . 1 7 0 . 4 0 . 2 1 1 0 . 2 0 . 3
F i g u re 3
Incidence of anopheline species and malaria cases according to calculation of Williams means (Xw)
a round the Serra da Mesa Reservoir, State of Goiás, Brazil, from January 1997 to December 1999.
( c o n t i n u e s )
Xw 0 40 80 120 160
0 malaria cases 10 20 30 40 50 60
malaria cases populational curve
nov sep jul may
1999 mar jan nov sep jul may
1998 total
mar jan nov sep jul may
1997 mar jan
Xw 0 20 40 60 80 100
0 malaria cases 10 20 30 40 50 60
malaria cases populational curve
nov sep jul may
1999 mar jan nov sep jul may
1998 mar jan nov sep jul may
1997 mar jan
F i g u re 3 (continued)
Incidence of anopheline species and malaria cases according to calculation of Williams means (Xw)
a round the Serra da Mesa Reservoir, State of Goiás, Brazil, from January 1997 to December 1999.
( c o n t i n u e s )
Xw 0 10 20 30 40 50
0 malaria cases 10 20 30 40 50 60
malaria cases populational curve
nov sep jul may
1999 mar jan nov sep jul may
1998 mar jan nov sep jul may
1997 mar jan
An. albitarsis
Xw 0 1 2 3 4 5
0 malaria cases 10 20 30 40 50 60
malaria cases populational curve
nov sep jul may
1999 mar jan nov sep jul may
1998 mar jan nov sep jul may
1997 mar jan
F i g u re 3 (continued)
Incidence of anopheline species and malaria cases according to calculation of Williams means (Xw)
a round the Serra da Mesa Reservoir, State of Goiás, Brazil, from January 1997 to December 1999.
Xw 0.0 0.5 1.0 1.5
0 malaria cases 10 20 30 40 50 60
malaria cases populational curve
nov sep jul may
1999 mar jan nov sep jul may
1998 mar jan nov sep jul may
1997 mar jan
An. oswaldoi
Xw 0.0 0.2 0.4 0.6
0 malaria cases 10 20 30 40 50 60
malaria cases populational curve
nov sep jul may
1999 mar jan nov sep jul may
1998 mar jan nov sep jul may
1997 mar jan
(RAPD-PCR). Wilkerson et al. 2 2h y p o t h e s i ze d the species as An . albitarsis sensu stricto, An . marajoara,An.deaneorum, and another s p e c i e s not described. An .m a ra j o a ra and An .d e a n e o-rum we re responsible for a malaria outbreak in Costa Ma rq u e s, Rondônia St a t e, as was An .m a-ra j o a a-rain Ig u a p e, São Paulo St a t e, and Ma ra j ó Island, Pará St a t e.2 2Conn et al.2 3o b s e rved a significant pro p o rtion of An . m a ra j o a rai n f e c t-ed with malaria parasites using ELISA and in-c riminated the spein-cies as a pri m a ry vein-ctor in sites near the city of Macapá, Amapá St a t e. Other authors have implicated species fro m the An . a l b i t a r s i s complex as the pri n c i p a l m a l a ria vector in certain locations, such as the Vale do Ribeira region in the State of São Pa u l o
2 0, around the Itaipu Hyd ro e l e c t ric Dam in the state of Pa raná 6, and in urban areas of Bo a Vista in the State of Ro raima 2 4. Although they consider An . albitarsis s.l. zoophilic 2 5, Lou-re n ç o - d e - Ol i ve i ra et al. 2, Fo rattini et al. 2 0, and Guimarães et al. 6re p o rt the species’ intense a n t h ropophilic behavior, biting humans inside and outside re s i d e n c e s, especially in the ab-sence of large animals (like cattle) in the sur-rounding area.
An . t r i a n n u l a t u s , An . o s w a l d o i, and An . e vansae we re captured much less fre q u e n t l y and are typically zoophilic and exo p h i l i c. An . triannulatus a n dAn . o s w a l d o ih a ve been im-plicated in the transmission of human malari a
2 6. Howe ve r, Klein 2 7 , 2 8d e m o n s t rated that An . t r i a n n u l a t u s in Costa Ma rq u e s, Ro n d o n i a St a t e, was a highly inefficient vector for both P. falciparum a n dP. v i va x. Specimens of An .o s-w a l d o iwe re even re p o rted to infrequently have s p o rozoites in the saliva ry glands, although they presented oocysts. Since naturally infect-ed specimens have been found, some authors i n c riminated the species as a secondary ve c t o r in certain locations 1 7 , 1 8 , 2 5 , 2 9. The low numbers of An .e va n s a ec a p t u red and lack of re p o rts c o n-c e rning its ven-ctor an-ctivity make this spen-cies’ in-vo l vement in malaria transmission ra re.
