The APICULTURAL SOCIETY OF KOREA
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Current Issue

Journal of Apiculture - Vol. 39 , No. 1

[ Original research article ]
Journal of Apiculture - Vol. 38, No. 3, pp. 175-188
Abbreviation: J. Apic.
ISSN: 1225-0252 (Print)
Print publication date 30 Sep 2023
Received 21 Jul 2023 Revised 09 Aug 2023 Accepted 09 Aug 2023
DOI: https://doi.org/10.17519/apiculture.2023.09.38.3.175

A Review of Current Beekeeping Status in Uganda
Ogweng Geoffrey Ebuu1, 2 ; Peter Njukang Akongte1 ; MinOo Hlaing1 ; Daegeun Oh1 ; Minwoong Son1 ; Bo-sun Park1 ; Su-bae Kim1 ; You-young Jo1 ; Changhoon Lee1 ; Yong-Soo Choi1 ; Dongwon Kim1, *
1Department of Agricultural Biology National Institute of Agricultural Science, RDA, Wanju 55365, Republic of Korea
2Apac District Local Government, Ministry of Agriculture, Animal, Industry and Fisheries, Uganda

Correspondence to : * E-mail: dongwonkim@korea.kr

Funding Information ▼

Abstract

Beekeeping benefits agriculture across the globe due to the pollination services provided by honeybees. Therefore, the disappearance of honeybees may lead to the extinction of some important plant species. Most beekeepers in Uganda keep western honeybee (Apis mellifera) and are under the umbrella body called The Uganda National Apiculture Development Organization (TUNADO). TUNADO supports beekeepers with technology dissemination, bulking hives products, and ensures that the quality of hive products meets the specified standards of various markets. The beekeeping systems in Uganda comprise of traditional, transitional, and modern approaches, with 87% beekeepers practicing the traditional system. This preference for the traditional system is primarily due to its lower cost, the limited availability of materials for modern setups, and its ease of management. Uganda has the potentials for beekeeping due to its natural resources, the presence of wild colonies of honeybees, and government policies. Beekeeping has contributed to farmers’ livelihoods both economically and ecologically. However, they are faced with challenges of agrochemicals, low colonization rate and absconding, climate change, parasites, pests, diseases, and unskilled labor. Beekeepers are undertaking extensive education in colony management to overcome the challenges. It is strongly recommended that a training center for queen breeding/rearing should be established to foster honey research in the country.


Keywords: Apis mellifera, Beekeeping systems, Pollination, Pests, Breeding, Uganda

INTRODUCTION

Beekeeping is one of the farming systems that most living organisms depend on due to pollination services provided by honeybees. Honeybees pollinate most of the agricultural crops, fruit trees and many wild plants which are both beneficial to man and animals (Kasina et al., 2009; Mumoki et al., 2014; Hung et al., 2018; Kasangaki et al., 2018; Ogihara et al., 2020). They produce honey that is used by human as food, medicine, pharmaceuticals, confectionery, and in the bakery and cosmetic industries (Tarunika Jain, 2014). Honeybee products like bee venom (Babaei et al., 2016) and propolis are anti-inflammatories (Alanazi et al., 2020) that can help boost the body’s immunity. This may help in fighting other diseases in the body including the corona virus pandemic which hit the world (Onlen et al., 2007; Caramalho et al., 2015; Anjum et al., 2019; Alanazi et al., 2020). In another study, honey added to water (22 g/L ad libitum) boosts the production of antibodies against the avian influenza virus H9N2 (Lima et al., 2020). In Uganda, honeybees are used to protect game parks, national, and forest reserves. In 2014, Gemeda reported that in Ethiopia, conservationists use beekeeping in watershed management including protected areas and for income generation (Gemeda, 2014).

The disappearance of honeybees would result in the loss of some plant species, crops, and potential ecosystems. According to Kasangaki et al. (2018), the common honeybee species reared in Uganda is western honeybee (Apis mellifera) with three different races (A. mellifera mellifera, A. mellifera scutellate and A. mellifera adansonii). A. mellifera adansonii are smaller in size, defensive, resistant to diseases and pests and are more productive compared to other races of A. mellifera (Petreanu, 2001). A. mellifera is referred to as Africanized honeybees because of its defensive behavior for their products and territory against any intruders (human and animals), disease and pests (Nouvian et al., 2016; Van Alphen et al., 2020; Düttmann et al., 2022). An understanding of the distribution of honeybee species is important in increasing our odds of successfully protecting such a critical player in most ecosystems. It also offers a source of employment to both elderly and youths, educated and uneducated (Makri et al., 2015).

To reduce the rural poverty in households, farming practices in both small and medium farmers need to be improved by embracing pollinators (Amulen et al., 2019). Improved technological practices in beekeeping being promoted in Uganda include modern hives, use of protective gears, smokers (Fig. 2A), honey processing, and packaging equipment (Tulu et al., 2020) (Fig. 1).


Fig. 1.  
Value addition chain in honeybee products processing A. Automatic honey packaging machine, B. Packed honey ready for supply/marketing, C. Various Value added on bee products and D. Ugandan Honey exhibition in Dubai 2022. Sponsored by TUNADO.

Uganda is endowed with natural resources that help boost the potential of beekeeping industry due to the presence of evergreen vegetation, national reserves protected by the government and several plantations (Kasangaki et al., 2015). The abundant resources provide ambient environmental conditions including forages for the honeybees and subsequently, increased production and productivity (Otim et al., 2019). Most of the beekeepers installed their hives in different forests away from farmland and only wait for the harvesting season. approximately (75%) of beekeepers depends on natural honeybee swarms to colonize their hives (Chemurot et al., 2017). However, it has not limited the production of honey and other hive products for which there are enormous potential markets. This is because honeybees are less affected by pathogenic micro-organisms (Masuku, 2013) and as a result, they produce a greater quantity of hive products that are beneficial to humans.

The beekeeping industry in Uganda was dominated by male (Fig. 2B) simply because in most African cultures, climbing trees by women was considered a taboo (UNECE, 2023) and yet hives were sited high on trees that require one to climb and harvest the products (Chemurot, 2011). Due to continuous education of women about the importance of beekeeping in households, there is an increase in the number of women participating in the development of the sector (Fig. 2A). This is due to the holistic approach in addressing rural poverty which involves promoting women’s participation in the agricultural production process.


