Background

Over the last decade there had been a dramatic increase in the emergence and re-emergence of vector-borne viral diseases (VBD) (Sudeep et al., 2008; Manimuda et al., 2008; Angel et al., 2008; Gubler et al., 2010; Sudeep et al., 2011; Dash et al., 2013; Kumawat et al., 2014; Bueno-Mari et al., 2015). Though the spread of VBDs depends on various factors like distribution and abundance of vectors, vector-host interactions and complicated vector-pathogen-host interactions, research has revealed the role of climatic factors in altering VBD transmission patterns (Shope, 1991; Epstein, 1998; Rieter, 2001; Gould et al., 2009; Lafferty, 2009; Roiz et al., 2014). It is getting established that climate change is affecting propagation of vectors, especially mosquitoes which in turn is driving the spread of VBDs (Monaghan et al., 2016).

Abundance, distribution and longevity of mosquitoes depend on the environmental /climatic parameters like temperature (maximum and minimum), rainfall and relative humidity. High abundance of mosquitoes has proved to be a prelude to epidemics (Lafferty, 2009; Kumawat et al., 2014). Temperature along with changes in rainfall pattern and humidity have influenced the rapid development of the vectors, their survival and vector competency (Rogers et al., 2006). In the last decade, chikungunya virus has re-emerged in an explosive form in 2004 and caused massive outbreaks in the Indian Ocean islands (La Reunion, Comoros, Mauritius, Seychelles etc), and subsequently in India and Southeast Asian countries (Schuffenecker et al., 2006; Tsetsarkin et al., 2007). Similarly, there has been a surge in the occurrences of other mosquito borne viral diseases like Dengue and Japanese encephalitis in India and South Asia (Dash et al., 2013) along with epidemics being reported from the Americas (Benelli et al., 2016). Most recently, the emergence and global spread of Zika virus has caused considerable damage in terms of human health and economy (Mourya et al., 2016).

Knowledge of mosquito abundance in any geographical location is essential for understanding the spread of vector borne diseases, evaluation of potential threats and possible interventions as mosquito control measures. This necessitates investigation of mosquito abundance and seasonal dynamics. Though India has a massive burden of vector borne diseases like malaria, dengue, chikungunya, a few to name, studies on mosquito distribution and dynamics is limited in scope and numbers (Murthy et al., 2010; Pandey et al., 2015). Country-wide data for India is not available and mosquito distribution of Pune has not been investigated recently.      

India being geographically and climatologically diverse, there is a need to investigate the distribution of mosquitoes and its abundance from different parts of the country, especially in regions where dengue and chikungunya are becoming endemic. Temperature, rainfall, humidity and land-use, are known important drivers of mosquito population dynamics and mosquito-borne disease risk (Lindblade et al., 2000; Koenraadt et al., 2004; Afrane et al., 2006; Patz et al., 2006; Stresman et al., 2010; Bomblies et al., 2012). These factors, in combination with intervention strategies, determine the dynamics of local mosquito populations and the intensity of transmission of mosquito-borne diseases.

Changing land use (urbanization, construction work, industrialization and increase in agriculture practices) and monsoon patterns in Pune region (Kantakumar et al., 2016), especially Pune city in the last ten years have resulted in ecological changes (Environmental survey for Pune, online TERI 2017). This with enhanced spread of dengue and chikungunya over the last decade is a major cause of concern due to continued impact on public health. This necessitates investigation on the distribution and seasonal variability of mosquito population in the Pune city. This study will be of help to understand the density and distribution of mosquito population in the Pune urban areas along with the seasonal variability.

In the present paper we report the results of a first ever survey conducted to understand the abundance, composition and dynamics of mosquito population in the Pashan area of Pune city, India over 6 months covering the South West monsoon and Post-monsoon seasons in 2016.

1 Materials and Methods

1.1 Location and climate

The study was conducted in the Pashan suburban area of the Pune City (18° 32" N and and 73° 51" E), Maharashtra state, India (Figure 1).

Pune city has an altitude of 560 m (1,840 ft) above sea level and located on the leeward side (Eastern slope) of the Sahyadri (Western Ghats) mountain range, which marks the western margin of the Deccan plateau. It is a hilly city with undulating landscape. The highest hill is Vetal Hill, rising to 800 m (2,600 ft) above the sea level. Just outside the city, the Sinhagad fort is at an altitude of 1,300 metres (4,300 feet), located on the Singhagad range.

