Crop and landscape factors affecting variation in composition and behaviour of the pollinator community in field bean crops
DOI:
https://doi.org/10.26786/1920-7603(2023)746Keywords:
Pollination, pollinators, Apoidea, Vicia faba, floral resources, crop yieldAbstract
The global decline in pollinators is likely to negatively affect the yield of insect pollinated crops such as field beans (Vicia faba). To understand the impact of such declines it is important to investigate how the abundance, composition and behaviour of the pollinator community relates to crop yield.
We observed pollinators (specifically Bombus spp. and Apis mellifera) foraging in field bean fields. Some bees actively pollinated flowers whereas others robbed the nectar without actively pollinating the flowers. As legitimate foraging visits are more likely to pollinate the crop, we explored infield and landscape scale factors affecting this variation in behaviour. Infield factors included sowing time (winter/spring) and plant density. Landscape factors were the area of flower-rich habitat, and of mass-flowering crops within 1 km of the bean field. We also explored how the abundance and behaviour of different functional groups (short-tongued bumblebees, long-tongued bumblebees or honeybees) responded to these factors. Finally, we assessed how the abundance and behaviour of these pollinators affected field bean yield.
Pollinators were more abundant in bean crops that were spring sown and where there was a smaller area of mass-flowering crops in the landscape. Functional groups varied in their predominant foraging behaviour and in how their behaviour was influenced by external factors. There was no relationship between pollinator abundance and bean yield however the proportion of pollinators legitimately foraging was negatively related to yield. Our findings align with previous research in suggesting that the benefits of insect pollinators for field beans are context specific. Additional work is required to develop pollinator conservation measures that will facilitate crop pollination.
References
Aouar-sadli M, Louadi K, Doumandji S-E (2008) Pollination of the broad bean (Vicia faba L.var. major) (Fabaceae) by wild bees and honey bees (Hymenoptera: Apoidea) and its impact on the seed production in the Tizi-Ouzou area (Algeria). African Journal of Agricultural Research 3:266–272. [online] URL: http://www.academicjournals.org/AJAR
Bailes EJ, Pattrick JG, Glover BJ (2018) An analysis of the energetic reward offered by field bean (Vicia faba) flowers : Nectar, pollen, and operative force. Ecology and Evolution 8:3161–3171. https://doi.org/10.1002/ece3.3851 DOI: https://doi.org/10.1002/ece3.3851
Balfour NJ, Garbuzov M, Ratnieks FLW (2013) Longer tongues and swifter handling: Why do more bumble bees (Bombus spp.) than honey bees (Apis mellifera) forage on lavender (Lavandula spp.)? Ecological Entomology 38:323–329. https://doi.org/10.1111/een.12019 DOI: https://doi.org/10.1111/een.12019
Barker JL, Dornhaus A, Bronstein JL, Muth F (2018) Learning about larceny: experience can bias bumble bees to rob nectar. Behavioral Ecology and Sociobiology 72 (68). https://doi.org/10.1007/s00265-018-2478-6 DOI: https://doi.org/10.1007/s00265-018-2478-6
Bartomeus I, Gagic V, Bommarco R (2015) Pollinators, pests and soil properties interactively shape oilseed rape yield. Basic and Applied Ecology 16:737–745. https://doi.org/10.1016/j.baae.2015.07.004 DOI: https://doi.org/10.1016/j.baae.2015.07.004