Fig. 2.  
A. Training female beekeepers on lighting smoker and apiary management, B. Training beekeepers on how to make smoker using locally available materials. Sponserd by TUNADO.

Beekeepers have formed themselves an umbrella body (Uganda National Apiculture Development Organization (TUNADO)) that deals with the welfare of beekeepers in the country. The organization started as a small association “Uganda honey beekeepers association (UHBA)” in 1995 (Petreanu, 2001) which was later transformed into TUNADO in 2009. Under the supervision of the Ministry of Agriculture, Animal Industry and Fisheries (MAAIF), TUNADO supports beekeepers with technology dissemination, bulking of hives products, and ensures that the quality of hive products meets the specified standards of various markets. The purpose of this review is to document the various beekeeping systems and beehive practices in Uganda, outlined challenges and give recommendations for action aiming at taking the industry to the next level.

1. Location and population of Uganda

Uganda is one of the smallest landlocked Country in East Africa. It is located at the line of zero-degree equator and bordered to the East by Kenya, to the West by Democratic Republic of Congo, to the South by Tanzania and Rwanda, and to the North by South Sudan (Fig. 3).


Fig. 3.  
Map of Uganda showing location in Africa. Source; google.

The country has Ten agro-ecological regions that include North-western savannah grasslands, North-eastern savannah grasslands, North-eastern dry lands, Southwestern farmlands, Pastoral rangelands, West savannah grasslands, Para savannah, Highland ranges, Lake Victoria crescent, and Kiyoga plains (MAAIF, 2018). All these agro-ecological zones share the two seasonal rainfalls with variations in the amount of rain received, soil types, agricultural systems, and terrain (Wortmann and Eledu, 1999).

Uganda has a total population of forty-seven million, two hundred and sixty-five thousand and forty-one (47,265,041), which is made up of males (49.1%) and females (50.9%) (UNBS, 2022) (Fig. 4).


Fig. 4.  
Total regional distribution of population in Uganda. Source UNBS 2022.

2. Bee forage plants

Uganda presents enormous potentials for beekeeping industry because of its natural resources that provides excellent forage and ambient climate for the honeybee colonies. The common bee forage plants in Uganda are; Coffee (Coffee arabica and Coffee rubasta), Combererirum (Combererirum spp), Calliandra (Calliandra calothyrsus), Albizia (Albizia spp), mango (Mangifera indica), Acacia (Acacia spp), Banana (Musa spp), Shea nut tree (Vitellaria paradoxa), including food and cash crops grown in open farm lands namely; maize (Zea mays), peas (Pisum sativum), sorghum (Sorghum bicolor), vegetables, cotton (Gossypium spp), sugar cane (Saccharum officinarum), and beans (Phaseolus vulgaris) (Otim et al., 2019) (Table 1).

Table 1. 
Common bee forage plants across all regions of Uganda
Common name Scientific name Plant form
Nile tolip Markhamia lutea Tree
Lantana Lantana camara, Shrub
Aleovera Aloe vera Herb
Grey bitter-apple Solanum incanum Herb
Camel's foot Bauhinia thonningii Tree
Coffee Coffee arabica Tree
Musase Albizia ferruginea Tree
Velvet bushwillow Combereritum molle Tree
Neem tree Azadirachta indica Tree
Albizia Albizia coriaria Tree
Calliandra Calliandra calothyrsus Tree
Phalsa or falsa Grewia mollis Shrub
Flamboyant Delonix regia Tree
Acacia Acacia polyacantha Tree
Large-leaved albizia Albizia grandibracteata Tree
Ficus Ficus natalensis Tree
Spider whisker Cleome gynandra Herb
Beef wood Bridelia micrantha Tree
Spike thorn Maytenus seneganalensis Tree/shrub
Adamant creeper Cissus quadrangularis Tree/shrub
Harrisonia Harrisonia abyssinica Shrub/tree
Tamarind Tamarindus indica Tree
Pigeon pen Cajanus cajan Shrub
Varriable bush-willow Combretum collinum Tree
Wild coffee Bridelia micrantha Tree
Flame tree Erythrina abyssinica Tree
Popcorn senna Cassia didymobotrya Tree
Lannea Lannea acida Shrub/tree
Bastard brandy bush Grewia bicolor Shrub
Acacia Acacia hockii Shrub
Eucalyptus Eucalyptus grandis Tree
Ocimum Ocimum tenuiflorum Herb
White berry-bush Flueggea virosa Shrub
Acacia Acacia brevispica Shrub
Black plums Vitex donianana Tree
Trema Tremas orientalis Tree
Bitter leaf Manihot esculenta Shrub
Coffee senna Cassia accidentalis Tree
Crotalaria Crotalaria cleomifalia Shrub
Bitter leaf Vernonia amygdalina Shrub
Red hot poker Erythrina abyssinica Tree
Mysore thorn Caesalpinia decapetala Shrub
Creeping foxglove Asystasia gangetica Herb
Mango Mangifera indica Tree
Bitter leaf Vernonia adoensis Shrub
Moringa Moringa oleifera Tree
Jacaranda Jacaranda mimosifolia Tree
African fan palm Borasus aethpicum Tree
Red thorn Acacia nilotica Shrub/tree

3. Honey production

In Uganda, due to the available natural resources providing bee forage plants, only few beekeepers (21%) provide supplementary feeds to the bees especially during dearth period. The bees depend entirely (79%) on natural food (nectar and pollen) for producing hive products (Kugonza and Nabakabya, 2008) which, therefore, increase the value of its natural honey in various markets. As a result, the supply of honey in Uganda became low and could not meet the rapidly expanding market demands both domestically and regionally. Majority of beekeepers trade their honey informally in the local markets and across borders within East African countries. Baseline survey conducted by Kimani (2021), showed that the main honey producing areas in Uganda were the West Nile, Eastern, Northern, Western, Southern, and Central regions. There are lots of informal cross border trade of bee products between Uganda and its neighboring countries (Petreanu, 2001). The local and cross-border markets are fast growing and have less stringent requirements compared to Europe. This has made it exceedingly difficult to quantify and produce accurate data about the actual production of hive products produced by beekeepers. However, the production of honey in the country is estimated at 500,000 metric tons annually but the actual data collected showed that the production of honey amidst all the potential is far less than estimated (Table 2). This is due to the demands in both local and cross border business and poor culture of record keeping (TUNADO, 2022).

