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Status of bee keeping in Himachal Pradesh, India: A review

Beekeeping in Himachal Pradesh is very primitive. Indigenous beekeeping with Apis cerana is an integral part of the social and cultural heritage of rural and tribal communities. Comparative morphological studies have revealed that Himachali bees are smaller than Kashmiri bees. Beekeeping with Apis mellifera is migratory and it helps in increasing the honey production through exploitation of different bee flora thereby providing opportunity for overcoming unfavorable climatic conditions as well as attack of local bee enemies. Comparative studies have revealed that A. mellifera bees were very prone to stinging and were easily distributed as compared to A. cerana which were less excitable and could be safely handled. Major bee enemies of the state include Thai sac brood, Nosema, Europeon Foul Brood, ectoparasitic mites, Wasps, birds and bear. Plectranthus is one of the major honey flow flora for the winter months in Himachal Pradesh.


Introduction History and Status of beekeeping in Himachal Pradesh
The earliest record of beekeeping in Himachal Pradesh was reported in 1882-1884 when Sir various locations. In addition to this, there were about 300 professional beekeepers having about 9800 A. mellifera and 100 A. cerana colonies. There were about 600 A. cerana colonies in log and wall hives (traditional). The number increased to about 90,000 colonies of A. mellifera and the number of beekeepers increased to 1500 with production of 1700 MT honey in low to high hills of Himachal Pradesh (Neha et al. 2020). Mattu (1992) [34] has reported 3-kg honey per A. cerana colony from Himachal Pradesh. Sharma (2001) reported in a survey of 60 beekeepers in district Kangra, Himachal Pradesh that migratory bee keeping resulted in higher honey yield (41.60 kg/colony) as compared to stationary beekeeping (15.66 kg/colony), the cost structure of the two was not statistically significant. The net returns were higher in former as compared to the later. Sharma et al. (2015) [68] also reported 20 kg average honey per A. mellifera and 3 kg honey per A. cerana colony. Kumar and Kaundal (2016) [32] reported annual honey production of 8.15 kg per colony in Kangra district which was quite low.

