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African Journal, Vol. 26, No. 1, pp. 1 - 17 ISSN 1021-9730/2018 $4.00 Printed in Uganda. All rights reserved © 2018, African Crop Science Society

African Crop Science Journal by African Crop Science Society is licensed under a Creative Commons Attribution 3.0 Uganda License. Based on a work at www.ajol.info/ and www.bioline.org.br/cs DOI: http://dx.doi.org/10.4314/acsj.v26i1.1

WESTERN MANAGEMENT FOR CROP

C.H. TONI1, B.A. DJOSSA1,2, H. YÉDOMONHAN3, E.T. ZANNOU4 and G.A. MENSAH5

1 Laboratoire d’Ecologie Appliquée, Faculté des Sciences Agronomiques, Université d’Abomey-Calavi, Bénin 2 Ecole de Foresterie et Ingénierie du Bois, Université Nationale d’, Benin 3 Faculté des Sciences et Techniques, Université d’Abomey-Calavi, Bénin 4 Laboratoire d’Entomologie Agricole, Faculté des Sciences Agronomiques, Université d’Abomey-Calavi, Bénin 5 Centre de Recherche Agronomique d’Agonkanmey, Institut National de Recherches Agricoles du Bénin

Corresponding author: [email protected]

(Received 11 September, 2017; accepted 9 February, 2018)

ABSTRACT

This literature review seeks to provide an outlook of the use of Western honeybee for crop pollination around the world. It was prepared by collecting information on the use of managed honey , Apis mellifera in crop pollination from different sources. To address pollination deficits, farmers around the world contract with that provide colonies of Western honey, Apis mellifera, in to perform crop pollination. Some farmers pay for the bee colonies they host in their farms; while others obtain them for free. Apis mellifera is widely used for pollination purposes for several reasons, including its polylectic , its wide distribution, its relatively ease and low cost management, and hive products from which the get additional incomes. The Western is used to pollinate 66 commodities on all continents, except Antarctica. A controlled use of for pollination services is reported mainly in developed countries. Because of the low application of technology in Africa, research must be conducted in order to access the need of pollination service and then the profitability of this technology in the current African entomological context. Despite its benefits, the use of managed Western honey bees can affect native and contribute to the spread of diseases, parasites and weeds.

Key Words: Apis mellifera, bee colonies, pollination deficit, pollination services

RÉSUMÉ

Cette synthèse bibliographique a pour objectif de faire le point de l’utilisation des colonies d’abeilles mellifères Apis mellifera pour assurer pollinisation des cultures à travers le monde. Différentes sources bibliographiques sur l’utilisation de l’abeille mellifère ont été utilisées. Il ressort que pour résoudre le problème de déficit de pollinisation, les producteurs à travers le monde contractent avec les apiculteurs pour bénéficier des services de pollinisation de leurs colonies d’abeilles. Certains producteurs payent les apiculteurs pour le service rendu, tandis que d’autres l’obtiennent gratuitement. Apis mellifera est largement utilisé pour assurer la pollinisation des cultures pour plusieurs raisons à savoir le fait que l’abeille butinent plusieurs plantes, sa large distribution dans le monde, la relative facilité à élever l’espèce et les revenus additionnels générés par les produits de la ruche. L’abeille mellifère est utilisée pour assurer la pollinisation de 66 cultures sur tous les continents excepté l’Antarctique. Ce recours aux colonies à des fins de pollinisation a été essentiellement rapporté dans les pays développés. Compte tenu du faible recours aux colonies d’abeilles en Afrique, des études devraient s’intéresser 2 C.H. TONI et al. aux besoins des services de pollinisation ainsi que la rentabilité d’une telle technique dans le contexte écologique africain. L’utilisation des colonies d’abeilles a aussi des effets néfastes tels que la dissémination des parasites et des adventices.

