International Scholarly Research Notices

International Scholarly Research Notices / 2014 / Article

Research Article | Open Access

Volume 2014 |Article ID 368953 | 52 pages | https://doi.org/10.1155/2014/368953

Is Cut-Flower Industry Promotion by the Government Negatively Affecting Pollinator Biodiversity and Environmental/Human Health in Uganda?

Academic Editor: P. K. S. Shin
Received27 Sep 2013
Accepted30 Oct 2013
Published16 Mar 2014

Abstract

A study was conducted from 2010 to 2012 around the flower growing areas in central Uganda to generate baseline information on the status of pollinators. Primary data were gathered using a questionnaire that aimed at determining farmers and flower farm officials’ perceptions on the impact of activities carried out inside greenhouses on pollinators, human health, and on crop production in the surroundings. Results indicated that the quantity of pesticides and fertilizers applied daily varied among the different flower farms visited. Bee species richness and abundance varied significantly () according to flower farm location, to the landscape vegetation type, and to field types found in the surrounding of flower farms. Bee richness found around flower farms varied in number from 20 to 40 species in total across seasons and years. Bee density increased significantly with the increase in flower density. Small-scale farmers were aware of the value and importance of pollination services in their farming business. There was no clear evidence of a direct effect of agrochemicals application on bee communities living in the surrounding habitats. There is a need for further research to be conducted on human health risks and for toxicological studies on soils, plants, flowers, and bees in the farm landscape.

1. Introduction

Due to government policy of enhancing crop productivity in response to population growth, agricultural modernization in many forms is increasing at high speed in Uganda. Uganda produces approximately 11.1 million tonnes of flowers and is the second largest in South Saharan Africa after Nigeria. Uganda is among the top 10 producing flowers in the world. The first rose farms in Uganda were planted in 1992 and since then, the country flower industry has grown gradually. The average exports of flowers increased from US$9.72 million in 1998 to US$29.45 million in 2009. About 95% of the production is exported and 5% is sold on local market or thrown away [1]. Uganda’s floricultural sector has over the last 16 years emerged as an important nontraditional export earner, contributing over US$35 million in foreign exchange earnings in 2012 and directly employing over 6500–9000 people. The current government of Uganda’s objective for the flower industry is to stimulate its rapid development because of its contribution to the diversification of the export base and rural development.

Practically, cut-flower industry is growing in Uganda. Currently, there are many flower firms established in the country. However, various stakeholders from government departments/agencies, the academia, research organization, community based organizationss, and nongovernmental organizations are of the view that this industry is impacting the health of the environment and the health of human beings [1]. Biodiversity (such as bee biodiversity) is suspected to be affected (disappearing) in the surrounding of flower farms [1]. Therefore, there was a need to conduct a baseline study to gather information about the potential effect of flower farms on pollinators (bees).

A pollinator is the biotic agent (vector) that moves pollen from the male (anthers) of a flower to the female (stigma) of a flower [2]. Pollinators are a key component of global biodiversity that play an important functional role in most terrestrial ecosystems [2]. They represent a key ecosystem service that is vital to the maintenance of both wild plant communities and agricultural productivity [36]. Pollinators are critically important for the maintenance of the human agricultural enterprise, since they provide vital ecosystem services to crops and wild plants through their pollinating activities [79]. The most important pollinators in the world are bees. Bees are essential for healthy and diverse ecosystems through their pollinating activities. Approximately 80% of flowering plants depend on pollinators, mainly bees. However, bees constitute a fragile link to food production chains due to their vulnerability to various factors, mainly anthropogenic factors. Without pollinators (bees), ecosystem functioning, trophic cascades, and the survival and maintenance of genetic diversity of many wild plant populations would be at risk and economic yields of crops may suffer a drastic reduction [2, 10]. Hence, pollination is an essential step in the production of fruits and many vegetables [11]. An estimated 70% of world crops experience increases in size, quality, or stability because of pollinator services, benefiting 35% of the global food supply [710, 12, 13]. Animal pollination also contributes to the stability of food prices, food security, food diversity, and human nutrition [1416].

The value of pollination to agricultural production worldwide is currently estimated to be worth €153 billion per year or approximately 39% of the world crop production value (€675 billion) from the total value of 46 insect pollinated direct crop species [1416]. This value (€153 billion) is of more than €600 billion when added the economic benefit received from beekeeping products (sale of honey, propolis, etc.).

Though crop pollinators include a wide array of insects (e.g., beetles, butterflies, flies, etc.), bees are the most important and effective of these pollinators [14, 15]. As the world’s primary pollinators, bees are a critically important functional group because, roughly 90% of the world’s plant species are pollinated by animals and the main animal pollinators in most ecosystems are bees [1517]. Although other taxa including butterflies, flies, beetles, wasps, bats, birds, lizards, and mammals can be important pollinators in certain habitats and for particular plant species, none achieve the numerical dominance as flower visitors worldwide as bees [18]. The likely reason for this is that unlike other taxa, bees are obligate florivores throughout their life cycle, with both adults and larvae depending on floral products, primarily pollen and nectar. Bees (Hymenoptera: Apoidea) constitute an extremely species rich fauna, with an estimated 20,000–30,000 species worldwide [1921] but approximately 3000 afrotropical species and only 700–1100 species recorded in Uganda so far [2128].

The tropics are home to immense faunal and floral diversity and encompass much of the world’s biodiversity hotspots including bees [19]. Much of the tropics exist as a mosaic of agricultural lands and forest patches, and these human-altered landscapes can have strong impacts on local bee biodiversity [2128]. Tropical Sub-Saharan Africa is also characterized by strong ecological and agricultural dependencies on pollination [24, 25]. Hence, pollination shortage/decline is of great concern for food security in a continent where scientists are just beginning to understand how anthropogenic land-use impacts wild and managed pollinators. Since bees are very important in agricultural production, their status is therefore of great concern not only to the farmers but to any responsible government as well, as it has a direct impact on people’s livelihoods and the economy. This concern can therefore be translated into developing management techniques for the conservation of effective native bee species.

Although bees provide enormous ecological and economic benefits to flowering plants, wildlife, and humans, they are, however, under increasing threat from anthropogenic factors. There is considerable evidence for the negative impacts of habitat alteration on pollinators in highly disturbed regions of the world [28, 29], particularly in Europe and North America [29]. Pollinator crisis exists even in tropical and subtropical areas, where natural habitat is well represented [28]. Studies indicate that native pollinator populations face many threats, and evidence of a global pollination crisis is steadily growing [28, 29]. Currently, there are sufficient scientific evidence of a sizeable decrease in the population and range of many pollinators such as bees, butterflies, moths, hummingbirds, and bats from most biomes of the globe [29, 30].

Pollinators are at risk from numerous threats and this, in turn, threatens the many benefits people and ecosystems derive from pollination services. Drivers (disturbance types) of pollinator loss/decline [31, 32] include seminatural and natural habitats loss/degradation (destruction) and fragmentation through intensive land-use, misuse/over-use of toxic pesticides in agriculture (agricultural chemicals), pathogens [31, 32], alien species, toxic effects of secondary compounds produced by genetically engineered plants [33], and climate change and the interactions between them [3436]. The current challenge for the conservation of pollination services in rural landscapes is to better quantify the relative importance of a range of drivers (and pressures) and in particular their simultaneous synergistic effects in order to understand the magnitude of their impact, particularly if these are coupled with the clear ecological and economic risks associated with pollinator loss and crop yield failures [35, 36] such as agriculture intensification activities.

Agricultural intensification has got around 13 components of intensification [2024]. However, the use of insecticides and fungicides is the component known to have consistent negative effects on biodiversity and ecosystem services delivery [35, 37]. Agriculture modernization or modern agricultural practices (agrochemical applications), landscape fragmentation, and habitat degradation have been identified as key drivers that negatively affect bee populations in rural landscapes by the elimination of resources needed for successful reproduction such as nesting sites and pollen and nectar sources [35]. In Uganda, agricultural intensification is taking place. An example of agricultural modernization in Uganda includes the upsurge of the floriculture industry. Flower farms with high agrochemical inputs are clear evidence of agricultural modernization. The negative effects of agrochemicals on biodiversity in farmlands are well documented [3539]. As mentioned above, pesticides are considered a threat to pollinators [40, 41] although little is known about the potential impacts of their widespread use on pollination services in flower growing regions in Uganda.

The negative effects of agrochemicals (synthetic insecticides, botanical insecticides, miticides, acaricides, biologicals and natural enemies, fungicides, herbicides, seed dressing, adjuvant, nematicides, horticultural detergents, flower preservatives, plant growth regulators, foliar fertilizers, soil amendments, chelates, specialty fertilizers, grain storage insecticides, termiticides, rodenticides, etc.) on biodiversity in farmlands are well documented [35, 38, 39]. As mentioned above, pesticides are considered as a threat to pollinators [40, 41] although little is known about the potential impact of their widespread use on pollination services in habitats surrounding flower growing regions in Uganda. Since it is well established that agricultural chemicals can pose negative effects to biodiversity and to the environment of the areas where they have been applied [40, 41], loss of biodiversity around flowers is therefore expected in Uganda. However, assessing negative effects of agrochemicals applied by flower farms on biodiversity in the surrounding environment is very challenging since these agrochemicals are applied inside greenhouses and therefore expected to have almost no effect on the surrounding environment.

To our knowledge, there exists no study on the impact of inorganic fertilizer (NPK) application in greenhouses of flower farms on pollinators living in the surrounding habitats. Even when studies of the impact of fertilizers on biodiversity exist, they generally conclude the overall range of effects of inorganic fertilizers on species richness and abundance being arguably negligible or of little impact [42]. Contrastingly, Le Féon et al. [41] showed that increased nitrogen (and related inorganic fertilizer) input can cause a decline in floral resource diversity and abundance (nectariferous native plants) in European farmland habitats.

Overall, there is a need to determine the trends in response of biotic organisms (including bees) to inorganic fertilizations in and outside flower farms since they are agrochemicals and they cannot be without disturbance on surrounding local ecosystems. The best way to detect negative effects of pesticides application by the flower farm on biodiversity is to study responses of most sensitive biota to pesticides application regimes. Pollinators (bees) are the best candidates for such studies. They are good bioindicators of environmental health [4244]. Since it is well established that agricultural chemicals can have negative effects on biodiversity and on the environment of the areas where they have been applied, loss of biodiversity around flowers is expected [40]. However, assessing negative effects of agrochemicals applied by flower farms on biodiversity in the surrounding environment is very challenging since these agrochemicals are applied inside greenhouses and therefore expected to have almost no effect on the surrounding environment.

Local people’s experiences and perceptions of the effects of rural development projects (e.g., flower farm industry) are often not reported or taken into account by decision-makers despite strong arguments that local opinions can help in building a policy enabling achieving a win-win conservation/development scenario to meet development targets, and that a community’s willingness to become involved in decision-making for the establishment of a project in their village is closely linked to their past experiences and to their perception of the benefit. Much as gender-based differences exist in perceptions of problems, integrating understanding of people’s perceptions with field observations of the functioning of environmental systems is critical for developing sustainable resource management activities. Previous work examining farmers’ perceptions about importance of pollinators in crop production has shown that farmers often have acute and accurate awareness of problems, and they can propose effective interventions, even if they appear unable or unwilling to tackle them [24].

In the absence of relevant information, decision-makers may be obliged to formulate their policies based on perceptions and views of farmers that appear very relevant. Since historical data collections do not exist in Uganda, it is difficult to know which bee species has declined. Thus, farmers’ surveys remain the only reliable source of information that can help to provide researchers with an idea or an indication of what might have happened in the environment few years ago. Using farmers’ knowledge and perceptions about changes in bee populations over the last 5 to 50 years can help to understand what happened in the area several years ago and potential causes that led to such a situation.

Even though pollinator declines are a global biodiversity threat, drivers of pollination decline/loss in natural and in agricultural ecosystems of Uganda have not been taken into account by policy-makers, conservationists, and researchers, although Ugandan agriculture owe much of its production to services delivered by locally available diverse pollinator species [2025]. The real magnitude of pollinator decline is not easy to determine, particularly in countries like Uganda where there has been no historical data collections.

Based on the above background, there was a need to assess bee activities in the surrounding environment where different flower farms have been established. Accurate measurements of population densities (visitations) and species richness of bees are essential for any meaningful assessment of decline [2325]. For nonsocial bees, this can be done with direct counts of individuals and classical abundance measures. For social bees, however, the number of colonies rather than the number of individuals is the crucial parameter for conservation [36] and assessment of decline. Density estimates derived from direct counts of bees are tedious and can be unreliable because natural nests are hard to detect particularly when there is little time in the field. For rapid surveys, the number of individuals can be used to give an indication on the potential richness of colonies in the landscape because the number of colonies in the wild can be sometimes very difficult to assess. The census of managed hives and detection of wild colonies of honeybees within a radius of 0.1–3 km from a given sampling location can exhaustively be surveyed but it needs personnel with knowledge of local beekeeping operations. Therefore, for a study of short period (<3 years) like the one presented here, the spatiotemporal assessment of visitations of different bee species to flowering plants in a given habitat can be a useful approach to detect historical or previous changes (decline, increase) in bee species and populations in relationship to farm management and local and landscape drivers such as pesticide application intensity, availability of floral resources, and so forth.

Currently, there exist no studies from Uganda addressing effects of multiple drivers on bee abundance and species richness. Information on how pollinators respond to different drivers may improve the understanding of the nature, causes, and consequences of declines in pollinator services at a local and national scale, as well as providing light on how to invest for the development of mitigation options to slow the decline of pollinators in Uganda.

As previously highlighted, in Uganda, there have been various protestations and complaints of farmers and various stakeholders from government agencies, academia, research organizations, civil society organisations, and nongovernmental organisations about the boom of flower farms [1]. There were strong views and suspicion regarding the negative unknown impact of flower farms on health of humans, environment, and biodiversity in areas where the flower farms have been established. Consequently, there was a need to check whether these claims/complaints had a scientific foundation, when regarding effects on sensitive taxa such as bees. A preliminary field visit was conducted by the researcher and from that visit, it was pointed out that pollinators (specifically bees) inhabiting the surrounding of flower growing areas were likely to be at risk of disappearing. To verify this suspicion, an in-depth field study was therefore needed to be conducted. This was found to be necessary to ascertain community complaints.

The general objective of this study was therefore to conduct a rapid assessment on the status of pollinators (bees) around flower farms in central Uganda and provide guidelines on the preparation of a monitoring plan for the pollinators in the flower growing areas around Lake Victoria.

The specific objectives were (i) to gather information on the agrochemicals used by flower farms and their potential impacts on pollinator bees inhabiting the surroundings of the flower farms; (ii) to measure pollinator activities and assess the richness, abundance, and diversity of bees in relationship to landscape and habitat types found in the surroundings of flower farms; (iii) to assess the level of knowledge of pollination service importance in crop production by small-scale farmers living in the surroundings of flower farms; (iv) to document perceptions of local people with regards to cause of pollinator decline in their villages, (v) to collect views and perceptions of farmers about benefits and negative effects of the flower farms established in their villages; (vi) to collect views of farmers on the ways to promote flower industry in a sustainable manner (floriculture industry that matches people’s needs and desires, requirements for living in a clean nonpolluted environment); (vii) to outline bee monitoring and conservation strategies in the flower farm growing regions.

