J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 106 http://jad.tums.ac.ir Published Online: March 31, 2020 Original Article Determination of Species Composition of Mosquitoes in Lahore, Pakistan *Farkhanda Manzoor1; Robeela Shabbir2; Madiha Sana2; Sumbal Nazir2; Muhammad Aslam Khan3 1Lahore College for Women University, Lahore College for Women University, Jail Road, Lahore, Pakistan 2Department of Zoology, Lahore College for Women University, Lahore, Pakistan 3University of Health Sciences Lahore, Lahore, Pakistan (Received 05 Apr 2017; accepted 25 Mar 2020) Abstract Background: Present study was conducted to determine species composition of mosquitoes (larvae, pupae and adults) collected from ten different towns of Lahore from September 2014 to August 2015. Methods: Mosquito larvae, pupae and adults (male and female) were collected by using dippers and aspirators from September 2014 to August 2015 in different sites of Lahore comprising of ten towns i.e. Iqbal, Aziz Bhatti, Data Ganj Baksh, Gulberg, Nishtar, Ravi, Samanabad, Shalimar, Wagah, and Lahore Cantonment. Mosquito larvae and adults were identified by standard entomological keys. Diversity, richness and rarity of mosquito fauna were analyzed by the Shannon, Simpson and Margalef indices respectively. Results: In this study, a total of 8656 mosquitoes belonging to four genera namely Anopheles, Culex, Aedes and Man- sonia were identified. Among fifteen species collected, Cx. quinquefasciatus was the most abundant species in the city having 25.8% relative abundance. However An. culicifacies s.l. (sensu lato) was reported as the least abundant species with 0.22% relative abundance. The highest diversity of mosquitoes was shown in the month of August (H= 2.25) while the lowest diversity was recorded June (H= 1.43). Extensive sewage water supported the maximum abundance of Cx. quinquifasciatus in urban areas of this city. Conclusions: This study has significantly elaborated the monthly varying species composition of mosquito fauna of this city. Hence this research will help us to find out the control strategies of mosquito borne diseases in this region. Keywords: Mosquito fauna; Lahore; Shannon Index; Simpson Index; Climatic factors Introduction Mosquito serves as a vector of various dead- ly diseases including Malaria, Dengue fever, Zika fever and Chikungunya. The vector causes deaths of more than one million people annually (1). Worldwide there are about 3541 species of mos- quitoes reported belonging to 42 different gen- era (2). However there are 134 species of mos- quitoes found in Pakistan belonging to Anophe- linae and Culicinae subfamilies (3). Mosquitoes play an important role in food chains of various ecosystems as well (4). Pakistan is one of those subtropical countries that have been under threat of vector borne dis- eases. Like other Asian countries, Pakistan is al- so withstanding substantial climatic changes that are sufficient to harbor the outbreaks of mos- quito borne diseases (5). Lahore, an urbanized city of Pakistan, was reported to have 11,283 cases of Dengue fever in the epidemics of 2012 (6). Recent Dengue fever outbreaks in Khyber Pakhtunkhwa resulted in 2179 positive cases (7). The shift in the climate of South Asian coun- tries tends to escalate the incidence of mosquito borne diseases (8). Moreover, the abiotic fac- tors like temperature, humidity and rainfall are positively supporting the population of mosqui- toes with increased sustainability of their breed- ing sites and long survivorship (9, 10). Likewise, certain studies have been conduct- ed in various regions of Pakistan reporting the mosquito fauna that have related the relative abundance of different species with the gradual shift in climatic trend (11–15). The relationship between the biodiversity of mosquitoes in La- *Corresponding author: Prof Farkhanda Manzoor, E-mail: drfarkhanda786@gmail.com http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 107 