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Comparison of automatic traps to capture mosquitoes (Diptera: Culicidae) in rural areas in the tropical Atlantic rainforest

Abstract

In several countries, surveillance of insect vectors is accomplished with automatic traps. This study addressed the performance of Mosquito Magnet® Independence (MMI) in comparison with those of CDC with CO2 and lactic acid (CDC-A) and CDC light trap (CDC-LT). The collection sites were in a rural region located in a fragment of secondary tropical Atlantic rainforest, southeastern Brazil. Limatus durhami and Limatus flavisetosus were the dominant species in the MMI, whereas Ochlerotatus scapularis was most abundant in CDC-A. Culex ribeirensis and Culex sacchettae were dominant species in the CDC-LT. Comparisons among traps were based on diversity indices. Results from the diversity analyses showed that the MMI captured a higher abundance of mosquitoes and that the species richness estimated with it was higher than with CDC-LT. Contrasting, difference between MMI and CDC-A was not statistically significant. Consequently, the latter trap seems to be both an alternative for the MMI and complementary to it for ecological studies and entomological surveillance.

CDC-LT; Mosquito Magnet ® ; carbon dioxide; lactic acid; surveillance


Kairomones chemicals can be employed in mosquito automatic traps to improve their attractiveness ( Service 1993Service MW 1993. Mosquito ecology - Field sampling methods , 2nd ed., Chapman & Hall, London, 988 pp. ). Carbon dioxide is one of the kairomones most largely used in Culicidae studies. Moreover, it can be used either alone or in combination with octenol, lactic acid, incandescent light or light-emitting diode ( Hoel et al. 2007Hoel DF, Kline DL, Allan SA, Grant A 2007. Evaluation of carbon dioxide, 1-octen-3l and acid lactic as baits in Mosquito MagnetTMPro traps for Aedes albopictus in north central Florida. J Am Mosq Control Assoc 23 : 11-17. , Brown et al. 2008Brown HE, Paladini M, Cook RA, Kline DL, Barnard D 2008. Effectiveness of mosquito trap in measuring species abundance and composition. J Med Entomol 45 : 517-521. , Xue et al. 2008Xue RD, Doyle MA, Kline DL 2008. Field evaluation of CDC and Mosquito Magnet X traps baited with dry ice, CO2sachet and octenol against mosquitoes. J Am Mosq Control Assoc 24 : 249-252. , Jawara et al. 2011Jawara M, Awolola TS, Pinder M, Jeffries D, Smallegange RCS, Takken W, Conway DJ 2011. Field testing of different chemical combinations as odour baits for trapping wild mosquitoes in the Gambia . PLoS ONE 6 : e19676. ).