Indigenous honey bee keeping with A. cerana
Honey bees have been serving mankind since time immemorial and beekeeping is one of the most traditional practices in India. Indigenous knowledge refers to the unique local knowledge existing within, and developed around a particular geographic area (Grenier 1998) [20] . Beekeeping with Apis cerana is an indigenous industry and forma an integral part of the social and cultural heritage of rural and tribal communities. The beekeeping industry forms an integral part of the social and cultural heritage of rural and tribal communities in the country. It is also an environment friendly occupation (Verma 1989;Verma and Partap 1993) [89,90] . A. cerana is gentle in temperament, industrious and well adapted to the ecological conditions of South and Southeast Asia. In this Himalayan region bee colonies require special care particularly in the winter and monsoon seasons. In these seasons, bee activities are reduced to a minimum due to the low outside environmental temperatures particularly during January and February, and the prolonged wet conditions during July-August. Consequently there are problems of inadequate food reserves, queenlessness, reduced fecundity and diseases. As a result of this Apis cerana colonies often abscond or desert the hives (Verma 1990) [84] . Indigenous bee keeping methods in log and wall hives are still in common in Kullu valley despite of the fact that modern beekeeping started here in 1934. Bees are kept in traditional hives made from wood of Pinus wallichiana (kail) and Picea smithiana (rai). Log hives are locally known as "dhindhor" in Kullu valley are made from hollowing out the tree trunk   [69] . They reported that sealed honey is harvested twice in a year during June (summer) and November (winter). According to survey conducted in Chamba, there were 2.45 traditional wall hives per house with occupancy rate of 53.94%, testifying the richness of the culture. These indigenous hives are locally known as "Ganari" in Chamba district (Verma and Attri 2008) [92] . In Sirmaur district of Himachal Pradesh Apis cerana are kept in traditional wall hives of different sizes, dimensions and designs (Thakur and Kumar 2009) [83] . A survey conducted in the Sirmaur district revealed that there are 2.92 wall hives per house and the occupancy rate of each hive is 71.94% testifying to the success of traditional methods (Kumar and Thakur 2014) [33] . Various substitutes and substrates have been tried as feed for A. cerana in Himachal Pradesh. The one of the earliest such references reported by Sharma (1951) [75] who reported that buckwheat flour prepared in the form of half-cooked sweetened pancake was the best among the cereals tried on A. cerana in Himachal Pradesh for bee colonies. But since then no major work was carried out for supplement feeding in Himachal Pradesh. An experiment was conducted to work out the optimum schedule for supplementary feeding to A. cerana in Katrain village in Kullu valley. The study revealed that there is no need of giving traditionally practiced supplementary feedings as in the form of pollen and sugar during the prolonged wet months of July to August in Katrain area as sufficient bee flora is available to the colonies during this period in this region. It may thus be possible to start economical bee keeping with Apis cerana on small scale at orchardist level (Nirupma et al. 2018a) [44] . In another study conducted at Kullu valley on brood rearing efficiency in indigenous bee A. cerana, it was revealed that per cent adult emergence on egg basis during the months of March and August averaged to 55 [45] . The colonies of A. mellifera are restricted only to modern hives. Hence A. cerana plays an important role even in forest ecosystem for maintaining biodiversity. Due to promotion of beekeeping with A. mellifera, the population of A. cerana is declining rapidly threatening its existence in the Himalayan region (Nirupma et al. 2018b) [45] . Dhaliwal and Sharma (1973) [14] in their studies on flight range of A. cerana on cauliflower and barberry flowers reveals that maximum foraging range in cauliflower was 900m and on barberry was 1,100m. Further, studies on flight range of A. cerana reveals that all the foraging bees collected syrup upto about 650 m from the hive along gentle gradients (below 10°), and up to 250-300 m along steep gradients (above 20°) (Dhaliwal and Sharma 1974) [15] . Foraging behavior of A. cerana in Shimla hills revealed that foraging activity was greater in summer and autumn as compared to other seasons of the year and the peak nectar collection was observed after the peak of pollen collection (Mattu and Verma 1985) [39] . Verma and Dulta (1986) [86] reported that the duration of a foraging trip in both the species of honeybees increased with the increase in altitude of the place and this duration was significantly longer at 24.00 and 18.75 m than at 13.50 m in Jubbal area of Shimla hills. At higher altitudes, both the species may make less trips per day than at lower altitudes.

