Productive Container Types for Aedes aegypti Immatures in Mérida, México

VECTOR-BORNE DISEASES, SURVEILLANCE, PREVENTION

Productive Container Types for Aedes aegypti Immatures in Me´rida, Me´xico ´ N,1 MILDRED P. LO ´ PEZ-URIBE,1 MARI´A ALBA LORON ˜ O-PINO,1 JULIA´N E. GARCI´A-REJO 1 JOSE´ ARTURO FARFA´N-ALE, MARIA DEL ROSARIO NAJERA-VAZQUEZ,2 SAUL LOZANO-FUENTES,3 BARRY J. BEATY,3

AND

LARS EISEN3,4

J. Med. Entomol. 48(3): 644Ð650 (2011); DOI: 10.1603/ME10253

ABSTRACT During 2007Ð2010, we examined which container types in Me´ rida, Me´ xico, are most productive for Aedes aegypti (L.) immatures. Surveys for mosquito immatures followed routine surveillance methodology and container type classiÞcations used by Servicios de Salud de Yucata´n. Our main Þndings were that 1) small and larger discarded containers that serve no particular purpose and therefore can be removed from the environment contribute strongly to larval and pupal production in Me´ rida, and 2) the importance of different container types can vary among sets of residential premises as well as between dry and wet periods. These results may help to guide future implementation in Me´ rida of control efforts that target the most productive container types for Ae. aegypti immatures. Furthermore, if the Patio Limpio cleanup campaign that currently is ongoing in Me´ rida proves successful in removing discarded containers as important immature development sites, then we should see dramatic changes in the most productive container types in the future as the mosquito is forced to switch to other container types, which perhaps also will be easier to include in highly targeted mosquito control interventions. KEY WORDS Aedes aegypti, immatures, productive container types, Me´ xico

The arbovirus vector Aedes aegypti (L.), that transmits the viruses causing dengue, yellow fever, and chikungunya is closely associated with indoor and peridomestic environments (Halstead 2008). The immature stages of the mosquito use a wide range of containers, located indoors or in backyards or other peridomestic settings, as development sites (Focks and Alexander 2006). Efforts to minimize the number of containers available to Ae. aegypti can include physical removal, repositioning or alteration to improve draining (e.g., turning containers upside down or adding holes to drain them), or treatment with control agents such as predators or biological or chemical insecticides. However, due to the wide range of container types that Ae. aegypti can use and the emergence of the “throw-away society” where sundry containers rapidly accumulate in peridomestic environments, it has become increasingly difÞcult for operational control programs to include all containers that are present in surveillance and control activities. This has led to considerable interest in limiting surveillance, control, or both of 1 Laboratorio de Arbovirologõ´a, Centro de Investigaciones Regionales Hideyo Noguchi, Universidad Auto´ noma de Yucata´n, Av. Itza´es No. 490 x 59, Centro, Me´ rida, Yucata´n, Me´ xico CP 97000. 2 Servicios de Salud de Yucata ´n, Calle 72 # 463 por 53 y 55, Centro, Me´ rida, Yucata´n, Me´ xico CP 97000. 3 Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO 80523. 4 Corresponding author, e-mail: [email protected].

immatures to especially productive container types (Focks and Chadee 1997, Focks 2003, Focks and Alexander 2006, Tun-Lin et al. 2009, WHO 2009, Arunachalam et al. 2010). On the surveillance side, this has been accompanied by increasing use in recent years of pupal-based surveillance (e.g., pupae per hectare or pupae per person) that, due to variable and potentially high larval mortality, is considered to more accurately predict abundance of adults compared with larval based surveillance (Focks 2003). One important lesson from the large number of studies that have focused on determining productive container types for Ae. aegypti immatures is that they can differ dramatically between local areas. This has been demonstrated in a series of multicountry studies (Focks and Alexander 2006, Tun-Lin et al. 2009, Arunachalam et al. 2010) and also is evident when comparing the results of studies focusing on individual geographical areas (Moore et al. 1978; Winch et al. 1992; Kittayapong and Strickman 1993; Focks and Chadee 1997; Danis-Lozano et al. 2002; Pinheiro and Tadei 2002; Arredondo-Jimenez and Valdez-Delgado 2006; Barrera et al. 2006, 2008; Bisset et al. 2006; Lenhart et al. 2006; Midega et al. 2006; Morrison et al. 2004, 2006; Romero-Vivas et al. 2006; Chadee et al. 2007, 2009; Hammond et al. 2007; Koenraadt et al. 2007; Maciel-de-Freitas et al. 2007; Barbazan et al. 2008; Manrique-Saide et al. 2008; Troyo et al. 2008; David et al. 2009; Garelli et al. 2009; Lambdin et al. 2009; Tsu-