Table 2. 
Regional average honey production level in Uganda (TUNADO, 2022)
Regions 2017 2018 2019 2020 2021
Northern 17043 23129 17005 25294 28319
West Nile 15975 28204 23971 28197 30718
Central 6004 8586 11006 10432 9928
Western 9909 9101 11965 7224 11918
Eastern 19286 9839 14631 9829 6426
Southern 19086 11078 7805 8082 12010
Total 87303 74937 76383 59058 154319

4. Number of beekeepers

Beekeepers in Uganda have organized themselves into smaller groups in different villages, but the management of hives/apiaries is done individually. According to TUNADO (2021), the total number of beekeepers are one million two hundred and seventy thousand, five hundred and forty-four (1,270,544) with the total number of six million three hundred and fifty-two thousand seven hundred and twenty (6,352,720) beehives, 77% of which are colonized and 23% uncolonized in all the beehive types (local, transitional, and modern).


BEEKEEPING SYSTEMS

Beekeeping is the maintenance of honeybees in colonies together in the hives. It started about ten thousand years ago and dominated by men as they used to go for hunting of wild animals. Honeybee colonies were quite common in anthills, cavity of trees and clustering on tree branches in the forest (Roberts, 1969). This was before man invented the idea of beehives and bee rearing for both ecological and economic reasons.

1. Traditional beekeeping

The first system invented was the traditional system which is still in practice to date by most beekeepers in Uganda to keep and maintain honeybee colonies (Otim et al., 2019). An un-published annual report of the United Nation Development Program (UNDP) (2017), Uganda chapter estimated that there are about three million (3 m) hives in Uganda, 87% of which were traditional log hives with 76% colonization rate. Although the traditional beehives had the least reported yield in terms of production, they were the most used and owned types of hives by most beekeepers to date (Al-Ghamdi et al., 2017). This was attributed to their low cost, availability of construction materials within the locality, and little technical skills required in making and management of these hives (Amulen et al., 2019; ChiEmela et al., 2022).

In traditional beehives, the production of honey ranges between 20-25 kg annually during flowering and honey flow seasons (Shimelis, 2017). Traditional beehives are of different types invented based on regions which were divided along different ethnic groups and availability of construction materials within a particular locality. The common types were the palm tree, log, woven, bamboo tree, twigs smeared with cow dung and tree bark (Fig. 5). However traditional beekeeping is associated with many problems such as fixed space and combs, vulnerable to pests, colony cannot be divided, and easily affected by weather and it is difficult to check for queen’s performance and other colony management practices (Amulen et al., 2019; ChiEmela et al., 2022).


Fig. 5.  
A. Beekeepers training on making local hivesfrom Bamboo tree ans B. Beekeeper smearing local hives made of twigs with cow dung. Sponsored by TUNADO.

2. Transitional beekeeping

Transitional beekeeping is the second most popular system commonly practiced. Top bar hives like Kenya Top-Bar hives (KTB) and Tanzania top-bars are used (Roberts, 1971). Adjare (1990), Amulen et al. (2019), and Abro et al. (2022) suggested that the early and serious beekeepers were not for the poor and for this reason, most African countries were capable of adopting beekeeping technologies only up to this level as would represents there satisfactory compromise. KTB hives (Fig. 6) were mostly used because they are less costly to manage in terms of skills and easy to construct as opposed to modern Langstroth hives. Also, Abro et al. (2022) reported that transitional hives yield more honey (50 kg or above) annually compared to the traditional hives.


Fig. 6.  
A. transitional hives sited in the forest and B. Demonstration on the best way to handle transitional hives to Beekeepers. Sponsored by Makerere University in Uganda.

3. Modern beekeeping

The fact that modern beekeeping (Langstroth hives) is environmentally friendly and easy to manage, produces more honey (Al-Ghamdi et al., 2017) which diversifies the farmers’ income (Amulen et al., 2019), the rate of adoption has remained exceptionally low (Amulen et al., 2019; Kaudjhis et al., 2020). Low adoption of Langstroth hive (Fig. 7) was attributed to high cost of production and management skills (Kaudjhis et al., 2020; Tulu et al., 2020; Mulatu et al., 2021).


Fig. 7.  
A. modern hives (Langstroth) installed in beehouse and B. demonstrating how to work with Langstroth hives. Sponsored by Makerere University.


OPPORTUNITIES OF BEEKEEPERS

Among all challenges faced by beekeepers in Uganda, they have lots of opportunities such as government policies which include recruitment of entomologists in all the districts of Uganda to carry on beekeeping activities, the Uganda National Bureau of Statistics (UNBS) that design, regulate and ensure quality and standard of honeybee products and equipment. Also, beekeepers benefit from apiculture policy and other environmentally related policies like National Environment Management Authority (NEMA), National Forestry Authority (NFA), and the Uganda Wildlife Authority (UWA) (UWA, 2019). These policies have given leeway for beekeepers to access and install their hives in such protected areas.


CONTRIBUTIONS OF THE BEEKEEPING INDUSTRY
1. Ecological contributions
1) Pollination

Honeybees are considered the best insect pollinators (Breeze et al., 2011) and play a vital role in the economy of Uganda. This has led to increase in agricultural production and productivity while reducing food insecurity (Hanley et al., 2015; Aryal et al., 2020). For instance, honeybees were regarded as the main pollinators of coffee plants because farmers experienced an increase in coffee production when colonies were placed in coffee farms (UCDA, 2023). Uganda is ranked seventh globally in coffee production and export countries, second in Africa after Ethiopia and first in East Africa (UCDA, 2023). It has also improved the household income of Ugandan and the country’s gross domestic products (GDP) by 1.5% (UNBS, 2022) in 2021/2022 financial year (Table 3).