Bartomeus I, Potts SG, Steffan-Dewenter I, Vaissière BE, Woyciechowski M, Krewenka KM, Tscheulin T, Roberts SPM, Szentgyörgyi H, Westphal C, Bommarco R (2014) Contribution of insect pollinators to crop yield and quality varies with agricultural intensification. PeerJ 2014:1–20. https://doi.org/10.7717/peerj.328 DOI: https://doi.org/10.7287/peerj.preprints.184v1
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1–48. ttps://doi.org/10.18637/jss.v067.i01 DOI: https://doi.org/10.18637/jss.v067.i01
Benachour K, Louadi K, Terzo M (2007) Rôle des abeilles sauvages et domestiques (Hymenoptera : Apoidea) dans la pollinisation de la fève (Vicia faba L. var. major) (Fabaceae) en région de Constantine (Algérie). Annales de la Societe Entomologique de France 43:213–219. https://doi.org/10.1080/00379271.2007.10697513 DOI: https://doi.org/10.1080/00379271.2007.10697513
Beyer N, Gabriel D, Kirsch F, Schulz-Kesting K, Dauber J, Westphal C (2020) Functional groups of wild bees respond differently to faba bean Vicia faba L. cultivation at landscape scale. Journal of Applied Ecology:2499–2508. https://doi.org/10.1111/1365-2664.13745 DOI: https://doi.org/10.1111/1365-2664.13745
Beyer N, Gabriel D, Westphal C (2022) Landscape composition modifies pollinator densities, foraging behavior and yield formation in faba beans. Basic and Applied Ecology 61:30–40. https://doi.org/10.1016/j.baae.2022.03.002 DOI: https://doi.org/10.1016/j.baae.2022.03.002
Beyer N, Kirsch F, Gabriel D, Westphal C (2021) Identity of mass-flowering crops moderates functional trait composition of pollinator communities. Landscape Ecology 36:2657-2671. https://doi.org/10.1007/s10980-021-01261-3 DOI: https://doi.org/10.1007/s10980-021-01261-3
Bishop J, Garratt MPD, Breeze TD (2020) Yield benefits of additional pollination to faba bean vary with cultivar, scale, yield parameter and experimental method. Scientific Reports 10:1–11. https://doi.org/10.1038/s41598-020-58518-1 DOI: https://doi.org/10.1038/s41598-020-58518-1
Bishop J, Jones HE, Lukac M, Potts SG (2016) Insect pollination reduces yield loss following heat stress in faba bean (Vicia faba L.). Agriculture, Ecosystems and Environment 220:89–96. http://dx.doi.org/10.1016/j.agee.2015.12.007 DOI: https://doi.org/10.1016/j.agee.2015.12.007
Bishop J, Jones HE, OSullivan DM, Potts SG (2017) Elevated temperature drives a shift from selfing to outcrossing in the insect-pollinated legume, faba bean (Vicia faba). Journal of Experimental Botany 68:2055–2063. https://doi.org/10.1093/jxb/erw430 DOI: https://doi.org/10.1093/jxb/erw430
Burns KLW, Stanley DA (2023) Irish faba beans (Fabales: Fabaceae) depend on wild bumblebee pollination for marketable yields. Agricultural and Forest Entomology:1–11. https://doi.org/10.1111/afe.12553 DOI: https://doi.org/10.1111/afe.12553
Carvell C, Bourke AFG, Osborne JL, Heard MS (2013) Effects of an agri-environment scheme on bumblebee reproduction at local and landscape scales. Basic and Applied Ecology 16:519–530. https://doi.org/10.1016/j.baae.2015.05.006 DOI: https://doi.org/10.1016/j.baae.2015.05.006
Carvell C, Meek W, Pywell R, Goulson D, Nowakowski M (2007) Comparing the efficacy of agri-environment schemes to enhance bumble bee abundance and diversity on arable field margins. Journal of Applied Ecology 44:29–40. https://doi.org/10.1111/j.1365-2664.2006.01249.x DOI: https://doi.org/10.1111/j.1365-2664.2006.01249.x
Clarke D, Robert D (2018) Predictive modelling of honey bee foraging activity using local weather conditions. Apidologie 49:386–396. https://doi.org/10.1007/s13592-018-0565-3 DOI: https://doi.org/10.1007/s13592-018-0565-3
Crawley MJ (2005) Statistics An introduction using R. John Wiley and Sons, Chichester. https://doi.org/10.1002/9781119941750 DOI: https://doi.org/10.1002/9781119941750