Anopheline population dynamics are di-rectly related to the availability of larval habi-tats for immature development. Some authors o b s e rved an association with increased ra i n f a l l that provides greater opportunity for accumu-lation of small bodies of water 8 , 3 0 , 3 1 , 3 2. Howe v-e r, Guimarãv-es v-et al. 6noted that in areas under the influence of the re s e rvo i r, anopheline pop-ulation dynamics are not directly influenced by rainfall, but by the level of the re s e rvoir which, while stable, offers a constant opportunity for female anophelines to lay their eggs.
In this study we observed the re l a t i o n s h i p b e t ween va riation in anopheline populations
and the water level of the re s e rvo i r. Climatic factors had a secondary influence, genera t i n g va riations in the conditions around the re s e r-voir and along the banks of tri b u t a ri e s. T h i s p rocess invo l ved three different stages.
Despite optimum tempera t u re conditions, re l a t i ve humidity, and heavy rainfall from Ja n-u a ry to Ap ril 1997 (Fi g n-u re 2), deforestation n-up to 10 meters above the expected level along the banks of the re s e rvoir and tri b u t a ries was a key factor for the absence of anophelines (Fi g u re 3). Erosion, muddy water, and direct exposure of breeding sites to sunlight we re unfavo ra b l e to anopheline species in the area, especially An .d a rl i n g i( Fi g u re 4).
With the gradual filling of the re s e rvoir and re f o restation along the banks beginning in Ma y 1997, a second stage began, with less fluctua-tion in the water levels and an immediate in-c rease in anophelines in-captured.
The third stage, beginning in July 1998, was c h a ra c t e ri zed by a continuous drop in the wa-ter level (Fi g u re 4) and a reduction in the oc-c u r renoc-ce of anophelines. In i t i a l l y, this oc-could be explained by the beginning of the opera t i o n stage of the Se r ra da Mesa Hyd ro e l e c t ric Pl a n t d u ring the dry season. Howe ve r, in July 1998 what would become one of the longest d ro u g h t s in history in the area hit nearly the entire coun-t ry for coun-the nexcoun-t coun-three ye a r s. From coun-the begin-ning, hyd ro e l e c t ric plants in va rious other ar-eas of the country we re threatened by the lack of water in their re s e rvo i r s, and the Se r ra da Mesa Plant was forced to work at higher capac-ity to compensate for the national power d e f i c i t . The rainy period that followed was short e r than expected, failed to produce more water than was released, and lasted until the end of our study.
The impact of the increased re s e rvoir leve l on the anopheline population was not the s a m e as observed during the drop in the water leve l . From the moment the water level reached the s u r rounding vegetation at a slowly incre a s i n g p a c e, conditions favo red the development of immature anopheline forms. On the other h a n d , when the water receded the banks we re soon exposed to sunlight and erosion and became less suitable for the development of immature f o rms (Fi g u re 4). The consequences of these conditions for the anopheline population we re i m m e d i a t e, and the data show a large decre a s e in adult specimens captured, concomitant w i t h reduced water levels in the re s e rvoir in Ju l y 1998 (Fi g u re 3).
F i g u re 4
Serra da Mesa Dam, State of Goiás, Brazil.
F i g u re 4a
Panoramic view of the Serra da Mesa Reservoir, State of Goiás, Brazil.
F i g u re 4b
Focus on decreased water level and direct exposure to sunlight on the banks of the re s e r v o i r.
S M D
Although the numbers did not reach the nor-mal values for the same period in pre v i o u s ye a r s, they we re sufficient to reduce the speed at which the water level decreased. Besides sta-bilizing the re s e rvoir for seve ral months, the rains resulted in increased vegetation, a typical c e r ra d ob e h a v i o r, and increased the potentially suitable larval habitats with a concurrent in-c rease in the number of anophelines in-capture d up to May 1999 (Fi g u re 3). In May 1999 the drought continued, resulting in decreased re s e r-voir leve l s. Few anophelines we re capture d d u ring this peri o d .
