REVIEW ARTICLE


The Contribution of Managed Honey Bees to Crop Pollination, Food Security, and Economic Stability: Case of Ethiopia



Zekiros Fikadu1, *
1 Department of Animal Science, Aksum University, Shire Campus, Shire, Ethiopia


© 2019 Zekiros Fikadu.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

* Address correspondence to this author at Department of Animal Science, Aksum University, Shire Campus, Shire, P.O.Box, 134 Shire, Ethiopia; Tel: +251914000729; Fax: +251344444898; E-mail: zekat2007@yahoo.com


Abstract

This paper reviews the role and economic importance of the pollination service by honey bees (Apis mellifera) to agricultural crops and food security in the Ethiopian context. Honey bees provide pollination services that are crucial for sexual reproduction and improving the quality and quantity of many agricultural crops. From the significant 53 crops cultivated in Ethiopia, 33 (62.2%) of them are dependent on biological pollinators. Besides this, honey bees play a vital economic role, and their contribution to pollination service in agriculture crops is around 0.815 billion dollars in Ethiopia. Nevertheless, this contribution is unnoticed by Ethiopian farmers. Pollination by honey bee plays an essential role in human nutrition and supplies food security, income in households, and ecosystem services. Declines in insect pollinators, including honey bees across the world, have raised concerns about the supply of pollination services to agriculture, and it is because one-third of agriculture productions depend upon pollination, mainly by honey bees. Among the several factors responsible for the decline of honey bee colonies, improper pesticide application, and climate change are the elements and make them at risk. The potential adverse effects of pollinator declines include direct economic losses incurred by reduced crop yields as well as broader impacts on the agricultural activity because of lower productivity in the ecosystems. Through promoting and the use of honey bee pollination service as agricultural development packages, it is possible to improve honey bee production and crop yield in Ethiopia.

Keywords: Crop yield, Economic benefit, Ethiopia, Honey bee, Pollination service, Public perception.



1. INTRODUCTION

Pollination is an essential process in the production of seed plants, and it results in a genetically diverse production of offspring [1]. Globally, one-third of the total human food supply depends on insect pollination [2-5]. Production of agriculture crops is increasing by 50% through bees pollination [2]. Honey bees (Apis mellifera) are economically essential insect pollinators all over the world [6-11]. They provide ecologically for pollination of natural, wild vegetation plants and agricultural crops; as a result, they play a significant role in the landscape and natural resource preservation [6, 10, 12, 13].

The apiculture sector is one of the essential livestock subsectors, which contributes significant importance to the livelihoods of the people in Ethiopia [14]. Beekeeping in Ethiopia plays a vital role in the agricultural, environmental activity, and it serves as a source of additional cash income for beekeepers [15, 16]. This sector plays a great role directly by providing valuable output such as honey, beeswax, queen, bee colonies and indirectly other products such as pollen, royal jelly jelly, bee venom and propolis in which it has high demand globally for different functions including medicinal and nutritional value [17-19].

Animal pollinators include many insect species (managed and wild), species of birds are crops pollinators, and the honey bee are considered one of the primary pollinators [20]. Honey bee plays a central role in agriculture as pollinators, and their contribution to the global economy for food production is estimated between $ 235 and $ 285 billion annually [21] and $0.815 billion in Ethiopia, which is 6.24% of the agricultural GDP [22]. According to Shrestha [23], the impact of honey bee pollination to crop production and quality has been estimated to be more than the value of honey and wax production. The economic benefit of the honey bees pollination service is 4.58 times higher than the honey production in Ethiopia [22].

Other sources revealed that income generation, food consumption, pollination of crops, and natural resource conservation are among the list of importance of the beekeeping sector [24]. Therefore, the objective of this paper will focus on reviewing the role, economic importance of honey bees (Apis mellifera) pollination service to agricultural crops, and food security in Ethiopia.

1.1. Role of Honey Bee Pollination Service on the Productivity of Different Agriculture Crops in Ethiopia

As Central Statistical Agency informs every year, fifty-three significant crops are cultivated in Ethiopia [22]. Out of the 53 major agricultural crops cultivated in Ethiopia, 33 of them (62.2%) are dependent on biological pollinators, and from the total biological pollinator, honey bees contribute 80% of pollination service [22]. This indicated that honey bees are the most efficient insect pollinators in cultivated crops. Workers of honey bees visit multi-flowering plant species at a time to collect nectar and pollen at a time they serve as cross-pollinator. Both survival and conservation of genetic diversity of many crops and wild plant populations largely depend on insect pollination service [25]. Concerning specific insects, it is expected that almost one-third of all plants or plant produced food eaten by humans is dependent directly or indirectly on bees for their pollination [26]. This shows that the life of humans somewhat depends on the existence of honey bee. Without any extra cost for inputs, only the use of crops pollinated by honey bees, has been proven to produce higher yields and better quality [27-29].