http://jad.tums.ac.ir Published Online: March 31, 2020 hore with its climatic conditions was studied in 2013. The reported species were Aedes aegypti, Culex quinquefasciatus, Anopheles stephensi and Anopheles subpictus s.l.. The population dynam- ics of these mosquito species was strongly cor- related with seasonal temperature variations of the region (15). The rapid urbanization of this city with extensive road construction projects and elimination of open fields is a reason to pro- vide the flourishing breeding sites for disease transmitting mosquito species. Hence, it is so crucial to monitor the abundance of various mos- quito species for maintaining vector control pro- grams in this region. The objective of current study was to de- scribe the abundance, diversity and rarity of dif- ferent species of mosquitoes in different habi- tat types. Morever this study would also find a link between environmental variables and the relative abundance of different species of mos- quitoes collected. Materials and Methods Lahore having a semi-arid climate and typ- ical monsoon season was selected as the area of study. The geological coordinates of Lahore are 31˚ 32̍ North and 74˚ 20̍ East respectively and is about 223 meter high from sea level. The selected towns of this city were Iqbal Town, Aziz Bhatti Town, Data Ganj Baksh Town, Gul- berg Town, Nishtar Town, Ravi Town, Sama- nabad Town, Shalimar Town, Wagah Town and Lahore Cantonment as shown in the Lahore Ad- ministrative Towns Boundary (Fig. 1). Sampling of larvae, pupae and adult mos- quitoes Mosquito samples were collected from fixed spots of ten towns four times in a month from September 2014 to August 2015. Mosquito lar- vae and pupae were collected by using strain- ers and dippers (16) from fresh as well as pol- luted water bodies of all towns (17). Simulta- neously, indoor and outdoor collection was done for adult mosquitoes by using sweeper and as- pirators (14). Open drains, freshwater reservoirs, discarded containers, flower vases, sewage wa- ter, tyres and tree-holes were keenly observed during sampling of larvae, pupae and adult mos- quitoes. The collected mosquitoes were transferred to plastic jars covered with net for further ex- perimentation. Preservation and identification of the mos- quitoes The adult mosquitoes were sucked through aspirator from different plastic jars and were then kept in airtight conical jars containing chloro- form dipped cotton swab that helped in killing the adult mosquitoes in two to four minutes. These killed mosquitoes were shifted in test tubes with a cork containing small amount of silica gel for preservation of the mosquitoes. The collected larvae and pupae were identified un- der the dissecting microscope. The mosquito larvae, pupae and killed adults were later identified using standard taxonomic keys given in “The fauna of British India includ- ing Ceylon and Burma, Diptera Family Cu- licidae, Tribe Anopheline, Vol. IV and Tribe Megarhinini and Culicini, Vol. V” (18, 19). Data analysis Relative abundance was determined by us- ing following formula. Where ‘n’ is the number of mosquito, and it is divided by the total number of mosquitoes collected and then it is multiplied by 100 (20). The mosquito species were termed as dominant species with more than 10% relative abundance and subdominant species with 3 to 10% relative abundance while mosquitoes species having less- er than 3% relative abundance were tagged sat- ellite species (21). The distribution status of collected mos- quito species in different collection sites was calculated by the formula as given (21), Distribution (C)= n x100/ N Where n is number of sites where species was http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 108 http://jad.tums.ac.ir Published Online: March 31, 2020 found, and N is the total number of sites. The distribution status of different species was cat- egorized as constant species (80–100%), frequent species (60–80%), moderate species (40–60%) and