Table 3. 
Variation in coffee production versus export value in the economy (UCDA, 2023)
Year Quantity of coffee (KG) Growth rate (%) Value exported ($)
2021 374760 4 303555.6
2020 360103 15 291683.4
2019 313933 10 108485.7
2018 284225 -6 230222.25
2017 302063 24 244671.03
2016 243061 6 196879.41
Total 1878145 53 1375497.39

Honeybee carryout cross pollination thus reducing the chances of inbreeding depression, causing reduction in genetic diversity which could results into negative traits in the population (Partap, 2011). However, the untapped opportunity by beekeepers in Uganda is the sale or hire of honeybee colonies for pollination services to commercial farmers. This could be linked to the abundance of wild colonies which are able to carry out pollination at a wider range. However, this would help improve livelihood of the beekeepers by providing a source of income (Garratt et al., 2014; Hanley et al., 2015; Picanço et al., 2017).

2) Conservation of the environment

Honeybees are an integral part of the intricate web of life that exists in fields and pastureland. They interact with many organisms like birds, bats, and other insects in performing their cardinal role of pollination. Beekeeping practices play a vital role in environmental conservation. Beekeepers through collaborative forest management (CFM) initiated by government agencies such as NFA and UWA, participate communally in protecting gazetted areas (Mackenzie et al., 2012). The purpose of beekeepers’ engagement was to reduce the number of timber dealers, poachers and charcoal activities in protected forests/games of Uganda thus supporting the ecosystems (Petreanu, 2001; Otim et al., 2019).

2. Economical contribution
1) Income generation

Beekeeping provides farmers with both direct and indirect capital. Beekeepers earn money directly from the sales of products harvested from the beehives crudely or processed, purified, and packaged. Statistics shows that there are 1.2 million beekeepers in Uganda and the confirmed quantity of honey produced is 316,940 metric tonnes and a kilogram of honey cost $5.5 in local markets. The common products sold includes honey, propolis, beeswax, and bee venom (Amulen et al., 2019). Youths earn their living from beekeeping by making Langstroth beehives which cost $70, KTB hives at $50, local hives $10 each and sale of other beekeeping equipment (Drost et al., 2014). However, the sale of colonies of raised queen with desirable traits (Vinícius-Silva et al., 2017; Patel et al., 2021) and medicinal products of honeybees (Hegazi, 2012) are still unexploited by most beekeepers in the country.

2) Medicines (Apitherapy)

Honeybees are social insects that produce honey and other hive products used as medicines by consuming the products directly or used in pharmaceutical industries. All the hive products are believed to have medicinal values (apitherapy) because of the several plants visited by bees (Zekarias et al., 2020). The common products include; honey, propolis, beeswax, royal jelly, pollen and bee venom (Akullu and Mwesigwa, 2021).

Honey is a natural sweetener collected by bees from the nectar of plants’ blossom or other sweet substances, stored and left to ripe in the comb’s cells. As a dietary supplement, honey can treat gastric ulcers and due to its anti-bactericidal activities, it can act against enteropathogenic organisms such as Salmonella, shigella and E. coli (Petreanu, 1979; Cortés et al., 2011; Roberts et al., 2015; Matzen et al., 2018) also treat cold and mouth, throat or bronchial irritations and infections (Emsen, 2007). Honey is non-irritative, non-toxic, self-sterile and has anti-bactericidal properties and its nutritive abilities used for treating septic wounds in its raw state (Armon, 1980). In addition, honey also contains twenty-two amino acids (Adebiyi et al., 2004) and the variation in the quantity depends on the source of pollen and nectar collected (Ogwal et al., 2021). Propolis have shown positive results in the control of fungal, bacterial, viruses and other microorganisms due to its antimicrobial properties (Zekarias et al., 2020).


CHALLENGES FACED BY BEEKEEPERS
1. Agrochemical application

Honeybees just like any other insects, are vulnerable to chemicals or pollutions from the environment (Amulen et al., 2017). Commercial farmers in Uganda (85%) spray their crops, fruit trees and domestic animals against several pests and fungal infections using different chemicals in attempt to reduce the level of damage with little or no consideration to pollinators (honeybees). Application of these chemicals are on the rise with increase in human population, and commercialization of agricultural products. A study conducted by Amulen et al. (2019) revealed the presence of minute traces of chemical residues in honey and beeswax. These chemicals, when taken by honeybees, lower their body immunity, strength to collect food, and resistance to pests and disease in the colony. It is estimated that over 40% of the global honeybee species are declining by more than a third (DeGrandi-Hoffman et al., 2013; Fikadu, 2020) due to the use of different chemicals in the environment.

2. Low colonization and absconding of colonies

In Uganda, beekeepers pay very little attention to the factors leading to colonization such as hive hygiene, baiting, and planting forages because there are lots of wild trees providing forages (Chemurot, 2011; Otim et al., 2019). It is important for beekeepers to understand where and when to install the hives (swarming period). However, due to inadequate knowledge about colony management, many hives were sited and abandoned in the forests. This is because they believed that there were many swarm colonies in the wild to colonize the hives in the forests. It was also proven that colonization is high when hives were sited high on trees than workable heights (Acai and Okullo, 2010). Therefore, many beekeepers were unable to climb the tree since it is a taboo for women in some cultures in Uganda. The commonly used baits included beeswax, propolis, Ocimum, lemon grass, honey, and smearing local hives with cow dung (Ande et al., 2008; Acai and Okullo, 2010).

Absconding is when honeybees abandon the hive and move to another location leaving uncapped and or capped brood and pollen in the hive. This could be attributed to inadequate forage plants within the vicinity, deforestation, pests, disease, predators, leaking hives or other human activities in the environment (Masuku, 2013; Kasangaki et al., 2015; Kajobe et al., 2016), and poor colony management (Amulen et al., 2019; Njukang et al., 2021).