Mots Clés: Apis mellifera, colonies d’abeilles, déficit de pollinisation, services de pollinisation

INTRODUCTION behaviour afterwards (Laurino et al., 2011; Cresswell, 2011). Besides, herbicides can Biotic pollination is a crucial service in the affect pollinators indirectly by decreasing floral reproduction process of flowering . resource availability (Potts et al., 2010). Other About 75% of the world’s crops benefit from factors such as climate change (Rader et al., biotic pollination (Klein et al., 2007). 2013), diseases and parasites (Potts et al., in general, and mainly bees, are the most 2010) have also been cited as causes of wild important pollinators; and contribute to bee decline. pollination of 90% of 250000 angiosperm Given the importance of pollinators in crop recognised worldwide (Pouvreau, production, decline of wild 2004), including 15–30% of production populations and diversity has resulted in decline from plants (McGregor,1976).Pollinators of crop yields in many parts of the world improve the quality, quantity and commercial (Garibaldi et al., 2011; Partap and Ya, 2012). value of crops (Sabbahi et al., 2005; Klatt et To face the pollination deficit problems, al., 2014). These important services different alternatives to ensure crop pollination are provided by wild and managed pollinators have been developed. Some farmers such as (Velthuis and Doorn, 2006; Blitzer et al., 2016). vanilla growers in Uganda, passion Before the development of intensive growers in Brazil and growers in agriculture, wild and native pollinators Sichuan- pollinate their crops by hand provided sufficient pollination to crops (Batra, (Klein et al., 2007; FAO, 2008; Partap and Ya, 1995; Mishra, 1995). However, to increase 2012). This pollination method is difficult and yields and food production, intensive expensive (Partap, 1999; Garibaldi et al., agricultural practices, including the destruction 2012). of natural to set large agricultural growers use hand-held electrical fields, and the use of and fertilisers, shakers mainly in , a method that were adopted by farmers in many countries. is also expensive and can damage These agricultural practices are not without (Bispo et al., 2009). In other cases, farmers negative consequences on natural pollinators. use sprays (Bahadur et al., 2015), but First, large agricultural fields surely fragment the majority of farmers have recourse to and disturb natural habitats on which managed bees to ensure crop pollination. The pollinators rely for , and nesting bees used include cutter bees ( (Kleijn and Raemakers, 2008; Bailey et al., rotundata), alkali bees ( melanderi), 2014). Large farms also reduce several species (Osmia spp.), the insect pollinators in surrounding fields (du Toit, gray-haired bee (Rhophitoides canus), 1988). Second, the use of pesticides reduce several bumble bees (Bombus spp.), several bee species richness and abundance in farms species of stingless bees and honey bees (Apis (Kovács-Hostyánszki et al., 2011). Pesticides spp.) (Bosch and Kemp, 2001; Goodwin, can harm pollinators by direct intoxication 2012). during sprays (Pilatic, 2012); and indirect Among bee species used for crop intoxication via indirect contacts with treated pollination, the Western or European honey plants, or accumulating in and pollen bee (Apis mellifera L.) is by far the most that affect pollinator performance and commonly used species (Klein et al., 2007) Western honey bee management for crop pollination 3 and the most efficient due to the size of its is currently the most used species for colonies, its foraging organisation and habits. pollination purposes for several reasons (Klein Nowadays, millions of hives of Apis mellifera et al., 2007). Apis mellifera is a polylectic are used by farmers and beekeepers for species that forages on a wide variety of pollination of several crops and around species (Cane and Sipes, 2006). By collecting the world. nectar and pollen on several flowers, the Several research documents highlight the Western honey bee contributes to pollination use of Western honeybee in some regions or of number of crops (Klein et al., 2007; Le countries of the world (Partap, 1999; Conte and Navajas, 2008). This bee species is Goodwin, 2012; Paudel et al., 2015). This quite easy to manage and the management literature review seeks to provide an outlook practices are well established and documented of the use of Western honeybee for crop in many regions of the world (Benecke, 2007; pollination around the world. Here, we Bradbear, 2010; Kumar, 2012). Rapid reviewed reasons of the wide use of Apis development of industry in the 19th mellifera for providing pollination services, the century eases keeping honey bee colonies in current state of Western honey bee colonies man-made movable hives, which can be use in crop pollination, crops in which growers transported easily to fields and orchards for use the species and finally limitations and pollination (Anderson et al., 1983; Partap, challenges of honey bee colonies