Most pollination ecosystem services studies have focussed on wild pollinators and their dependence on natural floral resources adjacent to crop fields. However, managed pollinators depend on a mixture of floral resources that are spatially separated from the crop field. Here, we consider the supporting role these resources play as an ecosystem services provider to quantify the use and availability of floral resources, and to estimate their relative contribution to support pollination services of managed honeybees. Beekeepers supplying pollination services to the Western Cape deciduous fruit industry were interviewed to obtain information on their use of floral resources. For 120 apiary sites, we also analysed floral resources within a two km radius of each site based on geographic data. The relative availability of floral resources at sites was compared to regional availability. The relative contribution of floral resources-types to sustain managed honeybees was estimated. Beekeepers showed a strong preference for eucalypts and canola. Beekeepers selectively placed more hives at sites with eucalypt and canola and less with natural vegetation. However, at the landscape-scale, eucalypt was the least available resource, whereas natural vegetation was most common. Based on analysis of apiary sites, we estimated that 700,818 ha of natural vegetation, 73,910 ha of canola fields, and 10,485 ha of eucalypt are used to support the managed honeybee industry in the Western Cape. Whereas the Cape managed honeybee system uses a bee native to the region, alien plant species appear disproportionately important among the floral resources being exploited. We suggest that an integrated approach, including evidence from interview and landscape data, and fine-scale biological data is needed to study floral resources supporting managed honeybees.
Managed honeybees are globally important for crop production (
(A) shows the delivery of pollination ecosystem services within an agricultural landscape (adapted and simplified from
The existing literature supports the idea that natural vegetation is an important resource for managed honeybees and represents a key supporting ecosystem service to sustain honeybee populations outside the months when the crop is in flower (
An important requirement when analysing the supporting ecosystem services provided by natural and human-modified landscapes is the spatial location of apiary sites and the factors that influence the use of apiary sites. Available floral resources delimit the landscape in which beekeepers operate, but there may be variation in how beekeepers manage their operational responses to maximise the long-term productivity of hives (
We examine managed honeybees in the context of the Western Cape (South Africa) where the endemic Cape honeybee (
Within this system, we specifically address the following questions:
Which floral resources do beekeepers consider most important for the long-term productivity and health of their hives?
Is beekeeper use consistent with availability of resources in the landscape?
What is the relative importance of natural vegetation versus human-modified landscapes for supporting ecosystem service for managed pollinators?
To answer these questions, we used a socio-ecological approach and collected data from beekeepers regarding their choice of locations for apiary sites and then undertook site surveys and spatial analyses of landscape features to determine the availability of floral resources at apiary sites. The relative availability of resources at apiary sites could then be compared to the availability of resources in the region.
The Cape managed honeybee system in South Africa can be defined by the biogeographic distribution of the Cape honeybee (
A summary of the three main floral resource-types, the source of the data used, and the habitat type category for each floral resource. We obtained information for floral resources from interviews with beekeepers and land cover type was derived from available spatial data when mapping BLUs.
Natural vegetation | Indigenous plant species of succulent karoo, fynbos, and renosterveld vegetation | Flower-rich vegetation including plants known to be used by honeybees such as |
Natural (near pristine) |
Eucalypt | Eucalypt stands digitized from aerial photos | Human-modified (invasive alien trees) | |
Crops (beekeeper dataset) | Canola, citrus, clover and lucerne | – | Human-modified (crops) |
Canola fields (landscape analysis) | 16% of arable field boundary data/layer [38]—see |
Human-modified (crops) |
Beekeepers were selected for one-to-one interviews using purposive sampling (
Six beekeepers were interviewed between June 2012 and October 2013. During the interviews, each of the beekeeper’s apiary sites were mapped using digital topographic maps (obtained from National Geo-Spatial Information, South Africa) with a scale of 1:50,000 in ArcGIS 10.1 (ESRI, Redlands, CA, USA).
