Pollinators and pollination of oilseed rape crops (Brassica napus L.) in Ireland: ecological and economic incentives for pollinator conservation
Pollinators are beneficial for many wild and crop plants. As a mass-flowering crop, oilseed rape has received much focus in terms of its pollination requirements but despite a threefold increase in area of cultivation of this crop in Ireland over the past 5 years, little is known about its pollination here. We surveyed the flower visiting insects found in commercial winter oilseed rape fields and evaluated the importance of different pollinator groups, investigated the contribution of insect pollination to oilseed rape seed production, and estimated the economic value of insect pollination to the crop at a national level. Our data showed that winter oilseed rape is visited by a wide variety of insect species, including the honeybee, bumblebees, solitary bees, and hoverflies. The honeybee, Eristalis hoverflies and bumblebees (especially Bombus sensu stricto and B. lapidarius) were the best pollinators of winter oilseed rape based on the number of pollen grains they carry, visitation rates per flower and their relative abundance per field. Exclusion of pollinators resulted in a 27 % decrease in the number of seeds produced, and a 30 % decrease in seed weight per pod in winter crops, with comparable values from a spring oilseed rape field also. The economic value of insect pollination to winter oilseed rape was estimated as €2.6 million per annum, while the contribution to spring oilseed rape was €1.3 million, resulting in an overall value of €3.9 million per annum. We can suggest the appropriate conservation and management of both honeybees and wild pollinators in agricultural areas to ensure continued provision of pollination services to oilseed rape, as a decrease in insect numbers has the potential to negatively influence crop yields.
KeywordsValuation of ecosystem servicesBombusBioenergy cropsOilseed cropsPollinator dependent cropsAgroecologyCrop pollinationAgricultureMass-flowering crops
Pollinating insects contribute to the reproduction of the majority of flowering plants worldwide (Ollerton et al. 2011), and they are also required for pollination of a wide variety of world crops (Klein et al. 2007). A large portion of the human diet (Klein et al. 2007) and essential nutrients (Eilers et al. 2011) come from crops pollinated by insects, and the global area cultivated with these crops is disproportionally increasing compared with pollination-independent crops (Aizen et al. 2008). Using a bioeconomic approach based on dependence ratios, it has been estimated that the value of pollination in agriculture to the world economy is €153 billion per year (Gallai et al. 2009). However, pollinators and the pollination services they provide are under threat from a range of pressures, primarily driven by the intensification of agriculture (Kremen et al. 2002; Klein et al. 2007). Declines in many pollinator groups have been recorded (e.g. Biesmeijer et al. 2006), and as a result crop pollination may be at risk with economic implications and threats to global food production (Gallai et al. 2009). The honeybee (as the main managed pollinator) is frequently attributed as providing the majority of pollination services, but often pollination services are largely provided by wild taxa (Winfree et al. 2008; Breeze et al. 2011; Rader et al. 2009, 2012), and the yield of many crops is increased by greater abundances of wild pollinators (e.g. Garibaldi et al. 2011, 2013; Kremen et al. 2002; Brittain et al. 2013). However, surprisingly little is known about the pollinators and pollination services required by some common crops (Klein et al. 2007).
Oilseed rape (Brassica napus L.) is a mass flowering crop commonly grown in Europe, USA, Canada, Brazil and China. Initially the crop was used for vegetable oil in the food industry and animal feed production, but it is now increasing in area planted worldwide due to its use as bioenergy crop; the pure plant oil produced can be used as a liquid biofuel or converted into biodiesel, mainly for use in the transport industry. Although oilseed rape has not been a common crop in the Irish landscape, in recent years it has increased dramatically (e.g. a 322 % increase in area planted between 2008 and 2012) and now accounts for approximately 4 % of arable land area (CSO 2011a).
