Estelar. The available literature on the present investigation and related aspects has been reviewed and presented below under following headings:

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1 CHAPTER-2 REVIEW OF LITERATURE The focus of agriculture in the north-western Himalayan region is slowly shifting from traditional cereal crops to high value cash crops such as fruits and vegetables. Vegetable brassicas such as cabbage, cauliflower, broccoli, mustard, radish and several leafy greens are important crops worldwide, with an acreage of 2.29 million ha. Asia alone accounts for more than 70% of global brassica acreage as well as production (AVRDC, 2011). India is also an important producer of brassica vegetables with an area of 659,000 ha under production (FAO, 2009). This transformation from subsistence systems to commercial agriculture poses new challenges for improving and maintaining productivity and quality. Among those challenges, crop failures due to inadequate pollination have been viewed as major challenge during recent past (Partap, 2002). Many cultivated crops do not yield seeds or fruits without crosspollination of their flowers by pollinators. Approximately, 95% of the species of Crucifers require cross-pollination, although some cauliflower varieties are self- fruitful. Wind is not a good pollinator in Brassica spp. and bees play an important role as pollen vectors. Selfing in the absence of cross pollination generally reduces seed yield, seed size and yield in subsequent generation (Delaplane and Mayer, 2000). Of the total pollination, insects contribute over 80% and amongst insects, bees contribute nearly 80% of the total insect pollination and therefore, they are considered as the best pollinators (Robinson and Morse, 1989). It is also noteworthy that about one-third of our total diet comes directly or indirectly from bee-pollinated crop plants (Hoopingarner and Waller, 1992). Most vegetables from the Brassicaceae family, which are commercially exploited, are represented by hybrids whose seed production depends on entomophilous pollination (Syafaruddin et al., 2006). However, considering the economic importance of these crops insufficient is known about their pollination requirements, or the likelihood of increasing pollination by using honeybee colonies. Thus, the present study aims at the utilization of honeybees for increasing productivity of the major crucifer crops leading to raised economy of the inhabitants of this geographically challenged part of the country. The available literature on the present investigation and related aspects has been reviewed and presented below under following headings:

2 2.1 Honeybee pollination in cruciferous crops Diversity and abundance of pollinators in crucifers Honeybee pollination in cruciferous crops Pollination behaviour of bees on crucifers Pollination efficiency of bees 2.2 Impact of honeybee introduction on pollinator guilds 2.3 Attractants for honeybees 2.4 Toxicity of pesticides to honeybees 2.1 Honeybee pollination in cruciferous crops Diversity and abundance of pollinators in crucifers Oilseed mustard, Brassica was reported to be pollinated by honey bee, Apis mellifera; solitary bee, Osmia cornifrons; native bee species, Osmia lignaria subsp. Lignaria in North Central Regional Plant Introduction Station (NCRPIS), Ames, Iowa state, USA (Abel et al., 2003). Likewise Saure et al. (2001) observed great numbers of bee species (Apidae), hoverflies (Syrphidae) and sawflies (Symphyta) on flowers of rape seed at Michigan State. Studies on pollinator diversity in Diriyah and Derab (Saudi Arabia) by Ahmad (2005) revealed a total of 22 and 16 hymenopterans and 7 and 5 dipteran species visiting mustard flowers. They observed honey bees as the dominant hymenopteran pollinators followed by other bees such as Andrena, Hexachysis, Halictus, Osmia, Pompilus and Dieles and wasps. More abundant dipteran genera on the other hand were Agromyza, Chrysoma, Drosophila and Syrphus. A wide range of insects were again observed visiting oil seed rape (Brassica compestris) by Langridge and Goodman (1975), of which honey bees were major visitors (32.9 %) followed by hover fly (30.7 %), blowflies (22.9 %), native bees (4.9 %) and others (8.8 %). Adegas and Nogueira (1992) reported Apis mellifera, Trigona spinipes and Dialictus sp. as the most frequent insect visitors of rape flowers (Brassica napus var. oleifera) in Brazil constituting 80.6%, 12.8% and 6.6% respectively. Chakravarty (2000) reported Eristalis, Syrphus sp., A. cerana indica, A. dorsata, A. mellifera, Mellipona sp., Bumbus sp., Haliothis armigera, Plusia orichalcea and Pieris brassicae as the visitors of Brassica napus at Pantnagar, Uttarakhand. Chaudhary (2001) reported honey bees (58%), leaf-cutter bee (Megachile hera; 14.4 % proportion), alkali bee (Nomia curvipes; 14.3%), Chalcidoma creusa (7.8%), Andrena sacrissima (2.0%), Sphicodes fumipennis (0.3%), Braunaspis moderata (0.1%), bumble bee (Bombus sp.; 0.1%) carpenter

