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Bionomics of Anopheles aquasalis Curry 1932, in Guarai, State of Rio de Janeiro, Southeastern Brazil-I. Seasonal Distribution and Parity Rates
Carmen Flores-Mendoza^+, Ricardo Lourenco-de-Oliveira
Laboratorio de Transmissores de Hematozoarios, Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil
Code Number: OC96052
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From a total of 12,721 anophelines collected in a lowland area in Guarai, Rio de Janeiro, from November 1991 to October 1992, 99.7% (12,688) were Anopheles aquasalis. This species occurred throughout the year, but in higher numbers from April to September, when rainfall was low or moderate. The proportion of parous females in June was significantly higher than the annual rate. An. aquasalis was weakly attracted by a light-trap, and no significant differences in abundance were detected between nights with and without moonlight.
Key words: mosquito bionomics - Anopheles acquasalis - Clicidae - parity - Brazil
Anopheles (Nyssorhynchus) aquasalis Curry l932, is a coastal mosquito whose malaria vector status and behavior vary throughout its distribution in South America. Its occurrence is usually associated with the presence of brackish water which limits its distribution in Brazil to no more than 30 km from the coast. Exceptions were observed by Lucena (1946), Deane et al. (1948), Rachou et al.(1950) and Rachou (1958). An. aquasalis has been a primary vector of malaria in coastal Brazil (Deane 1986). Preferred sources of blood and frequency indoors of An. aquasalis vary geographically, and its vector status may depend on density. The species is sometimes considered zoophilic, exophilic and a secondary malaria vector, as in some areas of the Amazon and in southeastern Brazil. However, An. aquasalis has been considered anthropophilic and endophilic and a primary vector in some localities in northeastern Brazil (Boyd 1926, Galv o et al. 1942, Coutinho & Ricciardi 1943, Ramos 1943, Lucena 1946, Coutinho 1947, Deane et al. 1948, Rachou et al. 1950, Ferreira l964). This paper describes the local anopheline fauna and the monthly frequency of nulliparous and parous An. aquasalis females at Guarai, a locality in the "Baixada Fluminense", the coastal lowlands in Rio de Janeiro, southeastern Brazil. An. aquasalis has been regarded as one of the malaria vectors in "Baixada Fluminense" together with An. darlingi and An. albitarsis since early in the century (Boyd 1926, Root 1926). Guarai, was up to few years ago, considered as part of the municipality of Mage, one of the most malarious areas in "Baixada Fluminense" until the 1950's. The annual incidence of malaria in Mage decreased to non endemic levels in the following decade due to extensive drainage and indoor spraying of DDT put into practice since the 1940's (Deane 1988, Moraes 1990). Recently (1970-1995), An. aquasalis has been considered the only potential vector during minor malaria outbreaks reported in "Baixada Fluminense" (Santanna 1995, pers. comm.). In spite of the epidemiological importance of An. aquasalis in this area few observations have been carried out, on its bionomics except for descriptions of its resting-places and blood-meal sources (Flores-Mendoza & Deane 1993, Flores-Mendoza et al. 1996).
MATERIALS AND METHODS The study was carried out in Guarai, municipality of Guapimirim (until recently considered part of Mage), State of Rio de Janeiro, from November 1991 to December l992. The field work was performed on a dairy farm, named "Meia Noite" (22^o41'S and 42^o57'W), where the Guarai River crosses the road BR-493, between the villages of Mage and Itambi (Fig.1). The sedimentary terrain is flat and crossed by channels of brackish water and several rivers and streams that flow from a distant mountain chain (the "Serra dos Org os") to Guanabara Bay. The land is predominantly pasture with a few scattered trees and small patches of sugar cane and banana. There is frequently a breeze in Guarai due to its proximity to the seashore and lack of high vegetation. The terrain is frequently flooded during the rainy season and by tides. The few houses on "Meia Noite" farm are separated by large pastures, where the cattle browse during the day. At night, the cattle are confined to an open wooden stable where they stay from sunset to dawn. Monthly rainfall