Portal de Periódicos da CAPES

Artigo Acesso aberto Produção Nacional Revisado por pares

BIBTEX RIS

Survival of Betta splendens fish (Regan, 1910) in domestic water containers and its effectiveness in controlling Aedes aegypti larvae (Linnaeus, 1762) in Northeast Brazil

2010; Wiley; Volume: 15; Issue: 12 Linguagem: Inglês

10.1111/j.1365-3156.2010.02658.x

1365-3156

José Wellington de Oliveira Lima, Luciano Pamplona de Góes Cavalcanti, Ricardo José Soares Pontes, Jörg Heukelbach,

Malaria Research and Control

Objective In Northeast Brazil, large domestic containers used to store water are important breeding sites of Aedes aegypti, the main vector of dengue fever. The objective of this study was to estimate the survival of Betta splendens (Perciformes: Osphronemidae) fish in domestic containers in Fortaleza (Ceará State), as well as its effectiveness in the control of premature A. aegypti stages. Methods The use of B. splendens was compared to Bacillus thuringiensis israelensis (Bti) in domestic containers. In a first home visit, B. splendens or Bti were applied to water containers. Two follow-up visits were conducted after 3–4 and 5–6 months to assess the presence of viable fish in the containers and infestation by larvae. Betta splendens fish were still present in 97.6% of containers 45–60 days after application. When the fish was present, the infestation rate was significantly higher (P < 0.001) in the Bti group (IR ratio = 21.60; 95% CI: 6.46–72.28). In deposits where the fish remained, efficacy was 85% better than Bti. The permanence of fish was higher in concrete tanks (48.5%) located outside the house (47.5%) and at ground level (53.3%). We conclude that B. splendens may be suitable for biological control of A. aegypti larvae in large domestic water containers, but that appropriate measures should be taken to assure prolonged survival and the presence of fish in the containers. Objectif: Dans le nord du Brésil, de grands conteneurs à usage domestique utilisés pour stocker l’eau sont d’importants sites de reproduction du moustique Aedes aegypti, principal vecteur de la dengue. L’objectif de cette étude était d’estimer la survie des poissons Betta splendens (Perciformes: Osphronemidae) dans les conteneurs à usage domestique à Fortaleza (Etat du Ceará), ainsi que leur efficacité dans la lutte contre les stades pré matures d’A. aegypti. Méthodes: L’utilisation de B. splendens a été comparée à celle de Bacillus thuringiensis israelensis (Bti) dans des récipients domestiques. Dans une première visite à domicile, B. splendens ou Bti a été introduit dans les réservoirs d’eau. Deux visites de suivi ont été effectuées au bout de 3-4 et 5-6 mois pour évaluer la présence de poissons viables dans les conteneurs et les infestations par les larves. Les poissons B. splendensétaient encore présents dans 97,6% des conteneurs 45-60 jours après l’introduction. Lorsque le poisson est présent, le taux d’infestation était significativement plus élevé (p <0,001) dans le groupe de Bti (IR ratio = 21,60; IC95%: 6,46 à 72,28). Dans les dépôts où le poisson a persisté, l’efficacitéétait 85% meilleure qu’avec Bti. La persistance des poissons était élevée dans les cuves béton (48,5%), situées à l’extérieur des maisons (47,5%) et au niveau du sol (53,3%). Nous concluons que B. splendens peut être adapté pour la lutte biologique contre les larves d’A. aegypti dans de grands conteneurs d’eau domestiques, mais que des mesures appropriées devraient être prises pour assurer la présence et la survie prolongée des poissons dans les conteneurs. Mots-clés: dengue, Aedes aegypti, lutte biologique, poissons larvivores, Betta splendens. Objetivo: En el nordeste de Brasil, los grandes contenedores domésticos utilizados para el almacenaje agua son importantes criaderos de Aedes aegypti, el principal vector de la fiebre del dengue. El objetivo de este estudio era estimar la supervivencia de peces Betta splendens (Perciformes: Osphronemidae) en contenedores domésticos en Fortaleza (Ceará State), así como su efectividad en el control de estadios más tempranos de A. aegypti. Métodos: Se comparó el uso de B.splendens con Bacillus thuringiensis israelensis (Bti) en contenedores domésticos. En una primera visita a los hogares, se depositaron B.splendens o Bti en los contenedores de agua. Se realizaron dos visitas de seguimiento después de 4 y 5-6 meses para evaluar la presencia de peces viables en los contenedores y el nivel de infestación de larvas. Los peces Betta splendens aún estaban presentes en un 97.6% de los contenedores 45-60 días después de haber sido depositados. Cuando los peces estaban presentes, la tasa de infestación era significativamente más alta (p 200 l. We used data collected by PMCD agents during routine field activities from October 2002 to April 2003. The Control Programme had a record, for every water container in the household, about the type of treatment (Fish or Bti) used in the previous cycle of treatment. Based on this information, containers were classified as Fish group or Bti group. On the first house study visit, containers from the Fish group were treated with a new specimen of B. splendens fish: a new specimen was placed if no fish was present in the container, or a specimen present in the container was replaced by a new one. Accordingly, the containers from the Bti group were treated with Bti at the first study visit. Subsequently, there were two follow-up visits, the first during the third or the forth month and the second between the fifth and sixth month of observation. During these visits, the presence of viable fish in the containers was checked and infestation status by immature forms of A. aegypti larvae assessed. The