using for crop 1999). Moreover, Apis mellifera colonies have pollination. sufficient number of bees (40,000-70,000 individuals per ), to perform efficiently METHODOLOGY crop pollination (Sammataro and Avitabile, 1988, Stanghellini et al., 1998). This paper was prepared by collecting Economic reasons also motivate the wide information on the use of managed honey bees use of A. mellifera. Besides, pollination Apis mellifera in crop pollination around the services, A. mellifera is managed for hive world. Information were collected from various products mainly the honey. In USA, the second sources including scientific articles, books, source of revenues of beekeepers, after proceedings papers, extension leaflets and pollination services, is the sale of honey publications, thesis dissertations, reports, (Champetier, 2010). Comparing the honey magazines, and personal communication. production, the Western honey bee, A. Crops in which Apis mellifera colonies are Mellifera, is 2 - 10 times more productive than used for pollination were searched on the web the Asian honey bee (), which is (see supplementary material) and sorted into managed for crop pollination in some Asian six groups based on 40 CFR 180.41 - crop countries (Partap, 2003). This comparative group tables (table established with the crop advantage has led to increased use of A. grouping regulation and published in the Federal mellifera for commercial honey production Register of US in 1995). Countries where and pollination services across Asia (Tsutsumi honey bee colonies are used for pollination and Oishi, 2010; Koetz, 2013). Moreover, the purpose were classified per continent. Western honey bee is cheaper than other managed pollinators, such as bumble bees RESULTS AND DISCUSSION (Mann, 2015). According to Partap (2003), the use of A. mellifera is the most cost- Scope for Western honey bee for effective method for pollinating fruit crops. pollination. Several bee species are managed Nests of this species are perennial and for crop pollination worldwide. However, the beekeepers or growers do not need to buy Western or European honey bee Apis mellifera another colony every year, even if they can 4 C.H. TONI et al. replace existing queens about every two years, Managed bees are usually hired by growers to avoid a decrease of the colony performance from private beekeepers or companies and in (Tsutsumi and Oishi, 2010). some cases from government institutions in Finally, the use of A. Mellifera is favoured Europe, America, South Africa and Asia. In by the occurrence of the species on several some countries such as USA and , continents (Africa and Europe) and its where bee colonies use is well developed, there successful introduction to Asia, Australia and are beekeepers for which the main objective the (Bradbear, 2010), covering then is providing pollination services. They move almost the whole world; even though it shows their hives from farm to farm over long some intra-species variability within and distances, throughout the year; and this activity between regions. Thus, the species has 25 constitutes the source of incomes for subspecies distributed and adapted to different them (Burgett, 1999). In recent years, the regions across the globe (Miguel et al., 2007). pollination service provided by managed honey bees alone was estimated to $14.6 billion in History and current status of honey bee the (Bauer and , 2010). colonies use for crop pollination. The use In Africa, the use of managed honeybee of managed honey bee, Apis mellifera, for has been reported only in Tunisia and South crop pollination likely started in 1895 in Virginia Africa (Barbouche, 2009; Allsopp, 2005; Melin (USA), where bee colonies were rented to et al., 2014). However, this practice has been pollinate pears (Waite, 1895). Later in 1909, reported in some scientific experiments in the species was rented for pollination of Democratic Republic of Congo with the in (Weber, 2012). The use of African , (Ndola, honey bee colonies for crop pollination is done 2015), in Benin and Ghana with the cashew, by placing bee hives in or near fields to ensure Anacardium occidentale (Aidoo et al., 2015) a good pollination of a focal crop. Nowadays, in order to assess its effect on crop yield and this practice is developed and well organised farmers income. in some countries such as USA, Canada, To rent managed bee colonies, beekeepers Australia and New-Zealand, Honey bee hives generally contract with growers (Melhim et used for crop pollination can be obtained in al., 2010), even if for some of them a written three different ways, namely (i) hives owned pollination contract is not necessary (Sagili and by growers (Goodwin, 2012; Plant Health Burgett, 2011). A pollination contract specifies Australia, 2013), (ii) hives placed for free mutual responsibilities of beekeepers and because a beekeeper wants to harvest honey growers (Dupree et al., 1995; Melhim et al., from the site (Rucker et al., 2012), and (iii) 2010; Sagili and Burgett, 2011), as it