averages and monthly minima, maxima and averages of relative humidity and temperature were obtained from Mage (Fig. 1), the nearest meteorological station. Monthly tide variations in Guanabara Bay were provided by the local Brazilian Navy Office. Domiciliary station - Mosquito captures were performed inside and immediately outside of a house, which was nearly 500 m from the road BR-493, and 30 m from the Guarai River and surrounded by narrow drainage ditches. The house was built simply with adobe and was inhabited by the same family (four persons) throughout the study. Its living-room, two bedrooms, kitchen, bathroom and small veranda were lined with tiles but had no ceiling. Windows had neither curtains nor screens. The house was frequently visited by neighbors to watch television from 6:00 to 9:00 p.m. Extradomiciliary station - The cattle stable, 100 m from the domiciliary station, was selected for captures outside the house (Fig. 2). Types of collections - At the domiciliary station, collections were conducted with two human baits, one indoors and another immediately outside. Indoor collections included specimens resting on the walls. Extradomiciliary collections were performed on a single horse, on one human bait, and from the wooden surfaces of the stable (extradomiciliary station). The catches on human bait and on the horse were carried out twice a month, from 7:00 to 9:00 p.m. from November 1991 to December 1992. Mosquitoes were aspirated also twice a month from the walls of the house from 6:55 to 7:00 p.m., 7:55 to 8:00 p.m. and from 9:00 to 9:05 p.m., and on the walls of the stable from 9:05 to 9:15 p.m. Correlations between monthly abundance of An. aquasalis females in night catches and rainfall were analyzed by Spearman's rank-order coefficient (Siegel 1956). Adult mosquitoes were also collected resting in vegetation and by light trap. Potential natural resting places were searched in open fields outside 500 m of the domiciliary station. This search was conducted from 9:00 a.m. to 1:00 p.m. two or three times a month. Mosquitoes were collected with a manual aspirator, an aerial insect net (30 cm ring diameter), and a battery powered portable suction apparatus slightly modified from Natal and Marucci (1984). One light trap (Falc o 1981, slightly modified by Aguiar et al. 1985) was operated for 19 hr in May and 5 hr in June, 1992 at one edge of the stable, while human bait collections were being conducted at the domiciliary station. Mosquitoes were transported to the laboratory in cardboard cages and morphologically identified to species, using taxonomic keys (Forattini 1962). The ovaries of approximately 10% of females caught in each month were dissected to estimate parity by the tracheolar skein- ing method of Detinova (1962). Only females whose ovaries were in stages I or II of Christophers (1911) were considered for parity determinations. The number of dissected females varied monthly according with the density. Chi-squared tests were used to compare the monthly frequency of parous An. aquasalis females with the mean annual frequency. Additionally, the influence of moonlight on the abundance of An. aquasalis was evaluated by comparing night collections during full and new moons performed in February, March, May, August and October. The two-tailed sign test (Siegel 1956) was used for data analysis.
RESULTS The mean monthly relative humidity in Guarai ranged from 85.8% in October to 91.8% in April (Fig. 3a). Most rain fell in Guarai between September and January, although a small peak in rainfall was recorded in July (Fig. 3b). The rainiest month was January (124.0mm^3) and the driest were May (18.0mm^3) and June (2.0mm^3). The temperature ranged from a minimum of 9^oC in August to a maximum of 30.5^oC in December, and the monthly average ranged from 15.2^oC in October to 22.6^oC in December. The tide (Fig. 3b) ranged from 0-18 cm minimum to 133-155 cm maximum; the average in the last five years was around 75 cm. Anopheline fauna - Only three anopheline species were collected. The predominant species was An. aquasalis with 12,688 specimens (99.74%), followed by An. albitarsis (0.04%), and An. darlingi (0.02%) (Table I). Seasonal distribution (Table II) - An. aquasalis was collected throughout the year, but in higher numbers from April through August. Its abundance diminished after September, coinciding