208 Journal of Vector Ecology December, 2003 Seasonal prevalence and container preferences of Aedes albopictus in Santo Domingo City, Dominican Republic Carlos J. Pena 1, Guillermo Gonzalvez 1, and Dave D. Chadee 2* 1 National Centre for the Control of Tropical Diseases (CENCET), Ave. Duarte No. 269, Villa Maria, Santo Domingo City, Dominican Republic 2 Insect Vector Control Division, 3 Queen Street, St. Joseph, Trinidad, West Indies * Corresponding author Received 14 March 2003; Accepted 9 May 2003 ABSTRACT: The seasonal prevalence and container preferences of Aedes albopictus (Skuse) were studied in the park, Parque Mirador del Norte in Santo Domingo City, Dominican Republic, from January to December 1994. Tire ovitraps were set along a transect through the park and monitored weekly while two larval surveys were conducted in both the park and surrounding houses using standard entomological methodology. No seasonal pattern of oviposition was observed with similar numbers of positive tire traps collected in the wet and dry season. Most of the positive ovitraps were located in the middle of the park. Within ovitraps, Aedes aegypti (L.), Ae. albopictus, Culex corniger (Theobald), Ochlerotatus albonotatus (Coquillett), and Toxorhynchites sp. were collected. The larval surveys found 7 associated mosquito species, including Ae. aegypti, Ae. albopictus, Ochleotatus mediovittatus (Coquillett), Anopheles albimanus (Weidemann), Culex nigripalpus (Theobald), and Culex quinquefasciatus Say. The Ae. albopictus breeding sites were plastic buckets (4), rock holes (3), and Styrofoam lunch containers (3). We suggest that further studies should be conducted to determine its geographic distribution and vector potential in the Journal of Vector Ecology 28 (2): 208-212. 2003. Keyword Index: Aedes albopictus mosquitoes, seasonal prevalence, container preferences, ovitraps, larval surveys, INTRODUCTION The invasion of Aedes albopictus (Skuse), the Asian tiger mosquito, into the Americas began in the continental U.S.A. with occasional reports on the collection of immatures by Pratt et al. (1946) and Eads (1972) from imported used tires from northern Asia. By 1985, breeding populations of Ae. albopictus were found to be well established in Houston, Texas (Reiter and Darsie 1985, Sprenger & Wuithiranyagool 1986), with further spread by the shipment of infested tires to most states in the east and midwest (Hawley 1988). The invasion pattern was similar in South America, with Ae. albopictus establishing its presence in Sao Paulo, Brazil, and spreading to other states. The source of Ae. albopictus was egg-infested used tires from Southeast Asia imported into Brazil (Hawley 1988). With the establishment of breeding populations in both North and South America, many countries within the Caribbean and Central American regions established Ae. albopictus surveillance programs (Rodhain 1996). Successful interceptions were immediately recorded with collections of immature stages in Santo Domingo City, Dominican Republic (Pena 1993), and on the wharves in Bridgetown, Barbados (Rodhain 1996). In 1993, Ae. albopictus was collected for the first time in the Caribbean region with four adult mosquitoes and over 30 immature stages collected in rock holes and abandoned fast food containers in a large recreational park, Parque Mirador del Norte, located in the southwestern part of Santo Domingo. In the Dominican Republic, Ae. albopictus surveillance was initiated in 1990 with annual surveys conducted throughout the major towns. In August 1993, immature stages of Ae. albopictus were collected from Santo Domingo City, including Rossmil, Mercurio and Autopista Duarte while San Cristobal, Santiago, and Puerto Plata remained free of this dengue vector. These observations suggested that the Ae. albopictus mosquitoes established breeding populations within Santo Domingo City and provided an excellent opportunity to study the population dynamics of this new vector species especially as it has been shown to be a vector of dengue fever in Southeast Asia (Hawley 1988).