generally hives hired from a commercial beekeeper or provides information on: government institutions (Partap, 1998; Morse and Calderone, 2000). (i) names and addresses of the contracting In the first case, growers must have parties; beekeeping skills to maintain large numbers of (ii) timing of colonies’ delivery and removal; robust hives year-round; or engage a (iii) the pollinated crop and its location; beekeeper to manage the colonies (Goodwin, (iv) number of colonies hired and their strength 2012). In the second case, growers have little (number of frames of brood and bees); control on bee colonies introduced and infected (v) pattern of colony placement throughout managed bees could spread infections to wild the crop; pollinators of their farms (Goodwin, 2012). (vi) right of access and entry for beekeeper Hiring bee hives is the most common method for colony maintenance; used by growers to obtain bee colonies. (vii) rental fee and terms of payment; Western honey bee management for crop pollination 5 (viii) advance notice to the beekeeper if (Sanford and Ellis, 1992). Hive density also pesticides are to be applied and rules of depends on varieties of a focal crop to be use; pollinated (Woodcock, 2012). The supply of (ix) special management practices; sufficient hives is important to ensure good (x) compensation to both parties for any pollination of crops. But high densities of honey additional unspecified tasks, damages, bees could be harmful to crop production since and violations. many flowers are pollinated leading to competition of ovules for the resources Contracts are usually signed early to blooming required for fruit or seed development (Lloyd, period so that beekeepers have time to prepare 1980). This competition could result in abortion colonies. of ovules, seeds and fruits and then reduce Rental fees and managed hive density vary the production (Teixeira et al., 2006). according to the crop to be pollinated. In During the blooming period, the number general, fees for pollination of non-honey of bee hives requested by growers is moved crops (apples, , pears, cherries and to the field by trucks and in the night generally. ) are higher than those for honey crops To avoid that they return to their initial location, such as radishes, red clover, blueberries bees are moved far from that location. Hives (Rucker et al., 2012). The rental fee of are introduced in farms when a sufficient managed bees is rising with time, because of blossom is available. Somerville (1999a, diseases and the increasing demand of hives 1999b) recommended introducing hives into for crop pollination due to the increase in the crops at 5% blossom to avoid bees searching fraction of agriculture that depends on for other sources of nectar and pollen. Hives pollination (Aizen and Harder, 2009; Rucker are spread evenly throughout the crop, or et al., 2012). In-kind payment of honey to placed in groups in a large number if it is not beekeepers is also practiced in some cases possible to distribute them within the crop (Rucker et al., 2012). (Scott-Dupree et al., 1995, Goodwin, 2012). As for hive density, it depends on the In the latter case, it is preferable to place hives attractiveness of the crop to pollinators close to the crop and downwind to allow (Paranhos et al., 1998; Finta, 2004). Higher scent to reach bees. Some orchardists densities of hives are necessary for good place hives on bin trailers that are moved pollination of crops whose flowers are not very throughout the orchard during the flowering attractive. It is really tricky to provide the period (Larue and Norton, 1989). Colonies that precise number of hives required per area for are not on the focal crop could be good pollination of crops, because many replaced by new ones (Scott-Dupree et al., recommendations are available in the literature 1995). During their stay in fields and orchards, for each crop. For avocado pollination, bees are fed with sugar syrup, pollen or pollen McGregor (1976) recommended two hives per substitutes. ha; Williams (1994) indicated eight hives per To increase pollination efficiency of ha; while Dixon (2006) recommended ten hives managed honey bees, different methods are per ha. The number of hives to use per area used to increase bee visits and pollen delivered for a given crop varies according to field and to flowers. Managed bee visits on flowers are colony conditions. Hive density could be increased by spraying honey bee attractants affected by availability of natural habitats near or chemical attractants on crops. Many the crops and then on availability of wild attractants of different compositions are pollinators (Klein et al., 2012; Bailey et al., marketed and their efficiency varies with crops 2014). (Ambrose et al., 1995; Patil et al., 2011; The strength of the colony should also be Jayaramappa et al., 2011). According to taken into account to determine the hive density Delaplane et al. (2010), the best chemical 6 C.H. TONI et al. attractants contain synthetic oilseeds crops