Background

Environmental disturbances such as deforestation, urbanization and/or pollution have been widely acknowledged to play a key role in the emergence of many infectious diseases. Mosquito surveys provide valuable information on occurrence, distribution, prevalence and species diversity of various mosquitoes in an area which assumes significance due to their public health importance (Senthamarai Selvan et al., 2015a), they prefer to breed in both standing and slowly running water bodies (Sundaravadivelan et al., 2011). Mosquitoes are considered as serious nuisance pests and vectors of many dreadful diseases like dengue, chikungunya, yellow fever, malaria, and filariasis both in rural and urban areas and recently Zika virus transmission was recorded in Dharmapuri district of Tamilnadu and Ahmadabad in Gujarat.

Mosquitoes are known to respond a range of environmental conditions, including disturbance, which can have their colonization (Williams, 2006; Carver et al., 2009). In India, climate change represents as additional stress on ecological and socioeconomic systems that are already facing tremendous pressures due to rapid urbanization, industrialization and economic development (Sumana et al., 2006). Among the potential effects of climate change on human health, the impact of vector borne diseases has attracted increasing attention in recent years. Theni district is a suitable place to carryout studies on mosquito and mosquito-borne diseases. Since warm temperature and rainfall in the area favour the development and survival of mosquitoes and humans are heavily exposed to mosquito biting. More ever, Theni not only holds rich biodiversity of mosquitoes but has nearly half of its population living and working in hilly areas and maintain close contact with hills, creating situation of epidemiological process. Though being aware of the presence of climate disturbance in Theni, data about the potential of mosquito abundance and their distribution in connection with climate change is meager.

The epidemiology of arboviruses is significantly influenced by climate. Temperature, rainfall pattern and humidity are important factors in the life-cycle of arthropod vectors, the arbovirus transmitted and the reservoirs (Rogers and Randolph, 2006; Semenza and Menne, 2009; Paz, 2015). Temperature increase causes an upsurge in the growth rates of mosquito populations, decrease the interval between blood meals, shorten incubation periods from infection to infectiousness in mosquitoes and accelerate the virus evolution rate (Baba et al., 2012). Above-average precipitation can also lead to a higher abundance of mosquitoes and increase the potential for disease outbreaks in humans (Landesman et al., 2007). A good knowledge of the changes and fluctuations that occur in natural populations of mosquito vectors is very important in the prevention and control of arboviral diseases in order to identify high and low risk transmission zones and periods (WHO, 1975). The physico-chemical parameters viz., temperature, pH, alkalinity, conductivity, TDS are the important factors in mosquitoes occurrence. The larval aquatic stage is an important part of the mosquito life cycle and habitat requirements may strongly influence the distribution and abundance of many species involved in pathogen transmission (Mckeon et al., 2013; Senthamarai Selvan et al., 2015b). Breeding habitats have associated with distribution and abundance of mosquitoes and mosquito-borne diseases in many parts of the world, especially in warm and tropical climatic regions.

The purpose of this entomological observations were to determine present mosquito species and their possible abundance changes, population dynamics and diversity of species in an area which assumes significance due to their public health, medical and veterinary importance (Pandian et al., 1997; Senthamarai Selvan and Jebanesan, 2014a). Hence the present study was carried out to determine the presence of mosquito’s distribution based on the meteorological variables and physicochemical parameters in their breeding habitats of selected sites of Theni district, Tamilnadu, India.

1 Materials and Methods

1.1 Study areas

The survey on the water-holding containers supporting mosquito breeding in the semi-urban and the surrounding rural areas at 10 sites, namely Periyakulam, Jayamangalam, Theni urban, Verapandi, Andipatti, Varusanadu, Kambam, Kumili, Bodinayakanur rural and Uttamapalayam in the Theni district (77.4768⁰ E and 10.0104⁰ N) of Tamilnadu, India (Figure 1). Selection of the study areas in Theni district was based on previous documentation of establishment of vector-host arbovirus transmission cycles. The vegetation of the study localities consists mainly of residual native forests and grassy areas. The vertebrate species include reptiles, amphibians, birds and rodents. Natural water bodies are present close to the study areas and used water dispose often creates artificial breeding sites where immature mosquitoes can develop.

