Pakistan J. Agric. Res. Vol. 29 No.3, 2016 DIVERSITY AND RELATIVE ABUNDANCE OF CITRUS POLLINATORS IN DISTRICT HARIPUR, PAKISTAN

Abdul Haq*, Anjum Shehzad**, Muhammad Ilyas**, Muhammad Ishaque Mastoi**, Abdul Rauf Bhatti** and Mian Inayatullah*

ABSTRACT:- As many as 3094 specimens of adult citrus pollinators collected from district Haripur represented four orders of i.e., Diptera with 16 species, with 14 species, Lepidoptera with 3 species and Coleoptera with 2 species. The calculated values of relative abundance showed thatMusca domestica is most abundant species in ecosystem followed bySarcophaga sp. and Apis mellifera . All calculated values of diversity indices except Shannon-H does not show significant difference. Shannon's diversity shows that Naseem Town is most diverse locality then Nikrian B with relative values of 2.213 and 1.136.

Key Words: Citrus; Pollinators; Species; Identification; Pakistan.

INTRODUCTION total pollination activities are done by insects and bees (Robinson and Pollination is one of the most Morse, 1989). Co-evolution of important mechanisms in the flowering plants and their pollinators maintenance and conservation of started about 225 million years ago biodiversity and life on earth. Two (Price, 1975). Both the abundance thirds of the world's 3000 species of and diversity of insect pollinators agricultural crops require pollinators. documented as beneficial to the yield Pollination by insects and other of numerous crops (Talavera et al., is a requirement for about 2001; Kremen et al., 2002). It has 90% of flowering plants (Linder, been established from records that 1998, Ollerton, 1999). Pollination is insects were potentially effective essential for the sexual reproduction pollinators and their visits to flowers of plants, required for the production increased` the fruit production (Luce of a wide range of crops including and Morris, 1928; Leppik, 1960). fruits, nuts and fibers and it Among the several , insects increases yield of other crops such as particularly honey bees, dominate in coffee and oranges (Gordon and providing pollination services to Davis, 2003; Klein et al., 2007). several plants (Meena, 2012). Thapa Worldwide economic value of the (2006) reported that over 50 species pollination service provided by insect of insects visited flowers of 17 pollinators, bees mainly was 153 different species of selected crops billion dollars in 2005 for the main during flowering periods. Asif et al. crops that feed the world (Blawat and (2008) studied the insect pollinators Fingler, 1994). More than 80% of the of onion. Saeed et al. (2012) con- * Department of Entomology, Faculty of Plant Sciences, The University of Agriculture, Peshawar, Pakistan. **National Insect Museum, National Agricultural Research Centre, Islamabad, Pakistan. Corresponding author: [email protected]

244 ABDUL HAQ ET AL cluded that pollinator community of adult pollinators were collected by bitter gourd comprised 15 insect using white, florescent blue and species belonging to 3 orders and 10 florescent yellow bowls traps. Seventy families, bees were the dominant two pan traps, 24 each of florescent- floral visitors while moths and wasps blue, florescent-yellow and were denoted as occasional and five florescent- white placed at 5 m apart major pollinators were tested for their from each other. Bowls were placed in single-visit efficacy, showing that A. a line with alternate colors at open, dorsata was the most effective visible and shiny place. Each pan trap pollinator, along withA. florea and was filled with water and a few grains Eristalinus laetus. Conservation and of detergent (surf ) in it to minimize the enhancement of these pollinators surface tension of water. Bowls were may increase bitter gourd (Momordica placed from 0900h to 1600h. At the charantia L.) production in Pakistan. end of sample period the liquid in pan Shahid et al. (2013) explored the traps was sieved to extract the insects pollinator fauna of Litchi resulting 23 and were washed in water 2-3 times. species under 16 genera in 8 families The collected insects were transferred of Orders Hymenoptera and Diptera to sealable killing jars with ethyl from Haripur. In Pakistan, Sarwar et acetate. The collected specimen were al. (2008 and 2012) studied effect of pinned, labeled and preserved in honey bee on fruit setting and yield of collection boxes. Specimens were cucumber and Sajjad et al. (2012) identified with relevant literature and studied spatial variation in pollinator deposited at National Insect Museum communities and reproductive National Agricultural Research performance ofProsopis julifora . Centre, Islamabad. Pakistan enjoys a well-known position among leading citrus pro- RESULTS AND DISCUSSION ducing countries of the world. Citrus is grown in Pakistan on 176400 ha with an annual production of 243800 During the present study total of tons (GoP, 2006). Orange, Tangerine, 3094 specimens were collected. Thi- Kino, Musammi, Lime, Grapefruit, rty five species in 25 genera belonging Lemon, etc. are produced in abun- to 4 orders, 13 families and 17 sub- dance in Pakistan. Khanpur in families were identified. The orders include Diptera, Coleoptera, Lepi- District Haripur, Pakistan is famous doptera and Hymenoptera (Table 1). for its unique orange production. The Order Diptera represented four Red orange and Succri are mostly families namely, Syrphidae, Musci- grown varieties in Haripur District. dae, Sarcophagidae and Calipho- Present study is under taken to ridae. Syrphidae is the much encoun- evaluate diversity and relative abun- tered family on citrus in the sampled dance of insect pollinators in citrus area and 13 species were collected. orchards at Haripur. The family is represented by three subfamilies including Syrphinae, MATERIALS AND METHOD Eristalinae and Chrysotoxinae. Family Muscidae was much The study was conducted from abundant but represented by a single March 13, 2013 to April 30, 2013. The species. Sarcophagidae was also not

