Flower Strips in Wheat Intercropping System: Effect on Pollinator Abundance and Diversity in Belgium

[en] The decline of pollinators in agricultural areas has been observed for some decades, this being partly due to landscape simplification in intensive agrosystems. Diversifying agricultural landscapes by sowing flower strips within fields could reduce these adverse effects on biodiversity. In this context, the study presented here aimed at assessing and comparing the abundance and diversity of bees (Hymenoptera: Anthophila) and hoverflies (Diptera: Syrphidae) found and visiting flowers in three types of flower strips in Belgium: (i) a mixture of 11 wild flowers, (ii) a monofloral strip of Dimorphoteca pluvialis (Asteraceae) and (iii) a monofloral strip of Camelina sativa (Brassicaceae), where the last two are considered to be intercrops since they are valuable on the market, all sown within a field of winter wheat (Triticum aestivum L.). Pollinators were captured with pan traps and by netting in standardised transects from May to July 2017. One-thousand one-hundred and eighty-four individuals belonging to 43 bee species and 18 hoverfly species were collected. Significant differences in hoverfly diversity were found between the different flower strips. The multifloral treatment supported a greater diversity of syrphid species. Various pollinator species visited the different flowers composing the mixture and also D. pluvialis. The pollinator community proved to be predominantly generalist, with the exception of an oligolectic species in Belgium, Andrena nitidiuscula. Moreover, the three tested flower strips were effective in attracting hoverflies, among them natural enemies of insect pests. This study opens new perspectives in the design of intercropping systems with flower strips towards the design of sustainable agro-ecosystems. Improving economic profitability of sowing flower strips could encourage farmers to diversify their agricultural systems and foster conservation biology strategies.

Disciplines :

Entomology & pest control

Author, co-author :

Amy, Clara ; Université de Liège - ULiège > Gembloux Agro-Bio Tech

Noël, Grégoire ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs

Hatt, Séverin ; Université de Liège - ULiège > R&D Direction : Chercheurs ULg en mobilité

Uyttenbroeck, Roel

Van de Meutter, Frank

Genoud, David

Francis, Frédéric ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Gestion durable des bio-agresseurs

Language :

English

Title :

Flower Strips in Wheat Intercropping System: Effect on Pollinator Abundance and Diversity in Belgium

Publication date :

04 September 2018

Journal title :

Insects

eISSN :

2075-4450

Publisher :

Multidisciplinary Digital Publishing Institute (MDPI), Switzerland

Volume :

Issue :

Pages :