2. Materials and Methods

2.1. Study Area Description, Visits to Flower Farms, and Dialogue with Production Managers

This study was conducted in the banana-coffee system of Lake Victoria Arc covering several districts of central Uganda. The study zone (latitude: 0.5°31′22′′; longitude: 31°11′71′′; altitude: 1080–1325 m) is characterized by ferris oils with high to medium fertility level and receives on average 1000–1800 mm of rainfall per annum on a bimodal pattern (rainy seasons: March–May, September–November; semidry to dry seasons: June–August, December–February) with 28.7 ± 2.77°C and 68.65 ± 8.91% of mean annual temperature and relative humidity, respectively [2226]. But the rainfall amounts and patterns are unpredictable. The study zone belongs to the Lake Victoria phytochorion [2325] with shrubs of Acacia spp., legume trees, melliferous plant species, Papyrus, and palms ranging from 2 to 15 m high dominating the remnant secondary vegetation [2022]. In this study region, coffee (Coffea canephora, Pierre ex Froehner) is the main cash crop and banana the main staple food crop. Several pollinator-dependent food and cash crops are grown in small-scale monoculture and/or polyculture fields that are integrated into this coffee-banana agroforestry system including home-gardens. There were no standard crops per study sites but most crops were found grown in almost all study sites. Crops grown as sole or in association with coffee and or banana include cassava (Manihot esculentum L.), sweetpotato (Ipomoea batatus L.), maize (Zea mays L.), beans (Phaseolus vulgaris L.), groundnut (Arachis hypogea L.), tomato (Lycopersicon esculentum L.), watermelon (Citrullus lanatus L.), pumpkin (Cucurbita moschata L.), cucumber (Cucumis sativus L.), melon (Cucumis melo L.), chilies (Capsicum spp.), and several other fruits, vegetables, and horticultural crops (cabbage, onion, etc., egg plants, sim-sim, etc.). The majority of these crops are grown in small-scale monoculture and or polyculture fields that are integrated into the coffee-banana agroforest production systems. The agroforestry system is also dominated by several native/indigenous fruit and agroforestry tree species. Banana-coffee agroforests and small-scale farms cover about 60% of the land, whereas mixed mosaic seminatural habitats cover approximately 40% of the farm-landscape studied. There exist in this study region some large monoculture plantations (sugar cane plantations, coffee plantations, tea plantations, etc.) and some flower farms companies.

Rural central Uganda is a mosaic landscape where “islands” of patches of natural habitats (forest fragments, forest reserves, wetlands, woodlands) and linear (eg., hedgerows) and nonlinear (fallow fields, grasslands, woodlots, cattle pastures, or rangelands) features of seminatural habitats [21] that serve as “field boundaries” of the variety of small-scale fields are found scattered within agricultural matrices. Compared to other districts of the country, the study area (central Uganda) is also characterized by high demographic pressure, limited access to arable lands, continuous cultivation, and over-exploited lands under unrevised land policies [20]. All study sites had also some forest remnant tree species retained within them, ranging from 1 to 175 trees/ha found both in crop fields as well as inside remnant natural vegetations scattered inside the forest. Flower farms are located in four major zones of central Uganda: the first zone is Entebbe airport zone located at 60 km from Kampala city (example: Wagagai flower farm and Rosebud-II. Wagagai and Rosebud II are separated by a distance of 30 km). The second zone is in Mukono district located at about 250 km from Kampala city (example: Mairye estates), the third zone is Ntungamo zone located at about 500 km far away from Kampala city (example: Pear flower farm). In addition, mantel test () showed that there was no evidence of significant spatial autocorrelation between pollinator counts on transects within a landscape surrounding a flower farm. The distance between greenhouses and people’s homes varied from a flower farm to another one: >20 m–100 m. In many cases, small-scale gardens are established closer (0–20 m) to greenhouses. Thus, field visits were conducted to make a rapid survey on the status of pollinators (bees) around the flower farms in the Lake Victoria shores. To be able to understand the actual activities and operations within the flower farm, four flower farms were visited out of a total of 12 existing and operating flower farms in central Uganda, given the budgetary and time constraints. The 4 selected flower farms included Fiduga (located at 15 km far from Kampala, Wakiso district), Pearl flower farm (located at about 400 km far from Kampala in Ntungamo district), Mairye estates (located at 30 km far from Kampala in Mukono district) and Wagagai flower famr (located at about 40 km far away from Kampala along Entebbe airport road). Overall, commercial floriculture is still a new industry in Uganda, dating back to only 1993. Cut-flowers, cut foliage and, to a lesser degree, pot plant cuttings are the main outputs. Cut-flowers include a variety of roses, chrysanthemum cuttings, carnations, and summer flowers. The four flowers grow different types of flowers and varieties (Table 1) and apply different levels of pesticides. The major flower varieties grown and exported from Kenya are roses, carnation, alstroemeria, lisianthus, statice, and cut foliage. Rose flower dominates.


MAIRYEPEARL and WAGAGAIFIDUGA

Category of cut-flowers Intermediate Varieties 120 varieties of Crysantemum cuttings
Sweet heartRed Calypso (Red)Eg. Ibis lime, Nimba, Copper, Maiko, Noa, Parrot
Super sweet heartAkito (White)City, Art Sunny, Ludmilla, Fire, Zembla, Avoriaz
IntermediateBlushing Akito (Pink)Grand Salmon, Zakumi, Goody, Fuego, Voyager, Lexy, Breezers,
Jetset (Yellow)Tory, Safin Purple, Bacardi Yellow, Managua,
Varieities are Mylo (Pink)Vivid Cream, Tuvalu Sunny, Kindly Salmon, Zembla Cream,
For Super sweet heart:Inka (Bicolur Red/Yellow)Champagne Pink, Ibis Pearl, Ping Pong, Browny,
 ValentinoTropizal Amazon (Orange)Motown, Baracardi, Raisa, Verdy
 AkitoSonrisa (Yellow)Rwins, Merlot, Art, Ping Pong, Kuga, Quinty
 BanjoJupiter (Yellow)Kindly, Ludmilla, Puma Sunny, Redstart
For sweet heart:
 Tropical AmazonWild Calypso (Hot Pink)Leopard, Zembla Yellow, Grand Pink, Athos, Anastasia Pink,
 Jet SetBelle Rose (Pink)Crystal, Streamer Splendid, Dance Sunny, Felling Green Dar
 Red RibbonHandsome, Gabd Cherry, Froggy, Arctic Queen, Roma, Ping Pong,
 Red GiantMarabou, Fire, Parrot, Noa, Nimba, Kaitylnn, Tiger, Harley, Browny
Cheops, Purple Rain, Sound, Delianne Yellow, Ritmo, Charming,
Intermediate varietiesSalinas, Jazzy, Husky, Oxana, Clearity, Lollipop Purple, Falcon
 Blashing AkitoJoker, campus, Candor, le Mans, Planet, Lexy, Sarasarane Pink,
 LambadaSyrup, Moonlight, Lerbin, Minty, Anky, Edge, Katinka, Marabou, Marimo,
 FriscoLollipop Yellow, Vogue, Energy, Magic, Teror, Ferry, Fuego, Central
Leopard, Voyager, Swan, Puma, Vatican, Stromboli, Crystal Pink, Classy,
Diva, Starling, Zodiac Lilac, Vulcano Dark, Spider White, Punch,
Copper, Juicy, Chamapagne Ora, Boris Becker, Rocky, Pisang,
Merlot, Rosas, Goody Orange, Supernova, Froggy, Gin Pink, Berdy, Pelican
Eleonora Lilac, Vireo, Snowdown, Cheeks, Ritmo, Tigerrag, Ely, Charming
Greenbird, Avoriaz, Swan, Motto, Katinka, Sound, Vivid, Vivid Cream
Dance Salmon, Arctic Queen, Delianne White, Reagan White Eli, Balloon
Tamarinda White, Tamarinda Violet, Margarita Dark Pin, Margarita Helena
Hypnotica Red, Carolina Orange, Juventa, lrmon, Bromo, Margarita Lilac


Fertilizers appliedQuantity mixed in 1000–2000 liters of water

MAIRYE flower farm
Macroelements
 Calcium nitrate600 g
 Potassium nitrate350 g
 Magnesium sulfate350 g
 Ammonium phosphate150 g
 Monopotassium phosphate150 g
Microelements
 Iron10 g
 Zinc5 g
 Manganese5 g
 Boran5 g
PEARL flower farm
Macroelements
 Calcium nitrate86 Kg
 Potassium nitrate77 Kg
 Magnesium nitrate27 Kg
 Monopotassium phosphate30 Kg
 Urea29 Kg
 Microfeed2.2 Kg
 Librel3.4 Kg
Trait-elements
 Nitric acid15 Kg
 Phosphorc acid12 Kg
 Zinc sulphate0.2 Kg
 Borate0.2 Kg
FIDUGA flower farm
Macroelements
 Lime25 Kg
 TSP (triple super phosphate)2.5 Kg
 Calcium Nitrate3.5 Kg
 N-P-K ( 12-10-18)3.5 Kg
 Magnesium sulfate150 Kg

Type of pesticides appliedQuantity mixed per liter of water

MAIRYE flower farm
Fungicides
 Ortiva1 g/liter
 Nimrod2.5 g/liter
 Meltatox2.5 g/liter
 Previcur2 g/liter
 Ridonil2.5 g/liter
 Daconil2 g/liter
 Ravaral2 mL/liter
Insecticide
 Methomex1 g/liter
 Confidor1.5 g/liter
 Duduthrin0.8 g/liter
 Othane1 g/liter
Miticide/Nematicides
 Nemacin1.1 mL/liter
 Vydate1.5 mL/liter
Herbicide
 Lalad Master2 mL/liter
 Round-up3 mL/liter
PEARL flower farm
Insecticides
 Meltaton2.5 mL/liter
 Milraz2 mL/liter
 Equation0.4 mL/liter
 Teldor1 g/liter
 Roural1.5 mL/liter
 Score0.8 mL/liter
 Previcur1.5 mL/liter
Acaricide-Miticide
 Silwet0.5 mL/liter
 Fedion2 mL/liter
 Floxelle0.7 mL/liter
 Nissuron0.6 mL/liter

Flower farm visits were conducted for two years (2010 to 2012). During a visit of each flower farm, discussions with production manager were engaged by the researchers. The discussion focused on collection of information likely to enlighten the potential negative effect of activities conducted at the flower farm on pollinators as well as collecting information likely to help generate information that is more rewarding to policy-makers. During the course of discussions, various types of information were collected, mainly, information about the type of agrochemicals (pesticides, fertilizers) used by the flower farms, the type of varieties grown, the type of production conducted (e.g., exporting flowers cuts or stems or roses), the total number of people employed (including the proportion of females employed), the total size of the flower farm (including the number of hectares in production), the number of years since the flower farm was established, the monthly total production exported, the gross income from sale of flower products, the costs of labor, the costs of other general inputs, costs of pesticides/fertilizers purchases, and information about measures taken to control runoff of chemicals into the surrounding environment. The researcher visited stores of agrochemicals to confirm trade names reported by the flower farm production managers. In addition, production managers were asked whether they understood pollination and if pollination by bees was an important factor in their production business.

2.2. Landscape/Habitat, Bee Biodiversity, and Floral Resources Surveys
2.2.1. Landscape/Habitat Surveys

After farmers’ interviews, surveys of bees were conducted in different landscape/habitats in the immediate surroundings of the flower farms. For each flower farm, surveys were conducted in all directions considering the flower farm to be at the center. Two types of fields were found in the surroundings of flower farms: cultivated fields and noncultivated fields. The type of dominant landscape vegetations characterizing these cultivated and uncultivated fields were cropland and grassland vegetations. Cropland vegetation types that dominated cultivated fields were composed of a mixture of crops grown under various cropping/agroforestry systems. The grassland vegetation types that dominated the uncultivated fields were composed by a mosaic of seminatural habitats. The dominant habitat types in the croplands were different land-use types or crop associations (e.g., maize + beans + banana), whereas the dominant seminatural habitats in grasslands were pastures, fallows, woodlots, hedgerows, field margins, and so forth.

2.2.2. Transect Counts for Bee Surveys

Different beneficial insect taxa respond to agricultural practices at different spatial scales and often at multiple spatial scales [45]. Therefore, it was found important to assess bee diversity and visitations at different spatial scales by placing sampling transects at different distances from the flower farm. Placing sampling transects at different distances was sought to help in determining at which spatial scale chemical applications in the flower farms could affect significantly activities of bees in cultivated and noncultivated fields in the surrounding landscape habitats. The collection on bees was conducted for five consecutive rounds across dry and rainy seasons during two years (2010–2012) at regular periods (dates) of visits of the flowers farms. Hence, five transects were set from the edge of the flower farm into either croplands or grasslands or both. Transects were established, extending from the flower farm boundary into farmlands. Transects were separated by a distance of 3–5 km. They were set in north, east, west, and southern part of each flower farm. With this distance, bee samples were independents since the normal foraging distance of most bees is 2 km. Each transect measured a total length of 2.2 km. Bees were sampled on these transects (20 m-large × 2.2 km-long) at 0–10 m, 500 m, 1500 m, and 2000 m from the edge of the flower farm. Transects were set parallel to flower farms at the above mentioned distances. Plots were set mainly at different flower patches alongside transects. In this study, flower patches were isolated groups of blooming plants; the group was composed of various plants of same or various species associated in a given site. Flowers were composed of either natural vegetation or crop plants and in some cases both.

While walking along transect, at each flower patch, data was collected on bee populations using field observations, hand-nets, and transect-count methods. Observations were also made on other pollinators, such as butterflies, moth, and hover flies; although detailed data is not presented since the focus was on bees.

Within each plot, bee species within the plots were counted and their visitation intensity was measured and recorded on datasheets. Parallel to bee surveys, habitat/land-use variables were also recorded such as the percentage cover and number of seminatural habitats. When needed (in some few cases), nests of solitary bees were recorded using subjective (focused) searches in particular habitats (nesting habitats). The different nests were also located either by chance during random searches or by inspecting tree-holes/termite mounds located alongside established belt transects of width 20 m and length 1.1 km per transect.

Bee collections/censuses were conducted from morning to evening hours (07:00 h to 17:00 h, local time). Pesticides applications inside greenhouses are commonly conducted at different interval of times: 5:00 h–7:30 h, 7:30 h–10:30 h, 15:30 h–18:30 h. Therefore, some bee collections coincided with periods of pesticides application.

