Abstract
Honey bee populations have experienced serious losses in Europe and North America. These losses highlight the potential risk to our agricultural systems that could result from loss of pollination. These losses include direct economic repercussions to multiple industries (beekeeping, fruit, vegetable, forage seed, oil seed and biofuel crops), and corresponding threats to human nutrition. Reasons for the losses are varied but include a lack of diverse nectar and pollen resources within intensively farmed agricultural landscapes. Focusing primarily on Europe and the USA, we review the potential approaches to provide and maintain diverse floral resources for honey bees, giving particular consideration to herbaceous plants (“forbs”). These approaches include the cultivation and maintenance of “bee pastures”, consisting of diverse native or non-native flower-rich plantings maintained in fallow areas, field margins, and conservation buffer strips to sustain bee populations, support honey bee health, and aid beekeeping activities. Within this review we examine specific governmental policy initiatives to support these efforts in the USA and Europe.
Zusammenfassung
Intensiv genutzte Agrarlandschaften, denen Blütenpflanzen fehlen, oder die nur minderwertige Nahrungspflanzen aufweisen, können imkerlich genutzte Honigbienenvölker nur mit Mühe ernähren. Ein Mangel an Menge und Qualität von Pollen und Nektar kann zu einer Schwächung des Bienenvolks führen, da eine angemessene Nektar- und Pollenversorgung entscheidend für den Erhalt der Bienengesundheit sind. Daher sind gesunde Bienenvölker und eine wirtschaftliche Imkerei auf Landschaften mit reichhaltigen und nährstoffreichen Pollenquellen und nektarspendenden Blüten angewiesen. Anhand von Beispielen aus Europa und den USA geben wir einen Überblick über mögliche Nahrungsquellen für Honigbienen im Landschaftsraum, mit besonderer Berücksichtigung von nicht kultivierten Flächen in der Agrarlandschaft. Wir beschreiben einige konkrete landwirtschaftliche Umweltmaßnahmen, die den Blütenreichtum verbessern und so der Bienenhaltung nützen könnten. Die in den nicht kultivierten Flächen (Feldränder, Hecken, Gehölze, Teiche, Gräben, Brachen) vorhandene Flora könnte zwischen den Blühzeiten der angebauten Pflanzen den Bienen ergänzende Nahrung bieten. Die bereits vorhandenen, an Ackerland angrenzenden naturnahen Habitate sollten daher dringend erhalten werden. Solche unkultivierten Flächen sind in den am intensivsten genutzten Agrarlandschaften jedoch oft selten. Diese Lücke könnte durch die Schaffung und den Schutz von zusätzlichen nicht kultivierten Flächen gefüllt werden. Als Maßnahme zur Erhaltung von Bestäubern in landwirtschaftlich genutzten Gebieten wurde die Anlage von ausgedehnten Streifen mit Nektarpflanzen zwischen den Anbaufeldern empfohlen. Gleichermaßen konnte gezeigt werden, dass die Reduzierung des Herbizideinsatzes in Anbauflächen für Bienen günstig ist, weil blühende Unkräuter neben den Äckern dadurch zunehmen. Darüberhinaus haben einige Pflanzen, die als Deckfrucht eingesetzt werden, kurze Entwicklungszeiten mit früher Blüte, und sind daher in der Lage, den Bienen früh Nahrung zu bieten, wenn sie abwechselnd mit, bzw. vor der Hauptertragspflanze gesät werden (Phazelie, einjährige Kleearten, Radieschen, Senf).