infrequent species (20–40%). Mosquito species richness was calculated by using Margalef’s index of richness (Dmg) Dmg= (S-1)/ In N. Where, S is total number of species and N is total number of individuals. Shannon-Weaver Index was also applied to find out the diversity of mosquitoes with respect to monthly variation (22). H= -∑pilnpi where H= Shannon diversity index and pi= ni/N Where ni= importance value index of the species and N= importance value index of all species. Simpson index (D) was also applied to find out the rarity of mosquito species (23) collect- ed. It was calculated by using formula, D= ∑n(n-1)\N(N-1) Whereas, n= no. of mosquitoes of individ- ual species, and N= No. of total mosquitoes spe- cies collected. Climate analysis Annual reports of climate data from Septem- ber 2014 to August 2015 were retrieved from Punjab Metrological Department for the analy- sis of temperature, humidity and rainfall. The collected data were further processed by plot- ting different graphs on MS Excel. Moreover, Poisson regression analysis was also performed on SPSS 16.0 to develop a correlation between the frequency of mosquitoes collected and chang- ing weather variables. Results Mosquito species were recovered from the different types of particular habitat such as open drains, fresh water, discarded containers, flow- er vases, sewage water, tyres and tree holes (Ta- ble 1). Anopheles species and Mansonia species was specifically found to be Fresh water. Cu- lex species were collected from their breeding sites of fresh water, discarded containers and sewage water. Aedes species were collected from different sites except sewage water, all of its breeding sites were predominately fresh wa- ter in nature. Relative abundance of fifteen different species of mosquitoes throughout Lahore with their abundance status and distribution class was shown in Table 2. Culex quinquefasciatus was the most abundant species with 25.80% relative abundance. In contrast An. culicifacies was appeared to be the least in number with 0.22% relative abundance. Culex sitiens and Cx. tritaeniorhynchus were reported as dominant species during collection. Moreover, An. pul- cherrimus, Cx. vagans, Cx. theileri, Cx. vishnui, Ae. albopictus and Ae. aegypti were found sub dominant species. However, An. annularis, An. nigerrimus, An. subpictus s.l., An. stephensi, and An. culicifacies were recovered as satellite spe- cies having least abundance and sporadic dis- tribution. Mansonia uniformis was found to be infrequent species in its distribution. In this study, total of 8656 mosquitoes were collected. Taxonomic identification revealed fif- teen species of mosquitoes such as An. annu- laris, An. pulcherrimus, An. stephensi, An. ni- gerrimus, An. subpictus s.l., An. culicifacies, Cx. vagans, Cx. quinquefasciatus, Cx. sitiens, Cx. tritaeniorhynchus, Cx. vishnui, Cx. theileri, Ae. aegypti, Ae. albopictus and Ma. uniformis. An overview of month wise abundance of all mos- quito species collected in one year of study was shown in Table 3. The highest mosquito sample size was shown in the month of September (Dmg= 4.17) while the lowest sample size was shown in June (Dmg= 1.63). On the basis of Shannon index, the highest diversity was shown in August (H= 2.24) while the lowest diversity was shown in June (H= 1.43). Due to the highest diversity of mosquitoes in August, less number of rare species of mosquitoes (D= 0.11) was present. The lowest diversity in June showed the highest http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 109 http://jad.tums.ac.ir Published Online: March 31, 2020 number of rare species (D= 0.25) in this month (Table 4). The relationship of seasonal condi- tions recorded in every month with the abun- dance of mosquitoes collected was shown in (Figs. 2–4). Table 5 enlisted the results of Poisson regres- sion analysis showing the correlation between various climatic variables and expected number of mosquitoes to be collected. Table 