114

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 05 October 2018

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Bibliography

Rasmont, P.; Devalez, J.; Pauly, A.; Michez, D.; Radchenko, V.G. Addition to the checklist of IUCN European wild bees (Hymenoptera: Apoidea). Ann. Soc. Entomol. Fr. 2017, 53, 17–32.
Michener, C.D. The Bees of the World, 2nd ed.; Johns Hopkins University Press: Baltimore, MD, USA, 2007; p. 972. ISBN 978-0-8018-6133-8.
Pfiffner, L.; Müller, A. Abeilles Sauvages et Pollinisation; FIBL, Faits et Chiffres: Frick, Suisse, 2007; p. 8.
Fründ, J.; Linsenmair, K.E.; Bluethgen, N. Pollinator diversity and specialization in relation to flower diversity. Oikos 2010, 119, 1581–1590.
Rader, R.; Bartomeus, I.; Garibaldi, L.A.G.; Michael, P.D.H.; Brad, G.W.; Rachael, C.; Saul, A.M.; Margaret, M.A.; Anthony, D.A.; Georg, K.S.B. et al. Non-bee insects are important contributors to global crop pollination. Proc. Natl. Acad. Sci. USA 2015, 11, 146–151.
Jauker, F.; Bondarenko, B.; Becker, H.C.; Steffan-Dewenter, I. Pollination efficiency of wild bees and hoverflies provided to oilseed rape. Agric. For. Entomol. 2012, 14, 81–87.
Orford, K.; Vaughan, I.; Memmott, J. The forgotten flies: The importance of non-syrphid Diptera as pollinators. Proc. Biol. Sci. 2015, 282, 20142934.
Breeze, T.D.; Gallai, N.; Garibaldi, L.A.; Li, X.S. Economic measures of pollination services: Shortcomings and future directions. Trends Ecol. Evol. 2016, 13, 927–939.
Klein, A.M.; Vaissière, B.E.; Cane, J.H.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Tscharntke, T. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B 2007, 274, 303–313.
Jacquemin, F.; Violle, C.; Rasmont, P.; Dufrêne, M. Mapping the dependency of crops on pollinators in Belgium. One Ecosyst. 2017, 2, 9.
Cameron, S.A.; Loziera, J.D.; Strange, J.P.; Kochb, J.B.; Cordesa, N.; Solterd, L.F.; Griswold, T.L. Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. USA 2011, 108, 662–667.
Carvalheiro, L.G.; Kunin, W.E.; Keil, P.; Aguirre-Gutiérrez, J.; Ellis, W.E.; Fox, R.; Groom, Q.; Hennekens, S.; Van Landuyt, W.; Maes, D. et al. Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol. Lett. 2013, 16, 870–878.
Potts, S.; Biesmeijer, W.; Bommarco, R.; Felicioli, A.; Fischer, M. Developing European conservation and mitigation tools for pollination services: Approaches of the STEP (Status and Trends of European Pollinators) project. J. Appl. Biol. 2011, 50, 154–162.
Carrié, R. Hétérogénéité des Paysages et des Pratiques Agricoles: Effets Sur la Diversité des Abeilles Sauvages et la Pollinisation. Ph.D. Thesis, Institut National Polytechnique de Toulouse, Toulouse, France, 2016.
Deguines, N.; Jono, C.; Baude, M.; Henry, M.; Julliard, R.; Fontaine, C. Large-scale trade-off between agricultural intensification and crop pollination services. Front. Ecol. Environ. 2014, 12, 212–217.
Potts, S.G.; Imperatriz-Fonseca, V.; Ngo, H.T.; Aizen, M.A.; Biesmeijer, J.C.; Breeze, T.D.; Dicks, L.V.; Garibaldi, L.A.; Hill, R.; Settele, J. et al. Safeguarding pollinators and their values to human well-being. Nature 2016, 540, 220–229.
Eilers, E.J.; Kremen, C.; Smith Greenleaf, S.; Garber, A.K.; Klein, A.M. Contribution of pollinator-mediated crops to nutrients in the human food supply. PLoS ONE 2011, 6, e21363.
Suttle, K.B. Pollinators as mediators of top-down effects on plants. Ecol. Lett. 2003, 6, 688–694.
European Commission. Agri-Environment Measures. Overview on General Principles, Types of Measures and Application 2015, European Commission, Directorate General for Agriculture and Rural Development. Available online: https://ec.europa.eu/agriculture/sites/agriculture/files/publi/reports/agrienv/rep_en.pdf (accessed on 24 June 2018).
NaTagriWal. 1995–2015: 20 Années de Mesures Agro-Environnementales (MAE) en Wallonie; Dossier de Presse; NaTagriWal: Belgium, 2015; p. 4.
