Distribution Patterns of Insect Pollinator Assemblages at Deva Vatala National Park, Bhimber, Azad Jammu and Kashmir

Mubashar Hussain1,2*, Hifza Liaqat1, Muhammad Faheem Malik1,

Kiran Aftab1, Moazama Batool3, Razia Iqbal1 and Somia Liaqat1

1Department of Zoology, University of Gujrat, Gujrat, 50700, Pakistan

2UWA School of Agriculture and Environment, University of Western Australia, Perth, Australia

3Department of Zoology, Govt College Women University, Sialkot, 51310, Pakistan

ABSTRACT

Diversity and distribution patterns of pollinator assemblages were explored at Deva Vatala National Park (DVNP), Bhimber, AJK, Pakistan. Sampling was recorded fortnightly by using pan traps, sweep nets, and handpicking. A one-year survey of pollinator fauna was recorded from selected locales of DVNP from October 2019 to September 2020. We observed the same species richness in all three study sites, but a great difference was observed in species abundance. A total of 5565 individuals of 58 species belonging to 23 families and four orders were collected from DVNP. Barmala was reported as the highest abundant site (2815 individuals), followed by the Vatala (1832 individuals) and Deva (918 individuals). SIMPER analysis indicated an overall dissimilarity of Deva-Vatala (18.88%), Deva-Barmala (29.12%), and Vatala-Barmala (10.84%). The biological dissimilarity was evaluated and based on insect taxonomy indicated that Coccinella septempunctata, Sceliphron madraspatanum, Aedes albopictus, Eristalis tenax, Crambus albellus, Zonitoschema melanarthra, Zonitoschema gibdoana, Camponotus vagus, Polistes carolira, and Episyrphus viridaureus were the main contributing species in the community dissimilarity. Results showed significant differences between Vatala - Deva with higher Shannon value in Vatala (H’ = 4.03) than Deva (H’ = 3.92), Deva-Barmala with higher Shannon index in Barmala (H’ = 4.05) than Deva (H’ = 3.92) and Vatala-Barmala have a higher average value of Shannon diversity in Barmala (H’ = 4.05) than Vatala (H’ = 4.03). DVNP offers habitat and plentiful resources for the insect pollinator assemblages of four major insect orders, viz. Lepidoptera, Hymenoptera, Diptera, and Coleoptera. We detected variations in the abundance of different insect groups (orders, families, and species) during different seasons and study sites within DVNP. This study emphasizes the conduct of research work based on more explorative surveys in association with vegetation types.

Article Information

Received 04 October 2022

Revised 20 January 2023

Accepted 11 February 2023

Available online 29 April 2023

(early access)

Published 22 May 2024

Authors’ Contribution

MH, HL and SL conceived the idea, conducted research, analyzed data and wrote the manuscript. MFM, KA, MB and RI contributed in data analysis and critically reviewed the manuscript.

Key words

Pollinators, DVNP, Insect fauna, Biodiversity

DOI: https://dx.doi.org/10.17582/journal.pjz/20221004171007

* Corresponding author: [email protected]

0030-9923/2024/0004-1639 $ 9.00/0

Copyright 2024 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

Insects represent the most abundant and diverse animal taxa, which provide a wide range of ecosystem services such as pollination, biological control of pests, decomposition, and conservation of biodiversity (Losey and Vaughan, 2006). Insect pollination contributes significantly to the ecological processes of all terrestrial ecosystems (Bohan et al., 2016). Insects are known to pollinate over 80% of wild plants and about 75% of cultivated species (Thomann et al., 2013; Sataral and Rustiawati, 2019). Insect pollinators diversity and ecological role directly or indirectly influence agriculture, human health, and natural resources (Scudder, 2017). For example, the ecological role of insect pollinators positively impacts the quality and quantity of crop yield by providing pollination services. Additionally, many insect pollinators are useful in environmental pollution monitoring, help in pest management, and have cultural and aesthetic significance (Katumo et al., 2022a).

Studies suggest a global decline in the diversity and densities of insect pollinators results in reduced pollination (Aizen et al., 2008; Aizen and Harder, 2009; Lautenbach et al., 2012; Polce et al., 2014). Global declines in the diversity of insect pollinators owes to many adverse factors including mainly adverse effects of climate change and habitat modifications (Didham et al., 1996; Siregar et al., 2016), mainly due to a decrease in food resources, nesting, oviposition, resting, and mating sites (Kevan, 1999). Additionally, recent shifts in land use, mainly converting natural habitats to croplands, may adversely affect species, which ultimately lower pollination services and consequently dent biodiversity (Astegiano et al., 2015; Klein et al., 2012; Kremen et al., 2002).

Several pollinator communities consist of many insect taxa but most of the pollinators insect species belong to four major insect orders: Coleoptera (beetles), Hymenoptera (bees and wasps), Diptera (flies), and Lepidoptera (moths and butterflies). Insect pollinators from these four major orders can provide pollination services to a variety of crops and plantations (Rader et al., 2016). These insects pollinate crops and wild plants which ensure biodiversity, provide food, form and improve habitats for many animals and provision of natural resources (Gill et al., 2016; Wardhaugh, 2015; Ollerton, 2017).

Several factors influence the composition, diversity and abundance of pollinator species such as habitat composition, floral abundance, plant diversity, agricultural practices, pesticide exposure, parasites and pathogens (Dyola et al., 2022; Khan et al., 2014; Macdonald et al., 2018; Katumo et al., 2022b; Ganuza et al., 2022; Abrahamczyk et al., 2011; Plascencia and Philpott, 2017). Population dynamics of pollinators vary during seasons and in different landscapes (Bashir et al., 2015). Deva Vatala National Park (DVNP) has a great significance in the conservation of many animal and wild plant species by providing habitat with plentiful resources (Akrim et al., 2015; Umar and Hussain, 2023). Pollinators in this protected area help to maintain a healthy ecosystem by ensuring genetic diversity (Anwar et al., 2015). Despite its ecological significance and contribution in the biodiversity conservation, the diversity of insects in DVNP is threatened due to habitat degradation, human population pressure, intensive agricultural practices and use of pesticides (Anwar et al., 2015; Umar et al., 2021). Therefore, keeping in view the significance of insect pollinators in the protected areas, we explored the diversity of four major insect pollinator taxa (coleoptera, diptera, lepidoptera and hymenoptera) at DVNP, Bhimber, AJK. Additionally, we studied the patterns of distribution of diversity and abundance of these species in three main sites, viz. Deva, Vatala and Barmala.

