Dominance of honey bees is negatively associated with wild bee diversity in commercial apple orchards regardless of management practices

Weekers, Timothy; Marshal, Leon; Leclereq, Nicolas; Wood, Thomas James; Cejas Acuna, Diego Manuel; Drepper, Bianca; Hutchinson, Louise; Michez, Denis; Molenberg, Jean-Marc; Smagghe, Guy; Vandamme, Peter; Vereecken, Nicolas

Article (Scientific journals)

Weekers, Timothy; Marshal, Leon; Leclereq, Nicolas et al.

2022 • In Agriculture, Ecosystems and Environment, 323

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/20.500.12907/14031

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Weekers_et_al._(2021)_Dominance_of_honey_bees_is_associated_with_lower_wild_bee_diversity.pdf

Publisher postprint (3.46 MB)

Request a copy

All documents in ORBi UMONS are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Abstract :

[en] Commercial apple production relies on managed honey bees (Apis mellifera) for pollination, and on intensive management for pest control. Previous studies have highlighted the potentially detrimental effects of intensive crop management on wild bee diversity in agroecosystems, potentially jeopardizing the pollination services they provide. However, the extent to which honey bee dominance and crop management interact under field-realistic conditions and drive the structure of wild bee assemblages has not been investigated so far. In this study, we measured species richness, as well as the functional and phylogenetic diversity of wild bee assemblages in 36 paired organic and non-organic apple orchards during their flowering season and along a geographic gradient across western Europe. Our results show a strong significant and negative association between honey bee dominance and all wild bee diversity metrics, regardless of local management. Semi-natural habitats had a significant and positive effect on functional diversity, while urbanization and crop cover around the orchards showed no effect on all measured diversity metrics. A greater number of species exhibited less common, or frequent, combinations of functional traits at sites with high honey bee dominance, especially larger bee species with longer tongues. Collectively, we show that wild bee diversity decreases with increasing honey bee dominance, and that this negative association is not buffered by alternative (i.e., organic) management practices in commercial apple orchards. Although organic farming can bring about biodiversity benefits, our study demonstrates that, in the context of commercial apple production, other measures are needed to enhance and harness biodiversity for sustainable and profitable crop production. In particular, a lowered reliance on honey bees and a redesign of orchards through configurational crop heterogeneity and/or the restoration of in-field semi-natural elements are required beyond agricultural input substitution.

Author, co-author :

Weekers, Timothy

Marshal, Leon

Leclereq, Nicolas

Wood, Thomas James ; Université de Mons > Faculté des Sciences > Service de Zoologie

Cejas Acuna, Diego Manuel ; Université de Mons > Faculté des Sciences > Service de Zoologie

Drepper, Bianca

Hutchinson, Louise

Michez, Denis ; Université de Mons > Faculté des Sciences > Service de Zoologie

Molenberg, Jean-Marc

Smagghe, Guy

Vandamme, Peter

Vereecken, Nicolas

Language :

English

Title :

Dominance of honey bees is negatively associated with wild bee diversity in commercial apple orchards regardless of management practices

Publication date :

01 January 2022

Journal title :

Agriculture, Ecosystems and Environment

ISSN :

0167-8809

eISSN :

1873-2305

Publisher :

Elsevier, Netherlands

Volume :

323

Peer reviewed :

Peer Reviewed verified by ORBi

Research unit :

S869 - Zoologie

Research institute :

R100 - Institut des Biosciences

Available on ORBi UMONS :

since 06 December 2021

Statistics

Number of views

133 (3 by UMONS)

