A SURVEY OF THE Anopheles MOSQUITOES (DIPTERA: CULICIDAE) ALONG THE ACRE AND PURUS RIVERS, AMAZON BASIN,

Robert H. ZIMMERMAN1, Francisco Xavier PAULINO2, Mercia de ARRUDA3

ABSTRACT — From January 19 to February 25, 1997 an entomological survey of the seringais and larger towns along the Acre and Purus rivers was made as part of the project “Revisitando a Amazônia de Carlos Chagas; da Borracha a Biodiversidad”. Eleven anopheline species and 1285 specimens were collected landing on human baits. The four most abundant species were Anopheles albitarsis s.l. (n=778), A. darlingi (n=359), A. rangeli (n=69) and A. oswaldoi (n=60). A total of 252 larvae were collected of which 10 anopheline species were identified. The most abundant species collected were A. albitarsis s.l. (n=88), A. deaneorum (n=45) and A. triannulatus (n=40). The low numbers of Anopheles collected and the absence of the principal malaria vector A. darlingi at the seringais sites suggests that they arc not high risk malarious areas. Other Diptera collected were Culex sp., Mansonia titillans, Mansonia pseudotitillans, Psorophora ciliata, Psorophora sp., Coquillettidia (Rhynchotaenia) sp., Simulium amazonicum and S. sanguineum.

Keywords: Anopheles, Malaria, Amazon Levantamento dos Mosquitos Anopheles (Diptera: Culiicidae) ao Longo dos Rios Acre e Purus, na Bacia Amazônica, Brasil. RESUMO — Entre os meses de Janeiro/Fevereiro de 1997, foi realizado um levantamento entomológico nos seringais c comunidades localizadas no vale do rios Acre e Purus, como parte do projeto “Revisitando a Amazônia de Carlos Chagas; da Borracha a Biodiversidade”. Foram capturados no processo de pouso, um total de 1.285 anofelinos pertencentes a 11 espécies. As quatro espécies encontradas em maior número foram: Anopheles albitarsis s.l. (n=778). A. darlingi (n=359) A. rangeli (n=69) e A. oswaldoi (n=60). Também foram coletadas um total de 252 larvas pertencentes a 10 espécies de anofelinos. As espécies mais abundantes foram: A. albitarsis (n=88), A. deaneorum (n=45) e A. triannulalus (n=40). O número reduzido de anofelinos coletados e a ausência do A. darlingi nos seringais sugere que essa região não é de alta endemicidade para malária. Outros mosquitos do gênero Diptera coletados foram: Culex sp., Mansonia titillans, Mansonia pseudotitillans, Psorophora ciliata, Psorophora sp., Coquillettidia (Rhynchotaenia) sp., Simulium amazonicum e S. sanguineum.

Palavras chaves: Anopheles, Malária, Amazonas INTRODUCTION nities. One of the most prevalent dis• eases that he found was malaria. At the In 1911 Carlos Chagas visited the same time, he collected several species of seringais (rubber production communi• mosquitoes including the suspected malaria ties) along the Acre and Purus rivers in vector Cellia albipes (= A. (Nys.) western Amazon (Fig. l)(Cruz, 1913). albimanus). Since that time very little The intent of the journey was to survey information has been collected from the the health situation in the local commu- riverine communities in the Purus River

1 Pan American Health Organization, Pan American Sanitary Bureau, Regional Office of the World Health Organization, Caixa Postal 08729, 70912-970, Brasilia, DF, BRAZIL. 2 Laboratório de Entomologia, Fundação Nacional de Saúde, Coordenação Regional do Acre, Rio Branco AC, BRAZIL. 3 Departmento de Imunologia, Instituto de Pesquisas Aggeu Magalhães, FIOCRUZ, Av. Moraes Rego S/N Campus de UFPE, 50670-420, Recife PE, BRAZIL. Purus River Basin •Beruri 355000 square kilometers 33.34

31 30 «Tapauá

PXapuri

Figure 1 . Sites of collection along the rivers Acre and Purus (Purus River Basin). See Tables 1 and 2 for site descriptions.