As per the Koppen classification (Critchfield, 1983; Peel et al., 2007; Rubel et al., 2011), Pune has a tropical wet and dry (bordering semi-arid tropical) climate type with rainfall occurring in the South West Monsoon (June/July to September) and dry for rest of the year. Summer day temperature may be as high as 41°C (April -May) and winter minimum temperature usually falls to 8°C (January). There are four seasons for the Indian subcontinent, namely, South West Monsoon (SW Monsoon from June/July to September), Post-Monsoon (October-November, an intermediate between end of monsoon and winter), Winter (December - February) and Pre-monsoon season (March - May/June, is spring and summer untill the SW monsoon arrives). Owing to its altitude, climate in Pune is moderately cold and wet (average temperature ~ 25.3°C for July/August).

The Pashan region of the Pune Metropolitan Area is a region with mixed neighborhood consisting of wide streets, apartment blocks, residential posh bunglows with gardens and a lot of green cover. There is a hillock, popularly called Pashan Hills, which marks the North-western limit of Pashan region. This hillock is covered with dry-deciduous forest type vegetation similar to all hills in and around Pune. Medium-sized trees along with shrubs constitute majority of the vegetation, while diversity of grasses (herbaceous species) is at its peak during the South West Monsoon season (June-September). This hill is surrounded by densely populated apartments and streets. Pashan lake, marks the South-western limit of Pashan. It should be noted that this region was integrated into Pune city in 2001 followed by rapid urbanization during 2001-2005 as agricultural and non-agricultural fallow lands were converted into planned urban neighborhoods.

1.2 Mosquito collection

Mosquitoes were collected using CDC sentinel traps and were operated from dusk to dawn. Time of operations extended from one hour before sunset to one hour after sunrise, hence covering the dawn and dusk activity period for mosquitoes (especially Aedes species). Traps were set up in 5 fixed locations in the Pashan area of Pune city. These included: i) a private bungalow with garden, ii) a populated apartment facing the main road, iii) a populated apartment sharing boundary to the Pashan hillock (described above), iv) a densely populated apartment (lower economic group) adjacent to the Pashan Lake and v) authors' institute campus (Government office set up) facing  main road.

Outdoor trapping took place every week once at each location. Trapped mosquitoes were transported to the laboratory, identified, pooled and stored at -80°C. Pooling of mosquitoes was based on gender and location. Species identification was undertaken using the standard taxonomic keys (Barraud, 1934; Knight et al, 1977). Pools of Aedes mosquitoes by species were considered for virus isolation.

1.3 Virus isolation

Attempts to isolate virus was restricted to Aedes species only. The method described by Sudeep et al. (2011), was followed. In brief, individual pools of mosquitoes were triturated in 1ml MEM (Minimum Essential Medium, Gibco, USA), clarified by centrifugation at 5000 rpm for 10 min at 4ºC. The supernatant was filtered with 0.22 µm filter (Milipore, India) and inoculated over Vero E6 cell line in 24 well plates (Nunc, Denmark). The cultures were observed daily for the exhibition of cytopathic effects.

1.4 Meteorological data

Meteorological data was recorded daily from the website of Indian Meteorological department (IMD) and the weather bulletins issued by IMD. Maximum and minimum daily temperatures (MXT and MNT respectively), daily rainfall (RF) and maximum and minimum relative humidity (mxRH and mnRH respectively) were recorded. We calculated the daily average temperature (AVT) and daily Diurnal temperature range (DTR, which is the difference between MXT and MNT for a particular day). For all parameters, fortnightly averages were calculated. Daily sunrise and sunset times were also recorded.

1.5 Statistical analyses

Statistical analyses were performed using the R software package. Graph was plotted and imagery executed in MS Excel. Mathematical calculations were performed in MATLAB.

1.6 Study design

The study was undertaken with a view to determine the composition of mosquito population and to ascertain the variation in mosquito population with meteorological parameters, if any, covering two seasons: South-West Monsoon (July to September) and Post-Monsoon (October -November) in 2016 in Pashan area of Pune. Mosquitoes were trapped weekly in dusk to dawn collection at fixed locations in the study area using CDC sentinel traps. Collected mosquitoes were identified to ascertain the composition and mosquito abundance (in terms of fortnightly averages of counts per trap). To study the effects of environment, mosquito abundance was compared with the fortnightly averages of meteorological parameters: maximum temperature (MXT), minimum temperature (MNT), average day temperature (AVT), diurnal temperature (DRT), relative humidity and rainfall. Correlation between climatological parameters and mosquito counts were determined by statistical analyses using the R software package.

