J Arthropod-Borne Dis, March 2017, 11(1): 50–59 Sh Nasir et al.: Effect of Climatic … 50 http://jad.tums.ac.ir Published Online: March 14, 2017 Original Article Effect of Climatic Conditions and Water Bodies on Population Dynamics of the Dengue Vector, Aedes aegypti (Diptera: Culicidae) *Shabab Nasir 1, Farhat Jabeen 1, Sadia Abbas 1, Iram Nasir 2, Mustapha Debboun 3 1Department of Zoology, Government College University, Faisalabad, Pakistan 2Department of Statistics, Government College University, Faisalabad, Pakisatn 3Harris County Public Health and Environmental Services, Houston, TX, USA (Received 13 Feb 2015; accepted 21 Nov 2015) Abstract Background: The population of mosquitoes is mainly influenced by the biotic and abiotic factors. Although Aedes aegypti was reported until 1960’s in the Punjab, Pakistan, the population has increased dramatically since 2009 and caused severe epidemics in 2011 due to heavy floods and rains. Thus, this study was carried out to know the effect of biotic and abiotic factors on the population of Aedes aegypti. Methods: Mosquitoes were collected from fresh, sewage, and rain water ponds, fish ponds, rice fields, tyres, tree holes, and manmade storage containers present in and around residential homes twice during every winter (October– February), summer (March–June) and monsoon season (July–September) from marked rural areas. Results: More mosquitoes were collected in 2010 and 2011 due to floods than other years with heavy rains. High population (52.4%) was recorded during the rainy season due to high temperature (28–36 °C) and high relative hu- midity (up to 75%), while low population was recorded during the winter due to low temperature (< 5 °C) and low relative humidity (< 22%). Specimens were recorded indoors when outside temperature was below freezing point. Ae. aegypti was largely collected from tyres and urban areas mostly during the rainy season from small water con- tainers. Years, months, seasons, temperature and relative humidity were statistically significant concerning the pop- ulation dynamics of mosquitoes. Conclusion: Abiotic factors (temperature & relative humidity) along with habitat have significant impact on popula- tion dynamics of mosquitoes. Keywords: Population dynamics, Climatic conditions, Dengue vector, Aedes aegypti Introduction Mosquitoes act as vectors for many vec- tor-borne diseases (Vaughn et al. 2009) such as malaria, dengue and yellow fever (Snow et al. 2005). They are found all over the world except in Antarctica (Gadahi et al. 2012). Anopheles, Culex and Aedes are three medi- cally important genera of mosquitoes. Aedes mosquitoes are recognized as daytime biters, widely distributed in more than 100 coun- tries of the world (Gratz 2004). Aedes ae- gypti and Ae. albopictus are two main mos- quito species involved in dengue transmis- sion to humans (Knudsen 1995). Dengue was a sporadic disease during the previous century. However, currently it has become a major health problem throughout the world due to the modern means of transportation, trade, population growth, mobility and environmen- tal change. Twenty two thousand deaths are reported annually worldwide mainly in chil- dren and young adults (Haile-Mariam and Polis 2009, Vaughn et al. 2009). Recent epidemic of dengue in Pakistan has been attributed to heavy rains and floods, de- terioration of health, and sanitation principles at all stages of the community (Anonymous 2011). In 1994, dengue fever (DF) and den- gue hemorrhagic fever (DHF) were first rec- *Corresponding authors: Dr Shabab Nasir, E-mail: flourenceshabab@yahoo.com J Arthropod-Borne Dis, March 2017, 11(1): 50–59 Sh Nasir et al.: Effect of Climatic … 51 http://jad.tums.ac.ir Published Online: March 14, 2017 orded in Karachi, Pakistan (Chan et al. 1994). In 2011, about two decades later from its first record in Pakistan, dengue appeared in its epidemic form in the Punjab province with 100 confirmed cases daily (Khawar 2011). The hotspot of the epidemic was the capital city Lahore where more than 131 people dead and over 12,000 people infected according to the Punjab Health Department (Anonymous 2011). Mosquitoes have a