Oilseed rape is self-fertile and is partially wind pollinated (Williams et al. 1986), but it produces large amounts of nectar and pollen and is visited by a wide range of insects (Bommarco et al. 2012). Insect pollination has been found to increase seed yield, quality and/or market value in Sweden (Bommarco et al. 2012), Canada (Morandin and Winston 2005; Sabbahi et al. 2005), Germany (Jauker and Wolters 2008; Hudewenz et al. 2013) and the UK (Hayter and Cresswell 2006). There are two main types of oilseed rape: winter oilseed rape is planted in autumn and flowers in early summer, while spring oilseed rape is planted in spring and flowers later in the summer, and there are differences between the two in terms of the proportion of pollen released that lands on stigmas (pollination efficiency) in the UK (Hayter and Cresswell 2006). Rough estimates of the value of oilseed rape pollination to the Irish economy were approximately €1 million per year in 2005 (Bullock et al. 2008), but this could substantially increase if oilseed rape continues to increase in land area.
A diversity of pollinators can improve yield of certain crops (Hoehn et al. 2008; Kremen et al. 2002) and can be important for a number of reasons (Klein et al. 2008): one pollinator can act as an “insurance policy” for another and so if one declines another may take its place (“ecological redundancy”); a higher diversity may increase activity period of pollinators, or ensure pollination services are delivered in a variety of weather conditions (as different pollinator species can differ in their phenology and activity with weather; Willmer et al. 1994); or higher diversity of pollinators means that individuals may interact with each other increasing their efficiency (e.g. Greenleaf and Kremen 2006; Brittain et al. 2013). Therefore supporting a diverse range of pollinators for pollination services could be important for maintenance of crop pollination, and wild pollinators have been previously shown to be important and efficient pollinators of mass flowering crops (Rader et al. 2009; Jauker and Wolters 2008; Jauker et al. 2012). However, the pollination and pollinators of oilseed rape in Ireland are unknown, and this information is essential in terms of managing and protecting pollination services for this crop into the future.
The aim of this study was to investigate (1) the diversity of flower visiting insects in winter oilseed rape crops in Ireland, (2) which of these are the most useful pollinators in terms of visitation, abundance and amount of pollen carried, (3) whether the crop yield benefits from insect pollination, (4) whether the crop is currently limited in production by the amount pollen received and (5) determine economic value of insect pollination of oilseed rape in Ireland, based on our seed set measurements from the South-East. To do this we surveyed pollinators in winter oilseed rape fields, and investigated (1) differences in pollinator species groups in terms of pollen transport and visitation rates in winter crops only, (2) measured seed set in response to pollination treatment and (3) calculated marginal values of oilseed rape production when pollinators are excluded and used this to estimate economic value. For comparison we also measured seed set and calculated marginal values of production for a single field of spring oilseed rape.
Pollinating insect diversity
To assess the diversity of flower-visiting insects present in winter oilseed rape fields, pan trapping was carried out in ten fields in 2009 throughout south-east Ireland (the region where oilseed rape is predominantly grown, CSO 2011b, Fig. S1 supplementary material). All fields were at least 1 km apart, and only one field was selected per farm to avoid potential bias due to specific management practices on one particular farm. Pan trapping allows the identification of specimens in the lab, and can be the most useful method for sampling diversity of hoverflies and solitary bees (Westphal et al. 2008). Pan traps were yellow, blue and white coloured UV painted bowls; a set of three bowls (one of each colour) was attached to a stake using a metal clamp and the rim of the bowls adjusted to the height of the oilseed rape flowers. Three stakes were left in the centre of each field, 20 m apart, for 48 h. Specimens were collected and identified in the lab. Type specimens of each species were verified by experts (see “Acknowledgements”) and deposited in Trinity College Dublin (Stanley and Stout 2013).