Dedej S, Delaplane KS (2005) Net energetic advantage drives honey bees (Apis mellifera L) to nectar larceny in Vaccinium ashei Reade. Behavioral Ecology and Sociobiology 57:398–403. https://doi.org/10.1007/s00265-004-0852-z DOI: https://doi.org/10.1007/s00265-004-0852-z
Dicks L V., Baude M, Roberts SPM, Phillips J, Green M, Carvell C (2015) How much flower-rich habitat is enough for wild pollinators? Answering a key policy question with incomplete knowledge. Ecological Entomology 40:22–35. https://doi.org/10.1111/een.12226 DOI: https://doi.org/10.1111/een.12226
Dicks L v., Breeze TD, Ngo HT, Senapathi D, An J, Aizen MA, Basu P, Buchori D, Galetto L, Garibaldi LA, Gemmill-Herren B, Howlett BG, Imperatriz-Fonseca VL, Johnson SD, Kovács-Hostyánszki A, Kwon YJ, Lattorff HMG, Lungharwo T, Seymour CL, Vanbergen AJ, Potts SG (2021) A global-scale expert assessment of drivers and risks associated with pollinator decline. Nature Ecology and Evolution 5:1453–1461. https://doi.org/10.1038/s41559-021-01534-9 DOI: https://doi.org/10.1038/s41559-021-01534-9
Fewell JH, Winston ML (1996) Regulation of nectar collection in relation to honey storage levels by honey bees, Apis mellifera. Behavioral Ecology 7:286–291. https://doi.org/10.1093/beheco/7.3.286 DOI: https://doi.org/10.1093/beheco/7.3.286
Free JB, Williams IH (1976) Pollination as a factor limiting the yield of field beans (Vicia faba L.). The Journal of Agricultural Science 87:395-399. https://doi.org/10.1017/S0021859600027714 DOI: https://doi.org/10.1017/S0021859600027714
Gallai N, Salles J-M, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68:810-821. https://doi.org/10.1016/j.ecolecon.2008.06.014 DOI: https://doi.org/10.1016/j.ecolecon.2008.06.014
Garratt MPD, Coston DJ, Truslove CL, Lappage MG, Polce C, Dean R, Biesmeijer JC, Potts SG (2014) The identity of crop pollinators helps target conservation for improved ecosystem services. Biological Conservation 169:128-135. https://doi.org/10.1016/j.biocon.2013.11.001 DOI: https://doi.org/10.1016/j.biocon.2013.11.001
Garratt MPD, de Groot GA, Albrecht M, Bosch J, Breeze TD, Fountain MT, Klein AlexM, McKerchar M, Park M, Paxton RJ, Potts SG, Pufal G, Rader R, Senapathi GD, Andersson GKS, Bernauer OM, Blitzer EJ, Boreux V, Campbell A, Carvell C, Földesi R, García D, Garibaldi LA, Hambäck PA, Kirkitadze G, Kovács‐Hostyánszki A, Martins KT, Miñarro M, O'Connor R, Radzeviciute R, Roquer‐Beni L, Samnegård U, Scott L, Vereecken NJ, Wäckers F, Webber S, Japoshvili G, Zhusupbaeva A (2021) Opportunities to reduce pollination deficits and address production shortfalls in an important insect pollinated crop. Ecological Applications 0:e02445. https://doi.org/10.1002/eap.2445 DOI: https://doi.org/10.1002/eap.2445
Goulson D, Hanley ME, Darvill B, Ellis JS, Knight ME (2005) Causes of rarity in bumblebees. Biological Conservation 122:1-8. https://doi.org/10.1016/j.biocon.2004.06.017 DOI: https://doi.org/10.1016/j.biocon.2004.06.017
Goulson D, Lye GC, Darvill B (2008) Diet breadth, coexistence and rarity in bumblebees. Biodiversity and Conservation 17:3269-3288. https://doi.org/10.1007/s10531-008-9428-y DOI: https://doi.org/10.1007/s10531-008-9428-y
Hanna AS, Lawes DA (1967) Studies on pollination and fertilization in the field bean (Vicia faba L.). Annals of Applied Biology 59:289-295. https://doi.org/10.1111/j.1744-7348.1967.tb04438.x DOI: https://doi.org/10.1111/j.1744-7348.1967.tb04438.x
Holden JHW, Bond DA (1960) Studies on the breeding system of the field bean, Vicia faba (L.). Heredity 15:175-192. https://doi.org/10.1038/hdy.1960.74 DOI: https://doi.org/10.1038/hdy.1960.74