2 Results

2.1 Mosquito composition

A total of 3081 mosquitoes were collected during July to November 2016 and their species composition was determined. The mosquitoes belonged to 21 species across four genera viz., Aedes, Anophelus, Culex and Armigerus. Among these, the genera Culex was most diverse in terms of species (8), followed by Anopheles (6) and Aedes (6) (Table 1). The top four most abundant species for the period July to November included Aedes vittatus (33.3%), Aedes albopictus (14.1%), Culex quinquefatiacus (15.3%) and Aedes vexans vexans (9.9%). Culex giledus (7%), Anopheles subpictus (4.3%) and An vegas (2%) in were also found in substantial numbers. Five specimen each for the following species were obtained during the SW monsoon season (July - September), i.e., Anopheles annularis, Culex bitaeniorhynchus and Culex pseudovishnui. Aedes lineotopennis, Aedes pseudotaeniatus, Anopheles barbirostris, Anopheles culicifacies, Culex vishnui and Culex fuscanus. Armigerus subalbatus mosquitoes were found in in negligible numbers (4.4%) throughout the study period. Only one specimen of Culex fuscitarsis was found during the study.

The variation of the top four most abundant species over the study period has been indicated in Figure 2. The populations of Ae vittatus, the most abundant during the SW Monsoon season, gradually decreased in the post-monsoon season (October to November). Similar was the case with Ae vexans vexans as the population peaked in July and decreased gradually till October. Ae albopictus was detected in October but their populaiton decreased at the end of November. The population of Culex quinquefasciatus remained steady (showed less fluctuations across the two seasons) throughout the study period (Figure 2).

It should be noted that after the onset of monsoon in Pune in mid-June 2016, the prevailing weather conditions over the last half of June included only 2-3 rainy days. Rest of the days was very windy with intermittent clouds, sunshine and scanty rains. Hence, trapping did not result in meaningful collections.

2.2 Mosquito abundance and meteorological parameters

To study the association between the mosquito abundance and meteorological parameters, we made a season-wise analysis. Mosquito abundance in terms of the number of mosquitoes per trap (fortnightly averages, M) were correlated with the maximum and minimum temperatures, Relative Humidity and rainfall for 20 weeks from 1st July 2016 to 30^th November 2016. Since trapping between 15^th-30^th June did not result in meaningful collections, this period has been excluded from the mathematical analyses.

A) SW Monsoon Season (July- November 2016)

i) Temperature and mosquito abundance

The number of mosquitoes per trap (fortnightly averages, M) were correlated with the maximum and minimum temperature (MXT and MNT respectively). Figure 3 shows the variation of mosquito count with temperature for the SW Monsoon season. The Pearson's correlation coefficient for M vs MXT was found to be r = ˗ 0.79883 with p-value = 0.0566 (95% confidence interval (˗0.9770; 0.03618)). The Pearson's correlation coefficient for M vs MNT was found to be r = 0.77561 with p-value = 0.06988 (95% confidence interval (˗ 0.09702; 0.97405)). With the average daily temperature, the mosquito count showed negative correlation, r = ˗ 0.11734 (95% confidence interval (˗ 0.8481; 0.76728), p-value = 0.8248).

ii) Relative Humidity and Mosquito abundance

Figure 4 shows the variation of mosquito numbers with relative humidity for the SW monsoon season. Mosquito count, M showed a positive correlation with the maximum Relative humidity, with Pearson's coefficient, r = 0.43917 (95% confidence interval (˗ 0.57861; 0.92208), p-value = 0.38368).

Similarly, positive correlation was also observed with minimum relative humidity, with Pearson's coefficient, r= 0.17351 (95% confidence interval (˗ 0.74261; 0.863482), p-value = 0.7423).

iii) Rainfall and Mosquito abundance

Mosquito abundance showed positive correlation with rainfall with Pearson's coefficient, r = 0.655847 (95% confidence interval (˗ 0.33290; 0.95767), p-value = 0.1573).