observation of the water container stopped when: (i) immature forms of A. aegypti were observed in the container; (ii) the Betta fish was absent; (iii) the study period had finished (censoring time). During the first visit, information about the containers was recorded regarding its type (elevated tanks or ground tanks), material (brick or cement, concrete, asbestos, plastic, metal or fibreglass), location (inside or outside the house), volume (calculated using the dimensions of the container), height above the ground and the presence of cover. Infestation of the containers was determined by the presence of immature forms of A. aegypti. The containers were inspected using a torch, and all immature forms were removed using a sweep net, placed in glass test tubes containing 75% alcohol and taken to the laboratory, where the immature A. aegypti were identified and counted. To calculate the infestation rate, the observation time was the period between the first visit and the date on which the immature forms of A. aegypti were observed, or the period between the first visit and the date of the last visit (censoring time) for those containers that never were infested. To calculate the permanence rate of the fish in the containers, the observation time was the period between the first visit and the date on which the absence of fish was observed, or the period from the first visit to the date of the last visit (censoring time) for those containers in which fish were present during all the visits. The probability of the permanence of B. splendens in the containers over time was estimated by the life table method. Permanence rate was calculated by dividing the number of containers with fish present by the sum of the observation time for the containers. Similarly, the infestation rate of containers was calculated by dividing the number of infested containers by the sum of the observation time for the containers. The association between containers’ characteristics and permanence of fish or infestation, as well as the association between containers’ characteristics and treatment (Bti or Fish) was assessed by means of permanence rate ratio and infestation rate ratio and its 95% confidence intervals, calculated through Poisson regression. Characteristics associated with infestation, in a multivariate model, with a P value ≤0.250 were considered confounders and were included in a final multivariate Poisson regression model to assess the relationship between treatment and infestation (Hosmer & Lemeshow 2000). In total, 1001 houses were inspected, and 974 large volume containers identified (>200 l). Five hundred and thirty-seven (55.1%) containers belonged to the B. splendens group and 437 (44.9%) to the Bti group. Initially, the duration of the presence of B. splendens in domestic water containers was estimated (Table 1). A high proportion (97.6%) was present at 45–60 days, and then this proportion dropped rapidly. In one container, the fish remained for at least 183 days. The characteristics of containers associated with the duration of the presence of the fish specimens were assessed (Table 2). The permanence rate was significantly longer in ground tanks (P < 0.001), in brick and cement or concrete tanks (P = 0.018), in containers situated outside the house (P = 0.038) and in those located <1 m above the ground (P = 0.002). The volume of the container and the presence of a cover were not significantly associated with the permanence of the fish. In the multivariate analysis, only the type of container remained significantly associated with the permanence of fish (adjusted incidence rate ratio = 1.99; 95% CI: 1.41–2.83; P < 0.001). Factors associated with container infestation by A. aegypti larvae were investigated to identify the potential confounders of the relationship between treatment and infestation (Table 3). The incidence rate of infestation by Aedes larvae was significantly higher in ground tanks (P < 0.001), in brick and cement/concrete containers (P = 0.008), in containers with a volume <2000 l (P = 0.013), in containers <1 m above the ground (P < 0.001) and in uncovered containers (P < 0.001). Infestation was not significantly associated with the location of the container. After adjustment, only the type of container was significantly (P < 0.001) associated with infestation. The infestation rate was 2.74; 95% CI: 1.58–4.76 times longer in ground tanks than in elevated tanks. To understand how a containers’ characteristics work as confounders, the association between containers’ characteristics and treatment was assessed (data not shown in tables). Type of deposits, material and the presence of cover were significantly associated with treatment group. Among containers from the Fish group, there was a higher proportion of ground tanks (P < 0.001), brick and cement/concrete containers (P < 0.001) and uncovered containers (P < 0.001). To estimate the relationship between treatment and infestation, not adjusted and adjusted to confounders, a multivariate analysis was performed by means of Poisson regression models (Table 4). In non-adjusted analysis, when the fish was present, the infestation rate was significantly higher (P = 0.001) in the Bti group [infestation rate (IR) ratio = 6.72; 95% CI: 2.08–21.64]. However, when the fish was not present in the container, the infestation rate was significantly lower (P < 0.001) in the Bti group (IR ratio = 0.39; 95%; CI: 0.27–0.57). Different results were obtained in the multivariate analysis. When the fish was present, the infestation rate was significantly higher (P < 0.001) in the Bti group (IR ratio = 21.60; 95% CI: 6.46–72.28). In deposits where the fish remained, efficacy was 85% better