2.2.3. Censuses of Bee-Visitations

Visitations are part of four measures of pollination services delivery by pollinators to plants/crops: (a) pollination rate (number of pollinators visiting flowers/min), (b) proportion of visited flowers (number of flowers visited by pollinators/total number of flowers in a plot), (c) flower handling time (seconds) or the mean time pollinators spent on individual flowers in a plot, and (d) pollination efficiency (% fruit set after single visit by a p). These four parameters of pollination services can be used to forecast high reproductive success of plants/crops after visitation of crops/plants as compared to those that were not visited. Thus, pollinator visitations (number of bee individuals landing on flower reproductive parts and moving/collecting floral resources such as pollen/nectar for at least 0.1–1 minute before flying away) to plants/crops species in flower patches were conducted from morning to evening hours each sampling day.

All floral visitors, pollinators and nonpollinators to male and female flowers and inflorescences of all flowering plant species were collected at the time of their greatest activity. The pollinator censuses were conducted for 2 full years (2010–2012 and for each year, data was collected during four consecutive sampling rounds (R1: December–February, R2: March–May, R3: June–August, R4: September–November)). The pollinator censuses were conducted within permanent plots (20 m × 100 m) that were placed in a systematic way (along line transects of 20 m × 1100 m) and separated by 10 m. Pollination information was basically collected on transects. Overall, data recorded was based on an observable number of bees per flower patch per 25 m2 (5 m × 5 m) from each sampling unit (plot). The data recorded and stored in datasheets was expressed as number of bee-visits per bee species per 100–500 flowers/15–20 min observations per flower patch of 25 m2 (5 m × 5 m).

While walking along transect, censuses of bees were performed during 15–30 min at each flowering patch met along the transect. In each census, several floral stems with 100–5000 flowers were observed. A total of 10 to 50 flower patches were met and censured each study visit. Minimum observation distance from the flowers was 2 m. In each census, the number and identity of visitors were recorded, including the number of flowers visited, the visitation intensity of each bee species, and the behavior of these visitors on the flowers. The abundance, diversity, and composition of the flower visitor assemblage of the focal populations were determined by counting the number of insects visiting the flowers by means of point-centered 30 min surveys. Sampling took place during full bloom of plants. Thus, fully blooming inflorescences/flowers were monitored during the entire foraging period of the day including the period of peak insect visitation activity (9:00 h–15:00 h).

Flower-visiting insects were identified, and buzz-pollinating ability (based on observation of sonication and pollen release by some bees such as Xylocopa) was recorded for each visit whenever possible. During bee counts, local temperature and wind speed were recorded at the start of each transect as these can affect pollinator behavior, although counting was conducted only at temperatures above 18°C to eliminate the impact of low temperatures on counts. Censuses were conducted along the day from 6:30 h to 17:30 h local time. Each study visit, surveys were carried out across the five transect.

Duration of flower visits to individual inflorescences/flowers of each plant species was recorded for several individual bees and rounded up to full minutes. A flower visit was defined as the period between the first landing on the inflorescence and final departure (irrespective of short hovering flights for scent transfer). More specifically, a visit was defined to have occurred when the visitor’s body contacted the reproductive organs (stigma or anther) of any available fresh flower. The bee observations were conducted each day that weather conditions allowed pollinator activities. The order of observation of plots alongside transect was random, each plot being observed only once per day. During each observation period on flowering patches in sampling plots, the number and identity of flower visitors to flowers or inflorescences (depending on the species) of all species blooming in the plots were noted.

The identification of some flower visitors was done in the field with the experience of the researcher. For species that could not be identified in the field during foraging observations, the visitor was given a morpho-species name and immediately after finishing foraging observation data collection on datasheets, a handnet was used to collect specimens. Voucher specimens of visiting bees were collected from flowering plants on separate moments to avoid disturbance to pollinator activity. The specimens were saved in alcohol 70% and later the identification confirmed in the laboratory using available collection of bees of Uganda. The bees were identified using the author’s reference collection of bees that is located at Makerere University zoology museum.

2.2.4. Assessment of Floral Resources

To account for the floral abundance of the plant species, after each observation period, each species’ number of open attraction units to bees which could be flowers or inflorescences was counted. The data recorded was expressed as number of fresh flowers (all plant species combined) per flower patch per 25 m2. In addition, the number of flowering plant species was recorded per sampling plot alongside transect walks.

2.3. Field Surveys and Farmer’s Interviews on Pollination Knowledge and on Causes of Pollinators Decline in Relationship to Activities Carried Out at Flower Farms

In the surrounding of each flower farm, four directions were followed. In each direction, 2 villages were selected in the north, south, east, and western directions of the flower farm. In each direction, the first village was selected between 0 m and 1 km far from the edge of the flower farm; the second village was selected between 2 and 3 km far from the flower farm. These villages were selected to cover the range of space at which a farmer could smell and could not smell the scent of the chemicals from the flower farms. In each village 20 people (10 men and 10 women) were randomly selected while walking alongside main trucks in the village. In total, 160 people were interviewed from 4 villages from the four directions in the surrounding of the 4 flower farms, making them 640 people interviewed in total from the surroundings of the four flower farms. Farmers interviewed were those met in their gardens busy farming. During interviews, after finishing the dialogue with farmers, the researcher conducted field inspection under their guidance. Field visit and inspection were conducted to enable scientists/researchers to verify whatever farmers were reporting when interested in gathering information about their ecological knowledge of pollination process.

Primary data were collected by administering a questionnaire to production managers of different flower farms and to small-scale farmers living in the surroundings of the flower farms. In addition, a separate datasheet was used to gather data on bee species diversity and populations. The questionnaire captured information on agrochemicals used, bee diversity, landscape/terrain, weather conditions, especially at the time of bee surveys, farmers, and flower official perceptions and the impact of their activities on pollinators and crops.

More specifically, the effects of farm management practices (agrochemical pesticides utilization intensity), landscape vegetation types, distance from the flower farm, and the flower farm location on bee communities foraging in environments surrounding flower farms were investigated. The investigation aimed at identifying factors that could help in understanding the potential role of agrochemical activities carried out inside flower farms on bee biodiversity living in the adjacent habitats. In addition, farmers’ surveys were conducted in order to get an idea of the potential causes of decline of bees in the villages including the impact of flower farm activities (agrochemical applications).

The questionnaire was also administered to assess if farmers understood the meaning of pollinators, pollination, and pollination service and its importance in crop production activity. Villages where flower farm activities were not expected to impact agricultural production were identified (villages located at more than 5 km far away from the edge of the flower farms) and sampled to ascertain the differences in bee populations and species richness. Only farmers found doing some activities in their gardens were interviewed. Efforts were made to be gender sensitive during the course of interview. However, women were frequently found in the gardens than men.

The questionnaire consisted of a mixture of open and closed ended questions. The questionnaire was pretested by the researcher a few weeks prior to field surveys. Semistructured interviews that had a number of predefined starting questions were used. Thus, farmers were interviewed using a pretested structured questionnaire. The questionnaire was piloted by the researcher one week prior to the actual survey and the necessary corrections were made. Interviews were largely conducted in the local languages (Luganda, Runyakore) with translation into English whenever necessary.

Data collection related to interviews at the different sites took place from 9:00 am onwards, because most women started their agricultural activities by 6:00 am and were completed by midday. Prior to data collection, the researchers solicited informed consent from participants. The questionnaires took approximately 20–30 minutes to administer to each individual respondent. The questionnaire was filled using face to face interviews. Interviews were conducted either at the farmer’s home or in the field, where such fields were within 0.5–1 km from a farmer’s homestead and the farmer was willing to be interviewed on site (field or garden). Once conversation on a topic was initiated, it was allowed to roam freely until exhausted at which point a new topic was begun. It was ensured that interviewees had the opportunity to ask the researchers questions at the end.

Notes were taken on individuals’ responses. The researcher visited every respondent’s crop field in order to verify some of their responses. The questionnaire submitted to small-scale farmers focused mainly on crop production and the relevance of pollinators in crop production. The survey questionnaire comprised two main parts. The first section sought general sociodemographic information about respondents, including age, gender, household income, gender labour in crop production, marital status, number of children, and formal education levels. The second section gathered information relating to respondents’ knowledge of crop pollination, pollinator types, perception of the importance of pollinators to crop yield, potential causes of decline of pollinators in the village, and potential role played by activities (application of agrochemicals) carried out by the flower farm located in the village. Specifically, farmers were asked to (i) describe/define their understanding of pollination, (ii) to name, identify, and differentiate between wild bees and honeybees and other insect pollinators they knew and indicate the area where they sleep (nesting site), (iii) mention the role of bees and other pollinators in crop fruit/seed set, (iv) to explain the importance of pollinators in their farming business, (v) to comment on the effects of pesticides application on wild bees and other pollinators, (vi) to list (and justify why they think so) the potential causes of decline/loss of pollinators in their village including describing the role played by activities carried out at the flower farm such as intensive application of agrochemicals, (vii) to comment on the linkage between crop yields reduction and bee decline in the village, (viii) to list advantages (benefits) they get by living near the flower farms, (ix) to propose sustainable solutions to resolve their conflicts with flower farms. Photographs of different bee species and different other pollinator species were presented to respondents to help in identification of different species of bees visiting crop flowers.

2.4. Data Analysis
2.4.1. Cumulative Analysis of Agrochemicals Application

From the raw data obtained during discussions with the flower farm managers, the total amount of agrochemicals applied on a daily basis was used to calculate the amount of agrochemicals used per annum in relationship to total amount of water used. Later on, the annual amount of pesticides used was cumulated based on the number of years since the flower has been in production. The cumulative analysis was undertaken using Microsoft Excel 2007.

2.4.2. Bee Visitation and Floral Resources Raw Data Files Pooling and Organizations

Data on bee counts and visitations that were recorded per each sampling plot were summed to obtain the total number of bee-visits and bee species per transect each study round. Similarly, the total number of fresh flowers and number of flowering plant species per transect was obtained by summing values obtained per sampling plot (20 m × 100 m).

2.4.3. Variation in Bee Abundance, Visitation, Species Richness, and in Flower Density between Surrounding Habitats of the Different Flower Farms

Cross-tabulations with selected variables (number of species and individuals, visitation frequency) were undertaken using pivot table in Microsoft Excel 2007, to verify anomalies and correct errors in raw data files before data analysis.

En ce qui concerne the diversity and numbers of bees, the abundance of flower visitors was estimated by standardizing the number of visits per time unit (expressed as visits per population per hour/flower patch). Flower visitor diversity was assessed by calculating species richness and evenness. Richness was calculated as the number of flower-visiting species found visiting flowers in flowering patches. Diversity of bee communities between the four flower farms was estimated using the Shannon-Wiener’s diversity index () and the similarity in bee communities among the four flower farms was estimated by the Sorensen similarity index according to Magurran [46] using raw data collected across four rounds of data collection over two years (2010–2012).

2.4.4. Effects of Landscape/Habitat Types on Bee Abundance and Species Richness

All variables were tested for normality and the strongly skewed variables were transformed prior to analyses if necessary to meet the assumption of normality and homogeneity of variances. Therefore, the percentage cover of flowering plants was arcsine-square-root (+0.5) transformed and number of species or counts of bee individuals and bee-visitations counts were transformed. The differences in number of bee individuals and species and in number of fresh flowers between the 4 flower farms were tested with general linear model (GLM) analysis of variance (ANOVA) in Minitab release version 165. GLM analyses were fitted with pesticides application intensity (very high: 4, high: 3, medium: 2, and low: 1) landscape vegetation types, flower farms, and number of transects as treatment factors (predictors) and the abundance, visitation frequency, species richness of bees, and number of fresh flowers as the response variables. Where GLM test indicated significant differences, posthoc Tukey’s test was used for means separations.

2.4.5. Farmers’ Surveys

The survey data were entered into a spreadsheet and checked prior to analysis. Cross-tabulation with selected variables, percentages, and means were undertaken using pivot table in Microsoft Excel 2007. Percentages were based on either the total number of respondents or total responses, details of which are provided in the respective text or tables. Chi-square test was used to determine association between variables such as to determine the effects of farmers’ sociodemographic profiles on their knowledge of pollinators, pollinator unfriendly farming practices, farmers’ perceptions of crop yield reduction, and causes of decline of pollinators in their villages. During interviews of farmers about potential negative effects of agrochemicals applied by the flower farms on crop yields, decline of bees, and environmental pollution, most often a farmer could give more than one justification/statement (opinion). Therefore, both the summary of the statements made by farmers and the full statements were presented in separate tables/figures. The frequency of occurrence of the statements from the entire population interviewed was calculated and presented in respective tables.

3. Results

3.1. Agronomic and Socioeconomic Characteristics of Flower Farms Studied

The different farms studied were established with clear production objectives. For example, Mairye and Pearl flower farms were found to be specialized in the production of cut flowers and roses whereas Fiduga flower farm was found to be specialized in the production and export of Crysantemum cuttings (stems). Hence, different companies grow different types of flower varieties (see Table 1). The land under production played a big role in the production potential for each farm.

The number of employed people was 800, 485, and 255, respectively, at Mairye, Fiduga, and Pearl flower farms. Across flower farms, the proportion of employed females oscillated between 55 and 65%. The monthly total production for export varied from one flower farm to another: 4 million cut-flowers for Mairye, 36 million cuttings for Fiduga, and 2 million cut flowers (including roses) for Pearl. Consequently, the declared total annual income obtained from sales of flower cuttings was US$90,000, US$47,000, and US$7000 for Mairye, Fiduga, and Pearl flowers farms, respectively. The monthly cost for pesticides/fertilizers purchase oscillated between US$10,000 and US$53,000 across flower farms.

There was a positive correlation between the monthly total income obtained per flower farm after sales of flower cuttings and (i) the cost of general inputs (, , ), (ii) cost of labor (; , ), (iii) the number of employed females by the flower farm (; ; ), and (iv) total size of the flower farm in production (, , ). On the other hand, there was no significant () correlation between the monthly total income obtained per flower farm after sales of flower cuttings and (i) the number of employed males (; , ), (ii) the total number of workers (; , ), (iii) the total farm size land (, , ), and (iv) the cost pesticides/fertilizers (; , ). This last result indicated that it may not be necessarily rational for a flower farm to over spend on agrochemicals (pesticides/fertilizers) that are dangerous to the health of human beings and to the environment. In other words, it is still possible to have a flower company reaching high profitability while spending little on toxic pesticides. Different options of buying and using nontoxic and effective pesticides can still be adopted by a flower company and obtain good profitability.

3.2. Variation among Flower Farms in the Application of Agrochemicals (Pesticides, Fertilizers) inside Greenhouses

During field visits, information on agrochemicals used by the different flower farms was collected. A checklist of different fertilizers and pesticides used and dosages are given in Tables 3 and 4, respectively. Long-term use of fertilizers for agricultural purposes has been an issue of concern to researchers. The presence of metals in some agricultural fertilizers raised fears that continued application of fertilizers may lead to accumulation of these metals to toxic levels in the soil for living organisms including plants. Prolonged fertilizers use is also a concern in sites where cut-flower industries are established in that it may affect neighboring small-scale lands.