B) Post-Monsoon Season (October-November)

i) Temperature and mosquito abundance

Fortnightly averages for the number of mosquitoes per trap were correlated with the maximum and minimum air temperatures (MXT and MNT). Figure 5 shows the variation of mosquito numbers with temperature for the Post-Monsoon season. It was observed that the overall mosquito counts decreased with the decrease in temperature. The Pearson's correlation coefficient for M vs MXT was found to be r = + 0.15566 with p-value = 0.8443 (95% confidence interval (˗ 0.94711; 0.97142)). The Pearson's correlation coefficient for M vs MNT was found to be r = 0.38677 with p-value = 0.6132 (95% confidence interval (˗ 0.9141; 0.9826)). With the average daily temperature (AVT), the mosquito count showed positive correlation, r = 0.51656 (95% confidence interval (˗ 0.88280; 0.98742), p-value = 0.4834).

ii) Relative humidity and mosquito abundance

Figure 6 shows the variation of mosquito numbers with relative humidity for the Post-monsoon season. Mosquito count, M showed a positive correlation with the maximum Relative humidity, with Pearson's coefficient, r = 0.78315 (95% confidence interval (˗ 0.71944; 0.92208), p-value = 0.2168). Mosquito abundance decreased with relative humidity in this season. Similarly, positive correlation was also observed with minimum relative humidity, with Pearson's coefficient, r = 0.80394 (95% confidence interval (˗ 0.69122; 0.99569), p-value = 0.1961)).

iii) Rainfall and Mosquito abundance

Rainfall did not occur in the study area during the period (post monsoon period).

C) Impact of diurnal temperature range (DTR) on mosquito abundance

Mosquito abundance in terms of average mosquito count per trap (M) was compared with the variation in averaged diurnal temperature range (DTR) from July to November 2016 (Figure 7). Mosquito abundance peaked in July -August while the DTR was low and steady. In the last week of September and early October when the SW monsoon rains came to an end, there were fluctuations in DTR as well as mosquito abundance. In the post-monsoon months, there was a sharp increase in DTR (by ~4 fold, compared to July-August values), that coincided with rapid decrease in the mosquito abundance.

Correlation analyses revealed a negative relationship between mosquito abundance and DTR with Pearson's coefficient, r = -0.55042 (p-value = 0.0992, 95% confidence interval (-0.87634; 0.12120)). This implied that as the days became warmer and nights colder due to withdrawal of the monsoon and arrival of the dry and colder northern winds, mosquito abundance decreased sharply in the post-monsoon season (Figure 6).

3 Discussion

Mosquitoes are excellent indicator species because they are sensitive to environmental variables such as temperature and rainfall. Even small changes in abiotic factors can influence development time and habitat availability with potentially cascading feedbacks on mosquito population density. Because of their sensitivity to environmental gradients and perturbations, mosquitoes represent an ideal sentinel taxon for evaluating the ecological effects of global climate change phenomena. The geographic distribution, demography and seasonal variation of mosquito species may be influenced by a variety of factors including climate, vegetation and host availability (Dhiman et al., 2010).

The present study was conducted with a purpose to understand the composition (diversity) of mosquito population and variation in seasonal abundance in the Pashan area of Pune urban zone. This geographical region has seen rapid urbanization during 2001-2005, immediately after it was incorporated into the Pune metropolitan area. No data exists regarding the mosquito fauna of this region of urban Pune and the present study is the first ever survey conducted. Location and land-use description has been provided in the Materials section. Five fixed locations of the Pashan area of Pune city were selected for collection of mosquitoes. These are representative of the urban features of the area. Trapping was done weekly at each site from 15^th June to 30^th November 2016. South West monsoon or Indian summer monsoon was established in Pune over the second week of June 2016. The weather conditions prevailing over the last half of June included only 2-3 rainy days. Rest of the days was very windy with intermittent clouds and sunshine. Rainfall was scanty. These may have contributed to poor trapping results (that is, lack of meaningful collections) between 15^th and 30^th June 2016. Hence, analyses are based on data available from 1^st July to 30^th November 2016.

