wild bees fauna associated with almond plantation in ...

Pak. J. Entomol. 31 (1): 117-125, 2016

CODEN: PJENEL, ISSN: 1018-1180

Web site: http://www.pjek.org.pk

E-mail address: [email protected]

WILD BEES FAUNA ASSOCIATED WITH ALMOND PLANTATION IN NORTHERN PAKISTAN ZAFAR IQBAL1, MUHAMMAD ATHER RAFI2, ANJUM SHEHZAD3, ABDUL HAQ4, AHMED ZIA5 ABDUL RAUF BHATTI6 AND SYED WAQAR SHAH7 1,2,3,5,6

National Insect Museum, National Agricultural Research Center, Park road, Islamabad. 4Crop Technical Advisor, Shabab Agro Services KPK, Pakistan 7 PIASA, PARC Institute of Advanced studies in Agriculture, NARC-Islamabad, Pakistan

Received for Publication : 05 March, 2016 C. Author E-mail: [email protected]

Plagiarism / Similar Index Report : 1 % Accepted for Publication : June.2016

ABSTRACT Wild bee fauna associated with almond plantations in northern Pakistan was explored. In district Ghizer of Galgit-Biltistan six localities were selected in different almond orchards for the collection of wild bees. Bees were collected throughout the flowering season during mid-March to 1st week of April 2012. Collected bees yielded ten species in seven genera under four families i.e. Apidae, Andrenidae, Halictidae and Megachilidae. Anthophora fulvitarsis, Anthophora sp., Bombus asciaticus Morawitz, Melecta luctuosa Scopoli, and Xylocopa collaris Lepeletier represented family Apidae. Genus Andrena represented its two unidentified species (i & ii) under family Andrenidae. While family Halictidae also represented genus Lassioglossum with its unidentified species. Osmia cornifrons Radoszkowski and Osmia sp. under family Megachilidae were explored. Biogeographically the wild bee fauna of northern Pakistan is affiliated with five regions namely, Oriental, Palearctic, Afrotropical, Australian and Nearctic.

Key words: Wild bees, Almond, Pollination, Gilgit-Baltistan, Pakistan. INTRODUCTION Various wild bees species involved in pollination of a range of fruit crops as well as almond (Batra, 1997), that results in improved fruit set (Bosch and Blas, 1994: Batra, 1997; Szabo et al., 1999; Bosh and Kemp, 2002). Almond blooms in early spring (Bar-Shay, 1995), and its flowers require biotic pollination for fruit set. Low temperatures with high wind and precipitation are very common at high altitudes at the time of almond blooming, which are major limiting factors for honeybee pollination in such areas (Free,

1993; Dag et al., 2006). However, most of the pollination services during that period are normally endorsed to honeybees, which are in fact carried out by wild bees, but their role is generally overlooked (Kevan, 1999; Cane, 2002; Javorek et al., 2002). However, honeybee species Apis mellifera is more active in less rainfall and warm temperatures as compared to the high altitudes in early spring weather conditions (Morse and Calderone 2000). Moreover, the number of honeybee hives has also severely declined due to parasitic mites

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(Winfree et al., 2007) and certain other concern in recent history (CSPNA, 2007; Efrat et al., 2007). All these problems decreases pollination efficiency of honeybees on almond and other fruit crops and this show the way to search for addition pollinators for fruit crops including almond (Dag et al., 2006). Therefore, dependence on a sole pollinator species such as Apis mellifera is generally at risky, as crop pollination is vulnerable to species-specific declines as mentioned above i.e. parasites and diseases (Winfree et al., 2007). Exploring wild bee fauna and their distribution in agro-natural landscapes is an essential step for further evaluating their potential as crop pollinators, their conservation and management which ensure the sustainability of pollination services in future. To achieve these targets base line studies on wild bees in Pakistan are lacking, despite the facts that insect pollination enhance the yield of almond and other fruits and vegetables crops. In Pakistan various studies on bees in relation to pollination have been conducted such as Fiaz (1977) studied role of wild bees (Andrena fulvicru, Xylocopa dissimilis, X. rufescens and X. collaris) in sunflower pollination. Rahoo et al. (1985) reported wild bee species (Anthophora confuse, A. zonata, Ceratina viridissima, Nomia thoracica, X. auripennis, and X. fenestrala) as important pollinators of sunflower. Dhuyo et al. (1986) studied the role of wild bees Anthophora confusa, A. zonata, Megachile menticola, X. aurepennis, X. collari, X. fenestrate and X. pubescens as pollinators of cotton crop. Rehman et al. (1990) studied bees fauna concerned with mango pollination.