3 bee (Xylocopa sp.; 0.1%) syrphid fly (1.3%), house fly (0.1%) and butterfly (Danais sp.; 0.2%) as the insect visitors on Brassica campestris var. brown sarson (cv. BSH-1), Brassica carinata cv. Carinata and Indian mustard cultivars RH-30, Laxmi and T-59 in Hisar, Haryana. Sinha et al. (1994) documented that honey bees like A. dorsata, A. cerana indica and A. florea together constituted 49 per cent and Dipterans 49.5 per cent while other pollinators such as solitary bees and Lepidopterans were less than one per cent in mustard. Honey bees were also reported as the most dominant pollinators of winter rape comprising of to per cent from the beginning to the end of blooming. The other pollinators noticed were Andrenidae, Halictidae and Bombicidae (Radechenko, 1964). Bhalla et al. (1983) recorded 7 species of insect pollinators viz., Apis indica, Andrena reticulata (F.), Lasioglossum sp., Eristalis polymacharus and E. tenax (L.) on mustard bloom. Among these, Dipteran were found most abundant visitors (47.08%) followed by honey bees (33.75 %), other insects (9.93 %) and wild bees (9.11 %) while Apoidea was reported predominant in rapeseed and mustard constituting 98.5 percent of total visitors by Chaudhary (2001). Among Apoidea, the social honey bees constituted 59.5 per cent. The little bee, A. florea was the most abundant (42.8%) followed by rock bee, A. dorsata (16.6%). Solitary bees constituted 39 per cent of total visitors. Mishra et al. (1988) observed Apis cerana indica as the most frequent visitor on mustard accounting for 69.5 per cent of total insect visits in Himachal Pradesh whereas Sihag (1988) collected Apis dorsata, A. florea, A. mellifera, Andrena ilerda, A. leaena, Megachile bicolor, M. flavipes, M. lanata and M. nana on mustard bloom in Hisar, Haryana. Abrol (1989) recorded 20 species of insect pollinator belonging to 11 families of Hymenoptera and 1 of Diptera. Of these Apis cerana, A. mellifera, halictid bees, Halictus sp. and Lasioglossum sp., were observed as the most prevalant visitors and important pollinators of Brassica crops. Observations taken at two different sites in Bihar, India, Prasad et al. (1989) revealed that Apis cerana constituted 35% and 20% of insect visitors to flowering B. juncea, A. florea 8% and 24%, A. dorsata 3% and 7%, and Xylocopa sp. 17% and 14%. Similarly Mahindru et al. (1995) found Apis dorsata, A. florea, A. mellifera and Andrena sp. dominantly on brown sarson at Ludhiana, Punjab with an average number of 7.67, 4.17, 3.50 and 0.83 bees per 30 net sweeps respectively. Singh et al. (2004) observed maximum population (23.65%) of A. florea followed by A. mellifera (20.15%) and A. dorsata (0.09%) pollinating toria flowers in Pusa, Bihar (India).

4 In a survey carried out by Kakkar (1981) 34 insect species belonging to 23 families under five orders were reported on cauliflower blossoms. Out of which 15 species belonged to Diptera and 15 species to Hymenoptera. However, the order Hymenoptera was reported to be the most abundant group of pollinator followed by dipterans species (Episyrphus sp. and Syrphus corollae). Likewise Priti and Sihag (1997) also observed 18 species of insect pollinators belonging to 14 families under five orders visiting cauliflower (Brassica oleracea L. var. botrytis cv. Hazipur local) at Hisar, Haryana, India. Of these, four hymenopterans species appeared as the most frequent and voluntary pollinators. Others were being occasional and non-voluntary. Nevertheless, Apis mellifera appeared as most abundant species of pollinator. Mesquida (1978) observed that honey bees were the most frequent visitors (83%) on Kale (Brassica oleracea L.) followed by bumble bees (5.4%) mainly Bombus terrestris, B. lapidarius and other wild bees (7.2 %). Kakar (1980) reported that the highest population of A. cerana (42.1%) on Cauliflower bloom followed by Eristalis sp. (20.9 %), Ceratina sp. (15.1%), Halictus sp. (5.3 %), Lasioglossum sp. (4.7 %) and other insects (10.9 %). Bhatia et al. (1999), while recording pollinator diversity in radish (Raphanus sativus Linnaeus), reported a total 12 insects species of which Hymenopterans (5 species) were the most abundant group followed by Dipterans (4 spp.) and Lepidopterans (2 sp.). Brar et al. (2009) studied the relative abundance of insect visitors on radish var. Pusa chetki blooms and concluded the majority of Apis bees with per cent followed by dipterans per cent, other hymenopterans 8.12 per cent, coleopterans 7.59 per cent, lepidopterans 7.33 per cent and hemipterans as 3.01 per cent respectively. Among the Apis bees, A. mellifera Linnaeus was dominating species (37.30% of total insect visitors) followed by A. cerana (19.11%) while populations of both A. dorsata and A. florea were very low (combined total 6.28%). Apoidea was again regarded as the most prominent flower visitors of radish by Verma and Poghat (1994) constituting per cent of total insect visitors. Among Apoidea, Indian bee, A. cerana was most predominant (47.94%) visitor followed by rock bee, A. dorsata (31.17%) and little bee, A. florea (20.89%). Priti et al. (2001) reported that the pollinators of radish included A. florea, A. mellifera (most dominant due to proximity of the area to an apiary), A. dorsata, Halictus sp. Chrysomya bezziana, Gasterophilus sp., Sarcophaga sp., respectively Honeybee pollination on cruciferous crops At least one-third of the world s agricultural crops depend upon pollination provided by insects and other animals (FAO, 2007). Roubik (1995) suggested that animals particularly

