Temporal distribution and spatial pattern of abundance of the Rift Valley fever and West Nile fever vectors in Barkedji, Senegal

The temporal distribution and spatial pattern of abundance of mosquito vectors of Rift Valley fever (RVf) and West Nile fever (WNf) were studied during the 2005 and 2006 rainy seasons at Barkedji, Senegal. Mosquitoes were collected every two weeks with CDC light traps with dry ice at 79 sites including temporary ponds, barren, shrubby savannah, wooded savannah, steppes, and villages at different distances (between 0 and 600 m) from the nearest pond. The temporal distributions of these vectors varied between 2005 and 2006 and were positively correlated with rainfall for Aedes (Aedimorphus) vexans Patton, with rainfall after a lag time of one month for Culex (Culex) poicilipes (Theobald) and Culex (Culex) neavei Theobald. All the vectors had their highest abundances and parity rates between September and November. The highest vector abundances were observed in the barren and temporary ponds. The distance of trap location to the nearest ponds was negatively correlated to the abundance of the vectors. Taking into account the linear regression equations, it was predicted that mosquitoes would not disperse and be collected by the light trap, up to 1,500 m to the nearest ponds. The implications of these findings in the epidemiology and control of RVF and WNF at Barkedji are discussed. Rift Valley fever (RVf) and West Nile fever (WNf) are two emerging mosquito-borne diseases of medical and veterinary importance. RVf virus (RVfv) is a phlebovirus of the family Bunyaviridae (Murphy et al. 1995). It causes an anthropo-zoonosis that affects mainly cattle, sheep, and goats leading to abortions among pregnant females and high mortality in newborn kids and lambs (Easterday 1965). Humans are generally infected by contact with blood, body fluids, or organs of infected animals and by mosquito bites. In humans, RVf manifestations are usually asymptomatic, but severe cases with complications such as encephalitis, hepatitis, and hemorrhagic syndromes associated with high mortality rates have been reported (Laughlin et al. 1979, Jouan et al. 1988). WN virus (WNv) is a flavivirus of the family Flaviviridae. WNv is maintained in nature in enzootic cycles involving birds and ornithophilic mosquitoes (Hayes et al. 2005). WNf may affect humans and horses under certain environmental conditions (Bunning et al. 2001). Infections in humans and horses are usually asymptomatic or mild, but cases of serious meningitis and encephalitis with high mortality rates were observed (O'Leary et al. 2002). RVf and WNf viruses are both transmitted by several species of mosquitoes, mainly of Aedes and Culex genera (Traore-Lamizana et al. 2001, Molaei et al. 2006). In the last decades, several animal and human outbreaks of RVF occurred in Africa and the Middle East (Hoogstraal et al. 1979, Faye et al. 2007, Woods et al. 2002). WNF outbreaks were also reported in Africa, Europe, the U.S.A., and Asia (Murgue et al. 2002, Mostashari et al. 2001). In Barkedji, many mosquito species (Fontenille et al.1995, Diallo et al. 2000), as well as humans and livestock (Wilson et al. 1994, Thonnon et al. 1999), have been found to be associated with RVfv and WNfv. The first documented RVf epizootic and epidemic in Senegal occurred in the Senegal River basin in 1987 with an identification of 200 human cases and an estimation of more than 1,000 human cases (Jouan et al. 1988). After that, several serologic surveys in human and animals indicated that RVf virus continuously circulates in Senegal (Saluzzo et al. 1987, Thonnon et al. 1999). WNv has been isolated from two humans and several mosquito species in Senegal and seroprevalence of 5.5%, 78.3% and 80% has been recorded in birds, horses, and humans, respectively (Traoré-Lamizana et al. 2001, Chevalier et al. 2006, 2009). These active viral circulations emphasize the need for more efficient surveillance and control measures. In this process of developing better surveillance tools, Vignolles et al. (2009) produced an early warning system by combining specific GIS, remote-sensing, entomological and livestock data. This tool may serve to produce a dynamic risk map but needs to be validated and extended to other vectors like Cx. poicilipes and Cx. neavei. A better understanding of the bio-ecology of the vectors could assist in the implementation of these measures. Mosquito