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Distribution of Bumblebee Bombus haemorrhoidalis Smith and its Association with Flora in Lower Northern Pakistan.

Byline: Umer Ayyaz Aslam Sheikh Munir Ahmad Muhammad Imran Muhammad Nasir Shafqat Saeed and Imran Bodlah

Abstract

Prevalence and floral host plant range of indigenous Bombus pollinators are considered to be important alternatives than the imported species. Commercial enclosed farming has increased the use of the bumblebees as economically important pollinators for high economic return and offseason crops. Indigenous bumblebee species has been considered important to rear and use for such pollination services than imported bumblebees to avoid possible environmental and pest problems. Bombus haemorrhoidalis Smith the only bumblebee species of this region was collected at monthly interval from different non-agricultural and agricultural flora of Margalla and Murree hills of Pakistan during 2011-12. Plant species for floral host plant resources variation in seasonal population and distribution with different climatic regions of this indigenous bumblebee were observed. Twenty four plant species of thirteen plant families were found as floral host plants visited for nectar and pollens with seven new localities ranging from 542-1986 m altitude. The most commonly visited plant family was Asteraceae. Reproductive stages including males and daughter queens were observed from October to December. Prevalence of queen workers and males differ from parks to forests with altitude. Workers were observed active in early and late day hours to avoid harsh climate of June to August. Present study provides the possible available floral host plants variation in its availability of different life stages and possible distribution for future utilization in possible alternate pollinator rearing programs. It also focuses on the ecological and biological interaction of the only bumblebee pollinators of this agro-ecological zone of Pakistan.

Key words: Indigenous bumblebee Bombus haemorrhoidalisfloral plants distribution Northern Pakistan.

INTRODUCTION

Bumblebees are important pollinators belonging to insect order Hymenoptera. High speed of pollination vibration to burst the pollen sacs and efficiency to forage at low temperature and light makes them the most reliable and efficient pollinators (Heinrich 1979; Abrol 2012). Increased world human population stresses the use of such crop pollinators especially for commercial crops grown under intensive cultivation (Griffiths and Robberts 1996). Crops like tomato pepper cucumber strawberries etc under plastic tunnel and systematic hydroponics farms need such pollinators to get low cost constituents (Abak et al. 1997; Kwon and Saeed 2003). Pollination by these important contributors help in better fruit

production weight size and other chemical characters to get cost effective production (Klein et al. 2007; Aizen et al. 2008).

Different Bombus species like Bombus terrestris B. impatiens B. occidentalis and some others have been utilized for commercial pollination of different crops worldwide (Kwon and Saeed

2003; Velthuis and van Doorn 2006; Klein et al.

2007). These species are quite costly to import and

hinder their use for crops pollination (Asada and Ono 2000; Velthuis and van Doorn 2006). They also results in different problems like competing with local species of pollinators especially Bombus for food nest sites and other resources (Couvillon et al. 2010). Possible replacement of the local species with the introduced ones may result in changes in flora visited by the indigenous species. These changes due to accidental release or escape of introduced Bombus species in local environment has been observed in different parts of the world (Stout and Goulson 2000). These escaped individuals can

Table I.- Collection locations in Margalla and Murree Hills of Pakistan.

###Location###Altitude a.s.l.###Global positioning###Major vegetation type

Lake view Park###542 m###33o 43' 05.16 N###Ornamental plants and weeds

###73o 08' 00.22 E

Pir Sohawa###1146 m###33 45 35.62 N###Dense forest

###73 04 10.03 E

Sunny bank Apple Research Station###1986 m###33 55 01.53 N###Apple orchard weeds ornamentals

###73 23 32.82 E

Shahdra###679 m###33 46 38.11 N###Dense forest

###73 10 17.58 E

Daman-e-koh###726 m###33 44 20.66 N###Ornamentals weeds and dense forest

###73 03 23.70 E

F-9 park###564 m###33 42 35.01 N###Ornamental plants and weeds

###73 01 21.72 E

Murree forest###1454 m###33 54 31.35 N###Dense forest and weeds

###73 21 06.76 E

also transfer their diseases and pests which might be new to our environment (Whittington and Winston 2003).

Thirteen Bombus species from northern Pakistan has been observed under agricultural and non-agricultural areas with four most dominant species including B. asiaticus B. avinoviellus B. biroi and B. haemorrhoidalis (Suhail et al. 2009; Makhdoom 2011). Presence of local indigenous Bombus species in Margalla and Murree hills for their natural occurrence host range and distribution under different plant situations were planned to see if there is some alternate indigenous species to get utilized. This was attempted to find the possible and easily available Bombus species for crop pollination which are most acclimatized to our environments.