MATERIALS AND METHODS

Study area

Deva Vatala National Park (DVNP), Bhimber (32°51-32°55 N, 74°16-74°24 E; an elevation of 267 to 536 m above sea level) covers an area of 2,993 ha was and it was declared as a National Park in 2007 (Umar et al., 2021). DVNP is characterized by sub-tropical semi-evergreen forests (Grimmett et al., 2008) and cultivated areas (Anwar et al., 2015) for wheat, maize, millet and mustard. Major plant species in the study area include Acacia modesta, Dalbergia sissoo, Acacia nilotica, Ficus benghalensis, Mangifera indica, Dodonaea viscosa, Carissa opaca, Ziziphus nummularia, Cynodon dactylon, Desmostachya bipinnata, Butea monosperma, Lannea coromandelica, S. spontaneum, V. nilotica, Salvia spp., Senna occidentalis, Zanthoxylum armatum and Saccharum spontaneum (Azam et al., 2007). We sampled insect pollinators during October 2019 to September 2020 from three main sites DVNP. These sites within DVNP were selected based on topography, anthropogenic activities, agricultural practices, access to the area and the significance of these sites to represent the DVNP (Umar et al., 2021) (Fig. 1).

 

The hilly forests of Barmala (32°52’58.7” N, 74°20’18.97” E; 350-411m asl) have seasonal streams and different vegetation layers. The forests of Deva (32°54’8.6” N, 74°21’29.7” E; 306-381m asl) is situated closer to the line of control (LoC) which is a military control line between the Indian and Pakistani controlled parts of the former princely state of Jammu and Kashmir, whereas Vatala (32°52’38.7” N, 74°17’44.7” E; 350-396 m asl) shares a similar plant community composition to the other sites (Umar et al., 2021).

Sampling methods

Sampling was performed fortnightly on bright sunny days by using pan traps, sweep nets and hand picking. Surveys were conducted randomly in the mornings (08:00-10:00 h) and afternoons (16:00-18:00 h). We used different pan traps (blue, yellow, and white) to capture the diversity of floral visitors (Wilson et al., 2008). The traps were filled with soap water to reduce surface tension and were placed with alternate colors in saline in open and visible places. The traps were fixed in a selected area in the morning and removed in the afternoon to record all the insect visitors. Then, soap water in pan traps was strained to separate trapped specimens by passing through a net. Insect collections were stored in sealed plastic bags. While using sweep nets (about 30 cm in diameter), we swept randomly over vegetation by transect walks (El-Abdouni, 2022). We also performed sampling by observations and handpicking along the transect walk. Based on the general floral resources in the study area, we grouped monthly sampling efforts into summer (March-September) and winter (October-February) months to document seasonal shifts in the diversity and abundance of the insect pollinators species.

Preservation and identification of specimens

The specimens were preserved in absolute alcohol (Schauff, 2001) and were identified using taxonomic identification keys up to species level (Perveen and Ahmad, 2012; Perveen and Fazal, 2013).

Statistical analysis

The species relative abundance was calculated to compare the species abundance in three sites. Species richness measures biodiversity by providing the number of species in each area, which depends greatly on sampling size and effort (Hussain et al., 2021; Magurran, 2004). Species abundance, dominance, richness and evenness were measured by using Shannon–Wiener index (Shannon and Weaver, 1949). We also applied Two-way ANOVA to determine the significance between means of the insects within each order among the three sites. We also determined the differences between insect pollinator species by using Analysis of Similarities (ANOSIM) by comparing the three study sites using PAST software. For ANOSIM, the data were pre-treated with square root transformation to down-weight the effect of the most abundant species (Umar et al., 2021). The contribution of each species (%) to the dissimilarity between sites was calculated using SIMPER (similarity percentages) analysis.

RESULTS

Relative abundance of four pollinator orders of insects at DVNP

We reported 58 species belonging to 23 families within four insect orders: Coleoptera, Diptera, Lepidoptera, and Hymenoptera. A total of 5565 insects were collected, the maximum number of individuals belonged to the order Lepidoptera which was significantly different from Hymenoptera, Diptera, and Coleoptera (Fig. 2).

 

Comparison of means between three sites using ANOVA indicated significant differences number of individuals of insects belonging to four orders (F(2, 162) = 215.5840, p < .0001). The data also showed differences in relative abundance between the three sites: Deva (48.02 %), Vatala (31.88%) and Barmala (16.69%). Interestingly, we observed non-significant differences in the means between individuals of different orders (F(3, 162) = 2.14, p = 0.079).

 

Seasonal abundance of insects at DVNP

ANOVA results showed significant differences in the means between summer and winter (F(3, 324) = 15.50, p < 0.0001).Data presented in Figure 3 showed lepidoptera was the most abundant insect order across the three sites. The highest relative abundance (%) of Lepidoptera was recorded in Barmala (44.51%) followed by Vatala (42.63%) and then in Deva (41.61%). Hymenoptera showed almost similar relative abundance in all three sites (Fig. 3). Coleoptera and Diptera showed relatively lower abundance though the difference between these orders was significant (F(2, 162) = 215.58, p = .0001).

 

Overall comparison of means across three sites indicated significant differences between winter and summer season (Fig. 4). We observed that higher mean values in summer across all three sites. Coleoptera in summer demonstrated highest mean individuals in Barmala followed by Vatala and Deva. Similar pattern of mean abundance was observed for Diptera, Hymenoptera and Lepidoptera (Fig. 4).

Diversity of insect pollinator families

Data presented in Table I shows the relative abundance (%) of insect orders, families, and species in Deva, Vatala, and Barmala. Results indicated that out of the four insect pollinator orders, the maximum number of families belonged to order Lepidoptera (ten families) followed by Hymenoptera (seven families), Diptera (three families), and Coleoptera (three families). within Hymenoptera order, we observed maximum species in vespidae (six) followed by Formicidae (five) and Apidae (three). However, the highest abundance was shown by Polistes carolira (2.83 %) in Deva (Table I). We recorded three families in order diptera with maximum number species belonged to the family syrphidae (six) with highest abundance showed by Episyrphus viridaureus (2.94 %) in Deva (Table I). We documented ten families from order Lepidoptera with greater number of species were detected in Pieridae (six) followed by Nymphalidae (five). In order Coleoptera, three species belonged to Meloidae followed by Coccinellidae (two species).

 

Table I. Relative abundance (%) of orders, families, and species in Deva, Vatala, and Barmala from Deva Vatala National Park (DVNP), Bhimber, AJK.