with an increase in rainfall (Fig. 3b). No significant correlation between rainfall and mean An. aquasalis density was detected (r^s = -0.3379, P > 0.05 - d.f. = 10), although the species was clearly more common during dry and moderately rainy periods and less abundant during the hot and rainy summer. The parous rate of An. aquasalis in June (Table III) was significantly higher than the annual rate (chi-squared = 91.29, P < 0.05). Other months were not significantly different from the annual rate (P > 0.05), except April when the proportion of nulliparous was significantly high (chi-squared = 4.344, P < 0.05) The hourly averages of An. aquasalis females were of 34.46 +/- 37.48 (SD) and 30.32 +/- 28.45 (SD) during new and full moons respectively. There was no significant difference between the hourly abundances with and without moonlight (P = 0.376). Only 56 An. aquasalis females and one male and two An. albitarsis males were collected in 24 hr of light trap operation in May and June 1992. DISCUSSION The two main seasons in southeastern Brazil are the hot and rainy summer occurring from September to January, and the dry fall and winter from February to September, when the lowest temperatures are usually recorded. In Guarai, An. aquasalis was more abundant after the rainy season or during the moderately rainy period. Heavy rainfall may flush breeding sites, strand larvae and pupae, cause egg mortality and therefor, reduce the abundance of adults. By contrast, moderate rains sustain the breeding places and facilitate their connections to tidal waters. During the dry months of May, June and August, the tides still cause the Guarai River to overflow, and surrounding breeding sites were maintained by brackish water. Similar results were obtained by Galv o et al. (1942) studying a population of An. aquasalis from Para in Amazonian Brazil, where this mosquito was more abundant between April and June when rainfall was moderate. Berti et al. (1993) found that An. aquasalis adults were not abundant in Guayana, Sucre State, Venezuela, during the heaviest rains. The opposite was observed by Senior-White (1952) in Trinidad, by Silvain and Pajot (1981) in Suriname, by Berti et al. (1993) in Santa Fe, Sucre State, Venezuela, by Lucena (1950) and Lourenco-de-Oliveira (1984), respectively, in northeastern and southeastern Brazil, where the abundance of An. aquasalis was highest in the rainy season. The parous rate of An. aquasalis was relatively high in Guarai, 46.8%, compared with the results of Panday (1973) in Suriname, where the parity rate of An. aquasalis was 46% at the end of July and beginning of August, but only 11% during the rest of the year. Berti et al. (1993) observed great differences in the incidence of parity of An. aquasalis in Santa Fe (82.5%) compared to nearly Guayana (37.4%), Venezuela. The low yield of An. aquasalis in light-traps indicates that this anopheline is little attracted to this collection device. No significant differences in abundance of An. aquasalis were detected between full and new moons in Guarai, although, Senior-White (1951) reported that An. aquasalis activity was greater in the first 2 hr after sunset on moonlit than on moonless nights. On the other hand, Lourenco-de-Oliveira (1984) reported an average of 2.9 An. aquasalis per 10 hr of captures during nights with new moon, while collections at other moon phases were less abundant (1.6, crescent; 1.4 full and 1.0, waning). Collections of An. nuneztovari, a species beloging to the same Albimanus Section of Nyssorhynchus as An. aquasalis, were 1.86 times larger during moonlit nights in Venezuela than during those with no moon (Rubio-Palis 1992). Ribbands (1945) noted that An. funestus entered houses and took blood more often during moonlit nights. The abundance of An. aquasalis with respect to moon phases as well as the variable parous rates need to be better evaluated throughout its territory with controls for variables, such as local landscape (vegetation, orography, availability of suitable resting-places), humidity and wind, generally disregarded by the authors. Our results show that An. aquasalis is the most abundant anopheline and the only potential malaria carrier in Guarai. It is also the commonest potential vector in other coastal low- lands adjacent to Guanabara Bay where malaria outbreaks have been reported and An. albitarsis