Haaland, C.; Naisbit, R.E.; Bersier, L.F. Sown wildflower strips for insect conservation: A review. Insect Conserv. Divers. 2011, 4, 60–80.
Uyttenbroeck, R.; Hatt, S.; Paul, A.; Boeraeve, F.; Piqueray, J.; Francis, F.; Danthine, S.; Frédérich, M.; Dufrêne, M.; Bodson, B. et al. Pros and cons of flowers strips for farmers. A review. Biotechnol. Agron. Soc. Environ. 2016, 20, 225–235.
Le Féon, V. Insectes Pollinisateurs Dans les Paysages agricoles: Approche Pluri-Echelle du Rôle des Habitats Semi-Naturels, des Pratiques Agricoles et des Cultures Entomophiles. Ph.D. Thesis, Université Rennes, Rennes, France, 2010.
Warzercha, D.; Diekotter, T.; Wolters, V.; Jauker, F. Attractiveness of wildflower mixtures for wild bees and hoverflies depends on some key plant species. Insect Conserv. Divers. 2018, 11, 32–41.
Potts, S.G.; Vulliamy, B.; Dafni, A.; Neeman, G.; Willmer, P. Linking bees and flowers: How do floral communities structure pollinator communities? Ecology 2003, 84, 2628–2642.
Uyttenbroeck, R.; Piqueray, J.; Hatt, S.; Mahy, G.; Monty, A. Increasing plant functional diversity is not the key for supporting pollinators in wildflower strips. Agric. Ecosyst. Environ. 2017, 249, 144–155.
Barbir, J.; Badenes-Pérez, F.R.; Fernández-Quintanilla, C.; Dorado, J. The attractiveness of flowering herbaceous plants to bees (Hymenoptera: Apoidea) and hoverflies (Diptera: Syrphidae) in agro-ecosystems of Central Spain. Agric. For. Entomol. 2015, 17, 20–28.
Hatt, S.; Boeraeve, F.; Artru, S.; Dufrêne, M.; Francis, F. Spatial diversification of agroecosystems to enhance biological control and other regulating services: An agroecological perspective. Sci. Total Environ. 2018, 621, 600–611.
Bedoussac, L.; Journet, E.P.; Hauggaard-Nielsen, H.; Naudin, C.; Corre-Hellou, G.; Jensen, E.S.; Prieur, L.; Justes, E. Ecological principles underlying the increase of productivity achieved by cereal-grain legume intercrops in organic farming: A review. Agron. Sustain. Dev. 2015, 35, 911–935.
Lopes, T.; Hatt, S.; Xu, Q.; Chen, J.; Liu, Y.; Francis, F. Wheat (Triticum aestivum L.)-based intercropping systems for biological pest control. Pest Manag. Sci. 2016, 72, 2193–2202.
Boudreau, M.A. Diseases in intercropping systems. Annu. Rev. Phytopathol. 2013, 51, 499–519.
Campbelle, M. Camelina—An Alternative Oil Crop. Biokerosene 2018, 12, 259–275.
Singer, S.D.; Weselake, R.J. Production of other Bioproducts from Plant Oils. Plant Bioprod. 2018, 59–85.
Pinochet, X. La marche vers les hybrides: Premiers bilans. La Filière Aujourd’hui Demain 1994, 1, 166–172.
Gugel, R.K.; Falk, K.C. Agronomic and seed quality evaluation of Camelina sativa in western Canada. Can. J. Plant Sci. 2006, 86, 1047–1058.
Westphal, C.; Bommarco, R.; Carré, G.; Lamborn, E.; Petanidou, T.; Potts, S.G.; Settele, J. Measuring bee diversity in different European habitats and biogeographical regions. Ecol. Monogr. 2008, 78, 653–671.
Fontaine, B. Suivi des Papillons Communs sur les Parcelles de Maïs BT en Régions Aquitaine et Midi-Pyrénées en 2007; MNHN: Paris, France, 2008; 9p.
Geroff, R.K.; Gibbs, J.; McCravy, K.W. Assessing bee (Hymenoptera: Apoidea) diversity of an Illinois restored tallgrass prairie: Methodology and conservation considerations. J. Insect Conserv. 2014, 18, 951–964.
Gezon, Z.J.; Wyman, E.S.; Ascher, J.S.; Inouye, D.W.; Irwin, R.E. The effect of repeated, lethal sampling on wild bee abundance and diversity. Methods Ecol. Evol. 2015, 6, 1044–1054.
Mouret, P.H.; Carre, G.; Roberts, S.P.M.; Morison, N.; Vaissiere, B.E. Mise en place d’une collection d’abeilles (Hymenoptera, Apoidae) dans le cadre d’une étude de la biodiversité. Osmia 2007, 1, 8–15.
Scheuchl, E. Clé des Genres de la Super-Famille des Apoidae; Apollo Books: Royaume-Uni, 2000; 11p.
Patiny, S.; Terzo, M. Catalogue et Clé des Sous-Genres et Espèces du Genre Andrena de Belgique et du Nord de la France (Hymenoptera, Apoidae); Université de Mons: Mons, Belgium, 2010; 39p.