Holland JM, Smith BM, Storkey J, Lutman PJW, Aebischer NJ (2015) Managing habitats on English farmland for insect pollinator conservation. Biological Conservation 182:215-222. https://doi.org/10.1016/j.biocon.2014.12.009 DOI: https://doi.org/10.1016/j.biocon.2014.12.009
Holzschuh A, Dainese M, González-Varo JP, Mudri-Stojnić S, Riedinger V, Rundlöf M, Scheper J, Wickens JB, Wickens VJ, Bommarco R, Kleijn D, Potts SG, Roberts SPM, Smith HG, Vilà M, Vujić A, Steffan-Dewenter I (2016) Mass-flowering crops dilute pollinator abundance in agricultural landscapes across Europe. Ecology letters 19:1228-1236. https://doi.org/10.1111/ele.12657 DOI: https://doi.org/10.1111/ele.12657
Holzschuh A, Dormann CF, Tscharntke T, Steffan-Dewenter I (2011) Expansion of mass-flowering crops leads to transient pollinator dilution and reduced wild plant pollination. Proceedings of the Royal Society B: Biological Sciences 278:3444-3451. https://doi.org/10.1098/rspb.2011.0268 DOI: https://doi.org/10.1098/rspb.2011.0268
Image M, Gardner E, Clough Y, Smith HG, Baldock KCR, Campbell A, Garratt M, Gillespie MAK, Kunin WE, McKerchar M, Memmott J, Potts SG, Senapathi D, Stone GN, Wackers F, Westbury DB, Wilby A, Oliver TH, Breeze TD (2022) Does agri-environment scheme participation in England increase pollinator populations and crop pollination services? Agriculture, Ecosystems and Environment 325:107755. https://doi.org/10.1016/j.agee.2021.107755 DOI: https://doi.org/10.1016/j.agee.2021.107755
Kambal AE, Bond DA, Toynbee-Clarke G (1976) A study on the pollination mechanism in field beans (Vicia faba L.). The Journal of Agricultural Science 87:519-526. https://doi.org/10.1017/S0021859600033128 DOI: https://doi.org/10.1017/S0021859600033128
Kendall DA, Smith BD (1975) The Pollinating Efficiency of Honeybee and Bumblebee Visits to Field Bean Flowers (Vicia faba L.). The Journal of Applied Ecology 12:709. https://doi.org/10.2307/2402083 DOI: https://doi.org/10.2307/2402083
Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274:303-313. https://doi.org/10.1098/rspb.2006.3721 DOI: https://doi.org/10.1098/rspb.2006.3721
Leadbeater E, Chittka L (2008) Social transmission of nectar-robbing behaviour in bumble-bees. Proceedings of the Royal Society B: Biological Sciences 275:1669-1674. https://doi.org/10.1098/rspb.2008.0270 DOI: https://doi.org/10.1098/rspb.2008.0270
Lundin O, Raderschall A (2021) Landscape complexity benefits bumble bee visitation in faba bean (Vicia faba minor L.) but crop productivity is not pollinator-dependent. Agriculture Ecosystems & Environment 314:107417. https://doi.org/10.1016/j.agee.2021.107417 DOI: https://doi.org/10.1016/j.agee.2021.107417
Mancini F (2022) Biodiversity and Ecosystem Services-status of pollinating insects-technical background document. In: England Biodiversity Indicators 2022. DEFRA
Marzinzig B, Brünjes L, Biagioni S, Behling H, Link W, Westphal C (2018) Bee pollinators of faba bean (Vicia faba L.) differ in their foraging behaviour and pollination efficiency. Agriculture, Ecosystems and Environment 264:24-33. https://doi.org/10.1016/j.agee.2018.05.003 DOI: https://doi.org/10.1016/j.agee.2018.05.003
McGregor (1976) Chapter 4: Legumes and Some Relatives. In: Insect Pollination Of Cultivated Crop Plants. Agricultural Research Service, U.S. Department of Agriculture
Nayak GK, Roberts SPM, Garratt M, Breeze TD, Tscheulin T, Harrison-Cripps J, Vogiatzakis IN, Stirpe MT, Potts SG (2015) Interactive effect of floral abundance and semi-natural habitats on pollinators in field beans (Vicia faba). Agriculture, Ecosystems and Environment 199:58-66. https://doi.org/10.1016/j.agee.2014.08.016 DOI: https://doi.org/10.1016/j.agee.2014.08.016