Basin (Deane et al., 1948; Roberts et Tributaries of the Acre and Purus riversar e al, 1987; Natal et al, 1992; Barata et usually clearwater streams and rivers al, 1993; Fundação Nacional de (igarapés). Throughout the basin there Saúde, unpublished data). are many lakes and flooded igapós From January 19 to February 25, (black and clearwater floodplains) and 1997, the project "Revisitando a várzeas ( muddy inundations) (Pires & Amazônia de Carlos Chagas; da Prance 1985). The ochre to brownish Borracha a Biodiversidade" conducted soils are of fluvial origin. Along the a survey of the seringais visited by main channel the shoreline varies from Carlos Chagas along the Acre and Purus vertical cliffs, stable sloping shoreline rivers. This article presents the results (45°) to beaches. Most towns and rub• of the survey of the anopheline fauna. ber communities visited are situated on cliffs overlooking the river or on slop• MATERIALS AND METHODS ing shorelines. Beach areas were used The rivers of the Purus River Ba• primarily for subsistence agriculture. sin meander from the foothills of the The survey began in the municipal• Andes in Peru to the Solimões river 100 ity of Xapuri (10° 39'S, 68° 30'W), Acre km west of , Brazil (Fig. 1). State and ended in the municipality of They are turbid, Whitewater rivers. Beruri, Amazonas State (03° 53'S, 61°

166 Zimmerman et al. 22'W). The latitude and longitude of (Tab. 2). Not all breeding sites in each each collection site was recorded using location were positive. Ten different a GarminR geographical positioning anopheline species were collected dur• system (GPS) recorder. ing the survey and a total of 252 larvae Adult mosquitoes were collected were identified. The most abundant landing on human baits from 18:00- species collected were A. albitarsis s.l. 21:00 h. Mosquitoes were put into (n=88), A. deaneorum (n=45) and A. small holding cartons and kept dry for triannulalus (n=40). Only one A. future identification. Larval surveys darlingi larva was collected at Yapui on were conducted for a minimum of 2 Rio Ituxi, Lábrea. The main larval hours at each site by 2 persons; using breeding sites were river backwaters, standardized larval dippers (500ml). streams, and artificial ponds. Várzeas Larval collections were made at all and igapós were consistently negative potential breeding sites that were ac• for Anopheles larvae. cessible in and around the seringais Along with the anophelines, we and the larger towns. Mosquitoes were collected several other genera of mos• identified using the keys of Faran quitoes. Culex sp. was almost always (1980) and Consoli & Lourenço de collected during human biting counts. Oliveira (1994). When one entered the forest in search A collection of other Culicidae of larval breeding sites large numbers and Simullidae, was made at various of Mansonia titillans, Mansonia seringais. pseudotitillans, Psorophora ciliata, Psorophora sp., and/or Coquillettidia RESULTS (Rhynchotaenia) sp. were found bit• The results of the survey are sum• ing. Simulium amazonicum and S. marized in Tables 1 and 2. Of the 18 sanguineum were the daytime biting adult collections made, 13 were positive Simuliidae collected during the survey. for Anopheles. Overall, 11 different DISCUSSION Anopheles species and 1285 specimens were collected landing in humans. The It is difficult to compare the results four most abundant species were of this survey with that of Carlos Chagas Anopheles albitarsis s.l. (n=778) A. because the anopheline species collected darlingi (n=359), A. rangeli (n=69) and by Chagas, Cellia albipes Theobald, is a A. oswaldoi (n=60). The presence and junior synonym of A. (Nys.) albimanus abundance of each species differed by whose name was erroneously applied to collection site (Tab. 1). The majority of other anophelines species of the subgenus the anophelines collected were from Nyssorhynchus (Faran, 1980). larger towns such as Lábrea and Boca The majority of adults and larvae do Acre. The seringais accounted for only were collected around the larger towns 14% of the total adults collected. (Tabs. 1 & 2). The seringais showed Larval collections were made in very low densities of anophelines. 21 localities of which 18 were positive This may have been due to the low

A Survey of the anopheles mosquitoes . 167 Table I. Adult Anopheles collected from the Acre and Purus rivers, Amazon Basin, Brazil, from January 19 to Febuary 22, 1997.