Order/Family	Species	Relative abundance (%)
		Deva	Vatala	Barmala	Overall DVNP
Order: Coleoptera (10.13 %)
Cantharidae (1.39)	Rhagonycha fulva	1.42	1.47	1.28	1.39
Coccinellidae (3.40)	Adalia bipunctata	1.2	1.09	1.24	1.18
	Coccinella septempunctata	2.61	2.07	1.99	2.22
Meloidae (6.54)	Mylabris postulate	2.07	2.02	1.99	2.03
	Zonitoschema gibdoana	2.51	2.02	1.81	2.11
	Zonitoschema melanarthra	2.94	2.24	2.02	2.40
Order: Diptera (13.19 %)
Culicidae (2.07)	Aedes albopictus	2.40	2.02	1.78	2.07
Muscidae (2.73)	Musca domestica	1.42	1.58	1.53	1.51
	Ophyra spinigera	0.97	1.36	1.31	1.21
Syrphidae (8.72)	Episyrphus viridaureus	2.94	2.02	1.74	2.23
	Eristalis arbustorum	1.09	1.31	1.46	1.29
	Eristalis nemorum	0.65	1.26	1.35	1.09
	Eristalis tenax	2.61	1.91	1.85	2.12
	Paragus annandalei	2.51	1.8	1.67	1.99
			Table continued on next page................
Order/Family	Species	Relative abundance (%)
		Deva	Vatala	Barmala	Overall DVNP
Order: Hymenoptera (32.47 %)
Apidae (6.17)	Amegilla punctifrons	1.96	1.75	1.85	1.85
	Apis dorsata	2.4	2.29	2.06	2.25
	Apis mellifera	2.18	1.97	2.06	2.07
Crabronidae (1.07)	Trypoxylon californicum	0.44	1.31	1.46	1.07
Eumenidae (1.70)	Anterhynchium flavomarginatum	2.07	1.42	1.6	1.70
Formicidae (8.74)	Camponotus pennsylvanicus	0.33	1.2	1.46	1.00
	Camponotus vagus	1.53	1.86	1.81	1.73
	Lasius nigar	1.96	1.97	1.85	1.93
	Solenopsis invicta	2.18	2.07	1.95	2.07
	Tapinoma sessile	2.18	2.02	1.85	2.02
Masaridae (1.23)	Celonites hermon	0.65	1.47	1.56	1.23
Sphecidae (2.35)	Sceliphron madraspatanum	2.51	2.4	2.13	2.35
Vespidae (10.98)	Allorhynchium argentatum	0.76	1.58	1.56	1.30
	Anterhynchium abdominale	0.65	1.09	1.21	0.98
	Delta conoideum	2.51	2.18	1.99	2.23
	Polistes carolira	2.83	2.51	2.13	2.49
	Polistes wattii	2.06	2.07	1.99	2.04
	Vespa tropica	1.84	2.02	1.95	1.94
Order: Lepidoptera (43.41 %)
Crambidae (5.14)	Cnaphalocrocis medinalis	2.4	1.91	1.95	2.09
	Crambus albellus	2.61	2.13	2.02	2.25
	Spoladea recurvalis	0.11	0.98	1.31	0.80
Erebidae (8.63)	Aloa lactinea	1.74	1.64	1.74	1.71
	Amata phegea	2.4	1.8	1.63	1.94
	Creatonotos gangis	1.53	1.47	1.56	1.52
	Pyrrharctia isabella	1.53	1.64	1.78	1.65
	Spilosoma obliqua	0.11	1.09	1.39	0.86
	Spirama retorta	0.22	1.15	1.49	0.95
Geometridae (1.76)	Lomographa vestaliata	1.74	1.8	1.74	1.76
Lycaenidae (1.65)	Azanus natalensis	1.53	1.64	1.78	1.65
Nymphalidae (8.74)	Pseudergolis wedah	1.53	1.86	1.88	1.76
	Danaus chrysippus	2.4	1.91	1.85	2.05
	Junonia orithya	2.06	1.8	1.74	1.87
	Parage aegeriatircis	2.4	1.97	1.95	2.11
	Ypthima inica	0.11	1.36	1.39	0.95
Papilionidae (1.64)	Papilio polytes	1.53	1.69	1.71	1.64
Pieridae (10.80)	Belenois aurota	1.73	1.69	1.81	1.74
	Catopsilia pomona	1.74	1.75	1.81	1.77
	Catopsilia pyranthe	1.53	1.64	1.78	1.65
	Eurema hecabe	2.4	1.75	1.74	1.96
	Pieris brassicae	1.73	1.69	1.81	1.74
	Pieris canidia	2.4	1.64	1.78	1.94
Pyralidae (2.08)	Plodia interpuntella	2.4	1.92	1.92	2.08
Saturniidae (1.55)	Antheraea pernyi	1.52	1.58	1.56	1.55
Sphingidae (0.92)	Hippotion celerio	0.22	1.15	1.39	0.92

 

Table II. Relative abundance (%) of families in three sites (Deva, Vatala and Barmala) and in DVNP (overall) during summer (March- September) and winter (October-February).

Family	Deva		Vatala		Barmala		DVNP
	Winter	Summer	Winter	Summer	Winter	Summer	Winter	Summer
Apidae	6.17	6.72	6.26	5.92	7.04	5.67	6.59	5.91
Chantharidae	1.30	1.48	2.32	1.21	0.82	1.41	1.41	1.35
Coccinellidae	5.19	3.11	2.55	3.35	3.27	3.22	3.48	3.25
Crabronidae	1.30	0.00	2.32	1.00	2.13	1.27	2.00	1.00
Crambidae	6.82	4.26	6.03	4.71	6.71	4.90	6.52	4.74
Culicidae	0.97	3.11	0.93	2.36	0.49	2.13	0.74	2.35
Erebidae	10.06	6.23	9.05	8.71	10.47	9.35	9.93	8.68
Eumenidae	1.95	2.13	0.70	1.64	1.31	1.68	1.26	1.73
Formicidae	6.49	9.02	9.98	8.85	9.33	8.80	8.89	8.85
Geometridae	2.27	1.48	2.32	1.64	1.96	1.68	2.15	1.64
Lycaenidae	1.95	1.31	1.86	1.57	2.29	1.63	2.07	1.57
Masaridae	0.00	0.98	1.62	1.43	1.64	1.54	1.26	1.42
Meloidae	5.52	8.52	6.26	6.28	6.38	5.67	6.15	6.29
Muscidae	2.27	2.46	2.09	3.21	1.15	3.31	1.70	3.16
Nymphalidae	8.77	8.36	10.44	8.42	9.82	8.53	9.78	8.47
Papilionidae	1.95	1.31	2.09	1.57	1.96	1.63	2.00	1.57
Pieridae	14.61	10.00	10.44	10.06	12.60	10.21	12.37	10.13
Pyralidae	2.92	2.13	1.86	1.93	2.13	1.86	2.22	1.92
Saturniidae	1.95	1.31	1.62	1.57	1.31	1.63	1.56	1.57
Sphecidae	1.62	2.95	1.86	2.57	1.64	2.27	1.70	2.47
Sphingidae	0.65	0.00	1.62	1.00	1.80	1.27	1.48	1.00
Syrphidae	6.49	11.48	2.78	9.99	2.78	9.53	3.63	9.96
Vespidae	8.77	11.64	12.99	10.99	10.97	10.80	11.11	10.98