well-adjusted life, par- ticularly by inhabiting quiet pools, under- ground buildings, and seepage areas near any bodies of water. Water bodies are differ- ent from each other in respect to chemical properties of water (acidity or alkalinity, fresh- ness, salty or brackish) and the type or amount of vegetation present in them (Foster and Walker 2002). Thus, there is no doubt some mosquito species use more than one kind of habitat. However, generally many mosquitoes can be grouped according to their preference for water bodies such as permanent, flood, temporary or container water (Vanwambeke et al. 2007). Since dengue fever is a viral in- fection, and no vaccine or treatment is avail- able for people, entomologists are key re- searchers who had better understand the vec- tor and its life cycle to develop an integrated mosquito management program (Rathor 1996, Gratz 2004). The study of the biology of the vector along with the climatic conditions suitable for his life cycle is vital for ento- mologists who help in the timely application of mosquito management system against den- gue vectors (Sharma et al. 2005). Container location and capacity, water source and tem- perature, all can vary seasonally. Aedes ae- gypti breeds in standing water generally in artificial containers. The amount of rainfall, temperature, and relative humidity are very important climatic factors that affect the pop- ulation of Aedes mosquitoes especially Ae. aegypti (Scott et al. 2000). Due to these reasons, we decided to ex- plore the role of the climate, water bodies (size and location), physical and chemical prop- erties of water, environmental abiotic factors and distance from human population on the population dynamics of Ae. aegypti. Materials and Methods This study was conducted from 2009 to 2013 involving the collection of Ae. aegypti from rural and urban areas of the Punjab (31.0000° N, 72.0000° E and 139m above sea level) (Anonymous 2014) and identifi- cation of key ecological factors affecting the population dynamics and seasonal abundance of Ae. aegypti. Punjab is the most populous province with an area of 79,284 square miles. Almost 70% of its population consists of farm- ers who live in villages or around the big cities. Its boundaries meet with Jammu and Kashmir in the northeast, Indian Punjab and Rajasthan in the east, province Sindh in the south, Baluchistan and KPK (Khyber Pakh- tunkhwa) in the west and Islamabad and Azad Kashmir in the north. It lies on the margin line of the monsoon climate. Its cli- mate is mixed, some areas are too cold like Murree (up to -4 °C) and some are hot like Multan (up to 47 °C). The average annual pre- cipitation is low, but sometimes-heavy rains occur due to monsoon airs during July–Sep- tember that become the cause of heavy floods (Anonymous 2015). Mosquitoes were collected randomly from forests, fields, parks, and residential areas (in and around the houses). Since Ae. aegypti prefers the small artificial containers, we col- lected from buckets, waste water near hous- es, seepage pools, dairy and poultry farms (Harrel et al. 2011), used tyres, broken vases, bottles, irrigation channels, cemented tanks, bamboo sticks (Bashar et al. 2005), tyre shops, and tree holes (Akram and Lee 2004). Adults were collected with aspirators and collection nets, while larvae and pupae with plastic dip- pers. J Arthropod-Borne Dis, March 2017, 11(1): 50–59 Sh Nasir et al.: Effect of Climatic … 52 http://jad.tums.ac.ir Published Online: March 14, 2017 Seasonal Abundance Collection (adults with aspirators and col- lection nets, while larvae and pupae with plas- tic dippers) was done seasonally to examine the population fluctuations in different areas of the Punjab, Pakistan (Fig. 1). Therefore, the year was divided into three quarters based on seasons, i.e. summer (March to June), rainy or monsoon (July to September) and winter (October to February) (Mohiuddin 2007). Global positioning system (GPS) was used to record the height from sea level and co- ordinates (longitude and latitude) of marked sample sites during the survey. Temperature, relative humidity and pH were measured with a multi-meter (Elmetro