species with high population densities in Barkedji and which were found most often infected with RVFV and WNV in Africa are Culex (Culex) poicilipes (Theobald), Aedes (Aedimorphus) vexans Patton, and Culex (Culex) neavei Theobald. All these vectors breed in temporary ponds that are flooded after the first rainfalls (Fontenille et al. 1998, Traore-Lamizana et al. 1994, 2001, Ba et al. 2005, 2006). The maximum flight distances of Ae. vexans and Cx. poicilipes from these ponds was 620 and 550 m respectively (Ba et al. 2005). But the flight range of Culex (Culex) neavei is still unknown. In Senegal, although the associations among these viruses and mosquitoes, humans, and animals are frequent, the mechanisms by which vertebrates become infected (i.e., vector-borne or as aerosols) remain unclear. The assumption that the enzootic and epizootic/epidemic cycles of the diseases are due to the movement of infected mosquitoes from ponds to villages has been examined in a field study (Ba et al. 2005), but in this case, the movement of mosquitoes occurred over relatively short distances and the study was limited to non-infected populations of Cx. poicilipes and Ae. vexans. Moreover, it is unknown if infected and non-infected vectors have similar flight behaviors. Further information about the ecological environments associated with each vector species, the flight range of each species, and the radius of risk-of-infection of a given population of vectors is crucial for planning vector control campaigns to be certain that treatment is implemented over adequate areas for each environment. Moreover, since 1990, most studies of the bio-ecology of mosquito vectors in Barkedji, a village in northern Senegal, have focused on temporary ponds and to a lesser extent on villages and did not explore other areas inhabited by known vertebrate hosts of the viruses. These studies were also carried out on a monthly basis, which may have underestimated the temporal fluctuations of mosquito populations, and were limited mainly to Cx. poicilipes and Ae. vexans (Fontenille et al. 1998, Traore-Lamizana et al. 2001). The aims of this work were to analyze the temporal distribution and the spatial pattern of abundance of RVF and WNF vectors in relation to environmental factors like rainfall, habitat characteristics, and distance to larval breeding sites. Our specific goal was to identify the period and area at risk of transmission of these diseases. The study was carried out within a radius of 13 km centered on the Barkedji village (14° 47′-14° 53'W, 15° 13′-15° 20'N) during the 2005 to 2007 rainy seasons. This area (Figure 1) belongs to the Sahelian biogeographic domain characterized by a shrubby vegetation, hot dry climate, short rainy season (from June to October), and long dry season (November to May), with annual rainfall ranging from 300 to 500 mm. Many temporary ponds flood at the beginning of the rainy season and are the main source of water for herders and their livestock in this period. People grow mainly millet during the rainy season and herd sheep, goats, and cattle year-round. Family groups and their herds may become seasonal nomads, temporarily relocating for a few months during which they use grass huts for shelter. Location of the study site. Different landscapes classes were defined by remote sensing and geospatial analyses from a SPOT 5 satellite image. The radiometric and geometric corrections were made by SPOT Image (http://www.spotimage.com.cn/spot5/ensavoirplus/eng/plus_niveau.html). The description of the vegetation classes is based on a combination of the FAO (1997) and Anon (1956). Thus the following landscape classes were selected for the study: 1) temporary ponds, 2) villages, and 3) vegetation classes of steppes, shrubby savannah, wooded savannah and barren. Adult mosquitoes were collected using CDC light traps with dry-ice in 79 sites selected to include all the landscape classes. All the sampling sites were geo-referenced with a hand-held GPS receiver and the Euclidean distance (in meters) from each sampling site to the nearest pond was estimated based on the spatial map of the study area. Mosquitoes were collected for one night in each site on a bi-weekly basis from June to December, 2005, July to November, 2006. For each sampling night, one trap was set in each site at about 50 cm above ground level. Traps were set in the late afternoon and were retrieved the following morning. Collections