than Bti. But when the fish was absent, the incidence rate was similar in both groups (P = 0.471). Our study suggests that B. splendens is more effective than the larvicide Bacillus thuringiensis israelensis (Bti) as a control method of immature forms of A. aegypti. When the fish was present in a container, the incidence of immature forms of A. aegypti was 19 times lower than in containers treated with Bti. This is the first investigation of the effectiveness of B. splendens as a control strategy of immature forms of A. aegypti in domestic water containers (Pamplona 2006). This study only considered containers with a volume equal or larger than 200 l, such as ground tanks and elevated tanks and drums. In Fortaleza, these big water containers are essential to store water because the public water supply usually only reaches households for a few hours each day (Caprara et al. 2009). The use of Betta fish to control the immature forms of A. aegypti in large volume containers may have a great impact on transmission, as these containers are responsible for a big proportion of pupae (Pamplona et al. 2004; Romero-Vivas et al. 2006; Koenraadt et al. 2007). On the other hand, these large volume containers consume the biggest amounts of larvicides. According to the Brazilian Ministry of Health, in the State of Ceará alone, in 2009, US$ 4.5 million was spent on larvicides for A. aegypti control (Brasil, 2009). This cost would be reduced if the larvicide was substituted by fish (Bheema et al. 1982; Neng et al. 1987; Conejo et al. 2000; Martinez-Ibara et al. 2002; Mohamed 2003). As the selection of the type of container to receive fish or be treated with Bti was not random, this result could be confounded if factors facilitating the infestation of containers with A. aegypti were positively associated with the containers treated with Bti. However, the opposite occurred. The fish group had a significantly higher proportion of ground tanks, brick and cement/concrete containers and uncovered containers (data not shown in table). These categories of the respective variables were associated with the highest infestation rate of A. aegypti (Table 2). As expected, the adjusted odds ratio (OR = 19.69) of infestation was much higher than the unadjusted one (OR = 6.72). Up to 60 days, only 2.4% of the containers were observed without any fish. However, this proportion increased to 37.4% at the end of the third month. Thus, in the routine of the control programme, after 60 days, all containers that received fish should be examined to replace any absent fish. Sixty days are also the critical point for the residual effects of the Bti. In an experimental study with renewed water, to simulate the conditions in a domestic water container, only 38–44% of A. aegypti larvae died 60 days after the water was treated with Bti larvicide (Pontes et al. 2005, 2010). The water in domestic water containers has some characteristics which may influence the longevity of Betta fish, such as the level of nutrients and the chlorine concentration. Assuming that the water for domestic consumption has a lower concentration of organic matter than natural breeding sites, it is probable that this restriction of nutrients is a factor reducing the longevity of Betta fish in domestic water containers. Regarding chlorine, it has been demonstrated that 27.5% of the fish specimens do not resist concentrations of chlorine of 1.5 mg/l (Cavalcanti et al. 2009). In Fortaleza, the concentration of chlorine in the public water supply varies between 0.55 and 1.83 mg/l (Companhia de água e esgoto do Ceará (CAGECE), 2007). The influence of certain characteristics of containers (type, material, location, volume, height and the presence of a cover) on the longevity of Betta fish was investigated. In particular, the volume of the container may influence the survival of the Betta because this species has the habit of being in constant movement (Bronstein 1994), and consequently, in large containers they would consume more energy, leading to a greater possibility of death because of energy exhaustion. However, in our study, no significant relationship was observed between the volume of the container and the longevity of the fish. During the study’s 6 month observation, the incidence rate of Betta fish was 1.99 times higher in the ground tanks than the elevated tanks, after adjustment for other characteristics of the containers. This result has great practical importance because it is easier to monitor the presence of fish in ground tanks than in elevated tanks. In this analysis, the presence of the Betta fish in a container at any time was used as an indicator of the fish’s survival until that point. When absent, the fish was considered dead. However, a fish may be absent because it left the container through the overflow pipe or when the container overflowed. Putting a mesh over the pipe would prevent the escape of fish while preventing the overflow of water. Monitoring the fish’s presence should be continuous and might be costly and inefficient if performed by the Control Programme agents. Hence, the monitoring should be performed by the community, who would report the absence of fish to the Control Programme, which would take the necessary measures. Community participation in integrated vector control programmes has produced good results and cost reductions (Neng et al. 1987; Martinez-Ibara et al. 2002). We thank the technicians Roberto Varela, Socorro Furtado and Carlos Alberto for supervision of the fieldwork and the endemic agents of Fortaleza for their important contributions to field activities. J.H. is a research fellow from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq/Brazil).