Effect of Urbanization and Season on the Spatiotemporal Distribution of Mosquitoes in Bahawalpur, Pakistan

Robeela Shabbir1*, Farkhanda Manzoor1, Muhammad Oneeb2, Furqan Awan2 and Hania Ramzan1

1Department of Zoology, Lahore College for Women University (LCWU), Jail Road, Lahore, Pakistan

2Department of Parasitology, University of Veterinary and Animal Sciences (UVAS), Outfall Road, Lahore, Pakistan

ABSTRACT

Mosquitoes are disease-causing vectors that carry a variety of pathogens. Their diversity and spatiotemporal distribution are highly affected by urbanization and seasons. In this study, the mosquitoes were collected from six tehsils (Hasilpur, Ahmedpur East, Khairpur Tamewali Yazman Bahawalpur City and Bahawalpur Saddar,) of district Bahawalpur from September 2020 to August 2021. All the mosquitoes were morphologically identified by using standard identification keys. The data was analyzed using the Shannon-Wiener diversity Index, one-way ANOVA, and unpaired t-test. The highest number of mosquitoes was found in tehsil Bahawalpur Saddar while the lowest number was observed in tehsil Ahmedpur East. Of all the three genera collected, the genus Culex was highly abundant (75.89%), followed by Anopheles (19.08%) and Aedes (5.03%). Culex and Anopheles mosquitoes were found in all the six tehsils of Bahawalpur while Aedes mosquitoes were found in Bahawalpur City and Bahawalpur Saddar, only. The number of mosquitoes was higher in rural areas as compared to urban areas of four tehsils of district Bahawalpur calculated through t test.

Article Information

Received 24 July 2023

Revised 05 November 2023

Accepted 17 November 2023

Available online 18 December 2023

(early access)

Published 18 April 2025

Authors’ Contribution

FM and MO conceptualized and designed the study. RS performed field work and lab work and prepared the first draft. FA analyzed the data. HR reviewed and revised the manuscript. All authors approved the final manuscript to be submitted.

Key words

Spatiotemporal, Urbanization, Culex, Anopheles, Aedes

DOI: https://dx.doi.org/10.17582/journal.pjz/20230724151647

* Corresponding author: [email protected]

0030-9923/2025/0003-1041 $ 9.00/00

Copyright 2025 by the authors. Licensee Zoological Society of Pakistan.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Pakistan is a subtropical country that is rich in mosquito fauna (Imran et al., 2022). Mosquitoes can cause deadly diseases like dengue (Knowlton et al., 2009), malaria (Lawler and Lanzaro, 2005) West Nile fever (Styer et al., 2011), Chikungunya (Higgs and Vanlandingham 2015), Japanese Encephalitis, etc. (Attaullah et al., 2023).

Bahawalpur, a highly populated district of Pakistan, is also experiencing rapid mosquito-borne disease outbursts due to the high level of urbanization which causes mismanagement and deterioration in solid waste disposal (Mohsin and Chinyama, 2016). Due to rapid urbanization a change in anthropogenic landscape i.e., the development of parks, gardens, swimming pools, urban sewage systems, etc. is occurring which is affecting the diversity, spatiotemporal distribution, and abundance of mosquitoes (Ferraguti et al., 2016).

The influence of seasons on the breeding habitats of mosquitoes affects mosquito abundance. In the different seasons, temperature plays a key role. Temperature changes the period of maturity of adult mosquitoes (Tun-Lin et al., 2000; Bayoh and Lindsay, 2004). Rainfall in different seasons directly affects their breeding sites (Ceccato et al., 2005; Byun and Webb, 2012). The relative humidity is also one of the factors in the seasonal effects that regulate the oviposition and metabolism of adult mosquitoes (Ceccato et al., 2005; Reiter, 2001). All these climatic variables are therefore responsible for controlling many mosquito-borne diseases. (Wongkoon et al., 2013; Bashar and Tuno, 2014).

The present study aims to determine the specific patterns of diversity, abundance, and community composition of mosquitoes in different tehsils of district Bahawalpur. The effect of urbanization and seasons on the spatiotemporal distribution of mosquitoes is also investigated in this study. This study would be helpful in developing strategy for control of mosquito-borne diseases.