were transported to the field lab where mosquitoes were killed in the freezer and transferred to a chill table. Mosquitoes were identified morphologically using the identification keys of Edwards (1941) for the culicines and Diagne et al. (1994) for the anophelines. Every two weeks, more than 50 specimens of each vector species were dissected to evaluate parity based on the presence of ovarian dilations, as described by Detinova (1962). The temporal distribution, expressed as mean number of females per trap per night (F/T/N), was calculated for each vector every two weeks from July to December, 2005 and from June to November, 2006. The associations between the temporal distribution of the vectors and rainfall were evaluated by the Pearson correlation. The mean numbers of mosquitoes collected annually in the different landscapes classes, expressed as mean number of females per trap per year (F/T/Y), were calculated and compared for each vector. Means were compared by ANOVA followed by Fisher PLSD tests. Statistical analyses were done after a log transformation log10 (n+1) of the data to normalize the distribution and minimize the standard error. To study the possible concentration of females near ponds (larval breeding sites), the Pearson correlation between abundance and distance to the nearest pond was investigated by grouping all the sites in seven distance intervals (0, 100, 200, 300, 400, 500, and 600 m) from trap site to the nearest breeding site. A simple linear regression analysis was also conducted to evaluate the impact of distance to the nearest ponds on the mosquito's vector abundance. Temporal mean parity rates (number of parous females divided by number of dissected females in percentage) of the vectors were determined. Data were analyzed using StatView 5.0®. A list of the mosquito species collected and their relative abundances during the study are presented in Table 1. A total of 14,908 mosquitoes, belonging to eight genera and 39 species were collected in 790 trap-nights in 2005. In 2006, 14,630 mosquitoes, belonging to seven genera and 38 species were collected in 636 trap-nights. Among females, Culex poicilipes (31.6%) was the most abundant species in 2005, followed by Aedes vexans (12.9%), Cx. neavei (11.4%), Ae. ochraceus (10.2%), and Mansonia uniformis (7.9%). In 2006, Ae. vexans (29.7%) was the most abundant mosquito, followed by Cx. poicilipes (25.1%), Cx. neavei (10.9%), Ae. ochraceus (10.7%), and Ma. uniformis (6.9%). The highest female to male ratio was that of Cx. poicilipes (148.9), followed by Ae. vexans (37.7) and Cx. neavei (9.4) in 2005. These ratios were 433.5 and 265.3 for Ae. vexans and Cx. neavei respectively in 2006. No Cx. poicilipes males were collected these years. The rainfall and temporal patterns in mosquito populations in 2005 and 2006 are shown in Figure 2. The rainfall patterns differed between the two years. Culex poicilipes appeared at the beginning of the rainy season in July, 2005 (1.2 F/T/N), with two peaks at 18.3 and 9.6 F/T/N in early September and late October, respectively. In 2006, Cx. poicilipes also appeared at the beginning of the rainy season in June (0.01 F/T/N) and had an important peak in early October (23.7 F/T/N). Culex neavei was captured at the end of July, with 0.4 F/T/N and 0.6 F/T/N in 2005 and 2006, respectively. This species had a single peak, with 9.9 F/T/N in late October in 2005. In 2006 it had two peaks in late September (12.2 F/T/N) and in late October (5.2 F/T/N). In 2005, the highest Ae. vexans peak was observed at the beginning of the rainy season in July, with 24.3 F/T/N. This species reached a second peak at the beginning of October, with 8.1 F/T/N. In 2006 the highest peak of Ae. vexans populations was observed later in late September (51.2 F/T/N). The first peak was observed in late July, with 5.2 F/T/N. Temporal distribution of RVFV and WNV vectors during the 2005 and 2006 rainy seasons at Barkedji, Senegal. The Pearson correlation analysis has shown a positive and significant correlation between temporal abundance and rainfall for Ae. vexans for both years (r= 0.64, P= 0.03 in 2005 and r= 0.62, P= 0.02 in 2006). This analysis showed a positive and significant correlation between temporal abundance and rainfall for Cx. poicilipes and Cx. neavei after one month, except for Cx. neavei in 2005 (r= 0.04, P= 0.9). Mean vector abundances in the different landscape classes are shown in Table 2. The