Semi-structured interviews (
Information was obtained for 6,700 managed hives, representing approximately 22% of the managed hives in the Western Cape Province. Data for 708 apiary sites (ranging from 26 to 364 apiary sites per beekeeper) was captured across a wide geographic distribution of the Cape managed honeybee system (
For each beekeeper, a random selection of 20 apiary sites (giving a total of 120 sites) was chosen for all further analyses. We tested whether the selected subset of apiary sites was representative of the full set of apiary sites by carrying out a Pearson’s chi-squared test. There was no significant difference in the proportion of resource-types between the full dataset and the subsample (
Schematic diagram showing how the BLU is typically separated from the crop field where the provision of pollination services occurs. Each BLU is typically composed of a range of floral resources providing essential pollen and nectar which sustains managed honeybee populations. (Refs for the data in
The landscape surrounding each site (
In finalising the BLU classification, areas unlikely to provide pollen and nectar resources for honeybees such as major water bodies (e.g., dams) and all other agricultural types (e.g., viticulture) were excluded. In addition, the BLU analysis is unlikely to be very effective for assessing floral resource availability of weeds or private gardens (e.g., in urban areas and rural farmhouses) which are patchily distributed and because of the lack of suitable land cover data to estimate landscape availability.
To calculate the average available floral resources across the study system (approximately 7,804,891 ha, 60% of the spatial extent of the Western Cape Province,
The total available area of natural vegetation and canola fields was determined from the same data and approach used to classify the BLUs.
We estimated that the study system was composed of 66.28% natural vegetation, 2.99% canola fields, and 0.09% eucalypt. Similar to the BLU classification, the remaining land cover (approximately 30.64%) was excluded because it was composed either of water bodies and other agricultural types (e.g., viticulture) that is unlikely to provide pollen and nectar resources for honeybees or floral resources that lacked suitable spatial data (e.g., weeds or private gardens).
The analyses were based on three datasets: first, a table giving the number of times (counts) a floral-resource category was specified by each beekeeper (beekeeper dataset;
To illustrate the different proportional use of resource-types, bipartite networks were constructed from the contingency table for each dataset using the “bipartite” package (
To determine whether the resources identified by beekeepers was consistent with what was available in the landscape and hive adjusted dataset, Pearson’s chi-squared tests were performed on the beekeeper dataset. This provided a test of whether the observed frequency of each floral resource-type was significantly different from expected. Expected values were based on: (i) proportions of all three floral resource-types derived from the landscape dataset (expected probabilities: eucalypt = 0.02, natural vegetation = 0.89 and canola = 0.09); (ii) the proportions derived from the hive adjusted dataset (expected probabilities: eucalypt = 0.89, natural vegetation = 0.02 and canola = 0.09) (
To determine if BLUs differed in composition from what is generally available in the region and indicate whether beekeepers exhibit a preference for specific floral resources, the relative availability of floral resources across BLUs was compared to the average available floral resources across the whole study system. We did this by performing a nonparametric rank-sum test to determine whether the BLU sample mean of each floral resource-type differed significantly from its corresponding regional average using the “ICSNP” package (
Using the total area of each floral resource category from the map of BLUs we estimated the relative contribution of natural and human-modified landscapes as resources for managed honeybee populations. We first divided the total area of each floral resource available within the BLUs by the total number of hives. Based on the required number of hives (approximately 30,000 managed hives) needed for pollination services for the Western Cape deciduous fruit industry, we estimated the supporting ecosystem service contribution of each floral resource. Although this estimate is a simple extrapolation from area and hive numbers there are currently a range of methods for mapping and measuring ecosystem services (
Research ethics clearance involving human participants was granted by the Science Faculty Research Ethics Committee at University of Cape Town (UCT), reference number: SFREC 34-2012. In accordance with UCT’s Code of research involving human subjects, the nature of the research was verbally explained before each interview and each participant was provided with an information sheet outlining the research and provided contact details if concerns or questions arose following the interview. AM obtained signed consent from each of the participants prior to each interview. In all cases inputs were coded to retain the anonymity of the beekeeper and location of their sites and we only provide summary results in this paper.