Poland, Model # CPC 401) while the location of sites were rec- orded with Magellan GPS (Explorist, 660). After the adult mosquitoes were killed using the poison bottle, the genera were separated and counted at the site to identify the sea- sonal abundance (Reisen and Milby 1986). The larvae were placed in 500ml plastic jars filled with water from the source to keep them alive during transport to the Vector Bi- ology Laboratory, Government College Uni- versity and Faisalabad, Pakistan and reared in rearing cages. After the adults emerged they were killed, pinned, and identified to species level with the help of available taxonomic keys (Barraud 1934, Darsi and Pradhan 1990). Specimens were identified using the micro- scope (Nikon Binocular Microscope Eclipse, Model # E-100). Biotic and abiotic factors Biotic (flora and fauna present in the wa- ter) and abiotic factors including the physi- cal condition of water (clear, turbid, and foul), pH, temperature and relative humidity (RH) (Akram and Lee 2004, Harrel et al. 2011) have been sampled from each site. We also recorded the location of each site as ur- ban or rural and the distance of each site from the residential areas. After ANOVA, chi- square test was applied on significant factors and then logistic regression was applied on highly significant factors effecting the pop- ulation. Statistical analysis We used Mathematica 7 to analyze the data for chi-square value to determine the rela- tionship between different variables affecting the population of Ae. aegypti. Logistic re- gression model was also used for significant factors from chi-square test to identify the key factors affecting the population of Ae. aegypti. A stepwise forward approach was applied, for this model (Vanwambeke et al. 2007). Results Aedes aegypti mosquitoes were collected from different rural and urban areas of the Central Punjab (Lahore, Faisalabad, Sargo- dha, Sheikhupura and Gujranwala) and Up- per Punjab (Rawalpindi, Islamabad and Mur- ree) but not from Northern Punjab (Multan, Dera Ghazi Khan, Bahawalpore and Rahim Yar Khan). They were mostly sampled from latitude (max 033º 45.403, min 29º 57.859) and longitude (max 074º 45.403, min 072º 57.859) with elevation (max 1218m, min. 144m). Max- imum population was collected from Lahore during the rainy season and minimum from Faisalabad during the winter season. Populations of Ae. aegypti From 810 water container sites, 83 sites (10.25%) were positive for Aedes mosquitoes. Populations of Ae. aegypti showed a great variation in their density during all seasons (P-value= < 0.001). Maximum population (52.4% of the total collected population) was collected during the rainy season followed by the summer season (41.7%) while the lowest percentage (5.9%) was found during the win- ter. Similarly, maximum population (42.7%) was recorded during 2011 due to heavy rains J Arthropod-Borne Dis, March 2017, 11(1): 50–59 Sh Nasir et al.: Effect of Climatic … 53 http://jad.tums.ac.ir Published Online: March 14, 2017 followed by 35% in 2010, likely due to heavy floods in the province. Water quality had significant influence on population density (P-value< 0.001). Most populations were col- lected from turbid water (46.1%) followed by turbid foul (33.8%), clear (17.4%) and clear foul (2.7%). In addition, most of the population (97.8%) was found in standing water than in flowing water (2.2%). Color of the water was also significant (P= 0.04) in relation with population density since most of the population of Ae. aegypti was found in colorless medium (29.6%). In addition, light had a significant (P< 0.002) impact on pop- ulation density with 60.0% population ex- posed in shady medium (60.0%) (Table 1). There were more breeding sites during 2010 and 2011 than other years due to more rainfall and floods. Aedes aegypti was most- ly collected from small containers such as buckets or cans and used tyres near or around residential areas (Fig. 2). Abiotic factors had a significant impact on the population of Ae. aegypti. More rain fell in 2011 resulting in an increase of its population. Thus, more rainfall in 2011, heavy floods in 2010, and the increase of the relative