and An. darlingi have become increasingly rare in the past several decades (Santanna & Lourenco-de-Oliveira, pers. comm.). The risk of malaria outbreaks in "Baixada Fluminense", with the immigration of infected people from endemic areas of the Amazon, seems to be greater during the dry and moderate rainy seasons when An. aquasalis is more abundant especially in June when a high parity rate indicated extended survivourship. ACKNOWLEDGEMENTS To Monique Motta, Marcia Castro and Mariangela Ziccardi for their help in field collections of An. aquasalis. To Tereza Fernandes da Silva, Genilton Vieira and Roberto Oscar for help with the illustrations. To LP Lounibos, MG Freitas-Sibajev, Marise Soares and Pedro Cabello for suggestions in the manuscript and help with statistical analysis. To Fundac o Superin-tendencia Estadual de Rios e Lagoas and Diretoria de Hidrografia e Navegac o (Brazilian Navy), respectively, for temperature, humidity, rainfall and tidal data. REFERENCES Aguiar GM, Schuback PA, Vilela ML, Azevedo ACR 1985. Aspectos da ecologia dos flebotomos do Parque Nacional da Serra dos rg os, Rio de Janeiro. IV. Frequencia mensal em armadilhas luminosas (Diptera, Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz 80: 465-482. Berti J, Zimmerman R, Amarista J 1993. Adult abundance, biting behavior and parity of Anopheles aquasalis, Curry 1932 in two malarious areas of Sucre State Venezuela. Mem Inst Oswaldo Cruz 88: 363-369. Boyd MF 1926. Studies of the epidemiology of malaria in the coastal lowlands of Brazil, made before and after execution of control measures. Am J Hyg Monographic series 5, 216 pp. Christophers RS 1911. The development of the egg follicle in anophelines. Paludism 2: 73-88. Coutinho JO 1947. Contribuic o para o estudo da distribuic o geografica dos anofelinos do Brasil. MSc thesis. Fac. Med. Univ. S o Paulo, S o Paulo, 117pp. Coutinho JO, Ricciardi I 1943. Transmiss o da malaria pelo An. tarsimaculatus Goeldi, 1905 em Bocaina no Litoral de S o Paulo Brasil. Arq Hig Rio de Janeiro 13: 27-32. Deane LM 1986. Malaria vectors in Brazil. Mem Inst Oswaldo Cruz 81(Suppl. II): 5-14. Deane LM 1988. Malaria studies and control in Brazil. Am J Trop Med Hyg 38: 223-230. Deane LM, Causey OR, Deane MP 1948. Notas sobre a distribuic o e a biologia dos anofelinos das Regi es Nordestina e Amaz“nica do Brasil. Rev Serv Esp Saude Publica 1: 827-965. Detinova TS 1962. Age-grouping methods in Diptera of medical importance. WHO Monogr Ser 47. Falc o AR 1981. Um novo modelo de armadilha luminosa de succ o para pequenos insetos. Mem Inst Oswaldo Cruz 76: 303- 305. Ferreira E 1964. Distribuic o geografica nos anofelinos do Brasil e sua relac o com o estado atual da erradicac o da malaria. Rev Bras Malariol D Trop 16: 329-338. Flores-Mendoza C, Deane LM 1993. Where are the resting-places of Anopheles aquasalis males? Mem Inst Oswaldo Cruz 88: 501-502. Flores-Mendoza C, Cunha RA, Rocha DS, Lourenco-de-Oliveira R 1996. Determinac o das fontes alimentares de Anopheles aqua- salis Curry, 1932 (Diptera: Culicidae) de Guapimirim, Rio de Janeiro, pelo teste de precipitina. Rev Saude Publica (accepted). Forattini OP 1962. Entomologia Medica. Universidade de S o Paulo, vol I, 662 pp. Galv o ALA, Damasceno RG, Marquez AP 1942. Algumas observac es sobre a biologia dos anofelinos de importancia epidemiologica de Belem, Para. Arq Hig Rio de Janeiro 12: 51-111. Lourenco-de-Oliveira R 1984. Estudo sobre a sistematica e alguns aspectos da ecologia dos mosquitos (Diptera; Culicidae) de uma area de planicie (Granjas Calabria) em Jacarepagua, Rio de Janeiro. MSc thesis. Inst. Oswaldo Cruz, Rio de Janeiro, 185 pp. Lucena DT 1946. Esb“co ecologico de An. (N.) tarsimaculatus Goeldi 1905, no Nordeste Brasileiro. A Folha Medica 27: 113-144. Lucena DT 1950. Habitos domiciliares do Anopheles tarsimaculatus Goeldi 1905. Rev Bras Malariol 2: 239- 260. Moraes HF 1990. SUCAM sua Origem, sua Historia. Ministerio da Saude, SUCAM, Brasilia, vol. I, 484 pp. Natal D, Marucci D 1984. Aparelho de succ o tipo aspirador para captura de mosquitos. Rev Saude Publica 18: 418-420. Panday SR 1973. Age structure of some mosquito populations in a coastal area in Surinam. Mosq News 35: 305-307. Rachou GR 1958. Anofelinos do Brasil: comportamento das especies vetoras de malaria. Rev Bras Malariol D Trop 10: 145- 181. Rachou GR, Moura-Lima M, Barbosa AL 1950. Considerac