December, 2003 Journal of Vector Ecology 209 The present study was conducted to determine the seasonal prevalence and container preferences of Ae. albopictus using tire traps and larval surveys in the recreational area at Parque Mirador, Santo Domingo City, MATERIALS AND METHODS Study area Tire trap surveys for Ae. albopictus were conducted from January to December 1994 in Parque Mirador del Norte, a 1625 hectare recreational area located at the southwestern part of the capital city, Santo Domingo (N 18º 26 20.1 W 69º 57 50.2 ). Delonix regia (Leguminosaea ) is the dominant tree present, followed by Casuarina equisetifolia (Casuarinaceae ) and Senna siamea (Leguminosaea). These trees form a closed canopy which allows little sunlight to penetrate to the ground and is therefore cool and dark in places, especially in the middle of the park (Figure 1). The soil is composed of clay and coral, with numerous rock holes which provide breeding sites for Ae. albopictus mosquitoes. The climate is tropical with temperatures ranging between 22 o C and 28 o C, and rainfall ranging between 1,400 and 1,500 cm/y (Tidwell et al. 1990). The rainfall is heaviest between May and November while the driest period is usually from December to April. Rainfall data for Santo Domingo was provided by the national meteorological services located at the airport in the Trapping Thirty-two tire traps were made from motorbike tires cut into 50 cm arcs, each forming semi-circular shaped pieces, tied at both ends so that they can be filled with Figure 1. Typical Aedes albopictus habitat in Parque Mirador del Norte in Santo Domingo City, Dominican Republic. water. Each trap was filled with 300 ml of tap water and secured to trees by nails 1 m high above ground level. These traps were set along a transect at 100 m intervals through the middle of the park and exposed for one week after which all immature stages were collected and tire traps refilled with fresh tap water. All immatures were collected using pipettes, placed into vials labeled according to trap number, and transported to the CENCET Entomology laboratory where they were counted and identified. Aedes albopictus larvae were identified using the characteristic shape of the comb scales shape, the size of the thoracic spines, and the number of branches in seta 7C on the head of the larvae (O Meara and Gettman 1991).Tire traps were used instead of conventional ovitraps because Ae. albopictus prefer tires, and it was felt that the black color and odors of the rubber enhanced oviposition and ensured the collection of large numbers of mosquitoes. Container preferences Two general larval surveys were conducted in Parque Mirador with all potential breeding sites, both artificial and natural, being inspected in January and October 1994. House-to-house inspections were conducted and every container in the park was examined to determine the number and type of containers which may serve as breeding sites of Ae. albopictus. All larvae and pupae from all containers were collected using standard entomological procedures as outlined by PAHO (1968). RESULTS During 1994, the monthly number of positive tire traps found ranged from 0 to 18, with a mean of 5.1 positive per month. The rainfall totaled 1,219 mm, averaging 80.5 mm/mo in the dry season (December to May) and 123.0 mm/mo in the wet season (June to November) (Table 1). Of the 1,664 tire traps set along the transect, 98 were lost. Five mosquito species were found occupying the remaining tire traps: Aedes aegypti (L.) (74.7%), Ae. albopictus (10.5%), Culex corniger (Theobald) (3.6%), Ochlerotatus albonotatus (Coquillett) (8.7%), and Toxorhynchites sp. (2.5%). A total of 518 Ae. albopictus immatures was collected from 63/1,664 (3.8 %) positive traps (Table 1). The seasonal distribution of Ae. albopictus fluctuated from 0% in March - July to 28% in January 1994. No significant (G=2.3; df.2; P>0.9) differences in the number of positive tire traps were observed between the wet and dry seasons (Table 1). From the 32 traps set along the Parque Mirador transect, tire traps located
210 Journal of Vector Ecology December, 2003 Table 1. Monthly tire trap collections of Aedes albopictus and rainfall patterns in Parque Mirador, Santo Domingo City, Dominican Republic (1994). Months No. tire traps positive/set % positive No. immatures Rainfall (mm) Dry Season December 4/128 3.1 22 74.8 January 18/160 11.6 279 167.9 February 9/128 7.0 36 11.3 March 0/160 0.0 0 94.9 April 0/128 0.0 0 79.1 May 0/160 0.0 0 55.1 Total 31/864 3.5 337 483.1 Wet Season June 0/128 0.0 0 12.2 July 0/128 0.0 0 132.6 August 2/128 1.6 24 105.2 September 7/160 4.5 71 270.0 October 16/128 12.5 19 92.7 November 7/128 5.4 67 123.7 Total 32/800 3.7 181 736.4 Total 63/1,664 3.8 518 1,219.5 Table 2. Container preferences of Aedes albopictus observed within Parque Mirador, Santo Domingo City, Dominican Republic (January and October 1994). Container types No. containers No. positive No. immatures examined containers collected January 1994 Rock holes 25 3 10 Plastic cups 201 0 0 Tanks 21 0 0 Buckets 60 0 0 Styrofoam lunch containers 781 1 4 Tree holes 32 0 0 Cement jars 41 0 0 Total 1161 4 11 October 1994 Tree holes 35 0 0 Tires 3 1 4 Rock holes 90 0 0 Buckets 79 4 150 Tanks 23 0 0 Styrofoam lunch containers 591 2 79 Total 821 7 233 Total 1,982 11 244