Number of downloads

4 (1 by UMONS)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

Bibliography

Aizen, M.A., Garibaldi, L.A., Cunningham, S.A., Klein, A.M., Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Curr. Biol. 18 (2008), 1572–1575, 10.1016/j.cub.2008.08.066.
Alignier, A., Solé-Senan, X.O., Robleño, I., Baraibar, B., Fahrig, L., Giralt, D., Gross, N., Martin, J.L., Recasens, J., Sirami, C., Siriwardena, G., Bosem Baillod, A., Bertrand, C., Carrié, R., Hass, A., Henckel, L., Miguet, P., Badenhausser, I., Baudry, J., Bota, G., Bretagnolle, V., Brotons, L., Burel, F., Calatayud, F., Clough, Y., Georges, R., Gibon, A., Girard, J., Lindsay, K., Minano, J., Mitchell, S., Patry, N., Poulin, B., Tscharntke, T., Vialatte, A., Violle, C., Yaverscovski, N., Batáry, P., Configurational crop heterogeneity increases within-field plant diversity. J. Appl. Ecol. 57 (2020), 654–663, 10.1111/1365-2664.13585.
Arnold, S.E.J., Elisante, F., Mkenda, P.A., Tembo, Y.L.B., Ndakidemi, P.A., Gurr, G.M., Darbyshire, I.A., Belmain, S.R., Stevenson, P.C., Beneficial insects are associated with botanically rich margins with trees on small farms. Sci. Rep., 2021, 11, 10.1038/S41598-021-94536-3.
Bänsch, S., Tscharntke, T., Ratnieks, F.L.W., Härtel, S., Westphal, C., Foraging of honey bees in agricultural landscapes with changing patterns of flower resources. Agric. Ecosyst. Environ., 291, 2020, 106792, 10.1016/j.agee.2019.106792.
Bates, D., Mächler, M., Bolker, B.M., Walker, S.C., Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67 (2015), 1–48, 10.18637/jss.v067.i01.
Birkhofer, K., Andersson, G.K.S., Bengtsson, J., Bommarco, R., Dänhardt, J., Ekbom, B., Ekroos, J., Hahn, T., Hedlund, K., Jönsson, A.M., Lindborg, R., Olsson, O., Rader, R., Rusch, A., Stjernman, M., Williams, A., Smith, H.G., Relationships between multiple biodiversity components and ecosystem services along a landscape complexity gradient. Biol. Conserv. 218 (2018), 247–253, 10.1016/j.biocon.2017.12.027.
Blitzer, E.J., Gibbs, J., Park, M.G., Danforth, B.N., Pollination services for apple are dependent on diverse wild bee communities. Agric. Ecosyst. Environ. 221 (2016), 1–7, 10.1016/j.agee.2016.01.004.
Boyle, E.E., Adamowicz, S.J., Community phylogenetics: assessing tree reconstruction methods and the utility of DNA barcodes. PLoS One, 10, 2015, e0126662, 10.1371/journal.pone.0126662.
Breeze, T.D., Bailey, A.P., Balcombe, K.G., Potts, S.G., Pollination services in the UK: how important are honeybees?. Agric. Ecosyst. Environ. 142 (2011), 137–143, 10.1016/j.agee.2011.03.020.
Brittain, C., Williams, N., Kremen, C., Klein, A.M., 2013. Synergistic effects of non-Apis bees and honey bees for pollination services. Proc. R. Soc. B Biol. Sci. 280, 1–7. 〈 https://doi.org/10.1098/rspb.2012.2767〉.
Buchhorn, M., Lesiv, M., Tsendbazar, N.E., Herold, M., Bertels, L., Smets, B., Copernicus global land cover layers-collection 2. Remote Sens., 2020, 12, 10.3390/rs12061044.
Campbell, A.J., Wilby, A., Sutton, P., Wäckers, F.L., Do sown flower strips boost wild pollinator abundance and pollination services in a spring-flowering crop? A case study from UK cider apple orchards. Agric. Ecosyst. Environ. 239 (2017), 20–29, 10.1016/j.agee.2017.01.005.