1. Different breeding habitats of mosquitoes in ten different towns of Lahore, Pakistan, September 2014 to Au- gust 2015 Mosquito Open drains Fresh water Discarded Containers Flower vases Sewage water Tyres Tree Holes An. annularis - + - - - - - An. pulcherrimus - + - - - - - An. subpictus s.l. - + - - - - - An. nigerrimus - + - - - - - An. stephensi - + - - - - - An. culicifacies s.l. - + - - - - - Cx. quinquefasciatus + - + - + - - Cx. tritaeniorhynchus + - + - + - - Cx. vagans + - + - + - - Cx. vishnui - - + - + - - Cx. theileri + - + - + - - Cx. sitiens + - + - + - - Ae. aegypti + + + + - + + Ae. albopictus + + + + - + + Ma. uniformis - + - - - - - Table 2. Relative abundance, status and distribution class of mosquitoes collected from all the ten towns of Lahore, Pakistan, September 2014 to August 2015 Species Abundance Relative Abundance Relative Abundance Status Distribution class An. annularis 217 2.51 Satellite Sporadic An. pulcherrimus 308 3.56 Satellite Sporadic An. subpictus s.l. 166 1.92 Satellite Sporadic An. nigerrimus 150 1.73 Satellite Sporadic An. stephensi 51 0.59 Satellite Sporadic An. culicifacies s.l. 19 0.22 Satellite Sporadic Cx. sitiens 1029 11.89 Dominant Sporadic Cx. quinquefasciatus 2233 25.80 Most dominant Moderate Cx. tritaeniorhynchus 868 10.03 Dominant Moderate Cx. vagans 795 9.18 Subdominant Moderate Cx. vishnui 141 1.63 Satellite Moderate Cx. theileri 810 9.36 Subdominant Moderate Ae. albopictus 962 11.11 Dominant Frequent Ae. aegypti 730 8.43 Subdominant Frequent Ma. uniformis 177 2.04 Satellite Infrequent http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 110 http://jad.tums.ac.ir Published Online: March 31, 2020 Table 3. Richness and abundance of mosquito population in Lahore, Pakistan, September 2014 to August 2015 Month A n . a n n u la ri s A n . p u lc h e rr im u s A n . su b p ic tu s s. l. A n . n ig e rr im u s A n . st e p h e n si A n . c u li c if a c ie s s. l. C x . s it ie n s C x . q u in q u e fa sc ia tu s C x . tr it a e -n io rh y n c h u s C x . v a g a n s C x . v is h n u i C x . th e il e ri A e . a lb o p ic tu s A e . a e g y p ti M a . u n if o rm is T o ta l Sep-2014 90 130 75 68 23 10 209 593 197 168 33 179 255 194 52 2276 Oct-2014 37 44 24 21 3 0 64 147 43 33 0 0 4 0 0 420 Nov-2014 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Dec-2014 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Jan-2015 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Feb-2015 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Mar-2015 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Apr-2015 0 0 0 0 0 0 167 314 141 152 28 162 138 108 34 1244 May-2015 0 0 0 0 0 0 160 341 123 131 23 165 146 122 25 1236 Jun-2015 0 0 0 0 0 0 40 100 85 26 0 35 0 0 0 286 Jul-2015 0 0 0 0 0 0 154 239 104 107 18 110 180 130 30 1072 Aug-2015 90 134 67 61 25 9 235 499 175 178 39 159 239 176 36 2122 Total 217 308 166 150 51 19 1029 2233 868 795 141 810 962 730 177 8656 Table 4. Monthly analysis of species composition of mosquitoes collected from different towns of Lahore, Pakistan, September 2014 to August 2015 Months Abundance Margalef’s Index (Dmg) Shannon index (H) Simpson Index (D) September 2276 4.17 2.15 0.12 October 420 3.43 1.82 0.18 November 0 0 0 0 December 0 0 0 0 January 0 0 0 0 February 0 0 0 0 March 0 0 0 0 April 1244 2.58 1.93 0.15 May 1236 2.59 1.91 0.16 June 286 1.63 1.43 0.25 July 1072 2.64 1.92 0.14 August 2122 2.40 2.24 0.11 Table 5. Parameter estimates of Poisson regression analysis showing correlation between weather variables and ex- pected mosquito frequency from different towns of Lahore, Pakistan, September 2014 to August 2015 Estimate Standard Errors Exp (B) P- value Intercept 2.038 .0068 7.677 .000 Temperature -0.012 .0020 0.989 .000 Humidity 0.010 .0021 1 .000 Rainfall 0.021 .0009 1.021 .000 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 111 http://jad.tums.ac.ir Published Online: March 31, 2020 Fig. 1. Location of study sites in towns of urban