Materials and Methods

Study area

Sampling was done from district Bahawalpur (29.418° N and 71.670° E). The total area of this district is 24,830 km2. It is located 117 m above sea level. Administratively, it is divided into six tehsils; Bahawalpur City, Yazman, Bahawalpur Saddar, Hasilpur, Khairpur Tamewali, Ahmadpur East, and Khairpur. These tehsils are further divided into 78 rural and 29 urban areas. It is a highly populated district with a total population of 3,668,106. The population density of district Bahawalpur is 153.4 persons per km2. The climate is extremely dry and hot during summers and dry and cold during winters. The mean annual rainfall of Bahawalpur district is 169.8 mm. The rainfall usually occurs during the monsoon season i.e., July and August (https://bahawalpur.org/tehsils/).

Collection of mosquitoes

Adult mosquitoes were collected from specific sites on monthly basis from September 2020 to August 2021 from inside the houses outside gutters, cattle sheds, lawns, graveyards, zoos, etc., from different tehsils of Bahawalpur. The adult mosquitoes were collected with a CDC sweeper and mechanical aspirators.

Identification of mosquitoes

Mosquitoes were identified based on their morphological features using taxonomic keys (Christophers, 1933; Rueda, 2004; Barraud, 1934).

Statistical analysis

The Shannon diversity index (H) was applied to characterize species diversity in the six tehsils of district Bahawalpur. Shannon’s index accounts for both the abundance and evenness of the species present (Strong, 2016). Adult mosquito abundance between the six tehsils was compared using a one-way analysis of variance test (ANOVA) where significant differences were observed in an ANOVA test, Tukey’s post hoc analysis was used to separate the means. One-way ANOVA also helped to find the relationship between the abundance of mosquitoes with the season (Kim, 2017). The comparison of the abundance of mosquitoes between rural and urban areas of different tehsils of district Bahawalpur was analyzed through a student t-test (Kim, 2015).

Results

A total of 18,354 mosquitoes were collected from the six tehsils of Bahawalpur. Among all the three genera, the genus Culex was highly abundant (75.89%), followed by Anopheles (19.08%) and Aedes (5.03%). Genus Culex and Anopheles were found in all six tehsils. However, Aedes mosquitoes were found in two tehsils only i.e., Bahawalpur city and Bahawalpur Saddar (Fig. 1). It was observed that the highest number of mosquitoes were found in the tehsil Bahawalpur Saddar while the lowest number of mosquitoes were found in tehsil Ahmedpur East. A total of five species from the genus Culex were identified i.e., Culex quinquefasciatus (30.49%). Culex tritaenorhychus (27.42%), Culex pipiens (11.83%), Culex pseudovishnui (4.23%), and Culex vagans (1.92%). Similarly, five species of the Anopheles genus were identified i.e., Anopheles subpictus (10.5%), Anopheles culcifacies (5.76%), Anopheles stephensi (2.8%), Anopheles pulcherrimus (1.72%), and Anopheles nigerrimus (0.87%). Only two species, Aedes albopictus (3.4%) and Aedes aegypti (1.6%) were identified from the genus Aedes (Fig. 2).

 

 

Species diversity and abundance

In general, there were considerable differences between tehsils in terms of the diversity of species identified (n), Shannon diversity (H), and Simpson diversity (D) (Table I).

 

 

Table II. Abundance (Mean ± SD) of mosquitoes in different Tehsils of District Bahawalpur.