Automatic traps are largely employed for monitoring mosquito vector-borne disease populations ( Cohnstaedt et al. 2008Cohnstaedt L, Gillen JI, Munstermann LE 2008. Light-emitting diode technology improves insect trapping. J Am Mosq Control Assoc 24 : 331-334. , Bisevac et al. 2009Bisevac L, Franklin DC, Williamson GJ, Whelan PI 2009. A comparison of two generic trap types for monitoring mosquitoes through an annual cycle in tropical Australia. J Am Mosq Control Assoc 25: 58-65. , Calzolari et al. 2010Calzolari M, Bonilauri P, Bellini R, Albieri A, Defilippo F, Maioli G, Galletti G, Gelati A, Barbieri I, Tamba M, Lelli D, Carra E, Cordioli P, Angelini P, Dottori M 2010. Evidence of Simultaneous Circulation of West Nile and Usutu viruses in mosquitoes sampled in Emilia-Romagna Region (Italy) in 2009. PLoS ONE 5 : e14324. ), ecological studies ( Forattini et al. 1991Forattini OP, Gomes AC, Kakitani I, Marucci D 1991. Observações sobre domiciliação de mosquitos Culex ( Melanoconion ) em ambiente com acentuadas modificações antrópicas. Rev Saude Publica 25 : 257-266. , Jones et al. 2004Jones JW, Turell MJ, Sardelis MR, Watts DM, Coleman RE, Fernandez R, Carbajal F, Pecor JE, Calampa C, Klein TA 2004. Seasonal distribution, biology and human attraction patterns of Culicine mosquitoes (Diptera: Culicidae) in a forest near Puerto Almendras, Iquitos, Peru. J Med Entomol 41 : 349-360. , Cardoso et al. 2011Cardoso JC, Paula MP, Fernandes A, Santos E, Almeida MAB, Fonseca DF, Sallum MAM 2011. Ecological aspects of mosquitoes (Diptera:Culicidae) in an Atlantic forest area on the north coast of Rio Grande do Sul state, Brazil. J Vector Ecol 36 : 175-186. ), biodiversity studies ( Montes 2005Montes J 2005. Fauna de Culicidae da Serra da Cantareira, São Paulo, Brasil. Rev Saude Publica 39 : 578-584. ) and species distribution ( Hutchings et al. 2011Hutchings RS, Sallum MA, Hutchings RW 2011. Mosquito (Diptera: Culicidae) diversity of a forest-fragment mosaic in the Amazon rain forest. J Med Entomol 48 : 173-187. ). However, automatic traps perform differently depending on the model of the trap and the kairomones added to it ( Gama et al. 2007Gama RA, Andrade AJ, Andrade MR, Resende MC, Eiras AE 2007. Avaliação da armadilha HP iscada com diferentes taxas de liberação de octenol na captura de anofelinos (Diptera: Culicidae) em Brejo do Mutambal, Município de Varzelândia, estado de Minas Gerais. Rev Soc Bras Med Trop 40 : 408-410. , Cohnstaedt et al. 2008Cohnstaedt L, Gillen JI, Munstermann LE 2008. Light-emitting diode technology improves insect trapping. J Am Mosq Control Assoc 24 : 331-334. , Bisevac et al. 2009Bisevac L, Franklin DC, Williamson GJ, Whelan PI 2009. A comparison of two generic trap types for monitoring mosquitoes through an annual cycle in tropical Australia. J Am Mosq Control Assoc 25: 58-65. , Dusfour et al. 2010Dusfour I, Carinci R, Gaborit P, Issaly J, Girod R 2010. Evaluation of four methods for collecting malaria vectors in French Guiana. J Econ Entomol 103 : 973-976. ). Consequently, it is important to be aware of limitations when selecting a trap and the kairomones to add to it in order to get the best sampling performance for the study in focus ( Gullan & Cranston 2005Gullan PJ, Cranston PS 2005. The insects: an outline of entomology , Blackwell Publishing, Oxford, 504 pp. , Gama et al. 2007Gama RA, Andrade AJ, Andrade MR, Resende MC, Eiras AE 2007. Avaliação da armadilha HP iscada com diferentes taxas de liberação de octenol na captura de anofelinos (Diptera: Culicidae) em Brejo do Mutambal, Município de Varzelândia, estado de Minas Gerais. Rev Soc Bras Med Trop 40 : 408-410. ). Furthermore, surveillance personal need to be sure that the selected trap is capable of sampling the target species, allowing them to estimate abundance, composition, distribution and seasonality of mosquito populations present in an environment under certain ecological conditions.