Visitation rates, pollen transport and pollinator importance
Three winter oilseed rape fields were selected in spring 2010; in Shillelagh Co. Wicklow (field 1), Bunclody Co. Wexford (field 2) and Tullow Co. Carlow (field 3, Fig. S2 supplementary material). In each field, the insect visitors visiting the crop were observed, and their pollen loads examined to investigate pollinator importance. Each field was visited seven times during the flowering period of the crop (8th May–14th June). On each visit, six patches of oilseed rape were observed, approximately 5 m into the crop, for 5 min. Patches were selected to be as large as possible while still allowing the observer to record all flower visitors of the taxa most commonly associated with pollination (bees (Apidae), butterflies (Lepidoptera) and hoverflies (Diptera: Syrphidae)), and on average included 32 stems of oilseed rape. Butterflies and bumblebees were identified to species level (except for individuals from the Bombus sensu stricto complex which are not distinguishable in the field, Carolan et al. 2012; three species of this complex have been previously identified from oilseed rape fields in Ireland using molecular methods; Stanley et al. 2013). Observations were carried out between the hours of 10 a.m. and 4:30 p.m., in warm dry conditions. Flower visitors, along with the number of flowers visited and the total number of flowers per patch were recorded. This allowed calculation of abundances and visitation rates for different species groups, calculated as the proportion of flowers visited per species in a 5 min period (where that species was present). In fields 2 and 3, insects were also caught for examination of pollen loads. We aimed to catch five individuals of the most abundant species groups visiting the crop. Insects were frozen and returned to the lab where each was swabbed with a cube of fuchsin gel which was then melted onto a microscope slide (pollen storage areas on bees were avoided as this pollen is unlikely to be available for pollination). All pollen grains on the slide were identified and counted. Although this did not give a total count of pollen loads, as all insects were sampled in the same way, relative pollen loads of the insects could be determined.
Pollinator importance indices were calculated for the seven most abundant insect groups (and any others where all data were available) as mean visitation rate per flower in 5 min × mean number of oilseed rape pollen grains carried × mean abundance observed visiting oilseed rape per field. Mean visitation rate and mean number of grains carried were calculated per insect group across all fields sampled, while mean abundance was calculated per area sampled in each field.
Seed set and economic valuation
Seed set was examined in four winter oilseed rape fields in 2010; the same three fields used to observe visitation rates and a fourth in Fenagh Co. Carlow (field 4, Fig. S2 supplementary material). All fields were of the “Castille” oilseed rape variety, or a mixture of “Castille” and “Excalibur”. Each field was visited in early May and four areas within each were selected, two in the edges of the field along an adjacent hedgerow, and two in the centre of the field (30 m from each other and from the field edge). Three pollination treatments were applied to six flowers (where possible, resulting in mean of four) on 4–6 plants per area (mean 85 flowers per treatment per field). Flowers were either (1) left un-manipulated to allow natural pollination, (2) the flower head was bagged prior to dehiscence using tulle netting (1.2 mm diameter mesh) to prevent insect pollinators from accessing the flower but still allowing wind pollination to occur (Jacobs et al. 2009; bags were removed as soon as the marked flowers had finished flowering to allow continued growth of the plant; Dafni et al. 2005) or (3) supplemental pollen from a neighbouring plant was placed on the stigmas of the flowers to supplement natural pollination. Seed pods were collected 6–8 weeks later when the pods had reached maturity. Pods were then dried in the laboratory and the number of seeds counted, and total seed weight per pod and mean seed weight per pod were also measured.
To estimate the value of pollination to winter oilseed rape crops, we used a method based on the economic loss that would take place in the absence of any insect pollinators. Initially yield and cost data for oilseed rape production were obtained from Teagasc and the Central Statistics Office for the years 2009–2011 (O’Donovan and O’Mahony 2011; O’Mahony and O’Donovan 2010; CSO 2009, 2010, 2011a; O’Mahony 2009), and the proportions of winter to spring crops each year were also obtained (Oliver Carter, personal communication). The net margins of the crop were then calculated per tonne for each year by dividing the costs per hectare (material, machinery and miscellaneous costs) by the average yield (tonne/Ha) and subtracting them from returns (per tonne). Secondly, the net margins were calculated in the absence of insect pollination by reducing the average yield by the 30 % decline in seed weight per pod obtained in the experimental field study. The percentage reduction in total seed weight per pod was used to reduce the yield as, at harvest, the seeds are separated from the pods and the yield is measured as grain/seed weight (Oliver Carter, personal communication). This reduced yield figure was then used to re-calculate the net margin per tonne as described above. Lastly, the contribution of insect pollinators to the economic value of oilseed rape was calculated as the loss in economic value of oilseed rape value between net margin of crop and net margin calculated when insect pollinators are not present (see Table S1 supplementary material). These figures were then calculated on a national scale, by multiplying values per tonne by total tonnage (calculated as the total area planted multiplied by the average yield, which differed with and without insect pollination).