MATERIALS AND METHODS

Host range new localities and spatial and temporal distribution of bumblebees were conducted in Margalla and Murree hills of northern Pakistan during 2011-12 on monthly basis. Bumblebees were observed from different natural habitats including parks mountains and rangelands of seven different locations. These bumblebees were collected with the help of Entomological net and identified as worker male or queen on the basis of their morphological characters (Dafni 1992). Their numbers visiting in different parts of survey time and locations were

made. Altitude and latitude details were identified using Google Earth for their possible floral host plants and host range. Samples of these bumblebees and flowering plants visited were kept for identification at species level (Malik and Farooq

1984; Williams 1991).

Bumblebees were collected during early morning to early evening hours by walking transect method. Monthly observations from the selected locations were made throughout the year and differences in their sexual and foraging worker bees

Taxonomic characteristics have been given for clear elaboration of indigenous bumblebee species. Interaction of bumblebees and flowering plants visited were estimated. Plant species has been classified on the basis of minor medium and major pollinating hosts for future easy collection of the studied bumblebees on the basis of their visitation rate by these bees. Location based variation of different stages as worker male and queen observations helped to develop their possible life cycle under field conditions and elaborated as graphs for all the locations under observation.

RESULTS

Collected bumblebees showed diverse range of its collection sites with diverse environments and climatic regions providing the successful establishment and survival in the nature (Table I). It

was observed from 540 to 2000 meters altitude in managed and natural mountainous landscapes. Their foraging plants mainly included weeds ornamental dense forest trees and some cultivated crops (Table I).

The bumblebees were collected from seven different locations throughout the year on monthly basis (Fig. 1). Hibernated queens started emerging in March to April with most prominent collection observed from the lake view surrounding. Early workers were observed in April and most commonly in May which started increasing and reached at peak during July to September (Fig. 1). Workers were observed foraging actively in early and late day hours to avoid harsh climate of June to August and reproductive stages including males and daughter queens were observed from October to December. Daughter queens were the most difficult to capture due to their high altitude flight patterns (Fig. 1).

Bumblebee populations were observed foraging for nectar and pollen more prominently in open managed parks than natural forest areas at Daman-e-koh Pir Sohawa Shahdra and Murree forest areas. They were more in numbers at managed park of lake view and its surroundings where Lantana camara is the most common weed flowering from March to November and other wild plants species (Fig. 1).

Twenty four plant species belonging to thirteen different plant families were observed as host plants in seven new localities ranging from

540-2000 m altitude (Table II). The families of plants visited for nectar and pollens belonged to Asteraceae Cisteraceae Cucurbitaceae Ebenaceae Fabaceae Iridaceae Lamiaceae Malvaceae Myrtaceae Plantaginaceae Rosaceae Solanaceae and Verbenaceae. The most commonly visited plants included Zinnia sp. Gladiolus sp. and Lantana camara belonging to the families Asteraceae Iridaceae and Verbenaceae respectively (Table II). Lantana (wild type spanish flag) was the most commonly observed weed in all the locations and even used as ornamental plant in some of the parks under observation. The least number of bees were observed in Margalla hills which might be due to the intensive presence of forest trees and little flowering vegetation to forage by these bees. Wild daisy (Bellis perennis) was observed to be the most

common wild flowering plant present on Murree foothills with common visitation of the observed bumblebee species. From cultivated plant species sunflower cucumber and muskmelon were also the source of their visitation for nectar as well as pollens whereas amaltas (golden shower tree) was the common wild tree with medium level of the bumblebee visitation. However it was difficult to collect the bees due to their flowering at inaccessible height.

B. haemorrhoidalis can be distinguished from other species by having thoracic pubescence black; large individuals (queen: 332mm; male: 251.6mm and worker: 204.4mm) with large wings (330.7mm queen; 251.3mm male and 203.2mm workers); forewing 2.2 times longer than wider in queen and 3 times in male and workers. Terga1-2 was bright yellow and 3-5 orange red with workers similar in coloration but quite smaller in size and thinner than queens. Male with pale fulvous red pubescence and has sooty-black pubescence mixed with pale hairs on the legs. Antennal segment 3 was 1.5 times the length of segment 4.

DISCUSSION

Different bee species play vital role in pollination and survival of plant species in nature. Some species have been used for crops pollination and increase in yields to meet their food requirements for humans and the economic value of the crops. Bumblebees are used under enclosed farming of crops especially vegetables and fruits. Their natural population depends on plant species composition flowering patterns and abundance.