0022-2585/11/0644Ð0650$04.00/0 䉷 2011 Entomological Society of America

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GARCI´A-REJO´ N ET AL.: PRODUCTIVE CONTAINERS FOR Ae. aegypti IMMATURES

zuki et al. 2009; Kamgang et al. 2010). Furthermore, the most productive container types can change over the year, especially in settings with dry and wet seasons where the importance of containers Þlled by rain, relative to those Þlled by human action, may vary over the year in response to the seasonal rainfall patterns (Pinheiro and Tadei 2002, Lenhart et al. 2006, RomeroVivas et al. 2006, Maciel-de-Freitas et al. 2007, Barbazan et al. 2008, Troyo et al. 2008, Chadee et al. 2009, Lambdin et al. 2009, Tsuzuki et al. 2009). Previous studies from Me´ rida, Me´ xico, on important container types for Ae. aegypti immatures incriminated disposable containers such as tin cans, bottles, and jars for larvae (Winch et al. 1992) and buckets and plastic rubbish for pupae (Manrique-Saide et al. 2008). Here, we present descriptive data, collected as part of studies focusing primarily on indoor infestation by dengue virus-infected Ae. aegypti females, on important container types for Ae. aegypti immatures in Me´ rida among two different sets of residential premises, sampled during March 2007ÐFebruary 2008 and May 2009 ÐJuly 2010, and for dry versus wet periods. Materials and Methods Study Site. Studies were conducted in the city of Me´ rida (population of ⬇800,000) in the Yucata´n peninsula of southern Me´ xico. Mean monthly maximum temperatures in Me´ rida range from 29⬚C in December to 34⬚C in July, and the majority of the rainfall occurs from MayÐOctober with a peak from JuneÐSeptember. Dengue cases may occur throughout the year but are most common from July to October (Loron˜ o-Pino et al. 1993, Garcõ´a-Rejo´ n et al. 2008). Weather data (rainfall and average maximum, mean, and minimum temperature) for the study period were obtained from a weather station at the Me´ rida airport operated by Comision Nacional del Agua. Study Premises and Temporal Sampling Scheme. Examined premises were part of two different research projects in Me´ rida: 1) a study conducted from March 2007 to February 2008, including 880 premises located mainly in the southern and eastern parts of the city, and aiming primarily to determine indoor infestation by dengue virus-infected Ae. aegypti females for dengue patient premises (Garcõ´a-Rejo´ n et al. 2008); and 2) a study conducted from May 2009 to July 2010, including 411 premises located mainly in the southern and eastern parts of the city, and aiming primarily to determine whether insecticide-treated curtains implemented as consumer products in single homes can reduce indoor infestation by dengue virus-infected Ae. aegypti and prevent dengue infections. Although both of these studies were focused in the southern and eastern parts of Me´ rida, there was no overlap between individual premises included for the March 2007 to February 2008 and May 2009 to July 2010 time periods. All houses had electricity and running water and were one-story buildings constructed from concrete. The selection of speciÞc residential premises to examine, and the frequency of mosquito collection on these premises, was driven by the nature of the two