Ac c o rding to Fo rattini et al. 8and Gu i m a-rães et al. 3 2, the alternation between Cu l i c i d a e population peaks and sudden decreases are o p p o rtunistic reactions to favo rable enviro n-mental situations; when the latter end, the anopheline populations re t u rn to their norm a l l e vel. This phenomenon was observed part i a l l y in the area around the Se r ra da Mesa Re s e rvo i r. The present study focused pri m a rily on en-tomological factors and ecological aspects af-fecting anopheline populations in an enviro n-ment altered by human activity. Howe ve r, in the epidemiology of malaria, the effects of man ecology are essential, and the flow of hu-mans in the Brazilian countryside has always been identified as a modulating factor in the d i s t ribution and frequency of the disease 7 , 9 , 2 5 , 3 3.
Co n s t ruction of highways, hyd ro e l e c t ric p l a n t s, and farming and mining opera t i o n s, including the best planned ones, always generate a disor-g a n i zed midisor-gration of people that makes sanita-tion and disease control ve ry difficult. Ac c o rd-ing to Guimarães et al. 6, construction of the Itaipu Hyd ro e l e c t ric Dam in the State of Pa ra n a resulted in an increase in anopheline popula-tions and the re t u rn of migrant workers who had failed to settle in the No rt h e rn re g i o n , many of whom we re infected with malaria, re-sulting in a serious epidemic, with nearly 3,000 cases of malaria in areas where the disease had a l ready been eliminated some 30 years before.
detachment that hinder epidemiologic contro l m e a s u re s. Many of these individuals are al-ready infected with malaria when they arri ve, having originated from or passed through re-gions where the disease is endemic 1 , 3 , 6 , 9 , 1 4 , 3 3.
The arri val of gold prospectors and all the risk components mentioned above became ev-ident in the area around the Se r ra da Me s a Re s e rvoir beginning in July 1997. As discussed, d u ring this same period we observed an
in-c rease in the anopheline population, espein-cially An .d a rl i n g i, in all the sites studied. T h e re ap-pears to be a direct relationship between this m i g ra t o ry flow, the advent of diagnosed malar-ia cases, and the increased frequency of An . d a rl i n g i(and perhaps also of An . a l b i t a r s i s) ( Fi g u re 3). The important relationship betwe e n these factors is indicated by the linear corre l a-tion indices obtained: An .d a rl i n g i= 0.606 and An .a l b i t a r s i s= 0.601 (r0 , 1 ( 2 ) , 9= 0.521).
A c k n o w l e d g e m e n t s
This work was accomplished with the help of Fu rn a s Ce n t rais El é t ricas S.A. The authors wish to thank the En v i ronmental De p a rtment of Fu rnas Ce n t rais El é t ri-cas S.A., re p resented by Dr. No rma Pinto Vilela, for p roviding logistic support during the fieldwork. We also thank our colleagues Ari ovaldo Gomes Co e l h o, Chisto So a res da Si l va, and Dion Kenede Vi e i ra for their collaboration in the field activities.
C o n t r i b u t o r s
A. E. Guimarães collaborated in the field work, s p e c i e s identification, statistical analysis, and drafting of the a rticle C. Gentile participated in the field work and statistical analysis. J. Alencar and C. M. Lopes part i c i-pated in the field activities and species identification. R. P. Melo participated in the field work .
R e s u m o
Fo ram estudados aspectos da ecologia de anofelinos ( Di p t e ra , Culicidae) em áreas da Usina Hi d relétrica de Se r ra da Me s a , Estado de Go i á s , Bra s i l . Fo ram analisa-dos a incidência das populações de anofelinos e os fa-t o res climáfa-ticos. Fo ram realizadas capfa-turas bimesfa-t ra i s , em isca humana e armadilha Sh a n n o n , ao longo de 36 meses consecutivos (janeiro de 1997 a deze m b ro de 1 9 9 9 ) . Ca p t u ramos um total de 5.205 anofelinos adul-t o s ,p e radul-tencenadul-tes a cinco espécies.Anopheles darlingi
foi o anofelino mais freqüente (61,4%), seguido de A n . albitarsis s. l. ( 3 5 , 4 % ) ,An. triannulatus ( 2 , 5 % ) ,An. os-waldoi (0,4%) eAn. evansae ( 0 , 2 % ) . O nível da água e a vegetação às margens do re s e rvatório foram deter-minantes para a freqüência das espécies de anofelinos. Os fatores climáticos tive ram influência secundária. A estabilidade do re s e rva t ó r i o, o aumento na fre q ü ê n c i a d oAn. darlingi e a chegada de garimpeiros foram re s-p o n s á veis s-pelos casos de malária diagnosticados.
Ma l á r i a ; Ecololgia de Ve t o re s ;E c o l o g i a
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Submitted on 11/Ma r / 2 0 0 3