Neben der regionalen und nationalen Gesetzgebung können regionale Bestäuberinitiativen die Erhaltung der Bestäuber fördern. Ein bedeutendes Ziel bei der Entwicklung von Standards für unbebautes Ackerland zum Erhalt von Bestäubern, einschließlich der Honigbiene, sollte es sein, zeitlich und räumlich heterogene Habitate zu vermehren. Die Schaffung von Richtlinien, die eine Bewirtschaftung von unkultivierten Flächen zur Vermehrung des Blütenreichtums und der Vielfalt vorschreiben, ist von entscheidender Bedeutung (besonders in intensiv bebauten Ackergebieten). Diese Maßnahmen bestehen typischerweise im Pflanzen von blühenden Hecken, Randstreifen um Felder, und blühenden Wiesen. Zwei verschiedene Vorgehensweisen sind üblich, um die Blütenvielfalt in unbebauten Flächen zu erhöhen: (i) die Unterstützung der natürlichen Regeneration der einheimischen Wildblumen, oder (ii) das Einsäen von verschiedenen Mischungen einjähriger oder mehrjähriger Pflanzen. Solche Richtlinien werden nicht nur die Bienenhaltung unterstützen, sondern durch verbesserte Bestäubung auch die Ernteerträge erhöhen, sowie die Biodiversität im Allgemeinen fördern (z.B. Vögel und Säugetiere).
Similar content being viewed by others
References
Aizen M.A., Harder L.D. (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination, Curr. Biol. 19, 915–918.
Alaux C., Ducloz F., Crauser D., Le Conte Y. (2010) Diet effects on honeybee immunocompetence, Biol. Lett., DOI:10.1098/rsbl.2009.0986.
Albrecht M., Duelli P., Müller C., Kleijn D., Schmid B. (2007) The Swiss agri-environment scheme enhances pollinator diversity and plant reproductive success in nearby intensively managed farmland, J.Appl.Ecol. 44, 813–822.
Aschwanden J., Holzgang O., Jenni L. (2007) Importance of ecological compensation areas for small mammals in intensively farmed areas, Wildl. Biol. 13, 150–158.
Banaszak J. (1995) Changes in fauna of wild bees in Europe, Pedagogical University, Bydgoszcz, Poland.
Barickman G., Vaughan M., Mader E. (2008) Pollinator Biology and Habitat, Illinois Biology Technical Note No. 23, Illinois NRCS, USA.
Biesmeijer J.C., Roberts S.P.M., Reemer M., Ohlemueller R., Edwards M., Peeters T., Schaffers A.P., Potts S.G., Kleukers R., Thomas C.D., Settele J., Kunin W.E. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands, Science 313, 351–354.
Byrne A., Fitzpatrick U. (2009) Bee conservation policy at the global, regional and national levels, Apidologie 40, 194–210.
Cain Z., Lovejoy S. (2004) History and Outlook for Farm Bill Conservation Programs, Choices: The Magazine of Food, Farm, and Resource Issues 4, 37–42.
Carreck N.L., Williams I.H. (1997) Observations on two commercial flower mixtures as food sources for beneficial insects in the UK, J. Agric. Sci. Camb. 128, 397–403.
Carreck N.L., Williams I.H. (2002) Food for insect pollinators on farmland: insect visits to flowers of annual seed mixtures, J. Insect Conserv. 6, 13–23.
Carreck N.L., Williams I.H., Oakley J.N. (1999) Enhancing farmland for insect pollinators using flower mixtures, Aspect. Appl. Biol. 54, 101–108.
Carvell C., Meek W.R., Pywell R.F., Goulson D., Nowakowski M. (2007) Comparing the efficiency of agri-environment schemes to enhance bumble bee abundance and diversity on arable field margins, J. Appl. Ecol. 44, 29–40.
Carvell C., Meek W.R., Pywell R.F., Nowakowski M. (2004) The response of bumblebees to successional change in newly created arable field margins, Biol. Conserv. 118, 327–339.
CEC (2006) Communication from the Commission, Halting the loss of biodiversity by 2010 and beyond: sustaining ecosystem services for human bell-being, Commission of the European Communities, Brussels, Belgium.
Cheesman O.D. (1998) The impact of some field boundary management practices on the development of Dipsacus fullonum L. flowering stems, and implications for conservation, Agric. Ecosyst. Environ. 68, 41–49.
Corbet S.A. (1995) Insects, plants and succession: advantages of long-term set-aside, Agric. Ecosyst. Environ. 55, 61–67.
Corbet S.A., Williams I.H., Osborne J.L. (1991) Bees and the pollination of crops and wild flowers in the European community, Bee World 71, 47–59.