Our study revealed that 21 species of mosquitoes covering four genera (Aedes, Culex, Anopheles and Armigerus) thrive in the area. Among these, Aedes was the most prevalent in Pashan for both the seasons. During the period of the study, four species were found most abundant viz., Ae. vittatus, Ae. vexans vexans, Ae. albopictus and Culex quinquefaciatus. Interestingly, a few specimens of uncommon species like An. barbirostris, An. annularis, An. culicifacies, Cx. vishnui, Cx. fuscanus and Cx. bitaeniorhynchus were also found during the study period.  The occurrence of these uncommon species was noted from two collection sites; one close to and the other adjacent to the hillock (Pashan hills). Such occurrence may be attributed to the presence of the hillock with natural vegetation preserved on it, in spite of heavy urbanization surrounding it.

Seasonal variability of the mosquito population was observed. In SW monsoon season (July - September 2016), mosquito abundance was high compared to the post-monsoon season (October- November). In the SW Monsoon season, we observed an increase in mosquito abundance with decreasing temperature (both MXT and MNT) indicating a negative association. In this period, mosquito abundance increased with humidity as positive correlation was obtained with maximum and minimum relative humidity and rainfall. This is consistent with findings elsewhere in the Indian subcontinent (Barker et al., 2010).

In the post-monsoon season, mosquito abundance decreased compared to SW monsoon season. As monsoon withdrew, rainfall, relative humidity and average temperature decreased. Mosquito abundance was also decreased during the period. Withdrawal of monsoon means cessation of rainfall, changes in wind flow patterns and resumption of sunny days. In the post-monsoon season, days were warm while nights were colder as the dry cold wind from northern India commenced blowing over Pune.

Our analyses revealed that the diurnal temperature range (DTR), which is the difference between maximum and minimum temperatures in a day, changes dramatically at the end of monsoon season. Figure 7 has shown the plot of mosquito abundance and diurnal temperatures for the period 1st July to 30^th November 2016. A negative correlation indicated that mosquito abundance is high when DRT is low (SW Monsoon) and vice versa. Impacts of temperature on population dynamics and vector competence are complex (Beck-Johnson et al., 2013). Mosquitoes are sensitive to temperature throughout their life cycle and it has been shown by mathematical modeling studies that the fluctuations in diurnal temperatures may affect the mosquito life cycle and malaria transmission (Beck-Johnson et al., 2017). Carrington et al., in a study conducted in northwest Thailand have found that large diurnal temperature range (DTR) adversely affects mosquito biology by extending immature development phase, lowered larval survival and reduced female reproductive capacity (Carrington et al., 2013a). Our findings of mosquito abundance and DTR reinforce these findings along with those from a diversity of laboratory studies demonstrating the effects of DTR (Lambrechts et al., 2011; Carrington et al., 2013b; Carrington et al., 2013c; Liu-Helmersson et al., 2014; Murdock et al., 2017) on a variety of mosquito life history traits like survival, fecundity, larval development, biting rates, vector competence, and viral transmissions.

The top four abundant species viz., Ae vittatus, Ae albopictus, Ae vexans vexans and Cx quinquefasciatus are of public health concern due to their potential for transmitting viral diseases like dengue, chikungunya (for Aedes sp), Japanese encephalitis, West Nile (for Culex sp) etc. However, from our laboratory analyses no virus could be detected from the collected mosquitoes.

Mosquito distributions are very dynamic in space and time, due to short life cycles and are heavily influenced by variation in environmental/climatological parameters (Crans et al., 2004). However, considering the diversity of India in terms of geological features, climate zones, etc, detailed and systematic mosquito survey for a longer duration is warranted for understanding the species distribution and diversity.

4 Conclusions

The present study was the first ever survey of mosquito population in Pashan region of urban Pune, India, and revealed the prevalence of 21 species comprising four genera viz. Aedes, Anopheles, Culex and Armigerus. Mosquito abundance varied between the two seasons, being high during SW Monsoon and decreased steadily during the Post-monsoon season. Interestingly, low diurnal temperature range during the SW monsoon season along with high humidity and rainfall had contributed to higher mosquito abundance compared to post-monsoon season with high diurnal temperature and low humidity.

Authors’ contributions

Study design: PS and ABS. Field work for data collection: AAP, ABS, PS. Laboratory techniques: GNS, AAP, ABS. Data analyses, meteorological data collections and mathematical analyses: PS. Analyses and interpretation of results: PS and ABS. Manuscript preparation: PS, GNS, AAP, and ABS.

Acknowledgements

Authors would like to thank Dr. DT Mourya, Director National Institute of Virology, Pune for encouragement and support.

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