5 bees, pollinate one or more cultivars of more than 66% of the world s 1500 crop species, which includes five species of honeybees namely Apis florea, A. cerana, A. dorsata, A. mellifera and Trigona iridipennis. However of these only A. cerana and A. mellifera are reared in hives in India, as stated by Singh (2007). Bees are more versatile pollinators than any other insects as a result of several behavioural adaptations. Honey bees, Apis mellifera, live in colonies consisting of a single queen, several thousand sterile females and several hundred males in a hive consisting of parallel wax combs. Because honeybees are long-lived and store resources, they are less affected by breaks in resources. They are also less affected by the seasonality (temperature, humidity and daylight) than many other insects, thus these bees may forage over a long period of time (Faegri and van der Pijl, 1971). In addition, honeybees have developed the means of communicating the location of a floral food source to other members of the hive. Recruitment of workers and conditioning of bees to flowers of a certain color or species, allows honeybees to efficiently exploit floral patches (Kapil, 1986). Crane (1980) stated honeybees as important primitive social insects as well as a rich source of honey. The honey has been traditionally used in various diet preparations, medicines, cosmetics, ointments, candles and house hold bee wax items, besides ayurvedic drug preparation. Besides this the use of other bee products as propolis of the bee hive in lip balms and tonics, royal jelly to strengthen the human body for improving appetite, preventing ageing of skin, leukemia and for treatment of other cancers has been emphasized by Singh (2000). Apart from this, utilizing pollinators especially honeybees is considered as one of the cheapest eco-friendly approach in maximizing the yield of cross pollinated crops (Free, 1970) Mohapatra et al. (2010) discussed bees as important components of agro-ecosystem as they provide free ecosystem services in the form of pollination which not only enhance the productivity of agricultural crops but also help in conservation of biological diversity through propagation of wild flora besides providing honey and other hive products. Honeybees during foraging for pollen and nectar from flowers of different plant species enhance agricultural productivity to the tune of % annually through cross pollination as stated by Singh (2000). Role of honeybees in pollination of various crops including cruciferous crops is also known through various sources (Williams, 1994; Singh and Chaudhary, 2006; Singh et al., 2009a). Radish is an important root vegetable crop grown from tropical to temperate climates, throughout the year due to the availability of its season specific cultivars (Brar et al., 2010). Due to sporophytic self-incompatibility, radish is a cross pollinated crop, whereby insects particularly honey bees are however, known to play an important role in its

6 pollination (Kapil, 1970; Rao and Suryanarayana, 1983; Sihag, 1986; Priti et al., 2001). A significant increase in radish seed yield has been reported by providing adequate number of pollinators (Sihag, 1986; Priti et al., 2001). Brar et al. (2010) revealed an increase of 20 to 80 percent in seed yields of radish using A. mellifera whereas 18 to 100 percent increase in radish seed yield has been achieved through introduction of A. cerana by Muhammad et al., 1973 and Kapila et al., According to Kapila et al. (2002) a comparision of the seed quantity and quality of radish var. Japanese white in open and closed conditions revealed higher grains per siliqua, seed yield per plant & 100 seed weight in open pollinated plants which revealed significant role of insect pollinators in seed production of this crop. Woyke (1981a) also reported radish to be a good source of pollen and the blooms pollinated by honeybees produced significant increase in seed yield and quality. Similarly, Verma and Phogat (1994) also reported significantly higher seed set, numbers of seeds per siliqua and test weight in open pollinated radish plants compared to wind and self-pollinated plants. Singh et al. (2009b) stated Brassica rapa var. toria as an important cross pollinated crop particularly of the northern India. Brassica rapa cultivars are generally considered self-sterile and require insect cross pollination for seed production (Singh and Singh, 1992; Singh and Singh, 2002). Several hymenopterous insects have been reported to visit the crop at blooming (Kumar et al., 1998) out of which honey bees (Apis spp.) affect substantial pollination of the crop (Kumar et al., 1998; Kumar and Singh, 2005) and augmentation of the crop yield (Sharma and Abrol, 2004; Singh et al., 2004 and Chhuneja et al., 2007). Honeybees and other insects are known to play an important role in seed setting of Brassica crops and their hybrid seed production (Westcott and Nelson, 2001; Singh and Singh, 2002). According to Howard et al. (1915), the mustard florets open between 9 a.m. and noon, and remain open for 3 days. Usually, the stigma projects about 2 mm beyond the petals the afternoon preceding opening of the flower and is immediately receptive. Soon afterwards, however, the corolla begins to grow and reingulfs the stigma. Then the stamens lengthen so that the anthers are level with the stigma, but when the corolla opens, they turn half around. At this period, nectar secretion by the inner nectaries begins. Just before the flower closes, the anthers turn to their former position, and, if any degree of self-fertility exists, selfing can result. Free and Spencer-Booth (1963) stated that mustard is an insectpollinated crop with ample pollen and nectar to attract pollinating insects. Honey bees in particular are attracted to it and benefit it as observed in case of B. hirta and possibly to B.