Seed set was also measured in one spring oilseed rape field in Oak Park, Co. Carlow (“Delight” variety). This field was visited in early June and five areas were selected, three in the edges of the field and two in the centre. The same three pollination treatments (as above) were applied to five marked flowers on two plants per area (50 flowers per treatment). Seeds were collected 4 weeks later, and processed as before. Economic value at a national scale was also calculated for spring oilseed rape using the same methods above; however, these estimates are based on a 35 % reduction in seed set from this one field only and so should be interpreted with caution.
Seed set data were analysed using mixed effects models in the lme package (Pinheiro et al. 2012) in R (R Development Core Team 2011). Total seed weight per pod, mean individual seed weight per pod and number of seeds per pod were all tested for differences between treatment (un-manipulated, bagged and supplemental pollination), location within field (edge and centre) and their interaction. Separate models were run for winter and spring crops. To account for the nested design, random terms were specified including field (for winter crops only), plot within field, and plant. Models were simplified by backwards selection, first removing non-significant interactions and then non-significant main effects, and validated by visual inspection of the residuals. If there was a significant treatment effect, Tukey all-pair comparisons were made between treatments using the multcomp package (Hothorn et al. 2008).
Flower visiting insect diversity
Insects identified from the pan traps in winter oilseed rape fields, and the number of fields that they were recorded in (out of a total of 10)
No fields present (out of 10)
Bombus sensu stricto
Visitation rates, pollen loads and pollinator importance
Mean (±standard error) values of parameters used to calculate pollinator importance (number of oilseed rape pollen grains carried × visitation rate × mean abundance from focal observations)
Mean visitation rate per flower in 5 min
Mean no. pollen grains carried per individual
Mean abundance per total sampled area in each field
0.03 ± 0.01
4,357 ± 895
5.7 ± 2.6
0.01 ± 0.003
2,076 ± 445
12.3 ± 2.9
Bombus sensu stricto
0.05 ± 0.01
1,813 ± 544
3.67 ± 2
0.06 ± 0.02
1,525 ± 684
1.67 ± 1.2
0.03 ± 0.02
1,212 ± 237
1.33 ± 0.9
0.01 ± 0.003
4,114 ± 1,348
0.67 ± 0.67
0.01 ± 0
4,872 ± 3,145
0.3 ± 0.3
0.01 ± 0.003
182 ± 0
3 ± 1.5
0.02 ± 0.003
165 ± 58
1.7 ± 1.2
Pollinator importance indices, based on abundance, visitation rate and pollen load, were highest for Apis mellifera (largely due to more pollen grains carried), followed by Eristalis hoverflies and bumblebees (predominantly from the Bombus sensu stricto group and B. lapidarius (Table 2).