Falk, S.; Lewington, R. Field Guide to the Bees of Great Britain and Ireland (Field Guides); British Wildlife Publishing Ltd.: Oxford, UK, 2015; 432p, ISBN 191038903X.
Pauly, A. Clés Illustrées Pour L’identification des Abeilles de Belgique et des Régions Limitrophes (Hymenoptera: Apoidae) I. Halictidae; Document de Travail du Projet BELBEES; Institut Royal des Sciences Naturelles de Belgique: Bruxelles, Belgium, 2015; 18p.
Uyttenbroeck, R.; Hatt, S.; Piqueray, J.; Paul, A.; Bodson, B.; Francis, F.; Monty, A. Creating perennial flower strips: Think functional! Agric. Agric. Sci. Procedia 2015, 6, 95–101.
R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2018; Available online: https://www.R-project.org/ (accessed on 10 July 2018).
Wickham, H. Ggplot2 Elegant graphics for data analysis. Biometrics 2016, 67, 678–679.
Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; Stevens, M.H.H.; Wagner, H. Vegan: Community Ecology Package; R Package Version 2; R Core Team: Vienna, Austria, 2015; Volume 2-1, p. 280.
Marcon, E. Mesures de la Biodiversité. Ph.D. Thesis, AgroParisTech, Kourou, France, 2015.
Dinno, A. Dunn.test: Dunn’s Test of Multiple Comparisons Using Rank Sums; R Package Version 1.3.5; R Core Team: Vienna, Austria, 2017; Available online: https://CRAN.R-project.org/package=dunn.test (accessed on 22 July 2018).
Magurran, A.E. Measuring Biological Diversity; Blackwell Publishing: Oxford, UK, 2004; 132p.
Hill, N.O. Diversity and Evenness: A Unifying Notation and Its Consequences. Ecology 1973, 54, 427–432.
Chao, A.; Gotelli, N.J.; Hsieh, T.C.; Sander, E.L.; Ma, K.M.; Colwell, R.K.; Ellison, A.M. Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. ESA 2014, 84, 45–67.
Colwell, R.K.; Chao, A.; Gotelli, N.J.; Lin, S.-Y.; Mao, C.X.; Chazdon, R.L.; Longino, J.T. Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J. Plant Ecol. 2012, 5, 3–21.
Chao, A.; Jost, L. Coverage-based rarefaction and extrapolation: Standardizing samples by completeness rather than size. Ecology 2012, 93, 2533–2547.
Nieto, A.; Roberts, S.P.M.; Kemp, J.; Rasmont, P.; Kuhlmann, M.; García Criado, M.; Biesmeijer, J.C.; Bogusch, P.; Dathe, H.H.; De la Rúa, P. et al. European Red List of Bees; Publication Office of the European Union: Luxembourg, 2014; 96p.
Colwell, R.K.; Mao, C.X.; Chang, J. Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 2004, 85, 2717–2727.
Syrph the Net Database. Available online: http://www.biodiversityireland.ie/projects/irish-pollinator-initiative/hoverflies/syrph-the-net/ (accessed on 27 February 2018).
Lindgren, J.; Lindborg, R.; Cousins, S. Local conditions in small habitats and surrounding landscape are important for pollination services, biological pest control and seed predation. Agric. Ecosyst. Environ. 2018, 251, 107–113.
Williams, N.M.; Crone, E.E.; Roulston, H.; Minckley, R.; Packer, L.; Potts, S. Ecological and life-history traits predict bee species responses to environmental disturbances. Biol. Conserv. 2010, 143, 2280–2291.
Potts, S.; Biesmeijer, K.; Bommarco, R.; Breeze, T.; Carvalheiro, L.; Franzén, M.; González-Varo, J.P.; Holz-Schuh, A.; Kleijn, D.; Klein, A.M. et al. Status and Trends of European Pollinators. Status and Trends of European Pollinators. Key Findings of the STEP Project; Pensoft Publishers: Sofia, Bulgaria, 2015; 72p, ISBN 978-954-642-762-5.
Senapathi, D.; Goddard, M.A.; Kunin, W.E.; Baldock, C.R. Landscape impacts on pollinator communities in temperate systems: Evidence and knowledge gaps. Funct. Ecol. 2017, 31, 26–37.
Andersson, G.K.S.; Birkhofer, K.; Rundlöf, M.; Smith, H.G. Landscape heterogeneity and farming practice alter the species composition and taxonomic breadth of pollinator communities. Basic Appl. Ecol. 2013, 7, 540–546.
Taki, H.; Kevan, P.G.; Ascher, S. Landscape effects of forest loss in a pollination system. Landsc. Ecol. 2007, 22, 1575–1587.
