Species composition, larval habitats, seasonal occurrence and distribution of potential malaria vectors and associated species of Anopheles (Diptera: Culicidae) from the Republic of Korea
© Rueda et al; licensee BioMed Central Ltd. 2010
Received: 7 October 2009
Accepted: 17 February 2010
Published: 17 February 2010
Larval mosquito habitats of potential malaria vectors and related species of Anopheles from three provinces (Gyeonggi, Gyeongsangbuk, Chungcheongbuk Provinces) of the Republic of Korea were surveyed in 2007. This study aimed to determine the species composition, seasonal occurrence and distributions of Anopheles mosquitoes. Satellite derived normalized difference vegetation index data (NDVI) was also used to study the seasonal abundance patterns of Anopheles mosquitoes.
Mosquito larvae from various habitats were collected using a standard larval dipper or a white plastic larval tray, placed in plastic bags, and were preserved in 100% ethyl alcohol for species identification by PCR and DNA sequencing. The habitats in the monthly larval surveys included artificial containers, ground depressions, irrigation ditches, drainage ditches, ground pools, ponds, rice paddies, stream margins, inlets and pools, swamps, and uncultivated fields. All field-collected specimens were identified to species, and relationships among habitats and locations based on species composition were determined using cluster statistical analysis.
In about 10,000 specimens collected, eight species of Anopheles belonging to three groups were identified: Hyrcanus Group - Anopheles sinensis, Anopheles kleini, Anopheles belenrae, Anopheles pullus, Anopheles lesteri, Anopheles sineroides; Barbirostris Group - Anopheles koreicus; and Lindesayi Group - Anopheles lindesayi japonicus. Only An. sinensis was collected from all habitats groups, while An. kleini, An. pullus and An. sineroides were sampled from all, except artificial containers. The highest number of Anopheles larvae was found in the rice paddies (34.8%), followed by irrigation ditches (23.4%), ponds (17.0%), and stream margins, inlets and pools (12.0%). Anopheles sinensis was the dominant species, followed by An. kleini, An. pullus and An. sineroides. The monthly abundance data of the Anopheles species from three locations (Munsan, Jinbo and Hayang) were compared against NDVI and NDVI anomalies.
The species composition of Anopheles larvae varied in different habitats at various locations. Anopheles populations fluctuated with the seasonal dynamics of vegetation for 2007. Multi-year data of mosquito collections are required to provide a better characterization of the abundance of these insects from year to year, which can potentially provide predictive capability of their population density based on remotely sensed ecological measurements.
Anopheles mosquitoes of the Republic of Korea (ROK) belong to subgenus Anopheles in three groups, namely Hyrcanus, Barbirostris and Lindesayi. The Hyrcanus Group comprises about 30 species worldwide, of which six species are known in the ROK, namely Anopheles belenrae, Anopheles kleini, Anopheles sinensis, Anopheles sineroides, Anopheles pullus and Anopheles lesteri[1, 2]. The other two species belong to the Barbirostris Group (Anopheles koreicus) and the Lindesayi Group (Anopheles lindesayi japonicus) . Preliminary data suggest that An. pullus and An. kleini are the primary vectors of Plasmodium vivax malaria near the demilitarized zone (DMZ), while An. sinensis is a secondary vector . Females of An. sineroides and An. belenrae have also been found positive for P. vivax by enzyme-linked immunosorbent assay (ELISA) and polymerase chain reaction (PCR), respectively (TAK, unpublished data). Anopheles lesteri (= An. anthropophagus) is a major vector of malaria in China ; however, its vectorial capacity is unknown in the ROK. The other remaining two Anopheles species are not considered to be malaria vectors in the ROK .