humidity in these years resulted in an increase of the population of Ae. aegypti and more numbers were collected (Fig. 3). In addition, more breeding sites were observed during the rainy seasons, particularly in 2010 and 2011. A little effect was observed on the population dynamics of Ae. aegypti because it was mostly collected from artificial water containers that were mostly found in the residential areas (Fig. 2). Habitat of Ae. aegypti The majority of Ae. aegypti population was sampled in artificial containers (44.8% in tyres, 37.8% in tanks and cans). The re- maining 17.4% has been collected in natural containers such as water bodies and none from natural tree holes (Fig. 2). Locality also showed a significant effect on the population level (P= 0.019). The population was rec- orded from urban areas (78.1%) than rural (21.9%). Among the flora, algae, grass, spi- rogyra, dragonflies, damselflies, frog tad- poles, and water bugs were recorded but we did not assess their role. Logistic regression analysis The seasons had a significant role in Ae. ae- gypti population dynamics as seen in the rainy season (OR: 0.287, P= 0.003) than the summer (OR: 0.052, P= 0.005). Location also had a significant effect on the future population dynamics of this mosquito as found in the rural environment (OR: 0.496, P= 0.048) (Table 2). Table 1. Key parameters for the presence of Aedes aegypti in Punjab area, Pakistan, 2009–2013 Characteristics Population of Aedes aegypti P-value 2009 2010 2011 2012 2013 % age Seasons ˂0.001 Winter 5 7 12 7 6 5.9 Summer 37 61 72 46 41 41.7 Rainy 49 75 92 57 52 52.4 Habitat ˂0.001 Tyres 38 66 79 49 44 44.8 Water bodies 18 24 29 19 17 17.4 Others (Tree holes, cans, tanks and any other) 35 53 66 42 38 37.8 Water quality ˂0.001 Clear 18 23 30 19 17 17.4 Turbid 41 67 81 51 46 46.1 J Arthropod-Borne Dis, March 2017, 11(1): 50–59 Sh Nasir et al.: Effect of Climatic … 54 http://jad.tums.ac.ir Published Online: March 14, 2017 Turbid foul 30 49 59 37 33 33.8 Clear foul 2 4 5 3 3 2.7 Water condition 0.100 Standing 89 141 169 108 97 97.8 Flowing 2 2 5 2 2 2.2 Light ˂0.002 Exposed 27 43 59 35 31 31.6 Exposed shady 57 87 101 66 60 60.0 Shady 7 13 14 9 8 8.4 pH 0.370 ≤ 7.00 0 0 0 0 0 0 7.01–8.00 15 34 43 25 22 22.5 8.01–9.00 57 79 93 62 56 56.2 ˃9.01 19 30 38 23 21 21.3 Area size (m) ˂0.001 ≤ 1.00 55 78 89 60 54 54.4 1.01–10.00 3 6 8 5 4 4.1 10.01–100.00 2 3 4 2 2 2.2 ˃ 100 31 56 73 43 39 39.3 Location 0.019 Urban 67 106 146 86 78 78.1 Rural 24 37 28 24 21 21.9 Temperature (°C) ˂0.001 ≤ 10 3 8 12 6 6 5.6 11–20 3 10 29 11 10 10.3 21–30 20 35 60 31 28 28.2 31–40 63 87 70 59 53 53.9 ˃41 2 3 3 3 2 2.0 Relative humidity (%) ˂0.001 ≤ 30 4 4 5 4 3 3.2 31–40 20 33 40 25 22 22.8 41–50 29 47 67 39 35 35.0 ˃51 38 59 62 42 39 39.0 Distance from houses (m) 0.160 ≤ 25 72 109 135 85 77 77.5 26–100 18 31 34 22 20 20.3 ˃100 1 3 5 3 2 2.2 Table 2. Logistic regression as predictor for the presence of Aedes aegypti, Punjab, 2009–2013 Variables Odds Ratio (OR) 95% confidence interval of OR P-value Lower Upper Seasons Summer 0.052 0.069 0.437 0.005 Rainy 0.287 0.195 0.798 0.003 Light Exposed 0.593 0.197 1.899 0.395 Exposed Shady 0.292 0.101 0.865 0.33 Turbid Water 0.998 0.998 1.454 0.067 Location Rural 0.496 0.259 1.106 0.048 Distance from houses ≤ 25 8.097 2.098 15.90 0.001 26-100 16.097 3.978 78.09 0.012 Table 1. Continued… J Arthropod-Borne Dis, March 2017, 11(1): 50–59 Sh Nasir et al.: Effect of Climatic … 55 http://jad.tums.ac.ir Published Online: March 14, 2017 Fig. 1. Location of selected districts of the Punjab for the collection of Aedes mosquitoes, 2009–2013 Fig. 2. Number of Aedes aegypti collected from different visited habitats in Punjab, 2009–2013 J Arthropod-Borne Dis, March 2017, 11(1): 50–59 Sh Nasir et al.: Effect of Climatic … 56 http://jad.tums.ac.ir Published Online: March 14, 2017 Fig. 3. The relationship between abiotic factors during different seasons from 2009–2013 and the population of Aedes aegypti Discussion During this study, the population of Ae. aegypti was collected from 83 sites (out of 810) and showed a great variation during the entire year with the majority collected dur- ing the rainy season