Cardoso, P., Rigal, F., Carvalho, J.C., BAT - biodiversity assessment tools, an R package for the measurement and estimation of alpha and beta taxon, phylogenetic and functional diversity. Methods Ecol. Evol. 6 (2015), 232–236, 10.1111/2041-210X.12310.
Cariveau, D.P., Nayak, G.K., Bartomeus, I., Zientek, J., Ascher, J.S., Gibbs, J., Winfree, R., The allometry of bee proboscis length and its uses in ecology. PLoS One, 11, 2016, e0151482, 10.1371/journal.pone.0151482.
Carreck, N., Field guide to the bees of Great Britain and Ireland, By Stephen Falk. Illustrated by Richard Lewington. Bee World, 93, 2016, 85, 10.1080/0005772x.2016.1257474.
Droege, S., Tepedino, V.J., Lebuhn, G., Link, W., Minckley, R.L., Chen, Q., Conrad, C., Spatial patterns of bee captures in North American bowl trapping surveys. Insect Conserv. Divers. 3 (2010), 15–23, 10.1111/j.1752-4598.2009.00074.x.
FAOSTAT, 2020. FAOSTAT (WWW Document). 〈http://www.fao.org/faostat/en/#home〉. (Accessed 19 June 2020).
Fontaine, C., Dajoz, I., Meriguet, J., Loreau, M., Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol., 4, 2005, e1, 10.1371/JOURNAL.PBIO.0040001.
Forrest, J.R.K., Thorp, R.W., Kremen, C., Williams, N.M., Contrasting patterns in species and functional-trait diversity of bees in an agricultural landscape. J. Appl. Ecol. 52 (2015), 706–715, 10.1111/1365-2664.12433.
Fox, J., Weisberg, S., An R companion to applied regression. Robust. Regres., 2014, 1–17.
Garibaldi, L.A., Carvalheiro, L.G., Vaissière, B.E., Gemmill-Herren, B., Hipólito, J., Freitas, B.M., Ngo, H.T., Azzu, N., Sáez, A., Åström, J., An, J., Blochtein, B., Buchori, D., Chamorro García, F.J., Da Silva, F.O., Devkota, K., De Fátima Ribeiro, M., Freitas, L., Gaglianone, M.C., Goss, M., Irshad, M., Kasina, M., Pacheco Filho, A.J.S., Piedade Kiill, L.H., Kwapong, P., Parra, G.N., Pires, C., Pires, V., Rawal, R.S., Rizali, A., Saraiva, A.M., Veldtman, R., Viana, B.F., Witter, S., Zhang, H., Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science 351 (2016), 388–391, 10.1126/science.aac7287.
Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., Cunningham, S.A., Kremen, C., Carvalheiro, L.G., Harder, L.D., Afik, O., Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N.P., Dudenhöffer, J.H., Freitas, B.M., Ghazoul, J., Greenleaf, S., Hipólito, J., Holzschuh, A., Howlett, B., Isaacs, R., Javorek, S.K., Kennedy, C.M., Krewenka, K.M., Krishnan, S., Mandelik, Y., Mayfield, M.M., Motzke, I., Munyuli, T., Nault, B.A., Otieno, M., Petersen, J., Pisanty, G., Potts, S.G., Rader, R., Ricketts, T.H., Rundlöf, M., Seymour, C.L., Schüepp, C., Szentgyörgyi, H., Taki, H., Tscharntke, T., Vergara, C.H., Viana, B.F., Wanger, T.C., Westphal, C., Williams, N., Klein, A.M., Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 340 (2013), 1608–1611, 10.1126/science.1230200.
Gathmann, A., Tscharntke, T., Foraging ranges of solitary bees. J. Anim. Ecol. 71 (2002), 757–764, 10.1046/j.1365-2656.2002.00641.x.
Geslin, B., Gauzens, B., Baude, M., Dajoz, I., Fontaine, C., Henry, M., Ropars, L., Rollin, O., Thébault, E., Vereecken, N.J., Massively introduced managed species and their consequences for plant–pollinator interactions. Advances in Ecological Research, 2017, Academic Press Inc, 147–199, 10.1016/bs.aecr.2016.10.007.
Geslin, B., Gauzens, B., Thébault, E., Dajoz, I., Plant pollinator networks along a gradient of urbanisation. PLoS One, 8, 2013, e63421, 10.1371/journal.pone.0063421.