Hussain et al. (2012) reported the diversity of hymenopterans bees from fruit orchards of district Skardu, Gilgit Baltistan and reported bee species Osmia cornifrons Panzer, Anthophora niveo-cincta (Smith), A. himalayensis Rad., A. crocea Bangham, Bombus tunicatus (Smith), Xylocopa dissimilis Lepel., X. rufescens Smith, Andrena harrietae Bangham and A. anonyma Cam. Jasra and Rafi (2003) studied pollinator fauna of apricot from Gilgit -Baltistan. While diversity of wild bees of pome and stone fruits orchards of Skurdu was reported by Hussain et al. (2012) which comprises wild bee species like Osmia conifrons, Anthophora niveo-cincta, A. himalayensis, A.crocea, Bombus tunicatus, Xylocopa dissimilis, X. rufescens, Andrena harrietae and A. anonyma. Maryam (2012) studied insect pollinator fauna of apricotfrom Gilgit- Baltistan and reported nine (09) species of bees namely, Anthophora sp., Andrena sp., B. asiatics, Ceratina viridissima, Lasioglossum sp., Nomia sp., Osmia sp., X. collaris and X. dissimilis. Ascher and Rasmussen (2010) reported 250 bee species from Pakistan without knowing their distribution detail, out of which 28 belongs to Andrenidae, 91 from family Apidae, 11 from family Colletidae, 73 from family Halicitidae, 45 from Megachilidae and two from family Melittidae. However, this gap is filled by Irshad et al. (2014) and reported 324 species of bees from various localities of Pakistan. Recently Bodlah et al., (2015; 2016) reported few species for wild bees form Pothwar region of Pakistan. District Ghizer of Gilgit-Baltistan is placed between two greatest mountain ranges of the world namely, Hindukush and

Wild Bees Fauna Associated With Almond Plantation in Northern Pakistan

Karakorum. It lies at 1600-2223m between the latitude 36°17'00" North and longitude 73°26'50". Here almond is widely cultivated with its most popular cultivated varieties i.e. Patasa, Kaghzi and Katha that are grown commercially. Few varieties of wild almonds grow as forest resources which are exploited for commercial reasons and their oil is used for cosmetic purposes. MATERIALS AND METHODS Almond orchards in six localities namely, Gulapur, Singal, Gulmuti, GahkuchBala Golodass and Gupis of district Ghizer in Gilgit- Baltistan were studied during flowering season from mid-March till first week of April, 2012. Collection was done randomly through sweep nets on weekly basis from each locality. Collected specimens were brought to National Insect Museum (NIM), National Agricultural Research Center (NARC), Islamabad for identification through Bingham (1897), Michener (2007), and through reference collection at National Insect Museum. RESULTS Ten species of seven genera under four families i.e. Apidae, Andrenidae, Halictidae and Megachilidae have been identified Family Apidae represented genus Anthophora with its species A. fulvitarsis and an unidentified Anthophora sp., genus Bombus represented species B. asiaticus Morawitz, identified species under genus Melecta M. luctuosa Scopoli, while genus Xylocopa represented only one species i.e. X. collaris Lepeletier. Family Andrenidae represented genus

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Andrena with its two unidentified species. However, genus Lassioglossum represented family Halictidae with an unidentified Lassioglossum sp. Family Megachilidae represented genus Osmia with its species O.cornifrons Radoszkowski and an unidentified Osmia sp. Among all represented wild bees species composition of family Apidae was higher with five species followed by families Megachilidae and Andrenidae with two species in each family while family Halictidae with on e species. It was also observed that specimens of genera Osmia and Anthophora were more abundant in the areas.

ORDER HYMENOPTERA Family Apidae Genus Bombus Latreille, 1802 Bombus asiatics Morawitz, 1875 Own Records: PAKISTAN: GilgitBaltistan, GahkuchBala, 19-23.iii.12, 3♀ 3♂, Zafar, ex NIM, GahkuchBala, 1.iv.12, 2♀,Zia, ex NIM; Golodass, 20-22.iii.12, 3♀ 2♂, Rafi, ex NIM. Golodass, 1.iv.12, 1♀ 1♂, Zia, ex NIM. Previous Records from Pakistan: Suhail et al. (2009) reported this species from Hunza, Darkot, Gilgit, Naltar, Doarian, Samgam and Sermik while Maryam (2012) reported this species from Skardu, Gilgit, Ghizer and Hunza of GilgitBaltistan. Range: India, Hindu-Kush Region (Reinig, 1940), Kashmir valley, Himalaya and PirPanjal region (Williams 1991). Kazakhstan, Kyrgyzstan, Mongolia, Nepal, Tajikistan, western and southwestern China (Saini and Ghattor, 2007), Afghanistan and India (Gupta, 2009). Biogeographical Affiliation: Paleooriental.