ResponsesFixed factorsdf value value

Bee species richnessIntensity of agrochemical applications (3,33)1.93 0.142
Flower farm name (location) (3,33)2.94 0.048
Landscape vegetation types (1,33)4.30 0.047
Transects (4,33)3.88 0.012

Bee abundancesIntensity of agrochemical applications (3,33)9.881 0.000
Flower farm name (location) (3,33)13.94 0.000
Landscape vegetation types (1,33)2.361 0.135
Transects (4,33)4.070.009

Bee visitation frequency Intensity of agrochemical applications (3,33)8.02 0.000
Flower farm name (location) (3,33)11.120.000
Landscape vegetation types (1,33)0.09 0.773
Transects (4,33)4.42 0.006

Blooming plants abundance Intensity of agrochemical applications (3,33)0.64 0.595
Flower farm name (location) (3,33)1.69 0.190
Landscape vegetation types (1,33)5.27 0.029
Transects (4,33)13.80 0.000

Blooming plant species richness Intensity of agrochemical applications (3,33)0.7110.598
Flower farm name (location) (3,33)0.7780.541
Landscape vegetation types (1,33)2.4150.018
Transects (4,33)3.3310.0016

Nests and nesting sites density (abundance) on transects Intensity of agrochemical applications (3,33)2.7430.033
Flower farm name (location) (3,33)2.5680.044
Landscape vegetation types (1,33)2.7960.027
Transects (4,33)23.120.000


Different types of crops grown in association by farmers
Frequency of crop associations in non-pollinator-dependent cropsFreq. (%)

Cassava-Banana 14.06
Cassava-Banana-Yams-Taro1.56
Banana-Maize-Millet 6.25
Banana-Sweetpotato-Cassava-Maize3.13
Banana-Sweetpotato-Maize 7.81
Cassava-Maize-Sweetpotato-Banana10.94
Cassava-Sweetpotato-Banana-Maize3.13
Maize-Cassava-Sweetpotato-Banana17.10
Sweetpotato-Banana14.06
Sweetpotato-Banana-Cassava 9.38
Sweetpotato-Banana-Maize-Cabbage 10.94
Sweetpotato-Maize-Cassava 1.56
Frequeny of crop associations in pollinator-dependent crops
Egg plant-Mango-Beans-Groundnut-Pepper-Pumpkin 3.03
Avocado-Mango-Pumpkin-Beans-Coffee15.15
Avocado-Pumpkin-Beans-Tomato-Coffee 12.12
Beans-Egg plants-Tomato3.03
Beans-Avocado-Mango 22.73
Beans-Groundnut-Pumpkin6.06
Beans-Papaw-Watermelon-Pumpkin-Egg plant-Tomato6.06
Beans-Tomato-Avocado-Papaya 6.06
Citrus-Papaw-Beans-Cowpea-Avocado-Mango1.52
Coffee-Avocado-Passion fruit-Vanilla1.52
Coffee-Tomato-Beans-Papaw-Vanilla 9.09
Pumpkin-Beans-Watermelon-Egg plant7.58

In these flower farms, spraying of pesticide is done manually by male workers provided with almost no means of protection apart from gumboot. There was a high variability in quantity of pesticides and fertilizers applied daily among the different flower farms visited (Tables 3 and 4). In the pesticide class, fungicides, miticide-nematicide, insecticides, and herbicides were applied by the different flower farms at different levels.

Types (herbicides, insecticides nematicides, miticides, and fungicides) and number of pesticide applications on flowers were retained as a surrogate variable for agricultural practice intensity inside the flower farm. Indeed, this variable reflected both the amount of inputs in field greenhouse (to increase flower productivity) and disturbance of environment and human health caused by each spray session by farming pumps or spray machines. Overall, the intensity of pesticide application (that combines both the types and number of pesticides applied per month) was considered as a proxy of flower production practice intensity. This surrogate has a potential indirect impact on pollinator communities living in habitats surrounding flower farms. The intensity of pesticide application by the flower farm was measured at four levels (very high: 4, high: 3, medium: 2, and low: 1). Based on quantity reported by the production mangers and based on field experiences (observations, field impressions), Fiduga flower farm was classified as the flower farm with very high level of intensity of pesticide application; and Rosebud-II was classified as with high level of intensity of pesticide application whereas Mairye was classified as flower farm with medium level of intensity of pesticide applications. The flower farm that was classified as with low level of intensity of pesticide applications was Pearl flower farm.

It was not clear whether the quantity of pesticides had an effect on pollinators living in the surrounding habitats, since most of the agrochemicals were applied inside greenhouses of the flower farms. However, daily application of pesticides cannot be without effect on the surrounding environment with its living organisms. In the short term, the effects may not be visible or perceptible. However, in the long-term, the effects may be visible/perceptible given the fact that different types of pesticides have different characteristics of persistence in the environment. The more pesticides were applied from one focal point, the more they would accumulate in the environment with consequences of disturbing/disorganizing natural and ecological systems.

The results indicated that the amount of agrochemicals spent so far per flower varied with the number of years since the flower farm was established (Figure 2). Among the 3 flower farms for which data was available, Mairye is likely to have applied 250,000 kg (m.a) of fungicides; 1200000 kg (m.a.) of insecticides; 65000 kg of nematicide-maticide; 35000 kg of herbicides; and approximately 200,000,000 liters of water for a total land in production of 18 ha. This amount of pesticide application with high environmental persistence cannot be with any consequence to the local environment. There is a need to choose to apply less toxic pesticides by the flower firms.

3.3. Precautionary Measures Taken by Owners of Flower Farms for Containing Chemical Runoff from Flowers into the Surrounding Environment

When asked about the strategies/measures taken by the flower farm to reduce negative effects of chemicals runoff into the environment, all production managers said they recycled and controlled well the quality of water before releasing it into the environment. Across all flower farms, greenhouses were set in such a way as to be always open to the outside; and this was suspected to have a great influence on pollinators and movement of pesticides into farmland habitats.

Production managers interviewed said management of agrochemicals and effluent from flower farms were a major concern by their companies. They also said that they were aware that pesticides, fertilisers, and herbicides can pollute river, lake, and wetland systems as a result of poor management of effluent from the flower farms and this constitutes a threat to aquatic life like fish and human health. Hence, they had to take measures that minimise soil and water pollution, such as constructing lagoons and planting papyrus to perform water purification (artificial wetlands). For example, production managers said that the water recycling system has enabled them to reduce water needs from 50,000 liters of water/day/ha to 13–20  liters/day/ha. However, during office discussion with the production managers, a question was asked about their perceptions/views in response to farmers’ complaints of chemicals sprayed in the flower farms affecting their crops/livestock and their own health in the village nearby, some production managers said that they have never received complaints from the nearby communities, others said they control perfectly chemical runoff, and therefore accusations of farmers living nearby were not correct.

3.4. Effects of the Types of Habitats Found in the Surrounding Landscape of Flower Farms on Bee Abundance and Species Richness and on Availability of Floral Resources

Bee nests density, species richness, abundance, and visitation frequency to blooming plants in landscapes found in the villages surrounding the flower farms varied significantly (GLM test, ) across transects and locations of the flower farms. They also varied by the intensity of agrochemicals (pesticides, fertilizers) applications by the flower farms (Table 3) since flower farms that used more agrochemicals were also involved in regular (frequent) throwing (dumping) of agricultural wastes (agrochemical wastes) in the grasslands/croplands in the villages nearby the flower farms. However, the richness and the abundance of blooming plant species were not significantly () affected by the intensity of application of agrochemicals (pesticides) nor by the flower farm location. But they varied significantly (, GLM test) across transects and according to landscape types/vegetation type. This result indicated that agrochemicals application during flower production process did not affect the richness of blooming plants in the neighborhood; few plant species managed to get adapted to such environment. Adapted plants were seen to be abundantly in bloom around the neighborhood of the flower farm (Table 3) even when there were few bees visiting such blossoms. Also, there was a significant positive correlation (, ) between the intensity of pesticides application by the different flower farms and the monthly net income from sales of cuttings.

Farmers living in the surrounding of different flower farms are engaged in the cultivation of different types of crop species in association. The average number of pollinator-dependent crop species inventoried during the study survey was 5.1 ± 0.9 (Fiduga), 3.1 ± 0.6 (Mairye), 2.3 ± 0.9 (Pearl), and 4.6 ± 0.85 (Rosebud = Wagagai). The number of nonpollinator-dependent crop species grown was 3.3 ± 0.35 (Fiduga), 1.9 ± 0.7 (Mairye), 2.2 ± 0.45 (Pearl), and 2.3 ± 1.12 (Rosebud) (Table 4).

In the surrounding of each flowering farm, there were significant () differences in species richness, abundance, visitation frequency, and number of fresh flowers per transect at different distances (0 m, 10 m, 50 m, 500 m, 1500 m) far away from the flower farm into farmland habitats. For example, for Pearl flower farm, there were significant differences between the 5 distances (0 m, 10 m, 50 m, 500 m, 1500 m, 2000 m) in species richness (GLM: , ), abundance (GLM: , ), bee visitation frequency (GLM: , ), and abundance of fresh flowers (GLM: , ) (Figure 3). Similar trends in the results were observed at Mairye, Rosebud, and Fiduga flower farms (Figure 3).

In the surrounding of each flower farm and across sampling rounds (R1, R2, R3, R4), there were significant differences in the species richness and abundance of bees. In fact, for Pearl flower farm, there were significant differences in species richness of blooming plants in croplands (GLM: , ) as well as in farmland habitats (GLM: , ). Results of similar trends were observed for the percentage cover of mass blooming plants/transects in both croplands (GLM: , ) and grassland habitats (GLM: , ; Figure 4).

The abundance of bees varied significantly (, test) across the different land-use types and seminatural habitats encountered on transects during transect counts of bees across the surroundings of the four flower farms (Table 5). The most visited land-use types were the banana + bean + cassava, followed by young fallows, field margins, and coffee + banana + cassava + beans + fruit trees + agroforestry trees. The most visited seminatural habitat among those encountered during transect counts of bees in grassland and rangeland habitats was “shrubby fallow”, followed by unfenced grazing plot followed by pad-docking fenced grazing plot with live fence, unreclaimed papyrus swampy habitat, and hedgerow (Table 5). Different bee species made visits to blooming plants in these different habitats/land-uses at different periods of the day; most frequently, they made intense visits from 10:30 h to 15:30 h. The spray of chemicals in flower farms is generally conducted between 6:30 h and 8:30 h or between 15:30 h and 18:30 h.

(a)

Field typesLand-use types encountered during bee transect counts in croplandsRelative abundance (%)

Cultivated fieldsAbandoned bushy gardens 0.1
Cultivated fieldsAgroforestry trees + Banana + Beans + Maize + Fruit trees3.3
Cultivated fields Banana + Bean + Cassava crops 29.7
Cultivated fields Banana + Beans + Sweetpotato + Agroforestry trees + Fruit trees 4.8
Cultivated fieldsBanana + Cassava + Beans + Maize0.9
Cultivated fieldsBanana + Cassava + Beans + Sweetpotato + Maize + Mango + Avocado3.3
Cultivated fieldsBanana + Cassava + Groundnut + Fruit trees0.8
Cultivated fieldsBanana + Coffee + Beans + Maize + Mango + Avocado1.7
Cultivated fieldsBanana + Egg plant + Tomato + Bean + Sweetpotato1.6
Cultivated fieldsBanana + Groundnut + Casssava + Maize + Agroforestry trees2.8
Cultivated fieldsBanana + Maize + Beans + Sweetpotato + Fruit trees2.2
Cultivated fieldsCoffee + Banana + Cassava + Beans + Fruit trees2.0
Cultivated fields Coffee-Banana-Cassava-Beans–Fruit trees-Agroforestry trees 7.1
Cultivated fieldsCoffee + Banana + Cassava + Groundnut + Maize + Fruit trees0.5
Cultivated fieldsFruits orchards + Homegardens1.2
Cultivated fieldsCommunal grazing fields1.3
Cultivated fields Field margins 9.3
Cultivated fields Hedgerows (established in farmlands) 6.8
Cultivated fields Swampy crops (Egg plant + Pumpkin + Watermelon + Tomato, etc.) 6.4
Cultivated fields Herbaceous young fallows 15.8

Chi-square test: , , , .
(b)

Field typesSemi-natural habitat types encountered during transect-counts of bees in grasslands/rangelandsRelative abundance (%)

Uncultivated fieldsEdge of natural wetlands (various plant species mixed) 0.22
Uncultivated fieldsForest fallow (Vernonia sp.)1.70
Uncultivated fieldsForest fallows 1.00
Uncultivated fieldsForested-swampy habitats2.21
Uncultivated fieldsGrassy fallows1.50
Uncultivated fields Hedgerows (established rangelands) 4.42
Uncultivated fieldsHerbaceous/shrubby grasslands1.43
Uncultivated fields Lake Victoria-edge vegetation (various species) 5.88
Uncultivated fieldsLantana camara-Erlangeya tomentosa old fallows0.83
Uncultivated fieldsLantana camara-Erythrina sp. hedges on roadsides10.07
Uncultivated fieldsNatural forest remnant patches0.44
Uncultivated fieldsOld fallows (Lantana camara-Cassia sp.-Maesa lancelota)1.12
Uncultivated fields Paddocking fenced grazing plots (with live fences) 12.64
Uncultivated fieldsReclaimed wetlands (with crops + natural vegetations)0.99
Uncultivated fields Shrubby old fallows 25.29
Uncultivated fields Swampy habitat vegetation (various plant species mixed) 3.66
Uncultivated fields Unfenced grazing plots 19.97
Uncultivated fields Unreclaimed-papyrus swampy habitats 4.60
Uncultivated fieldsWoodlands (Euphorbia sp.)0.15
Uncultivated fieldsWoodlots (Eucalyptus-Pine)0.46
Uncultivated fieldsWoodlots (native and exotic species mixed)1.42

Chi-square test: , , , .

Different bee species were recorded significantly ( 3 df = 7.87, ) in the different cropland and grassland habitats in the surrounding of the flower farms. They occurred with different abundance. In total: 37, 26, 45, and 33 bee species were recorded in the surrounding of respectively, Fiduga, Mairye, Pearl, and Wagagai (Rosebud-II) flower farms. Landscape habitats surrounding Pearl flower supported more diverse bee communities (mean ± SE of ) than Mairye (mean ± SE of ), Fiduga (mean ± SE of ), and Wagagai (mean ± SE of ) flower farms (GLM-ANOVA: , ). However, there were no significant differences (, , df = 3) among flower farms in the average similarity index values of shared bee species. In other words, bee communities from these flowers were statistically similar in species composition. Common bee species were frequently recorded to be abundant on flowers than specialist bees. In the tropics, the structure of most bee communities is not different from that of other insects. There is always 1–5% of dominant bee species and 90–95% of species that are rare or appear as singletons or doubletons.