city Lahore, Pakistan, September 2014 to August 2015 Fig. 2. Relationship between temperature and the total number of mosquitoes collected monthly in Lahore, Pakistan, September 2014 to August 2015 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 112 http://jad.tums.ac.ir Published Online: March 31, 2020 Fig. 3. Relationship between the average humidity and the total number of mosquitoes collected monthly in Lahore, Pakistan, September 2014 to August 2015 Fig. 4. Relationship between rainfall and the total number of mosquitoes collected monthly in Lahore, Pakistan, Sep- tember 2014 to August 2015 Discussion Fifteen species of mosquitoes belonging to four genera Anopheles, Aedes, Culex and Man- sonia were recovered from the urban city La- hore during the period of September 2014 to August 2015. Firstly there were twenty nine species of mosquitoes ever reported in Lahore, Pakistan (24). In 1971, the mosquito fauna of this city was highly enriched with the identification of 31 different species belonging to seven genera N o . o f C o ll e c te d M o sq u it o e s . A v e r a g e R a in fa ll ( M .M ) http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 113 http://jad.tums.ac.ir Published Online: March 31, 2020 (7). However, current study exhibited reduc- tion in the number of collected mosquito spe- cies. This decline in reported mosquito species of this city during last forty years is due to dras- tic change in environmental conditions, expand- ing sewage system and due to diminishing fresh- water habitats. Mosquito collection performed in this study by dippers and aspirator mainly focused on indoor and outdoor breeding sites. However by employing other methods such as, ovitrap, CDC light traps, BG traps, human and animal baits, the species composition of the re- gion can modulate accordingly. Culex quinquefasciatus was the most abun- dant species found in all the towns with the highest diversity. Same species was also report- ed as the most dominant species of Pakistan in a study analyzing the mosquito diversity based on barcoding (5). This species breeds in pollut- ed water therefore it is found in sewage canal which is an air conditioned breeding place for this mosquito. Mukhtar et al. (2003) investigated the breed- ing of mosquitoes in waste water irrigation where he found three genera Aedes, Culex and Anopheles. The present study discovered near- ly all the species such as An. pulcherrimus, An. culicifacies s.l., An. subpictus s.l., An. stephensi, Cx. quinquefasciatus and Cx. tritaeniorhynchus which were previously collected from waste- water (25). Ali and Rashid (26) studied polluted water of Palosai stream near Peshawar. They identi- fied Cx. quinquefasciatus and An. stephensi while Aedes was missing. This shows that Ae- des species are the inhabitants of temporary hab- itats only. By using different traps and trapping techniques twelve different mosquito species were collected in Lahore in 2013 (15). In our study An. subpictus s.l., An. culicifacies s.l., and Ma. uniformis were additionally reported. Anopheles culicifacies s.l. and An. stephen- si are fresh water breeders. They have almost disappeared from main city and are recovered from suburb areas getting more susceptible to diseases like malaria. Anopheles annularis and An. nigerrimus are usually found in clean and still water. The species were recovered from all the ten towns of Lahore. Both of the spe- cies are considered as vector of malaria in In- dia, Nepal and Srilanka (27). The risk of trans- mission of malaria by these species is quite low, because in Pakistan there is no evidence of their vectorial capacity. However further studies can be conducted to investigate these species as suspected vectors of malaria in this region. The disappearance of fresh water in this city has low- ered the relative abundance of fresh water dwell- ing species like An. pulcherrimus and An. sub- pictus s.l. thus enlisting them as sporadic in dis- tribution. Aedes