Species	Bahawalpur	Hasilpur	Ahmadpur east	Khairpur	Yazman	Saddar	F	P
C. quinquefasciatus	738.67± 17.04e	1128.33± 15.28a	705e± 16.09	105.67± 10.5b	1005.3± 18c	963.33± 12.01d	394.56	0.001
C. tritaenorhychus	828.67± 16.56b	816b± 14.73c	717.67d±17.04	773.7± 17.5c	774± 17.09c	1118.7± 17.6a	217.62	0.001
C. pseudovishnui	91.33± 17.01d	171.67± 15.04ab	75.67d± 11.5	134± 15.72bc	102± 13.11cd	201.67± 14.57a	34.1	0.001
C. pipiens	293± 13.11c	460±12a	238.67± 16.04b	383.67± 13.05b	327.67± 11.5c	464±11a	150.3	0.001
C. vagans	35.67± 2.52c	74.33a± 14.5b	35±2c	65.67± 5.13ab	58.33± 3.51b	82.67± 3.06a	26.26	0.001
A. subpictus	324± 17.09b	396.3± 17.6a	273±14c	346.67± 12.06b	316.33± 16.5b	272.33± 13.5c	28.45	0.001
A. stephensi	64.33± 5.13d	134.67± 5.03a	64d± 5.29	103.33± 7.64b	84± 5.29c	17.33± 4.51cd	74.73	0.001
A. culcifacies	159.67± 16.17bc	237.3± 19.5a	137.67± 17.01c	201.67± 10.5ab	178.67± 13.58bc	146.67± 14.5c	17.6	0.001
A. pulcharimus	39.33± 1.52d	80.67± 3.06a	39.67d± 1.52	64.33± 3.06b	53.33± 4.16c	40.33± 2.52d	108.69	0.001
A. negirrimus	21.67b± 1.52c	37.67± 2.52a	21±1bc	32.67± 2.08a	26±3b	20±1c	38.82	0.001
A. albopictus	217.3± 30.4b	0±0c	0±0c	0±0c	0±0c	419.3± 30a	307.17	0.001
A. aegypti	77.33±15.04a	0±0c	0±0c	0±0c	0±0c	214.33± 16.17a	278.61	0.001

 

The Shannon and Simpson diversity indices for the six tehsils, respectively, ranged from 2.01 to 1.76 and 0.82 to 0.77. The tehsil Saddar has the greatest and tehsil Ahmedpur East had the lowest values for both indices, respectively. Significant variations in mosquito abundance were found in all of the tehsils after analysis of variance (ANOVA) tests were performed. Hasilpur had the highest concentration of Culex quinquefasciatus (F = 394.56, df = 5, P < 0.001), followed by Khairpur Tamewali, Yazman, Saddar, Bahawalpur, and Ahmedpur East with the lowest concentration (Table II). Aedes aegypti was a rare species in this district that was absent from Hasilpur, Khairpur Tamewali, Yazman, and Ahmedpur East tehsils but highly dispersed in Bahawalpur and Saddar tehsils (F = 278.61, df = 5, P < 0.001). In the other tehsils of Bahawalpur, every species displayed a similar trend of abundance.

Relationship of the abundance of mosquitoes with seasons

Interesting findings were obtained via a one-way ANOVA on the seasonal abundance of mosquitoes. The research revealed that each tehsil’s mosquito population was at its highest during the monsoon season, followed by fall, and at its lowest during the winter. In comparison to the summer, there were more mosquitoes in the spring. The Hasilpur tehsil had the greatest Culex quinquefasciatus count (F = 85.81, df = 4, P = 0.001) (Table III). Its peak levels of abundance were noted in the autumn (Mean = 299, SD= 15.72) and monsoon seasons (Mean = 299.33, SD= 12.06), with a sharp decline in abundance throughout the winter (Mean = 125, SD= 15.01). In the spring, it increases once more (Mean = 237, SD = 17), and in the summer, it decreases (Mean = 160, SD = 14.1) (Table III). Anopheles subpictus of the genus Anopheles displayed the same

 

Table III. Relationship of abundance of species of mosquitoes with seasons in Tehsil Hasilpur of District Bahawalpur.