Gotelli, N.J., Colwell, R.K., Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4 (2001), 379–391, 10.1046/j.1461-0248.2001.00230.x.
Grab, H., Branstetter, M.G., Amon, N., Urban-Mead, K.R., Park, M.G., Gibbs, J., Blitzer, E.J., Poveda, K., Loeb, G., Danforth, B.N., Agriculturally dominated landscapes reduce bee phylogenetic diversity and pollination services. Science 363 (2019), 282–284, 10.1126/science.aat6016.
Graystock, P., Ng, W.H., Parks, K., Tripodi, A.D., Muñiz, P.A., Fersch, A.A., Myers, C.R., McFrederick, Q.S., McArt, S.H., Dominant bee species and floral abundance drive parasite temporal dynamics in plant-pollinator communities. Nat. Ecol. Evol. 4 (2020), 1358–1367, 10.1038/s41559-020-1247-x.
Guala, G., Döring, M., 2021. Integrated taxonomic information system (ITIS) (WWW Document). Choice Rev. Online. 〈 https://doi.org/10.5860/choice.49-6871〉.
Hesselbarth, M.H.K., Sciaini, M., With, K.A., Wiegand, K., Nowosad, J., Landscapemetrics: an open-source R tool to calculate landscape metrics. Ecography 42 (2019), 1648–1657, 10.1111/ecog.04617.
Hill, S., Redesigning the food system for sustainability. Alternatives 12 (1985), 32–36.
Hillebrand, H., Bennett, D.M., Cadotte, M.W., Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89 (2008), 1510–1520, 10.1890/07-1053.1.
Hoehn, P., Tscharntke, T., Tylianakis, J.M., Steffan-Dewenter, I., 2008. Functional group diversity of bee pollinators increases crop yield. Proc. R. Soc. B Biol. Sci., 275, 2283–2291. 〈 https://doi.org/10.1098/rspb.2008.0405〉.
Holzschuh, A., Steffan-Dewenter, I., Tscharntke, T., Agricultural landscapes with organic crops support higher pollinator diversity. Oikos 117 (2008), 354–361, 10.1111/j.2007.0030-1299.16303.x.
Hristov, P., Shumkova, R., Palova, N., Neov, B., Factors associated with honey bee colony losses: a mini-review. Vet. Sci. 7 (2020), 1–16, 10.3390/vetsci7040166.
Hung, K.L.J., Kingston, J.M., Lee, A., Holway, D.A., Kohn, J.R., 2019. Non-native honey bees disproportionately dominate the most abundant floral resources in a biodiversity hotspot. Proc. R. Soc. B Biol. Sci., 286. 〈 https://doi.org/10.1098/rspb.2018.2901〉.
Isbell, F., Adler, P.R., Eisenhauer, N., Fornara, D., Kimmel, K., Kremen, C., Letourneau, D.K., Liebman, M., Polley, H.W., Quijas, S., Scherer-Lorenzen, M., Benefits of increasing plant diversity in sustainable agroecosystems. J. Ecol. 105 (2017), 871–879, 10.1111/1365-2745.12789.
Joshi, N.K., Leslie, T., Rajotte, E.G., Biddinger, D.J., Environmental impacts of reduced-risk and conventional pesticide programs differ in commercial apple orchards, but similarly influence pollinator community. Chemosphere, 240, 2020, 124926, 10.1016/j.chemosphere.2019.124926.
Joshi, N.K., Otieno, M., Rajotte, E.G., Fleischer, S.J., Biddinger, D.J., Proximity to woodland and landscape structure drives pollinator visitation in apple orchard ecosystem. Front. Ecol. Evol. 4 (2016), 1–9, 10.3389/fevo.2016.00038.
Kirchmann, H., Kätterer, T., Bergström, L., Börjesson, G., Bolinder, M.A., Flaws and criteria for design and evaluation of comparative organic and conventional cropping systems. F. Crop. Res. 186 (2016), 99–106, 10.1016/J.FCR.2015.11.006.
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. B Biol. Sci., 274, 303–313. 〈 https://doi.org/10.1098/rspb.2006.3721〉.