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above-mentioned research projects. In the Þrst study, conducted from March 2007 to February 2008, dengue patient homes were visited, and immatures collected, on a single occasion (Garcõ´a-Rejo´ n et al. 2008). This was done in close collaboration with Servicios de Salud de Yucata´n (SSY), which is the agency responsible for vector surveillance and control in Yucata´n state, and coincided with the date on which SSY Þrst visited the premise of a newly recognized dengue patient to implement mosquito control. Immatures were collected, as described below, just before, or during the SSY visits to the dengue patient premises. In the second study, conducted from May 2009 to July 2010, the premises of study participants were visited on multiple occasions. Immature collections were done during MayÐAugust, September, and November in 2009 and during January, March, May, and July in 2010. The number of times when single premises could be examined for immatures ranged from two to seven (based on lack of access to speciÞc premises during some months or participants dropping out of the study). Mosquito Collection. Surveys for mosquito immatures followed the national Mexican guidelines for surveillance methodology and container type classiÞcation which are used by SSY and other state health agencies in Me´ xico (Manual para la vigilancia, diagno´ stico, prevencio´ n y control del dengue de la Secretaria de Salud de Me´ xico, EA-1 Informe de Exploracio´ n Entomolo´ gica; http://www.pediatria.gob. mx/sgc/manussa_den.pdf). Container types were further grouped as follows: 1) discardable containers Þlled by rain (small discarded containersÑ diversos chicos [e.g., bottles, cans, plastic bags ]; larger discarded containersÑ diversos grandes [e.g., washing machines, refrigerators]; tiresÑllantas), 2) nondiscardable containers Þlled in part by human action (ßower potsÑmacetas; bucketsÑ cubetas), and 3) nondiscardable containers Þlled mostly by human action (cement cisternsÑ cisternas; cement troughs for animal drinking waterÑpiletas; cement troughs for aquatic plantsÑpiletas; cement water tanksÑtanques; large earthen jarsÑtinajas; metal or plastic drumsÑ tambores; plastic containersÑ botes; plastic water tanksÑtinacos; swimming poolsÑpiscinas; vasesÑ ßoreros). Container capacities (volumes) are given in Table 1. The surveys included inspection, by trained entomologists from Universidad Auto´ noma de Yucata´n, of potential container development sites for immatures inside the home and in the backyard or patio. Containers were classiÞed with regards to presence of water, and the numbers of larvae or pupae in waterÞlled containers were counted. This included removing immatures from the containers and counting them, one by one, on a white tray. Subsamples of immatures were identiÞed using stereomicroscopes and published identiÞcation keys (Carpenter and LaCasse 1955, Darsie and Ward 2005). Our previous study from Me´ rida showed that Ae. aegypti accounts for the majority (⬎99.9%) of Aedes immatures collected from container habitats, with the remaining few Aedes im-

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Table 1. Collection of Ae. aegypti immatures by container type from residential premises in Me´rida, Yucatán, Me´xico during March 2007–February 2008 and May 2009 –July 2010 Container characteristics Container type Discardable containers Þlled by rain Small discarded containersa Larger discarded containersa Tires Nondiscardable containers Þlled in part by human action Flower pots Buckets Nondiscardable containers Þlled mostly by human action Vases Cement troughs (aquatic plants) Cement troughs (animal water) Large earthen jars Swimming pools Metal or plastic drums Plastic water tanks Plastic containers Cement water tanks Cement cisterns Total

2007Ð2008 Capacity (liters)

Larvae No.

2009 Ð2010 Pupae

% of total

Larvae

No.

% of total

Pupae

No.

% of total

No.

% of total

⬍5 5Ð20 ⬍5

989 293 135

42.6 12.6 5.8

300 40 40

59.6 8.0 8.0

3,000 3,102 1,736

21.9 22.7 12.7

497 1,045 387

15.3 32.1 11.9

⬍5 5Ð20

216 389

9.3 16.7

50 30

9.9 6.0

1,485 3,200

10.8 23.4

186 822

5.7 25.2

45 88 19 10 33 30 32 24 19 2 2,324

1.9 3.8 0.8 0.4 1.4 1.3 1.4 1.1 0.8 0.1 100

15 15 8 5 0 0 0 0 0 0 503

3.0 3.0 1.6 1.0 0 0 0 0 0 0 100

0 147 412 107 0 238 131 0 0 120 13,678

0 1.1 3.0 0.8 0 1.7 1.0 0 0 0.9 100

0 15 125 22 0 93 39 0 0 26 3,257

0 0.4 3.8 0.7 0 2.9 1.2 0 0 0.8 100

⬍5 20Ð40 20Ð40 40Ð60 ⬎200 200 ⬎200 20Ð100 ⬎200 ⬎200

There was no overlap between residential premises included for the studies conducted in 2007Ð2008 versus 2009 Ð2010. a Small discarded containers include e.g., bottles, cans, and plastic bags, and similar items; larger discarded containers include e.g., washing machines refrigerators, and similar items.