such as the sunflower and the or components of Nasonov pheromone. canola (10.61%); forage plants such as clovers Instead of using bee attractants, sugar syrup and the alfalfa (6.06%); tree nuts such as the is sprayed on flowers (Scott-Dupree et al., cashew and the ccoffee (6.06%), herbs and 1995; Goodwin, 2012) or flowers of the crop spices such as the bitter weed and the lavender are ground and steeped in the sugar syrup or (6.06%), pulses such as the runner bean and put in the hive (Larue and Norton, 1989). the field beans (4.55%) and cereal grains such Additionally, removing competing blooms as the corn (1.52%). Most of the crops within or surrounding the farm or orchard identified depend to some extent (1 to 100%) contributes to maintain bee activity on the crop. on pollinators. Crops like the cashew, the To improve the amount of pollen dispersed by canola and durian depend highly (40 to 90%) managed bees, hive inserts are set into the hive on the pollination services; while others like entrance and filled with pollen of crop to be lychee, longan and cabbage have a little (0 to pollinated (Larue and Norton, 1989). When 10%) dependence on pollinators (Klein et al., leaving the hive, bees pick up more pollen that 2007). Managed honey bees pollination will be dispersed on flowers. services improve fruit or crop production For some crops such as apples, it is (apple, almond, pepper, , avocado, necessary to plant appropriate polliniser etc.) as well as seed production (carrot, onion, varieties throughout the commercial cultivar etc.) in greenhouses and on open fields. This (Gupta, 2012). It is also possible to provide confirms that honey bees, in general and pollen to bees by placing flowering branches especially managed colonies, contribute to of pollinisers on the ground underneath the food security and directly trees, in the trees close to flowers to be (fruits, vegetables, nuts, pulses, oilseeds, pollinated, in containers of water spread spices) and indirectly (forage). throughout the crop or grafting polliniser on The use of managed bee colonies for commercial cultivars (Scott-Dupree et al., pollination services has been reported for 22 1995; Gupta, 2012; Goodwin, 2012). Another countries distributed on the five continents way to improve the quantity of pollen collected (Table 2). The practice has been reported by managed bees is to increase pollen foragers mainly in USA (31 crops), Australia (24 crops), of the colony. This is done by increasing the Netherlands (22 crops) and brood to adult bee ratios, trapping pollen or (21 crops). In some countries such as Spain, stripping pollen from hives and feeding sugar Sweden, Germany and Japan, the practice has syrup (Goodwin, 2012). However, for crops also been mentioned. It is noticeable that almost pollinated mainly by nectar foragers, bees can all countries where Apis mellifera colonies are be feed with pollen to increase collection of used to perform crop pollination are developed nectar. countries as stated by Bahadur et al. (2015). Globally, the use of honey bee colonies to Managed honey bee colonies for crops pollinate crops is poorly developed in Africa pollination. Colonies of the honey bee, Apis (2 countries, 15 crops) and in South America mellifera, are used to pollinate several crops. (2 countries, 4 crops). In Africa, bee colonies This review identified 66 crops, which are used to pollinate crops such as carrots, growers successfully pollinate using managed peaches, peppers, mangoes and apples in honey bees (Table 1). The most pollinated Tunisia and South Africa. The low use of groups of crops include fruits such as oranges, Western honey bee colonies for crop mangoes, the kiwifruit (34.85%) and pollination in Africa could be due to weak vegetables such as cabbages, the ccucumber losses of wild pollinators in the continent and tomatoes (30.30%). They are followed by because of a limited agricultural intensification Western honey bee management for crop pollination 7 Herbs and spices Caraway Lavender Phacelia Bitter weed Cereal grains Corn Pulses Coriander Field beans Runner bean Tree nuts Cashew Macadamia Coffee etch Forage and fodder Lucerne/ alfalfa Clovers V Sainfoin/ esparcette Apis mellifera atermelon egetables omatoes Eggplant Turnips Chicory Ginseng Parsley Leek Fennel W and Pumpkins squash, , courgette Rocket/ arugula Radish T V Carrots Onion Peppers Asparagus Cabbages, cauliflowers, broccoli, kale Parsnip Mustard Oilseeds Meadowfoam Rape, canola, swede Sunflower Sesame Linseed Borage vocado ychee ABLE 1. Crops pollinated with managed colonies of honey bee Cranberry Kiwifruit Blueberry Apricots Blackberry/ loganberry/ brambleberry/raspberry Strawberry Currants and gooseberries Passion fruit L Grape Longan Rambutan Durian Holly Cherries A Plums and prunes Fruits T Pears/nashi Oranges, mandarin, Mango tangerine, clementine Apple Peaches and nectarines Pomegranate 8 C.H. TONI et al. TABLE 2. Countries and number of use (crops) of managed honey bee colonies reported for the present study