7 juncea. The data also indicated that repeated visits would be beneficial and therefore an ample supply of bees should be present during blooming. Toria (Brassica campestris var. toria) is also a highly cross pollinated crop and its seed production depends on insect pollinators (Chhuneja et al., 2007). The entomophilic pollen has large number and greater amount of amino acids (Singh and Singh, 1991) and is nutritionally superior to anemophilic pollen (Stanley and Linskens, 1974). Koutensky (1958) showed that in Czechoslovakia three fields of B. campestris, well provided with honeybee colonies, had seed harvests which were 775, 830 and 820 kg/ha greater than control plotswithout colonies nearby. Free and Nuttal (1968) also reported an increase of 13 percent in the seed yield of Brassica napus plots with bees as compared to those without bees. Free and Spencer-Booth (1963) found that bees more than doubled seed production of B. alba while in B. juncea, the production was increased by 14 percent, which could be of great significance to the grower. Pritsch (1965) also obtained significantly greater yields of white mustard in cages with bees than in cages where bees were excluded. Similarly Koutensky (1959) showed that the seed yield of white mustard was increased 66 percent by honey bee pollination Pollination behaviour of bees on crucifers Bees feed almost exclusively on pollen and nectar (Masierowska, 2003) and need to visit a great number of flowers in order to satisfy the colony s needs (Corbet et al., 1991). The attractiveness of a crop to honeybees may be related to its fragrance (Mussury and Fernandes, 2000) and abundant food resources (Williams, 1980; Mesquida et al., 1988). The behaviour of pollinator matters in pollination. The pollinating efficiency of anthophilous insects is intimately related to the floral biology of the vegetable species and to their foraging behaviour (Flores and Trindade, 2007). For a pollinating agent to be effective, this behaviour should favour the transportation of anther pollen to flower stigmas on the same plant or different target species plants (Freitas and Paxton, 1996). Honey bees are included in this context, whose foraging behaviour is favourable to the increase of crop productivity (D Avila and Marchini, 2005). In a comparative study on foraging behaviour of A. mellifera and A. c. indica on mustard at Palampur, Himachal Pradesh, Thakur et al. (1982) recorded that A. mellifera constituted a maximum of 29 per cent of total foragers as compared to A. cerana indica which accounted for 27 per cent at 1000 h. He also reported higher number of A. cerana indica bees foraging in mustard in the morning than A. mellifera but both species had a similar peak in the noon.

8 The number of A. mellifera was higher than A. cerana indica after h. Pollen foragers of both the species were found in more number in the morning than afternoon, constituting a maximum of 29 percent at h and 27 percent at h of the total foragers respectively. They observed highest pollen foraging activity during February to March and July to October and that of nectar-foraging during February to April and October to November. Benedek et al. (1972) recorded that individual honey bee (A. mellifera) took on an average of 4.4 min to visit 39 flowers on oilseed rape. One bee visited 342 flowers on 186 plants in 35.5 min. While Kapil and Kumar (1974) recorded A. dorsata foragers visit an average of and flowers per minute on Brassica juncea. Verma and Joshi (1983) observed that the foragers especially honey bees (A. cerana, A. mellifera and A. indica) were found active throughout the year on cauliflower, higher pollen collection between 0800 and 1100 h in February-March and July-September, while higher nectar collection between 1200 h to 1400 h during February-April and October- November at Jeolikote (Nainital). They also reported that Apis cerana indica stopped foraging on cauliflower after 1800 h under mid hills conditions. Dhaliwal and Bhalla (1981) found that 70% of cross-pollination in cauliflower occurred between 0900 and 1500 h, with most set resulting from visits between 1100 and 1300 h. In Brazil, Adegas and Nogueira Couto (1992) noticed that rape flowers were visited by A. mellifera, Dihalictus sp., Megachile sp., Thectochlora alaris and Trigona spinipes and documented the highest daily visit frequency at around 0900 h for A. mellifera and 1000 h for T. spinipes and Dihalictus sp. Chand et al (1994) reported the foraging activity of the insect pollinators, Apis cerana indica, A. mellifera, A. dorsata, A. florea, other hymenopterans, lepidopterans and dipteran insects on Indian mustard from December 2, 1990 to January 14, 1991 at weekly intervals, from 0900 to 1600 h at Pusa, Bihar, India. According to them A. c. indica was the dominant pollinator of Indian mustard, followed by A. dorsata, A. mellifera and A. florea. The maximum number of visits was recorded with A. c. indica (34 to 43 percent), followed by A. dorsata (20 to 26%). The average activities of A. mellifera, A. florea and other insects were below 13 per cent throughout. They also worked out a positive correlation of A. c. indica activity with temperature, while humidity had no significant effect. However, A. florea had a significant negative correlation with minimum temperature. He also reported that the foraging activity of A. cerana indica increased at 1000 hr and reached peak at 1100 hr on mustard bloom. While the activity of A. dorsata increased from 1400 hr and reached the peak at 1600 hr.