Species	Mean ± Standard Deviation					F	P
	Autumn	Winter	Spring	Summer	Monsoon
Culex quinquefasciatus	299± 15.72a	125± 15.01c	237±17b	160± 14.11c	299.33±12.06a	85.81	0.001
Culex tritaenorhychus	243.67±11.02a	79.3± 18.5c	149±14b	109.33± 13.01c	238.67±11.02a	88.01	0.001
Culex pseudovishnui	46±3b	15±3c	32.33±2.52bc	26.66± 1.52c	54.33±15.04a	14.4	0.001
Culex pipiens	120±16.52a	37.67± 2.52b	103.33±13.5a	64± 17.09b	133±12.53a	26.06	0.001
Culex vagans	20.66±1.52a	6±1c	10.33±2.08bc	11.33± 1.52b	25.33±2.52a	58.49	0.001
Anopheles subpictus	141.33±14.05a	22±3b	116±16a	0b	119.7±17.5a	79.98	0.001
Anopheles stephensi	45.67±2.52a	9.76± 2.08c	38.33±1.52b	0b	41.67±2.08ab	372.42	0.001
Anopheles culcifacies	67.3±18a	7±1b	61.7±17.5a	0b	66.67±15.5a	19.82	0.001
Anopheles pulcherrimus	19.33±1.52ab	6.33± 1.52c	17.33±2.52b	0b	23.67±2.08a	94.29	0.001
Anophels nigerrimus	11.66±1.52a	2.67b± 2.08c	6.3±1.52b	0c	11.33±2.08a	30.09	0.001
Aedes albopictus	0	0	0	0	0	0	0
Aedes aegypti	0	0	0	0	0	0	0

 

Table IV. Relationship of abundance of species of mosquitoes with seasons in Tehsil Saddar of District Bahawalpur.

Species	Mean ± Standard deviation					F	P
	Autumn	Winter	Spring	Summer	Monsoon
Culex quinquefasciatus	295.67±14.57a	80±20c	139.6±16.17b	167.3± 12.01b	283.33±15.57a	104.06	0.001
Culex tritaenorhychus	320±17a	98.67± 13.01c	171.6±14.01b	200.6± 17.04b	325.67±14.5a	125.1	0.001
Culex pseudovishnui	48±15.72b	11±3d	36.67±2.08bc	19.33± 2.52d	81.67±13.05a	26.41	0.001
Culex pipiens	138.6±12.01a	35±3c	69.67±14.5b	74± 14.53b	149.67±13.58a	47.26	0.001
Culex vagans	15±3bc	2.67± 2.08d	16.66±1.52b	10.33± 2.08c	37.33±2.52a	94.79	0.001
Anopheles subpictus	87.33±16.01a	16.67± 2.52b	78±a14.73	0b	93±18.5a	34.25	0.001
Anopheles stephensi	19±3b	5±1c	21±1ab	0d	24.33±2a	11.93	0.001
Anopheles culcifacies	52.33±13.05a	10.33± 1.52b	37±3a	0b	48.66±1.52a	44.48	0.001
Anopheles pulcherrimus	10.33±1.52a	3.33± 1.52b	13.66±1.52a	0b	12.67±2.52a	40.81	0.001
Anopheles negirrimus	5±1b	2±1cd	4±1bc	0d	9.33±1.52a	34.75	0.001
Aedes albopictus	146.6±16.17a	16.33± 2.52c	71±15.52b	62.33± 15.01b	125±14.11a	43.51	0.001
Aedes aegypti	72.33±14.5a	9±1c	35.67±2.52b	26.33± 2.08bc	73±13a	31.15	0.001

 

Table V. Relationship of abundance of species of mosquitoes with seasons in Tehsil Khairpur East of District Bahawalpur.

Species	Mean ± Standard deviation					F	P
	Autumn	Winter	Spring	Summer	Monsoon
Culex quinquefasciatus	289.67±13.58a	109.67±15.18d	222.67± 10.5b	152.67± 13.01c	284.67±16.62a	98.2	0.001
Culex tritaenorhychus	226.3±19.5a	71.67±15.57c	152.67± 17.01b	99±14c	226.67±15.5a	56.49	0.001
Culex pseudovishnui	36.33±2.08a	13.66±1.52c	27.33± 2.52b	18.67± 2.08c	35.67±2.08a	70.5	0.001
Culex pipiens	102.33±15.5a	32.66±1.52c	84.67± 13.65ab	51.67± 15.28bc	108.3±17.5a	16.58	0.001
Culex vagans	16.66±1.52b	5.33±1.52d	11±2c	10.33± 2.08cd	23±3a	31.19	0.001
Anopheles subpictus	120±18a	18.67±2.08b	101±16a	0b	107.67±16.04a	55.31	0.001
Anopheles stephensi	33±3a	8.67±2.08b	30±1a	0c	34.67±2.08a	201.8	0.001
Anopheles culcifacies	67.3±18a	7±1b	61.7± 17.5a	0b	66.67±15.5a	19.82	0.001
Anopheles pulcherrimus	19.33±1.52ab	6.33±1.52c	17.33± 2.52b	0d	23.67±2.08a	94.29	0.001
Anopheles nigerrimus	11.66±1.52a	2.67±2.08bc	6.33± 1.52b	0c	11.33±2.08a	30.09	0.001
Aedes albopictus	0	0	0	0	0	0	0
Aedes aegypti	0	0	0	0	0	0	0

 

Table VI. Relationship of abundance of species of mosquitoes with seasons in Tehsil Yazman of District Bahawalpur.