Even though improved agricultural technologies include the use of the quality seed, applying techniques, high-yielding varieties, good agronomic practices (timely irrigation and fertilizers) increased agricultural crop production. However, without pollination, neither the fruit nor the seed will be set appropriately. The pollination process is an essential activity for the production of fruit plants, a variety of flowering plants deal with fundamental ecosystems facilities to human welfare [2, 12]. Beekeeping plays a parallel role in the cross-pollination of industrial farming crops and medicinal plants with the manufacturing of honey. The honey bee is a strong pollinator for many crops. It is the pollinator species that can be most easily managed by humans in enormous numbers for the pollination of highly diverse crops [30, 31]. Reports indicate that honey bee boosts the production of different fruit crops up to 30-40% [32] and increases the production of most agriculture crops by 5-50% [2].

Honey bee pollination is as essential for crop production as water and fertilizer but, its role is not well understood and appreciated in the local farming system [33]. Exposing sesame (Sesamum indicum L.) to honey bee during flowering time increases the pod and seed productions [34]. In a study conducted previously, both open pollination and Apis mellifera pollination treatments were sufficient to increase the seed yield of sesame by 22% and 33% [35], and 43.92% and 35.23% [36] respectively, which is more than that of pollination excluding insects. Other scientific documents describe that it is possible to increase the production of sarsoon (Brassica Rapa rilocularis) and toria (Brassica napus) by 47% [37] and yield and physicochemical properties of tomatoes (Solanum Lycopersicum) [38] through honey bees pollination and insect pollinators respectively.

In Ethiopia, research evidence documented that honey bee pollination increased the seed yield of Niger seed by about 43% [39], onion (Allium cepa L.) yield by double [40] and by 94% [7]. According to Bezabih & Gebretsadikan [41], the seed yield of onion increased by 41.2%, the mass of 1000 seeds by 25%, and the germination percentage by 68% through open pollination especially by honey bees. Crane [42], also reported that honey bees pollination increases the yield of Citrus sinesis by 30%, watermelon by 100%, and tomato by 25%. Besides the yield maximization of honey bee pollination service, they also contribute to improving the quality of different crops such as onion [41], apple fruit [43], and sesame seeds [34].

According to Tura et al. [43] from Table 1 through honey bees pollination, it is possible to increase the marketable apple fruit yield by about 50%, and the average marketable apple fruit yield per individual tree is 3.2 kg (caged with honey bees), and 2.2 kg (open to all insect pollinators). Another study by Gebremedhn and Tadesse [44], revealed that pollination of crops caged with a honey bee was significantly affecting the seed yield Niger seed (16.7 quintals/ ha) than crops yield caged without insects (9.6 quintals/ha). Sufficient pollination service results in higher marketable fruit yields and quality, per tree of apple crops, compared with those unexposed to insect pollinators [30, 43, 45]. Generally, the fruit yield of Malus sylvestris increased by 77.8% if we were using honey bee as pollinators and by 22.2% using insect pollinators with free access to the apple trees compared to trees caged without pollinators [43]. The productivity and quality of strawberry were increased by the use of honey bee as a pollinator [46]. Stimulating the use of beekeeping for pollination of crops will be of benefit to both the beekeeper and the farmer. Therefore, farmers should use pollination service to maximize their income without paying an extra cost through only placing the honey bees on the cropland during the flowering session.

1.2. Economic Value of Honey Bee Pollination Service

Cross-pollination through honey bee is essential to increase quality through a more unified ripening period and earlier harvesting time. Honey bees pollination service not only maximizes agricultural crop production but also increases the honey yield harvested from the hive because honey bees collect more nectar and pollen while they pollinate the flowering The economic value of pollinators for some agricultural crops was estimated to be $ 0.815 billion dollars in Ethiopia, and in addition to this, the regional distribution is shown as Oromia and Amhara regional being ranked the first and second regional states to benefit from biological pollinators in the country [22]. In the absence of the pollinators, the economic value may drop by 16% [47].

Table 1. The mean and standard error (SE) of marketable fruit yield per tree, per hectare of apple trees, and seed yield of Niger seed /hectare under different treatment.
Treatment Mean Marketable Apple Fruit Yield
kg/tree + SE (kg)
Average Apple Fruit Yield
kg/ha
Seed Yield of Niger Seed /ha(kg)
T1 = Caged with honey bees 3.2 + 0.4a 3,560 1669a
T2 = Open pollination 2.2 + 0.37ab 2,440 1324ac
T3= Caged without insect pollinators 1.8 + 0.22b 2,000 960c
Table 2. Economic Value of Pollination (EVP) service for biotically pollinated crops (agricultural and horticultural) in Ethiopia.
Crops EVP in US$ Rank Crops EVP in US$ Rank
Coffee 2,500,905.0 1 Groundnut 50,262.1 18
Faba beans 1,431,599.4 2 Linseed 45,561.6 19
Niger seed 1,430,488.6 3 White haricot bean 27,764.2 20
Sesame 549,087.7 4 Ethiopian cabbage 27,082.1 21
Cotton 485,714.2 5 Fenugreek 23,506.0 22
Red pepper 383,424.3 6 Green pepper 14,050.8 23
Mangoes 175,806.2 7 Mung bean 12,932.8 24
Chick peas 166,539.2 8 Safflower 10,192.7 25
Field peas 118,422.3 9 Tomatoes 8,139.8 26
Rape seed 101,567.4 10 Papayas 6,174.8 27
Lentils 99,589.2 11 Oranges 4,473.4 28
Potatoes 90,280.9 12 Head cabbage 4,091.3 29
Grass peas 85,822.8 13 Lupine 3,565.0 30
Avocados 85,132.5 14 Beetroot 3,378.3 31
Soya beans 81,145.1 15 Guavas 1,622.5 32
Red haricot bean 66,134.4 16 Lemons 1,010.7 33
Onion 57,005.6 17