There was a significance ( test, ) in relative abundance of different bee species in the surrounding of different flower farms. The most abundant bee species in the surrounding habitats (croplands, grasslands) were Apis mellifera adansonii (14.08%), followed by Meliponula ferruginea (10.90%) and Nomia brevipes (9.03%). The most abundant species in the farmland around Mairye were Apis mellifera adansonii (23.3%), followed by Meliponula ferruginea (19.84%) and Apis mellifera scutellata (8.67%). The most abundant species in the surrounding of Pearl flower farm were Apis mellifera adansonii (23.67%), followed by Apis mellifera scutellata (10.64%) and Ceratina tanganyicensis (8.58%). The most abundant species in the surrounding habitats of Wagagai (Rosebud-II) were Apis mellifera adnasonii (37.25%), followed by Apis mellifera scutelatta (15.7%) and Halictus orientalis (9.59%) (Table 6).


Name of the flower farmBee species recorded around Relative abundance (%)
( individuals)

FidugaApis mellifera adansonii (Linnaeus,  1758)14.08
FidugaMeliponula ferruginea (Lepeletier, 1836)10.90
FidugaNomia brevipes (Friese, 1914)9.03
FidugaLassioglossum kampalense (Cockerell, 1945)6.92
FidugaScrapter armatipes (Friese, 1913)5.62
FidugaCeratina rufigastra (Cockerell, 1937)5.13
FidugaHalictus jucundus (Smith, 1853)4.98
FidugaApis mellifera scutellata (Latreille, 1804)3.69
FidugaCeratina whiteheadi (Eardley and Daly, 2007)3.47
FidugaPseudoheriades moricei (Friese, 1897)3.19
FidugaPatellapis flavorufa (Cockerell, 1937)3.11
FidugaMegachile torrida (Smith, 1853)2.64
FidugaMegachile rufipennis (Fabricius, 1793)2.48
FidugaAnthophora armata (Friese, 1905)2.30
FidugaXylocopa inconstans (Smith, 1874)2.09
FidugaCtenoplectra ugandica (Cockerell, 1944)2.03
FidugaScrapter flavipes (Friese, 1925)1.95
FidugaScrapter flavostictus (Cockerell, 1934)1.55
FidugaBraunsapis angolensis (Cockerell, 1933)1.49
FidugaMegachile rufiventris (Guérin-Méneville, 1834)1.37
FidugaXylocopa caffra (Linnaeus, 1767)1.37
FidugaCeratina tanganyicensis (Strand, 1911)1.19
FidugaAmegilla calens (Lepeletier, 1841)1.18
FidugaNomia bouyssoui (Vachal, 1903)1.14
FidugaPatellapis neavei (Cockerell, 1946)1.12
FidugaAmegilla velutina (Friese, 1909)1.02
FidugaTetraloniella braunsiana (Friese, 1905)0.77
FidugaNomia atripes (Friese, 1909)0.68
FidugaTetralonia macrognatha (Gerstäcker, 1870)0.60
FidugaTetralonia caudata (Friese, 1905)0.59
FidugaLipotriches dentipes (Friese, 1930)0.57
FidugaMegachile acraensis (Friese, 1903) 0.52
FidugaLasioglossum ugandicum (Cockerell, 1937)0.43
FidugaPatellapis vittata (Smith, 1853)0.42
FidugaLithurgus rufipes (Smith, 1853)0.39

Name of the flower farmBee species recorded around Relative abundance (%)
( individuals)

Mairye Estates Apis mellifera adansonii (Linnaeus, 1758)22.30
Mairye Estates Meliponula ferruginea (Lepeletier, 1836)19.84
Mairye Estates Apis mellifera scutellata (Latreille, 1804)8.67
Mairye Estates Halictus jucundus (Smith, 1853)4.44
Mairye Estates Ceratina braunsi (Eardley and Daly, 2007)4.25
Mairye Estates Amegilla calens (Lepeletier, 1841)4.17
Mairye Estates Patellapis terminalis (Smith, 1853)4.17
Mairye Estates Patellapis schultzei (Friese, 1909)4.12
Mairye Estates Lithurgus pullatus (Vachal, 1903)3.75
Mairye Estates Braunsapis angolensis (Cockerell, 1933)3.24
Mairye Estates Nomia bouyssoui (Vachal, 1903)3.21
Mairye Estates Lassioglossum kampalense (Cockerell, 1945)2.60
Mairye Estates Nomia rozeni (Pauly, 2000)1.79
Mairye Estates Xylocopa caffra (Linnaeus, 1767)1.57
Mairye Estates Tetraloniella junodi (Friese, 1909)1.35
Mairye Estates Allodape friesei (Strand, 1915)1.28
Mairye Estates Nomia lutea (Warncke, 1976)1.23
Mairye Estates Scrapter algoensis (Friese, 1925)1.20
Mairye Estates Megachile hopilitis (Vachal, 1903)1.01
Mairye Estates Tetralonia caudata (Friese, 1905)1.01
Mairye Estates Stenoheriades braunsi (Cockerell, 1932)0.91
Mairye Estates Megachile torrida (Smith, 1853)0.78
Mairye Estates Meliponula nebulata (Smith, 1854)0.71
Mairye Estates Megachile rufipennis (Fabricius, 1793)0.79
Mairye Estates Ctenoplectra armata (Magretti, 1895)0.64
Mairye Estates Amegilla acraensis (Fabricius, 1793)0.61
Mairye Estates Thyreus bouyssoui (Vachal, 1903)0.59

Name of the flower farmBee species recorded around Relative abundance (%)
( individuals)

PearlApis mellifera adansonii (Linnaeus, 1758)23.67
PearlApis mellifera scutellata (Latreille, 1804)10.64
PearlCeratina tanganyicensis (Strand, 1911)8.58
PearlCeratina rufigastra (Cockerell, 1937)4.12
PearlNomia senticosa (Vachal, 1897)5.75
PearlNomia theryi (Gribodo, 1894)5.43
PearlCeratina lineola (Vachal, 1903)3.33
PearlHalictus jucundus (Smith, 1853)2.57
PearlHalictus niveocinctulus (Cockerell, 1940)2.24
PearlAmegilla velutina (Friese, 1909)2.20
PearlLasioglossum aethiopicum (Cameron, 1905)2.00
PearlMeliponula ferruginea (Lepeletier, 1836)1.80
PearlBraunsapis angolensis (Cockerell, 1933)1.79
PearlAnthophora armata (Friese, 1905)1.73
PearlMegachile rufiventris (Guérin-Méneville, 1834)1.68
PearlNomia bouyssoui (Vachal, 1903)1.55
PearlBraunsapis facialis (Gerstäcker, 1857) 1.39
PearlMegachile junodi (Friese, 1904)1.18
PearlPatellapis vittata (Smith, 1853)1.18
PearlMegachile felina (Gerstäcker, 1857)1.15
PearlMegachile eurymera (Smith, 1864) 1.03
PearlLipotriches digitata (Friese, 1909)1.02
PearlAndrena africana (Friese, 1909)1.01
PearlPatellapis disposita (Cameron, 1905)0.99
PearlAllodape stellarum (Cockerell, 1916)0.96
PearlAfromelecta bicuspis (Stadelmann, 1898)0.95
PearlMegachile niveofasciata (Friese, 1904)0.79
PearlAmegilla acraensis (Fabricius, 1793)0.77
PearlThyreus somalicus (Strand, 1911)0.73
PearlMegachile rufipennis (Fabricius, 1793)0.70
PearlLithurgus rufipes (Smith, 1853)0.67
PearlMacrogalea candida (Smith, 1879)0.63
PearlMegachile nasalis (Smith, 1879)0.63
PearlHalictus obscurifrons (Cockerell, 1945)0.59
PearlLipotriches tanganyicensis (Strand, 1913)0.59
PearlMelitta whiteheadi (Eardley, 2006)0.58
PearlPlebeiella lendliana (Friese, 1900)0.51
PearlMelitta arrogans (Smith, 1879)0.31
PearlAmegilla niveata (Friese, 1905)0.27
PearlMelitta danae (Eardley, 2006)0.27
PearlMegachile natalica (Cockerell, 1920)0.26
PearlAmegilla rufipes (Lepeletier, 1841)0.26
PearlPlebeina hildebrandti (Friese, 1900) 0.23
PearlAllodape friesei (Strand, 1915)0.23
PearlCtenoplectra terminalis (Smith, 1879)0.20
PearlCeratina viridis (Guérin-Méneville, 1844)0.18
PearlNomia rozeni (Pauly, 2000)0.18
PearlTetralonia macrognatha (Gerstäcker, 1870)0.18
PearlXylocopa caffra (Linnaeus, 1767)0.18
PearlMegachile torrida (Smith, 1853)0.11

Name of the flower farmBee species recorded around Relative abundance (%)
( individuals)

WagagaiApis mellifera adansonii (Linnaeus, 1758)37.25
WagagaiApis mellifera scutellata (Latreille, 1804)15.76
WagagaiHalictus orientalis (Lepeletier, 1841)9.59
WagagaiMeliponula ferruginea (Lepeletier, 1836)6.63
WagagaiHypotrigona gribodoi (Magretti, 1884)8.23
WagagaiBraunsapis bouyssoui (Vachal, 1903)3.04
WagagaiCeratina tanganyicensis (Strand, 1911)2.63
WagagaiNomia atripes (Friese, 1909)1.89
WagagaiAllodape friesei (Strand, 1915)1.88
WagagaiAllodape ceratinoides (Gribodo, 1884) 1.81
WagagaiAllodapula acutigera (Cockerell, 1936)1.78
WagagaiBraunsapis angolensis (Cockerell, 1933)1.70
WagagaiNomia bouyssoui (Vachal, 1903)1.51
WagagaiTetralonia caudata (Friese, 1905)0.84
WagagaiMegachile eurymera (Smith, 1864) 0.74
WagagaiPatellapis disposita (Cameron, 1905)0.64
WagagaiMegachile rufipes (Fabricius, 1781)0.63
WagagaiScrapter whiteheadi (Eardley, 1996)0.64
WagagaiThyreus neavei (Cockerell, 1933)0.55
WagagaiMacrogalea candida (Smith, 1879)0.54
WagagaiLasioglossum ugandicum (Cockerell, 1937)0.45
WagagaiAmegilla calens (Lepeletier, 1841)0.40
WagagaiTetralonia macrognatha (Gerstäcker, 1870)0.31
WagagaiMegachile rufipennis (Fabricius, 1793)0.30
WagagaiXylocopa inconstans (Smith, 1874)0.25

Overall, high bee species richness was associated with different habitats (land-uses) found around Pearl flower farm, probably because the flower farm was young (recently established). There may be little accumulation in the environment of chemicals applied at Pearl flower farm to affect bee populations. The majority of bee species recorded were characterized by different ecological requirements. They belonged to different functional groups, but on overall most species recorded were solitary, polylectic, multivoltine, and ground nesting bees. However, high population density was observed in the less rich functional groups of species: social bees (Apini, Meliponini). In addition, a high number of nesting sites and nests was counted for various solitary bee species in the landscapes. On average, nest density (10.98 to 183.91 nests/transect) was high in rangelands/pasturelands than in agroforestry landscapes around Pearl flower farm. Few (2.5 to 5.89/transect) stingless bee nests were counted in croplands, indicating the fact that most managed and wild bee species found in the surrounding of flower farms used natural and seminatural habitats as preferential nesting sites (reservoirs). However, the different bee species used different foraging habitat types. While walking in croplands, “banana + beans-cassava” and “young fallows” were found to harbor a high number of bee foragers, whereas frequency of visitations by individual bees belonging to different bee species was intense in old and bushy fallows and in hedgerows. This indicated that the conservation of bees in the flower producing zones has to involve the conservation of seminatural habitats (hedgerows, fallows) in the surrounding of flower farms. It may be relevant to say here that both flower farm managers and small-scale farms should be sensitized about the value of conserving seminatural habitats for the maintenance of pollinators in the habitats surrounding their flower farms.

3.5. Farmers’ Surveys Results
3.5.1. Characteristics of Interviewed Farmers

Several farmers from Baganda, Bakiga, and Banyankore tribes were interviewed. Across flower farm location, the majority of respondents were females (62%), aged between 35–60 years. The main lucrative activity of these farmers was crop production, although in Ntungamo, farmers interviewed were cattle keepers (cattle keeping being the main lucrative activity and crop production being the secondary subsistence activity). The majority of small-scale farmers interviewed had a total land allocated to crop production of 0.1 to 10 ha maximum. The majority of these farmers hired or paid 1 to 2 workers and this result indicated that they had almost no labour cost. Interviewed farmers did grow various crop species in association. Most frequently, it was common to find a mixture of pollinator-dependent crops with non-pollinator-dependent crops (Table 7).


Statement no.Question: What do you think bees are doing while visiting crop flowers?Freq. (%) of the statements among interviewed people

1 Bees come and urinate on flowers of my crops; that urine makes fruits/seeds to come, a blessing from God carried out by bees 4.6
2 Bees come to facilitate marriage of my crops 0.8
3 Bees and other pollinators facilitate the marriage of flowers 2.3
4Bees are just visiting my crops to get nectar only1.5
5 Bees bring wild pollen (“Ngwaso”), drop them onto flowers to enable flower to open and give fruits/seeds 3.8
6 Bees come to drink water and collect other foods I do not know 11.5
7 Bees come to my crops to do the natural job of fertilizing my crops as God created them for that job 5.4
8 Bees come, bust, and later fertilize the flowers of my crops 3.1
9Bees comes to take pollen/nectar from crops to their hives because they are pests (thieves), and of what they take, my crop miss it0.8
10Bees fall on flower of my crops, eating from there and later I get fruits/seeds 1.68
11Bees fertilize my crops by transporting pollen between male and female flowers3.1
12Bees fertilize my crops, but wind can also fertilize my crops if bees do not come, so I am not bothered5.4
13Bees get nectar from my crops, they help us to get better yield and help themselves2.3
14Bees just come to drink juice from my crops but they do nothing good or bad on my crops2.3
15Bees just take pollen (“ebivu”) from flowers, go away, and disseminate these pollen on other plants in forests8.5
16 Bees must visit flowers of my crops to get good yield (seeds/fruits): rules of Nature and God0.8
17Bees pollinate on my crop for good growth and good seeds/fruit1.5
18 Bees provide a two-way benefit (collect nectar for their hives and bring pollen to my crops)0.8
19 I do not know (I cannot tell)1.5
20 I do not know but was told in a workshop that bees have to pollinate my crops for good yield1.5
21 I see bees visiting flowers of my crops but I do not know what they are after on my crops 2.3
22 I still do not know/understand what bees bring to my flowers to enable me to get better fruits/seeds0.8
If bees fall on flowers of my crops, I will see fruits/seeds coming in 1 to 3 weeks 14.6
Just playing (they do nothing valuable) 3.8
They pollinate most of the crops I grow 5.4
They come to fertilize crop flowers 3.8

Chi-square test for difference in knowledge of what bees are after on crop flowers: , , , .
3.5.2. Farmers’ Knowledge of Pollination, Pollinator Groups, Pollination Processes, and Value of Pollinating Services to Their Crops

The percentage of farmers understanding the word pollination (those knowing different pollinators of their crops) increased and was significantly () positively related to (a) the education level of the farmer (number of years schooling), (b) the age of the respondent, (c) the number of years the farmer has been growing pollinator-dependent crops among those interviewed, (e) the total land allocated for crop production by a farmer, and (f) the proportion of rich farmers in the village (community) among those interviewed (Figure 5). Surprisingly, there was a negative relationship between the number of rich farmers and knowledge about pollination (Figure 5(f)).