Anova showed a statistically significant difference among the different classes for Cx. poicilipes in (F= 7.25; df = 5, 137; P < 0.0001), Cx. neavei (F= 10.7; df = 5, 137; P < 0.0001), and Ae. vexans (F= 3.54; df = 5, 137; P= 0.005). The highest Cx. poicilipes abundances were observed in the barren and temporary ponds, which were statistically comparable, followed by shrubby savannah, wooded savannah and steppes. Culex neavei abundances were statistically higher in barren, temporary ponds and wooded savannah compared to the other classes. Barren had the highest abundance of Ae. vexans followed by temporary ponds, shrubby, and wooded savannah. Villages and steppes had the lowest abundance of this species. The average vector abundance according to the trap distance from nearest pond are presented in Figure 3. The Pearson correlation analysis has shown a strong negative and significant correlation between average abundance and trap distance from nearest ponds for Cx. poicilipes (r=– 0.95, P= 0.0004) and Cx. neavei (r=– 0.97, P < 0.0001) but not for Ae. vexans (r=– 0.55, P= 0.22), Relationship between vector abundance and distance to the nearest pond during the rainy seasons of 2005 to 2007 at Barkedji, Senegal. Regression analysis of the abundance of the mosquito vector in relation to distance from the nearest ponds produced the equation: log (abundance + 1) = 1.394 – 0.001× distance for Ae. vexans, log (abundance + 1) = 1.356 – 0.001 × distance for Cx. neavei, and log (abundance + 1) = 1.686 – 0.002 × distance for Cx. poicilipes. Taking into account these equations, the predicted distances from which no mosquitoes would be collected by the light trap will be 1,394 m, 1,356 m and 843 m for Ae. vexans, Cx. neavei and Cx. poicilipes, respectively. The temporal variations in the vectors’ parity rates were statistically different in 2005 and 2006 (Figure 4). Culex poicilipes parity rates presented a peak in early August and a plateau between late September and late November before becoming zero at the end of December in 2005. In 2006, all Cx. poicilipes females were between late June and early this species showed two parity peaks in late August and October Culex neavei females showed parity peaks in 2005, with and of the dissected females parous in late early November, and late December, respectively. were two parity peaks in late August and late October 2006, with and of parous females, respectively. Aedes vexans also showed parity peaks in 2005, with and of the dissected females parous in late July, late and late October, respectively. The single of Ae. vexans collected in June 2006 was This vector showed two parity peaks at in late August and early Temporal of the RVFV and parity rates during 2005 and 2006 rainy seasons at Barkedji, Senegal. the species of the Barkedji mosquito populations was high in found species than studies in this area (Wilson et al. 1994, Traore-Lamizana et al. 2001). These may be by the sampling but also by in the mosquito by environmental Our study has as have studies in the area (Fontenille et al. 1998, Ba et al. 2005), a of Cx. poicilipes and Ae. vexans in the mosquito Culex poicilipes the in 2005, in 2006 it was Ae. vexans. This of between Cx. poicilipes and Ae. vexans at Barkedji has been observed on a basis between and (Traore-Lamizana et al. 2001). The for this as well as impact on the epidemiology of RVf and unknown and needs It is that, into account the data presented and data (Traore-Lamizana et al. 2001, Ba et al. 2005), all RVfv were isolated at Barkedji during the years Ae. vexans the mosquito The peaks of Ae. vexans abundance were observed later in the in late September in 2006 compared to 2005. This could be by the difference in rainfall patterns between 2005 and 2006. Culex the end of the season during the two years. This between Aedes and Culex has been described for Barkedji (Traore-Lamizana et al. and for Africa et al. It could be by the of these two the Aedes the season as that as as the are the Aedes populations their peak at the beginning of the rainy The Culex the dry season as females that at the beginning of the rainy The population to peak All the vectors had their highest parity rates between September and October, which is the period outbreaks of RVf and WNf occurred at The spatial of mosquitoes is important for understanding epidemiology as well as for the most control it where and an could if a of that vector RVf and WNf vectors were