December, 2003 Journal of Vector Ecology 211 No. positive 14 12 10 8 6 4 2 0 0 16 32 Tire trap numbers within the middle of the park, in close proximity to the seated areas, were found positive (Figure 2) with over 80% (50 tire traps) containing immature stages of Ae. albopictus. From the larval surveys conducted in the Parque Mirador and surrounding houses (100), 1,982 containers were identified as potential breeding sites with Styrofoam lunch containers (1,372), plastic glasses (201), plastic buckets (139), rock holes (50), and tree holes (67) being the most common. The House index was 2/100= 2.0% positive with 11 positive containers (Container index 11/ 1,982 = 0.6%) and a Breteau index of 11/100= 11.0. The associated mosquito larvae collected included Ae. aegypti accounting for 75.4% of mosquitoes collected, Ae. albopictus (16.5%), Anopheles albimanus (Weidemann) (2.0%), Culex nigripalpus (Theobald) (2.0%), Culex quinquefasciatus Say (2.0%), Oc. mediovittatus (Coquillett) (1.5%), and Oc. albonotatus (0.6%). Plastic buckets (4), rock holes (3), and Styrofoam lunch containers (3) were the breeding sites of Ae. albopictus (Table 2). All the breeding sites were found concentrated in the middle of the park where the seating accommodations have been provided for public use. DISCUSSION No. positive Figure 2. Distribution of positive tire traps along the transect in Parque Mirador, Santo Domingo City, Dominican Republic (1994). These results clearly demonstrate that Ae. albopictus mosquitoes have established at least one breeding population within the capital city, Santo Domingo, The invasion pattern followed very closely that observed in Houston, Texas, with the establishment of Ae. albopictus population within the Parque Mirador, a wooded area providing suitable breeding habitats, both natural and artificial, human blood from joggers and workers having lunch in the park, and the closed canopy of the trees providing the shade, temperature, and humidity preferred by this mosquito species (Moore 1999). Although the Dominican Republic imported over 3,764,553 used tires over the period 1988 to 1995 from Japan and over 59,957 used tires over the period 1989 to 1994 from the USA (Reiter 1998), one of the three tires inspected was found positive for Ae. albopictus in the Parque Mirador area. It is possible that other egginfested imported tires were redistributed throughout the However, in 1994 the surveillance program for Ae. albopictus was discontinued, thus we may only speculate that pockets of infestation may be festering throughout the We recommend that an intensive country-wide Ae. albopictus surveillance program be conducted to determine the geographical distribution of this mosquito species. The seasonal distribution of Ae. albopictus monitored using tire traps showed no positive correlation with rainfall and this may be due to the low numbers of positive traps and immatures recovered. However, these results suggest that tire traps may be a suitable monitoring device similar to conventional or modified ovitraps (Fay and Eliason 1966). It is possible that in 1994 the tire traps may have been monitoring a small population not well established in the Dominican Republic, and the low numbers of immatures collected in the tire traps and larval surveys may reflect this fact. In addition, eggs adhering to the sides of these tire traps were not counted and may be a source of error in counting the immature stages of Ae. albopictus. To date, it has not been determined whether the Ae. albopictus population in the Dominican Republic originated from the temperate regions of Asia or tropical Southeast Asia. However, since tires were not imported from Southeast Asia but rather from the continental U.S.A. and Japan, it is quite possible that the Dominican Republic invasion came from the U.S.A. and the imported strain may be temperate in origin. This temperate strain has been observed to spread very slowly in lower latitudes, and the Florida invasion patterns shows rapid selection in the Ae. albopictus populations along the southern border, especially as day length triggers egg diapause. That is, diapause prevents the hatching of eggs, development of immatures, and the production of adults for dispersal to other areas (O Meara and Gettman 1991). The results of this study show a low Ae. albopictus population level which might be due to the fact that the temperate strain is a slow invading species and not well adapted to tropical latitudes, thus making the Dominican Republic an ideal testing ground for understanding the dynamics of invasion of this temperate strain.