The lowest altitude where these bumblebees were observed is around 540 m altitude which is from the parks of Rawalpindi area. However another species B. terrestris widely used in commercial crop pollination has been observed from zero altitude in the east Mediterranean region showing their diverse climatic adaptations (Gurel et al. 2008). Their absence in our areas below this level might be due to the harsh summer in the subtropical environment and in the range observed might be due to their mountainous region with harsh winter months to meet their hibernation needs. This represents to be their

specific needs of certain temperature range and other climatic parameters. Another species B. atratus from Java however has been reported

throughout the year with presence of reproductives (Michener and Amir 1977). Their numbers were more in rainy climate rather than dry however their

Table II.- Plant species visited by Bombus haemorrhoidalis form Margalla and Murree hills Pakistan throughout the year 2011-12.

Family###Plants###Scientific name###Status###Flowering time###Location

Asteraceae###Zinnia###Zinnia sp###Major###Jul-Aug###Murree F-9 Park

Asteraceae###Wild daisy###Bellis perennis###Medium###Mar-Oct###Murree

Asteraceae###Lesser knapweed###Centaurea nigra###Minor###Jul-Aug###Murree Pir Sohawa

Asteraceae###Centaurea blue###Centaurea cyanus###Minor###Jul-Aug###Margalla

Asteraceae###Sunflower###Helianthus annuus###Medium###Apr-May###Rawalpindi AAUR

Asteraceae###Blue Thistle###Carduus sp###Minor###Jun-Sep###Rawalpindi Pir Sohawa

Cisteraceae###Rock rose###Cistaceae sp###Minor###Jul-Aug###Islamabad Murree

Cucurbitaceae###Cucumber###Cucumis sativus###Medium###Jul-Aug###Rawalpindi Murree

Cucurbitaceae###Musk melon###Cucurbita pepo###Medium###Jul-Aug###Rawalpindi Murree

Ebenaceae###Persimmon###Diospyros kaki###Minor###Mar-Apr###Murree

Fabaceae###Kachnar###Bauhinia variegate###Minor###Mar-Apr###Margalla AAUR

Fabaceae###Amaltas###Cassia fistula###Medium###Jul-Aug###Rawalpindi Margalla

Fabaceae###Lupin flower###Lupinus sp###Minor###Jul-Aug###Murree

Iridaceae###Gladiolus###Gladiolus sp.###Major###Jul-Aug###Murree F-9 Park

Lamiaceae###Sage###Salvia officinalis###Minor###Jul-Aug###Pir Sohawa Murree

Lamiaceae###Dead-nettle white###Lamium sp###Minor###Jul-Aug###Margalla hills

Malvaceae###Okra###Abelmoschus esculentus###Minor###Mar-Jun###Rawalpindi AAUR

Malvaceae###Hollyhock###Alcea rosea###Minor###Jul-Aug###Murree Pir Sohawa

Myrtaceae###Guava###Psidium guajava###Minor###Mar-Apr###Rawalpindi

Plantaginaceae###Fox glove pink###Digitalis sp###Minor###Jul-Aug###Murree

Rosaceae###Apple###Malus domestica###Minor###Mar-Apr###Murree

Solanaceae###Tomato###Solanum lycopersicum###Minor###Mar-Jun###Rawalpindi AAUR

Solanaceae###Brinjal###Solanum melongena###Minor###Mar-Jun###Rawalpindi AAUR

Verbenaceae###Lantana###Lantana camara###Major###Mar-Dec###Margalla

greater numbers was also observed to be due to favorable environmental conditions for their collection. Present studies however were performed on monthly basis and such possibility can be excluded for its collection and observation in the specified region under study.

These bumblebees have established an interaction with their wild host plants for centuries to meet their pollen and nectar needs. Previously no work has shown the foraging range of this bumblebee species. Presence of perennials and annual plants throughout the observation range showed their preference of different plant species belonging to different families. However perennials showed higher preference due to their ability to produce more nectar and pollens based on their longer growth periods (Fussel and Corbet 1992). Flower morphology color and scent are important in cues to meet their pollen and nectar needs by the bees (Stone et al. 2003; Cnaani et al. 2006). Choice of flowers as minor medium or major

source of visitation by these bumblebees might be due to variation of sucrose concentration to decrease their foraging time with maximum reward (Cnaani et al. 2006). The collection of the food resources has been considered as important factor for their survival and fecundity (Raine et al. 2006). Honeybees and bumblebees keep the record of suitable host plants for food reserves and develop interactive responses with their quick learning abilities (Ali et al. 2014). Body size of the foraging bumblebees been observed as important factor in foraging competitiveness yet B. haemorrhoidalis workers showed non-significant size variation but longer beak size than B. terrestris workers (Ings et al. 2005). Pollen collected by bumblebees can also help to identify the food supply for these important pollinators.