Biochemical studies
The extraction and quantitative extraction of the thoracic flight muscles of different species of the genus Apis and two ecotypes (Himachali and Kashmiri) of Apis cerana were done in summer (active) and winter (inactive) seasons. Glycogen was the major fuel source in the flight muscles of the different species of honeybees, and the ecotypes of A. cerana. The amounts of glycogen, total lipids, glycogen phosphorylase, succinic dehydrogenase and glycerophosphate dehydrogenase per mg of thoracic flight muscle (fresh weight) of the 4 species of honeybee and two ecotypes of A. cerana followed the pattern, A. dorsata > A. mellifera > A. cerana > A. florea, P<0·01; A. cerana Kashmiri > A. cerana Himachali, P<0·05. The amounts of glycogen, total lipids and activities of all the ~ 259 ~ The Pharma Innovation Journal http://www.thepharmajournal.com enzymes were significantly higher (P<0.01) in summer than in winter, for all the species and ecotypes (Dulta and Verma 1989) [19] . Dulta and Verma (1987b) [8] reported that all four species of honeybees and two ecotypes of A. cerana (Kashmiri and Himachali bees) differ from each other in the size of flight muscles. With a few minor exceptions the length and breadth of indirect and accessory indirect Right muscles followed the order A. dorsata > A. mellifera > A. cerana indica > A. florea, with statistically significant differences between species (P<0.01). The order of size for direct flight muscles differed from the indirect muscles, with A. cerana indica > A. dorsata > A. florea > A. mellifera. Mattu andVerma (1983, 1984a, b) [35] reported three different ecotypes of A. cerana indica in the Manipur, Himachal and Kashmir regions of the north-east and north-west Himalayas, and arbitrarily called them Manipuri, Himachali and Kashmiri bees. The order of body size of these ecotypes was Kashmiri > Himachali > Manipuri. In the studies on tongue length of Indian honey bees collected from Himachal and Kashmir, it was indicated that this character was not related to altitude. A significant positive correlation was established between altitude and different parts of the antenna for bees of the Himachal region (Mattu and Verma 1983) [35] . Similar studies were done with wings. The results revealed that length and breadth of both fore and hind wings, proportions of several wing-vein cells, size of some cell angles, and number of hamuli of Himachali bees was positively correlated with altitude (Mattu and Verma 1984a) [36] . Comparative morphometric studies on hind leg, tergites and sternites of Indian honey bee indicated that these tended to be larger among Kashmiri bees as compared to Himachali bees (Mattu and Verma 1948b). Sharma (1990) [76] found higher dimensions of metatarsus in A. mellifera from Himachal Pradesh (India).There was significant variation with locality and a positive correlation with altitude for all measured parameters of the hind leg in Himachali bees. These studies are well supported by the recent research studies which reveals that Hindu Kush/Kashmir bees are somewhat larger than those of Himachal Pradesh (Radloff et al. 2005) [47] .

Morphometric studies on honey bees
Morphometric studies on A. mellifera samples collected from different locations of Himachal Pradesh revealed that head height × width, proboscis length, thorax length, abdomen length, fore wing length × width, cubital index, hind wing length × width, number of hamuli, coxa length, trochanter length, femur length, tibia length and metatarsus length × width were found to be 3.19±0. 10 [24] .

Stationary and migratory beekeeping with A. mellifera
Migratory beekeeping helps in increasing the honey production through exploitation of different bee flora thereby providing opportunity for overcoming unfavorable climatic conditions as well as attack of local bee enemies (Sharma and Raj 1985) [73] . Kumar and Kashyap (1996) conducted studies at sub-temperate, sub-humid mid hills and wet temperate high hills and found that sugar feeding is necessary during different seasons for maintaining A. mellifera as stationary beekeeping.   [63,65]

Comparative studies between Apis cerana and Apis mellifera
A. mellifera bees were found to be very prone to stinging and were easily distributed as compared to A. cerana which were less excitable and could be safely handled (Atwal and Dhaliwal 1969) [3] . A. cerana is more tolerant of low temperatures, compared to A. mellifera. Verma (1970) [87] found that A. cerana started working early in the day when the temperature was quite low during autumn and winter. The brood rearing activity of A. mellifera and A. cerana was compared by Hameed and Adlakha (1973) [23] in Kullu valley. It was observed that A. mellifera reared 38 per cent more brood than A. cerana during spring season. Mattu andVerma (1984a, b, c, 1985) [36,38,39] reported that heavier pollen load is carried by A. mellifera compared with A. cerana which is contributed to the larger body parts of the former. Gupta Verma and Dulta (1986) [86] in Shimla which reveals that worker bees of A. cerana started their foraging activity earlier in the morning (mean time 0603 hours) than A. mellifera (mean time 0627 hours). In the evening also, A. mellifera ceased their foraging activity earlier (mean time1855 hours) than A. cerana (mean time1913 hours). Foraging trips by A.mellifera lasted significantly longer. According to studies conducted on apple orchard at Mashobra (2282 m), it was reported that maximum number of bees visited blooms viz. 3-4 bees/10 flowers for A. cerana and 2-4 bees/ 10 flowers for A. mellifera, when kept in the center of the orchard. Comparative hoarding behavior of A. mellifera and A. cerana in terms of amount of sugar syrup hoarded per bee per day revealed that A. mellifera hoards significantly more sugar syrup than A. cerana (Rana 1989) [60] . Aggressive behavior of both bees was also studied by Rana (1989) [60] [1] . It was reported that middle branches of apple, plum and kiwi crops were more attractive for honeybees than lower and upper heights (Mattu et al. 2012) [40] . Mattu and Bhagat (2016) [41] reported that A. cerana foraged for significantly longer time and visited more flowers per minute than A. mellifera, however, A. mellifera took greater time for completing a single forging trip and spent significantly more time per flower than A. cerana in Kullu Hills of the state. Peak foraging activity for A. cerana occurred at 1000 to 1300 hours and it was between 1200 to 1500 hours for A. mellifera.