When asked the question, do you know or understand what we mean by pollination?, the percentage of farmers saying they understand what pollination means was of 80% against 20% who said they did not understand or know what pollination means ( 1 df = 36.56, ). When asked to name 1 to 6 species of pollinators they knew and saw visiting the flower of their crops, approximately 5%, 37%, 38%, 14%, 4%, and 2% of farmers interviewed declared knowing (were able to name), respectively, at least 0, 1, 2, 3, 4, and 6 bee species/groups ( 1 df = 85.129, ). But, when asked to describe the types of pollinator/bee groups (species) they see visiting flowers of their crops, interviewed farmers had significantly ( test, ) correct knowledge of more than 2 pollinator groups. Farmers (14.1–19.3%) knew honeybees, Xylocopa (“Civuvumira” in local language: Luganda) and stingless bees (“Kadoma” in local language: Luganda) as the frequent flower bee species/groups of their crops (Figure 6).

There were significantly (, test) different farmers’ perceptions on roles played by bees in crop flowers. When asked about what they think bees are doing on flowers of their crops, farmers provided different responses. Most frequent statement (14.6%) from farmers was that they believed that if “bees fall on flowers on their crops, they will see fruits/seeds coming in 1 to 3 weeks.” Other farmers (11.5%) believed that “bees come to drink water and collect other foods on their crops.” In 0.8% of frequency of statements, some farmers believed that “bees come to facilitate marriage of their crops.” However, some farmers believed that bees were just playing with flowers of their crops and doing nothing valuable for their crops (Table 7). When asked the question: “is crop pollination by bees important in your crop production?”, 73.9%, 9.9%, and 16.2% ( 2 df = 74.81, ) of farmers declared, respectively, that they believe (i) bees are important, (ii) they are not important, and (iii) they are not sure if bees are important in their crop production activities. More frequently, farmers reported that they “think crop pollination by bees is important in their farming business because they frequently believed (8.15%) that “with bees, they will get honey and they are convinced that if no bee-visits, there is no yield from their crops” (Table 8). Farmers who grow vegetables and fruits had higher understanding of pollination than those who grow legume, cereals, root, and tubers. Other farmers said bees contribute little and for them they are aware that bees that visit their crops come from community hives and or from surrounding forests and lake edges/wetlands; but for them they are convinced that “if no bees visiting crop flowers, wind & other insects will still pollinate and they will still harvest something.”


Statement no.Question: Why do you think crop pollination by bees is important in your farming business?Freq. (%)

1Bees are important for honey production and for pollinating flowers of my crops1.48
2I know bees collect only their nectar but I am not sure if they do anything beneficial to my crops1.48
3I know no bee-visits, no yields. Please teach me how to make a home for them near my crops0.74
4 I was told by extension workers and neighbours to care for bees because if no bee-visits, no fruit/seeds I will harvest and sell, yet I need money to pay school fees 8.15
5If bees fall on flowers of my crops (avocado), I see a fruit coming; cropping is my business and bees help me free0.74
6Bee visitation to coffee has no value; they add nothing, whether they come or not, my coffee will set fruits0.74
7 Bees are important because if no bee-visits, no yields I get at all 7.41
8 Bees are important to get honey and also if no bee-visits, no fruit/seed I get from most of my crops 8.15
9 Bees are important because I have seen that no bee-visits, no fruits on all crops I grow 2.22
10 Bees are important and visit my commercial and vegetable crops; but I ask myself a question, where do they sleep? 2.96
11Bees are important for my pulse crops, I need to know how to build a small house for them so that they stay near 0.74
12When building a house for wild bees, how should it look? Like a beehive or like a rat hole?0.74
13 Bees are important because all flowering plants/crops on this earth want bee-visits to perpetuate well 2.96
14Bees are important for honey production and for pollinating flowers of crops I feed on and make money from0.74
15Bees are important for honey production and for pollinating flowers of my crops, especially crops wanted at market1.48
16 Bees are important for pollinating our crops and they provide honey, wax, propolis, candle 5.19
17 Bees are important to help make my crops grow and get better yield;they do free work 2.22
18 Bees get nectar from my crops, but they bring manure from the hive to make turn into seeds/fruits 5.19
19By field experience, I know no bee-visits, all flowers will die off, no fruits/seeds will come out1.48
20Either bees visit my beans/peas or not, I will still get my 5 to 12 pods per plant (bees have no value to my crops)0.74
21Either bees visit my beans or not, I will still get my 5 to 12 pods per plant (bees have no value to my crops)1.48
22Every time bees fall on flowers of my crops (avocado, mango), few days later, I see a beautiful fruit/seed/pod coming; no hunger at home in the future0.74
23If there are few or no visits of my crop flowers, I get no or poor yield0.74
24For most fruit crops (mango, avocado, papaw) I grow, they have to get pollinated by bees to get sweet fruits and high yields competitive in the markets0.74
25From my observations if no bees visit flowers in the village abundantly, no pods on my bean plants 0.74
26 I know without bee-visitations to flowers I can not harvest. However, I do not know where they come from or sleep; with bee-visits, I get fruits most wanted at market by my customers 2.96
27 I know, no bees, no harvest. However, I do not know how to rear and make them many in my crops 2.22
28 I am not sure if bees are important in crop production business (for my crops) 11.11
29I know from my grandparents that no bees (pollinators) visits, no single mango fruit I will get acceptable at market0.74
30 I know they are important but can not explain why it is only after their visit that I see fruits/seeds coming? 2.96
31I see bees visit my coffee flowers but I do not know for which purpose apart from feeding there0.74
32 I see bees visit my avocado/coffee flowers but I donot know what do they bring to my flowers to get exciting fruits/seeds 2.22
33I was told by my neighbours by extension service agents that if no bee-visits to my crops, no yield at all but I can not explain why0.74
34If bees fall on flowers of my crops (avocado), I see a fruit coming later and that fruit is wanted at market and if children feed on it, they grow well because it is rich in vitamins, hence no stunting of children in my family1.48
35If no bee-visits, no yields; however, I do not know where they come from (sleep)0.74
36 Important because all the crops I grow need bee-visitations, even flowers of my cassava 5.19
37 My crops have to get high bee-visitations, otherwise they will not yield properly well 2.96
38No mango fruits or bean seeds I get if no abundant and diverse bees flying around in the village, if you feed on fruits not visited by bees, you fall ill1.48
39The more bees fall on my (avocado/watermelon/pumpkin/tomato) flowers, the more fruits I get in my bag Fruits/seeds that were obtained after bee-visits last longer and are attractive to customers at local market1.48
40The more bees fall on my crop flowers, the more fruits/seeds I get1.48
41Without bees, no farmer can harvest in our village0.74
42Yes, if no bee-visits happen/occur to flowers during the blooming season, no yields I will get0.74

Chi-square test for difference in knowledge of what bees are after on crop flowers: , , , .

When asked “how much do you think bee-visitations to flowers of your crops contribute to crop yields?”, approximately 23 to 28% of farmers perceived significantly ( test, ) that bees contributed, respectively, to half (41–50%) or to third (26–40%) of yield increase of crop yields in their villages (Figure 7). In fact, there were significant differences ( test, ) between the average pollination experimental data [21, 22] and the farmers’ perceived contribution of bees to yield of different crops such as beans, citrus, coffee, cowpea, mangoes, passion fruit, and pepper (Table 10). In most cases, farmers guessed little value as compared to the pollination experimentally derived data [2123]. For other crops (avocado, egg plant, watermelon, tomato, etc.) farmers perceived the value of the contribution of bees to yield that was statistically ( test, ) similar to the one that was derived empirically after conducting field pollination experiments (Table 9) by the author.


Crop 
categories
Crops 
reported
Yield 
parameters
YNFBV 
(Mean ± SD)
YHBV 
(Mean ± SD)
A = Fruit/Seed
set (%)
B = Fruit set (%)
Experimental data (2007)
Statistics for difference in fruit set between A and B

FruitsAvocadoNbr fruits/branch 57.4582.674.539310.033
PulsesBeansNbr pods/plant 77.9527.11 24.6022 <0.001
FruitsCitrus-lemonNbr fruits/branch 83.4324.65 31.9679 <0.001
FruitsCitrus-orange Nbr fruits/branch 70.4732.23 14.2385 <0.001
IndustrialCoffea arabica Nbr berry-fruits/branch 59.2662.120.0673890.795
IndustrialCoffee robustaNbr bags of coffee beans/ha 51.7568.712.3878690.122
IndustrialCoffee robustaNbr berry-fruits/branch 53.8678.32 4.52634 0.033
PulsesCowpeaNbr pods/plant 74.5145.43 7.05058 0.008
VegetablesEgg plant Nbr fruits/plant 59.7341.653.224370.073
PulsesGroundnutNbr pods/plant 72.8568.550.1307640.718
FruitsMangos Nbr sacs of 100 Kg/tree 33.2183.87 21.9204 <0.001
FruitsMangosNbr Kg fruits/branch 60.0529.34 10.5504 <0.001
FruitsPapaya Nbr fruits/plant 69.8131.55 14.4419 <0.001
FruitsPassion fruitNbr fruits/plant 22.1078.98 32.0077 <0.001
PulsesPigeonpeas Nbr pods/branch 66.2865.720.0023760.961
PulsesPeas Nbr pods/plant 72.2165.410.3359980.562
VegetablesPepperNbr fruits/branch 67.8719.89 26.2315 <0.001
Fruits“Prune” Nbr fruits/branch 100.076.543.117550.077
FruitsPumpkinNbr fruits/plant 100.082.211.736920.188
PulsesSimsim Nbr pods/plant 84.171.670.9918780.319
IndustrialSunflower Nbr seeds/head 69.4769.770.0006460.98
VegetablesTomato Nbr fruits/plant 43.0637.540.3780450.539
FruitsWatermelon Nbr fruits/plant 100.079.432.358160.125
FruitsAppleNbr fruits/branch 100.078.452.602420.107

Legend:
YNFBV: When no/few; YNFBV: yields when very few or no bees visit my crop flowers (bad yield).
YHBV: When I receive high bee-visits to crops; YHBV: yields if bees came with high visitation frequency to flowers of my crop.
A: (Fruit/seed set in %) = (mean YHBV − mean YNFBV)/mean YHBV   *  100.
B: (Fruit/seed set in %); this is data obtained after conducting pollination experiments.

Statement no.Question: Where do you think bees are abundant, near the flower farm (0.1–0.5 km) or further (>2 km) in the village?Freq. (%)

I have no idea but think bees should be many in the villages where there are abundant flowers for them 11.5
1 Bee populations should be high up-country than near the flower farm with toxic chemical sprays they use 2.3
2 Bees are many in the village (>2 km far from the flower farm) and no bees will stay near chemicals 4.6
3 Bees are many in the village (>2 km far from the flower farm), everywhere where wild/crop flowers are freshly/abundant 3.8
4 Bees are many in the village because we have abundant flowers there than near the flower farm with toxic fumes 2.3
5Bees are many in the village compared to near (edge) the flower farm0.8
6 Bees are many in the village (>2 km) because they spray daily near the farm and bees can not survive there 14.5
7 Bees are many in the villages (in every place where there are many flowers, bees will be there) 3.1
8 Bees are many in the villages because they have no enemy there, they are free to go everywhere in the village 2.3
9 Bees are many of course in the village (>2 km far from the flower farm) 8.4
10Bees are no longer many in the village because the flower farm is killing them with the toxic sprays they make every day1.5
11Bees are not strong like humans, if they smell the fumes from the flower farm when foraging, they end up dying in their nests 0.8
12 Bees are obviously many in the village with fresh air, not polluted by toxic chemicals of flower farms 3.1
13 Bees are still many in the village compared to near the flower farm where nesting sites have been destroyed 5.3
14Every bee flying for forage from the village to the edge of the flower farm will die there because of too many pesticides there1.5
15 I am not sure (I cannot tell with confidence where exactly) 5.3
16 I am not sure if bees are many in the village (>2 km) than near the flower farm but I see few bees on gardens located in the proximity of flower farm (0.2 km) 3.8
17 I cannot tell exactly but I think they should be many in the village where healthy-non-polluted wild flowers are 3.1
18 I donot know; I cannot tell; I am not sure (I cannot even guess) 18.3
19Obviously bees are many in the village than near the flower farm where they spray a lot1.5
20Pesticides have a long-persistence smell near the flower farm so bees will die there quickly1.5

Chi-square test for differences in beliefs of farmers about area where bees are abundant: , , , .
3.5.3. Farmers’ Knowledge and Perception of Drivers of Bees in Villages Immediately Surrounding Flower Companies

When farmers were asked to explain where do they think bees are abundant between the edge of the flower farm (0.01–0.2 km) and far away (>2 km) in the village, most (90%) farmers believed that bees should be abundant in their villages since the “fumes” or chemicals sprayed daily inside greenhouses of the flower farms will not reach at such distance (>2 km) (Table 10). Some villagers frequently stated that bees were many in the village (>2 km far away from flower farm) because “bees cannot survive where they spray daily toxic chemicals.” However, the answer “I do not know, I am not sure, I cannot tell” was frequently given by farmers (18.3% of frequency) and this indicated that some farmers were not good naturalists or had almost no interest in understanding the work of bees in their farming business. Different justifications (reasons) for getting higher yields far away from the flower farm were given, but must frequently, farmers believed that higher yields can only be due to difference in field management systems, fertility levels, types of varieties grown, and to difference in bee-visitations (Table 11) because bee-visitations are almost absent near the flower farm where they apply toxic chemicals.