In Ethiopia, during the 2015/16 production season (Table 2), the economic value of pollination service for the specific crops ranges from $ 2,500,905.0 to $ 1,010.7 in which coffee is higher pollination economic value ($ 2.5 million), followed by Faba bean ($ 1.431 million) and Niger seed ($ 1.430 million) respectively [22]. Honey bee pollination service improves both the quantity and quality of apples and its impact is increasing the market value and growers’ profits [48-50]. According to Tura et al. [43], application honey bees pollination service has boosted the income by 136.6 US$ per 100 apple trees. It is important to use honey bees pollination service as a yield-enhancing tool and/or technology and as a development extension package to improve productivity and food security in individual producers’ level and boosting the national economy in Ethiopia (Table 3).

1.3. Perception of Farmers’ on Pollinators and Pollination

Nowadays, there is a global loss of pollination services that resulted in a $302 billion reduction in the value of production across all sectors [57]. Reduction in output through pollination service is due to human-induced impacts such as habitat destruction, land-use change, use of chemicals (pesticides and herbicides), climate change, and invasive species [58, 59]. Abundances and distributions of pollinator species are affecting agricultural yields, and other agroecosystem functions in many ways. About 77% of farmers in the gozamin district of the Amhara region in Ethiopia did not know pollination and the importance of insect pollinator, and they consider crop pests to insect pollinators [60]. The majority of cocoa producing farmers in Ghana (87.6%) did not have the general scientific concept of pollination [61]. However, 50% of beekeeping farmers in the Chitwan district of Nepal were aware of the pollination services provided by the bees [29].

Only a few farmers (23%) know the role honey bees play in pollination service [60], and similar to this the majority of farmers in western Kenya [62] and Uganda [63] were not aware of the importance of pollination for crop production. This indicates the need for training and awareness creation to the farmers on the significance of pollinators to enhance productivity. In most parts of Ethiopia, golden pollination service of honey bees is not recognized well. Therefore, it is still a need and essential to create awareness on the relevance of honey bees pollination service to farmers.

Table 3. Economic values of honey bee pollination in different parts of the world.
Country Economic Values (US$) References
United States of America 14.6 billion [51]
Australia 4-6 billion [52]
East Africa 1.2 billion [53]
Ethiopia 0.815 billion [22]
China 0.7 billion [54]
Uganda 0.46 billion [55]
Benin 0.199 billion [56]

1.4. Pollination and Human Nutrition

The most significant benefit of beekeeping lies in the fact that honey bees pollinate agricultural and horticultural plants. Pollinators play an essential role in human nutrition in the developing world [64]. Besides, the economic impacts and the possible consequences for the socio-economics of human societies, loss of pollination may also affect human nutrition [65]. Insect-pollinated crops are crucial for proper human diet [66], and they provide nutritional variety and nutrients, including lipids, vitamins, folic acid, and minerals, which are essential for human health [2, 66]. In addition to the quality and quantity improvement, insect-pollinated crops also provide about 70% vitamin the deficiency of which is a primary human health concern worldwide, and pollinators are responsible for up to 40 percent of the world’s supply of nutrients [66]. Hence, generally, it is possible to deduce that loss of pollinators and the service they provide could produce a potential problem on human nutrition, although the magnitude of the problem will often depend on geographical location and degree of societal development.

1.5. Contribution of Apiculture to Food Security

Ethiopia designed a competitive advantage in honey and beeswax production improvement to develop a substantial export trade is an essential goal of the Growth and Transformation Plan (GTP) to eradicate poverty [67]. Apiculture is one of the livelihood sources in most developing countries, and its success has been noted in countries like Ethiopia [68]. Beekeeping plays a critical role in agriculture and having many comparative advantages that help farmers to improve their livelihoods and ensure food security [69, 70]. In addition, it is an excellent source of income for landless farmers [71]. Beekeeping has a significant contribution in alleviating poverty and improving the standard and wellbeing of the rural beekeeping community through the income from the sector as secures of financial power [72]. Practically, beekeeping does not compete with crop production and animal husbandry practice, but it is advantageous for agricultural and horticultural plants.

Ethiopian government focuses on the rehabilitated Ex-closure areas given to landless youths through organizing them as trained cooperatives and providing initial capital to run modern beekeeping activities as alternative employment opportunities and food security [73]. The honey bee produces honey, and brood is an essential source of food [74, 75]. In agriculture production, pollination plays a crucial role in enhancing food security and yield stability through the linking of an ecosystem with agricultural production [76-78].