Role of honey bees in Pollination
A. cerana is reported as the predominant visitor of mustard accounted for 27% of the total flower visitors of mustard in Himachal Pradesh, India (Thakur et al. 1982) [82] . In another study, A. cerana was found to be the most frequent insect visitor in Allium spp. A. dorsata foraged exclusively for nectar, but although most A. cerana collected nectar, a small percentage collected both nectar and pollen. The amounts of pollen adhering to the bodies of foraging insects varied greatly (Kumar et al. 1985) [31] . A lot of work has been done regarding the role of honey bees in pollination of apple bloom in many developed countries but very little has been done in the temperate regions of Hindu-Kush Himalayas. Verma (1987) [88] ; Dulta and Verma (1987a) [17] studied the role of honey bees on fruit set, fruit drop and fruit quality of apples in Shimla Hills. Higher fruit sets reported in honey bees The Pharma Innovation Journal http://www.thepharmajournal.com pollinated flowers than in open pollinated flowers suggested that degree of cross pollination done by honey bees was greater than that done by other natural insect pollinators. Most apple cultivars grown on a commercial scale in Himachal Pradesh are self unfruitful. They require a compatible cultivar for cross pollination to get a good fruit set. Orchardists rely on honey bees for effective pollination. In order to supplement bee population during flowering, The Europeon honey bee, A. mellifera was tried on apple (Verma 1992;Kakkar 1993) [85,26] . In another study on kiwi fruit conducted at kiwi orchard (var Allison) of Dr. Y. S Parmar University of Horticulture and Forestry, Nauni University farm, it was reported that six species of insect pollinators visited the kiwi fruit bloom; A. mellifera, A. cerana, A. dorsata, Eristalisn sp., Episyrphus sp. and  [22] . Maximum fruit set (6.08 per cent) was recorded when pollinizers were located at the shortest distance (Kakkar 2000) [27] .