Recent studies [2, 5, 6] have reported occurrence data of mosquito species from different areas in the ROK. In this study, we conducted comprehensive monthly (May to October) larval collections from selected habitats at three distant locations (Munsan, Hayang and Jinbo). The objectives of this study were to determine the species composition, habitats, seasonal occurrence and geographic distributions of members of the Hyrcanus Group and other group-species from representative areas in the ROK. Monthly satellite-derived normalized difference vegetation index (NDVI) data for the collection sites were compiled to determine the seasonal patterns of larval abundance from various habitats in relation to the background ecological conditions. Previous studies [7–11] have shown that the emergence of various disease vectors and pests including mosquitoes, rodents and locust, tends to follow the flush green vegetation. Therefore, monitoring the ecological conditions can provide valuable information on mosquito population dynamics for use in ecological niche modeling
Specimen collection and identification
Relationship among habitats and locations based on the mosquito species composition
Seasonal occurrence of Anopheles species from three selected locations
Monthly larval surveys of Anopheles species were conducted from three locations, namely Munsan (MU, Gyeonggi Province), Jinbo (JI, Gyeongsangbuk Province), and Hayang (HA, Gyeongsangbuk Province) (Figure 1). The larval sampling techniques (using larval dipper and tray), as mentioned above, were used to collect larvae from various habitats (AC, DE, DI, DR, GP, PR, RP, SM, SW, and UC). For each above location, the same habitats (collection sites) were sampled for mosquito larvae monthly from May through October.
Relationship between normalized difference vegetation index (NDVI) data and mosquito larval population densities from various habitats in three locations
The NDVI data used in this study were derived from the atmospherically corrected 8-day surface reflectance Moderate Resolution Imaging Spectroradiometer (MODIS) product MOD09A2 , which has a spatial resolution of one kilometer. In order to derive monthly near cloud-free data, we combined the original 16-day data into ~32-day data to create monthly maximum-value composites for 2007 . These monthly data sets were required to compare against mosquito species data that were collected on a monthly time step. Monthly NDVI anomalies were calculated by subtracting the monthly composite data for the 2007 growing season from their respective long-term means covering the period 2000-2008 to determine if there were any site differences from long-term ecological patterns.
Mosquito larval density data were grouped and totaled according to proximity to each other resulting in 15 locations with numerous unique collection sites. Of the 15 locations mentioned above, only three (Hayang, Jinbo, and Munsan) contained complete records for the six months (May through October). The location analyses for NDVI and anomaly values were restricted to these three (Figure 1). A three pixel by three pixel window surrounding each location was used to extract NDVI values. NDVI values were then compared to Anopheles larval densities.
Results and discussion
Relationship among habitats and locations based on the species composition
Like An. sinensis, the two major malaria vectors in the ROK, An. kleini and An. pullus, were commonly collected from rice paddies, irrigation ditches and ponds. Non-Hyrcanus Group species, such as An. koreicus and An. lindesayi, were usually collected from swamps, and stream margins (including stream inlets and pools), respectively. A previous study  indicated that overwintering larvae of An. lindesayi were found along the stream margins and stream pools of moderate to fast flowing streams, while first and second instars were collected in abundance in the late fall among shaded mountain stream eddies and margins. Some larvae (n = 66; 17% of total collected from all locations sampled) of An. lindesayi were also collected from rice paddies. However, those rice paddies were apparently not the primary habitats of this species. Sames et al suggested that during heavy rains, stream pools may flood and some An. lindesayi larvae maybe washed down to rice-growing areas.
Seasonal occurrence of Anopheles species from three locations
In Jinbo areas (Figure 6B), a total of 1,897 Anopheles larvae from five species (An. belenrae, An. kleini, An. lesteri, An. pullus, and An. sinensis) were collected from five larval habitats (DI, PR, RP, SM, and SW). Overall, An. pullus was the most frequently collected species, followed by An. sinensis, An. kleini, An. belenrae, and An. lesteri. As in Munsan, An. pullus populations were highest in May, but in Jinbo the population peak of An. kleini was much later, occurring instead in August. Anopheles sinensis populations were high from June to October, with peak populations during August. Anopheles kleini populations peaked in October (Figure 6B).
In the Hayang area (Figure 6C), a total of 1,860 Anopheles larvae from four species (An. belenrae, An. kleini, An. pullus, and An. sinensis) were collected monthly from five larval habitats (DE, DI, RP, SW, and UC). Anopheles sinensis was the dominant species from May to October, followed by An. kleini, An. belenrae and An. pullus. Peak populations of An. kleini, An. sinensis and An. belenrae were in August, September and October, respectively, while An. pullus was collected only in October (Figure 6C).