The CDC light trap (CDC-LT) ( Sudia & Chamberlain 1962Sudia WD, Chamberlain RW 1962. Battery-operated light trap, an improved model. Mosq News 22 : 126-129. ) is the standard trap for surveillance and ecological studies on mosquito ( Gomes et al. 1985Gomes AC, Rabello EX, Natal D 1985. Uma nova câmara coletora para armadilha CDC-miniatura. Rev Saude Publica 19 : 190-191. , 1987, Hoel et al. 2009Hoel DF, Kline DL, Allan SA 2009. Evaluation of six mosquito traps for collection of Aedes albipictus and associated mosquito species in a suburban setting in north central Florida. J Am Mosq Control Assoc 25 : 47-57. ). Consequently, it has been largely employed in studies that aimed to compare the performance of different traps ( Brown et al. 2008Brown HE, Paladini M, Cook RA, Kline DL, Barnard D 2008. Effectiveness of mosquito trap in measuring species abundance and composition. J Med Entomol 45 : 517-521. , Xue et al. 2008Xue RD, Doyle MA, Kline DL 2008. Field evaluation of CDC and Mosquito Magnet X traps baited with dry ice, CO2sachet and octenol against mosquitoes. J Am Mosq Control Assoc 24 : 249-252. , Dusfour et al. 2010Dusfour I, Carinci R, Gaborit P, Issaly J, Girod R 2010. Evaluation of four methods for collecting malaria vectors in French Guiana. J Econ Entomol 103 : 973-976. , Hiwat et al. 2011bHiwat H, Rijk M, Andriessen R, Koenraadt CJM, Takken W 2011b. Evaluation of methods for sampling the malaria vector Anopheles darlingi (Diptera, Culicidae) in Suriname and the relation with its biting behaviour. J Med Entomol 48 : 1039-1046. ), including in forested areas within the domain of Atlantic Forest biome ( Laporta & Sallum 2011Laporta GZ, Sallum MAM 2011. Effect of CO2and 1-octen-3-ol attractants for estimating species richness and the abundance of diurnal mosquitoes in the southeastern Atlantic forest, Brazil. Mem Inst Oswaldo Cruz 106 : 279-284. ).

Currently, Mosquito Magnet ® (MM) (Woodstream Corporation, Lititz, PA, USA) automatic traps are becoming an increasingly important instrument for mosquito surveillance ( Bell et al. 2005Bell JA, Mickelson NJ, Vaughab JA 2005. West Nile virus in host-seeking mosquitoes within a residential neighborhood in Grand Forks, North Dakota. Vector Borne Zoonotic Dis 5 : 373-382. ). Studies using distinct models of MM were conducted in several countries to address the most efficient trap for sampling mosquito vector species in urban and rural areas ( Brown et al. 2008Brown HE, Paladini M, Cook RA, Kline DL, Barnard D 2008. Effectiveness of mosquito trap in measuring species abundance and composition. J Med Entomol 45 : 517-521. , Dusfour et al. 2010Dusfour I, Carinci R, Gaborit P, Issaly J, Girod R 2010. Evaluation of four methods for collecting malaria vectors in French Guiana. J Econ Entomol 103 : 973-976. , Hiwat et al. 2011aHiwat H, Andriessen R, Rijk M, Koenraadt CJM, Takken W 2011a. Carbon dioxide baited trap catches do not correlate with human landing collections of Anopheles aquasalis in Suriname. Mem Inst Oswaldo Cruz 106 : 360-364. , Rubio-Palis et al. 2012Rubio-Palis Y, Moreno JE, Sánchez V, Estrada Y, Anaya W, Bevilacqua M, Cárdenas L, Martínez A, Medina D 2012. Can Mosquito Magnet®substitute for human-landing catches to sample anophe- line populations? Mem Inst Oswaldo Cruz 107 : 546-549. ). There is no record regarding the performance of MM in areas of the Atlantic rainforest. The major objectives of the present study were: (i) to assess the performance of the Mosquito Magnet ® Independence (MMI) and (ii) to compare the capacity of the MMI to that of CDC associated with CO 2 and Lurex3 ® (lactic acid). A CDC-LT with incandescent light was employed as control. Comparisons among the traps were mainly based on the assessment of mosquito fauna present in areas situated within the Atlantic Forest domain. Field collections were carried out in three rural localities with different environmental characteristics at Agronomy Center for the Vale do Ribeira, Agronomic Institute of Campinas, Pariquera Açu, state of São Paulo (SP), Brazil.