collected in all the study study has shown that they barren and temporary ponds than villages and the classes. This is in with the of Ba et al. in a study of the of Cx. poicilipes and Ae. vexans that they were within This that these vectors on the vertebrates hosts near temporary ponds. are many birds, and other animals the ponds. herders the and their livestock use barren for shelter. night, also the ponds after their In a study on the pattern of these Ba et al. have found that Ae. vexans mainly on Our study also showed that abundances of RVf and WNf vectors are to trap to the ponds which are their larval breeding the mosquito abundance with distance from the nearest pond. is for a between the abundance of a specific vector species in a site and the distance of the site to that breeding several studies have shown a negative correlation between mosquito abundance and distance to larval et al. 2005). In a study on Ae. vexans and Cx. poicilipes, in the Ba et al. found that the number of mosquitoes with distance from the ponds. The maximum distances from this that females were were 620 and 550 m for Ae. vexans and Cx. poicilipes, respectively. This difference in the flight range of the two vectors was also observed in Culex poicilipes have the range compared to the other vectors. This is important into account that Cx. poicilipes is the mosquito in which the highest numbers of RVfv and WNv have been isolated in Senegal et al. 2005, Ba et al. 2005, Traore-Lamizana et al. 1994, 2001). It is also the species in which RVfv have been isolated during outbreaks in West Africa et al. 2005, Faye et al. vector control during outbreaks will a area of of this species. Mosquitoes disperse to and sites. these are is It is for this that the vectors are the ponds. The spatial of the mosquitoes near the ponds has The first is that the hosts to the ponds would be more to be by these vectors and are at more risk of were numbers of hosts that serve as source near the ponds, the mosquitoes did not have to disperse long distances from their larval the distance of a from the ponds is an important that could affect risk of infected by viruses. This is by the that a higher than number of cases of River virus have been reported in from areas near larval et al. et al. and for transmission in et al. The second of the spatial of the vectors near the ponds is that the vertebrate hosts of the viruses in these environments and be examined data also the that than mosquitoes the within and among of the implications of study is that vertebrate hosts be vector by at distance from mosquito larval et al. et al. shown in this study in the Barkedji and their livestock could be by more than 1,500 m from the nearest ponds. the other the spatial pattern of vector abundance the need to vector control than more et al. the identification of areas with high or numbers of vectors may control to be focused in areas with the risk of transmission et al. The control of RVf and WNf vectors in the Barkedji area the ponds and the 1,500 m area in the of an infected mosquitoes ponds is not to the of in other areas infected are more to is an of and it early of the virus before human and vertebrates are It is done mainly by entomological and surveys et al. et al. 2005). Among other the of a surveillance to the early presence of an on the of the in a mosquito et al. 1995). For a more efficient surveillance of RVf and WNf virus at Barkedji, light traps and be at the ponds and the area at their as other et al. that areas with high vector abundance will be associated with a higher risk of that at Barkedji, and the area to the ponds, are at higher risk for RVf and WNf the livestock of the herders and the are at higher risk to be infected with RVf and WNf than the population and their the livestock of the herders and the that at the ponds and at night the population and their in most vector-borne transmission cycles are and the of vector mosquitoes is not correlated with transmission et al. 1999). In this study showed that the spatial pattern of RVf and WNf vectors is in the area of These vectors remain to ponds and this area is at a higher risk of RVf and WNf Our could be in the to map areas at risk of RVf and WNf environmental and and will be to better this the first in the planning and of vector control and for their The also from the for with remote sensing and geospatial This work was by is by the as The of this are the of the and not the of the