Teper (2006) Identified the foraging plants of B. terrestris by pollen analysis from the bumblebee feces showed 56 pollen grains types from 28 plant families with most of the pollens collected from the entomophilous plants (Teper

2006). Previously observed 29 pollen sources comprised a diverse source for this protein necessary to build the cells breed their young ones and use as a food (Teper 2004). Such a long floral host range provides suitable development of interactions for long term survival for the bumblebee pollinators. Food nest sites and other resources may be shared or competed with exotic Bombus species imported for pollination as observed previously in different parts of the world (Couvillon et al. 2010; Stout and Goulson 2000; Whittington and Winston 2003).

Biological cycle of B. haemorrhoidalis showed a single generation per year (Fig. 1) however it lasted longer than B. terrestris observed previously where diapause period was longer than for the observed species lasting no longer than three months (personal observations). They also observed one generation per year in the coastal Mediterranean region. Different environmental factors including temperature moisture photoperiod and availability of food are also very important limiting factors for their normal colony development. Variation in temperature may also hinder their foraging potential when used for crop pollination (Kwon and Saeed

2003). Under natural field conditions these factors not only activate diapause but also help to wake up and initiate the colony which must be synchronized with flowering plant species (Wuellner 1999; Danks 2007). Decrease in rainfall can also be an important factor for plant development and flower phenology ultimately affecting the visiting insect pollinators (Ogaya and Penuelas 2007) and it was mainly responsible to break the aestivation in bumblebee queens (Rasmont et al. 2005).

Present studies highlighted the importance of this only bumblebee species of this region observed at different altitudes and habitats. Its seasonal distribution in different locations with different flora showed diverse floral host range for collection of nectar and pollens. It has established interaction with certain plant species as a major source of pollination. There existed quite variable population trends of the three castes of this species at the seven locations with maximum population at Lake View Park and Daman-e-koh. Further detailed studies focusing the floral needs nesting behavior and laboratory rearing conditions are desired for this

species to serve under controlled farming systems and benefit the cultivated plant species of economic value.

CONCLUSIONS

Bombus haemorrhoidalis Smith visitation was observed on twenty four plants with diverse plant families as floral resources. These floral plants were the main source for provision of nectar and pollens present in wild and managed parks. The range of the only observed species B. haemorrhoidalis was quite diverse and the most commonly visited plants belonged to family Asteraceae. However plants with longer available floral resources were visited more than short season flowering. Sexual including daughter queens and males were more in fall during October to November after which the mated queen burrow the soil and diapause to avoid harsh winter months. Prevalence of queen workers and males differ from parks to forests with altitude and floral composition.

ACKNOWLEDGEMENTS

We are grateful to the Higher Education Commission for providing funds for the present studies. This is the part of research work of the first author for his Ph.D. degree.

REFERENCES

ABAK K. DASGAN H.Y. IKIZ O. UYGUN N. SAYALAN M. KAFTANOGLU O. AND YENINAR H. 1997. Pollen production and quality of pepper grown in unheated greenhouses during winter and the effects of bumblebees (Bombus terrestris) pollination on fruit yield and quality. Acta Hort. 437:

303307.

ABROL D.P. 2012. Pollination biology: Biodiversity conservation and agricultural production. Springer. New York. pp. 792.

ALI M. S. SAEED A. SAJJAD AND M. A. BASHIR. 2014.

Exploring the best native pollinators for pumpkin (Cucurbita pepo) production in Punjab Pakistan. Pakistan J. Zool. 46: 531-539.

AIZEN M. GARIBALDI L. CUNNINGHAMM S. AND KLEIN A. 2008. Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol. 18:

15721575.

ASADA S. AND ONO M. 2000. Difference in colony development of two Japanese bumblebees Bombus hypocrita and Bombus ignitus (Hymenoptera: Apidae). Appl. Ent. Zool. 35: 597-603.

COUVILLON M. JANDT J. DUONG N. AND DORNHAUS A. 2010. Ontogeny of worker body size distribution in bumble bee (Bombus impatiens) colonies. Ecol. Ent. 35: 424435.

CNAANI J. THOMSON J.D. AND PAPAJ D.R. 2006.

Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration. Ethology 112: 278285.

DAFNI A. 1992. Pollination ecology a practical approach. Irl

Press at Oxford University Press. New York pp. 250.

DANKS H.V. 2007. The elements of seasonal adaptations in insects. Canadian Ent. 139: 144.

FUSSEL M. AND CORBET S.A. 1992. Flower usage by bumblebees: A basis for forage plant management. J. appl. Ecol. 29: 451-465.