Municipality Locality Geographic A. A. A. A. A. trian• A. A. benar- A.brazil- A. A. matto- A. medio- Coordinates rangeli oswaldoi darlingi albitarsis s.l. nulalus rondoni rochi iensis minor grossensis punctalus

Xapuri Larangal1 (1)J 10° 39 S 0 0 0 0 0 0 0 0 0 0 0 68° 30 W Xapuri Sao Francisco 10° 31 S 0 0 1 1 0 0 0 0 0 0 0 de Iracema' (2) 68° 07 W Xapuri Paraíso' (3) 10*15*8 19 34 0 0 3 0 0 0 1 1 1 67°48'W Rio Branco Univ.Federal 0 2 0 0 0 0 0 0 0 0 0 Acre (5) Rio Branco Novo Horizonte' 09° 55 S 0 0 0 0 0 0 0 0 0 0 0 (6) 67° 37 W Rio Branco Bela Vista' (7) • • 0 0 0 0 0 0 0 0 0 0 0 Boca do Sao Francisco' 1 2 0 0 0 0 0 0 0 0 0 Acre (8) Rio Branco Riozinho do 10° 03'S 48 19 0 17 4 2 2 0 0 0 0 Rola' (9) 67° 51 W Boca do Bairro 08° 45 S 1 1 0 496 0 0 3 0 0 0 0 Acre Ma each era I (10) 67° 23 W Boca do Bairro - " 0 0 0 264 0 0 0 0 0 0 0 Acre Macacheral (11) Bairro Cozoma 07° 43 S 0 0 33 0 0 0 0 0 0 0 0 (14) 67°00'W Pauini Guajarrã' (15) 07° 41 S 0 0 0 0 0 0 0 0 0 0 0 06° 53 W Pauini Sta. Candida' 07° 42 S 0 0 0 0 0 0 0 0 0 0 0 (16) 65" 41 W Lábrea Lábrea (21) 07° 15 S 0 0 260 0 0 0 0 2 0 0 0 64° 48 W Camutama Bairro Tanque 06° 32 S 0 0 29 0 0 0 0 0 0 0 0 (25) 64° 23 W Lábrea Camahá' (26) 06°42'S 0 0 29 0 0 0 0 0 0 0 0 N 64" 20 W 3 Tapauá Boca do 05° 45 S 0 0 0 0 0 0 0 0 0 0 0 3 Tapauá (28) 64° 23 W CD Tapauá Bairro Fernando 05° 37 S 0 2 7 0 0 0 0 0 0 0 0 3 Mendes (30) 63° 11 W Z3 Total 69 60 359 778 7 2 5 2 1 1 1 CD «-* ' Seringais; all other localities are villages along the rivers. 2 () Locality number from Figure 1. Table 2. Larval Anopheles collected from the Acre and Purus rivers, Amazon Basin. Brazil, from January 19 to Febuary 22, 1997'.

Municipality Locality Geographic A. nunez- A. A. A. A. albi• A. trian• A. A. brazil- A. deane- A. per- Coordinates tovari rangeli oswaldoi darlingi tarsis s.l. nulalus shanoni iensis orum yassui

Xapuri Larangal2 (1) 10° 39'S 0 0 0 0 2 6 0 0 0 0 68» 30 W Xapuri Sao Fransisco 10° 31 S 0 0 0 0 0 13 0 0 0 0 de Iracema2 (2) 68° 07 W Xapuri Itú2 (4) — 0 0 0 0 8 0 0 0 0 0 Bairro Praia 08° 45 S do Gado (12) 67° 23 W 0 1 0 0 53 0 0 0 31 0 Boca do Acre Rio Mapiá2 (13) — 1 2 0 0 2 0 0 0 8 0 Pauini Cidade Alta (17) 07° 43 S 0 0 0 0 4 0 0 0 0 0 67° 00 W Pauini Bairro Coza ma (18) 0 0 0 0 0 0 1 0 0 0 Pauini Cachoeira do 07° 40 S Hilário2 (19) 65° 59 "W 0 0 0 0 0 0 0 0 0 0 Pauini Santa Candida2 (20) 07° 42 S 0 0 0 0 0 0 0 0 0 0 65° 41 W Lábrea Marraâ2 (22) 07° 28 S 0 0 0 0 1 0 0 0 5 0 65° 18'W Lábrea Faz. Paiva (23) 07° 15'S 0 0 0 0 0 15 0 3 0 0 64°48'W Lábrea B.R. 230, Km 3 (24) " " 0 0 0 0 12 6 0 8 1 0 Lábrea Rio Ituxi, Yapui-' 07° 19 S 3 0 0 1 0 0 0 0 0 0 (27) 64° 55 W Lábrea Camahá2 (26) 06° 42 S 0 0 0 0 0 0 0 0 0 0 64 20 W Tapauá Boca de Tapauá (28) 05° 45 S 0 0 0 0 4 0 0 0 0 0 64°23'W Tapauá Vila Tapauá- 05° 42 S 0 0 0 0 0 0 0 0 0 2 (Floresta) (29) 64°24W Tapauá Bairro Açais (30) 05° 37 S 0 0 0 0 2 0 0 0 0 0 63° 11 TV Tapauá Tambaqui2 (31) 05° 11 S 0 0 0 0 0 0 0 0 0 2 62° 54 W Tapauá Aracari2 (32) 05° 11 S 0 0 15 0 0 0 0 0 0 0 62° 54 W Beruri Nova Trombeta2 04° 28 S 0 0 0 0 0 0 0 0 0 6 (33) 81° 22'W Beruri Boca do Assair (34) 03° 53 S 0 0 8 0 0 0 0 0 0 0 81° 22'W