species were largely taken from tem- porary habitats over the entire city in suitable breeding sites of fresh water like water tanks, broken pots, pans and old tyres that explain the vulnerability of Dengue epidemics in Lahore. In our study, the recorded optimum temper- ature, 25 ˚C, optimum humidity, 80% and 15mm rainfall in the months having maximum num- ber of species built the positive correlation be- tween the climatic conditions and abundance of mosquitoes collected. The Poisson regres- sion analysis in table 5 proposed that for every unit increase in temperature the expected mos- quito frequency increased by e-0.012= 0.988. Like- wise, for every unit increase in rainfall and hu- midity, collected mosquito number would be in- creased by e0.21= 1.233 and e0.01= 1.01 respec- tively. The climatic analysis of this study showed the most suitable environmental conditions like temperature, humidity and rainfall in the month of August and September that is referred as the typical monsoon period in Pakistan. Along with suitable climatic variables for survival, this sea- son also provides extensive breeding sites for different species of mosquitoes. The results of this study also exhibited fresh water sources, discarded containers and open drains as more productive breeding sites for dwelling mosquito species and all of these sites are more function- ing in the months of monsoon. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 114 http://jad.tums.ac.ir Published Online: March 31, 2020 The highest mosquito diversity (H= 2.24) was reported in August due to the availability of high rainfall and suitable humidity. This ultimately enhances the dissemination of vec- tor borne diseases. Due to the highest diversi- ty of mosquitoes in August, the least number of rare species were recorded. Likewise, the highest species richness was found in Septem- ber (Dmg= 4.17). In these months, high tem- perature in water also boosts larval develop- ment making the survival of mosquitoes more feasible (28). Conclusions From the findings of this study and previ- ous studies it can be concluded that a world- wide climatic shift along extensive urbaniza- tion is influencing the distribution as well as the diversity of mosquito fauna of this cosmopoli- tan city. Hence, there is always a potential risk of the outbreak of the mosquito borne diseas- es. The results of this research provide signif- icant help to plan effective control strategies against mosquito borne diseases before time. Moreover, it is further suggested to plan simi- lar studies by employing other methods of mos- quito collection to assess current species com- position in Lahore, Pakistan. Acknowledements We thank the staff of Department of Zool- ogy, Lahore College for Women University for providing facilities and support to conduct field work. Moreover, we pay our gratitutde to Mr Saeed Ahmad for his help during the field trips and collecting the specimens. The authors declare that there is no conflict of interests. References 1. World Health Organization (2009) Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control. Available at: https://www.who.int/neglected_diseases /resources/9789241547871/en/ 2. Harrison BA (2014) Field identification of adult or larval mosquitoes. Available at: http://www.gamosquito.org/resources/fg uideid.pdf 3. Aslamkhan M (1971) The mosquitoes of Pakistan I. Mosq Syst Newsletter. 3 (14): 147–159. 4. Rueda LM (2008) Global diversity of mos- quitoes (Insecta: Diptera: Culicidae) in fresh water. Hydrobiologia. 595: 477– 487. 5. Ashfaq M, Hebert PDN, Mirza JH, Khan AM, Zafar Y, Mirza MS (2014) Analyz- ing Mosquito (Diptera: Culicidae) diver- sity in Pakistan by DNA barcoding. PLoS One. 9(5): e97268. 6. Ali Z, Zahra G, Ali H, Khan BN, Bibi F, Khan MA (2015) Prevalence of dengue fever during 2011–2012. J Anim Plant Sci. 25(3 Supp. 2): 348–354. 