 

Based on the general floral resources in the study area, we grouped monthly sampling efforts into summer (March-September) and winter (October-February) months to document seasonal shifts in the diversity and abundance of insect pollinators species. The relative abundance of insect pollinator families indicated significant differences between winter and summer (F(1, 44) = 239.66, p = .0001). The comparison of means indicated significant differences in the means of families between winter and summer. The relative abundance of few insect pollinator families varied greatly between the two seasons such as Crabronidae, Sphecidae, Sphingidae, Pieridae and Erebidae (Table II). Higher relative abundance of Crambidae, Erebidae, Geometridae, Nymphalidae, Pieridae and Sphingidae was observed in winter. We also detected higher abundance of Culicidae, Meloidae, and Syrphidae in summer.

Diversity and abundance of pollinator species

Our results indicated higher abundance of pollinator assemblages at Barmala as compared to other two sites, but we did not observe a single species to be present uniquely in any of the three sites. Insect pollinator communities were significantly different in composition across all three sites (ANOSIM; R = 0.331, P= 0.0001). All pairwise comparisons of insect pollinator communities between sites were significantly different (Barmala-Deva, R = 0.573, P = 0.006; Barmala-Vatala, R = 0.178, P = 0.0135); Deva-Vatala, R = 0.5162, P = 0.0003).

For assessing the contribution of these species in the diversity of different sites, we calculated similarity percentages (SIMPER) of these species at deva, Vatala and Barmala. The results of SIMPER analysis indicated an average dissimilarity ranged between Barmala-Vatala (30.94%), Deva-Vatala (37.46%), and Deva-Barmala (42.01%).

 

Table III. SIMPER Analysis indicating species contributing to dissimilarities of communities between three sites: Deva, Vatala and Barmala. Only the top ten contributing species are listed for each pairwise comparison. Analysis is based on pre-treated square-root transformed abundance (Clarke and Warwick, 2001).

Species	Overall dissimilarity	Mean abundance		Mean dissimilarity	% Contribution	Cumulative
		Deva	Vatala
Ypthima inica	37.46 %	0.08	1.44	1.03	2.76	2.76
Coccinella septempunctata		0.78	1.52	1.00	2.66	5.42
Camponotus vagus		0.66	1.59	0.87	2.31	7.73
Trypoxylon californicum		0.17	1.26	0.86	2.29	10.02
Aedes albopictus		0.99	1.51	0.83	2.21	12.22
Allorhynchium argentatum		0.49	1.54	0.82	2.19	14.41
Celonites hermon		0.39	1.41	0.81	2.16	16.58
Adalia bipunctata		0.47	1.23	0.79	2.10	18.68
Eristalis tenax		1.24	1.35	0.79	2.10	20.79
Spirama retorta		0.12	1.19	0.78	2.07	22.86
		Deva	Barmala
Spirama retorta	42.01 %	0.12	1.77	1.04	2.46	2.46
Coccinella septempunctata		0.78	1.92	1.02	2.44	4.90
Spilosoma obliqua		0.08	1.69	0.98	2.32	7.22
Ypthima inica		0.08	1.69	0.97	2.31	9.53
Spoladea recurvalis		0.08	1.64	0.94	2.24	11.77
Camponotus pennsylvanicus		0.25	1.74	0.94	2.23	14.00
Trypoxylon californicum		0.17	1.65	0.91	2.17	16.18
Camponotus vagus		0.66	1.90	0.91	2.17	18.34
Hippotion celerio		0.12	1.62	0.90	2.14	20.48
Celonites hermon		0.39	1.78	0.89	2.12	22.61
		Vatala	Barmala
Episyrphus viridaureus	30.94%	1.52	1.60	0.72	2.33	02.33
Eristalis tenax		1.35	1.85	0.69	2.23	04.55
Paragus annandalei		1.36	1.63	0.68	2.21	06.76
Sceliphron madraspatanum		1.69	1.98	0.67	2.17	8.93
Zonitoschema gibdoana		1.51	1.73	0.67	2.16	11.10
Aedes albopictus		1.51	1.74	0.66	2.14	13.23
Crambus albellus		1.59	1.94	0.65	2.10	15.33
Pieris canidia		1.29	1.88	0.64	2.07	17.40
Danaus chrysippus		1.54	1.80	0.64	2.06	19.45
Eurema hecabe		1.46	1.74	0.63	2.03	21.48

 

Ypthima inica was the highest contributing species (2.76%) whilst Spirama retorta was the least contributing species (2.07%) towards dissimilarity between Deva-Vatala. An overall dissimilarity of 42.01% was observed between Deva-Barmala. Spirama retorta (2.46%) was the highest contributing species while Celonites hermon (2.12%) was the least contributing species towards dissimilarity between Deva - Barmala. Similarly, an overall dissimilarity of 30.94% was observed between Vatala and Barmala. Episyrphus viridaureus (2.33%) was the highest contributing species while, Pyrrharctia isabella (2.03%) was the least contributing species towards dissimilarity between the two sites (Table III).

We also compared diversity by calculating Shannon-Wiener index for species and applied t-test between sites to determine statistical significance. The results showed significant differences between Vatala - Deva (t = -7.31, d.f. = 1199.5, P < 0.00001) with higher average value of Shannon diversity in Vatala (H’ = 4.03) than Deva (H’ = 3.92). Similarly, we recorded significant differences between Deva - Barmala (t = -8.43, d.f. = 1013, P< 0.0001) with higher average value of Shannon diversity in Barmala (H’ = 4.05) than Deva (H’ = 3.92). Vatala had a higher average value of Shannon diversity (H’ = 4.03) compared to Barmala (H’ = 4.05) but the difference was not statistically significant (P= 0.071).

Rank abundance curves

We also plotted rank abundance curves of species for three sites. The shallow gradient of rank abundance curve for Barmala and Vatala indicated that species were evenly distributed in these areas whereas, the steep curve for Deva indicated less dispersion of species at this study site (Fig. 5).

 

DISCUSSION

Our study provides a first comprehensive estimation of species richness and the relative abundance of insect pollinators in DVNP. We documented the relative contribution of species belonging to four major insect orders in Deva, Vatala and Barmala. Results showed variations in the species richness and relative abundance of in family groups of four major insect orders. Our results demonstrated variable contributions of four major groups of insect pollinator communities in the descending order: Lepidoptera > Hymenoptera > Diptera > Coleoptera.