1.2 Mosquito collection and meteorological data acquisition

The containers such as cess pits, drainage, ponds, cess pools, tree holes, septic tanks, plastic cups and discarded tyres were examined for the presence of mosquito larvae. The surveys were carried out twice in each of the six months viz., July, August, September, October, November and December, 2015. Adult mosquitoes were collected using carbon dioxide-baited Centre for Disease Control (CDC) light traps and human landing collection (HLC) methods. HLC is the only effective method for sampling sylvatic Aedes and the most appropriate method for determining human risk of infection (Diallo et al., 2012). The two methods were combined in order to have representative catch of the different mosquito species present at the farms. For each site, one CDC trap was set close to the cattle shed while trained mosquito scouts collected mosquitoes from study locations. Collectors were dressed in thick clothing materials with hoods, hand gloves and socks. They collected mosquitoes landing on their socks covered legs to minimize exposure to mosquito bites. Immatures were collected by using suction tube and pipette (Jebanesan et al., 2013; Senthamarai Selvan et al., 2013). The collection was done once weekly on each farm for a 5 hours trapping periods from 16:00 to 21:00. Weather data namely rainfall, relative humidity and temperature were taken into consideration throughout the study period. This was obtained from the Regional Meteorological Centre (RMC), Chennai and Tamilnadu Agricultural University (TNAU), Coimbatore. The collected mosquitoes (immature and adults) were brought to the laboratory and identified by the keys of Barraud (1934) and Christopher (1933).

1.3 Physicochemical characteristics

Water samples were collected monthly twice during July – December 2015 from all selected mosquito breeding sources of all the study areas by small sterilized 250 mL container. The bottles were covered with perforated caps, labelled properly with date and place of collection. The collected water samples were carried carefully and transferred to the laboratory. Within 8-10 hrs after collection the breeding water characteristics of pH, dissolved oxygen (mg/L), conductivity (µS/cm), total dissolved solids (mg/L), turbidity (NTU), were recorded using standard procedure (APHA, 2005). Temperature was measured by mercury thermometer at the time of sample collection (Senthamarai Selvan and Jebanesan, 2014b).

1.4 Data analysis

The abundance of container breeding mosquitoes was calculated by larval density and container index. The overall collected mosquitoes (immature and adults) diversity and dominant species was calculated by Shannon-Weiner diversity index and Simpson’s dominance index respectively.

1.4.1 Larval density

Larval density is the study of numerical strength of a species in relation to the total number of individuals of all the species and can be calculated as:

1.4.2 Shannon and Weiner (1949) diversity Index

The following formula was used for calculating the diversity of mosquitoes:

Where, H’ = Shannon index of diversity; Pi = the proportion of important value of the ith species; (pi = ni/N) ni is the important value index of ith species and N is the important value index of all the species.

1.4.3 Simpson’s (1949) dominance Index

The following equation was used to calculate the mosquitoes dominance:

Where, As D increases, diversity decreases and Simpson’s index was therefore usually expressed as 1 – D or 1/D.

2 Results

A survey was conducted in Theni district for the collection of larvae and adult mosquitoes during the period from July 2015 to December 2015. The collected mosquitoes were identified in the species level. A total of 21 species belongs to 7 genera of 1226 individuals were identified (Table 1). Among the 21 species, 9 species belonging to highly polluted water habitat comes under Culex and Anopheles genus viz., Cx. mimulus, Cx. pseudovishnui, Cx. quinquefasciatus, Cx. vishnui, Cx. pallidothorax and Cx. minutissimus, An. stephensi, An. culiciformis and An. maculatus. Among all the collected species Culex was collected frequently in most of the habitats with polluted water and the result indicates that the Culex were most abundant species in Theni district. The genus Armigeres includes only one species Armigeres subalbatus and it belongs to Armigeres sub genera, which was less abundance in this area followed by Ochlerotatus grenii and Orthopodomyia flavithorax (Figure 2).

Mosquito breeding in the selected containers did commence with less in number until the month of September. This is due to lack of rainfall during this month in the study areas. Among the collected individuals of 1226 mosquitoes (immature and adults) 816 were immatures and 410 adults. Breeding in the habitat started in July but less in number and subsequently increased mosquito’s population and the high peak of mosquitoes was recorded in post monsoon season of late October, November and December months. This suggests that frequency and pattern of rainfall affect the composition and distribution of larvae and pupae in containers, animal foot prints, rocky pools, stream slow flowing, discarded tyres, tree holes etc (Figure 3). This finding was supported by Gubler et al. (2001); Afolabi et al. (2010). Water temperature of 23.2°C-25.6°C is optimum for mosquitoes breeding with relative humidity of 83-86%.