245 DIVERSITY AND RELATIVE ABUNDANCE OF CITRUS POLLINATORS Table 1. Number of individuals of sented only by one species of genus citrus pollinators in Haripur Lucilia. Similarly Syrphidae were District represented by Ischiodon scutellaris Fabricius, Scaevea pyrastri S. No Species No of Linnaeus,Betasyrpus issaci Bhatia, specimens Melanostoma orientale Wiedeman, 1 Musca domestica 2023 Episyrphus balteatus De Geer, 2 Sarcophaga sp. 228 Eupeodesspp. Eristalis cerealis 3 Apis mellifera 124 Fabricius,Eristalis tenax Linnaeus, 4 0rthalia sp. 110 Eristalinus quinquelineatus Fabricus 5 Episyrphus balteatus 108 andChrysotoxum baphyrus Walk. 6 Lasioglossum (Evylaeus) sp. 96 Order Hymenoptera is repre- 7 Apis cerana 86 sented by five families; , 8 Apis florae 72 Halictidae, Megachilidae, Apidae and 9 Lucilia sp. 61 Vespidae. Among all families of 10 Osmia sp. 48 Hymenoptera, Apidae is most abun- 11 Apis dorsata 20 dant with two subfamilies and eight 12 Ischiodon scutellaris 18 species while family Halictidae resul- 13 L. (Lasioglossum s. str.) sp. 17 ted in only one subfamily including 14 Melanostoma orientale 14 four species. Family Andrenidae, 15 Megandrena s.str. sp. 12 16 Eupeodes confrater 9 Megachilidae and Vespidae resulted 17 Scaevea pyrastri 6 with only one subfamily and one 18 Vaspid Wasp 5 species each. 19 Eristalis cerealis 5 Subfamily repre- 20 Harmonia dimidiata 4 sented by only one species of genus 21 Coccinella septempunctata 4 Megandrena sp. Subfamily Helictinae 22 Ceratina sexmaculata 4 contained four species. Subfamily 23 Ceratina hieroglyphica 4 Megachilinae was rare one with only 24 Ceratina binghami 3 one species. Subfamily Apinae was 25 Xylocopa fenstrata 2 most abundant subfamily of order 26 Sphecodes sp. 2 Hymenoptera as pollinator of citrus 27 Pieris brassicae 1 with seven species. Subfamilies 28 Lycaena phlaeas 1 Xylocopinae and Vespinae also 29 Eupeodes pseudonitens 1 recorded by only one species each. 30 Eupeodes corollae 1 31 Eristalis tenax 1 Species of order Hymenoptera are 32 Eristalis quinquelineatus 1 Megandrena s.str, Cockrell, 33 Chrysotoxum baphyrus 1 Sphecodessp. L. ( Lasioglossum s. str. ) 34 Betasyrpus issaci 1 sp., Lasioglossum (Evylaeus) sp. 35 Argyreus hyperbius 1 Osmia Panzer s.strsp. Apis florea , Apis mellifera,, Apis dorsata Apis Total 3094 cerana,, Ceratina hieroglyphica Certaina sexmaculata, Certaina represented well and only one i.e., binghami, Xylocopa fenstrata and Sarcophaga sp. belonging to Sarco- wasp species. phaginae was visiting the citrus Order Coleoptera is identified flowers. Family Calliphoridae is not a with only one family Coccinellidae frequent group on citrus and repre- subfamily Coccinellinae species are