Species	Mean ± Standard deviation					F	P
	Autumn	Winter	Spring	Summer	Monsoon
Culex quinquefasciatus	282±12.53a	89.3± 17.5d	216.67±16.5b	136.7± 19c	277.33±14.57a	83.74	0.001
Culex tritaenorhychus	211.67±16.01a	59± 11.53c	183.67±13.58a	108.3± 18b	59±13.5c	66.25	0.001
Culex pseudovishnui	29.33±2.52a	10.33± 1.52c	21.67±2.08b	15.67± 2.52c	27.33±2.08ab	39.95	0.001
Culex pipiens	87.67±11.02a	25.33± 2.08c	77.7±17.5ab	50± 1bc	85.67±13.05a	18.02	0.001
Culex vagans	14.33±2.52b	5.67± 2.08c	10.33±1.52bc	10± 1bc	19.33±1.52a	24.36	0.001
Anopheles subpictus	107±14.53a	14±1b	94.33±12.5a	0b	99±18.5a	55.79	0.001
Anopheles stephensi	45.67±2.52a	9.67± 2.08c	88.33±1.52b	0d	41.67±2.08b	372.42	0.001
Anopheles culcifacies	74±19a	7±1b	69.67±16.62a	0b	83±11.53a	30.86	0.001
Anopheles pulcherrimus	27±3a	9±1c	19.33±2.52b	0d	24.33±2.08ab	91.91	0.001
Anopheles nigerrimus	15±1a	3±1c	8±1b	0c	12.33±2.52a	62.77	0.001
Aedes albopictus	0	0	0	0	0	0	0
Aedes aegypti	0	0	0	0	0	0	0

 

Table VII. Relationship of abundance of species of mosquitoes with seasons in Tehsil Ahmadpur East of District Bahawalpur.

Species	Mean ± Standard deviation					F	P
	Autumn	Winter	Spring	Summer	Monsoon
Culex quinquefasciatus	229.33±12.01a	80±15.1b	89.67±17.01b	80.67± 11.02b	230±20a	81.52	0.001
Culex tritaenorhychus	227±15.52a	77±18b	99.67±11.02b	93.33± 17.04b	220.33±14.57a	69.04	0.001
Culex pseudovishnui	23.66±1.52a	9.33±1.52b	7±1b	9.67± 2.08b	27±3a	67.72	0.001
Culex pipiens	77.33±10.5a	26.33±2.52b	30.67±2.08b	29.66± 1.52b	77.33±16.5a	26.79	0.001
Culex vagans	9.67±2.08a	2±1b	6.67±2.08a	8.33± 1.52a	10.33±1.52a	11.59	0.001
Anopheles subpictus	86.67±16.56a	13±1b	86.67±15.28a	0	85.3±18.5a	3.99	0.001
Anopheles stephensi	116.67±2.08b	4±1c	18±3b	0c	23.66±1.52a	90.18	0.001
Anopheles culcifacies	43.33±2.08ab	5.67±2.08c	40±2b	0d	47.67±2.52a	403.9	0.001
Anopheles pulcherrimus	10±1b	4.67±2.08c	15±2a	0d	10.66±1.52b	43.46	0.001
Anopheles nigerrimus	5.33±1.52a	2±1b	7±1a	0b	7±1a	27.72	0.001
Aedes albopictus	0	0	0	0	0	0	0
Aedes aegypti	0	0	0	0	0	0	0

 

Table VIII. Relationship of abundance of species of mosquitoes with seasons in Tehsil Bahawalpur of District Bahawalpur.