The network figure (
Importance of floral resource-types according to (A) the beekeeper dataset, (B) the landscape dataset (area in ha), (C) hive adjusted dataset (landscape availability adjusted by number of hives placed at apiaries). For (A) the floral resource-types and beekeepers are represented by rectangles (top and bottom of each graph). The lengths of the upper rectangles are proportional use of a resource-type considered across all beekeepers. The widths of the ties linking resource-types to beekeepers are proportional to the number of times a beekeeper used a particular resource-type. Interpretation for (B) and (C) is similar to (A), except that (B) is the area of a resource-type available to bees, rather than counts, and (C) is the area of a resource-type adjusted by hive number. Supporting ecosystem-services provided by natural vegetation are shown in light grey, whereas contributions provided by human-modified landscapes (in the form of eucalypt and crops) are shown in dark grey.
Analysis of the resources available to beekeepers within BLUs provided a significantly different perspective to that provided by beekeepers (
When the availability of different floral resources was adjusted according to the number of hives at an apiary site (hive adjusted dataset), eucalypt was found to be of primary importance (
Each panel represents the main floral resource-types (A–C). Within each panel, we plot the distribution of the data across the BLU samples. The BLU sample mean is shown as a circle and 95% confidence intervals were estimated using bootstrap methods (20,000 iterations). The estimated regional average is shown as a triangle. We interpret the position (above or below) of the BLU sample mean in relation to the regional average to determine if more or less hectares are being used across all beekeepers.
When analysing the beekeeper dataset against the hive adjusted dataset we find that these are significantly different (
In contrast, natural vegetation was used significantly less than the regional average despite it making up a large proportion (
Based on the composition of BLUs, the population of managed honeybees in the Western Cape uses the following areas of floral resources: 700,818 ha of natural vegetation (13% of study system), 10,485 ha of eucalypt (0.2% of study system), and 73,910 ha of canola fields (1.4% of study system) (
Estimate of the relative contribution of supporting ecosystem services provided by natural and human-modified landscapes to sustain the population of 30,000 managed honeybee hives in the Western Cape.
Natural vegetation | 67,325.22 | 23.36 | 700,818 | 13.0 |
Eucalypt | 1,007.24 | 0.35 | 10,485 | 0.2 |
Canola fields | 7,100.33 | 2.46 | 73,910 | 1.4 |
This paper focused on managed pollinators, which may be supported by diverse floral resources that are spatially dispersed across a broad region far away from the target crop field. In this situation, the different floral resources become connected through the actions of beekeepers and this has three important implications for the way ecosystem services for pollination are conceptualised and evaluated. First, it shifts the scale at which ecosystem services for pollination are evaluated from the target crop field to a larger geographical region. Second, it expands the type of ecosystem services being evaluated from provisioning services for pollination at the level of the crop field to include supporting services provided by floral resources for managed bees at the landscape and regional scale. Third, it means that the relative importance of different floral resources to support pollination may be influenced both by their availability in the region where managed bees occur as well as by operational responses of beekeepers to the available resources.
Several studies have used beekeeper surveys to identify floral resources (e.g.,
The combination of beekeeper surveys and field studies highlights the value of using more than a single proxy measure (such as beekeeper surveys) to determine floral resources. Data on the number of hives in relation to the available floral resources provided critical information on beekeeper operational responses. The ‘hive adjusted’ dataset provided the most informative results in that it provided a more nuanced measure of what the beekeepers said relative to what was available in the landscape.