Nichols RN, Goulson D, Holland JM (2019) The best wildflowers for wild bees. Journal of Insect Conservation 23:819-830. https://doi.org/10.1007/s10841-019-00180-8 DOI: https://doi.org/10.1007/s10841-019-00180-8
Nichols RN, Holland JM, Goulson D (2022) Can novel seed mixes provide a more diverse, abundant, earlier, and longer-lasting floral resource for bees than current mixes? Basic and Applied Ecology 60:34-47. https://doi.org/10.1016/j.baae.2022.02.002 DOI: https://doi.org/10.1016/j.baae.2022.02.002
North Sea Region Programme (2015) NUTS regions. [online] URL: https://northsearegion.eu/about-the-programme/facts-and-figures/programme-area/nuts-regions/ (accessed 26 February 2023).
Poulsen MH (1973) The frequency and foraging behaviour of honeybees and bumble bees on field beans in Denmark. Journal of Apicultural Research 12:75-80. https://doi.org/10.1080/00218839.1973.11099733 DOI: https://doi.org/10.1080/00218839.1973.11099733
Powney GD, Carvell C, Edwards M, Morris RKA, Roy HE, Woodcock BA, Isaac NJB (2019) Widespread losses of pollinating insects in Britain. Nature Communications 10:1018. https://doi.org/10.1038/s41467-019-08974-9 DOI: https://doi.org/10.1038/s41467-019-08974-9
Processors and Growers Research Organisation (2023) Choice and use of seed. Online Pulse Agronomy Guide [online] URL: https://www.pgro.org/choice-and-use-of-seed1/ (accessed 26 February 2023).
Pywell R, Warman E, Hulmes L, Hulmes S, Nuttall R, Sparks T, Critchley C, Sherwood A (2006) Effectiveness of new agri-environment schemes in providing foraging resources for bumblebees in intensively farmed landscapes. Biological Conservation 129:192-206. https://doi.org/10.1016/j.biocon.2005.10.034 DOI: https://doi.org/10.1016/j.biocon.2005.10.034
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. [online] URL: https://www.r-project.org/
Raderschall CA, Bommarco R, Lindström SAM, Lundin O (2021) Landscape crop diversity and semi-natural habitat affect crop pollinators, pollination benefit and yield. Agriculture, Ecosystems and Environment 306:107189. https://doi.org/10.1016/j.agee.2020.107189 DOI: https://doi.org/10.1016/j.agee.2020.107189
Requier F, Jowanowitsch KK, Kallnik K, Steffan-Dewenter I (2020) Limitation of complementary resources affects colony growth, foraging behavior, and reproduction in bumble bees. Ecology 101:e02946. https://doi.org/10.1002/ecy.2946 DOI: https://doi.org/10.1002/ecy.2946
Rural Payments Agency (2020) Countryside Stewardship (CS): Mid Tier and Wildlife Offers manual for agreements starting on 1 January 2023. London. [online] URL: www.gov.uk/claim-rural-payments
Scheper J, Holzschuh A, Kuussaari M, Potts SG, Rundlöf M, Smith HG, Kleijn D (2013) Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss - a meta-analysis. Ecology Letters 16:912-920. https://doi.org/10.1111/ele.12128 DOI: https://doi.org/10.1111/ele.12128
Shaw RF, Phillips BB, Doyle T, Pell JK, Redhead JW, Savage J, Woodcock BA, Bullock JM, Osborne JL (2020) Mass-flowering crops have a greater impact than semi-natural habitat on crop pollinators and pollen deposition. Landscape Ecology 35:513-527. https://doi.org/10.1007/s10980-019-00962-0 DOI: https://doi.org/10.1007/s10980-019-00962-0
Stoddard FL (1986) Pollination and fertilization in commercial crops of field beans (Vicia faba L.). The Journal of Agricultural Science 106:89-97. https://doi.org/10.1017/S0021859600061785 DOI: https://doi.org/10.1017/S0021859600061785
Stoddard FL, Bond DA (1987) The pollination requirements of the Faba Bean. Bee World 68:144-152. https://doi.org/10.1080/0005772X.1987.11098923 DOI: https://doi.org/10.1080/0005772X.1987.11098923
Thomas R, Vaughan I, Lello J (2015) Data analysis with R statistical software: A guidebook for scientists. Eco-explore, Cardiff.