matures belonging to Aedes trivittatus (Wiedemann) (Garcõ´a-Rejo´ n et al. 2008). This is because locally present Aedes species other than Ae. aegypti, Aedes taeniorhynchus (Say), and Aedes trivittatus (Coquillett) (Garcõ´a-Rejo´ n et al. 2008, 2011), very rarely use containers as immature development sites. Aedes albopictus (Skuse), which frequently uses containers as immature development sites and is present in other parts of Me´ xico (Iban˜ ez-Bernal and Martinez-Campos 1994, Casas-Martinez and Torres-Estrada 2003, Mercado-Hernandez et al. 2006, Ponce-Garcia et al. 2009, Villegas-Trejo et al. 2010), has not yet been recorded from Me´ rida or other parts of the Yucata´n peninsula. Data Presentation. Because the designs of the studies during which immatures were collected were driven primarily by factors unrelated to the ideal design of studies examining container productivity in space and over time, we have restricted the presentation to descriptive data and statistical analyses based on summary data. This includes data for overall numbers of Ae. aegypti larvae and pupae collected by container type, and the percentage contribution by container type to all collected larvae or pupae, for the two study periods (Table 1). For the second study period, when individual premises were sampled repeatedly, we also present data for production of immatures by container type grouping (discardable containers Þlled by rain, nondiscardable containers Þlled in part by human action, and nondiscardable containers Þlled mostly by human action) broken down by dry months (6Ð17 mm of monthly rainfall; January and March 2010) versus wet months (129Ð220 mm of monthly rainfall; September and November 2009 and May and July 2010)

(Fig. 1). Statistical analyses were carried out using the JMP statistical package (Sall et al. 2005), and results are considered signiÞcant when P ⬍ 0.05.

Fig. 1. Container contribution to Ae. aegypti larvae and pupae by Þll method during dry and wet periods, September 2009ÐJuly 2010.

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Results

Discussion

Summary Data for Productive Container Types. Comparison of productive container types for premises examined during March 2007ÐFebruary 2008 versus May 2009 ÐJuly 2010, which represent different sets of residential premises in the southern and eastern parts of the city of Me´ rida, underscores the variability in productive container types that can occur in space and over time even within a single city (Table 1). For example, sampling during March 2007ÐFebruary 2008 indicated that small discarded containers accounted for the majority (59.6%) of Ae. aegypti pupal production (Table 1). No other container type exceeded 10% of the pupae collected. In contrast to this result, during May 2009 ÐJuly 2010 small discarded containers accounted for only 15.3% of collected Ae. aegypti pupae; larger discarded containers and buckets were more productive (contributing 32.1 and 25.2% of Ae. aegypti pupae, respectively) than small discarded containers (Table 1). A similar pattern was seen also for larvae (Table 1). Seasonal Changes in Productive Container Type Groupings. For premises sampled from September 2009 to July 2010, we also examined container productivity in relation to monthly rainfall. Two sampling months fell within the dry period (January and March 2010; ⬍20 mm of rain per mo) and four sampling months fell within the wet period (September and November 2009 and May and July 2010; ⬎120 mm of rain per mo). Discardable containers Þlled by rain were important producers of Ae. aegypti pupae during both the dry and wet periods, with an increasing relative contribution from the dry period (45.1% of total pupae collected) to the wet period (56.1%) (contingency table analysis likelihood ratio: ␹2 ⫽ 7.83, df ⫽ 1, P ⫽ 0.005) (Fig. 1). Nondiscardable containers Þlled mostly by human action were more important contributors to pupal production during the dry period (30.6%) compared with the wet period (5.7%) (␹2 ⫽ 91.87, df ⫽ 1, P ⬍ 0.001). Nondiscardable containers Þlled in part by human action contributed more strongly to overall pupae collected during the wet period (38.2%) than for the dry period (24.3%) (␹2 ⫽ 14.18, df ⫽ 1, P ⬍ 0.001). The overall pattern for larvae was similar to that seen for pupae (Fig. 1). Discardable containers Þlled by rain were important producers of larvae during both the dry and wet periods, with an increasing contribution from the dry period (39.9% of total larvae collected) to the wet period (52.4%) (␹2 ⫽ 42.31, df ⫽ 1, P ⬍ 0.001). Nondiscardable containers Þlled mostly by human action were more important contributors to larval production during the dry period (21.1%) compared with the wet period (6.6%) (␹2 ⫽ 146.55, df ⫽ 1, P ⬍ 0.001). Nondiscardable containers Þlled in part by human action had similar relative contributions to larvae collected in the dry and wet periods (39.0 and 41.0%, respectively; ␹2 ⫽ 1.15, df ⫽ 1, P ⫽ 0.28).