In the country, about 1.55 million households are engaged and getting incomes from beekeeping [79]. Due to bimodal rains, beekeepers harvested honey twice a year [73, 80, 81]. The country produces about 47,352 tons of crude honey and 5.4 thousand tons per year [82-84]. Out of the total honey produced, almost 80%is used for local consumption and for local brewing called Tej, and the remaining is sold either as table honey in the domestic market or to the export market [74]. Keeping a resilient honey bee colony and managing them in a wall manner help to ensure the future viability of crops. It provides vital stability in the agricultural sector and millions of people as employment opportunities. Maximizing the yield of honey bee-pollinated plants can improve the performance of the agriculture sector, increase national wealth, and help to ensure the long-term food security and economic resilience of the rural populations.

1.6. Challenges of Honey Bee Pollination Services

Farmers use different inputs, including pesticides, to grow subsistence and commercial crops of different varieties for agricultural crop maximization. Even if honey bees pollination has proved to be essential for food production, directly and indirectly, the supply of human food and animal feed resources are considered to be at risk today [85-87]. Beekeepers are experiencing high colony losses due to the unwise application of pesticides [88, 89] and climate change [90]. Insecticides and herbicides have been reported as significant causes of death and absconding of the honey bee colonies [91, 92] and their food source [88]. Due to the misapplication of these chemicals, honey bee mortality and reduction of honey bee colonies, which eventually results in a reduction of bee products and crop yield are faced [88, 93]. Reports indicate that there was a decline of honey bee colonies in Ethiopia [47, 60, 91, 94] due to pesticide application and deforestation. The impacts of pesticides on honey bee production are likely to be aggravated by the limited knowledge among users on the toxicological and chemical properties of these substances and the fact that labels on pesticide containers were in a language that cannot be understood.

Even variation in the production system, the average honey bee colony holding capacity of beekeepers is 5 [24, 95, 96]. Agrochemical poisoning is the primary challenge for the beekeeping sector, and three-quarters of beekeepers lose two honey bee colonies per year [89] and some beekeepers lost all their colonies [88] due to unwise application. Through the application of pesticides, the subsequent financial loss to the beekeepers is estimated to be about 819291.4 US$ at selected districts of the Amhara Region, Ethiopia [91]. Scientific study indicates that all of the farmers apply agrochemicals on barley, wheat, millet, and onion before blooming [89] and majority of farmers apply chemicals on mango (92.9%), orange (97.2%), potato (81%) and maize (81%) at blooming and liquid spray at the morning and the middle of the day [89, 91, 92]. The majority of farmers use pesticides at the time when the honey bees most visited the flowering plants to collect nectar and pollen; as a result, they poison themselves or contaminate the resources found in the hive. Pesticide application is increasing its impact, including honey yield, killing flowering plants, pollination service, and efficiency and honey bees population. Limiting the use of pesticides [94] and wise application of pesticides during the flowering period of crops is important to minimize honey bee losses in Ethiopia.

1.7. Knowledge Gaps and Priorities for Future Research on Honey bee Pollination Service

  • The contribution honey bees to pollination service to the yield and/or quality of multiple crops from individual pollinator species and pollinator communities should be identified and documented appropriately.
  • It needs a further assessment of why farmers do not use pollination services as yield and quality improvement tools and technology.
  • The socioeconomic and environmental relevance of honey bees pollination service should be assessed and documented.
  • Skill and knowledge gap on the farmers how and when to use pesticides [89, 91, 92].
  • Farmer’s awareness of honey bees pollination service to agricultural crop production is low [60].
  • Developing conservation policy for pollinators; especially, honey bees, and legislation and monitoring for pesticide application [47, 89, 92].
  • Awareness creation on protecting the honey bees from pesticide poisoning and the importance of honey bees on agricultural crop pollination [47, 60].

CONCLUSION

Globally, one-third of the total human food supply depends on insect pollination and animal pollination. The honey bee is responsible to pollinate 62.2% of crops cultivated in Ethiopia. In this respect, mainly, the honey bee has brought about a significant economic contribution to improve agricultural crop production quantity and quality, essential for ecological maintenance and improvement, human food, and nutrition security in Ethiopia. Nevertheless, the double benefit approach of honey bees pollination service has been overlooked in agricultural development strategies and has not been included as a technological input in agricultural development packages. High-value agriculture is being promoted in several areas and extension institutions offer packages of practices for each type of crop. However, the importance of managing pollination to achieve higher yields still has been overlooked in Ethiopia.

In Ethiopia, farmers have no way of knowing how essential honey bees pollination services to their crops. This gap in the agricultural extension system needs to be addressed by designing policies and strategies to use honey bees pollination service as a tool and technology for the improvement in production and sustainability.

Recently, a decline in honey bee keeping has been reported in Ethiopia, owing to several factors including the unwise use of pesticide climate change. The use of pesticides has been affecting the honey bees through poisoning, death, destroying the honey bees forage, pollination service, and efficiency. This, in turn, results in a reduction of bee products and crop yield.

To reduce the ecological damage and losses, what is required is understanding the commercial and pollination service needs of the country. Furthermore, utilizing honey bees pollination services will help to maintain and sustain the ecology and agricultural crop production. In conclusion, promoting the honey bees pollination service as the tool for improving honey production and crop yield in Ethiopia is essential.