MATERIALS AND METHODS

Mosquitoes were sampled in rural areas interspersed with fragments of secondary forest at Agronomy Center for the Vale do Ribeira ( Fig. 1 ). Three localities equidistant by 1 km were selected to install one MMI, one CDC with CO 2 and Lurex3 ® [CDC with CO 2 and lactic acid (CDC-A)] and one CDC-LT. Mosquito collections were carried out monthly, from 15:00 pm until 21:00 pm, from December 2010-November 2011. A 3 x 3 Latin square design was used to control environmental variations relative to the localities were traps were installed. Accordingly, each trap was placed in a specific locality in day 1 and in the following two days they were rotated in a way that each trap sampled all three localities in three consecutive days. The sampling effort of each trap per month was 18-h (6 h/per day in 3 consecutive days). Specimens were identified employing morphological keys proposed by Lane (1953)Lane J 1953. Neotropical Culicidae , Vol. II, Editora da Universidade de São Paulo, São Paulo, 1.112 pp. for the genus Limatus , Galindo et al. (1954)Galindo P, Blanton FS, Peyton EL 1954. A revision of the Uranotaenia of Panama with notes on other American species of the genus (Diptera, Culicidae). Ann Entomol Soc Am 47 : 105-177. for the genus Uranotaenia , Correa and Ramalho (1956)Correa RR, Ramalho GR 1956. Revisão de Phoniomyia Theobald, 1903 (Diptera: Culicidae, Sabethini). Folia Clin Biol 25 : 1-176. for the subgenus Phoniomyia of Wyeomyia , Consoli and Lourenço-de-Oliveira (1994)Consoli RAGB, Lourenço-de-Oliveira R 1994. Principais mosquitos de importância sanitária no Brasil , Fiocruz, Rio de Janeiro, 225 pp. for the Aedini , Forattini (2002)Forattini OP 2002. Culicidologia médica - Identificação, biologia e epidemiologia, Vol. II, Editora da Universidade de São Paulo, São Paulo, 864 pp. for the genus Anopheles and for the spissipes section of Culex ( Melanoconion ).

Fig. 1
: location of the municipality of Pariquera Açu, Vale do Ribeira, state of São Paulo, Brazil.

The CDC-LT possessed a motor powered by a 6-V battery, a head connected to a collecting metal chamber and a 3-W incandescent bulb. The CDC-A was operated by a similar system, with no incandescent bulb, but with CO 2 and latic acid as attractive. A cartridge of the Lurex3 ® (American Biophysics Corporation) provided the lactic acid. Each cartridge contained 4.88 g of lactic acid incorporated to 13.8 g of a gel matrix. This mixture was stored inside a plastic tube, allowing the release of approximately 230 mg/day of lactic acid ( Hoel et al. 2007Hoel DF, Kline DL, Allan SA, Grant A 2007. Evaluation of carbon dioxide, 1-octen-3l and acid lactic as baits in Mosquito MagnetTMPro traps for Aedes albopictus in north central Florida. J Am Mosq Control Assoc 23 : 11-17. ). The CO 2 was provided by a metal cylinder with four and a half pounds (White Martins ® ), with an adjustable valve (Swagelok ® ) that released 450-500 mL of CO 2 per minute. The MMI used a mixture of propane and butane, which through its combustion releases CO 2 , heat and water vapour ( Hoel et al. 2009Hoel DF, Kline DL, Allan SA 2009. Evaluation of six mosquito traps for collection of Aedes albipictus and associated mosquito species in a suburban setting in north central Florida. J Am Mosq Control Assoc 25 : 47-57. ). All traps were installed at 1.5 m heights.