Krishna, S., Keasar, T., Morphological complexity as a floral signal: from perception by insect pollinators to co-evolutionary implications. Int. J. Mol. Sci., 2018, 19, 10.3390/IJMS19061681.
Laliberté, E., Legendre, P., Shipley, B., FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R. Packag. Version 1 (2015), 0–12.
Lindström, S.A.M., Herbertsson, L., Rundlöf, M., Bommarco, R., Smith, H.G., 2016. Experimental evidence that honeybees depress wild insect densities in a flowering crop. Proc. R. Soc. B Biol. Sci., 283, 20161641. 〈 https://doi.org/10.1098/rspb.2016.1641〉.
Mallinger, R.E., Gaines-Day, H.R., Gratton, C., Do managed bees have negative effects on wild bees? A systematic review of the literature. PLoS One, 12, 2017, e0189268, 10.1371/journal.pone.0189268.
Mallinger, R.E., Gratton, C., Species richness of wild bees, but not the use of managed honeybees, increases fruit set of a pollinator-dependent crop. J. Appl. Ecol. 52 (2015), 323–330, 10.1111/1365-2664.12377.
Marini, L., Quaranta, M., Fontana, P., Biesmeijer, J.C., Bommarco, R., Landscape context and elevation affect pollinator communities in intensive apple orchards. Basic Appl. Ecol. 13 (2012), 681–689, 10.1016/j.baae.2012.09.003.
Marliac, G., Penvern, S., Barbier, J.M., Lescourret, F., Capowiez, Y., Impact of crop protection strategies on natural enemies in organic apple production. Agron. Sustain. Dev. 35 (2015), 803–813, 10.1007/s13593-015-0282-5.
Martins, K.T., Gonzalez, A., Lechowicz, M.J., Pollination services are mediated by bee functional diversity and landscape context. Agric. Ecosyst. Environ. 200 (2015), 12–20, 10.1016/j.agee.2014.10.018.
Mateos-Fierro, Z., Fountain, M.T., Garratt, M.P.D., Ashbrook, K., Westbury, D.B., Active management of wildflower strips in commercial sweet cherry orchards enhances natural enemies and pest regulation services. Agric. Ecosyst. Environ., 317, 2021, 107485, 10.1016/j.agee.2021.107485.
McKerchar, M., Potts, S.G., Fountain, M.T., Garratt, M.P.D., Westbury, D.B., The potential for wildflower interventions to enhance natural enemies and pollinators in commercial apple orchards is limited by other management practices. Agric. Ecosyst. Environ., 301, 2020, 107034, 10.1016/J.AGEE.2020.107034.
Merfield, C., Moller, H., Manhire, J., Rosin, C., Norton, S., Carey, P., Hunt, L., Reid, J., Fairweather, J., Benge, J., Quellec, I., Le, Campbell, H., Lucock, D., Saunders, C., MacLeod, C., Barber, A., McCarthy, A., Are organic standards sufficient to ensure sustainable agriculture? Lessons from New Zealand's ARGOS and sustainability dashboard projects. Sustain. Agric. Res., 4, 2015, 158, 10.5539/sar.v4n3p158.
Mouchet, M.A., Villéger, S., Mason, N.W.H., Mouillot, D., Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct. Ecol. 24 (2010), 867–876, 10.1111/j.1365-2435.2010.01695.x.
Mouillot, D., Graham, N.A.J., Villéger, S., Mason, N.W.H., Bellwood, D.R., A functional approach reveals community responses to disturbances. Trends Ecol. Evol. 28 (2013), 167–177, 10.1016/j.tree.2012.10.004.
Nicholls, C.I., Altieri, M.A., Plant biodiversity enhances bees and other insect pollinators in agroecosystems. A review. Agron. Sustain. Dev. 33 (2013), 257–274, 10.1007/s13593-012-0092-y.