CONSENT FOR PUBLICATION

Not applicable.

FUNDING

None.

CONFLICT OF INTEREST

The author declares no conflict of interest, financial or otherwise.

ACKNOWLEDEGEMENTS

I would like to express my heart full gratitude to my friend Mr. Gedam Brhane for providing critical comments and suggestions besides spending lots of his valuable time editing the manuscript.

REFERENCES

[1] Dafni A, Kevan PG, Husband BC. Practical pollination biology. Cambridge (Ont.). Enviroquest Ltd 2005; 20: 114-28. [https://www.cabdirect.org/cabdirect/abstract/20053155384].
[2] Klein AM, Vaissière BE, Cane JH, et al. Importance of pollinators in changing landscapes for world crops. Proc Biol Sci 2007; 274(1608): 303-13.
[3] Jivan A. The impact of pesticides on honey bees and hence on humans. Lucr Stiint Zooteh Biotehnol 2013; 46(2): 272-7.
[4] Said F, Inayatullah M, Ahmad S, et al. Foraging behavior of the Himalayan Honeybee, Apis cerana (Hymenoptera: Apidae) associated with sunflower (Helianthus annuus L.) at Peshawar District of Khyber Pakhtunkhwa (KP). J Entomol Zool Stud 2015; 3(3): 203-7.
[5] Food and Agriculture Organization of the United Nations (FAO) Roubik DW, Adriano-Anaya ML, Campos LA, et al. The Pollination of Cultivated Plants: A Compendium for Practitioners12018;
[6] Calderone NW. Insect pollinated crops, insect pollinators and US agriculture: Trend analysis of aggregate data for the period 1992-2009. PLoS One 2012; 7(5):e37235.
[7] Amssalu B, Nuru A, Radloff E, Hepburn R. Multivariate morphometric analysis of honeybees (Apis mellifera) in the Ethiopian region. Apidologie (Celle) 2004; 35(1): 71-81.
[8] Allsopp MH, de Lange WJ, Veldtman R. Valuing insect pollination services with cost of replacement. PLoS One 2008; 3(9):e3128.
[9] Le Conte Y, Navajas M. Climate change: Impact on honey bee populations and diseases. Rev - Off Int Epizoot 2008; 27(2): 485-497, 499-510.
[10] Muli E, Patch H, Frazier M, et al. Evaluation of the distribution and impacts of parasites, pathogens, and pesticides on honey bee (Apis mellifera) populations in East Africa. PLoS One 2014; 9(4):e94459.
[11] Pashte VV, Said PP. Honey Bees: Beneficial Robbers. Int J Agri Sci Res 2015; 5(5): 343-52. [https://www.researchgate.net/publication/283010724].
[12] Kevan PG. Pollinators as bioindicators of the state of the environment: species, activity, and diversity. Agric Ecosyst Environ 1999; 74: 373-93.
[13] Garibaldi LA, Steffan-Dewenter I, Winfree R, et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 2013; 339(6127): 1608-11.
[14] Aklilu Y. An audit of the livestock marketing status in Kenya, Ethiopia and Sudan (volume 1). AU-IBAR (Africa Union-Inter-African Bureau for Animal Resources), Nairobi, Kenya 2002; 1-19.
[15] Abebe J, Amssalu B, Kefelegn K. Floral phenology and pollen potential of honeybee plants in North- East dryland areas of Amhara region, Ethiopia. J Agric Vet Sci 2014; 7(5): 36-49.
[16] Gemechis L. Honey production and marketing in Ethiopia. Am J Life Sci 2015; 3(1): 42-6.
[17] Wakhal MD, Bhujbal M, Pais EVD. Analysis of honey, pollen and royal jelly by high performance liquid chromatography-A review. Apiacta 1999; 30(1): 6-11.
[18] Workneh A, Ranjitha P, Ranjan S. Adopting improved box hive in Atsbi Wemberta district of Eastern Zone, Tigray Region: Determinants and financial benefits, IPMS (Improving Productivity and Market Success) of Ethiopian Farmers Project Working Paper 10. ILRI (International Livestock Research Institute) 2008.30
[19] Koshiyama AS, Lorenzon MCA, Tassinaria WD. Spatial econometrics applied to study the influencing factors of honey prices in brazil. Braz J Oper Prod Manag 2011; 8(1): 121-32.
[20] Nielsen A, Reitan T, Rinvoll WA, Brysting KA. Effects of competition and climate on a crop pollinator community. Agric Ecosyst Environ 2017; 246: 253-60.
[21] Lautenbach S, Seppelt R, Liebscher J, Dormann CF. Spatial and temporal trends of global pollination benefit. PLoS One 2012; 7(4):e35954.
[22] Alebachew WG. Economic value of pollination service of agricultural crops in Ethiopia: Biological Pollinators. J Apic Sci 2018; 62(2): 265-73.
[23] Shrestha B. Honeybees and Environment. Agriculture and Environment. Gender Equity and Environment Division. Ministry of Agriculture and Cooperatives, HMG 2004; 1-8.