Species	Mean ± Standard deviation					F	P
	Autumn	Winter	Spring	Summer	Monsoon
Culex quinquefasciatus	227±15.72a	74±15.52b	104±17.09b	98±12b	234.33±12.06a	82.78	0.001
Culex tritaenorhychus	251±15a	108±14b	108±14.73b	103.33± 11.02b	251±15.1a	95.29	0.001
Culex pseudovishnui	31.33±2.52a	13.67±2.08b	10±1b	11±2b	27±3a	59.1	0.001
Culex pipiens	95.67±16.5a	34.33±1.528b	37.67±2.08b	38.67± 2.52b	92±14.73a	29.18	0.001
Culex vagans	10±1a	2±1b	6.67±2.08a	8.33± 1.52a	10.33±1.52a	15.65	0.001
Anopheles subpictus	96.67±16.04a	14±3b	104±14.11a	0	110±13.11a	66.93	0.001
Anopheles stephensi	19.33±2.52a	5±1b	19.67±2.08a	0c	20±2a	87.69	0.001
Anopheles culcifacies	50.33±1.52a	6.67±2.08b	46.33±1.52a	0b	55±19a	27.73	0.001
Anopheles pulcherrimus	11.33±1.52b	3±1c	16±2a	0c	9.67±2.08b	53.64	0.001
Anopheles nigerrimus	6±1ab	2.67±2.08bc	6±1ab	0c	8.67±2.08a	15.94	0.001
Aedes albopictus	64±12.53a	16.33±2.08b	24±2b	23.33± 2.08b	83.33±14.05a	36	0.001
Aedes aegypti	28.33±2.08a	6.33±1.52c	9.67±2.08c	11±2c	21±1b	78.04	0.001

 

pattern of abundance as that of Culex quinquefasciatus. It was highest in the autumn season (Mean =119.33, SD=17.5), and it was lowest in the winter (Mean =0, SD = 0). It was highest during the monsoon season (Mean =119 SD=17.5) and spring (Mean =116, SD=16). This tehsil’s Aedes aegypti population was found to be missing. Its existence in Tehsil Saddar (F = 31.15, df = 4, P = 0.001) demonstrated a consistent seasonal pattern, with monsoon season occurrence being highest (Mean =73, SD=13) and winter season occurrence being lowest (Mean=9, SD=1) (Table IV) The association between abundance and the season of the other species displayed the similar trend as that of Culex and Anopheles (Tables III-VIII).

 

 

Comparative analysis between rural and urban areas

The unpaired t-test was used to compare mosquito populations in different tehsils of the Bahawalpur district between rural and urban areas. According to the findings, the abundance of mosquitoes in the tehsils of Hasilpur, Ahmedpur East, Khairpur Tamewali, and Yazman were significantly high in rural as compared to urban areas (Fig. 3 and Table IX). Tehsil Yazman recorded a highly significant outcome (t= 2.64, p= 0.028, F= 3.530). Results in the tehsils of Bahawalpur (t= 1.617, p= 0.144) and Saddar (t= 2.059, p= 0.073) were not statistically significant (Fig. 4), indicating that these areas are heavily urbanized with little distinction between rural and urban areas.

 

Table IX. Comparative analysis between rural and urban areas of different tehsils of district Bahawalpur.

Tehsils	t	p	F	Difference between Means± Standard error
Hasilpur	2	0.0396	3.117	561.6±228.7
Ahmedpur east	2.38	0.044	3.163	410.4±171.9
Khairpur	2.50	0.0347	3.247	528±207.9
Yazman	2.664	0.0286	3.530	521.2±195.6
Saddar	2.059	0.0734	2.291	523.2±245
Bahawalpur	1.617	0.1446	1.86	326.4±201.9

 

Discussion

This is the first time in Pakistan that the spatiotemporal distribution of the mosquitoes in all the tehsils of Bahawalpur is studied along with the comparative analysis of diversity, composition, and abundance of all the genera of mosquitoes between rural and urban areas of different tehsils of Bahawalpur. This study also describes the effect of urbanization and environmental variables on the spatiotemporal distribution of mosquitoes in the Bahawalpur district.