Insect pests and diseases
The Melissococus plutonius infection killed about 60% of the native bee colonies during 2002 in Himachal Pradesh, north India. The disease exhibited field symptoms similar to those of mite infestation, Thai sac brood virus and also to the symptoms of European foulbrood disease (EFB). In A. cerana, symptoms similar to TSBV (Figure 1) were tonguelike projection, mortality of brood at the second day after sealing in perforated diseased combs, and change in color of the brood which can be easily removed and absconded. (Rana et al. 2004). EFB is still prevalent in A. cerana throughout the country. In 2003, sac brood virus was detected at two locations in Himachal Pradesh. EFB disease affected 6.18 to 18.56% colonies and and 7.88 to 25.33% brood of A. cerana. The diseased colonies were treated by feeding four doses of 10 mg of ciprofloxacin (98% a.i.) until the disappearance of all EFB symptoms (Rana et al. 2012) [57] . At Nauni (district Solan), it was detected in colonies during spring and summer (March-May) affecting 0.39 per cent to 5.20 per cent of the brood where as at Jachh (district Kangra), the disease was also detected during March to June infecting 0.23per cent to 2.10 per cent of brood (Rana and Rana 2015) [50] . Survey studies in six districts of Himachal Pradesh reveals that the period of incidence of European foulbrood was different in Kullu (April-May), Solan (May-June) and Sirmaur (June-July) districts. In Himachal Pradesh, the disease was effectively controlled by feeding terramycin/ oxytetracycline in A. mellifera within 10 days of feeding it @ 200mg (5% a.i.) in 300 ml sugar syrup/ colony (Bahman and Rana 2002) [5] . Sacbrood disease was recorded for the first time in India during 1998 from the Kangra district of Himachal Pradesh, Northern India (Chandel et al. 1999) [9] . The severity of the TSBV gets reduced in due course of time in Himachal Pradesh. According to different studies, it killed 80% brood in 95% colonies in mid-eighties (Rana et al. 1986) [52] , 27.5% brood in 25% colonies in late nineties (Rana et al. 2001) [53] , and 7% brood in 47% colonies during 2005-2006 (Rana 2008) [59] . Later, Sac Brood Virus (SBV) was detected in two locations of Himachal Pradesh viz. Nauni and Jachh. At Nauni, it was detected in colonies during spring and summer (March to May) when it affected 0.39% to 5.20% of the brood. At the second location, Jachh, the disease was also detected during spring and summer (March to June) when it affected 0.23% to 2.10% of brood. The incidences of the disease were found to be significantly correlated with colony strength and brood rearing   [59] . Studies conducted on disease and other natural enemies on A. cerana in Kullu valley indicated that colonies were highly infected with Thai sac brood disease whole year. Due to this disease, absconding in 10 bee colonies was also observed (Nirupma et al. 2018c) [46] . In India, studies on etiology of the disease have not been done. However, characterization with regard to isolation, purification, serology, antigenecity, electron microscopy, and molecular level has been conducted at HP University, Shimla, and University of Horticulture and Forestry, Solan, in collaboration with Central Potato Research Institute (CPRI), Shimla (Rana et al. 1986;Rana et al. 1987;Rana et al. 1991;Rana et al. 2001;Rana et al. 2003a, b;Rana et al. 2007;Rana and Rana 2008) [52,51,53,63,65,52] Nosema disease infestation was observed by beekeepers during May-June at Una and August-September at Nalagarh (Solan). Among enemies, bear and lizard were observed by beekeepers to attack A. mellifera colonies during different timings of year. Bear was reported as a major problem in Kinnaur area (Telangi and Reckong Peo) during May to July. A. mellifera colonies migrated to Kinnaur were also attacked by lizard in May-June. As per as concerned with the management of Varroa, beekeepers are using sulphur (Nalagarh, Kinnaur, Kullu and Lahaul and Spiti), Thymol (Nalagarh and Kinnaur) and Formic acid (Bajaura) in A. mellifera colonies (Brar et al. 2018) [6] . Five apiaries of A. mellifera were surveyed during autumn and winter months to study the symptoms of Nosema ceranae in Himachal Pradesh. The results revealed that the infected bees were crawling in front of hives with swollen abdomens. They were unable to fly and walk properly. In diseased bees, the ventriculus was white with less constriction. The microscopic studies revealed the presence of several, oval to sausage shaped spores (4.5 μm ± 0.109 x 2.1 μm ± 0.093). Pathogenic studies showed that 81.06% bees died at 16th day of post infection which confirms the virulence of the disease. Confinement of A. mellifera bees in hives was avoided by feeding sugar syrup (50%) to each colony in order to manage the disease was not found to be effective (Divya et al. 2018) [16] . Thakur and Sharma (1984) [81] found spiders as enemies of A. mellifera at Palampur, Himachal Pradesh. Large mammals such as skunks and bears are classified as the pests because they do a little damage to the colony, generally thought as predators (Sharma and Raj 1988) [74] . Kumar and Sharma (2003) [30] reported that September to October was the period of high incidence of ectoparasitic mite, Tropilaelaps clareae in A. mellifera at Bajaura in Kullu valley. Wasps are the one of the major threat to beekeeping industry. Wasps are not only mortal to the bees, but also burgle their egg, brood and honey stores. Maximum incidence of V. auraria was reported during July to November when temperature and relative humidity was high (Kumar et al. 1998; [28,54,55] [30,77] also reported that September to October was the period of high incidence of Tropilaelaps clareae in A. mellifera at Bajaura in Kullu valley. Maximum predatory activity of V. auraria and V. mandarinia was observed during August, September, October and November months of the year in Himachal Pradesh (Sharma et al. 2011a) [78] . In other studies in Shivalik Hills of Himachal Pradesh, the incidence of ectoparasitic mites, Varroa spp., was found maximum in the months of November, whereas peak attack of Tropilaelaps clareae was recorded in the month of September (Sharma et al. 2011b) [79] . An intensive survey was conducted in 30 apiaries, located in different agro climatic zones of Himachal Pradesh reveals, among invertebrates, insects and arachnids were the most prominent pest of honeybees. Hymenoptera (17), Diptera (3), Lepidoptera (2) and Coleoptera (2) and Orthoptera (1), Dictyoptera (1), Odonata (1) and Thysanura (1) were prominent (Sharma et al. 2013). A positive correlation between number of V. auraria and V. mandarina in honey bees colonies was established by Sharma and Mattu (2014) [77] in Himachal Pradesh. Survey conducted in Kangra district revealed that ectoparasitic mite, Varroa jacobsoni caused a severe damage. Beekeepers also reported the presence of pests like lesser wax moths (Achroia grisella), Greater wax moth (Galleria mellonella) and Hawk moth (Acherontia styx) (Kumar and Kaundal 2016) [32] .  [6] . Ectoprasitic mites, Nosema, Sac Brood and EFB have been reported in Kangra, Kinnaur, Solan districts of Himachal Pradesh. Wasps were reported as major insect pest in these three districts causing 15-18 per cent (July-October 2017, Solan), 12-15 per cent (June-October 2017, Kangra) and 8-10 per cent (June-August, Kinnaur) damage to A. mellifera colonies. Hand killing of wasps by flapping and burning wasp nests were the management practices adopted by beekeepers (Neha et al. 2020).