Nielsen, A., Steffan-Dewenter, I., Westphal, C., Messinger, O., Potts, S.G., Roberts, S.P.M., Settele, J., Szentgyörgyi, H., Vaissière, B.E., Vaitis, M., Woyciechowski, M., Bazos, I., Biesmeijer, J.C., Bommarco, R., Kunin, W.E., Tscheulin, T., Lamborn, E., Petanidou, T., Assessing bee species richness in two Mediterranean communities: importance of habitat type and sampling techniques. Ecol. Res. 26 (2011), 969–983, 10.1007/s11284-011-0852-1.
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., De Meulemeester, T., Dehon, M., Dewulf, A., Ortiz-Sánchez, F.J., Lhomme, P., Pauly, A., Potts, S.G., Praz, C., Q., Window, J., Michez, D., European Red List of Bees. 2014, IUCN Global Species Programme, 10.2779/77003.
Normandin, É., Vereecken, N.J., Buddle, C.M., Fournier, V., Taxonomic and functional trait diversity of wild bees in different urban settings. PeerJ, 5, 2017, e3051, 10.7717/peerj.3051.
Nunes-Silva, P., Witter, S., da Rosa, J.M., Halinski, R., Schlemmer, L.M., Arioli, C.J., Ramos, J.D., Botton, M., Blochtein, B., Diversity of floral visitors in apple orchards: influence on fruit characteristics depends on apple cultivar. Neotrop. Entomol. 49 (2020), 511–524, 10.1007/s13744-020-00762-1.
Odanaka, K.A., Rehan, S.M., Impact indicators: effects of land use management on functional trait and phylogenetic diversity of wild bees. Agric. Ecosyst. Environ., 2019, 286, 10.1016/j.agee.2019.106663.
Ollerton, J., Winfree, R., Tarrant, S., How many flowering plants are pollinated by animals?. Oikos 120 (2011), 321–326, 10.1111/j.1600-0706.2010.18644.x.
Orpet, R.J., Jones, V.P., Beers, E.H., Reganold, J.P., Goldberger, J.R., Crowder, D.W., Perceptions and outcomes of conventional vs. organic apple orchard management. Agric. Ecosyst. Environ., 289, 2020, 106723, 10.1016/j.agee.2019.106723.
Paradis, E., Schliep, K., Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35 (2019), 526–528, 10.1093/bioinformatics/bty633.
Pardo, A., Borges, P.A.V., Worldwide importance of insect pollination in apple orchards: a review. Agric. Ecosyst. Environ., 293, 2020, 106839, 10.1016/j.agee.2020.106839.
Park, M.G., Joshi, N.K., Rajotte, E.G., Biddinger, D.J., Losey, J.E., Danforth, B.N., Apple grower pollination practices and perceptions of alternative pollinators in New York and Pennsylvania. Renew. Agric. Food Syst. 35 (2020), 1–14, 10.1017/S1742170518000145.
Penvern, S., Fernique, S., Cardona, A., Herz, A., Ahrenfeldt, E., Dufils, A., Jamar, L., Korsgaard, M., Kruczyńska, D., Matray, S., Ozolina-Pole, L., Porcel, M., Ralle, B., Steinemann, B., Świergiel, W., Tasin, M., Telfser, J., Warlop, F., Sigsgaard, L., Farmers’ management of functional biodiversity goes beyond pest management in organic European apple orchards. Agric. Ecosyst. Environ., 284, 2019, 106555, 10.1016/j.agee.2019.05.014.
Penvern, S., Simon, S., Bellon, S., Alaphilippe, A., Lateur, M., Lauri, P.-E., Dapena, E., Jamar, L., Hemptinne, J.-L., Warlop, F., 2012. Sustainable Orchards’ Redesign: at the Crossroads of Multiple Approaches, 13.
Pérez-Méndez, N., Andersson, G.K.S., Requier, F., Hipólito, J., Aizen, M.A., Morales, C.L., García, N., Gennari, G.P., Garibaldi, L.A., The economic cost of losing native pollinator species for orchard production. J. Appl. Ecol. 57 (2020), 599–608, 10.1111/1365-2664.13561.
Petchey, O.L., Gaston, K.J., Functional diversity: back to basics and looking forward. Ecol. Lett. 9 (2006), 741–758, 10.1111/j.1461-0248.2006.00924.x.