3. Climate changes

Human activities on the environment such as cutting of trees for poles, timbers and curing bricks has led to deforestation which is depriving honeybees from suitable habitats and forages (Forneri et al., 2006; Aggrey et al., 2010) and because of these, colonies of honeybees are seen colonizing ceiling board of houses occupied by human being. A similar study was conducted in Nigeria by Mustafa et al. (2015) where man was labeled as the worst enemy to honeybees and its environment. Abnormal changes in air, shift in temperatures, increased frequency and intensity of droughts have contributed to the high mortality of honeybees. A situation that has progressively reduced the population of honeybees over time and pollination services hence reducing agricultural production and productivity. This is because there were no bloom and flower synchrony, some plants were able to emerge earlier than the normal time (Kimani, 2021). The effects have led to direct influence in the behavioral and physiological characteristics of honeybees and floral environment (Büchler et al., 2014).

The fall in the population of worker bees reduces the yield of agricultural crops and other wild plants, thus resulting in food insecurity. This has also affected the ecological functioning of honeybees in their ecosystems (Safe et al., 2020; Rahimi et al., 2021). In some instances, the beekeepers have abandoned their hives as it was recorded in Benin (Paraïso et al., 2012). The change may also favor the growth of honeybee pathogens with haplotypes of varying virulent on different honeybee populations leading to absconding (Reddy et al., 2012). The effect of climate change is a global problem. In Uganda, there are two rainy seasons and ten agro-ecological zones with varied weather. This causes prolonged drought, rise in temperature, floods, and wildfires (Josephat, 2018) which are a threat to beekeeping environments and survival. It has affected the seasonal pollination services, bee habitats, foraging cycle (Reddy et al., 2012; Kalanzi et al., 2015) because of short season or no flowers, and compromising their body immunity leading to high mortality rate (Markandya et al., 2015).

4. Pests, diseases, and predators

Common honeybee pests, parasites and diseases of economic importance to beekeepers includes; Little black ants (Monomorium minimum), small hive beetles (Aethina tumida), Greater wax moths (Galleria mellonella) (Fig. 8), Oriental hornrts (Vespa orientalis), black rats (Rattus rattus), Honey badger (Mellivora capensis), Birds (Indicator indicator) and varroa mites (Varroa destructor) (Kajobe et al., 2016; Chemurot, 2017). V. destructor and black queen cell virus (BQCV) were first detected by Kajobe et al. (2010) while studying the viral infection of honeybees and later deformed wing virus (DWV) and American foul brood (AFB) disease (Chemurot et al., 2016), Nosema, chronic bee paralysis virus (CBPV), acute bee paralysis virus (ABPV) and Sacbrood virus (SBV) were also confirmed in Uganda by Otim et al. (2020). Apart from the known species of Nosema (Nosema apis and Nosema ceranae), Otim et al. (2020) also identified a new species of Nosema (N. neumanni). However, the fact about its effect is not yet known though it seems less virulent than N. ceranae and N. apis (Stainton, 2018).


Fig. 8.  
Common honeybee pests and parasite in Uganda A. Greater wax moths (Galleria mellonella), B. Small black ants (Monomorium minimum), C. Small hive beetles (Aethina tumida), and D. Varroa mites (Varroa destructor),

5. Unskilled beekeepers

Burning of bushes, use of direct fire instead of smoker for hive inspection and harvesting of hive products, and poor handling colonies are some of human activities which are problematic to beekeeping as a result of poor skills (Amulen et al., 2017).


CONCLUSION AND RECOMMENDATIONS

The environmental conditions of Uganda coupled with its many agro-ecological zones have promoted beekeeping in the country. This activity has provided a source of income to both the youth and elderly people through the sale of hive products and equipment. Thus, reducing unemployment rate and crime wave in some localities. Beekeeping in Uganda is motivated by the government, TUNADO and other non-governmental organizations. However, beekeepers are still being faced with many challenges including poor colony management, pests and diseases, climate, the use of agrochemicals, and high cost of beekeeping equipment. Honey production and quality is influenced by different beekeeping systems and practices, irrespective of these challenges, Uganda still have high potentials of producing quality honey in the continent if proper measures are taken to addressed some of the challenges.

Some of the strategic measures include collaboration between MAAIF and the ministry of water and environment to do environmental education and protection against deforestation, agrochemicals, bush fires, and pollution. This would help protect pollinators from getting exposed to toxic environments and reduce the mortality rate of honeybees.

MAAIF should build the capacity of entomologists across the country with technical skills in colony multiplication to address the problem of low colonization and production of honeybee products.

Research as a guiding tool for development should be embraced and funded so gaps are identified and addressed.


Acknowledgments

This study is part of the “2023 Korean-Africa Food and Agriculture Cooperation Initiative (KAFACI) Long-term Training Program” of Rural Development Administration (RDA), Republic of Korea.

I am grateful to the KAFACI Secretariat and RDA for the financial support. Department of Agricultural Biology, National Institute of Agricultural Science (Division of Apiculture) for all the guidance given in different forms. I also thank the government of Uganda through the Department of Entomology at the MAAIF and Apac District Local Government for granting me permission to attend this training. Lastly, I thank Mr. Kagenda Gabriel A, Ebuu Martin Odwong, and Acola Judith for their input in writing this paper.