es s“bre o An. (N.) tarsimaculatus Goeldi, 1905 (An. (N.) aquasalis, Curry, 1932) no Estado do Ceara, com especial referencia ao seu encontro a 52 km da orla maritima. Rev Bras Malariol 2: 57-65. Ramos AS 1943. Observac es sobre os anofelinos do litoral Paulis- ta Anopheles (Nyssorhynchus) tarsimaculatus (Goeldi, 1905), Anopheles (Nyssorhynchus) oswaldoi (Peryassu, 1922). Arq Hig Saude Publica 8: 51-52. Ribbands CR 1945. Moonlight and the house-haunting habits of female anophelines in West Africa. Bull Ent Res 36: 395- 415. Root FM 1926. Studies on Brazilian mosquitoes. I. The Anophelines of the Nyssorhynchus group. Amer J Hyg 6: 684- 717. Rubio-Palis Y 1992. Influence of moonlight on light trap catches of the malaria vector Anopheles nuneztovari in Venezuela. J Am Mosq Control Assoc 8: 178-180. Senior-White RA 1951. Studies on the bionomics of Anopheles aquasalis Curry, 1932. Part II. Ind J Malariol 5: 465- 512. Senior-White RA 1952. Studies on the bionomics of Anopheles aquasalis Curry, 1932. Part III. Ind J Malariol 6: 31- 72. Siegel S 1956. Non-parametric Statistics for the Behavioural Sciences. New York, Mc Graw-Hill, 350 pp. Silvain JF, Pajot FX 1981. cologie d'Anopheles (Nyssorhynchus) aquasalis Curry, 1932 en Guyane Francaise. Cah ORSTOM Ser Ent Med et Parasitol 19: 11-21. Supported by CNPq and FIOCRUZ. ^+Corresponding author. Fax: 55-21-290.9339 Received 14 September 1995 Accepted 13 February 1996 Fig. 1: study area in Guarai, State of Rio de Janeiro, Brazil. Fig. 2: "Meia noite" farm domiciliary and extradomiciliary stations in Guarai, State of Rio de Janeiro, Brazil. Fig. 3: a - Monthly variation of temperature (maximum, minimum and average), and relative humidity of the air. b - Monthly average (per hour) of Anopheles aquasalis females captured at the domiciliary (human bait indoors, outdoors and inner walls) and extradomiciliary stations (human and animal baits), and variation of rainfall and tide, in Guarai, State of Rio de Janeiro, Brazil, November 1991 to October 1992. TABLE I Number of anophelines, females and males, collected per month, at the domiciliary (on human bait indoors and outdoors, and on the inner walls of a house) and extradomiciliary stations (on human and animal baits, on the internal wooden surfaces of the stable, and with light trap) and at natural resting places, in Guarai, State of Rio de Janeiro, Brazil, from November 1991 to December 1992
Anopheline species
-------------------------------------------------
An. aquasalis An. darlingi An. albitarsis An.^a
Year\Month female male female male female male spp.
--------------------------------------------------------------
1991 November 60 - - - - - 1
December 8 - - - - - -
1992 January 323 1 - - - - 2
February 398 - - - 1 - 1
March 235 - 2 - - - 1
April 1,003 6 - - 1 - 3
May 1,114 16 - - - - 2
June 1,556 103 - - - 2 3
July 944 186 - - - - 3
August 1,838 547 - - - - 2
September
2,213 652 - - - - 4
October 734 33 - - - - 2
November 417 200 - - 1 - 1
December 101 - - - - - 1
Total 10,944 1,744 2 - 3 2 26
a: non identifiable females TABLE II Monthly number of Anopheles aquasalis females captured at the domiciliary (on human baits indoors and outdoors, and on the inner walls) and extradomiciliary stations (on man and horse) in Guarai, State of Rio de Janeiro, Brazil, from November 1991 to October 1992
Year/Month Total Hours spent Number of
collected with capture mosquito/
man-hour
----------------------------------------------
1991 November 60 10.25 5.85
December 8 6.16 1.21
1992 January 214 12.20 17.12
February 349 12.25 28.49
March 12 12.20 0.96
April 674 12.25 55.02
May 1,063 12.20 85.04
June 459 12.33 27.23
July 393 5.33 73.39
August 1,029 12.25 84.00
September 631 12.20 50.38
October 196 10.20 18.67
Total 5,086 135.33 37.58TABLE III Monthly frequency of parous Anopheles aquasalis collected at the domiciliary and extradomiciliary stations in Guarai, State of Rio de Janeiro, Brazil, from November 1991 to October 1992
Number Parous
Year/Month dissected No %
------------------------------------
1991 November 20 9 45.0
December 4 3 75.0
1992 January 159 65 40.9
February 188 79 42.0
March 11 7 63.6
April 271 99 36.5
May 235 116 49.4
June 166 136 81.9
July 114 53 46.5
August 266 113 42.5
September 183 82 44.8
October 58 22 37.9
Total 1,675 784 46.8Copyright 1996 Fundacao Oswaldo Cruz
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