Several important features of communities like diversity of species, seasonal pattern of abundance, number of individuals and their relative proportion at three sites were observed. These may be attributed to the variations in the landscape features, vegetation type and the anthropogenic activities associated with these sites. For example, Barmala has the hilly forests with seasonal streams and is relatively undisturbed area though impacted by livestock grazing, cutting wood for fuel, and grass collection and burning all impact upon the area (Umar et al., 2021). This would have contributed to the lower number of individuals in Barmala. Similarly in Deva, human population density is lower than in Vatala and has the luxury of field crops and seasonal flowering flora maintained in the nurseries. With higher population density, among these sites, Vatala has the highest human disturbance mainly due to the army deployment, summer visitors, and stone quarrying and livestock grazing. This area may have lesser floral diversity to be exploited by insect pollinators resulting in the lower levels of the insect pollinator species diversity and abundance.

Four major groups of insect pollinators with higher relative abundance of Lepidoptera (butterflies) followed by Hymenoptera (mainly bees, wasps, ants), and Diptera (flies and mosquitoes). Insect pollinators may benefit different resources to maintain their density at relatively higher numbers. A large number of species in different families of Lepidoptera, Hymenoptera and Diptera owes to variations in exploitation of floral resources in different landscapes are pollinators of global importance (Mawdsley, 2003).

Insect pollinators including bees, flies, beetles, moths, and butterflies have been associated with the crops and wild plants (Rader et al., 2009; Jauker and Wolters, 2008; Blanche and Cunningham, 2005; Jarlan et al., 1997a, b; Kendall and Solomon, 1973). Insect belonging diptera, lepidoptera, and coleoptera have been reported to pollinate different field crops of Brassicaceae family (Shakeel et al., 2015, 2019; Chaudhary, 2001).

In our study, Lepidoptera was dominant order in all three sites with species contributed differently to the dissimilarity. This may be attributed to the heterogeneity of the three habitats. Lepidopterans are important pollinators of flowering plants both in wild ecosystems and managed systems such as parks (Ostiguy, 2011). Lepidopterans are identified as an important group of insects pollinating plant species in almost all terrestrial ecosystems across the world (Macgregor et al., 2015).

Individual Lepidopterans have varied morphological and behavioural adaptations for pollination such as papilionids, pierids, and groups of nymphalids have long proboscis to reach nectar in specialized flowers (Corbet, 2000; Tiple et al., 2009; Mertens et al., 2021; Webb, 2008). Lepidoptera has shown the highest diversity and abundance at DVNP that indicates the variety of floral resources in the study area. Lepidopterans have been reported for having attraction towards bright colors. The variety of flora in the study area offered such a plentiful variations in the color of flowers and this may be the reason of high number of lepidoptera than other insect orders (Shakeel et al., 2019). 

Many hymenopterous insects like bees and wasps are designated as key pollinators of many wild plants and cultivated crops. Hymenopteran showed as the highest abundance among pollinator species with A. mellifera was recorded as most prominent insect pollinator species (Shakeel et al., 2019). We collected some species collected are known specialists on other plant taxa, suggesting they may be tourist species (Parys et al., 2020).

We observed Hymenoptera as second dominant order in our study. Hymenopterans have been reported to be attracted to flowers having high amount of nectar like Brassica spp. and many wild plants. The reason could be high amount of nectar secretions in the wild plants and cultivated crops like Brassica (Shakeel et al., 2019; Silva and Dean, 2000). Bees and other pollinators of Hymenoptera like to visit the flower with high sugar and nectar. This could be the one reason for their higher diversity and abundance. A. dorsata was also reported as pollinator of forest plantations at Sarawak (Momose et al., 1998). T. californicum showed higher abundance in Barmala and Vatala than Deva which demonstrates its preference for habitat. Many members of superfamily Apoidea including bees and wasps pollinate many food and feed crops of agricultural importance (Lorenzo-Felipe et al., 2020). Many hymenopterous insects like social bees are usually found in higher densities near the tree plantations than cropped areas which could be due to the availability of suitable nesting sites and greater foraging opportunities in the adjacent agroecosystems.

Dipterous syrphid flies in both agricultural landscapes and natural ecosystems contribute to the pollination of crops and plantations (Saleem et al., 2001; Sajjad et al., 2010; Khan and Hanif, 2016). Dipterous flies are an important group of pollinators of agrobiodiversity and plant biodiversity (Ssymank et al., 2008). Many dipterans such as syrphid flies are important generalized pollinators which visit many of the same flowers as hymenopterous bees and lepidopterous butterflies. Similar results were reported other parts of the world such as 43 species belonging to hymenoptera, diptera, and lepidoptera from Agricultural lands of Jambi, Sumatra (Siregar et al., 2016). Similarly, higher number of pollinators species belonging to Lepidoptera, Coleoptera, Hymenoptera, and Diptera was reported from other parts of the world (Wardhaugh, 2015; Ollerton, 2017).

We found higher relative abundance in summer for example in Syrphidae as compared to winter. Similarly, we recorded higher abundance of Crabronidae, Pieridae, Crambidae, Nymphalidae, and Erebidae in winter than summer. This suggests that different floral resources have contributed to the abundance of the individuals of these species in DVNP.

Similar finding was communicated in a study which reported 11 of Coleopteran pollinator species (Mawdsley, 2003). Earlier studies reported that pollinator diversity varies between habitats (Mudri-Stojnić et al., 2012). Hymenopterous pollinators like honeybees, wasps and ants were abundant in Deva but A. dorsata was dominant in Vatala. Bees are the most important generalist insect pollinators for many crops (Bawa et al., 1985) and essential pollinators for some crops and wild plants (Aebi et al., 2012). In central Sumatera, the study reported that bees visited 73.5% of flowers and A. dorsata was recorded in high abundance.

Surprisingly, we detected only six species of Coleoptera with an overall 10.13% contribution in the abundance. Only three species of Meloidae and two species of Coccinellidae were observed in the study area. However, we are uncertain about the possible factors that may have contributed in the lower coccinellid population observed in our study. This lower diversity and abundance of coccinellid assemblages may be attributed to their global decline in their population. mainly due to use of farm inputs like the use of insecticides in the cropped areas for pest management lowering prey density in addition to direct hazardous effects. Many native and ornamental plants in tropical and temperate areas rely on beetles for pollination (Saravy et al., 2021). Earlier studies have reported six species of Coleoptera from Israel pollinating mangoes (Dag and Gazit, 2000). Coleoptera is ranked as fourth among pollinators importance after hymenoptera, diptera, and birds (Sayers et al., 2019). Studies have shown that the coleoptera are common and important visitors to flowers (Bernhardt, 2000; Wardhaugh et al., 2012).