[24] Zekiros F, Gangwar SK, Meseret H. Challenges on different honey production system in Agro-ecology of Tahtay-koraro north western tigray, ethiopia. Glob J of Bio-Sci and Biotechnol 2018; 7(3): 331-5.
[25] FAO, (Food and Agricultural Organization). Conservation and management of pollinators for sustainable agriculture. The International response. A contribution to the International Workshop on solitary bees and their role in pollination held in Berberibe, Cerara 200419
[26] Bradbear N. Bees and their role in forest livelihoods: A guide to the services provided by bees and the sustainable harvesting, processing and marketing of their products 2009. FAO.Pub.
[27] Kozin RB. Insect pollination of crops.Amsterdam Publishing Press 1976; 125-34.
[28] Berenbaum MR. The Birds and the Bees-How Pollinators Help Maintain Healthy Ecosystems Testimonial before the Subcommittee on Fisheries, Wildlife and Oceans, Committee on Natural Resources 2007.
[29] Devkota K, Dhakal SC, Thapa RB. Economics of beekeeping as pollination management practices adopted by farmers in Chitwan district of Nepal. Agric Food Secur 2016; 5(6): 1-6.
[30] Aebi A, Vaissiere BE, Vanengelsdorp D, Delaplane KS, Roubik DW, Neumann P. Back to the future: Apis versus non-Apis pollination. Trends Ecol Evol 2012; 27(3): 142-3.
[31] Hung KJ, Kingston JM, Albrecht M, Holway DA, Kohn JR. The worldwide importance of honey bees as pollinators in natural habitats. Proc Biol Sci 2018; 285(1870):20172140.
[32] Jadran KK. Measurement of economic efficiency for the projects of bee raising inside and outside towns in Wasit Governorate. Al-Anbar J Vet Sci 2011; 9(3): 112-21.
[33] Jacobs F, Simoens C, Graaf D, Deckers J. Scope for non-wood forest products income generation from rehabilitation areas: Focus on beekeeping. J Drylands 2006; 1(2): 171-85.
[34] Pharaon MA, Dounia Chantal D, Esther NO, Fernand-Nestor TF. Pollination Efficiency of Apis mellifera L. (Hymenoptera: Apidae) on Flowers of Sesamum indicum L. (Pedaliaceae) at Bilone (Obala, Cameroon). Int J Res Stud Agri Sci 2018; 4(3): 12-20. [http://dx.doi.org/10.20431/2454-6224.0403003].
[35] Panda P, Sontakke BK, Sarangi PK. Preliminary studies on the effect of bee (Apis cerana indica F.) Pollination on yield of sesamum and niger. Indian Bee J 1988; 50: 63-4.
[36] Das R, Jha S. Insect pollinators of sesame and the effect of entomophilous pollination on seed production in new alluvial zone of west bengal. Int J Curr Microbiol Appl Sci 2019; 3(8): 1400-9.
[37] Stephen E, Irshad M. Economics impact of pollinators in crop production of Pakistan 2012.
[38] Bashir MA, Alvi AM, Khan KA, et al. Role of pollination in yield and physicochemical properties of tomatoes (Lycopersicon esculentum). Saudi J Biol Sci 2018; 25(7): 1291-7.
[39] Admasu A, Nuru A. Effect of honeybee pollination on seed yield and oil content of niger (Guizotiaabyssinica Proceedings of the First National Conference of Ethiopian Beekeepers Association Addis Ababa, Ethiopia. 2002; pp. 2002; 67-73.
[40] Debisa L, Adimasu A, Gizaw E, Amsalu B. Effects of honeybee pollination on seed allium cepa: HBRC, ethiopia. Ethiopian J Anim Prod 2008; 8(1): 79-84.
[41] Bezabih G, Gebretsadikan K. Managed honeybees (Apis mellifera L.) increase onion (Alliun cepa) seed yield and quality. Livest Res Rural Dev 2014; 26(1) [http://www.lrrd.org/lrrd26/1/gebr26008.htm].
[42] Crane E. Bees and Beekeeping: Science, practice and world resources. Comstock Publishing Associates (Cornell University Press) 1990.
[43] Tura B, Admassu A, Kibebew W. Role and economic benefits of honey bees’ pollination on fruit yield of wild apple (Malus sylvestris (L.) Mill.) in central highlands of ethiopia. Bee World 2018; 95(4): 113-6.
[44] Gebremedhn H, Tadesse A. Effect of honeybee (Apis mellifera) pollination on seed yield and yield parameters of Guizotia abyssinica (L.f.). Afr J Agric Res 2014; 9(51): 3687-91. [https://www.academicjournals.org/AJAR].
[45] Khan AK, Ahmad JK, Razzaq A, et al. Pollination effect of honey bees, Apis mellifera L. (Hymenoptera: Apidae) on apple fruit development and its weight. Persian Gulf Crop Prot 2012; 1(2): 1-5. [https://www.researchgate.net/publication/256838387].
[46] Çolak AM, Sahinler N, Islamoglu M. The effect of honeybee pollination on productivity and quality of strawberry. J Agric Sci 2017; 32(2): 87-90. [https://doi.org/10.28955/alinterizbd.335835].