9 Kumar et al (1994) recorded the foraging speed of different types of honey bees and solitary bees in toria. Honey bees showed higher foraging speed than solitary bees because the former spent less time on a flower. The time spent by the nectar gatherer and pollen gatherer was different. Nectar gatherer of A. mellifera spent 3.64 second per flower whereas pollen gatherer spent 3.37 second per flower and their foraging speed was higher than the nectar gatherer. A. ilerda, H. catullus and H. splendidulus spent 4.24, and sec per flower. Foraging activity of honey bees (Apis dorsata, A. cerana, and A. florea) and syrphids were studied by Desh Raj and Rana (1994) and Sinha et al. (1994). They noticed maximum visits between 1200 to 1400 h when 70 per cent of the pollinators visited the mustard crop. This was in comparison to A. mellifera and A. c. indica on B. campestris var. brown sarson which spent maximum time per flower at 0900 h and thereafter between 1200 to 1500h. Rana et al. (1997) on the other hand observed higher foraging activity at 1200 h for both A. mellifera and A. c. indica and lowest at 0900 h. However, both the species were found in equal proportion on the crop from 1200 to 1500 hr. The mean number of A. cerana foragers was significantly higher (1.90±0.35/m 2 /2 min) than the A. mellifera foragers (0.54±0.08/m 2 /2 min). Meanwhile Rao (1997) reported that A. mellifera initiated foraging late and stopped early, while A. cerana started foraging early, almost coinciding with the anthesis of flowers, dehiscence of anthers and liberation of pollen in flowers. From pollination point of view he considered it important as fresh pollen is available when stigma becomes receptive. Kumar and Singh (2005) reported that A. mellifera dominated over the rest of the Apis species visiting Brassica spp. while A. florea was least dominant. It was reported that Apis spp. was highest in the week having comparatively higher temperature and lower relative humidity. They also recorded abundance of Apis spp. at different hours of the day and noticed their peak activity at 1300 h (27.76) and minimum at 1500 h (14.91). Sarangi and Baral (2006) observed that the population of A. cerana indica, A. mellifera and A. dorsata on mustard reached their peaks at 1100 h when average temperature was C as compared to the population of A. florea which attained its peak at 1300 to 1400 h at an average temperature of 27 0 C. They also reported that the population of Apis species increased with the decrease in RH and attained peak at 47.1% RH except A. florea which peaked at 43.2%. They further reported that activity of A. cerana indica, A. mellifera and A.

10 dorsata peaked at an average wind speed of 10.5 km/h. However, further increase in wind speed was found to have an adverse effect on their population. Radchenko (1966) worked out the foraging rate of honey bees visiting cauliflowers to the extent of 5-6 flowers/minute. Likewise Atwal et al. (1970) recorded the foraging rate of A. cerana indica, A. florea and A. dorsata on mustard with an average of 12.7, 17.2 and 16.6 flowers per minute respectively. Pandey and Tripathi (2003) reported that A. cerana indica showed the highest frequency of visits followed by A. dorsata, A. mellifera and A. florea in mustard. Regarding the time spent A. dorsata workers took the least time followed by A. mellifera, A. cerana indica and A. florea. Experiment conducted by Raju et al (1997) revealed highest average foraging rate (9.31 bees per flower) of A. mellifera in mustard followed by A. dorsata (9.91), A. florea (6.42), Halictus sp. (5.40) and flies (4.76). However, somewhat different results were obtained in sunflower crop. Amongst the four species of honey bees A. florea visited maximum number of flowers (6.28 flowers/minute) followed by A. cerana (5.47), A. mellifera (4.47) and A. dorsata (3.54). The peak hours of foraging for A. dorsata, A. florea, A. mellifera and A. cerana as observed by them were 0900, 0831, 11:50 and 17:00 and 0800 to 1200 h, respectively. Chakravarty (2000) recorded the foraging rate of Apis cerana, A. mellifera, A. dorsata and A. florea as 19.25, 18.80, and flowers/ minute respectively. He further observed that A. mellifera visited an average of flowers/ minute in caged mustard as compared to flowers/ minute under exposed condition. Sharma et al. (2001) also carried out experiment to observe the foraging behaviour of Apis spp. on the flowers of Brassica campestris var. sarson and showed that Apis florea spent maximum time (3.5 sec per flower) but visited least number of 6.7 flowers per minute. However, A. mellifera spent least time (1.64 sec per flower) but visited highest number of 15.2 flowers per minute on mustard followed by A. dorsata that spent 2.18 sec per flower and visited 12.0 flowers per minute. Rana et al. (1993) conducted studies on foraging activity of A. mellifera and A. cerana indica at the hive entrance during rape seed bloom. The results revealed that the returned foragers were significantly maximum in A. cerana indica (22.22 ± 0.82) compared to A. mellifera (17.59 ± 0.82) at hive entrance. In both species, highest peak foragers were recorded at 1200 hr and there was no much difference in the number of foragers at 0900 and 1500 hr. Uma and Verma (1994) made observations on A. cerana foraging on radish flowers from 0640 to 1839 hr with peak foraging between 1100 and 1400 hr. Workers spent on an average

11 of 4.5, 5.3 and 12.8 sec. per flower, visited 8.0, 9.0 and 5.0 flowers per minute and collected 11, 10 and 7 mg of pollen at 0900, 1200 and 1500 hr, respectively. Verma and Phogat (1994) reported the foraging activity of A. cerana, A. dorsata, A. florea and other insects on radish from morning to evening with peak foraging activity between 0800 to 1000 hr, respectively. There after the activity declined as the hours of the day progressed. While Sihag et al. (1999) during his studies on foraging pattern of A. dorsata, A. mellifera and A. florea on eight cultivars of oil seed crop, reported low honey bee visitation frequency in the morning whereas peak was obtained between 1100 to 1300 hr which again declined in the evening. Sharma and Singh (2001) noticed the foraging time of A. florea and A. dorsata in carrot ecosystem. A. florea spent more time (37.09 sec/flower) and visited less number of flowers (2.20/min) as compared to A. dorsata that visited more number of flowers (4.31/min) and spent less time (9.20 sec/flower). Foraging behaviour has also been recorded for A. dorsata by Neupane et.al. (2006) on different crops viz., litchi, lemon, bottlebrush, cucumber, summer squash and radish in terms of bees foraging per m 2 per minute at different flowering densities during different hours of the day. He concluded the highest mean no. of foragers (8.04/min/m 2 ) on bottle brush at 7.30 am during early flowering period followed by litchi, summer squash and lowest (0.25/min/m 2 ) on citrus at 5.30 pm during late flowering. The bees never visited radish and cucumber. Pollen was preferentially collected from bottlebrush, summer squash and citrus in the morning and nectar from litchi and bottlebrush throughout the day. Foraging behaviour of Apis cerana was also recorded on buckwheat (Fagopyrum esculentum Moench) by Singh (2008). He recorded the daily time of initiation and cessation of foraging, total duration of foraging activity, peak foraging hours, time spent on the inflorescence and the number of inflorescence visited per minute by marked bees at 9.00 h, h and h Pollination efficiency of bees The pollinators efficiency in transferring pollen grains partially determines a species reproductive success (Schlindwein et al., 2005). Since most species of angiosperms rely at least in part on animals for reproduction, the interaction between plants and pollinators is one of the most pervasive mutualisms in the natural world. Plant-pollinator interactions are also extremely variable. Although the relative frequency of generalization in plant pollination systems in nature is not fully known to us (Waser et al., 1996; Johnson and Steiner, 2000; Vazquez and Aizen, 2003), the pollinating community visiting a plant is often quite diverse during a given year (Fishbein and Venable, 1996; Olsen, 1997; Kandori, 2002; Ivey et al.,