In the last decade, there have been numerous reports from various dengue endemic areas on productive container types for Ae. aegypti immatures (see citations given in Introduction). A picture is now emerging where the locally most productive container types often differ between geographical areas. For example, a recent multicountry study found that, in residential settings, cement tanks were the single most important producers of pupae in India and Indonesia, whereas spiritual ßower bowls, drums/barrels, bowls, and buckets/bowls were the most productive container types in Myanmar, the Philippines, Sri Lanka, and Thailand, respectively (Arunachalam et al. 2010). Another multicountry study reported similarly variable results, with the most important container types for pupal production ranging from drums in Venezuela and Kenya to buckets and pots in Mexico; clay jars and toilet tanks in Thailand; drums, tanks, and spirit worship ßower vases in Myanmar; 100 Ð1,000-liter jars in Vietnam; and tires, drums, and waste containers in the Philippines (Focks and Alexander 2006, Tun-Lin et al. 2009). Additional variability in productive container types is observed when comparing residential to nonresidential environments such as commercial properties, public places, and industrial areas (Morrison et al. 2006, Arunachalam et al. 2010). Another issue is the potential role of atypical, overlooked development sites that may be important contributors to Ae. aegypti immatures in some settings, especially after the container types perceived as being most productive have been controlled. For example, atypical or nontraditional development sites (ditches, holes, depressions in ßoors, drains, puddles, plastic tarpaulins, tubing or bags, and rain gutters) were found to contribute to production of Ae. aegypti pupae in Peru (Morrison et al. 2004, 2006), and septic tanks were recognized as important producers of Ae. aegypti in Puerto Rico (Barrera et al. 2008). Furthermore, roof gutters and various subterranean habitats (e.g., wells, drain sumps, and service manholes) have been incriminated as productive sources for Ae. aegypti in Australia (Russell et al. 1996, 1997; Kay et al. 2000; Montgomery and Ritchie 2002; Montgomery et al. 2004). Our study adds to the emerging picture of local variability by comparing productive container types for Ae. aegypti immatures for two different sets of residential premises within the city of Me´ rida. The results also can be compared with those presented by Manrique-Saide et al. (2008) for a third set of residential premises which were sampled in 2003 in Me´ rida, although the container classiÞcation schemes differ in some respects. Notably, the most productive container types for Ae. aegypti pupae differed between these three sets of residential premises in Me´ rida: small discarded containers contributed 59% of pupae for the premises sampled by us from March 2007 to February 2008 (Table 1), whereas larger discarded containers and buckets contributed 55% of pupae for the premises sampled by us from May 2009 to July 2010

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(Table 1), and buckets and plastic rubbish contributed 55% for the premises sampled by Manrique-Saide et al. (2008). For all three sets of residential premises, reaching a contribution to pupal production of 80% required inclusion of at least four container types. These results underscore that local variability in productive container types may occur for residential premises even within a single city. Some of the variability observed by us could have resulted from variable intensity in different years of vector control targeting development sites for immatures. For example, the Patio Limpio cleanup campaign (http://www. cenave.gob.mx/dengue/default.asp?id⫽81), which is ongoing in Me´ rida (and other Me´ xican cities), could have impacted the abundance of discardable containers to different extents based on variable homeowner compliance between sets of premises or between years. Several previous studies have compared productive container types during dry and wet parts of the year (Pinheiro and Tadei 2002, Lenhart et al. 2006, RomeroVivas et al. 2006, Maciel-de-Freitas et al. 2007, Barbazan et al. 2008, Troyo et al. 2008, Chadee et al. 2009, Lambdin et al. 2009, Tsuzuki et al. 2009). Not surprisingly, a trend emerges from these studies toward containers Þlled by human action being more important producers of Ae. aegypti immatures during dry compared with wet periods, whereas objects Þlled by rain such as tires and various small discarded containers gain in importance during the wet period. We classiÞed the container types included in our study into three groupings: 1) discardable containers Þlled by rain, 2) nondiscardable containers Þlled in part by human action, and 3) nondiscardable containers Þlled mostly by human action. This revealed that, as expected, nondiscardable containers Þlled mostly by human action contributed more strongly to both larval and pupal production during the dry versus wet period. Although the relative production of larvae and pupae from discardable containers Þlled by rain increased from the dry to the wet season, these container types (e.g., small discarded containers, including bottles, cans, plastic bags; larger discarded containers, including washing machines, refrigerators; and tires) were strong contributors both during the wet season and dry season. Similarly, Winch et al. (1992) reported that disposable containers such as tin cans, bottles, and jars are important year-round larval production sites for Ae. aegypti in Me´rida. Apparently, enough water to support production of immatures accumulates in containers of these types even during the dry season in Me´rida, when rainfall is sporadic. Perhaps this also may be aided by humans engaging in watering activities, with unintended spillover of water into discarded containers and tires. Our results underscore the importance of determination of the most productive container types during the wet as well as dry periods of the year to ensure that seasonal variability in productive container types is accounted for in container-targeted control efforts. SpeciÞcally targeting the most productive container types for mosquito control in Me´ rida is complicated by that some of the locally most important container