CONCLUSION

We observed that documented pollinator diversity at DVNP has essentially contributed to maintain the natural plant communities that regulate this ecosystem. Variations in the insect pollinator diversity of the studied taxa indicate positive impact of floral resources in three sites, viz. Deva, Vatala, and Barmala.

ACKNOWLEDGEMENTS

Authors are grateful to Dr. Muhammad Umar and Mr. Waqas Asghar for their help during the data collection and preservation of specimens.

Funding

The study received no external funds.

IRB approval

This study was approved by the Advanced Study and Research Board of the University of Gujrat.

Ethical statement

All efforts were taken to minimize pain and discomfort to the animal while conducting this research.

Statement of conflict of interest

The authors have declared no conflict of interest.

REFERENCES

Abrahamczyk, S., Kluge, J., Gareca, Y., Reichle, S. and Kessler, M., 2011. The influence of climatic seasonality on the diversity of different tropical pollinator groups. PLoS One, 6: e27115. https://doi.org/10.1371/journal.pone.0027115

Aebi, A., Vaissière, B.E., Van Engelsdorp, D., Delaplane, K.S., Roubik, D.W. and Neumann, P., 2012. Back to the future: Apis versus non-Apis pollination-a response to Ollerton et al. Trends Ecol. Evol., 27: 142–143. https://doi.org/10.1016/j.tree.2011.11.017

Aizen, M.A., and Harder, L.D., 2009. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr. Biol., 19: 915-918. https://doi.org/10.1016/j.cub.2009.03.071

Aizen, M.A., Garibaldi, L.A., Cunningham, S.A. and Klein, A.M., 2008. Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol., 18: 1572-1575. https://doi.org/10.1016/j.cub.2008.08.066

Akrim, F., Awan, M.S., Mahmood, T., Anjum, M.Z., Qasim, S., Khalid, J. and Andleeb, S., 2015. Threats to red junglefowl (Gallus gallus murghi) in Deva Vatala National Park, District Bhimber, Azad Jammu and Kashmir, Pakistan. Annls Res. Rev. Biol., 6: 59-65. https://doi.org/10.9734/ARRB/2015/9596

Anwar, M., Mahmood, A., Rais, M., Hussain, I., Ashraf, N. and Khalil, S., 2015. Population density and habitat preference of Indian peafowl (Pavo cristatus) in Deva Vatala National park, Azad Jammu and Kashmir, Pakistan. Pakistan J. Zool., 47: 1381-1386.

Astegiano, J., Guimarães, Jr, P.R., Cheptou, P.O., Vidal, M.M., Mandai, C.Y., Ashworth, L. and Massol, F., 2015. Persistence of plants and pollinators in the face of habitat loss: Insights from trait-based metacommunity models. Adv. Ecol. Res. Elsevier, https://doi.org/10.1016/bs.aecr.2015.09.005

Azam, M., Hussain, R., Ali, M., Ahmed, W. and Abbas, N., 2007. Some observations on the biodiversity of Deva and Vatala Game Reserves, District Bhimber, AJK. Unpubl. Rep., 21.

Bashir, M.A., Saeed, S., Sajjad, A. and Ali, M., 2015. Seasonal variations in abundance and diversity of insect pollinator in forest ecosystems of Southern Punjab Pakistan. Pure appl. Biol., 4: 441-452. https://doi.org/10.19045/bspab.2015.43021

Bawa, K.S., Bullock, S.H., Perry, D.R., Coville, R.E. and Grayum, M.H., 1985. Reproductive biology of tropical lowland rain forest trees. II. Pollination systems. Am. J. Bot., 72: 346-356. https://doi.org/10.1002/j.1537-2197.1985.tb05358.x

Bernhardt, P., 2000. Convergent evolution and adaptive radiation of beetle-pollinated angiosperms. Pollen and pollination. Springer. https://doi.org/10.1007/978-3-7091-6306-1_16

Blanche, R. and Cunningham, S.A., 2005. Rain forest provides pollinating beetles for atemoya crops. J. econ. Ent., 98: 1193-1201. https://doi.org/10.1603/0022-0493-98.4.1193

Bohan, D., Pocock, M.J., and Woodward, G., 2016. Ecosystem services: From biodiversity to society, Part 2. Adv. Ecol. Res., 54: 1-306.

Chaudhary, O., 2001. Abundance of wild pollinators on rapeseed and mustard. Insect Environ., 7: 141-142.

Clarke, K. and Warwick, R., 2001. A further biodiversity index applicable to species lists: Variation in taxonomic distinctness. Mar. Ecol. Prog. Ser., 216: 265-278. https://doi.org/10.3354/meps216265

Corbet, S.A., 2000. Butterfly nectaring flowers: Butterfly morphology and flower form. Ent. Exp. appl., 96: 289-298. https://doi.org/10.1046/j.1570-7458.2000.00708.x

Dag, A. and Gazit, S., 2000. Mango pollinators in Israel. J. appl. Hortic., 2: 39-43. https://doi.org/10.37855/jah.2000.v02i01.12

Didham, R.K., Ghazoul, J., Stork, N.E. and Davis, A.J., 1996. Insects in fragmented forests: A functional approach. Trends Ecol. Evol., 11: 255-260. https://doi.org/10.1016/0169-5347(96)20047-3

Dyola, U., Baniya, C.B., Acharya, P.R., Subedi, P., Pandey, A. and Sapkota, K., 2022. Community structure of pollinating insects and its driving factors in different habitats of Shivapuri-Nagarjun National Park, Nepal. Ecol. Evol., 12: e8653. https://doi.org/10.1002/ece3.8653

El-Abdouni, I., 2022. Diversity and relative abundance of insect pollinators in moroccan agroecosystems. Front. Ecol. Evol., 10. https://doi.org/10.3389/fevo.2022.866581

Ganuza, C., Redlich, S., Uhler, J., Tobisch, C., Rojas-Botero, S., Peters, M.K., Zhang, J., Benjamin, C.S., Englmeier, J. and Ewald, J., 2022. Interactive effects of climate and land use on pollinator diversity differ among taxa and scales. Sci. Adv., 8: eabm9359. https://doi.org/10.1126/sciadv.abm9359

Gill, R.J., Baldock, K.C., Brown, M.J., Cresswell, J.E., Dicks, L.V., Fountain, M.T., Garratt, M.P., Gough, L.A., Heard, M.S. and Holland, J.M., 2016. Protecting an ecosystem service: Approaches to understanding and mitigating threats to wild insect pollinators. Adv. Ecol. Res. Elsevier, https://doi.org/10.1016/bs.aecr.2015.10.007

Grimmett, R., Roberts, T.J., Inskipp, T., and Byers, C., 2008. Birds of Pakistan, A & C Black.