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Genus Xylocopa Latreille, 1802 Xylocopa collaris Lepeletier, 1841. Own Records: PAKISTAN: GilgitBaltistan, Gulapur, 15-27.iii.12, 4♀ 2♂ Zafar, ex NIM. Previous Records from Pakistan: Bibi (1984) reported it from Peshawar while Dhuyo et al. (1986) and Rahoo et al. (1985) reported Sindh . Maryam (2012) reported from districts Gilgit and Ghizer, Gilgit-Baltistan. Range:Sri Lanka and India: Malayan region and Siam (Bingham, 1897; Cockerell, 1939 and Wijesekara, 2001). Biogeographical Affiliation: Oriental and Palearctic. Genus Melecta Latreille, 1805 Melecta luctuosa Scopoli, 1770 Own Records: PAKISTAN: GilgitBaltistan, GahkuchBala, 19-23.iii.12, 5♀ 3♂, Zia, ex NIM, GahkuchBala, 2.iv.2012, 2♀ 1♂, Zafar, ex NIM. Previous Records from Pakistan: Reported from Pakistan without any distributional details (Ascher and Rasmussen, 2010). Range: Europe, North Africa, West Asia and India (Bingham, 1897). Biogeographical Affiliation: Holarctic. Genus Anthophora Latreille, 1804 Anthopho rafulvitarsis Brulle, 1832 Own Records: PAKISTAN: GilgitBaltistan, Gulapur, 15-29.iii.12, 3♀ 1♂, Rafi, ex NIM; Gulmuti, l7-24.iii112, 4♀ 2♂, Zia, ex NIM; GahkuchBala, 19-23. iii.12, 6♀ 3♂, Zafar, ex NIM, GahkuchBala, 2.iv.2012, 2♀, Zafar, ex NIM. Previous Records from Pakistan: Gupta (2009) reported this species from Quetta while Ascher and Rasmussen (2010) reported it from Pakistan.

Range: China, Algeria, America and African regions (Cockerell, 1910; Michener, 2007). Biogeographical Affiliation: Oriental and Afrotropical. Anthophora sp. Own Records: PAKISTAN: GilgitBaltistan, Gulapur, 15-29.iii.12, 4♀, Zia, ex NIM; Singal, 16-30.iii.12, 4♀ 3♂, Rafi, ex NIM; Gulmuti, 17-31.iii.12, 3♀ 2♂, Shehzad, ex NIM; GahkuchBala, l923.iii.12, 5♀ 3♂, Zia, ex NIM, GahkuchBala, 2.iv.2012, 1♀ 1♂, Zafar, ex NIM; Golodass, 20-22.iii.12, 2♀ 2♂, Rafi, ex NIM. Previous Records from Pakistan: Rahoo et al. (1985) reported this genus from Tandojam, Sindh . Hassain et al. (2012), while Maryam (2012) also reported this genus from from Gilgit-Baltistan. Range:From Pakistan. African regions and southern Asia (Michener, 2007). Biogeographical Affiliation: Oriental and Afrotropical Family Andrenidae, Genus Andrena Fabricius, 1775 Andrena sp. Own Records: PAKISTAN: GilgitBaltistan, Gulapur, 29.iii.l2, 2♂, Zia, ex NIM. Previous Records from Pakistan: Ascher and Rasmussen (2010) reported this genus from Pakistan. Range:North Persia, Siberia and northern Africa (Brunetti, 1923), India (Abrol 1993). Biogeographical Affiliation: Paleooriental and Afrotropical


Family Halictidae Genus Lassioglossum Curtis, 1833 Lassioglossum sp. Own Records: PAKISTAN: GilgitBaltistan, GahkuchBala, 19-23.iii.12, 4♂, Zafar, ex NIM. Previous Records from Pakistan: Ascher and Rasmussen (2010) reported this genus from Pakistan without providing any geographical distribution. World Distribution: Africa and Australia (Michener, 2007). Biogeographical Affiliation: Afrotropical and Australian. Family Megachilidae Genus Osmia Panzer, 1806 Osmia cornifrons Radoszkowski, 1887 Own Records: PAKISTAN: GilgitBaltistan, Singal, 16-30.iii.12, 14♀ 5♂, Zafar, ex NIM; Gulmuti, 17-24.iii.12, 4♀ 2♂, Zia, ex NIM; GahkuchBala, 1923.iii.12, 11♀ 10♂, Rafi, ex NIM, GahkuchBala, 2.iv.2012, 4♀ 1♂, Shehzad, ex NIM; Golodass, 20-22. iii. 12, 3♀ 2♂, Zia, ex NIM, Gupis, 3.iv.12, 1♂, Zafar, ex NIM. Previous Records from Pakistan:: Hussain et al. (2012) reported this species from district Skardu, Gilgit-Baltistan. Range: China, Japan, Europe and America (Torchio, 1990; Michener, 2007; Yong and Shi, 2007). Biogeographical Affiliation: Holarctic. Osmia sp. Own Records: PAKISTAN: GilgitBaltistan, Gulmuti, 17-31.iii.12, 9♀ 4♂,Rafi, ex NIM; GahkuchBala, 1923.iii.12, 9♀ 11♂,Zia, ex NIM, GahkuchBala, 2.iv.2012, 4♀ 3♂,Zafar, ex NIM; Golodass, 20-22.iii.12, 5♀ 3♂,Zafar,