12 2003). Pollinator communities may also vary in the relative abundance of each taxon visiting a plant (visitation rate) and in the effectiveness of each taxon at transferring pollen (pollen effectiveness), with some plant visitors not pollinating at all (Spears, 1983; Armbruster et al., 1989; Fishbein and Venable, 1996). Pollinators often have considerable spatial and temporal variation in their visitation rates to a single plant species (Herrera, 1988; Traveset and Saez, 1997; Fenster and Dudash, 2001; Ivey et al., 2003). Thus, to understand plant reproduction and floral evolution in generalist plant species, a thorough understanding of each pollinator taxon s effectiveness and visitation rates is essential. Several pollination biologists have recognized the need to estimate the relative importance value for each visiting taxon (Johnson and Steiner, 2000; Fenster et al., 2004), which incorporates both pollinator s quantity (visitation rates) and quality (effectiveness) (Lindsey, 1984; Olsen, 1997). According to them, effectiveness can be estimated by various methods such as the amount of removal and/or deposition of pollen (Herrera, 1987; Pettersson, 1991; Fishbein and Venable, 1996; Ivey et al., 2003), the pollen load on pollinators (Lindsey, 1984; Sugden, 1986; Talavera et al., 2001; Moeller, 2005) and the probability of contacting stigmas and anthers (Lindsey, 1984; Sugden, 1986; Armbruster, 1988). Combining estimates of pollen removal with pollen deposition effectiveness (or with seed set) can provide an estimate of pollinator efficiency, defined as the number of pollen grains deposited or seeds set per pollen grain removed (Galen and Stanton, 1989; Harder and Thomson, 1989; Young and Stanton, 1990; Conner et al., 1995). Many of the organisms visiting a population of flowering plants are not pollinating agents but nectar or pollen thieves that do not benefit the plants (Barrows, 1976; Rust, 1979; McDade and Kinsman, 1980). Before any meaningful investigation into a plantpollination system can be undertaken, it is often essential to determine the importance of a visiting species to the plant population under investigation. A measure of pollinator effectiveness is needed (Eugene Spears, 1983). Measures of pollinator effectiveness can be divided into direct and indirect measures. Indirect measures, in general, rely on the pollen carried by the visitor as an indicator of effectiveness (Beattie, 1972; Ehrenfeld, 1979) whereas direct measures of pollinator effectiveness are measures of seed set by a plant population in response to pollinator visits. Direct measures are commonly used in agricultural research (Alderz, 1966; Tepedino, 1981) Importance of bees as pollinators of crops has been revealed by Grigorenko (1979) in buckwheat whereby a single visit of a blossom by a bee increases plant productivity by 25-

13 30% and 3-4 insect visits are enough to pollinate one blossom. Thus the efficiency of a pollinator in pollinating a flower can be measured as how efficient the insect deposit pollen in a single visit to the flower. This can be indirectly measured as how many visits of a pollinator are required to have an optimum seed set in the particular plant. 2.2 Impact of honeybee introduction on pollinator guild Insect pollination of agricultural crops is a critical ecosystem service. The value of managed vs. wild pollinator services has recently been the focus of much attention (Allsopp et al. 2008), particularly with reference to global food crops and their pollination requirements (Klein et al., 2007; Aizen et al., 2008; Winfree 2008). Many studies have demonstrated a positive relationship between pollinator diversity and existing vegetation in agro-ecosystems (Steffan-Dewenter et al., 2002; Klein et al., 2003; Blanche et al., 2006; Ricketts et al., 2008). Fruit, vegetable or seed production from 87 of the 115 leading global food crops depends upon animal pollination (Klein et al., 2007). There are over 16,350 species of bees in the world, of these several have been developed as crop pollinators, while the Honeybee is still the "queen" of the pollinators and are most widely recognized and known pollinators of many crops of the world (Gupta, 2003). But honeybees while foraging, in some crops, are often able to remove nectar or pollen without effecting pollination and for this reason, native bees are considered more efficient pollinator compared to other pollinators in several crops. Thus efforts for conservation and management of the diversified group of Non-Apis bees should seriously be made to utilize their potential as crop pollinators (Westerkamp, 1994). Wild and domesticated Non-Apis bees effectively complement honey bee pollination in many crops (Greenleaf and Kremen, 2006; Hoehn et al., 2008). Thus in order to obtain optimum seed set from various crops, it is necessary to focus on other locally available or native pollinators which are usually wild in nature. For understanding this, the prevalence of any competitive interactions between the two i.e. honeybees and other native pollinators is of great importance. Honey bees are known to affect the foraging behaviour of native fauna on flowers elsewhere in the world (Butz Huryn, 1997). Effect of bee introduction on the foraging activity of native bees in Melastoma affine D. Don (Gross 2001) and bumblebees on Phacelia tanacetifolia (Walther- Hellwig et al., 2006) are well documented. Thomson (2004) experimentally introduced honeybees and found that proximity to hives significantly reduced the foraging rates and reproductive success of Bombus occidentalis colonies. Roselaini- Mendes et al. (2004) reported the detrimental effects of introduced honeybees (A. mellifera.)