Continents Africa Asia Europe America Oceania

Countries South Africa(13) China(1) France (19) Canada(19) Australia (24) Tunisia(2) India(1) Germany (1) Brazil (3) New Zealand (16) Israel (2) Netherlands(22) Chile (1) Japan (1) Norway (1) USA (31) Korea(6) UK (21) Thailand (7) Spain (NA) Swede (NA) Bulgaria (1)

NA: Crops’ names are not available

(Vandame and Palacio, 2010; van der Valk et occurring in the continent which are currently al., 2013). managed for honey production could be used Apart from South Africa (13 crops listed), for this purpose. the use of honey bee colonies for crop pollination, mainly the payments for pollination Limitations and challenges of the use of services are almost unknown in Africa Apis mellifera colonies. The use of managed (Bosselmann and Hansted, 2015). Similarly, honey bees, Apis mellifera, for crop pollination poor use of managed bees for pollination of is beneficial for crop production, growers and crops was reported for countries such as beekeepers. However, this practice has some Brazil and Bulgaria, because growers were limits and challenges to overcome. Thought unaware of the importance of bees (Imperatriz the honey bee is the most used species for Fonseca et al., 2006; Panchev et al., 2014). crop pollination, it is not a for all In countries such as USA, Australia, pollination deficit problems. Apis mellifera is Canada and New Zealand, the use of managed not the most effective pollinators of all crops bees in pollination services is so well developed (Stanghellini et al., 1998; Greenleaf and that companies and beekeepers specialised in Kremen, 2006; Bispo dos Santos et al., 2009). providing these services to growers are Therefore, other managed bees such as bumble developed. This practice is so prominent that bees (Bombus spp.) or alfalfa leafcutting bees in , the majority of managed () are preferably utilised honey bee colonies are used for crop for pollination of tomato and alfalfa pollination (The Heinz Center, 2013). respectively. Some wild insects, mainly Delivering pollination services generates assemblages of wild insects have been significant incomes for many US professional demonstrated to be more effective than honey beekeepers; while European beekeepers are bees in pollination of certain crops (Garibaldi rarely paid for such services (OPERA Research et al., 2013). Then pollination services Centre, 2012). provided by wild bees cannot be fully replaced To promote this technology in Africa, by the one delivered by managed honey bees. researches must be conducted in order to Besides, wild bees sometimes contribute to access the need of pollination service and then improve pollination efficiency of honey bees, its profitability in the current African by forcing them to move to many flowers entomological fauna context. Positive results (Greenleaf and Kremen, 2006) as resources from investigations must be followed by are then shared. sensitisation of farmers who are unaware of The pollination efficiency of A. mellifera the importance of bees. Honeybee species is also affected by climate conditions since the Western honey bee management for crop pollination 9 species was found to be less active on flowers et al. (2011), who reported a decline of Apis than wild bumble bees and the Asian honey cerana populations in some Asian countries bee, Apis cerana at lower temperatures after introduction of A. mellifera. In addition (Willmer et al., 1994; Li et al., 2012). In hard to insect pollinators, honey bees could decrease climate conditions (wet, cloudy, or cool), visits of other kind of pollinators ( and Western honey bees remain in their hives ) onto flowers by limiting floral resources (Vaughan et al., 2015) and become difficult (Beard, 2015). Consequently, the effect of to use for pollination of off-season crops. honey bees on foraging behavior and Despite the aforementioned limitations, the population size of pollinators influenced the Western honey bee is probably used for reproduction of some plant species and pollination of many crops because growers do changed the structure of plant communities not have any other commercial alternatives (Howlett and Donovan, 2010). (Greenleaf and Kremen, 2006) and the majority Another effect of the Western honey bee of wild effective pollinators of these crops on wild pollinators is its implication in the have not yet been domesticated. Nevertheless, spread of diseases and parasites. Pathogens some farm management practices providing originally hosted by honey bees have spilled nesting sites around farms or orchards are over to other insect species in which they are established and promoted to ensure the more virulent. For example, introduction of presence of wild pollinators in crops. the honey bee into Asia was followed by a rise Introduction of the honey bee (A. in a pathogen agent, Acarapis woodi, which mellifera) in a crop could lead to competition caused severe losses of A. cerana colonies in with native pollinators for floral resources. For India and Pakistan (FAO, 2006). Pathogens instance, honey bees lessened the availability affecting honey bees were also transmitted to of pollen and nectar of foraging sites, obliging other insect pollinators. This is the case of the other insects to forage elsewhere (Horskins , which occurred in and Turner, 1999; Gross, 2001). In another bumble bees and caused important