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ex NIM, Golodass, 1.iv.1♀,Zia, ex NIM; Gupis, 3.iv.12, 3♀, Rafi, ex NIM. Previous Records from Pakistan: This genus was earlier reported by Hussain et al. (2012) from Skardu while Maryam (2012) reported it from districts Gilgit, Hunza, Ghizer and Skardu district,GilgitBaltistan. Range: Europe, North America, Southwest Asia (Michener, 2007). DISSCUSION Almond is a mass flowering crop that requires biotic pollination for fruit set. Especially through insects among insects most important are apis and non-apis bees (wild bees). Almond blooms early in the year when high wind speeds, low temperatures and precipitation are common at high altitudes that naturally prevent honey bees activities as honey bee species are more active in less rainfall and warmer temperatures. In comparison to honey bees, considerably higher abundance of wild bee species are observed in fruit orchards at higher altitudes. Among wild bees, diverse species composition under genera Lasioglossum and Bombus spp. popularly pollinate various fruits including almonds (Batra, 1997). In Pakistan, the diversity of wild bees from pome and stone fruits orchards in the diverse agro ecosystems of Himalayan foot hills at altitudes ranging from 2200 to 3000m of district Skardu, Pakistan was studied by Hussain, et al. (2012) that comprises wild bee species namely Osmia conifrons, Anthophora niveo-cincta, A. himalayensis, A. crocea, Bombus tunicatus, Xylocopa dissimilis, X. rufescens, Andrena harrietae and A. anonyma. In another study, Maryam (2012) reported only single honey bee,

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Apis mellifera and nine (09) wild bees species like, Anthophora sp., Andrena sp., B.asiatics, Ceratina viridissima, Lasioglossum sp., Nomia sp., Osmia sp., Xylocopa collaris and X dissimilis from apricot orchards. During present investigation diverse bee species community was reported from high altitude almond orchards of Gilgit Baltistan inlcluding Apis mellifera and wild bees Andrena sp. (i) Andrena sp. (ii), Anthophora fulvitarsis, Anthophora sp., Bombus asiatics, Lasioglossum sp. Melecta luctuosa, Osmia cornifrons, Osmia sp. and Xylocopa collaris. It was observed amoung honey bee species only Apis mellifera was observed were with very few in numbers which were active during the last week of blossom in two localities i.e. Gulmuti and Golodas when the temperature was slightly higher. However, in all six localities bloom started from mid of March to first week of April and at that time temperature was very low and climate was so windy and rainy that naturally prevented honey bees activities which are again supporting wild bees. These finding further support that early spring bloom may be a major limitation for honeybee pollination (Free, 1993; Dag et al., 2006; Mandelik & Uri 2009). CONCLUSION In the Study Apis mellifera activities were observed to be very limited because of prevailing inclement weather condition. However under same climatic conditions, lot of wild bee genera were found which highlights their potential to withstand adverse climatic conditions and work as active flower visitors of different fruit crops including almonds. It is therefore

concluded that wild bees are essential pollinators of almond in higher altitude areas and further studies should be undertaken to explore their pollinating potential by studying their bio ecology and diversity and to take necessary measures for their conservation.

Contribution of Co-authors Zafar Iqbal1: Collected specimens for identification and identified. Muhammad Ather Rafi2 reviews the paper. Anjum Shehzad3 and Abdul Haq4 help in identification. Ahmed Zia5 Abdul Rauf Bhatti6 and Syed Waqar Shah7: help in preparation and further submission of manuscript. REFERENCES ABROL, D.P., (1993). New pollinator bee. Curr. Res. Univ.of Agric. Sci. (Bangalore), 22(9/10):l30. ASCHER, J .S. & RASMUSSEN, C. (2010). Bee species list for Pakistan. FAO, Rome. BAR-SHAY, N. (1995). Factors affecting almond (Amygdalus communis) pollination efficiency. M.Sc. dissertation. Hebrew Univ., Jerusalem (in Hebrew, English abstract). BATRA, S.W.T. (1997). Fruit-pollinating bees of the Garhwal Himalaya, U.P., India. Acta Hort. (ISHS), 437:325-328. http://www.actahort.org/books/437/437_ 39.htm


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