Final linear mixed effects models describing effects of pollination treatment (un-manipulated, bagged and supplemental pollination) on total seed weight per pod, number of seeds produced per flower, and mean weight per seed in winter oilseed rape
Total seed weight per pod
Location in field
Treatment × location
Number of seeds
Location in field
Treatment × location
Mean weight per seed
Final linear mixed effects models describing effects of pollination treatment (un-manipulated, bagged and supplemental pollination) on total seed weight per pod, number of seeds produced per flower, and mean weight per seed in spring oilseed rape
Total seed weight per pod
Number of seeds
Mean weight per seed
The contribution of insect pollination to the economic value of oilseed rape (€) from 2019 to 2011
Spring oilseed rape
Winter oilseed rape
In a similar way to previous studies from other countries (e.g. Bommarco et al. 2012; Morandin and Winston 2005; Le Feon et al. 2013) we found a diverse range of insects in oilseed rape fields, with a total of 26 bee and hoverfly species in winter oilseed rape. Pollinators can differ in terms of their efficiency of crop pollination (Rader et al. 2009; Jauker et al. 2012); we found that the honeybee, Eristalis hoverflies and bumblebees were the most useful pollinators of winter oilseed rape based on the amount of pollen carried, visitation rates and their abundance. However, other factors may also influence the importance of pollinator groups such as the stability of pollinator groups over time, the amount of pollen deposited per visit (which may not be linked to the amount of pollen carried), stigmatic contact and pollen export and deposition which can vary among taxa (Hayter and Cresswell 2006; Rader et al. 2012; Thomson and Goodell 2001). Also, some pollinators may be more sensitive to weather conditions than others which may affect their importance as pollinators; for example bumblebees can forage for longer day periods and in worse weather than honeybees (Willmer et al. 1994). Interestingly, A. mellifera was not present in all oilseed rape fields surveyed and may be limited to where beekeepers place their hives; therefore, in many fields wild bumblebees (in particular Bombus sensu stricto and B. lapidarius) and hoverflies would be the most important pollinators. Other studies have shown that wild pollinators can be relevant for stability of crop production even when honeybees are present (Garibaldi et al. 2011).
Although not the dominant flower visitors found in oilseed rape, additional hoverfly species (other than Eristalis) and solitary bees were also observed visiting flowers. These taxa can also be efficient pollinators of oilseed rape (Jauker and Wolters 2008; Jauker et al. 2012), although they may not be as effective due to lower abundances than the honeybee (Rader et al. 2009) or bumblebees. However, if abundances of these taxa were increased in agricultural areas, potentially through agri-environmental schemes (e.g. Haenke et al. 2009), they may become more effective pollinators of the crop or may help increase biocontrol of crop pests as their larvae can be effective predators (Leroy et al. 2010).
Pollinator importance indices were calculated from surveys near the field edge. However, most pollinator groups are more abundant in field edges than the centres of fields in Ireland (Stanley and Stout 2013; Power and Stout 2011), and the composition of pollinators may also change with increasing distance into the crop; therefore pollinator importance indices may differ in more central areas of crop fields. For example abundances of Eristalis hoverflies in the centre of oilseed rape fields can be less than other pollinator groups in comparison to the edges (DS, personal observations) and so they may decrease in importance as pollinators further into the crop when other groups such as bumblebees may become more important. In addition, all the fields used in this study were surrounded by hedgerows, and elsewhere pollination services have been found to decrease with increasing distances from semi-natural habitats (Carvalheiro et al. 2012; Garibaldi et al. 2011). Therefore, although not measured in this study, fields without surrounding hedgerows or field margins (or larger fields where distances from hedgerows or margins may be greater) may receive different pollination services from insects than those measured here.
Although in this study we primarily examined winter oilseed rape which flowers early in the summer, spring oilseed rape is also grown and flowers later in the season. Overall abundances of social bees have been shown to be higher in spring than winter crops in the UK (Hayter and Cresswell 2006; Fig. S3 supplementary material). Winter oilseed rape is likely to attract worker honeybees and bumblebee queens, whereas bumblebee colonies will be established when spring rape begins to flower and so spring crops will be visited by honeybee and bumblebee workers, meaning visitors will be much more numerous. This may result in spring oilseed rape being pollinated more efficiently and quickly than winter oilseed rape: previous work has found flowers of spring oilseed rape to be adequately pollinated after 3 h receiving approximately 3 bee visits per hour, whereas winter oilseed rape was only adequately pollinated after 5 days and only 10 % of flowers received a bee visit (Hayter and Cresswell 2006). Thus spring oilseed rape may benefit more from insect pollination than winter oilseed rape, and although honeybees may be important for pollination of winter crops when bumblebees are at the beginning of their colony cycle, bumblebees may be more important for spring crops that flower later on in the season.