Statement no.Question: Have you observed any changes (reduction, increase) in crop yields in the village over the last 5 to 20 years?Freq. (%)

1 Yield of crop is also reducing in the last 10–20 years. I think it is because; soil is old/currently infertile in our area 5.38
2Changes in crop yield may be due to infertility of the lands and to flowers fumes0.77
3 I have not yet observed changes (reduction/increase) in my yields of crops 8.46
4 I have observed changes (reduction) in yields for the last 5–10 years 5.38
5 I have seen some change these days (reduction) in yields of many crops although I donot know the exact causes 8.46
6No change, for me, yield is increasing because I live far from the flower farm and I manage well my gardens1.54
7No changes (reduction), instead I see increase because I do fertilization with cow dung to increase my yield0.77
8 No changes (reduction) in yields apart from thieves in the villages 2.31
9 Not sure (I can not tell) 20.10
10There has been change (reduction) and this may be linked to practice of bad farming methods1.54
11There has been changes in yield of many crop species for unknown reasons of changes in the global system0.77
12There have been drastic changes (reduction of 50 to 80% compared to previous harvests) in most of the crop yields I grow3.08
13There is a general decrease in yield of all crops we grow but I think it may be due to soil/land infertility0.77
14 There is a change (reduction) and bad yields are due to soil infertility, excess sunshine/rains, and climate change 4.62
15 There is a change (reduction) in crop yields but do not know what it is due to exactly 3.08
16Yes, there is a change (reduction) in yields over time but I can not explain clearly the changes are due to what exactly0.77
17There is a change in yields probably due to soil infertility because I have over-used the land to grown different crops over years1.54
18 There is a reduction in yield due to over-use of soils, growing crops/bad varieties in a wrong season, no respect of growing seasons 3.85
19There are changes (reduction) in yields probably due to soil infertility of my gardens and to fumes from flower farms0.77
20There is yield reduction because bees are disappearing in the village due to chemical sprays from the flower farm6.15
21 There is very little change (decrease)/to not much changes in yield of my crops 14.62
22Yield of crops has reduced in the village over the last 5–20 years but I do not know why5.38

Chi-square test for difference in arguments (statements) frequency: , , , .

When asked if they have ever observed any changes (reduction, increase) in crop yields in the village over the last 5 to 20 years, and if yes, this may be due to what farmers perceived as significant ( test, ) changes (reductions) in crop yields during the last 5–20 years for various reasons such as soil infertility of their lands (Table 11). The presence of the flower farm spraying chemical toxic pesticides nearby and environmental degradation were key reasons provided by farmers even when some farmers said that there has been little change (14.62%) while most farmers (20.10%) said they were not sure if change has ever happened or affected crop yields in their villages (Table 11).

When farmers were asked if they have seen any change in the population density (abundance) of bees in the village, most farmers were not sure if there has been change. Farmers who believed in changes attributed that to declining in beekeeping, “flower fumes”, bad farming practices, or forest bush clear-cutting (Table 12). When asked if they felt that bee populations have been stable or changing (increasing/decreasing) over the last 5 to 15 years in their village landscapes, there were various answers (perceptions) among farmers. Most (45%) of farmers perceived that bee populations have been reducing (declining) seriously in their villages in the last 5 to 15 years. Some farmers (32.1%) were not sure or had no idea (they did not know anything) whether changed has occurred or not. A few farmers (19.8%) said they perceived no changes while only 3.1% of these respondents felt that there has been an increase of bee populations in the village over the last 5 to 15 years. The difference in perceptions among the four categories of respondents was significant ( 3 df = 38.367, ).


Statmenet no.Question: Have you observed any changes in bee populations (abundances) in the village over the last 5 to 20 years? It is because of what?Freq. (%)

Not sure if there has been strong changes in bees, but I watch few bee-visits (I see few bees feeding) in my farm these days 8.40
1 I have observed no reduction in bees in the village; there are enough hives, wild nest sites, and food plants for bees 5.34
2 I think bees are reducing in the village because of too much pollutants and toxic chemicals applied in the flower farm around there 3.05
3 Not sure if any change has occurred because I donot know how many bees were there before compared to now 6.11
4Bee populations are declining over years because many termite mounds and tree/stamps where bees used to nest have been destroyed.0.76
5 Bee populations are declining in the village over the years because beekeeping is also declining in the village (few hives in the village) 2.29
6 Beekeeping attracts all wild bees to hives and concentrates them where the hives are placed, so they will visit only that area, then we shall think bees have disappeared 3.05
7Bees have been reducing in the village over the last 5–10 years, but I do not know why Maybe you can tell me more about it0.76
8Bees are increasing these days because we have planted many flowering trees and shrubs they are interested in1.53
9Bees are increasing; they are many in all bushes in the village, even in crops, I see many these days1.53
10Bees are no longer coming on my crops (beans) these days and I do not know why0.76
11Bees are reducing because many beehives/wild nests have been destroyed 5–10 years ago with crop production intensification due to too many children we are producing these days0.76
12Bees are reducing because the flower farms do not want bees, any insect around their flower farm is killed0.76
13Bees are reducing because the crop varieties we grow these days are noninteresting foods for bees anymore. No good scents of flowers to attract bees0.76
14Bees are reducing because may be these days we are growing crops that produce noninteresting/attractive flowers to bees0.76
15Bees are reducing because we have destroyed underground nests of wild bees and we are cutting trees to make charcoal0.76
16Bees have been reducing in the village over the last 5–10 years, but do not know why May be you can tell me more about it because you stay with people who know things than us0.76
17Bees have been decreasing because no abundant hives in the village these days0.76
18 Bees have drastically reduced; they are few these days because farmers are cuttingoff all flowering herbs/weeds near fields (bad farming practices) 3.05
19 Bees have reduced because many of them are dying in the village after smelling the toxic fumes of the flower farm 3.05
20Bees have reduced because the flower farm has killed them with their toxic sprays from the flower farm in the surroundings0.76
21Bees have reduced because the flower farm sprayed everywhere at night and their fumes chased away all bees0.76
22Bees have reduced ever since the flower farm came around here, no more bees come to my crop flowers1.53
23 Bees number have drastically reduced (e.g., could count around 100 bees/ in the bean field, these days I count less than 10/ ) 3.05
24Bees reduced because no abundant bees coming to the village these days compared to a previous time when I was young0.76
25Bees used to be many in the village (5–20 years ago), these days, they have reduced I do not know why0.76
26Changes (reductions) came with human population increasing (pressure), destroying nesting sites (habitats) of bees to grow crops0.76
27 Drastic reduction in bees occurred because people have cleared all bushes and forests for livestock/crop productions intensification 3.05
28 I am not sure if bees have reduced/increased in the village, I have no interest in bees 2.29
29 I am not sure, I have never paid attention (no curiosity) to observe change in bee populations 1.53
30I cannot explain (do not know) why bee populations are reducing in the village these days0.76
31I do not know, I think bees will be every where because there are tasty/fresh flowers in the village0.76
32 I have observed no changes in bee populations in the village since my childhood up to now, it is the same thing I see 3.82
33 I have never paid attention (no curiosity) to observe changes in bee populations 4.58
34 I have no idea if bees have reduced (declined) or not; I will start making my observations from today in many gardens 6.87
35 I have observed no changes in bee numbers these days; in fact, there are many coming to visit flowers as usual 6.11
36I see no change in bees numbers in the village because we have even received beehives from NAADS; numbers are increasing these days0.76
37I used to see 2-3 colonies moving (flying around/month) in the village, these days I see one colony flying-out around our villages once a year0.76
38I used to see bees hovering cups, saucepans left outside, these days, no bees come to visit my cups left outside, only flies and ants0.76
39I used to see many bees flying around/feeding on flowers in my fields; but since the flower farm came, I see few or no bees at all1.53

Chi-square test for differences in explanations about causes of changes in bee numbers: , , .

Also, when asked if they felt that crop yields have been stable or changing (increasing/decreasing) over the last 5 to 15 years in their village landscapes, most (48.3%) of the farmers perceived that crop yield has been reduced by 10–50% in their villages in the last 5 to 15 years. Some farmers (17.8%) felt that crop yield has been stable. Another group of respondents (18%) perceived that they were not sure (they could not tell) if change has occurred or not. A small portion of respondents (6.1%) perceived that crop yield has been increasing slightly in the 10 to 35% proportions. Approximately 3.8% of respondents perceived that crop yield has increased in the 40–85% proportion while another small group of respondents (6%) perceived that crop has declined seriously by 50 to 85%. The difference in views/perceptions among the 6 groups of respondents interviewed was significant ( 5 df = 7.87, ). Overall, when asked if the currently observed changes (reductions) in crop yield are a consequence of reduction in bee populations in the villages, most farmers perceived that there has been a reduction in crop yield as a consequence of the decline in bee populations in the villages (Table 13).


Statement no.Question: Have you observed any changes (reduction, increase) in crop yields in the village over the last 5 to 20 years?Freq. (%)

1 Yield of crop is also reducing in the last 10–20 years, we think it is because soil is old/infertile in our area 5.38
2However, changes in yield may be due to infertility of the lands and to flowers fumes0.77
3 I have not yet observed changes (reduction/increase) in my yields of my crops 8.46
4 I have observed changes (reduction) in yields for the last 5–10 years 5.38
5 I have seen these days some change (reduction) in yields of many crops although I donot know the exact causes 8.46
6No change, for me, yield is increasing because I live far from the flower farm and I manage well my gardens1.54
7No changes (reduction), instead I see an increase because I do fertilization with cow dung to increase my yield0.77
8 No changes (reduction) in yields apart from thieves 2.31
9 Not sure (I cannot tell) 20.10
10There have been a change (reduction) and this may be linked to practice of bad farming methods1.54
11There have been changes in yield of many crop species for unknown changes in the global system0.77
12There has been drastic changes (reduction of 50 to 80% compared to previous harvests) in most of the crop yields I grow3.08
13There is a general decrease in yield of all crops we grow but I think it may be due to soil/land infertility0.77
14 There is a change (reduction) and bad yields are due to soil infertility, excess sunshine/rains, and climate change 4.62
15 There is a change (reduction) in crop yields but do not know what it is due to exactly 3.08
16There is a change (reduction) in yields over time but we can’t explain clearly the changes are due to what exactly0.77
17There is change in yields probably due to soil infertility because I have over-used the land to grow different crops over the years1.54
18 There is areduction in yield due to over-use of soils, growing crops/bad varieties in a wrong season 3.85
19There are changes (reduction) in yields probably due to soil infertility of my gardens and to fumes from flower farms0.77
20There is yield reduction because bees are disappearing in the village due to chemical sprays from the flower farm6.15
21 There has been very little change (decrease)/to not much changes in yield of my crops 14.62
22Yield of crops has reduced in the village over the last 5–10 years but I do not know why5.38

Chi-square test for difference in arguments (statements) frequency: , , , .

When asked if they believed that if “crop yield reduction/loss was linked to decline in bee populations in the village”, there were different statements given by farmers (Table 14). Overall, 35.4% of respondents were of neutral views, 39.2% disagreed, and 25.45% agreed. The difference in views between the 3 categories of respondents (neutral, disagreeing, agreeing) was significant ( 2 df = 3.056, ). In fact, around 58% of farmers interviewed believed that growing crops far away (>2 km) from the flower farm was a better option to obtain higher yields even when some farmers (22.9%) believed that it should be similar yields. Only a few farmers (1.5%) believed that the one growing crops at (0.1–0.3 km) the edge of the flower farm could get better yield. A small proportion (17.6%) of farmers stated that they were not sure (they did not know). The difference in views/perceptions of the 4 groups of respondents was statistically significant ( 3 df = 68.032, ). Overall the majority of farmers doubted negative effects of the proximity to the flower farm on yields of their crops.


St. noQuestion: Do you think (agree/disagree) that changes (reductions) in crop yields are associated with changes (decline/loss) in bee-visitations? Why not?Freq. (%)

1 I am not sure and do not know, someone should explain to me why there is too much yield reduction these days in our village2.3
2 I am not sure (I have no idea at all and cannot even speculate or guess)8.5
3 Because most of our grown crops need bees, if bees are few in the village, then low yield obviously is due to that 14.6
4 Change (reduction) in crop yields over time is due to the fact that FIDUGA dumped toxic chemicals around our villages1.5
5 Change (reduction) in yields can only be related to thieves of my harvests3.8
6 Changes in yield may be due to land infertility/degradation and fumes from the flower farms0.8
7 Changes in yields are due to lack (reduction) in bee population in the village because all crops I grow need bees to fertilize them1.5
8 Changes in yields are due to lack (reduction) in bee population in the village because all crops I grow need bees to fertilize them0.8
9 Currently observed yield loss (reduction) in many crops is due to pests/diseases emergence but not at all to decline in bees1.5
10 I am not sure if change in yield can be associated with decline in bees, I need someone to explain to me how 8.5
11 I can't relate yield reduction to loss of bees because in the village, their habitats (nests) are still many 3.1
12 I do not think low yield is linked to reduction because theses days yield reduction is generalized in all crops even in those
that don't need pollinators to yield better
5.4
13 I don’t agree/believe that low yield is due to lack (low) of numbers of bees in the village2.3
14 I don't think the changes (reductions) in yield are due to few bees currently seen in the villages0.8
15 I have no idea if they have changed or not 11.5
16 No, I think yield reduction is due to drought and climate change, but not to low bee-visitations or lack of bees in the village1.5
17 Not sure (I donot believe low yield is due to absence or low bee-visitations to my crops) 4.6
18 Reduction in coffee/beans yields may be due to climate change and to diseases/pests emergency 3.1
19 The change (reduction) in yield is due to change in rainfall pattern prevalence infertile soils, but not due to bees reduction in the village 3.1
20 The change (reduction) in yields is only associated with low rainfall, these days, we receive little rainfall that can help get good harvests 3.8
21 The change (reduction) in yield is due to chemical sprays of the flower farm that have killed bees and then we get little yield 5.4
22 There have been changes in yields of many crops but I don't believe low yields is due to lack of bees2.3
23 There is little harvest these days because there is not much rainfall coming these days1.5
24 Yield reduction is due to interacting factors (including chemical, poor farming methods) leading to reduced bee-visitations to flowers of our crops 6.2
25 Yield reduction is due to the fact that NARO (agricultural research institute) has released crop varieties that are very susceptible or contain pests/disease germs in the village1.5

Chi-square test for difference in statement frequency: , , , .

When asked to guess the place where someone can get better yield between near the flower farm and far away >2 km) from the flower farm, most farmers were not sure (10.9%), while others stated that there should be no difference in yield (11.6%). A small proportion of farmers felt that yield will be higher in the villages (>2 km far away) because the fumes of the flower farms do not reach over there (Table 13).

When farmers were asked to say when they started observing changes (in bee populations/crop yields) in their villages the majority of farmers (22.3–44%) believed there has been significant ( test, ) changes (reductions) occurring in either crop yields or bee populations. However, some farmers (29-30%) believed that changes in bee populations started occurring some 5 to 10 years ago (Figure 8).

Several drivers of bees in farmlands have been identified worldwide. During discussion meetings, farmers were asked to name key factors likely leading to the current ongoing bee loss in their villages. These drivers were put together on a paper and farmers were again asked to rank them in terms of importance from the most important (dangerous) to the less important factors that may be associated directly/indirectly with bee loss in the village. There were variations in assessment (ranking) of drivers by farmers from the four study districts (where the 4 flower farms are located). However, on average, all farmers ranked as significant (, Kruskal-Wallis test) primary drivers the following drivers: (i) fragmentation of national habitats such as forests/wetlands (average rank: 1.90 ± 0.13), (ii) forests/bush clear-cutting in the village (average rank: 1.26 ± 0.002), (iii) logging, charcoal burning, timber/poles/firewood collection (average rank: 1.26 ± 0.02), (iv) fires burning intensification (1.69 ± 0.04), and (v) local climate change such as rainfall pattern changes (1.84 ± 0.002).