Hussain, M., Kanwal, M., Aftab, K., Khalid, M., Liaqat, S., Iqbal, T., Rahman, G. and Umar, M., 2021. Distribution patterns of dung beetle (Coleoptera: Scarabaeidae) assemblages in croplands and pastures across two climatic zones of Pakistan. Orient Insects, pp. 1-16. https://doi.org/10.1080/00305316.2021.2010617

Jarlan, A., De Oliveiha, D. and Gingras, J., 1997a. Effects of Eristalis tenax (Diptera: Syrphidae) pollination on characteristics of greenhouse sweet pepper fruits. J. econ. Ent., 90: 1650-1654. https://doi.org/10.1093/jee/90.6.1650

Jarlan, A., De Oliveira, D. and Gingras, J., 1997b. Pollination by Eristalis tenax (Diptera: Syrphidae) and seed set of greenhouse sweet pepper. J. econ. Ent., 90: 1646-1649. https://doi.org/10.1093/jee/90.6.1646

Jauker, F. and Wolters, V., 2008. Hover flies are efficient pollinators of oilseed rape. Oecologia, 156: 819-823. https://doi.org/10.1007/s00442-008-1034-x

Katumo, D.M., Liang, H., Ochola, A.C., Lv, M., Wang, Q.F. and Yang, C.F., 2022a. Pollinator diversity benefits natural and agricultural ecosystems, environmental health, and human welfare. Pl. Diversity, 44: 429-435. https://doi.org/10.1016/j.pld.2022.01.005

Katumo, D.M., Liang, H., Ochola, A.C., Lv, M., Wang, Q.F. and Yang, C.F. 2022b. Pollinator diversity benefits natural and agricultural ecosystems, environmental health, and human welfare. Pl. Diversity, 44: 429-435. https://doi.org/10.1016/j.pld.2022.01.005

Kendall, D. and Solomon, M., 1973. Quantities of pollen on the bodies of insects visiting apple blossom. J. appl. Ecol., 10: 627-634. https://doi.org/10.2307/2402306

Kevan, P.G., 1999. Pollinators as bioindicators of the state of the environment: Species, activity and diversity. Invertebrate biodiversity as bioindicators of sustainable landscapes. Elsevier. https://doi.org/10.1016/B978-0-444-50019-9.50021-2

Khan , S. and Hanif, H., 2016. Diversity and fauna of hoverflies (Syrphidae) in Chakwal, Pakistan. Int. J. Zool. Stud., 1: 22-23.

Khan, K.A., Ansari, M.J., Al-Ghamdi, A., Sharma, D. and Ali, H., 2014. Biodiversity and relative abundance of different honeybee species (Hymenoptera: Apidae) in Murree-Punjab, Pakistan. J. Ent. Zool. Stud., 2: 324-327.

Klein, A.M., Brittain, C., Hendrix, S.D., Thorp, R., Williams, N. and Kremen, C., 2012. Wild pollination services to California almond rely on semi‐natural habitat. J. appl. Ecol., 49: 723-732. https://doi.org/10.1111/j.1365-2664.2012.02144.x

Kremen, C., Williams, N.M. and Thorp, R.W., 2002. Crop pollination from native bees at risk from agricultural intensification. Proc. natl. Acad. Sci. U.S.A., 99: 16812-16816. https://doi.org/10.1073/pnas.262413599

Lautenbach, S., Seppelt, R., Liebscher, J. and Dormann, C.F., 2012. Spatial and temporal trends of global pollination benefit. PLoS One, 7: e35954. https://doi.org/10.1371/journal.pone.0035954

Lorenzo-Felipe, I., Blanco, C.A. and Corona, M., 2020. Impact of apoidea (Hymenoptera) on the world’s food production and diets. Annls entomol. Soc. Am., 113: 407-424. https://doi.org/10.1093/aesa/saaa016

Losey, J.E. and Vaughan, M., 2006. The economic value of ecological services provided by insects. Bioscience, 56: 311-323. https://doi.org/10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2

Macdonald, K.J., Kelly, D. and Tylianakis, J.M., 2018. Do local landscape features affect wild pollinator abundance, diversity and community composition on Canterbury farms? N. Z. J. Ecol., 42: 262-268. https://doi.org/10.20417/nzjecol.42.29

Macgregor, C.J., Pocock, M.J., Fox, R. and Evans, D.M., 2015. Pollination by nocturnal L epidoptera, and the effects of light pollution: A review. Ecol. Ent., 40: 187-198. https://doi.org/10.1111/een.12174

Magurran, A., 2004. Measuring biological diversity. Blackwells, Oxford, UK.

Mawdsley, J.R., 2003. The importance of species of Dasytinae (Coleoptera: Melyridae) as pollinators in western North America. Coleopterists Bull., 57: 154-160. https://doi.org/10.1649/541

Mertens, J.E., Brisson, L., Janeček, Š., Klomberg, Y., Maicher, V., Sáfián, S., Delabye, S., Potocký, P., Kobe, I. N. and Pyrcz, T. 2021. Elevational and seasonal patterns of butterflies and hawkmoths in plant-pollinator networks in tropical rainforests of Mount Cameroon. Sci. Rep., 11: 1-12. https://doi.org/10.1038/s41598-021-89012-x

Momose, K., Yumoto, T., Nagamitsu, T., Kato, M., Nagamasu, H., Sakai, S., Harrison, R.D., Itioka, T., Hamid, A.A. and Inoue, T., 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am. J. Bot., 85: 1477-1501. https://doi.org/10.2307/2446404

Mudri-Stojnić, S., Andrić, A., Jozan, Z. and Vujić, A., 2012. Pollinator diversity (Hymenoptera and Diptera) in semi-natural habitats in Serbia during summer. Arch. Biol. Sci., 64: 777-786. https://doi.org/10.2298/ABS1202777S

Ollerton, J., 2017. Pollinator diversity: Distribution, ecological function, and conservation. Annls Rev. Ecol., Evol. Syst., 48: 353-376. https://doi.org/10.1146/annurev-ecolsys-110316-022919

Ostiguy, N., 2011. Pests and pollinators. Nat. Educ. Knowledge, 3: 3.

Parys, K.A., Esquivel, I.L., Wright, K.W., Griswold, T. and Brewer, M.J., 2020. Native pollinators (Hymenoptera: Anthophila) in cotton grown in the gulf south, United States. Agronomy, 10: 698. https://doi.org/10.3390/agronomy10050698

Perveen, F. and Ahmad, A., 2012. Checklist of butterfly fauna of Kohat, Khyber Pakhtunkhwa, Pakistan. Arthropods, 1: 112-117.