14 on native plant (Clusia arrudae) pollination due to deterrence or expulsion of native pollinators or depletion of their floral resources. According to them, floral visitation by the introduced honeybee affects male fitness and probably fruit and seed production of this tropical tree. Clusia arrudae is a dioecious species and is pollinated by individuals of euglossine bees, Eufriesea nigrohirta that visit its flowers to collect resin. Male flowers are also visited by individuals of A. mellifera, which removes approximately 99 percent of their pollen grains. When E. nigrohirta visits flowers previously visited by A. mellifera, they carry on their bodies less than 0.1 percent of the pollen grains carried by bees leaving flowers not visited by the honeybee. Thus bee visits is negatively correlated with seed set of C. arrudae. In New Zealand, honey bees forage on a vast number of native and introduced plant species (Butz Huryn, 1995; Donovan, 2007), suggesting the potential for competition with native flower visitors for floral resources. While acknowledging the potential for floral resource competition, Donovan (1980) concluded that anthropogenic factors, such as land disturbance through agriculture and the removal of native vegetation are more likely to influence native bee abundance than competition with honey bees. Several native bee species have also been observed exploiting pollen and nectar resources alongside honey bees on introduced plants such as onion and Brassica rapa (Howlett et al., 2005; 2009). Competition for nesting sites does not occur as native species are ground nesting (Leoiproctus and Lasioglossum spp.) or nest within the hollows of plant material (Hylaeus spp.) (Donovan, 2007). Some researchers indicate that foraging patterns and abundance of native pollinators are altered in the presence of honey bees (Roubik, 1978; Schaffer et al., 1983; Sugden and Pyke, 1991; Paton, 1993; Wenner and Thorp, 1994; Vaughton, 1996; Gross and Mackay, 1998; Gross, 2001; Hansen et al., 2002). Although they could not succeed to investigate any potential detrimental effects of introduced honey bees on food storage or on reproduction of native bee species (Roubik, 1983; Sugden et al., 1996; Butz Huryn, 1997; Steffan-Dewenter and Tscharntke, 2000; Thorp et al., 2000). In a long-term study, Roubik and Wolda (2001) found no decrease in population size of native insects in the presence of Africanized honey bees in a Central American rain forest. Walther- Hellwig et al. (2006) found that short-tongued bumblebees avoided areas of forage close to honeybee hives, while carder bumblebees switched to foraging later in the day and were displaced from their preferred food plant. Thomson (2006) found a strong overlap between the foraging preferences of the two species, which peaked at the end of the season

15 when floral resources were scarce, corresponding with a negative relationship between honeybee and bumblebee abundance. In Scotland, Goulson and Sparrow (2009) found that workers of four common bumblebee species were all significantly smaller in areas where honeybees were present. 2.3 Attractants for honeybees Crucifers are important crops grown for seed production. As already reported honeybees are important pollinators contributing to fruit or seed setting of crucifers. According to Langridge and Goodman (1974) foraging honeybees tend to move from one flower cluster to another flower cluster rather than visiting all the flowers in one cluster. Therefore a chance of incomplete pollination still prevails. Further, when different flowers bloom at a certain time, bees tend to move to the most preferred flowers leaving the crop of interest unattended. Thus the use of attractants may prove effective in inviting bees to untouched flowers/ crop of interest. According to earlier reports, Woodrow et al. (1965) screened the natural and synthetic materials as attractants and repellents of A. mellifera by observing response of bees to their vapours. Out of 195 formulations tested, four were rated as weak to moderate attractants and 19 were moderate to very strong repellents (materials viz., alcohols and one fatty acid having more carbon atoms). Allsopp and Cherry (1991) studied the attraction of A. mellifera to volatile compounds and concluded that anetholes and commercial traces of Japanese beetle lure (10:22:11, 2 phenyl ethyl propionate: eugenol: geraniol) exposed in trace in Japanese beetle traps attracted A. mellifera but other floral lures and fatty acids did not attract the bees. Henning et al. (1992) studied behavioural responses of A. mellifera to primary alfalfa floral volatiles in a screened flight chamber. They found that linalool was the only compound attractive to honey bees at the optimized concentration. Two other compounds, 3-octanone and methyl salicylate were repellents. The remaining two compounds cis-3-hexenyl acetone and ocimine were neither attractive nor repellent. Two application of Bee-scent (a liquid formulation containing 9.00 per cent pheromone and per cent other natural attractants) tested on watermelon cultivars in Florida increased total fruit yield to 3000 fruits/acre in farm with the treatment as compared to 1500 fruits/acre without treatment. The number of seeds per fruit was also found higher on the treated farms (Elmstrom and Maynard, 1991). Zvendenok (1996) treated onion with secondary attractants viz., citral, geraniol, limonene and carrot seed extract and recorded significant increase in pollination with citral per cent having the greatest effect.