Some worldwide documented key drivers of bee biodiversity loss (road construction up-country, land-use change, global climate change, environmental/degradation, grazing intensification, and agriculture modernization plan by the government) were perceived by local farmers as factors playing a tertiary role or as factors playing no role in the decline process or as factors having nothing to do with bee decline in the villages. Most farmers said they were not sure if these factors could affect bees even when a few of them believed that these factors could be associated to some extent with bee disappearance in the villages (Table 16). There was a great variability in perception of farmers concerning the place (area) where to get better yield between the near and the far areas to the flower farm (Table 15).


Statement No.Question: Who can get higher yields between the one growing close to the flower farm compared to the one growing crops far away (>2 km) and why? (all growing/environmental conditions are standards and similar)Frequency (%)

1 I am not sure (I do not know) 10.9
2 I am not sure if the distance has an effect on yield but difference in yields can be due to varieties, age of plants, and fertility conditions2.3
3 I know, I will get higher yield at >2 Km far from the flower than growing near it, but I still cannot explain why2.3
4 No difference in yield and if there exist differences, it depends on good care and management of crops and fields 3.9
5 The same yield everywhere (I see no reason for difference in yields), there should be no difference in yields 10.8
6 The yield is high in the village because of difference in fertility levels of fields1.6
7 There should be no difference in yields but difference can be due to difference in fertility levels of the fields 11.6
8 Definitively, mangos/avocado will yield more in the village because bees have been killed near the flower farm 7.8
9Digging at the edge of the flower farm with toxic fumes, you must get no (low) yields 2.3
10Even when the level of fertility of the soil is the same, yield will still differ (being high in the village) but I do not know why?1.6
11Growing crops near flower farm, no yield because no bees; but in the village there are some bees, flies, and wasps to pollinate my crops 1.6
12Higher yields are in the village because we pose no harm to bees in the village but the flower spray alot to chase them away1.6
13Higher yields are in the village because soils are fertile there and people care more for their crops up there0.8
14 I am not sure if someone who grows coffee faraway from the flower farm will harvest more than me 4.7
15I can harvest more in the village than near the flower farms, I am sure 0.8
16I think it should be the same yield if all variables and growing conditions (rainfall, management, bee-visits, soil, and fertility levels) remain the same over time0.8
17 I think the one who grows far away will get higher yield even if I donot why 3.1
18 I will get the same yields if we receive the same quantity of rain 4.7
19If everything is constant at all farms, the yield would be the same, I see nothing bringing a difference0.8
20No difference in yields, but if it exists, it can only be due to bad weather, infertility of soils, management techniques, and planting bad varieties 1.6
21Similar yields if we manage fields equally2.3
22 The yields will be different since we have different levels of weed management system/soil fertility/bee-visitations and thus bee-visitations will be different and consequently yield different 3.9
23Higher yields are in the village due to different levels of fertility, management, and bee-abundances compared to flower farm edge where bees are continuously killed3.1
24There will be higher yields in the village because there are many bees to enable getting better yields than near the flower farm0.8
25 Yields near the flower farm cannot be similar to that in the village (>2 km) because growing conditions are not the same 3.9
26Yields will be higher in the village because of high fertility levels in the village1.6
27Yields will be higher in the village probably due to difference in environmental conditions and not due to difference in bees1.6
28 Yields will be high in the village because there are many bees at >2 km far from the flower farm 7.0
29Yields are high in the village (>2 km) because polluted water from the flower farm is not running up there to kill crops and bees are not drinking polluted water here0.8


Type of drivers/pressures/disturbances of pollinatorsWagagai MairyeFiduga PearlOverall mean    Kruskal-Wallis test
Mean ± SEMean ± SEMean ± SEMean ± SE Mean ± SE (adj)

General land-use changes/shifts pattern 381.71<0.0001
Fragmentation of natural habitats (forests, wetlands) 388.78 <0.0001
Loss/degradation of semi-natural habitats (hedges, grasslands) 379.51<0.0001
Forest/bushes clear-cutting in the village 362.44 <0.0001
Logging, charcoal burning, timber/poles/firewood collection 365.13 <0.0001
Forest habitats conversion into grazing fields/crop fields 388.82 <0.0001
Over-harvesting of specific resources in the forests 376.48 <0.0001
Agriculture modernization plan by the government 316.270.001
Cultivation intensification (cropping intensification) 363.92 <0.0001
Indigenous/native trees cutting/degradation in villages 388.92<0.0001
Intensification of farm management practices 389.07<0.0001
Increasing application of pesticides/other agrochemicals 374.56 <0.0001
Grazing intensification 373.38<0.0001
Fires burning intensification 380.11 <0.0001
General environmental pollution/degradation 361.61<0.0001
Decreased/degradation of floral/nesting resources diversity 391.04 <0.0001
Alien invasive species spread in the village 364.23<0.0001
Cultivation of exotic high yielding varieties/genotypes 390.85 <0.0001
Bee diseases/parasites and predation 394.22 <0.0001
Increasing urbanization of rural towns 383.85<0.0001
Road construction 36.890.075
Demographic pressures (human population increase, refugees migration) 314.670.02
Natural calamities (landslide, river floods) 376.73<0.0001
Research and tourism (wildlife visits) intensification 367.15 <0.0001
Local climate change (rainfall pattern changes) 360.58 <0.0001
Regional and global climate changes 377.20<0.0001

Ranks: 1: very important (or primary causal) agent; 2: important causal agent; 3: associate (secondary) important causal agent, 4: playing tertiary role; 5: play very little or no role in the decline process; 6: has nothing to do with bee decline (not sure this can affect bees).

Farmers were requested to relate the rate of disappearance of bees due to degradation of natural/seminatural habitats; and it was observed that only old farmers (aged 70–80 years) think/perceive that forests and other good seminatural habitats disappeared 10–50 years ago. Old farmers perceived also that in areas covered by forests, it is possible to observe visits of bees to crop flowers at the rate of 500 bee-visits/10 min/50 m2 garden plot. Young people (20–35 years old) perceived that forests disappeared in the villages some 5–10 years ago and that bee-visits to crop do not exceed 20 bee-visits/10 min observations/50 m2 garden plots (Figure 9) even in regions covered by forests or plenty of seminatural habitats.

3.5.4. Farmers’ Attitudes towards Flower Industry Growth and Development in the Surrounding of Their Villages: Perceptions of the Negative Effects of Flower Industries on Environmental, Human, and Agricultural Health

When asked about the benefit of living near the flower farm, most (66%) respondents significantly ( test, ) declared (stressed) gaining no benefit (advantage) by having their homesteads established close to flower farms (Figure 10). However, the proportion of farmers declaring having no problem with the presence of the flower farm in their villages was of 86% against 14% of farmers who said they had a problem with the flower farm ( 1 df = 51.46, ). Those who had problems with the presence of the flower farm in their village raised several reasons for why they had problems with the presence of the flower farm in their village (Table 17).


Statement no.Question: Do you have any problem with the presence of the flower farm in the village?Frequency (%) of reasons/statements

1 I doubt if a single animal/insect will survive where that chemically-enriched waste soil has been dumped by flower farm2.31
2 My animals have been seek ever since the farm came around0.77
3 Papaw/avocado/pumpkin/mango flowers are aborting; even the few that formed fruits started rotting on the tree before the fruit is mature 1.55
4 People working for a long time (2–5 years) get contaminated by chemicals and eventually died when they came out from work 1.55
5 Ever since this flower farm come around, we are experiencing yield loss and abnormal (reduction) crop production 1.54
6A flower farm should never be placed near people because the chemical sprays travel towards our village (>3 Km) up to inside our homestead and children get respiratory diseases0.77
7All our crops these days seek and can't breathe properly because of chemicals they apply there0.77
8Avocado, mango, papaw, and pumpkin are ripening/falling down earlier and are not tasty, ever since the flower farm came around0.77
9 Avocado/mangos don't look good anymore since the establishment of the flower farm, may be because of the pesticides they spray which are poisons 1.54
10Bees are moving away from the flower farm to our villages these days, crops near flower farms suffer0.77
11Cassava is stunt; other fruits are rotting these days due to chemicals; it used not be like that0.77
12Chemical dumped/deposited, at flower farm edge, during night hours, has a strong smell for >6 months0.77
13Chemical of the flower farm is dangerous to humans/livestock/wildlife because can't guarantee keeping polluted water there everyday0.77
14Chemical sprays from the flower farm smell alot in our village and they kill flowers of our crops0.77
15Chemicals sprayed daily from the flower farm have reduced the bee population in our village1.54
16Chemicals sprayed leave the flower farm and move in the air and we smell them too much; my kids fall sick regularly0.77
17Emerging pests and diseases in many crops may be due to fume from the flower farm0.77
18 Every time the river/swamp water-enriched with water from the flower farm crosses my gardens, I harvestno fruits (egg plants/tomato) 3.80
19Few crops are not very affected by these chemicals, but for most crops their yields are reducing dramatically0.77
20 Flower farm dump regularly chemical wastes into the rivers around our villages and this kills fish 1.54
21 Crop flowers are quickly aborting and few formed fruits (mangos, avocado, papaw) do not taste well anymore0.77
22From most crops, few flowers are turning into fruits/seeds these days ever since the flower farm was established around0.77
23Fruit rotting problem started some 3 to 5 years ago; these days, no more good fruits; most of them are rotting0.77
24Fumes sprayed in the flower farm kill bees and other animals in the nature around because they smell strongly0.77
25 I am convinced that bees disappearing in the village is due to toxic pesticides applied in the flower farm 3.08
26I am not affected in my farming business by any activities around the flower farm0.77
27I am now abandoning growing fruit tree crops because they will not give good fruits or if a fruit comes, it is of low quality0.77
28I believe that the flower farm chemicals must have contributed to reduced yields and to poor yield performance of crops0.77
29I do not think chemicals sprayed in the flower farm are dangerous to our crops or to bees0.77
30 I have no problem with the flower farm, either they are there or not I benefit or lose nothing 5.38
31I have no problem, either they are there or not, it does not matter to me0.77
32 I regularly see dead fish on the edge of the river that cross the flower farm into our village 3.08
33 I regularly see vehicles moving at night from the flower farm dumping smelly chemicals near our village 2.31
34 I see no problem may be because I am a migrant worker, but one from this village has always complained about bees declining (disappearance) 2.31
35I strongly believe that the fume of pesticides applied in the flower is responsible for currently observed flower abortion in most fruit crops in the village0.77
36I suspect the flower farm is dangerous to people and animals because of the nature of smelling the toxic chemicals they apply0.77
37I used to see many snakes/soil ant colonies around the village, these days I rarely see them passing around0.77
38Insect pests chased near the flower farm came in my (>1000 m) garden to eat/destroy my crops 0.77
39Many children who went to work at the flower farm got exposed to these pesticides and died0.77
40Most of the mango/avocado fruits grown near the flower farm are no longer tasty or juicy2.31
41Never place flower farms near people because they don't need bees but farmers need bee'-visits to crops0.77
42No activity from the flower farm affects my crops; egg plants and tomato grow here in the village0.77
43No one has ever complained about chemicals applied there to kill his crops0.77
44No problem because I was informed that they have constructed several dams for recycling their water and for containing chemical wastes there0.77
45 Papaw/avocado are no longer sweet, too many fruit diseases emerging these days; tree crops are currently yielding low 2.31
46People living near the flower farm breathe polluted air with dangerous chemicals, fall sick frequently, and many die0.77
47People working at the flower farm become tiny and die after 3–5 years of working there0.77
48 People fear to use the stream water because they believe it is full off chemical wastes dumped regularly by the flower farm 3.08
49 People living at the edge of the flower farm can smell the fumes (pesticides) scent from the flower farm daily 2.31
50 People who grow mango/avocado/papaw near (at the edge of) the flower farm experience low yields these days;they are complaining 2.31
51People who work at the flower farm all get sick because of chemical breathing and many die after 2–5 years working 0.77
52 People who work in the flower farm start falling sick 3–5 years later 1.54
53Pesticides applied in the flower farm are decolorating (changing the colour) our crops in the village0.77
54 People who work in these flower farms complain all time about their health status andlow salaries (not paid in time) 3.08
55Pumpkin and watermelon flowers do not turn into fruits anymore near the flower farm, but in the village (>2 km) fruits are many0.77
56 Since the farm was established here, we experience rotting of fruits (avocado, papaw) and it may be due to chemicals 1.54
57When smelling chemicals up to 2-3 Km here in the village, I lose my appétite and my children fall sick all the time0.77
58So far no complaint apart from the risk of our cows drinking the river water-enriched with chemical water from the flower farm0.77
59The flower farm is dumping the crop residues full of chemicals in our village and they smell a lot for 6 months0.77
60 The flower farm pollute river/wetland waters crossing our village 1.54
61The flower farm pour chemically-enriched water into the river that people use as drinking water and we drink that water0.77
62The flower farm spray daily massive toxic chemical that flies up to 2–4 km in the village 0.77
63The fumes from the flower farm smell badly everyday their are applied; and we fall seek after being exposed for long time0.77
64The rate of abortion of my cows is very high these days and I think it is due to drinking polluted water from the flower farm0.77
65 The rate of abortion of my cows is very high these days and I think it is due to drinking polluted water from the flower farm 1.54
66The recycling of water around the flower farm is not properly done/controlled, there is still leakage of their water into the river0.77
67 The reduction in crop yields in the village may be due to the fact that bees smell pesticides from the flower and die 1.54
68 The soil from the waste dumping point can smell a lot for more than 5 months 2.31
69The yield of fruits (mango/avocado/passion fruits) has reduced to 15 to 35% since the flower farm came around0.77
70 There are rumors that chemicals applied spoil our crops, but I am not sure if it is linked to seasonal/climate changes 2.31
71 There are several dumping holes of chemical wastes near our gardens 1.54
72There are no more bees and honey production is absent in the village ever since the flower farm is around0.77
73 There are several dumping points of chemically-enriched soils in our village 1.54
74There was a problem of water leakage from the flower farm into the river, but they claimed to have controlled it (properly closed it), it is not correct0.77
75 These days I see many fish dying/stunting because the water I use in my 12 fish ponds cross the flower farm 1.54
76These days, there is too much water in the swamp because the flower sends a lot there daily0.77
77These people claim recycling/reutilizing water 2 times only, after that water, where do they put it? Not in the river?0.77
78 These days, there is too much crop failure due to pests/diseases/chemicals applied in the flower farm 1.54
79They kill bees with chemicals in the village because they don't want any single bee to land on the flower farm0.77
80Water from the flower farm is currently still leaking into the river and both human beings and cows drink that water and fall sick and die.1.54
81We meet several hundreds of dead bees/snakes/fish/lizard in the fields a day after they have sprayed0.77
82We are all migrant and care little about effects of pesticides on crops grown here0.77
83We regularly see several thousands fish dying near the flower farm where they eject water into Lake Victoria0.77
84Whenever they are at spraying the flower farm, the fumes comes into the air and reaches our houses and make us fall sick; including our wives and children0.77
85Yields of my crops are reducing because I think the flower farm killed all the bees in the village that pollinate my crops0.77