[47] Bareke T, Addi A. Effect of honeybee pollination on seed and fruit yield of agricultural crops in Ethiopia. MOJ Eco Environ Sci 2019; 4(5): 205-9.
[48] Garibaldi LA, Aizen MA, Klein AM, Cunningham SA, Harder LD. Global growth and stability of agricultural yield decrease with pollinator dependence. Proc Natl Acad Sci USA 2011; 108(14): 5909-14.
[49] Garratt MPD, Breeze TD, Jenner N, Polce C, Biesmeijer JC, Potts SG. Avoiding a bad apple: Insect pollination enhances fruit quality and economic value. Agric Ecosyst Environ 2014; 184(100): 34-40.
[50] Geslin B, Aizen AM, García N, Pereira A, Vaissiére EB, Garibaldi AL. The impact of honeybee colony quality on crop yield and farmers’ profit in apples and pears. Agric Ecosyst Environ 2017; 248: 153-61.
[51] Morse RA, Calderone NW. The value of honey bees as pollinators of US crops in 2000. Bee Culture Magazine, Published by the AI Root Company, Medina, OH, USA 2001; 1-5.
[52] Commonwealth of Australia. More Than Honey: The future of the Australian honey bee and pollination industries. House of Representatives Standing Committee on Primary Industries and Resources May 2008.
[53] Kasina JM, Mburu J, Kraemer M, Holm-Mueller K. Economic benefit of crop pollination by bees: A case of Kakamega small-holder farming in western Kenya. J Econ Entomol 2009; 102(2): 467-73.
[54] Chen YC. Apiculture in China 1993.
[55] Munyuli MBT. Pollinator biodiversity in Uganda and in Sub Sahara Africa: Landscape and habitat management strategies for its conservation. Int J Biodivers Conserv 2011; 3(11): 551-609. [http://www.academicjournals.org/IJBC].
[56] Toni H, Djossa AB. Economic value of pollination services on crops in Benin, West Africa. Int J Biol Chem Sci 2015; 9(1): 225-33.
[57] Bauer DM. The Macroeconomic Cost of Catastrophic Pollinator Declines 2011; 13.
[58] Kearns CA, Inouye DW, Waser NM. Endangered Mutualism: The Conservation of Plant-pollinator Interaction. Annu Rev Ecol Syst 1998; 29(1): 83-112.
[59] FAO, (Food and Agricultural Organization). Tools for Conservation and use of pollination service, Initial Survey of Good Pollination Practices, Glob­al Action on Pollination Services For Sustainable Agriculture 2018.
[60] Misganaw M, Mengesha G, Awas T. Perception of farmers on importance of insect pollinators in gozamin district of Amhara Region, Ethiopia. Biodiversity Int J 2017; 1(5): 54-60.
[61] Frimpong AK, Kwapong PK, Gordon I. Cocoa farmers’ awareness of pollination and its implication for pollinator-friendly practices. Res Rev Biosci 2013; 7(12): 504-14.
[62] Kasina JM, Kraemer M, Martius C, Wittmann D. Farmers’ knowledge of bees and their natural history in Kakamega district, Kenya. J Apic Res 2009; 48(2): 126-33.
[63] Munyuli T. Farmers’ perceptions of pollinators’ importance in coffee production in Uganda. Agric Sci 2011; 2(3): 318-33.
[64] Ellis AM, Myers SS, Ricketts TH. Do pollinators contribute to nutritional health? PLoS One 2015; 10(1):e114805.
[65] Vanbergen JA, Hear M, Breeze T, Potts SG, Hanley N. Status and value of pollinators and pollination services; A report to the department for environment, food and rural affairs (Defra) 2014. ID PH0514.
[66] Eilers EJ, Kremen C, Smith Greenleaf S, Garber AK, Klein AM. Contribution of pollinator-mediated crops to nutrients in the human food supply. PLoS One 2011; 6(6):e21363.
[67] Ethiopia’s agricultural sector Policy and Investment Framework (PIF) 2010–2020. Addis Ababa, Ethiopia: 2010 2010. MoARD.
[68] Mazorodze BT. The contribution of apiculture towards rural income in honde valley Zimbabwe. 2015.National Capacity Building Strategy for Sustainable Development and Poverty Alleviation Conference May 26-28, 2015; 2015.
[69] Aynalem T. Beekeeping, climate change and food security: The case of Eastern Amhara Region, Ethiopia. Livest Res Rural Dev 2017; 29(83). [http://www.lrrd.org/lrrd29/5/tess29083.html].
[70] Reda GK, Girmay S, Gebremichael B. Beekeeping practice and honey production potential in Afar Regional State, Ethiopia. Acta Universitatis Sapientiae Agri Environ 2018; 10(1): 66-82.
[71] Tufo B, Jimma A, Zeleke B. Demonstration and participatory evaluation of improved beehives and cooperative and market linkage formation in dawro zone southern ethiopia. J Fisheries Livest Prod 2017; 5(3): 1-5.