GRIFFITHS D. AND ROBBERTS E.J. 1996. Bumble bees as pollinators of glasshouse crops. In: Bumble bees for pleasure and profit. (ed. A. Matheson) IBRA Cardiff pp. 3339.

GUREL F. GOSTERIT A. AND EREN O. 2008. Life- cycle and foraging patterns of native Bombus terrestris (L.) (Hymenoptera Apidae) in the Mediterranean region. Insect Soc. 55: 123128.

HEINRICH B. 1979. Majoring and minoring by foraging bumblebees Bombus vagans. Ecology 60: 245255.

INGS T.C. SCHIKORA J. AND CHITTKA L. 2005.

Bumblebees humble pollinators or assiduous invaders A population comparison of foraging performance in Bombus terrestris. Oecologia 144: 508-516.

KLEIN A.M. VAISSIERE B.E. CANEM J.H. STEFFAN- DEWENTER I. CUNNINGHAM S.A. KREMEN C. AND TSCHARNTKE T. 2007. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B. 274: 303313.

KWON Y.J. AND SAEED S. 2003. Effect of temperature on the foraging activity of Bombus terrestris L. (Hymenoptera: Apidae) on greenhouse hot pepper (Capsicum annuum L.). Appl. Ent. Zool. 38: 275280.

MAKHDOOM S.A. 2011. Diversity of Bombus species (Apidae: Hymenoptera) and utilization of food resources in northern Pakistan. PhD thesis. University of Agriculture. Faisalabad pp. 221.

MALIK S. AND FAROOQ S. 1984. Cultivated trees shrubs and climbers of gardens of Pakistan: Taxonomic studies. PCSIR and Peshawar University pp. 144.

MICHENER D.C. AND AMIR M. 1977. The seasonal cycle and habitat of a tropical bumble bee. Pacif. Insects 17:

237-240.

OGAYA R. AND PENUELAS J. 2007. Species-specific drought effects on flower and fruit production in a Mediterranean holm oak forest. Forestry 80: 351357.

RAINE N.E. INGS T.C. DORNHAUS A. SALEH N. AND CHITTKA L. 2006. Adaptation genetic drift pleiotropy and history in the evolution of bee foraging behavior. Adv. Stud. Behav. 36: 305-354.

RASMONT P. REGALI A. INGS T.C. LOGNAY G. BAUDART E. MARLIER M. DELCARTE E. VIVILLE P. MAROT C. FALMAGNE P. VERHAEGHE J.C. AND CHITTKA L. 2005. Analysis of pollen and nectar of Arbutus unedo as a food source for Bombus terrestris (Hymenoptera: Apidae). J. econ. Ent. 98: 656663.

STONE G.N. RAINE N.E. PRESCOTT M. AND WILLMER P.G. 2003. The pollination ecology of acacias (Fabaceae: Mimosoideae). Aust. Syst. Bot. 16:

103-118.

STOUT J.C. AND GOULSON D. 2000. Bumble bees in Tasmania: their distribution and potential impact on Australian flora and fauna. Bee World 81: 8086.

SUHAIL A. SABER A.M. ASGHAR M. RAFI M.A. AND QADIR A. 2009. Geographic distributional patterns of the genus Bombus (Bombini Apidae: Hymenoptera) in northern Pakistan. BioDiCon 2/1: 1-9.

TEPER D. 2004. Food plants of Bombus terrestris L. determined by palynological analysis of pollen loads. J. Apic. Sci. 48: 7581.

TEPER D. 2006. Food plants of Bombus terrestris L. as determined by pollen analysis of faeces. J. Apic. Sci.

50: 101-108.

VELTHUIS H.H.W. AND VANDOORN A. 2006. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidology 37: 421

451.

WHITTINGTON R. AND WINSTON M.L. 2003. Effects of Nosema bombi and its treatment fumagillin on bumble bee (Bombus occidentalis) colonies. J. Invert. Path. 84:

5458.

WILLIAMS P.H. 1991. The bumble bees of the Kashmir Himalaya (Hymenoptera: Apidae: Bombini). Bull. Natu. Hist. Mus. London (Ent.). 60: 1- 204.

WUELLNER C.T. 1999. Nest site preference and success in a gregarious ground-nesting bee Dieunomia triangulifera. Ecol. Ent. 24: 471479.
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Author:Aslam, Umer Ayyaz; Munir, Sheikh; Imran, Ahmad Muhammad; Nasir, Muhammad; Saeed, Shafqat; Bodlah, Im
Publication:Pakistan Journal of Zoology
Article Type:Report
Geographic Code:9PAKI
Date:Aug 31, 2014
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