Timberlake TP, Vaughan IP, Memmott J (2019) Phenology of farmland floral resources reveals seasonal gaps in nectar availability for bumblebees. Journal of Applied Ecology 56:1585-1596. https://doi.org/10.1111/1365-2664.13403 DOI: https://doi.org/10.1111/1365-2664.13403
Vaudo AD, Patch HM, Mortensen DA, Tooker JF, Grozinger CM (2016) Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proceedings of the National Academy of Sciences of the United States of America 113:E4035-E4042. https://doi.org/10.1073/pnas.1606101113 DOI: https://doi.org/10.1073/pnas.1606101113
Vaudo AD, Tooker JF, Grozinger CM, Patch HM (2015) Bee nutrition and floral resource restoration. Current Opinion in Insect Science 10:133-141. https://doi.org/10.1016/j.cois.2015.05.008 DOI: https://doi.org/10.1016/j.cois.2015.05.008
Venables WN, Ripley BD (2002) Modern Applied Statistics with S, Fourth. Spring, New York. https://doi.org/10.1007/978-0-387-21706-2 DOI: https://doi.org/10.1007/978-0-387-21706-2
Wermuth KH, Dupont YL (2010) Effects of field characteristics on abundance of bumblebees (Bombus spp.) and seed yield in red clover fields. Apidologie 41:657-666. https://doi.org/10.1051/apido/2010038 DOI: https://doi.org/10.1051/apido/2010038
Wickham H, (2016). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag. https://doi.org/10.1007/978-3-319-24277-4 DOI: https://doi.org/10.1007/978-3-319-24277-4
Williams NM, Regetz J, Kremen C (2012) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049-1058. https://doi.org/10.1890/11-1006.1 DOI: https://doi.org/10.1890/11-1006.1
Wood TJ, Holland JM, Goulson D (2015) Pollinator-friendly management does not increase the diversity of farmland bees and wasps. Biological Conservation 187:120-126. https://doi.org/10.1016/j.biocon.2015.04.022 DOI: https://doi.org/10.1016/j.biocon.2015.04.022
Woodcock BA, Edwards M, Redhead J, Meek WR, Nuttall P, Falk S, Nowakowski M, Pywell RF (2013) Crop flower visitation by honeybees, bumblebees and solitary bees: Behavioural differences and diversity responses to landscape. Agriculture, Ecosystems and Environment 171:1-8. https://doi.org/10.1016/j.agee.2013.03.005 DOI: https://doi.org/10.1016/j.agee.2013.03.005
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1:3-14. https://doi.org/10.1111/j.2041-210X.2009.00001.x DOI: https://doi.org/10.1111/j.2041-210X.2009.00001.x
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Lucy Capstick, Jayna Connelly, Niamh McHugh, John Holland
This work is licensed under a Creative Commons Attribution 4.0 International License.