16 Naik et al. (2003) reported that sugar syrup containing extract of dried fruits of Fagara budrunga Roxb. plant was more attractive to A. cerana than sugar syrup. Spray of fruit boost and Bee-Q significantly enhanced visitation by A. dorsata, A. cerana, A. mellifera and other pollinators in sunflower. However, attractants lost their efficacy after 5 days of spraying (Manjunath, 2003). According to Nidagundi (2004) significantly more number of fruits (14.00) was obtained in the treatment with cacumbe in comparision to 8.40 and 5.33 fruits obtained in open pollinated and caged crop without bees, respectively. Significantly highest length of fruits, seed to pulp ratio, fruit weight and total yield were obtained in crop sprayed with bee attractants compared to crop caged without bees in bitter gourd. Ortiz-Sanchoz (1993) reported the efficacy of Bee-here (Nasonov pheromone, other honey bee attractants and control release formulation aids) as honey bee attractant to marrow crop (Cucurbita pepo L.) under greenhouse conditions in Almeria, Spain. Honey bee counts were made on plants sprayed with recommended dose (3 ml/l), plants sprayed with half the dose, plants sprayed with water and untreated plants. The bees did not exhibit preference for any experimental treatment indicating that this product being ineffective as honey bee attractant to marrow flowers. Evans et al. (1995) reported that a lure containing liver and sodium sulfide had no significant effect in improving carrot seed weight. 2.4 Toxicity of pesticides to honeybees Cruciferous crops are attacked by many insect pests as DBM, head caterpillar (Crocidolomia binotalis), web worm (Hellula undalis), butterfly (Pieris spp.), flea beetle (Phyllotreta spp.) and aphids (Brevicoryne brassicae, Lipaphis erysimi, Myzus persicae) which cause significant yield losses. Farmers prefer to use chemical pesticides for controlling these pests because chemicals have an immediate knock down effect, and are readily available in local markets (AVRDC, 2011). All cruciferous crops are cross pollinated whereby insect pollination plays an important role. Important pollinators or flower visitors of the crops include honeybees, bumble bees, flies and many others (Muhammad et al., 1973; Hussein and Abdel-Aal, 1982; Free, 1993; TNAU Agritech portal, 2008), but honeybees are known to be the predominant species. Pesticides used on field crops for the control of pests have their side effects, one of which is toxicity to honeybees. Honeybees are susceptible to many pesticides. Three types of harmful effects evident in agriculture are loss in production of honey, contamination of bee products and reduction in the yield of cross pollinated crops. Apart from direct mortality, synthetic insecticide may cause alteration in the social behaviour of honeybees as an increase in agitation, aggressiveness and pollen contamination in

17 honeybees treated with insecticides (Johansen, 1984). The harmful effects may be due to the direct exposure of honeybees to pesticides or through indirect contact with their residues. Direct exposure occurs from bees visiting the field at the time of spray, while the indirect exposure occurs from the spray drift or bee foraging in sprayed crops (TNAU Agritech portal, 2008) or contact with the contaminated/ sprayed parts. Use of insecticides results in repellence or toxicity to bees, thus reducing the crop yield (Haq and Gardezi, 1983; Illarionov, 1995). By definition insecticides are harmful to insects but individual products vary greatly in their toxicity to bees. An ideal insecticide should be effective against target pests but safe to pollinators and beneficial insects. Hence the knowledge of relative safety of insecticides during flowering stage is essential to obtain the maximum benefit from the bee population (Gour and Pareek, 2004). Habitat loss/ fragmentation, diseases and parasites and exposure to broad spectrum insecticides are reported as important factors contributing to declining populations of honeybees, native bee species and other pollinators worldwide (Watanabe, 1994; Kearns et al., 1998). Flowering rape is extremely attractive to foraging honeybees and is sought after by beekeepers as a source of honey. Even at the yellow bud stage there are likely to be some bees on the crop. There is therefore a considerable risk that insecticide applications will poison honeybees, particularly if it coincides with flowering. Insecticide formulations which minimize this hazard while still giving effective control of the pests are therefore desirable (Needham and Stevenson, 1973). Domesticated honey bee pollinators are constantly exposed to pesticides particularly when their colonies are sited in agricultural areas (Weick and Thorn, 2002). Many experiments revealed different insecticides having differential toxicity to honeybees. In an experiment based on LC 50 values, Kapil and Lamba (1974) concluded methyl demeton, endrin and dieldrin as moderately toxic whereas, malathion, parathion, phosphamidan, lipdane, phorate and mevinphos as toxic insecticides to Apis cerana. Deshmukh (1991) also reported malathion as highly toxic to honey bees in field experiments resulting in minimum visits. Chlorpyriphos was reported as highly toxic to A. cerana foragers (Thomas and Phadke, 1994). To this point the fungicides have reported relatively less toxic to the bees. However, even though fungicides may not affect bees, residues can be found in pollen grains and nectar collected by bees from treated plants (Kubik et al., 1999).

18 MATERIALS AND METHODS

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