212 Journal of Vector Ecology December, 2003 The collection of associated species within larval habitats and tire traps suggests that the Ae. albopictus population is not well established in the Dominican Republic because in northern Florida the Ae. aegypti population declined drastically and rapidly with the introduction of the Asian tiger mosquito (O Meara and Getttman 1991). The patterns observed in the Dominican Republic may again be associated with Ae. albopictus strain differences because over 75% of all mosquitoes collected in the tire traps and 75.4% found during the larval surveys were Ae. aegypti. Further studies are needed in the Dominican Republic to characterize the strain of Ae. albopictus, the invasion patterns post 1994, and vector competence especially as dengue is endemic in the Acknowledgments We thank Angel Solis, Gabino Guzman, Dorian Montero, and Gilda Ventura at CENCET, Santo Domingo, Dominican Republic for assistance in the laboratory and field. In addition, we thank Dr. J.M. Sutherland, University of Dundee, Scotland, UK and Dr. C. G. Moore, Colorado State University, for reviewing a draft of the manuscript. REFERENCES CITED Eads, R.B. 1972. Recovery of Aedes albopictus from used tires shipped to United States ports. Mosq. News 32:113-114. Fay, R.W. and D.A. Eliason. 1966. A preferred oviposition site as a surveillance method for Aedes aegypti. Mosq. News 26:531-535. Hawley W.A. 1988. The biology of Aedes albopictus. J. Am. Mosq. Contr. Assoc. (Suppl. 1) 1-40. Moore C.G. 1999. Aedes albopictus in the United States: Current status and prospects for further spread. J. Am. Mosq. Contr. Assoc. 15:221-227. O Meara, G.F. and A.D. Gettman. 1991. The Asian Tiger Mosquito in Florida. A Florida Mosquito Factsheet, December 1991. PAHO. 1968. Aedes aegypti Eradication Policy Guidelines for Planning of PAHO/WHO Programs. Washington, D.C. Pan Am. Hlth. Org. 60 pp. Pena, C.J. 1993. First report of Aedes (Stegomyia) albopictus (Skuse) from the Vect. Ecol. Newsletter, 24: 68. Pratt, J.J., R.H. Heterick, J.B.Harrison, and L. Haber. 1946. Tires as a factor in the transportation of mosquitoes by ships. Milit. Surg. 99: 785-788. Reiter, P. 1998. Aedes albopictus and the world trade in used tires. 1988-1995: the shape of things to come? J. Am. Mosq. Contr. Assoc. 14:83-94. Reiter, P, and R.F. Darsie Jr. 1985. Aedes albopictus in Memphis, Tennessee (USA): An achievement of modern transportation? Mosq. News 44:396-399. Rodhain, F. 1996. Problems posed by the spread of Aedes albopictus. Bull. Soc. Pathol. Exot. 89:137-140. Sprenger, D. and T. Wuithiranyagool. 1986. The discovery and distribution of Aedes albopictus in Harris County, Texas. J. Am. Mosq. Contr. Assoc. 2:217-219. Tidwell, M.A., D.C. Williams, T. Carvalho, C.J. Pena, T.A. Gwinn, D.A. Focks, A. Zaglal, and M. Mercedes. 1990. Baseline data on Aedes aegypti populations in Santo Domingo, Dominican Republic. J. Am. Mosq. Contr. Assoc. 6: 514-522.