7. World Health Organization (2017) Weekly Epidemiological Monitor. Available at: http://www.who.int. 8. Ramasay R, Sunderan SN (2012) Global cli- mate change and its potential impact on disease transmission by salinity-tolerant mosquito vectors in coastal zones. Front Physiol. 3: 198–210. 9. Sutherst RW (2004) Global change and hu- man vulnerability to vector borne dis- eases. Clin Micrbiol Rev. 17: 136–173. 10. Reiter P (2001) Climate change and mos- quito-borne disease. Environ Health Per- spect. 109(1): 141–161. 11. Gadahi J, Bhutto IB, Arijo AG, Akhtar N, Laghari Z, Memon MR (2012) Popula- tion diversity of mosquito fauna in and around Tandojam Pakistan. Int J Agro Vet Med Sci. 6(4): 290–295. 12. Qasim M, Naeem M, Bodlah I (2014) Mos- quito (Diptera: Culicidae) of Murree Hills, Punjab, Pakistan. Pak J Zool. 46(2): 523– 529. http://jad.tums.ac.ir/ https://www.who.int/neglected_diseases/resources/9789241547871/en/ https://www.who.int/neglected_diseases/resources/9789241547871/en/ http://www.gamosquito.org/resources/fguideid.pdf http://www.gamosquito.org/resources/fguideid.pdf http://www.scopemed.org/?jid=25&iid=2012-6-4.000 J Arthropod-Borne Dis, March 2020, 14(1): 106–115 F Manzoor et al.: Determination of … 115 http://jad.tums.ac.ir Published Online: March 31, 2020 13. Naeem-Ullah U, Akram W, Suhail A, Rana SA (2010) Grouping of different mosqui- to species on the bases of larval habitat, Pakistan. J Agri Sci. 47(2): 124–131. 14. Ali N, Rasheed SB (2009) Determination of species composition of mosquitoes found in Palosai stream, Peshawar. Pak Ento- mol. 31(1): 47–51. 15. Manzoor F, Nasir A, Fazal A (2013) Pop- ulation dynamics of different mosquito species at Lahore College for Women University, Lahore, Pakistan. J Mosq Res. 3: 12–20. 16. Aziz AT, Dieng H, Ahmad AH, Mahyoub JA, Turkistani AM, Mesed H (2012) Household survey of container-breeding mosquitoes and climatic factors influ- encing the prevalence of Aedes aegypti (Diptera: Culicidae) in Makkah City Sau- di Arabia. Asian Pac J Trop Biomed. 2(11): 849–857. 17. Yee DA, Allgood D, Kneitel JM, Kuehn KA (2012) Constitutive differences be- tween natural and artificial container mosquito habitats vector communities, resources, microorganisms, and habitat pa- rameters. J Med Entomol. 49(3): 482– 491. 18. Christophers SR (1933) The fauna of Brit- ish India including Ceylon and Burma, Diptera Family Culicidae, Tribe Anophe- line, Vol. 4. Taylor and Francis, London, p. 384. 19. Barraud PJ (1934) The fauna of British India including Ceylon and Burma, Dip- tera Family Culcidae, Tribe Megarhinini and Culicini, Vol. 5. Taylor and Francis, London, p. 384. 20. MacArthur R (1960) On the relative abun- dance of species. Am Nat. 94: 25–36. 21. Sengil AZ, Akkaya H Gonenc D (2011) Species composition and monthly distri- bution of mosquito (Culcidae) larvae in the metropolitan area Turkey. Int J Biol Med Res. 2(1): 415–424. 22. Shannon CE, Weaver W (1963) The Math- ematical Theory of Communication. Uni- versity of Illinois Press, Urbana. p. 131. 23. Simpson EH (1949) Measurement of diver- sity. Nature. 163: 688–689. 24. Khan MA, Salman C (1969) The bionomics of the mosquitoes of the Changa Manga National forest, West Pakistan. Pakistan J Zool. 1: 183–205. 25. Mukhtar M, Herrel N, Amerasinghe F, Ensink J, Hoek W, Konradsen F (2003) Role of waste water irrigation in mos- quito breeding in South Punjab, Paki- stan. Southeast Asian J Trop Med Pub- lic Health. 34(1): 72–80. 26. Ali N, Rasheed SB (2009) Determination of species composition of mosquitoes found in Palosai stream, Peshawar. Pak Ento- mol. 31(1): 47–51. 27. Service WM, Towson H (2002) The Anoph- eles vector, In: Arnold (Eds): Essential Malariology, Vol 2. London, UK, pp. 59–84. 28. World Health Organization (2013) World malaria report, Geneva. Available at: https://www.who.int/malaria/publicatio ns/world_malaria_report_2013/en/ http://jad.tums.ac.ir/ mailto:doc_farkhanda@yahoo.com https://www.who.int/malaria/publications/world_malaria_report_2013/en/ https://www.who.int/malaria/publications/world_malaria_report_2013/en/