References
1. Adebiyi, F. M., I. A. Akpan, E. I. Obiajunwa and H. B. Olaniyi. 2004. Chemical/Physical Characterization of Nigerian Honey. Pak. J. Nutr. 3(5): 278-281.
2. Abro, Z., M. Kassie, H. A. Tiku, B. Taye, Z. A. Ayele and W. Ayalew. 2022. The impact of beekeeping on household income: Evidence from north-western Ethiopia. Heliyon 8 (5): e09492.
3. Acai, J. and P. Okullo. 2010. Effects of apiary management on colonization and colony performance of African honeybee (Apis mellifera) in the North-Western Agro-ecological zone of Uganda. Livest. Res. Rural Dev. 22(5).
4. Adjare, S. O. 1990. Beekeeping in Africa (No. 68/6). FAO.
5. Aggrey, N., S. Wambugu, J. Karugia and E. Wanga. 2010. An Investigation of the Poverty - Environmental Degradation Nexus: A Case Study of Katonga Basin in Uganda. R. J. Environ. & Earth Sci. 2(2).
6. Akullu, P. S. and D. Mwesigwa. 2021. Embracing bee-keeping technology to enhance smart farming: Evidence from Lira city, mid-north Uganda. 9 (2).
7. Alanazi, S., N. Alenzi, J. Fearnley, W. Harnett and D. G. Watson. 2020. Temperate Propolis has Anti-inflammatory Effects and is a Potent Inhibitor of Nitric Oxide Formation in Macrophages. Metabolites 10(10): 413.
8. Al-Ghamdi, A. A., N. Adgaba, A. H. Herab and M. J. Ansari, 2017. Comparative analysis of profitability of honey production using traditional and box hives. Saudi J. Biol. Sci. 24(5): 1075.
9. Amulen, D. R., M. D’Haese, E. Ahikiriza, J. G. Agea, F. J. Jacobs, D. C. De Graaf, G. Smagghe and P. Cross. 2017. The buzz about bees and poverty alleviation: Identifying drivers and barriers of beekeeping in sub-Saharan Africa. PLoS One 12(2): e0172820.
10. Amulen, D. R., M. D’Haese, E. D’Haene, J. Okwee Acai, J. G. Agea, G. Smagghe and P. Cross. 2019. Estimating the potential of beekeeping to alleviate household poverty in rural Uganda. PLoS One 14(3): e0214113.
11. Amulen, D. R., P. Spanoghe, M. Houbraken, A. Tamale, D. C. De Graaf, P. Cross and G. Smagghe. 2017. Environmental contaminants of honeybee products in Uganda detected using LC-MS/MS and GC-ECD. PLoS One 12(6): e0178546.
12. Ande, A. T., A. A. Oyerinde and M. N. Jibril. 2008. Comparative Study of the Efficacy of Six Different Baiting Materials on Bee Colony Performance in Traditional and Modern Hives. Adv. Biol. Res. 2(1-2): 13-16.
13. Anjum, S. I., A. Ullah, K. A. Khan, M. Attaullah, H. Khan, H. Ali, M. A. Bashir, M. Tahir, M. J. Ansari, H. A. Ghramh, N. Adgaba and C. K. Dash. 2019. Composition and functional properties of propolis (bee glue): A review. Saudi J. Biol. Sci. 26(7): 1695-1703.
14. Armon, P. J. 1980. The Use of Honey in the Treatment of Infected Wounds. Trop. Dr. 10(2): 91-91.
15. Aryal, S., S. Ghosh and C. Jung. 2020. Ecosystem Services of Honeybees; Regulating, Provisioning and Cultural Functions. J. Apic. 35(2): 119-128.
16. Babaei, S., S. Rahimi, M. A. Karimi Torshizi, G. Tahmasebi and S. N. Khaleghi Miran. 2016. Effects of propolis, royal jelly, honey and bee pollen on growth performance and immune system of Japanese quails. Vet. Res. Forum 7(1): 13-20.
17. Breeze, T. D., A. P. Bailey, K. G. Balcombe and S. G. Potts, 2011. Pollination services in the UK: How important are honeybees? Agric. Ecosyst. Environ. 142 (3-4), 137-143.
18. Büchler, R., C. Costa, F. Hatjina, S. Andonov, M. D. Meixner, Y. L. Conte and J. Wilde. 2014. The influence of genetic origin and its interaction with environmental effects on the survival of Apis mellifera L. colonies in Europe. J. Apic. Res. 53(2): 205-214.
19. Caramalho, I., A. Melo, E. Pedro, M. M. P. Barbosa, R. M. M. Victorino, M. C. Pereira Santos and A. E. Sousa. 2015. Bee venom enhances the differentiation of human regulatory T cells. Allergy: Eur. J. Allergy Clin. Immunol. 70(10): 1340-1345.
20. Chemurot, M. 2011. Beekeeping In Adjumani District, Uganda. Bee World 88 (3): 58-61.
21. Chemurot, M. 2017. The distribution, infestation levels and effects of honeybee parasites and pathogens on colony performance in two agro-ecological zones of Uganda. Ghent University (Doctoral dissertation, Ghent University).
22. Chemurot, M., M. Brunain, A. M. Akol, T. Descamps and D. C. De Graaf. 2016. First detection of Paenibacillus larvae the causative agent of American Foulbrood in a Ugandan honeybee colony. SpringerPlus 5(1): 1090.
23. Chemurot, M., L. De Smet, M. Brunain, R. De Rycke and D. C. de Graaf. 2017. Nosema neumanni n. sp. (Microsporidia, Nosematidae), a new microsporidian parasite of honeybees, Apis mellifera in Uganda. Eur. J. Protistol. 61: 13-19.
24. ChiEmela, C., R. MukaiLa, I. Ukwuaba and A. Obetta. 2022. Economics analysis of the use of modern and traditional methods in honey production among farmers in Enugu State Nigeria. Ege Üniv. Ziraat Fak. Derg. 59(4): 611-619.
25. Cortés, M. E., P. Vigil and G. Montenegro. 2011. The medicinal value of honey: A review on its benefits to human health, with a special focus on its effects on glycemic regulation. Cienc. Investig. Agrar. 38(2): 303-317.
26. DeGrandi-Hoffman, G., Y. Chen and R. Simonds. 2013. The Effects of Pesticides on Queen Rearing and Virus Titers in Honeybees (A. mellifera L.). Insects 4(1): 71-89.
27. Drost, S., J. van Wijk and D. de Boer. 2014. Including conflict-affected youth in agri-food chains: Agribusiness in northern Uganda. Confl. Secur. Dev. 14(2): 125-150.