Petchey, O.L., Gaston, K.J., Dendrograms and measuring functional diversity. Oikos 116 (2007), 1422–1426, 10.1111/j.0030-1299.2007.15894.x.
Porcel, M., Andersson, G.K.S., Pålsson, J., Tasin, M., Organic management in apple orchards: Higher impacts on biological control than on pollination. J. Appl. Ecol. 55 (2018), 2779–2789, 10.1111/1365-2664.13247.
Potts, S., Biesmeijer, K., Bommarco, R., Breeze, T., Carvalheiro, L., Franzen, M., González-Varo, J.P., Holzschuh, A., Kleijn, D., Klein, A.-M., Kunin, B., Lecocq, T., Lundin,O., Michez, D., Neumann, P., Nieto, A., Penev, L., Rasmont, P., Ratamäki, O.,Riedinger, V., Roberts, S.P.M., Rundlöf, M., Scheper, J., Sorensen, P., Steffan-Dewenter, I., Stoev, P., Vila, M., Schweiger, O., 2015. Status andtrends of European pollinators. Key findings of the STEP project.
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E., Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25 (2010), 345–353, 10.1016/j.tree.2010.01.007.
Prendergast, K.S., Leclercq, N., Vereecken, N.J., Honey bees (Hymenoptera: Apidae) outnumber native bees in Tasmanian apple orchards: perspectives for balancing crop production and native bee conservation. Austral Entomol. 60 (2021), 422–435, 10.1111/aen.12521.
Prendergast, K.S., Ollerton, J., Plant-pollinator networks in Australian urban bushland remnants are not structurally equivalent to those in residential gardens. Urban Ecosyst. 24 (2021), 973–987, 10.1007/s11252-020-01089-w.
Pretty, J., New opportunities for the redesign of agricultural and food systems. Agric. Hum. Values 37 (2020), 629–630, 10.1007/s10460-020-10056-2.
R Core Team, A language and environment for statistical computing. R. Found. Stat. Comput., 2013, 2 〈https://www.R-project.org〉.
Rader, R., Howlett, B.G., Cunningham, S.A., Westcott, D.A., Newstrom-Lloyd, L.E., Walker, M.K., Teulon, D.A.J., Edwards, W., Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop. J. Appl. Ecol. 46 (2009), 1080–1087, 10.1111/j.1365-2664.2009.01700.x.
Raderschall, C.A., Bommarco, R., Lindström, S.A.M., Lundin, O., Landscape crop diversity and semi-natural habitat affect crop pollinators, pollination benefit and yield. Agric. Ecosyst. Environ., 2021, 306, 10.1016/j.agee.2020.107189.
Radzevičiūtė, R., Theodorou, P., Schlegel, M., Paxton, R.J., A two-part modelling approach reveals a positive effect of pollinator biodiversity in boosting the pollination of apple flowers. Agric. Ecosyst. Environ., 306, 2021, 107197, 10.1016/j.agee.2020.107197.
Ramírez, F., Davenport, T.L., Apple pollination: a review. Sci. Hortic. 162 (2013), 188–203, 10.1016/j.scienta.2013.08.007.
Reganold, J.P., Glover, J.D., Andrews, P.K., Hinman, H.R., 2001. Sustainability of three apple production systems. Nature, 2001 4106831 410, 926–930. 〈 https://doi.org/10.1038/35073574〉.
Rodríguez-Gironés, M.A., Santamaría, L., Models of optimal foraging and resource partitioning: deep corollas for long tongues. Behav. Ecol. 17 (2006), 905–910, 10.1093/BEHECO/ARL024.
Ropars, L., Affre, L., Schurr, L., Flacher, F., Genoud, D., Mutillod, C., Geslin, B., Land cover composition, local plant community composition and honeybee colony density affect wild bee species assemblages in a Mediterranean biodiversity hot-spot. Acta Oecol., 104, 2020, 103546, 10.1016/j.actao.2020.103546.