Corre-Hellou G., Fustec J., Crozat Y. (2006) Interspecific competition for soil N and its interaction with N2 fixation, leaf expansion and crop growth in pea-barley intercrops, Plant Soil 282, 195–208.
Cox-Foster D.L., Conlan S., Holmes E.C., Palacios G., Evans J.D., Moran N.A., Quan P.L., Briese T., Hornig M., Geiser D.M., Martinson V., vanEngelsdorp D., Kalkstein A.L., Drysdale A., Hui J., Zhai J., Cui L., Hutchison S.K., Simons J.F., Egholm M., Pettis J.S., Lipkin W.I. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder, Science 318, 283–287.
Critchley C.N.R., Fowbert J.A. (2000) Development of vegetation on set-aside land for up to nine years from a national perspective, Agric. Ecosyst. Environ. 79, 159–174.
Decourtye A., Devillers J. (2010) Ecotoxicology of neonicotinoids insecticides in the bees, in: Thany S. (Ed.), Insect Nicotinic Acetylcholine Receptors, Landes Bioscience.
Decourtye A., Lecompte P., Pierre J., Chauzat M.P., Thiébeau P. (2007) Introduction de jachères florales en zones de grandes cultures — ou comment mieux concilier agriculture et biodiversité, et par conséquent, l’apiculture, Le Courrier de l’Environnement de l’INRA 54, 33–56.
Decourtye A., Odoux J.-F., Cluzeau-Moulay S. (2008) Influence des aménagements floristiques sur les abeilles, Bull. Tech. Apic. 35, 114–123.
Desneux N., Decourtye A., Delpuech J.M. (2007) The sublethal effects of pesticides on beneficial arthropods, Annu. Rev. Entomol. 52, 81–106.
Dover J., Sparks T., Clarke S., Gobbett K., Glossop S. (2000) Linear features and butterflies: the importance of green lanes, Agric. Ecosyst. Environ. 80, 227–242.
Dunn C.P., Stearns F., Guntenspergen G.R., Sharpe D.M. (1993) Ecological benefits of the conservation reserve program, Conserv. Biol. 7, 132–139.
Firbank L.G., Telfer M.G., Eversham B.C., Arnold H.R. (1994) The use of species-decline statistics to help target conservation policy for set-aside arable land, J. Environ. Manage. 42, 415–422.
Flowers T.L. (2003) CRP Grass Mixtures. Why? USDA-Natural Resources Conservation Service (NRCS), Meade, Kansas, USA.
Fluri P., Frick R. (2002) Honey bee losses during mowing of flowering fields, Bee World 83, 109–118.
Forman R.T., Sperling D., Bissonette J.A., Clevenger A.P., Cutshall C.D., Dale V.H., Fahrig L., France R., Goldman C.R., Heanue K., Jones J.A., Swanson F.J., Turrentine T., Winter T.C. (2003) Road Ecology: Science and Solutions, Island Press, Washington, DC.
Free J.B. (1993) Insect pollination of crops, 2nd ed., Academic Press, London.
Freemark K., Boutin C. (1995) Impacts of agricultural herbicide use on terrestrial wildlife in temperate landscapes: a review with special reference to North America, Agric. Ecosyst. Environ. 52, 67–91.
Freitas B.M., Imperatriz-Fonseca V.L., Medina L.M., Kleinert A.D.P., Galetto L., Nates-Parra G., Quezada-Euan J.J.G. (2009) Diversity, threats and conservation of native bees in the Neotropics, Apidologie 40, 332–346.
Fussell M., Corbet S.A. (1991) Forage for bumble bees and honey bees in farmland: a case study, J. Apic. Res. 30, 87–97.
Fussell M., Corbet S.A. (1992) Flower usage by bumble-bees: a basis for forage plan management, J. Appl. Ecol. 29, 451–465.
Goulson D., Lye G.C., Darvill B. (2008) Decline and conservation of bumble bees, Annu. Rev. Entomol. 53, 191–208.
Hald A.B. (1999) Weed vegetation (wild flora) of long established organic versus conventional cereal fields in Denmark, Ann. Appl. Biol. 134, 307–314.