The statistical analyses were performed in the program R 2.12, using the packages Mvabund, Venneuler and Biodiversity R and the software SPSS v.13.0. Levene, Shapiro-Wilk and Kolmogorov-Smirnov tests were performed to explore the normality of abundance data. Indices of diversity were employed to address and compare the performance of the traps. The Rényi diversity index ( Henderson 2006Henderson PA 2006. Practical methods in ecology , Blackwell Publishing, Oxford, 172 pp. ) that generalizes total richness (α = 0), diversity (Shannon-Weiner α = 1; Simpson-Yule α = 2) and dominance (Berger-Parker α = inf) indices was employed to explore differences in species diversity among traps. The Kruskal-Wallis (KW) test (p > 0.05) was used to assess differences among the Rényi diversity indices estimated by each trap and the Bonferroni test was utilised to perform multiple comparisons among the traps. Additionally, the similarity of species captured by the traps was estimated using the Jaccard and Sorensen index. The Veen diagram was constructed to illustrate the similarities and differences among the traps, because it shows both exclusive and shared species obtained by the traps. To assess potential associations among mosquito species and traps we employed the Pearson chi-square test (χ 2 ). The nonparametric test of second order Jackknife was used to estimate the expected species richness for each trap. Multivariate analyses of abundance values were employed to address both the effect of the traps and effect of the localities in the frequency of individuals of a species sampled by each trap. For the multivariate analyses, we employed a generalised linear model (GLM) implemented in the mvabund package of statistics program R 2.12 ( Wang et al. 2012Wang Y, Naumann U, Wright ST, Warton DI 2012. Mvabund - an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3 : 471-474. ). The mvabund package uses a hypothesis test based on resampling to address potential factors associated with variables ( Bálint et al. 2013Bálint M, Tiffin P, Hallström B, O’Hara RB, Olson MS, Fankhauser JD, Piepenbring M, Schmitt I 2013. Host genotype shapes the foliar fungal microbiome of balsam poplar ( Populus balsamifera ). PLoS ONE 8 : e53987. ). A GLM was employed by Warnick et al. (1990)Warnick RM, Clarke KR, Gee JM 1990. The effect of disturbance by soldier crabs Mictyris platycheles H. Milne Edwards on meiobenthic community structure. J Exp Mar Biol Ecol 135 : 19-33. to replace a model based on the distance of abundance. According to Wang et al. (2012)Wang Y, Naumann U, Wright ST, Warton DI 2012. Mvabund - an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3 : 471-474. , models based on distance do not clarify the effect of sampling units.

RESULTS

Six thousand three hundred and ninety one mosquitoes were captured with a 216-h sampling effort. Three hundred thirty six specimens could not be identified because they were damaged. The remaining 6,055 specimens were identified in 70 species or taxonomic units of 12 genera ( Table I ).

TABLE I
Species and taxonomic units abundance per sampling trap in rural areas in the tropical Atlantic rainforest, southeastern Brazil

Results of the normality tests showed that the abundance data has a non-normal distribution. Accordingly, Levene’s test obtained value p = 0.001, whereas in both Kolmogorov-Sminorv and Shapiro-Wilk tests was p = 0.000. These values indicated that the abundance data had a non-normal distribution.

The Pearson χ-square statistics showed potential association between CDC-LT and the tribe Culicini. Species from this tribe represented 78.9% of total mosquitoes captured by the trap (χ 2 = 2760.04; p < 0.00). For the CDC-A, a positive association was found for representatives of the tribe Aedini with 58.3% of the total sampled by it, whereas a positive association was observed between Sabethini mosquitoes and MMI. This trap captured 36.1% of specimens.

The Rényi diversity index ( Fig. 2 ) showed that the MMI found the highest values for the diversity indexes in comparison to CDC-LT and CDC-A, whereas results of the KW test indicated that the differences in the diversity indexes were statistically significant, i.e., richness (KWχ 2 = 14.88, p = 0.0006), Shannon-Weiner diversity (KWχ 2 = 19.62, p = 0.00005), Simpson-Yule diversity (KWχ 2 = 19:35, p = 0.00006) and Berger-Parker dominance (KWχ 2 = 4.19, p = 0.00007).

Fig. 2
: Rényi index illustrating differences in diversities estimated by the traps. A: CDC light trap: B: CDC with CO 2 and lactic acid; C: Mosquito Magnet ® Independence.

Results of the Bonferroni test indicated that differences in the diversity indexes were significant and mainly caused by the values estimated for the MMI in comparison to those for CDC-LT, whereas differences between CDC-A and MMI were not significant. Complete results of the KW and Bonferroni tests are in Supplementary data 1 .

The extrapolated species richness using second-order Jackknife estimator to CDC-LT, CDC-A and MMI was 59, 67 and 77 species, respectively. Of the 42 species collected in CDC-LT, seven were singletons and eight were doubletons. In the CDC-A, 14 species were singletons and two were doubletons among 41 species collected, whereas the MMI captured 46 species with 13 singletons and three doubletons.