246 ABDUL HAQ ET AL Coccinella septempunctata and sample, as large sampled locality Harmonia dimidiataFabricius . In this contain more taxa. order both species showed same Nakamura index results showed abundance. that all values were less than one, Order Lepidoptera is represented which did not show any difference by three families; Nymphalidae, among all localities as this index Lyceanidae and Pieridae. All three increases towards one. subfamilies of this order are resulted Localities selected for sampling by only one species and same were 3 orchards with red blood abundance from all orchards of citrus variety of citrus and two with mixed in sampling localities. Species cultivation. Among mixed cultivation include Argyreus hyperbius one orchard of red blood was mixed Johanssen, Lycaena phlaeas with grape fruit and 2nd was mixed Linnaeus and Pieris brassicae with Mandarin and Kino Oranges. Linnaeus. Grapefruit mixed orchard showed Data revealed insect pollinators more diverse insect pollinator abundance i.e.,Musca domestica , community as compare to Kino, Episyrphus balteatus and Mandarin mixed orchard and red Lasioglossum evyleaus were the blood variety containing orchards. principle insect pollinators of citrus Red blood variety at Sikandarpur (Table 1). Subfamily Syrphinae resulted more evenness as compared showed highest value of relative to other localities which is due to percentage abundance. Among all presence of other flowering fruits four orders of insect in citrus present around the orchard such as orchards, Diptera was most loquat, peach and litchi which abundant pollinator. Clement et al. finished flowering few days before (2007) concluded that Musca starting of citrus flowering. Margalef, domestica L. (Diptera: Muscidae), and Nakamura diversity indices and Calliphora vicina Robineau-Desvoidy Equitability did not show any (Diptera: Calliphoridae) were difference and have almost same pollinators on Allium ampeloprasum values in all localities (Figure 1). L. (Alliaceae). The calculated values of Simpson, Menhinick, Nakamura, Simpson's index (D) at all localities Evenness and Equitability indices ranged from 0.291 to 0.3954. The have no significant difference and values of Shannon diversity ranged almost values of all localities are from 2.213 to 1.136 of all localities approximately same. Shannon diver- which mean that there is a slight sity indices showed that water avail- difference of species diversity. ability when needed, provided better Shannon equitability values lies diversity as compare to localities between 0.1499 and 0.2713, showing where water was available for 24 h. that all species are equally distri- All calculated values of diversity buted among all localities. indices did not show big difference. Menhinick index ranged in all The present study is the first study of localities from 0.5109 to 0.7618 this type in the Khyber Pakhtun- which means there is no significant khwa. Therefore, it is very difficult to difference in all localities as value of say whether any species is supported this index depends upon the size of by the enriched flora or any species

247 DIVERSITY AND RELATIVE ABUNDANCE OF CITRUS POLLINATORS

Nikrian A Red biood 24 hours available LITERATURE CITED Sikandarpur Red blood on need provided

Aam Gah Red blood 24 hours available Asif, S., S. Saeed and A. Masood. 2008. Pollinator community of Naseem Town Mixed cultivation on need provided onion (Allium cepa L.) and its role Naseem Town Mixed cultivation on 24 hours available in crop reproductive success. 4.5 Pakistan J. Zool. 40(6): 451-456. Blawat, P. and B. Fingler. 1994. 4.0 Guidelines for estimating cost of 3.5 production; Alfalfa seed. Farm 3.0 Business Management Infor- 2.5 mation Update. Manitoba Agri- culture, Winnipeg, Manitoba, 2.0 Canada. 1.5 Clement, S.L., B.C. Hellier, L.R. 1.0 Elberson, R.T. Staska and M.A. 0.5 Evans. 2007. Flies (Diptera: Muscidae: Calliphoridae) are 0 efficient pollinators of Allium ampeloprasum L. (Alliaceae) in field cages. J. Econ. Entomol. Margalef Menhinick Nakamura 100(1): 131-135. Shannon_H Simpson_1-D Dominance_D Equitability_J GoP. 2006. Pakistan Statistical Year