Haydak M.H. (1970) Honey bee nutrition, Annu. Rev. Entomol. 15, 143–156.
Holland J., Fahrig L. (2000) Effect of woody borders on insect density and diversity in crop fields: a landscape-scale analysis, Agric. Ecosyst. Environ. 78, 115–122.
Holzschuh A., Steffan-Dewenter I., Kleijn D., Tscharntke T. (2007) Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context, J. Appl. Ecol. 44, 41–49.
Holzgang O., Pfister H.P., Heynen D., Blant M., Righetti A., Berthoud G., Marchesi P.l, Maddalena T., Müri H., Wendelspiess M., Dändliker G., Mollet P., Bornhauser-Sieber U. (2002) Les corridors faunistiques en Suisse, Cahier de l’environnement No. 326, Office fédéral de l’environnement, des forêts et du paysage (OFEFP), Société suisse de Biologie de la Faune (SSBF), Station ornithologique suisse de Sempach, Berne, 120 p.
Holzgang O., Righetti A., Pfister H.P. (2005) Swiss wildlife corridors on paper, imagined and in the countryside, GAIA — Ecol. Perspect. Sci. Soc. 14, 148–151.
Hopwood J.L. (2008) The contribution of roadside grassland restorations to native bee conservation, Biol. Conserv. 141, 2632–2640.
Hopwood J.L. (2010) Pollinators and Roadsides: Verge Management for Bees and utterflies, The Xerces Society Invertebrate Conservation Fact Sheet.
Johnson R.M., Ellis M.D., Mullin C.A., Frazier M. (2010) Pesticides and honey bee toxicity — USA, Apidologie 41, 312–331.
Johnson R.M., Evans J.D., Robinson G.E., Berenbaum M.R. (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera), Proc. Natl. Acad. Sci. USA 106, 14790–14795.
Justes E., Thiébeau P., Cattin G., Larbre D., Nicolardot B. (2001) Libération d’azote après retournement d’une culture de luzerne: un effet sur deux campagnes, Perspectives Agricoles 264, 22–28.
Justes E., Dorsainvil F., Alexandre M., Thiébeau P. (2004) Simulation with STICS soil-crop model of catch crop effects on nitrate leaching during the fallow period and on N released for the succeeding main crop, in: Hatch D.R., Chadwick S.C., Jarvis J.A., Roker D.J. (Eds.), Controlling nitrogen flows and losses, Wageningen Academic Publishers, Wageningen, The Netherlands, pp. 444–446.
Kearns C.A., Inouye D.W., Waser N.M. (1998) Endangered mutualisms: the conservation of plant-pollinator interactions, Annu. Rev. Ecol. Syst. 29, 83–112.
Keller I., Fluri P., Imdorf A. (2005) Pollen nutrition and colony development in honey bees, Part II, Bee World 86, 27–34.
Kevan P.G. (1977) Blueberry crops in Nova Scotia and New Brunswick: pesticides and crop reductions, Can. J. Agr. Econ. 25, 61–64.
Kevan P.G., Phillips T. (2001) The economics of pollinator declines: assessing the consequences, Conserv. Ecol. 5, 8.
Kleijn D., Baquero R.A., Clough Y., Diaz M., De Esteban J., Fernandez F., Gabriel D., Herzog F., Holzschuh A., Johl R., Knop E., Kruess A., Marshall E.J.P., Steffan-Dewenter I., Tscharntke T., Verhulst J., West T.M., Yela J.L. (2006) Mixed biodiversity benefits of agri-environment schemes in five European countries, Ecol. Lett. 9, 243–254.
Klein A.M., Vaissière B.E., Cane J.H., Steffan-Dewenter I., Cunningham S.A., Kremen C., Tscharntke T. (2007) Importance of pollinators in changing landscapes for world crops, Proc. R. Soc. Lond. B Biol. 274, 303–313.
Kremen C., Williams N.M., Thorp R.W. (2002) Crop pollination from native bees at risk from agricultural intensification, Proc. Natl. Acad. Sci. USA 99, 16812–16816.
Lacas J.G., Voltz M., Gouy V., Carluer N., Gril J.J. (2005) Using grassed strips to limit pesticide transfer to surface water: a review, Agron. Sustain. Dev. 25, 253–266.