TOTAL 4 3 23 1 88 40 1 11 45 10 ' Thirty Anopheles larvae could not be identified to species. 2 Seringais; all other localities are villages along the rivers. 3 () Locality number from Figure 1. number of positive breeding sites. It diference was that we could separate An. was somewhat surprising that the deaneorum from An. albitarsis s.l. and they flooded várzea and igapós were negative could not. In conclusion, we extend the because they have been considered im• distribution records for several species of portant anopheline breeding sites; par• anophelines, including the new species An. ticularly for A darlingi (Forattini, 1962). deaneorum, to include previously unsur- It may be due to the fact that the Acre veyed stretches of the Acre and Purus riv• and Purus rivers are muddy water riv• ers from the municipality of Xapuri, Acre ers and A. darlingi prefers clear water State, to Beruri, Amazonas State. (Deane et al, 1948). The presence of The low number of anophelines col• adult A. darlingi next to clear water lected at the seringais sites suggests that the igarapés in the towns of Lábrea and seringais along the Acre and Purus rivers and along the Mucuim river are not high-risk malarious areas. This is would support this conclusion. supported by the results of the malaria se• The four most abundant Anoph• rology survey conducted during this study eles collected in this study, A. albitarsis (Arruda, unpublished data). However, s.l., A. darlingi, A. rangeli and A. Deane et al. (1948) found seringais along oswaldoi, have been implicated in the Rio Zinho, Acre State to have high malaria transmission of malaria in the Amazon prevalence and large numbers of A. Basin (Arruda et al, 1986; Deane, 1986; darlingi. In contrast, our entomological Zimmerman, 1992; Branquinho et al, data suggest that the risk of malaria trans• 1993). A. albitarsis is a species complex mission in the communities along and next (Wilkerson et al, 1995) and only one to the igarapés is higher. Further research other member of this complex, A. is warranted to confirm this conclusion. deaneorum, can be separated by mor• phological characteristics (Rosa-Freitas, ACKNOWLEDGEMENTS 1989). In this survey we did not collect To Casa Oswaldo Cruz/ FIOCRUZ any adults of A. deaneorum (Tab. 2). for organizing the survey and partial The results of our survey comple• funding. To the Panamerican Health Or• ment previous studies on Anopheles from ganization, Pan American Sanitary Bu• Acre State (Deane et al., 1948; Natal et al., reau, Regional Office of the World 1992; Baratas al., 1993) and Amazonas Health Organization for partial funding. State (Deane et al., 1948; Xavier & Mattos, Fundação Nacional de Saúde, 1976; Roberts et al. 1987; Tadei et al., Coordenação Regional do Acre provided 1993; Osório Quintero etal, 1996; Baggio, logistic and entomological support. Drs. unpublished data). Deane et al. (1948) sur• G. Calderón and R. Galvão assisted with veyed several sites from Acre State to Para the identification of the Diptera. State. During their survey anophelines Literature cited were collected from Xapuri, Rio Branco, Boca do Acre, and Lábrea. The results of Arruda, M.; Carvalho, M.B.; Nusscnzweig, R.S.; our survey at these same sites were simi• Maracic, M.; Ferreira, A.W.; Cochrane, A.H. 1986. Potential vectors of malaria and lar to Deane et al. (1948). The major their different susceptibility to Plasmo-