The values estimated with Jaccard (cj = 0.58) and Sorensen (Cn = 0.52) indexes showed that species composition in the CDC-A was similar to that in the MMI. The Venn diagram ( Fig. 3 ) illustrated species distribution in each trap and those species that were shared among them. A complete list of species captured in each trap and those shared by two or all traps are in Supplementary data 2 .

Fig. 3
: Venn diagram illustrating the similarity of the mosquito species captured and shared between traps, CDC light trap (CDC-LT), CDC with CO 2 and lactic acid (CDC-A) and Mosquito Magnet ® Independence (MMI), Pariquera Açu, Vale do Ribeira, state of São Paulo, Brazil.

Results of multivariate analysis of the abundance using a GLM showed that differences observed among the traps were statistically significant [Deviance of model’s prediction (Dev) = 476.4, p = 0.001]. Comparing the values of abundance relative to the localities where the traps were installed, the variance values showed that differences were not significant (Dev = 19.0, p = 0.76) and that there was no interaction between the traps and the localities (Dev = 0.0, p = 0.709). Species that were more abundant in each trap are in Table II .

TABLE II
Results of multivariate analyses using a generalised linear model to compare the values of abundance of mosquito species and taxonomic units obtained with each automatic trap

DISCUSSION

Results of the analyses carried out in the present study indicated that the MMI is the most efficient trap to capture mosquito species present in rural areas located in the deforested areas within the domain of tropical rainforests. Similar results were obtained by Brown et al. (2008)Brown HE, Paladini M, Cook RA, Kline DL, Barnard D 2008. Effectiveness of mosquito trap in measuring species abundance and composition. J Med Entomol 45 : 517-521. , Hoel et al. (2009)Hoel DF, Kline DL, Allan SA 2009. Evaluation of six mosquito traps for collection of Aedes albipictus and associated mosquito species in a suburban setting in north central Florida. J Am Mosq Control Assoc 25 : 47-57. and Dusfour et al. (2010)Dusfour I, Carinci R, Gaborit P, Issaly J, Girod R 2010. Evaluation of four methods for collecting malaria vectors in French Guiana. J Econ Entomol 103 : 973-976. with distinct models of MM automatic traps. These studies demonstrate that any model of MM trap is capable of removing large numbers of mosquito specimens from the environment, especially individuals from species with a great potential to become pest in environments impacted by human activities. This is the case of some species such as Ochlerotatus scapularis , Culex ribeirensis and Coquillettidia chrysonotum . These mosquitoes were abundant and had potential to become pests in both rural and urban environments ( Forattini et al. 1991Forattini OP, Gomes AC, Kakitani I, Marucci D 1991. Observações sobre domiciliação de mosquitos Culex ( Melanoconion ) em ambiente com acentuadas modificações antrópicas. Rev Saude Publica 25 : 257-266. , 1993a, Cardoso et al. 2011Cardoso JC, Paula MP, Fernandes A, Santos E, Almeida MAB, Fonseca DF, Sallum MAM 2011. Ecological aspects of mosquitoes (Diptera:Culicidae) in an Atlantic forest area on the north coast of Rio Grande do Sul state, Brazil. J Vector Ecol 36 : 175-186. ).