The fresh water habitat genus Aedes dominate next to Culex spp., it includes four species viz., Ae. aegypti, Ae. albopictus, Ae. subalbopicta and Ae. psedoalbopictus. Immediately after rain Aedes species were emerged in peak because of more availability of fresh water in discarded tyres, small containers in and around human dwellings. When compared with An. stephensi and Cx. quinquefasciatus, Ae. aegypti was predominantly occur in the rainy months of November and December (Figure 4). Cx. quinquefasciatus species were dominantly recorded in waste waters (cess pits and cess pools). Based on the diversity index analysis, high number of Shannon-Weiner diversity value 0.1596 was recorded for Culex and 0.1564 for Aedes species, the species of Culex (0.1270 Simpson’s dominance index) were dominantly recorded in polluted water bodies (Table 2).

Different species of mosquitoes showed variation in selection of breeding sites and resting places at Theni district. An idea of this can be obtained from the varied larval habitat and resting places of the larval and adult mosquitoes respectively. The different breeding habitats such as discarded containers, tree holes, animal foot prints, cattle sheds, bamboo stump, spring pool, stream slow flowing, leaf axil and cement tanks were observed in the different stations of the Theni district based on the availability and non-availability of the breeding habitats. Discarded containers (357), Cement tanks (289) and tree holes (214) were the most favourable habitats for mosquito breeding in selected study localities (Figure 5). Totally 10 different types of 300 breeding sources were searched for mosquitoes survey among them 193 were identified as mosquito breeding places within that 816 immatures were collected. The high number of larval density and container index were recorded in the discarded containers (105.18; 20.0) followed by tree holes (94.30; 17.0) (Table 3).

The physicochemical factors viz., pH, conductivity, turbidity, nitrate, total dissolved solids, total suspended solids, phosphate and dissolved oxygen of different breeding habitats in various stations of Theni district were studied and they are influenced in the selection of breeding habitats of different mosquitoes. The pH of 6.8-7.1 ± 0.52 and dissolved oxygen of 6.18 ± 0.04 mg/L were shown the suitable conditions for Anopheles and Culex mosquitoes breeding. The turbidity is influenced in the presence of Aedes mosquitoes, if the value of turbidity is less than 50 NTU are more suitable for fresh water habitat mosquito species (Table 4). The breeding water pH is mainly depending on the meteorological variations. Immediately after rain the pH is in basic, if the pH is at acidic in nature the Aedes mosquitoes is very less in number.

3 Discussion

In Tamilnadu, increased rainfall was recorded in the months of late October and November; it may increases the larval habitat and vector population by creating a new habitat in many of the localities. While excessive rain would eliminate habitats through flooding, thus decreasing the vector population (Mishra et al., 1984; Geevarghese et al., 1994; Gajana et al., 1997). Present study demonstrated that the diversity and breeding habitats of mosquitoes in Theni district. The combined mosquito population gradually build up during September and October, reached its maximum during November and December and declined to a low level during July and August months. Percentage of dengue, JE and malaria vectors collected during November and December was high as 11.25%, 6.36% and 5.95% respectively. The pattern of physicochemical factors affects larval habitats and vector population size (Tyagi et al., 1997; Kelly et al., 2004; Senthamarai Selvan et al., 2015a).

The physico-chemical factors and environmental variables are influencing the distribution of adult and larval mosquito populations (Smith et al., 2004). However, the containers are the major substrates for supporting the production of mosquitoes in containers after rainy or monsoons observed in the present study. The species from Culex and Aedes are dominant and widely distributed in study sites. This finding is correlated with previous observations that the higher number of Culex and Aedes species have recorded in forest areas (Amr et al., 1997; Sinka et al., 2011).