Lagerhöf J., Wallin H. (1993) The abundance of arthropods along two field margins with different types of vegetation composition: an experimental study, Agric. Ecosyst. Environ. 43, 141–154.
Lagerhöf J., Stark J., Svensson B. (1992) Margins of agricultural field as habitats for pollinating insects, Agric. Ecosyst. Environ. 40, 117–124.
Larsen T.H., Williams N., Kremen C. (2005) Extinction order and altered community structure rapidly disrupt ecosystem functioning, Ecol. Lett. 8, 538–547.
Le Conte Y., Ellis M., Ritter W. (2010) Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie 41, 353–363.
Le Roux X., Barbault R., Baudry J., Burel F., Doussan I., Garnier E., Herzog F., Lavorel S., Lifran R., Roger-Estrade J., Sarthou J.P., Trommetter M. (2008) Agriculture et biodiversité — Valoriser les synergies — Synthèse du rapport d’expertise — 2ème partie, Expertise scientifique collective INRA.
Longley M., Sotherton N.W. (1997) Factors determining the effects of pesticides upon butterflies inhabiting arable farmland, Agric. Ecosyst. Environ. 61, 1–12.
Mader E. (2008) Financial incentives for pollinator conservation, Newsletter of the Midwest Organic Tree Fruit Growers Network 3, 4–5.
Malraux J.-B., Parguel P. (2007) Préétude des relations entre la qualité des miels et pratiques herbagères en zone de production du morbier, Bull. Tech. Apic. 34, 55–67.
Mary B., Beaudoin N., Justes E., Machet J.M. (1999) Calculation of nitrogen mineralization and leaching in fallow soil using a simple dynamic model, Eur. J. Soil Sci. 50, 549–566.
Mattila H.R., Otis G.W. (2006) Influence of pollen diet in spring on development of honey bee (Hymenoptera: Apidae) colonies, J. Econ. Entomol. 99, 604–613.
Maurizio A. (1950) The influence of pollen feeding and brood rearing on the length of life and physiological condition of the honeybee, Bee World 31, 9–12.
Meek B., Loxton D., Sparks T., Pywell R., Pickett H., Nowakowski M. (2002) The effect of arable field margin composition on invertebrate biodiversity, Biol. Conserv. 106, 259–271.
Meisinger J.J., Hargrove W.L., Mikkelsen R.L., Williams J.R., Benson V.W. (1991) Effects of cover crops on groundwater quality, in: Hargrove W.L. (Ed.), Cover crops for clean water, Conservation Society, Jackson, Tennessee, USA, pp. 57–68.
Michener C.D. (2007) The bees of the world, 2nd edition, The Johns Hopkins University Press, Baltimore and London, USA and UK.
Murray T.E., Kuhlmann M., Potts S.G. (2009) Conservation ecology of bees: populations, species and communities, Apidologie 40, 211–236.
National Research Council (2007) Status of pollinators in North America, The National Academies Press, Washington DC, USA.
Nearing M.A., Jetten V., Baffaut C., Cerdan O., Couturier A., Hernandez M., Le Bissonnais Y., Nichols M.H., Nunes J.P., Renschler C.S., Souchere V., van Oost K. (2005) Modelling response of soil erosion and runoff to changes in precipitation and cover, Catena 61, 131–154.
Ockinger E., Smith H.G. (2007) Semi-natural grasslands as population sources for pollinating insects in agricultural landscapes, J. Appl. Ecol. 44, 50–59.
Oldroyd B.P. (2007) What’s killing American honey bees? PLoS Biol. 5, 1195–1199.
Pedersen K., Omholt S.W. (1993) A comparison of diets for honeybee, Norwegian J. Agric. Sci. 7, 213–219.
Pienkowski M.W., Pain D.J. (1997) Farming and Birds in Europe: the Common Agricultural Policy and its implications for bird conservation, Academic Press, London, UK.
Plantureux S., Peeters A., Mccracken D. (2005) Biodiversity in intensive grasslands: effects of management, improvement and challenges, Agron. Res. 3, 153–164.