rather than the summer one. Small breeding habitats around or inside the residential areas, old tyres and exposed shady water pools were the sites chosen and preferred by Ae. aegypti. Water temperature ranging from 21 to 38 °C and a relative hu- midity higher than 35% supported the popu- lation density. However, the maximum pop- ulation density was observed at 32–38 °C with relative humidity of about 50%. Aedes ae- gypti population was generally more support- ed in the urban environment than the rural one. Other scientists who also studied the distribution patterns according to seasons had similar results as ours showing that the cool season put a greater stress on the sur- vival of adults and larvae than on the eggs (Preechaporn et al. 2007). Population density was flexible throughout the year depending on the larval breeding habitats. Rainfall plays an important role in the pop- ulation density of Aedes (Ndiaye et al. 2006). Our results showed that Aedes mosquitoes were collected during the rainy as well as sum- mer season and these circumstances were most- ly found in areas where the elevation was higher and ecological conditions were mild (Alto and Juliano 2001, Preechaporn et al. 2007). In Bangladesh, mosquitoes were col- lected from all sampling sites in the rural areas (Bashar et al. 2005). The domestic wa- ter storage containers (drinking water jars, buckets, and tanks) followed by tyres were the regular productive containers in our study area. The number of containers primarily filled with rainwater increased during the rainy sea- son, generally in the used tyres. Therefore, this is a possible reason why Ae. aegypti pop- ulation did not reach low levels at a time when rainfall was limited. As the people manage J Arthropod-Borne Dis, March 2017, 11(1): 50–59 Sh Nasir et al.: Effect of Climatic … 57 http://jad.tums.ac.ir Published Online: March 14, 2017 these containers, they also manage the pro- duction of mosquitoes in these containers un- intentionally. These results are in agreement with the results of previous studies (Koenraadt et al. 2004, Barbazan et al. 2008). Mainly, a few key types of containers play important role for a large proportion of the pupal and adult production (Koenraadt et al. 2004, Bar- bazan et al. 2008). However, the control measures such as placement of lids on water containers, use of larvicides or biological control agents, re- moval of discarded and unused containers have decreased the mosquito population den- sity. Container capacity, water temperature, source of water, and container location, all of which could vary seasonally (Koenraadt et al. 2004, Kay and Nam 2005) have been reported as key ecological factors affecting population of Ae. aegypti. A study in Samoa Island revealed that the most productive containers during the dry and wet seasons were the buckets and used tyres (Lambdin et al. 2009). During this study, they also noted that the knowledge of environmental varia- bles such as habitat density, water source, seasonal variations and neighborhood condi- tions played a significant role in container productivity. The typical rainfall system in the Punjab, normally during July–August was associated with a peak of Aedes population. A better understanding of the environ- mental factors affecting the water container productivity is a key part of adaptive vector control efforts (Scott and Morrison 2008). Work is being carried out in tropical regions to investigate the effect of source reduction on the population of Ae. aegypti (Arun- chalam et al. 2010). We can understand the population dynamics of Ae. aegypti more con- sistently and design a better effective vector control program by integrating the knowledge of breeding site density and the ecology of larval breeding sites. Conclusion Environmental factors and breeding sites had a strong influence on the population dy- namics of Ae. aegypti mosquito. Although the population was recorded during the en- tire year but most of the population was rec- orded during the rainy season. In addition, man’s activities had a strong relationship with the mosquito population. 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