Several models of MM were developed to effectively removing synanthropic mosquitoes from urban and rural environments ( Cilek & Hallmon 2005Cilek JE, Hallmon CF 2005. The effectiveness of the Mosquito Magnet trap for reducing biting midge (Diptera: Ceratopogonidae) populations in coastal residential backyards. J Am Mosq Control Assoc 21 : 218-221. ). However, MM traps were also employed for surveillance of mosquito species with potential to transmit the West Nile virus in the United Kingdom ( Hutchinson et al. 2007Hutchinson RA, West PA, Lindsay SW 2007. Suitability of two carbon dioxide-baited traps for mosquito surveillance in the United Kingdom. Bull Entomol Res 97 : 591-597. ). In Denmark, the same trap was utilised to sample Ceratopogonidae insects in agricultural areas and thus to monitor the circulation of the Schmallenberg virus. Infections by the Schmallenberg virus can cause congenital malformations and stillbirths in cattle and goats ( Rasmussen et al. 2012Rasmussen LD, Kristensen B, Kirkeby C, Rasmussen TB, Belsham GJ, BØdker R, BØtner A 2012. Culicoids as vectors of Schmallenberg virus. Emerg Infect Dis 18 : 1204-1206. ). In Venezuela, studies employing MM traps showed that it was efficient for collecting Anopheles nuneztovari mosquitoes in a malaria-endemic area in the Amazon Basin ( Rubio-Palis et al. 2012Rubio-Palis Y, Moreno JE, Sánchez V, Estrada Y, Anaya W, Bevilacqua M, Cárdenas L, Martínez A, Medina D 2012. Can Mosquito Magnet®substitute for human-landing catches to sample anophe- line populations? Mem Inst Oswaldo Cruz 107 : 546-549. ).

Results of the statistical tests indicated a significant difference regarding to diversity indexes obtained with both CDC-A and MMI in comparison to those with CDC-LT. Moreover, differences between CDC-A and MMI were not statistically significant. This can be explained by similarity between CDC-A and MMI, which was likely caused by the use of kairomones that promoted the capture of the same species. Forattini et al. (1987Forattini OP, Gomes AC, Natal D, Kakitani I, Marucci D 1987. Preferências alimentares de mosquitos Culicidae no Vale do Ribeira, São Paulo, Brasil. Rev Saude Publica 21 : 171-187. , 1993bForattini OP, Kakitani I, Massad E, Marucci D 1993b. Studies on mosquitoes (Diptera: Culicidae) and anthropic environment. 3. Survey of adult stages at the rice irrigation system and the emergence of Anopheles albitarsis in south-eastern, Brazil. Rev Saude Publica 27 : 313-325. ) used carbon dioxide in CDC-LT to study the population dynamics, feeding behaviour and ecological characteristics of mosquito communities in a gradient of environments in the Vale do Ribeira. Accordingly, those authors showed that Oc. scapularis was abundant in rice plantation areas ( Forattini et al. 1993bForattini OP, Kakitani I, Massad E, Marucci D 1993b. Studies on mosquitoes (Diptera: Culicidae) and anthropic environment. 3. Survey of adult stages at the rice irrigation system and the emergence of Anopheles albitarsis in south-eastern, Brazil. Rev Saude Publica 27 : 313-325. ) and in anthropic environments. Additionally, the species showed capacity to invade, establish and disperse in domiciliary environments ( Forattini et al. 1987Forattini OP, Gomes AC, Natal D, Kakitani I, Marucci D 1987. Preferências alimentares de mosquitos Culicidae no Vale do Ribeira, São Paulo, Brasil. Rev Saude Publica 21 : 171-187. ).

As a result of the study, CDC-A and CDC-LT were similar regarding to species richness, but distinct in addressing both species composition and abundance. However, the CDC-A sampled a higher number of Oc. scapularis and Ochlerotatus serratus . These species can feed on mammals, including humans and other vertebrates and thus seems to be capable of participating in the transmission cycle of pathogens from rural to urban environments ( Forattini et al. 1989Forattini OP, Gomes AC, Natal D, Kakitani I, Marucci D 1989. Preferências alimentares e domiciliação de mosquitos no Vale do Ribeira, São Paulo, Brasil, com especial referência a Aedes scapularis e a Culex ( Melanoconion ). Rev Saude Publica 23 : 9-19. , Laporta & Sallum 2011Laporta GZ, Sallum MAM 2011. Effect of CO2and 1-octen-3-ol attractants for estimating species richness and the abundance of diurnal mosquitoes in the southeastern Atlantic forest, Brazil. Mem Inst Oswaldo Cruz 106 : 279-284. ). It is noteworthy that only CDC-LT captured specimens of the genus Uranotaenia , corroborating the results of Xue et al. (2008)Xue RD, Doyle MA, Kline DL 2008. Field evaluation of CDC and Mosquito Magnet X traps baited with dry ice, CO2sachet and octenol against mosquitoes. J Am Mosq Control Assoc 24 : 249-252. . Species of the genus Uranotaenia are not anthropophilic and therefore were not attracted to kairomones employees in CDC-A and MMI. These chemicals were developed to attract insects that feed on humans and domestic animals and therefore they are not suitable to sample zoophilic species, for instance, Uranotaenia species that mostly feed upon amphibian blood ( Cupp et al. 2004Cupp EW, Zhang D, Yue X, Cupp MS, Guyer C, Sprender TR, Unnash TR 2004. Identification of reptilian and amphibian blood meals from mosquitoes in an eastern equine encephalomyelitis virus focus in central Alabama. Am J Trop Med Hyg 71 : 272-276. ) that can be reservoirs of the eastern equine encephalitis virus in North America ( Graham et al. 2012Graham SP, Hassan HK, Chapman T, White G, Guyer C, Unnash TR 2012. Serosurveillance of eastern equine encephalitis virus in amphibians and reptiles from Alabama, USA. Am J Trop Med Hyg 86 : 540-544. ).