Pywell R.F., Warman E.A., Carvell C., Sparks T.H., Dicks L.V., Bennett D., Wright A., Critchley C.N.R., Sherwood A. (2005) Providing foraging resources for bumblebees in intensively farmed landscapes, Biol. Conserv. 121, 479–494.
Rasmont P., Mersch P. (1988) Première estimation de la dérive faunique chez les bourdons de la Belgique (Hymenoptera: Apidae), Ann. Soc. R. Zool. Belgique, 118, 141–147.
Richards A.J. (2001) Does low biodiversity resulting from modern agricultural practice affect crop pollination and yield? Ann. Bot.-London 88, 165–172.
Ricketts T.H., Regetz J., Steffan-Dewenter I., Cunningham S.A., Kremen C., Bogdanski A., Gemmill-Herren B., Greenleaf S.S., Klein A.M., Mayfield M.M., Morandin L.A., Ochieng A., Viana B.F. (2008) Landscape effects on crop pollination services: are there general patterns? Ecol. Lett. 11, 499–515.
Ries L., Debinski D.M., Wieland M.L. (2001) Conservation value of roadside prairie restoration to butterfly communities, Conserv. Biol. 15, 401–411.
Steffan-Dewenter I., Munzenberg U., Burger C., Thies C., Tscharntke T. (2002) Scale-dependent effects of landscape context on three pollinator guilds, Ecology 83, 1421–1432.
Steffan-Dewenter I., Potts S.G., Packer L. (2005) Pollinator diversity and crop pollination services are at risk, Trends Ecol. Evol. 20, 1–2.
Steffan-Dewenter I., Tscharntke T. (1999) Effects of habitat isolation on pollinator communities and seed set, Oecologia 121, 432–440.
Thönnissen C., Mimore D.J., Ladha J.K., Olk D.C., Schmidhlater U. (2000) Legume decomposition and nitrogen release when applied as green manures to tropical vegetable production systems, Agron. J. 92, 253–260.
UK Game Conservancy (1994) Game and shooting crops, Game Conservancy, Fordingbridge, Hampshire, UK.
USDA National Agroforestry Center (2006) Agroforestry: Sustaining Native Bee Habitat For Crop Pollination, Agroforestry Notes, August 2006, pp. 1–4.
Vaughan M., Skinner M. (2008) Using Farm Bill Programs for Pollinator Conservation, USDA-NRCS National Plant Data Center, online: http:// www.xerces.org/wp-content/uploads/2008/11/using_farm_bill_programs_xerces_society.pdf.
Vaughan M., Mader E., Norment J., Keirstead D., Alexander T., Barrett N. Schreier B., Lipsky A., Giorgi K., Henery H., Stubbs C. (2009) New England Pollinator Conservation Handbook, USDA-NRCS, online: ftp://ftp-fc.sc.egov.usda.gov/NH/WWW/Technical/New_England_NRCS_Pollinator_Tech_Note_FINAL.pdf.
Watanabe M.E. (1994) Pollination worries rise as honey bees decline, Science 265, 1170–1170.
Way J.M. (1977) Roadside verges and conservation in Britain: a review, Biol. Conserv. 12, 65–74.
Whittingham M.J. (2007) Will agri-environment schemes deliver substantial biodiversity gain, and if not why not? J. Appl. Ecol. 44, 1–5.
Williams I.H., Christian D.G. (1991) Observations on Phacelia tanacetifolia Bentham (Hydrophyllaceae) as a food plant for honey bees and bumble bees, J. Apic. Res. 30, 3–12.
Yliskyla-Peuralahti J. (2003) Biodiversity — a new spatial challenge for Finnish agri-environmental policies? J. Rural Stud. 19, 215–231.
Author information
Authors and Affiliations
Corresponding author
Additional information
Manuscript editor: Yves Le Conte
Rights and permissions
About this article
Cite this article
Decourtye, A., Mader, E. & Desneux, N. Landscape enhancement of floral resources for honey bees in agro-ecosystems. Apidologie 41, 264–277 (2010). https://doi.org/10.1051/apido/2010024
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1051/apido/2010024