damages study, the presence of the honeybee, A. (Genersch et al., 2006). Managed honey bee Mellifera, in pumpkin fields significantly colonies could also be affected by diseases and reduced visits of pruinosa, a parasites from wild pollinators. The pollinator of this crop (Artz et al., 2011). (), which jumped from Apis Furthermore, owing to their aggressive cerana to managed colonies of A. mellifera competitor behavior, honey bees robbed nests (Rosenkranz et al., 2010) leading to a dramatic and honey of other honey bees like Apis cerana decline of A. mellifera colonies worldwide, is (Moritz et al., 2005). probably a good example in this context. Apart Competition with the Western honey bee from that, managed honey bees could also could affect the of individuals and later contribute to proliferation of weeds because the survival of populations of inferior insect the species was implicated in pollination of species because their reproductive success some weed species (Collevatti et al., 1998; can be reduced (Thomson, 2004; Elbgami et Barthell et al., 2001). al., 2014). Goulson and Sparrow (2008) Negative consequences of the Western noticed that workers of four bumble bee honeybee introduction in a new area suggest species, coexisting in the same area with honey that researches must be conducted to assess bees had smaller size. Similar results were the effect of the western honeybees on wild reported on bumble bee queens and males close pollinators in controlled conditions before to a honey bee in UK (Elbgami et al., introducing A. mellifera in an area. Several 2014). subspecies of the Western honeybee occur Evidence of the effect of A. mellifera on around the world and are used for honey other insect populations was provided by Yang production by local communities (Bradbear, 10 C.H. TONI et al. 2010). Subspecies naturally occurring in each domestic honey bee colonies to perform area could be used to limit negative effects of pollination of crops effectively pollinated by this practice on the local . A. mellifera. Adoption of this pollination Beekeepers and growers are confronted method will reduce pollination inputs and help with several problems hampering the use of farmers to increase their productivity and honey bee hives for crop pollination. One of incomes. the most important concerns is diseases and parasites, which affect bee colonies, causing CONCLUSION range decline in many parts of the world. The phenomenon of Managed colonies of the Western honey bee, (CCD) whose causes are still unknown, has Apis mellifera, contribute to world food decimated honey bee colonies in some security because of their utilisation for countries (Cox-Foster and van Engelsdorp, pollination of several crops. The fact that honey 2009). Unfortunately, some control products bee use for crop pollination is mainly practiced (miticides and antibiotics) used to treat in developed countries, should guide infections can increase honey bees’ developing countries in the conception of their susceptibility to viruses (Locke et al., 2011). agricultural development models. Some of Honey bee mortality due to queen failure them are already engaged in modernisation of and starvation is another problem that their agriculture, destroying natural habitats beekeepers must overcome to maintain their and increasing agrochemical use. Considering colonies healthy for pollination. These factors the importance of managed colonies of Apis have contributed to large decline, i.e. a mellifera in crop production, and their decline reduction by 26.5 and 49.5% of managed during last decades, it is necessary to improve colonies in Europe and North America management practices of other managed respectively (vanEngelsdorp and Meixner, pollinators or establish favorable habitats for 2010), where managed hive using for native pollinators around farms and orchards. pollination is important. This situation could Diversification of pollinators will surely affect availability of bee colonies to satisfy the improve pollination of crop and secure the increasing demand of pollination services. world against a rapid and unexpected drop of Shortage of honey bee colonies has already honey bee colonies. been reported in some US states, obliging beekeepers to import bees from Australia ACKNOWLEDGEMENT (National Research Council; 2007). Owing to the overuse of pesticides, some We thank Roland Holou for its useful beekeepers are reluctant to rent their colonies comments and suggestions on the manuscript. for pollination in some countries (Partap, 1998; Benecke, 2007). Even if growers renting bee REFERENCES colonies may take precautions before spraying according to contractual arrangements, Aidoo, K., Adzanyo, M., Weidinger, R. and pesticides can be applied in the surrounding Tandjiekpon, A. 2015. The economic farms that could be visited by bees without benefits of integrating beekeeping into any precautions. cashew farms in Ghana and Benin. Countries experiencing lack of sufficient Abstract book of the 44th APIMONDIA pollination, where are utilised as International Apicultural Congress hold pollinators such as in some African countries, from 16th to 19th September 2015 at Daejeon should also improve knowledge of farmers on in South Korea. 118pp. the importance of honey bees in crop Aizen, A.M. and Harder, D.L. 2009. 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