170 Zimmerman et al. dittm falciparum and Plasmodium vivax in Osório Quintero, L.; Dutary Thatcher, B.; Tadei, P. northern Brazil identified by immunoassay. 1996. Biologia de anofelinos Amazônicos. Am. J. Prop. Med. Hyg., 35: 873-881. XXI. Ocorrência de espécies de Anopheles e outros culicideos na área de influência da Barata, J.M.S.; Natal, D; Lagos, C.B.T.; hidrelétrica de Balbina - cinco anos após o Urbinatti, P.R.; Rocha R.M. 1993. Fauna de enchimento do reservatório. Acta mosquitos (Diptera:Culicidae) da bacia do Amazônica, 26: 281-296. rio Purus (Acre, Brasil). Identificação de formas imaturas em área de projeto de Pires, J.M.; Prance, G.T. 1985. The vegetation colonização. Revta bras. Ent. 37: 365-368. types of the Brazilian Amazon, pp. 109B145. In: Prance, G.T; Lovejoy, T.E. Branquinho, M.S.; Taipe Lagos, C.B.T.; Rocha, (Eds). Key environments, Amazônia. R.M.; Natal, D.; Barata, J.M.; Cochrane, A.H.; Pergamon, New York. Nardin, E.; Nussenzweig, R.S.; Kloetzel, J.K. Roberts, D.R.; Alecrim, W.D.; Tavares, A.M.; 1993. Anophelines in the state of Acre, Bra• Radke, M.G. 1987. The house-frequent• zil, infected with Plasmodium falciparum, P. ing, host-seeking and resting behavior of vivax, the P. vivax variant P. vivax VK247 and Anopheles darlingi in southeastern P. malariae. Trans. R. Soc. Trop. Med. Hyg., Amazonas, Brazil. J. Amer. Mosq. Control 87: 391-394. Assoc., 3: 433-441. Consoli, R.A.G.B.; Lourcnço De Oliveira, R. Rosa-Freitas, M.G. 1989. Anopheles 1994. Principais mosquitos de (Nyssorhynchus) deaneorum; a new spe• importância sanitária no Brasil. Editora cies in the albitarsis complex (Diptera: Fiocruz, Rio de Janeiro, 225pp. Culicidae). Mem. Inst. Oswaldo Cruz, 84: Cruz, O. 1913. Relatório sobre as condições 535-43. medico-sanitárias do vale do Amazonas, Tadei, W.P.; Santos, J.M.M.; Scarpassa, V.M.; Typographia do Journal do Commercio, Rodrigues, LB. 1993. Incidência, distri• Rio de Janeiro. buição, c aspectos ecológicos de espécies de Anopheles (Diptera: Culicidae), em regiões Deane, L. M. 1986. Malaria vectors in Brazil. Mem. naturais e sob impacto ambiental da Inst. Oswaldo Cruz, 81 (suppl.3): 5-14. Amazônia Brasileira. In: Ferreira, E.J.G.; Deane, L.M.; Causey, R.; Deane, M.P. 1948. Santos, G.M.; Leão, E.L.M.; Oliveira, L.A. Notas sobre a distribuição e a biologia dos (Eds). Bases cientificas para estratégias de anofelinos das regiões nordestina e preservação e desenvolvimento da Amazônica do Brasil. Rev. Serv. Espec. Amazônia. Vol. 2. INPA, Manaus, AM.: Saúde PúbL, 1: 827-965. 167-196. Faran, M.E. 1980. Mosquito studies (Diptera, Cu- Wilkcrson, R.C.; Gaffigan, TV; Lima, J.B.1995. licidae). XXXIV. A revision of the Albimanus Identification of species related to Anoph• Section of the subgenus Nyssorhynchus of eles {Nyssorhynchus) albitarsis by random Anopheles. Contrib. Am. Entomol. Inst. (Ann amplified polymorphic DNA-polymerase Arbor) 15: 1-215. chain reaction (Diptera: Culicidae). Mem. Forattini, O.P. 1962. Entomologia Médica. I. Inst. Oswaldo Cruz, 90: 721-732. Parte Geral, Diptera, Anophelini. Fac. Xavier, S.H.; Mattos, S. 1976. Geographical Hig. Saúde Publ., São Paulo, 662pp. distribution of Culicinae in Brazil - IV. Natal, D.; Barata, J.M.S.; Lagos, C.B.T.; State of Amazonas (Diptera, Culicidae). Mosq. Syst., 8: 386-412. Rocha, R.M. 1992. Nota sobre culicideos (Diptera: Culicidae) da bacia do rio Purus, Zimmerman, R.H. 1992. Ecology of malaria vectors in the Americas and future direc• Acre Amazônia (Brasil). Rev. Saúde públ. tion. Mem. Inst. Oswaldo Cruz, 87, (suppl São Paulo, 26: 129-131. 3): 371-383.

Aceito para publicação em 26.08.98

A Survey of the anopheles mosquitoes .