Pesticides residues in honey
Pesticides consumption in the state of Himachal Pradesh is very low compared to other states of India. So it is speculated that honey collected from the state is free from the pesticide residues. In contrary to this Sharma and Kashyap (2002) [66] recorded pesticide residues in honey. Among different pesticides analysed in honey, HCH and its isomers were the most frequently detected followed by DDT and its isomers. Cypermethrin was the only synthetic pyrethroid found in honey samples. Residues of organophosphates viz. acephate, chlorpyriphos, ethion and monocrotophos were not detected, however malathion's residue was found exceeding the MRL (5 ppb) proposed by the Ministry of Commerce, Government of India (Choudhary and Sharma 2008) [12] . Pesticides poisoning has been reported by Kumar and Kaundal (2016) [32] in Kangra district where dead or dying bees were seen in the entrance of bee colonies. In the recent studies, residues of pesticides were detected in 12 per cent of samples, of which a majority contained organophosphate residues. Assessment of human health risks suggests that contaminated honey at current levels has minimal contribution to toxicological risks (Atul et al. 2018) [2] . a b

Conclusion
With the introduction of A. mellifera into the state a decline in the population of A. cerana has been noticed threatening its existence in the Himalayan region. Conservation of Indian bee should be encouraged with the promotion of organic farming and avoiding excessive use of pesticides. Crop diversification is required especially in winter months to reduce the periods of floral scarcity. Farmers need to be trained and get aware about the benefits of beekeeping and role of honeybees on pollination of fruits, vegetables and cereals. Queen rearing techniques should be popularized and surplus mated queen must be maintained in nucleus hives.

Disclosure statement
No potential conflict of interest was reported by the authors.