Wood, T.J.; Holland, J.M. Goulson, Diet characterisation of solitary bees on farmland: Dietary specialisation predicts rarity. Biodivers. Conserv. 2016, 13, 2655–2671.
Kleijn, D.; Langeveldeb, F.V. Interacting effects of landscape context and habitat quality on flower visiting insects in agricultural landscapes. Basic Appl. Ecol. 2006, 7, 201–214.
The IUCN Red List of Threatened Species, Lasioglossum Morio. Available online: http://www.iucnredlist.org/details/19199775/1 (accessed on 15 March 2018).
Branquart, E.; Hemptinne, J.L. Selectivity in the exploitation of floral resources by hoverflies (Diptera: Syrphinae). Ecography 2000, 23, 732–742.
Morales, I.; Díaz, B.M.; Nebreda, M.; López-Lastra, C.; Goldarazena, A.; Sánchez, J.A.; Pineda, A.; Marcos-García, M.A.; Fereres, A. Principales agentes de biocontrol en cultivos de lechuga en la zona centro de España. Rev. Hortic. 2007, 49, 46–49.
Chabert, A.; Sarthou, J.P. Practices of conservation agriculture prevail over cropping systems and landscape heterogeneity in understanding the ecosystem service of aphid biocontrol. Agric. Ecosyst. Environ. 2017, 249, 70–79.
Mueller, A.L.; Dauber, J. Hoverflies (Diptera: Syrphidae) benefit from a cultivation of the bioenergy crop Silphium perfoliatum L. (Asteraceae) depending onlarval feeding type, landscape composition and crop management. Agric. For. Entomol. 2016, 18, 419–431.
Raemakers, I. De schermbloemzandbij Andrena nitidiuscula terug in Nederland (Hymenoptera: Apidae). Nederlandse Faunistische Mededelingen 2005, 23, 13–16.
BWARS Bees, Wasps & Ants Recording Society. Available online: http://www.bwars.com/bee/andrenidae/andrena-nitidiuscula (accessed on 27 February 2018).
Popic, T.J.; Davila, Y.C.; Wardle, G.M. Evaluation of common methods for sampling invertebrate pollinator assemblages: Net sampling out-perform pan traps. PLoS ONE 2013, 8, e66665.
Bilan Climatologique Saisonnier, Printemps. 2017. Available online: http://www.meteo.be/resources/climateReportWeb/bilan_climatologique_saisonnier_2017_S2.pdf (accessed on 27 February 2018).
Rollin, O.; Benelli, G.; Benvenuti, S.; Decourtye, A.; Wratten, S.D.; Canale, A.; Desneux, N. Weed-insect pollinator networks as bio-indicators of ecological sustainability in agriculture: A review. Agron. Sustain. Dev. 2015, 36, 8.
Fornoff, F.; Klein, A.M.; Hartig, F.; Benadi, G.; Venjakob, C.; Schaefer, H.M.; Ebeling, A. Functional flower traits and their diversity drive pollinator visitation. Oikos 2017, 126, 1020–1030.
Van Rijn, P.C.; Wäckers, F.L. Nectar accessibility determines fitness, flower choice and abundance of hoverflies that provide natural pest control. J. Appl. Ecol. 2016, 53, 925–933.
Bauer, A.; Clayton, M.; Brunnet, J. Floral traits influencing plant attractiveness to three bee species: Consequences for plant reproductive success. Am. J. Bot. 2017, 104, 772–781.
Colley, M.R.; Luna, J.M. Relative attractiveness of potential beneficial insectary plants to aphidophagous hoverflies (Diptera: Syrphidae). Environ. Entomol. 2000, 29, 1054–1059.
McCravy, K.W.; Ruholl, J.D. Bee (Hymenoptera: Apoidae) diversity and sampling methodology in a Midwestern USA deciduous forest. Insects 2017, 8, 81.
Müller, H. Alpenblumen, Ihre Befruchtung Durch Insekten und Ihre Anpassungen an Dieselben; Arkose Press: Leipzig, Germany, 1881.
Kolz, S.; Kühn, I.; Durka, W. BIOLFLOR—Eine Datenbank zu Biologisch-Ökologischen Merkmalen der Gefäßpflanzen in Deutschland; Bundesamt für Naturschutz: Bonn, Germnay, 2002; Available online: http://www2.ufz.de/biolflor/index.jsp (accessed on 12 May 2018).
Gómez, J.M.; Bosch, J.; Perfectti, F.; Fernández, J.D.; Abdelaziz, M.; Camacho, J.P.M. Association between floral traits and rewards in Erysimum mediohispanicum (Brassicaceae). Ann. Bot. 2008, 101, 1413–1420.
Hatt, S.; Lopes, T.; Boeraeve, F.; Chen, J.; Francis, F. Pest regulation and support of natural enemies in agriculture: Experimental evidence of within field wildflower strips. Ecol. Eng. 2017, 98, 240–245.