Evenness_e^H/S Book. Federal Bureau of Statis- tics, Government of Pakistan, Figure 1. Calculated values of diver- Islamabad. 34 p. sity indices in all localities of Gordon, J. and L. Davis. 2003. Valu- District Haripur ing honeybee pollination. Rural Industries Research and Deve- threatened to extinction. lopment Corporation Paper 03/ 077, Canberra, ACT, Australia. It is concluded that Musca Klein, A. M., B. Vaissière, J.H. Cane, domestica, Episyrphus balteatus and I. Steffan-Dewenter, S.A. Lasioglossum (Evyleaus) sp. were the Cunningham and C. Kremen. principle insect pollinators of citrus. 2007. Importance of crop polli- Subfamily Syrphinae showed highest nators in changing landscapes value of relative percentage for world crops. Proc. Royal Soc. abundance. Among all four orders of Bio. Sci. 247(1608): 303-313. insect in citrus orchards, Diptera was Kremen, C., N.M. Williams and R.W. most abundant pollinator. Thorp. 2002. Crop pollination Diversity indices i.e, Shannon's from native bees at risk from diversity index with equitability agricultural intensification. Proc. component, Margalef's index, National Acad. Sci. 99: 16812- Nakamura's index and Menhinick's 16816. index were used. All calculated values Leppik, E.E. 1960. Early evolution of of diversity from entire localities did flower types.Loydia. 23: 72-92. not show significant difference in Linder, H.P. 1998. Morphology and total number of individuals. evolution of wind pollination. In:

248 ABDUL HAQ ET AL Owens, S. J. and P. J. Rudall. nator communities and repro- (eds.) Reproductive Biology in ductive performance of Prosopis Systematics, Conservation and julifora (Fabricius). J. Pollination Economic Botany.Royal Botanic Ecology. 8(9): 59-66. Gardens, Kew. p. 123-135. Sarwar, G., M. Aslam, M.S. Munawar, Luce, W.A. and O.M. Morris. 1928. R. Shazia and R. Mahmood. Pollination of deciduous fruits. 2008. Effect of honeybee (Apis Wash. Agr. Exptl. Stn. Bull. 223: mellifera L.) pollination on fruit 22. setting and yield of cucumber Meena, T. 2012. Bees as pollinators – (Cucumis sativus L.). Pakistan biodiversity and conservation Entomologist, 30(2): 185-191. Intern. Res. J. Agric. Sci. and Soil Sarwar, G., S. Raja, R. Mahmood and Sci. 2(1): 1-7. M.S. Munawar. 2012. Fruit Ollerton, J. 1999. The evolution of setting and yield of Loquats pollinator-plant relationship (Eriobytria japionica ) as affected within the arthropods. (Evolution by pollinators. Pakistan and phylogeny of arthro- Entomologist, 34(1): 43-46. poda).Bol.S.E.A. 26: 741-758. Shahid, A., A. Shehzad, M.A. Rafi and Price, P. 1975. Insect Ecology. John A. Zia. 2013. Insect pollinators of Wiley and Sons, New York. USA. Litchi chinesis from District Robinson, W.E. and R.A. Morse. Haripur, Pakistan. Pakistan J. 1989. The value of honeybees as Agric. 26: 220-229. pollinators of US crops. American Talavera, S., F. Bastida, P.L. Ortiz Bee. 129(1): 477-487. and M. Arista. 2001. Pollinator Saeed, S., A. Sajjad and K.Y. Jung. attendance and reproductive 2012. Bumble bees (Bombus err- success inCitrus libanotus . estalis) can be the efficient Intern. J. Plant. Sci. 162(2): 343. pollinators of cotton. Pakistan Thapa, R.B. 2006. Honeybees and Entomologist, 34(1): 17-20. other insect pollinators of Sajjad, A., S. Saeed and M.A. Bashir. cultivated plants. A Review. J. 2012. Spatial variation in polli- Inst. Agric. Sci. 27: 1-23.

AUTHORSHIP AND CONTRIBUTION DECLARATION

S.No Author Name Contribution to the paper

1. Mr. Abdul Haq Did SPSS analysis, Conclusion, Data collection, Results and Discussion, Introduction, References 2. Mr. Anjum Shehzad Conceived the idea, Wrote abstract, Methodology, Technical input at every step, Overall management of the article 3. Mr. Muhammad Ilyas Technical input at every step 4. Dr. Muhammad Ishaque Mastoi Wrote abstract, Methodology, Technical input at every step 5. Mr. Abdul Rauf Bhatti Technical input at every step 6. Dr. Mian Inayat ullah Technical input at every step

(Received July 2015 and Accepted November 2015)

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