[72] Gezahegne T. Apiculture in Ethiopian. Agriculture Third ApiExpo Africa 2012. 26th - 29th September 2012 Addis Ababa, Ethiopia.
[73] Zekiros F, Gangwar SK. Assessment of honey production on different agro- ecology in Woreda Tahtay-Koraro North Western of Tigray, Ethiopia. Int J Sci Nature 2017; 8(4): 765-9.
[74] Teferi K. Status of Beekeeping in Ethiopia- A Review. J Dairy Vet Sci 2018; 8(4): 1-12.
[75] Agrawal TJ. Beekeeping Industry in India: Future Potential. Int J Res Appl Natu Soci Sci 2014; 2(7): 133-40.
[76] Dicks LV, Abrahams J, Atkinson J, et al. Identifying key knowledge needs for evidence-based conservation of wild insect pollinators: A collaborative cross-sectoral exercise. Insect Conserv Divers 2013; 6(3): 435-46.
[77] Ollerton J. Pollinator diversity: Distribution, ecological function, and conservation. Annu Rev Ecol Evol Syst 2017; 48: 353-76.
[78] Sutter L, Jeanneret P, Bartual AM, Bocci G, Albrecht M. Enhancing plant diversity in agricultural landscapes promotes both rare bees and dominant crop-pollinating bees through complementary increase in key floral resources 2017.
[79] Sebeho HK. Production and Quality Characteristics of Ethiopian Honey: A Review. Academic J Entomol 2015; 8(4): 168-73.
[80] Gidey Y, Bethelhem K, Dawit K, Alem M. Assessment of beekeeping practices in Asgede Tsimbla district, Northern Ethiopia: Absconding, bee forage and bee pests. Afr J Agric Res 2012; 7(1): 1-5.
[81] Haftom G, Zelealem T, Girmay M, Awet E. Seasonal honeybee forage availability, swarming, absconding and honey harvesting in Debrekidan and Begasheka Watersheds of Tigray, Northern Ethiopia. Livest Res Rural Dev 2013; 25(4). [http://www.lrrd.org/lrrd25/4/haft25061.htm].
[82] Food FAO. Food and Agriculture Organization: Livestock Primary 2017.
[83] Sahle H, Enbiyale G, Negash A, Neges T. Assessment of Honey Production System, Constraints and Opportunities in Ethiopia. Pharmacy and Pharmacology Int J 2018; 6(2): 2379-67.
[84] Seyoum E, Anja A. Assessment of beekeeping production system and constraints in basketo special woreda, Southern Ethiopia. Hortic Int J 2018; 2(3): 124-7.
[85] Daily GC. Nature’s Services: Societal Dependence on Natural Ecosystems 1997; 392.
[86] Palmer M, Bernhardt E, Chornesky E, et al. Ecology. Ecology for a crowded planet. Science 2004; 304(5675): 1251-2.
[87] Abrol DP. Plant-pollinator interactions in the context of climate change - an endangered mutualism. J Palynology 2009; 45(2): 1-25.
[88] Kerealem E, Tilahun G, Preston TR. Constraints and prospects for apiculture research and development in Amhara region, Ethiopia. Livest Res Rural Dev 2009; 21(172). [http://www.lrrd.org/lrrd21/10/ejig21172.htm].
[89] Mengistu ZM, Beyene JT. Beekeeping in Ethiopia, a case of agrochemical uses in west Gojjam Zone. Bee World 2014; 91(1): 8-11.
[90] Tessema A. Beekeeping, climate change and food security: the case of Eastern Amhara Region, Ethiopia. Livest Res Rural Dev 2017; 29(83). [http://www.lrrd.org/lrrd29/5/tess29083.html].
[91] Desalegn B. Assessment of pesticides use and its economic impact on the apiculture subsector in selected districts of Amhara region, Ethiopia. J Environ Anal Toxicol 2014; 5(3): 1-4.
[92] Melisie M, Damte T, Thakur KA. Farmers’ insecticide use practice and its effect on honeybees (Apis mellifera) foraging on onion flower in Adami Tullu district of Ethiopia. Glob J Pests Dis Crop Prot 2016; 4(1): 139-45. [http://www.globalscienceresearchjournals.org/].
[93] Melisie M, Damte T, Thakur KA. Effect of some insecticidal chemicals under laboratory condition on honey bees [Apismellifera L. (hymenoptera: Apidae)] that forage on onion flowers. Afr J Agric Res 2015; 10(11): 1295-300. [ https://doi.org/10.5897/AJAR2014.9277].
[94] Serda B, Zewudu T, Dereje M, Aman M. Beekeeping practices, production potential and challenges of bee keeping among beekeepers in haramaya district, eastern ethiopia. J Veterinar Sci Technol 2015; 6(5): 2-5.
[95] Tesfaye B, Begna D, Eshetu M. Beekeeping practices, trends and constraints in bale, south-eastern ethiopia. J Fisheries Livest Prod 2017; 5(1): 1-9.
[96] Tessema AA, Zeleke MZ. Study on the beekeeping situation, the level of beekeepers knowledge concerning local honeybee subspecies, their productive characteristics, and behavior in eastern amhara region, ethiopia. Advan Agri 2017. ID 6354250.