Perveen, F. and Fazal, F., 2013. Biology and distribution of butterfly fauna of Hazara university, garden campus, Mansehra, Pakistan. Open J. Anim. Sci., 3: 28-36. https://doi.org/10.4236/ojas.2013.32A004

Plascencia, M. and Philpott, S., 2017. Floral abundance, richness, and spatial distribution drive urban garden bee communities. Bull. entomol. Res., 107: 658-667. https://doi.org/10.1017/S0007485317000153

Polce, C., Garratt, M.P., Termansen, M., Ramirez-Villegas, J., Challinor, A.J., Lappage, M.G., Boatman, N.D., Crowe, A., Endalew, A.M. and Potts, S.G., 2014. Climate-driven spatial mismatches between British orchards and their pollinators: increased risks of pollination deficits. Glob. Change Biol., 20: 2815-2828. https://doi.org/10.1111/gcb.12577

Rader, R., Bartomeus, I., Garibaldi, L.A., Garratt, M.P., Howlett, B.G., Winfree, R., Cunningham, S.A., Mayfield, M.M., Arthur, A.D. and Andersson, G.K., 2016. Non-bee insects are important contributors to global crop pollination. Proc. natl. Acad. Sci., 113: 146-151. https://doi.org/10.1073/pnas.1517092112

Rader, R., Howlett, B.G., Cunningham, S.A., Westcott, D.A., Newstrom-Lloyd, L.E., Walker, M.K., Teulon, D.A. and Edwards, W., 2009. Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop. J. appl. Ecol., 46: 1080-1087. https://doi.org/10.1111/j.1365-2664.2009.01700.x

Sajjad, A., Saeed, S., and Ashfaq, M., 2010. Seasonal variation in abundance and composition of hoverfly (Diptera: Syrphidae) communities in Multan, Pakistan. Pakistan J. Zool., 42: 105-115.

Saleem, M., Arif, M. and Suhail, A., 2001. Taxonomic studies of syrphidae of Peshawar, Pakistan. Int. J. Agric. Biol., 3: 533-534.

Saravy, F.P., Marques, M.I. and Schuchmann, K.L., 2021. Coleopteran pollinators of annonaceae in the Brazilian Cerrado. A review. Diversity, 13: 1-20. https://doi.org/10.3390/d13090438

Sataral, M. and Rustiawati, Y., 2019. Diversity of insect pollinators on Citrullus lanatus thunb. IOP Publishing, J. Phys. Conf. Ser., pp. 012043. https://doi.org/10.1088/1742-6596/1242/1/012043

Sayers, T.D., Steinbauer, M.J. and Miller, R.E., 2019. Visitor or vector? The extent of rove beetle (Coleoptera: Staphylinidae) pollination and floral interactions. Arthropod Pl. Interact., 13: 685-701. https://doi.org/10.1007/s11829-019-09698-9

Schauff, M.E., 2001. Collecting and preserving insects and mites: Techniques and tools. National Museum of Natural History, NHB-168, Washington, DC 20560, Systematic Entomology Laboratory, USDA.

Scudder, G.G., 2017. The importance of insects. Insect Biodivers. Sci. Soc., 1: 9-43. https://doi.org/10.1002/9781118945568.ch2

Shakeel, M., Ali, H., Ahmad, S., Said, F., Khan, K.A., Bashir, M.A., Anjum, S.I., Islam, W., Ghramh, H.A. and Ansari, M.J., 2019. Insect pollinators diversity and abundance in Eruca sativa Mill. (Arugula) and Brassica rapa L. (Field mustard) crops. Saudi J. biol. Sci., 26: 1704-1709. https://doi.org/10.1016/j.sjbs.2018.08.012

Shakeel, M., Inayatullah, M. and Ali, H., 2015. Checklist of insect pollinators and their relative abundance on two canola (Brassica napus) cultivars in Peshawar, Pakistan. J. Ent. Zool. Stud., 3: 326-330.

Shannon, C.E. and Weaver, W., 1949. The mathematical theory of communication, University of illinois Press Champaign, IL, USA.

Silva, E. and Dean, B.B., 2000. Effect of nectar composition and nectar concentration on honey bee (Hymenoptera: Apidae) visitations to hybrid onion flowers. J. econ. Ent., 93: 1216-1221. https://doi.org/10.1603/0022-0493-93.4.1216

Siregar, E.H., Atmowidi, T. and Kahono, S., 2016. Diversity and abundance of insect pollinators in different agricultural lands in Jambi, Sumatera. Hayati J. Biosci., 23: 13-17. https://doi.org/10.1016/j.hjb.2015.11.002

Ssymank, A., Kearns, C., Pape, T. and Thompson, F.C., 2008. Pollinating flies (Diptera): A major contribution to plant diversity and agricultural production. Biodiversity, 9: 86-89. https://doi.org/10.1080/14888386.2008.9712892

Thomann, M., Imbert, E., Devaux, C. and Cheptou, P.O., 2013. Flowering plants under global pollinator decline. Trends Pl. Sci., 18: 353-359. https://doi.org/10.1016/j.tplants.2013.04.002

Tiple, A.D., Khurad, A.M. and Dennis, R.L., 2009. Adult butterfly feeding–nectar flower associations: Constraints of taxonomic affiliation, butterfly, and nectar flower morphology. J. Nat. Hist., 43: 855-884. https://doi.org/10.1080/00222930802610568

Umar, M. and Hussain, M., 2023. Faunistic analysis of insects of Deva Vatala National Park and agroecosystem of Gujrat Pakistan. Kuwait J. Sci., 50: 1-25.

Umar, M., Hussain, M., Malik, M.F., Awan, M.N. and Lee, D.C., 2021. Avian community composition and spatio-temporal patterns at Deva Vatala National Park, Azad Jammu and Kashmir, Pakistan. Pakistan J. Zool., 53: 921-929 https://doi.org/10.17582/journal.pjz/20190711190734.

Wardhaugh, C.W., 2015. How many species of arthropods visit flowers? Arthropod. Pl. Interact., 9: 547-565. https://doi.org/10.1007/s11829-015-9398-4

Wardhaugh, C.W., Stork, N.E., Edwards, W. and Grimbacher, P.S., 2012. The overlooked biodiversity of flower-visiting invertebrates. PLoS One, 9: 1-8. https://doi.org/10.1371/journal.pone.0045796

Webb, J.K., 2008. Beyond butterflies: Gardening for native pollinators. Coopertive Extension, Colleges of Environmental and Agricultural Sciences. The University of Georgia.

Wilson, J.S., Griswold, T. and Messinger, O.J., 2008. Sampling bee communities (Hymenoptera: Apiformes) in a desert landscape: Are pan traps sufficient? J. Kans. entomol. Soc., 81: 288-300. https://doi.org/10.2317/JKES-802.06.1