Relationship between normalized difference vegetation index (NDVI) data and mosquito larval population densities from various habitats in three locations
Remote sensing data are commonly used to identify ecological conditions associated with vector-borne diseases especially mosquito vectors [8, 23]. Most of these data were derived from measurements made by the Advanced High-Resolution Radiometer instrument aboard the National Oceanographic and Atmospheric Administration series of polar orbiting satellites. Measurements in the visible red and near infrared bands on this instrument are of specific relevance to ecology. The spectral signature of plant canopies is characterized by a strong chlorophyll absorption in the red portion of the spectrum and a very high reflectance in the near infrared portion. This unique spectral response of vegetation makes it possible to differentiate vegetation from other surface materials remotely. Derived NDVI values range between -1 to +1, with values below zero indicating absence of vegetation and those above zero showing increasing amounts of green vegetation. Precipitation and green vegetation dynamics are a major determinant of the life cycles of insects in a wide range of environments [9, 24].
Remote sensing data are useful to identify conditions favorable for larval mosquito development, due to their preference for vegetated and humid areas. The distribution of mosquitoes is partly related to land use factors such as the presence or absence of wetlands, the type of surrounding vegetation, elevation and agricultural land use . Many of these environmental factors can be mapped using remotely sensed data, and the normalized difference vegetation index (NDVI) can be used to explore or explain the relationship between mosquito population densities and vegetation/water seasonal patterns. Little is known about the use of remotely sensed data to estimate mosquito distributions in the ROK, except the initial work of Sithiprasasna et al. Data on NDVI values and NDVI anomalies may be useful to predict the potential geographical distribution of Anopheles vectors and related species in the ROK. They may also be considered in developing ecological niche models for mosquito distributions [25, 26], or to improve other existing statistical and related models.
In summary, the Anopheles larval populations fluctuated with the seasonal dynamics of vegetation for 2007. The peak in the mosquito populations coincided with the peak vegetative season in July - August (Figures 9A, C, E). During that period the landscape was more homogenous, creating more widespread conditions related to increased populations of mosquitoes over a much larger area than in the spring or the fall. However, in order to be able to accurately predict mosquito populations, the 2007 data are insufficient as they only reflect ordinary or average conditions. It is, therefore, necessary to have a sample of at least three to four years of mosquito population density data in order to compare the seasonal conditions and Anopheles populations over several years, and also to discern any differences that would provide predictive capability.
Finally, any geographical approach to sampling the natural habitats that includes all possible vector habitats, would lead to significant improvements of disease prevention and control programs . Knowledge of Anopheles species composition from various breeding habitats, and the seasonal fluctuations of larval and adult populations from specific habitats and locations in the ROK, in addition to remote sensing data, will help in developing effective malaria and mosquito control strategies.
The species composition of Anopheles larvae varied in different habitats at various geographical locations in the ROK. However, the higher numbers of species (seven out of eight) were collected from the rice paddies and streams (particularly margins, inlets and pool). Only An. sinensis larvae were collected from all ten habitat groups surveyed. Cluster analysis for the positive habitat sites (combined habitats and locations), based on species composition, showed two distinct basal clusters, with one cluster composed of An. lindesayi habitats, and the other cluster, the habitats of the other seven An. species. Anopheles larval populations fluctuated or increased with the seasonal dynamics of vegetation for 2007, as observed in Munsan, Jinbo and Hayang. Multi-year data of mosquito collections are required to provide a better characterization of the abundance of these insects from year to year which can potentially provide predictive capability of their population density based on remotely sensed ecological measurements.
Thanks go to A. Driskell and G. Harrison (Laboratory of Analytical Biology, Smithsonian Institution) for conducting PCR/sequencing of some mosquito samples; personnel of the 5th Medical Detachment, and staff of 65th Medical Brigade, U.S. Army, ROK, for field collections of mosquito specimens; and J. Pecor and WRBU staff for curatorial help. Special thanks go to D. J. Brambilla (Research Triangle Institute, Research Triangle Park, NC) for statistical analysis; and G. Bieler (RTP, NC), C. Lim (WRAIR) and V. Sherwood (WRAIR) for statistical and related support. We are grateful to F. Ruiz, C. R. Summers and B. P. Rueda for helpful reviews of the manuscript. Funding for this work was provided by the Center for Health Promotion and Preventive Medicine, Global Emerging Infections Surveillance and Response Systems, Silver Spring, MD. This research was performed under a Memorandum of Understanding between the Walter Reed Army Institute of Research and the Smithsonian Institution, with institutional support provided by both organizations. The opinions and assertions contained herein are those of the authors and are not to be construed as official or reflecting the views of the Department of the Army or the Department of Defense.
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