As a partially wind pollinated and self-fertile crop, oilseed rape sets some seed without insect visitation. However, we found that flowers where pollinators were excluded produced fewer seeds (and therefore less seed weight per pod and average seed weight) than those open to pollination. This has also been illustrated in other countries (e.g. Sabbahi et al. 2005; Bommarco et al. 2012), and can lead to differences in oil content, chlorophyll content and market value (Bommarco et al. 2012). Interestingly, we found no increase in seed set when additional pollen was added to the flowers. This suggests that oilseed rape is not pollen limited in the fields studied in Ireland, and currently receives sufficient pollination services for maximum seed yield from existing wild pollinators.
However, there was a significant interaction between pollination treatment and location within the field (edge and centre) in winter oilseed rape. The magnitude of pollination benefit (in terms of number of seeds produced, but not mean weight per seed) was larger at the field edge than in the centres, but the bagged treatment also produced less seed in the edges than the crop centres. Plants at the edges of the field may receive less wind-dispersed pollen because they are more sheltered by hedgerows and field boundaries, and/or surrounded by fewer pollen donors. However, pollinators are more abundant in field edges and this may compensate for reduced wind pollination resulting in comparable overall seed set.
Our estimate of the value of oilseed rape pollination to the Irish economy is comparable to the only other estimate in Ireland previously. Bullock et al. (2008) valued oilseed rape in Ireland at €5 million, with the subsequent value of insect pollination valued at €1 million. Here, we estimate the value of insect pollination at €3.9 million. However, neither estimate takes into account other additional benefits of pollination to oilseed rape crops. For example, pollination can increase the quality of seed including higher oil and lower chlorophyll content (Bommarco et al. 2012), and can also reduce the blooming period of the crop (Sabbahi et al. 2006); these factors in turn may also further increase the value of pollination to the crop. Although oilseed rape pollination in Ireland is not currently managed, these figures do not include the economic costs of the replacement of wild pollinators with managed ones (Allsopp et al. 2008). Nonetheless, our figures here are based on responses from a small number of fields of one variety of oilseed rape in the South-East of Ireland only; additional work on a wider scale with additional oilseed rape varieties (for example Hudewenz et al. 2013), and a more comprehensive study of spring oilseed rape in particular, could help to refine the estimates of value of pollination to this crop in Ireland.
Oilseed rape production in Ireland has increased substantially in recent years and is set to increase further in the future, especially with demands for bioenergy. Crop yields are improved with insect pollination, and all the fields studied (which were surrounded by hedgerows) currently appear to receive sufficient pollination services. The majority of insect visitors to the crop are wild pollinators, but also the managed honeybee. Therefore, to maintain current pollination services, efforts should be made to conserve existing pollinators in Irish farmland and augment their abundance and diversity to provision for increased service demands in the future.
We would like to thank the farmers that kindly participated in this study; Alan Matthews for advice on economic valuation; Michael Slawski for providing information on crop yields and values; Oliver Carter for providing information on proportions of spring and winter oilseed rape; Conor Owens for help with field work; Soledad Colombe, James Desaegher and other volunteers for help with weighing and counting seeds; Colm Roynane for identifying solitary bees and type specimens of wasps; and Tom Gittings for verification of type specimens of hoverflies. David Stanley and two anonymous reviewers provided valuable comments on previous versions of this manuscript. This research was funded by the project SIMBIOSYS (www.simbiosys.ie, 2007-B-CD-1-S1) as part of the Science, Technology, Research and Innovation for the Environment (STRIVE) Programme, financed by the Irish Government under the National Development Plan 2007–2013, administered on behalf of the Department of the Environment, Heritage and Local Government by the Irish Environmental Protection Agency (EPA).