Laporta and Sallum (2011)Laporta GZ, Sallum MAM 2011. Effect of CO2and 1-octen-3-ol attractants for estimating species richness and the abundance of diurnal mosquitoes in the southeastern Atlantic forest, Brazil. Mem Inst Oswaldo Cruz 106 : 279-284. investigated the potential of using carbon dioxide and octenol combined and separated as attractive in CDC-LT in a preserved Atlantic Forest area, in Cananéia, SP. As a result, authors showed that the addition of CO 2 in the CDC-LT increased both abundance and richness of mosquitoes sampled by CDC-LT. Contrasting, either octenol only or a combination octenol and CO 2 did not improve the results of CDC-LT. It is possible that the low concentration of octenol employed in the traps did not contribute to a synergistic effect with CO 2 . Similar studies carried out in Florida, United States of America, to investigate the attractiveness of chemicals on mosquitoes showed that the performance of CDC-LT increased with the addition of CO 2 ( Kline et al. 1990Kline DL, Takken W, Wood JR, Carlson DA 1990. Field studies on the potential of butanone, carbon dioxide, honey extract, 1-octen-3-ol, L-lactic acid and phenols as attractants for mosquitoes. Med Vet Entomol 4 : 383-391. ). Moreover, the lactic acid added to the CDC-LT increased the potential of the trap to capture Culex nigripalpus , an important vector-borne species in North America.

Thus, MMI and CDC-A seems to be important traps for surveillance to the mosquito species. It is noteworthy that for the control of sucking species or synanthropic vector with potential role of pathogens to humans, the use of MMI, with carbon dioxide and lactic acid, is the most suitable. However, to realisation of collections in places with difficult access or stratification studies, for example, their use may be impaired. Accordingly CDC-A, which uses the same attractive may be an option to replace the MMI, as it can be more easily handled and compared to MMI relative for the ability to collection of the number and composition of the assembly of mosquitoes present in the focus of research.

These studies encouraging for further studies employed MM trap for surveillance of mosquito species involved in the parasite transmission to humans and ecological studies.

Supplementary data 1


Results of the Bonferroni test to verify the statistical significance for the indices obtained in the Rényi diversity index

Supplementary data 2


Species unique to each traps and shared between them

ACKNOWLEDGEMENTS

To LA Sáes, for allowing the collections in Experimental Estation, to the field team from Epidemiological Department of Epidemiology, for helping with field collections, to A Fernandes, for assistance in mosquito identifications, and to G Laporta, for helping in statistical analysis in the R package mvabund.

REFERENCES

  • Bálint M, Tiffin P, Hallström B, O’Hara RB, Olson MS, Fankhauser JD, Piepenbring M, Schmitt I 2013. Host genotype shapes the foliar fungal microbiome of balsam poplar ( Populus balsamifera ). PLoS ONE 8 : e53987.
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Publication Dates

  • Publication in this collection
    06 Dec 2013

History

  • Received
    25 Sept 2013
  • Accepted
    5 Dec 2013
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