28. Düttmann, C., B. Flores, J. Sheleby-Elías, G. Castillo, D. Rodriguez, M. Maggi and J. Demedio. 2022. Africanized honeybee population (A. mellifera L.) in Nicaragua: Forewing length and mitotype lineages. PLoS One 17(4): e0267600.
29. Emsen, I. M. 2007. A different and safe method of split thickness skin graft fixation: Medical honey application. Burns 33(6): 782-787.
30. Fikadu, Z. 2020. Pesticides use, practice and its effect on honeybee in Ethiopia: A review. Int. J. Trop. Insect Sci. 40(3): 473-481.
31. Forneri, C., J. Blaser, F. Jotzo and C. Robledo. 2006. Keeping the forest for the climate’s sake: Avoiding deforestation in developing countries under the UNFCCC. Clim. Policy 6(3): 275-294.
32. Garratt, M. P. D., T. D. Breeze, N. Jenner, C. Polce, J. C. Biesmeijer and S. G. Potts. 2014. Avoiding a bad apple: Insect pollination enhances fruit quality and economic value. Agric. Ecosyst. Environ. 184: 34-40.
33. Gemeda, T. K. 2014. Integrating improved beekeeping as economic incentive to community watershed management: The case of sasiga and Sagure districts in Oromiya region, Ethiopia. AFF 3(1): 52-57.
34. Hanley, N., T. D. Breeze, C. Ellis and D. Goulson. 2015. Measuring the economic value of pollination services: Principles, evidence, and knowledge gaps. Ecosyst. Serv. 14: 124-132.
35. Hegazi, A. G. 2012. Medical importance of bee products. Uludağ Arıcılık Dergisi 12(4): 136-146.
36. Hung, K.-L. J., J. M. Kingston, M. Albretch, D. A. Holway and J. R. Kohn. 2018. The worldwide importance of honeybees as pollinators in natural habitats. Proc. Roy. Soc. B: Biol. Sci. 285(1870): 2017240.
37. Josephat, M. 2018. Deforestation in Uganda: Population increase, forests loss and climate change. Environ. Risk Assess. Remediat. 2(2): 46-50.
38. Kalanz, F., S. Nanseereko, J. Buyinja, P. Kiwuso and G. Niyibizi. 2015. Socio-economic analysis of beekeeping enterprise in communities adjacent to Kalinzu forest, Western Uganda. Int. J. Land-use Sustainability 2(1): 81-90.
39. Kajobe, R., E. K. Kato, A. Otim, P. Kasangaki and P. Abila. 2016. The status of Honeybee pests in Uganda. Bulletin of Animal Health and Production in Africa. Bull. Anim. Health Prod. Afr. 64(1): 105-117.
40. Kajobe, R., G. Marris, G. Budge, L. Laurenson, G. Cordoni, B. Jones, S. Wilkins, A. G. S. Cuthbertson and M. A. Brown. 2010. First molecular detection of a viral pathogen in Ugandan honeybees. J. Invertebr. Pathol. 104(2): 153-156.
41. Kasangaki, P., A. Sarah Otim, P. P’Odyek Abila, C. Angiro, M. Chemurot and R. Kajobe. 2015. The presence of varroa in Uganda and knowledge about it by the beekeeping industry. J. Apic. Res. 54(4): 373-377.
42. Kasangaki, P., G. Nyamasyo, P. Ndegwa and R. Kajobe. 2018. Assessment of Honeybee Colony Performance in the Agro-Ecological Zones of Uganda. CIACR 1(5): 1-6.
43. Kasina, J. M., J. Mburu, M. Kraemer and K. Holm-Mueller. 2009. Economic Benefit of Crop Pollination by Bees: A Case of Kakamega Small-Holder Farming in Western Kenya. J. Econ. Entomol. 102(2): 467-473.
44. Kaudjhis Assi, C., G. Eric-Kevin, B. Soumaïla and S. Nguessan Koffi. 2020. Traditional and modern beekeeping practices in the center of Côte dIvoire: The case of the western part of Yamoussoukro. IJSRP 10(11): 347-357.
45. Kimani, J. 2021. Effect of Climate Change on Bee Farming. A Critical Review of Literature. International Journal of Climatic Studies 1(1): 65-73.
46. Kugonza, D. R. and D. Nabakabya. 2008. Honey quality as affected by handling, processing, and marketing channels in Uganda. Tropicultura 26(2): 113-118.
47. Lima, W. G., J. C. M. Brito and W. S. da Cruz Nizer. 2020. Bee products as a source of promising therapeutic and chemoprophylaxis strategies against COVID-19 (SARS-CoV-2). Phytother. Res. 35(2): 743-750.
48. Mackenzie, C. A., C. A. Chapman and R. Sengupta. 2012. Spatial patterns of illegal resource extraction in Kibale National Park, Uganda. Environ. Conserv. 39(1): 38-50.
49. Makri, P., P. Papanagiotou and E. Papanagiotou. 2015. Efficiency and economic analysis of Greek beekeeping farms. Bul. J. Agric. Sci. 21(3): 479-484.
50. Markandya, A., C. Cabot-Venton and O. Beucher. 2015. Economic assessment of the impacts of the climate change in Uganda: Key results. Climate change department, Ministry of Water and Environment, Uganda 110 pp.
51. Masuku, B. 2013. Socioeconomic analysis of beekeeping in Swaziland: A case study of the Manzini Region, Swaziland. J. Dev. Agric. Econ. 5(6): 236-241.
52. Matzen, R. D., J. Zinck Leth-Espensen, T. Jansson, D. S. Nielsen, M. N. Lund and S. Matzen. 2018. The Antibacterial Effect In Vitro of Honey Derived from Various Danish Flora. Dermatol. Res. Pract. 2018: 1-10.
53. Ministry of Agriculture, Animal, Industry and Fisheries (MAAIF). 2018. National adaption plan for the Agricultural Sector; National-Adaptation-Plan-for-the-Agriculture-Sector.pd.
54. Mulatu, A., S. Marisennayya and E. Bojago. 2021. Adoption of Modern Hive Beekeeping Technology: The Case of Kacha-Birra Woreda, Kembata Tembaro Zone, Southern Ethiopia. Adv. Agric. 2021: 4714020.
55. Mumoki, F. N., A. Fombong, E. Muli, A. W. T. Muigai and D. Masiga. 2014. An Inventory of Documented Diseases of African Honeybees. Afr. Entomol. 22(3): 473-487.