One rationale for studies of ecosystem services is to identify and evaluate those natural assets that are required to provide services to people (
Human-modified landscapes played a significant role in sustaining a large number of hives. The relative importance of these different floral resources therefore needs to be considered when estimating the landscape components required to provide the supporting ecosystem services for managed honeybees. Our study could only give an approximate indication of the floral resource requirements to support managed pollination services and further refinement through fine-scale field-based research is needed to determine what honeybees are using in the landscape (e.g., see
Of particular interest is that the area of eucalypt needed to support the current number of hives for managed pollination services is estimated at a little over 10,000 ha. This is probably an under-estimate due to the exclusion of riverine species of eucalypt in BLUs
It was surprising that beekeepers ranked crop floral resources (different to the target crop requiring pollination) as the least important resource. Beekeepers are thought to be shifting towards a greater use of crops such as canola to “boost” managed honeybee populations before hives are moved to farms for pollination (
An important question to consider in terms of overall sustainability is what would happen if particular “supporting” resources, such as eucalypt was removed or lost. Would this constrain crop production in the Western Cape or could hive numbers be sustained on other resources such as natural vegetation despite its seemingly lower carrying capacity for managed hives. It is not clear how and if beekeepers would adapt to changes in floral resource availability, i.e., would beekeepers switch to alternative resources or would such losses result in decreased profitability and ultimately closure of their business? Conducting detailed behavioural studies to investigate beekeeper’s responses to changing resource availability could provide insights into the future direction of the industry and how it relates to the provision of pollination services. The analyses in this study do not fully answer this question and it is clear that we are only beginning to understand the importance of different floral resources for managed honeybees in South Africa and other regions that are heavily reliant on managed pollinators.
The results of this study are not unique to the South African context. Many agricultural systems rely on managed honeybees (
Inclusion of supporting services brings in additional complexity to the management of ecosystem services for pollination because the managers of land where supporting services for pollinators are provided may not derive any direct benefit. In addition, the managed bees being supported at remote locations may provide pollination services to multiple crops. As a result, the management of floral resources for managed bees may benefit from studies of other ecosystem services such as water provision where there is a need to incentivise appropriate land management in water catchments to provide water to downstream users (
An additional complexity that would need to be considered in landscape models incorporating managed honeybees is the importance of both natural and human-modified landscapes. One of the main conclusions of our study is that human-modified components of the landscape (eucalypt stands) can play an integral role in supporting managed honeybees (
This paper improves our understanding of honeybee landscape ecology and the floral resources needed to support managed honeybees. Existing conceptual models focus on landscapes surrounding the target crop but this study showed how managed pollinators are moved around a greater area and the need to consider a complex range of factors such as: social factors (e.g., beekeeper’s preference), ecological factors (e.g., the type of floral resources available), spatial factors (e.g., the landscape distribution of apiary sites), behavioural (e.g., bee foraging) and biological (e.g., plant phenology). Incorporating such factors has important implications for managed honeybees because each floral resource-type requires its own set of management or conservation interventions. These should be incorporated in a broader understanding of how to sustain pollination services. Ultimately, the practical value of estimating the relative contribution of floral resources needed to sustain managed pollinators is that it could inform land managers in maintaining and conserving the current level of floral resources (see
Map of Cape managed honeybee system including the Western Cape deciduous fruit growing areas (Extracted from Western Cape Department of Agricultural Department Aerial Commodity Census, 2013) and the distribution of apiary sites based on beekeeper subsample of 120 sites (using quarter degree squares (QDS) so that the exact location of the apiary sites cannot be identified).
Detailed methods of the BLU classification for each floral resource-type: Natural vegetation, eucalypts and canola (see ‘Bee Landscape Unit (BLU) definition and floral resource classification’ in manuscript).
Summary of data derived from interviews with beekeepers (see ‘Data analysis’ in manuscript).
Summary of data derived from the available resource-types (see ‘Data analysis’ in manuscript).
Summary of data derived from the area of available resource-types adjusted according to the number of hives associated with the apiary site (see ‘Data analysis’ in manuscript).
We wish to thank the Western Cape beekeepers whom AM interviewed for participating in this research, giving generously of their time and providing essential information on managing honeybees. We also wish thank Dr. Mark Difford who provided helpful statistical consultation, Chris Broderick for assistance with digitising eucalypt and ground-truthing of canola fields, Dr. MG Wallace, Western Cape Department of Agriculture for providing agricultural spatial data, Fahiema Daniels for providing spatial data and GIS support, and Regional AgriSA officers for canola production data. This study was part of the Global Pollination Project in South Africa.
The authors declare there are no competing interests.
The following information was supplied relating to ethical approvals (i.e., approving body and any reference numbers):
Research ethics clearance involving human participants was granted by the Science Faculty Research Ethics Committee at University of Cape Town (UCT) (Ethical application reference number: SFREC 34-2012).
The following information was supplied regarding data availability:
The raw data are provided in the