Mashaal (1964) has reported only 2 species of Anopheles, Anopheles stephensi and Anopheles culcifacies as malaria vectors in South Punjab. Different species of Anopheles i.e., Anopheles subpictus, Anopheles culicifacies, Anopheles stephensi, Anopheles pulcherrimus, Anopheles Peditaeniatus, and Anopheles nigerrimus have also been reported from South Punjab (Herrel, 2001). All species except Anopheles Peditaeniatus were found in this current study. Similarly, Anopheles subpictus, Anopheles stephensi, Anopheles culcifacies, and Anopheles pulcherrimus have also been reported, previously. Culex quinquefasciatus, Culex tritaeniorhynchus, and Aedes mosquitoes were also found in wastewater in South Punjab (Mukhtar et al., 2003).

In the current study, the species of genus Culex (5 species) and genus Anopheles (5 species) were reported in all the rural and urban areas of Bahawalpur. Mosquito abundance and species richness were higher in rural areas than in urban areas. These results agreed with those from previous studies conducted in Europe (Hay et al., 1997; Johnston et al., 2014) where anthropogenic habitats usually show the lowest abundance of mosquitoes. Rural areas, with freshwater, are more favorable breeding environments, despite those urban areas that may provide suitable habitats for some particular mosquito species (Cox et al., 2007).

Aedes mosquitoes were found absent from Tehsil Hasilpur, Khairpur Tamewali, Yazman, and Ahmedpur East. These are periurban areas that are in transition from rural to urban. zone. The species of Aedes were sparsely distributed in tehsils Bahawalpur and Saddar. The main reason for the occurrence of Aedes in these tehsils was heavy urbanization which was not found in other tehsils. With time, urbanization has increased in these areas due to the conversion of agricultural, forest, and fallow land into urban land (Hussain et al., 2020). With exceptional population growth and rapid urban development, the number of hospitals and clinics has increased several folds which has resulted in huge hospital waste and poor drainage providing favorable conditions for mosquito breeding, especially Culex spp. (Khan et al., 2020). The high number of animals in the Bahawalpur Zoo also benefits a variety of mosquito species (Derraik, 2004), especially the Aedes mosquitoes which require artificial containers for their breeding (Tuten et al., 2012). In highly urban areas, used tires are not disposed of properly. They effectively hold rainwater and rapidly warm in sunlight even during winter thus providing an ideal breeding habitat for Aedes (Khan et al., 2017). Similar results were found in a study conducted in North India where it was observed that tires provide favorable breeding sites for Aedes aegypti (Sikhon and Minhas, 2014).

Our study showed that the mosquito species occurred in all six tehsils of Punjab throughout the year in all seasons. The highest abundance was found in the season of monsoon that was during July and August. This has been proved in Pakistan (Resin and Milby, 1986; Mukhtar et al., 2003; Ashfaq et al., 2014; Akram et al., 2009; Fatima et al., 2016) and other countries (Roiz et al., 2014; Valentine et al., 2020). We found the positive effect of precipitation on the relative abundance of mosquito species. The precipitation increases the number of habitats of larvae (Evans et al., 2019). It also has a profound effect on the relative humidity which in turn increases the richness, life span, and host-seeking behavior of mosquitoes (Asigau and Parker, 2018). On the other hand, excessive rain may flush larvae from their habitats and decrease adult mosquito populations (Dieng, 2012).

The current study showed that a high number of species were also found during spring and autumn. During early spring and winter, few species were recorded. The number of species increased again in late April with an especially high peak in May. In addition, the population density was higher in autumn, especially in September and October. The same results were observed in Pakistan, previously (Akram et al., 2009) and around the globe (Alten et al., 2000; Santos et al., 2020).

It is concluded through this study that changes in the landscape due to urbanization strongly affect the abundance, community composition, and diversity of mosquitoes. Mosquito populations are also affected by changes in climate. This information in the future would be helpful for the public health to design surveillance programs to control the diseases caused by mosquitoes in the reported areas.

Acknowledgement

The author acknowledge the help of the Muhammad Asif (Entomologist), MEP Department, Institute of Public Health Lahore for the collection of mosquito.

Funding

The author received no financial support for research, authorship, and/or publication of this article

Statement of conflict of interest

The authors have declared no conflict of interest.

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