56. Mustafa, M. O., O. T. Adeoye, F. I. Abdulalzeez and O. D. Akinyemi. 2015. Mitigating Effects of Climate Change and Deforestation on Bees with Respect to Their Ecology and Biology. J. Environ. Ecol. 6(2): 1.
57. Njukang, A. P., D. Kim, E.-J. Kang, H.-G. Park and Y.-S. Choi. 2021. Status of Honeybee (A. mellifera L.) Industry in Cameroon: A Review Article. J. Apic. 36(1): 1-10.
58. Nouvian, M., J. Reinhard and M. Giurfa. 2016. The defensive response of the honeybee A. mellifera. J. Exp. Biol. 219(22): 3505-3517.
59. Ogihara, M. H., M. Yoshiyama, N. Morimoto and K. Kimura. 2020. Dominant honeybee colony infestation by Varroa destructor (Acari: Varroidae) K haplotype in Japan. Appl. Entomol. Zool. 55(2)
60. Ogwal, A., K. K. Toitole, V. Medeyi, E. Nkonge and H. Ariaka. 2021. Telemedicine Clinic Reviews as an Alternative to Traditional Postoperative Clinic Visits: Sub-Saharan Africa Dilemma. Int. J. Surg. Res. Pract. 8: 132.
61. Onlen, Y., N. Duran, E. Atik, L. Savas, E. Altug, S. Yakan and O. Aslantas. 2007. Antibacterial activity of propolis against MRSA and synergism with topical mupirocin. J.Altern. Complement. Med. 13(7): 713-718.
62. Otim, A. S., R. Kajobe, P. P. Abila, P. Kasangaki and R. Echodu. 2019. Important Plants for Honey Production in Four Agro Ecological Zones of Uganda. Bee World 96(3): 81-86.
63. Otim, A. S., R. Kajobe, P. P. Abila, P. Kasangaki and R. Echodu. 2020. Viruses Circulating in African Honeybees in Uganda. Bee World 97(1): 21-25.
64. Paraïso, A. A., A. Sossou, D. Iz-Haquou, R. Nérice and A. Sanni. 2012. Perceptions and Adaptations of Beekeepers and Honey Hunters to Climate Change: The case of the Communes of Natitingou and Tanguieta in Northwest of Benin. Afr. Crop Sci. J. 20(s2): 523-532.
65. Partap, U. 2011. The Pollination Role of Honeybees. pp. 227-255. in Honeybees of Asia, eds. by Hepburn, H. R. and S. E. Radloff. Springer Berlin Heidelberg.
66. Patel, V., N. Pauli, E. Biggs, L. Barbour.and B. Boruff. 2021. Why bees are critical for achieving sustainable development. Ambio 50(1): 49-59.
67. Petreanu, D. 1979. Antibacterial Effect of Honey.
68. Petreanu, D. 2001. Beekeeping in Africa.
69. Picanço, A., A. Gil, F. Rigal and P. A. V. Borges. 2017. Pollination services mapping and economic valuation from insect communities: A case study in the Azores (Terceira Island). Nat. Conserv. 18: 1-25
70. Rahimi, E., S. Barghjelveh and P. Dong. 2021. Estimating potential range shift of some wild bees in response to climate change scenarios in northwestern regions of Iran. J. Ecol. Environ. 45(1): 1-13.
71. Reddy, P. V. R., A. Verghese and V. V. Rajan. 2012. Potential impact of climate change on honeybees (Apis spp.) and their pollination services. Pest Manage. Hortic. Ecosyst. 18(2): 121-127.
72. Roberts, E. 1969. Projects for the development of the beekeeping industry in Uganda.
73. Roberts, E. 1971. A Survey of Beekeeping in Uganda. Bee World 52(2): 57-67.
74. Roberts, A. E. L., H. L. Brown and R. E. Jenkins. 2015. On the antibacterial effects of manuka honey: mechanistic insights. Research and Reports in Biology, 215-224.
75. Safa, M., P. A. Sari, M. Shariati, M. Suhatril, N. T. Trung, K. Wakil and M. Khorami. 2020. Development of neuro-fuzzy and neuro-bee predictive models for prediction of the safety factor of eco-protection slopes. Phys. A: Stat. 550: 124046.
76. Shimelis, S. 2017. Survey of Honey Production System and Honeybee Disease and Pests in Ejere District, West Shewa Zone, Oromia Regional State, Ethiopia. Mvsc. Thesis. http://etd.aau.edu.et/handle/123456789/14659
77. Stainton, K. 2018. Recent Research on Nosema.
78. Tarunika Jain, A. 2014. Beekeeping Industry in India: Future Potential. IJRANSS 2(7): 133-140.
79. Tulu, D., M. Aleme, G. Mengistu, A. Bogale, A. Bezabeh and E. Mendesil. 2020. Improved beekeeping technology in Southwestern Ethiopia: Focus on beekeepers’ perception, adoption rate, and adoption determinants. Cogent Food Agric. 6(1): 1814070.
80. TUNADO. 2021. The Uganda National Apiculture Development Organization, Annual Report.
81. TUNADO. 2022. The Uganda National Apiculture Development Organization, Annual Report.
82. UCDA. 2023. Annual report. Uganda Coffee Development Authority. https://ugandacoffee.go.ug.
83. UNBS. 2022. Annual report. https://www.unbs.go.ug/attachments/34/UNBS/annualreoprt/fy2021-2022
84. UNECE. 2023. United Nation Economic Commission for Europe, Annual Midterm report.
85. UWA. 2019. Protected areas of Uganda. Wildlife Act. https://www.go.ug/documents/3345/acts-2019.
86. Van Alphen, J. J. M. and B. J. Fernhout. 2020. Natural selection, selective breeding, and the evolution of resistance of honeybees (A. mellifera) against Varroa. Zool. Lett. 6(1): 6.
87. Vinícius-Silva, R., D. D. F. Parma, R. B. Tostes, V. M. Arruda and M. D. V. Werneck. 2017. Importance of bees in pollination of Solanum lycopersicum L. (Solanaceae) in open field of the Southeast of Minas Gerais State, Brazil. Hoehnea 44(3): 349-360.
88. Wortmann, C. S. and C. S. Eledu. 1999. Uganda’s agroecological zones. A Guide for Planners and Policy Makers; Centro Internacional de Agricultura Tropica (CIAT): Kampala, Uganda, 54.
89. Zekarias, T., T. Tantasa and A. Ashebo. 2020. Medicinal Values of Hive Products: A Review. AJE 13(2): 26-34.