The population trends shown by the various mosquito species during the work may provisionally be taken as a guide to their seasonal variations. It was not to say what factors were critical for the abundance or scarcity of a particular species in a given area, since the answer demands critical investigation of the factors affecting a population and such studies were not undertaken during the present work. As for example, Ae aegypti and Ae. albopictus were very less in the month of July but after that both population gradually increased up to December which indicated both species were active at monsoon and post monsoon seasons. Similar studies were also observed by Ahmed et al. (2007) and Makesh Kumar et al., (2015). In contrast Ae. aegyptii and Ae. albopicts was present in much greater numbers in the immature forms, with only a few adults, probably because it bites during the day, Ae. aeypti has a high ecological valence and inhabits wild, rural and urban environments, while in Asia and some Pacific Islands (Senthamarai Selvan and Jebanesan, 2016). It is the vector for dengue fever. The pH of the breeding water in the present study ranged from 6.8 to 7.1 showed a positive correlation with the larval density. The survival of Cx. quinquefasciatus and Ae. aegypti larvae was found to be the maximum in the pH range of 7.1 and 6.5-6.9 respectively (Umar and Don Pedro, 2008). The breeding habitat characteristics were found to exert a significant influence on the abundance of container-breeding mosquitoes in the study areas in Theni district, Tamilnadu.

Adult and immature forms of Cx. quinquefasciatus were also abundant in study sites of Theni. The most common larval habitats used by this species were human waste water and industry waste water with exposed internodes, showing the species ability to colonize different environments, weather natural or artificial. In urban environment Cx. quinquefasciatus breeds in polluted water collections rich in organic matter (Nguyen et al., 2013). It is the primary vector of bancraftian filariasis in some of Theni district and also southern India and has the potential to transmit various arboviruses as well as cause a nuisance to the human population because of its anthropophilic behaviours and its high abundance in urban areas (WHO, 2011).

When exposed to the rain, receptacles such as cans, discarded tyres and water tanks become breeding sites for mosquitoes. In India Ae. aegypti has taken advantage of the population habit of allowing such breeding sites to develop, leading to thousands of dengue cases annually. In the present study, several other species in addition to Ae. aegypti were found in artificial breeding sites, including species of the genera Culex (Culex sub genera), Oclerotatus, Armigeres, Orthopodomyia and Anopheles. This may indicate both adaptations to human changes to the environment as well as an opportunistic response to the availability of these breeding sites.

Increased abundance of mosquitoes in warm-rainy months (October and December) occurred along the six months of study. An area in temperature and rainfall tends to accelerate mosquito development and lead to greater availability of breeding sites for many species of mosquitoes (Franklin and Whelan, 2009). Water availability, temperature and light are strong drivers of the development of mosquitoes and the regulation of their population densities (Senthamarai Selvan et al., 2016). Thus, the effects of such environmental changes are particularly evident in mosquito-borne diseases. For example, the mosquito vector of dengue fever, Aedes aegypti has been associated with urbanization and deforestation (Jebanesan et al., 2013; Senthamarai Selvan and Jebanesan, 2014c).

In addition to domestic water storage containers, Ae. aegypti breeds in a plethora of waste containers such as discarded tyres, empty metal cans, plastic containers, bottles, jars and old automobile bodies. Household water storage is likely to change with intensive educational programs. Indoor waste jars produced more pupae per house than all the other containers combined. The infestation rate of covered containers was significantly higher than that of uncovered containers, perhaps because loose-fitting lids allowed entrance of gravid females to the attractive, darkened interior of the container. In some places outdoor water jars with covers were found to be ingested significantly more than those without covers. Some of the measures like filling up of all the defective ground surfaces with sand, mud or cement, wrap up disused tyres properly or puncture them to prevent water being trapped, changing or removing water in flower vases or saucers underneath potted plants at least once a week will definitely prevent breeding in these areas (Senthamarai Selvan and Jebanesan, 2016).

4 Conclusions

Industrial development, urbanization, improper agricultural etc., have increased the population of mosquitoes much beyond their natural levels. The association of vector species with different study sites of Theni district was documented. The nomadic communities annually migrate with livestock and there is high level of interaction between humans, wildlife, livestock and mosquito vectors in the migration routes. The findings of this study therefore demonstrate the potential vulnerability of nomadic communities to infection by arboviral diseases transmitted by mosquito vectors. This calls for comprehensive mechanisms of vector control and management.

Authors’ contributions

PSS conducted both the field and laboratory study and wrote the manuscript. AJ designed and supervised the entire experiment. JS, KM, SK, MV assisted in field collections. GD contributed in statistical analysis and field collections. All authors agree with manuscript results and conclusion; finally the authors read and approved the final manuscript.

Acknowledgements

The authors are grateful to the University Grants Commission for providing financial assistance under UGC – Major Research Project, UGC Ref. letter No: 42-558/2013 (SR) dated 22.03.2013 and also acknowledge the Professor and Head, Department of Zoology, Annamalai University for facilities provided.

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