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types are discarded containers that proliferate in the peridomestic environment (Table 1; Winch et al. 1992; Manrique-Saide et al. 2008). Indeed, Winch et al. (1992) noted that effective control of Ae. aegypti in the neighborhood of Me´ rida that they examined would require improved refuse collection services throughout the year. This, together with our demonstration of the importance of discardable containers Þlled by rain as immature development sites for Ae. aegypti in Me´ rida, argues strongly for cleanup campaigns such as the Patio Limpio initiative. If this campaign proves successful in removing discarded containers as important immature development sites, we expect to see dramatic changes in the most productive container types in Me´ rida in the future as the mosquito is forced to switch to other development sites (potentially a combination of currently recognized and new, atypical development sites) which perhaps also will be easier to include in highly targeted mosquito control interventions.

Acknowledgments We thank Carlos Baak, Carlos Estrella, Alex Ic, Roger Arana, Wilberth Chi, Hugo Valenzuela, Iva´n Villanueva, Maria Puc, Victor Rivero, and Carlos Coba (Universidad Autonoma de Yucata´n) for technical assistance. The study was funded by the Innovative Vector Control Consortium.

References Cited Arredondo-Jimenez, J. I., and K. M. Valdez-Delgado. 2006. Aedes aegypti pupal/demographic surveys in southern Mexico: consistency and practicality. Ann. Trop. Med. Parasitol. 100: S17ÐS32. Arunachalam, N., S. Tana, F. Espino, P. Kittayapong, W. Abeyewickreme, K. T. Wai, B. K. Tyagi, A. Kroeger, J. Sommerfeld, and M. Petzold. 2010. Eco-bio-social determinants of dengue vector breeding: a multicountry study in urban and periurban Asia. Bull. WHO 88: 173Ð 184. Barbazan, P., W. Tuntaprasart, M. Souris, F. Demoraes, N. Nitatpattana, W. Boonyuan, and J. P. Gonzalez. 2008. Assessment of a new strategy, based on Aedes aegypti (L.) pupal productivity, for the surveillance and control of dengue transmission in Thailand. Ann. Trop. Med. Parasitol. 102: 161Ð171. Barrera, R., M. Amador, and G. G. Clark. 2006. Use of the pupal survey technique for measuring Aedes aegypti (Diptera: Culicidae) productivity in Puerto Rico. Am. J. Trop. Med. Hyg. 74: 290 Ð302. Barrera, R., M. Amador, A. Diaz, J. Smith, J. L. MunozJordan, and Y. Rosario. 2008. Unusual productivity of Aedes aegypti in septic tanks and its implications for dengue control. Med. Vet. Entomol. 22: 62Ð 69. Bisset, J. A., M. C. Marquetti, S. Suarez, M. M. Rodriguez, and H. Padmanabha. 2006. Application of the pupal/demographic-survey methodology in an area of Havana, Cuba, with low densities of Aedes aegypti (L.). Ann. Trop. Med. Parasitol. 100: S45ÐS51. Carpenter, S. J., and W. J. LaCasse. 1955. Mosquitoes of North America (north of Mexico). University of California Press, Berkeley, CA.

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GARCI´A-REJO´ N ET AL.: PRODUCTIVE CONTAINERS FOR Ae. aegypti IMMATURES

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