Ropars, L., Dajoz, I., Fontaine, C., Muratet, A., Geslin, B., Wild pollinator activity negatively related to honey bee colony densities in urban context. PLoS One, 2019, 14, 10.1371/journal.pone.0222316.
Roulston, T.H., Smith, S.A., Brewster, A.L., Short communication: a comparison of pan trap and intensive net sampling techniques for documenting a bee (Hymenoptera: Apiformes) fauna. J. Kans. Entomol. Soc. 80 (2007), 179–181, 10.2317/0022-8567(2007)80[179:ACOPTA]2.0.CO;2.
Rousset, F., Ferdy, J.B., Testing environmental and genetic effects in the presence of spatial autocorrelation. Ecography 37 (2014), 781–790, 10.1111/ecog.00566.
Rundlöf, M., Smith, H.G., Birkhofer, K., Effects of Organic Farming on Biodiversity. ELS, 2016, John Wiley & Sons Ltd, 1–7, 10.1002/9780470015902.a0026342.
Sheffield, C.S., Ngo, H.T., Azzu, N., 2016. A Manual on Apple Pollination.
Shennan, C., Krupnik, T.J., Baird, G., Cohen, H., Forbush, K., Lovell, R.J., Olimpi, E.M., Organic and conventional agriculture: a useful framing?. Annu. Rev. Environ. Resour. 42 (2017), 317–346, 10.1146/annurev-environ-110615-085750.
Simon, S., Brun, L., Guinaudeau, J., Sauphanor, B., Pesticide use in current and innovative apple orchard systems. Agron. Sustain. Dev. 31 (2011), 541–555, 10.1007/s13593-011-0003-7.
Stefan, V., 2019. Geobuffer: Geodesic Buffer Around Points (Long, Lat) Using Metric Radius.
Theodorou, P., Radzevičiūtė, R., Lentendu, G., Kahnt, B., Husemann, M., Bleidorn, C., Settele, J., Schweiger, O., Grosse, I., Wubet, T., Murray, T.E., Paxton, R.J., Urban areas as hotspots for bees and pollination but not a panacea for all insects. Nat. Commun., 11, 2020, 576, 10.1038/s41467-020-14496-6.
Tscharntke, T., Grass, I., Wanger, T.C., Westphal, C., Batáry, P., Beyond organic farming - harnessing biodiversity-friendly landscapes. Trends Ecol. Evol. 36 (2021), 919–930, 10.1016/j.tree.2021.06.010.
Valido, A., Rodríguez-Rodríguez, M.C., Jordano, P., Honeybees disrupt the structure and functionality of plant-pollinator networks. Sci. Rep., 2019, 9, 10.1038/s41598-019-41271-5.
Vereecken, N.J., 2017. Découvrir et Protéger Nos Abeilles Sauvages, Glénat. ed.
Vereecken, N.J., Weekers, T., Leclercq, N., De Greef, S., Hainaut, H., Molenberg, J.-M., Martin, Y., Janssens, X., Noël, G., Pauly, A., Roberts, S.P.M., Marshall, L., Insect biomass is not a consistent proxy for biodiversity metrics in wild bees. Ecol. Indic., 2020, 107132, 10.1016/j.ecolind.2020.107132.
Wagner, D.L., Insect declines in the anthropocene. Annu. Rev. Entomol. 65 (2020), 457–480, 10.1146/annurev-ento-011019-025151.
Westphal, C., Bommarco, R., Carré, G., Lamborn, E., Morison, N., Petanidou, T., Potts, S.G., Roberts, S.P.M., Szentgyörgyi, H., Tscheulin, T., Vaissière, B.E., Woyciechowski, M., Biesmeuer, J.C., Kunin, W.E., Settele, J., Steffan-Dewenter, I., Measuring bee diversity in different European habitats and biogeographical regions. Ecol. Monogr. 78 (2008), 653–671, 10.1890/07-1292.1.
Wignall, V.R., Brolly, M., Uthoff, C., Norton, K.E., Chipperfield, H.M., Balfour, N.J., Ratnieks, F.L.W., Exploitative competition and displacement mediated by eusocial bees: experimental evidence in a wild pollinator community. Behav. Ecol. Sociobiol. 74 (2020), 1–15, 10.1007/s00265-020-02924-y.
Willer, H., Travnicek, J., Meier, C., Schlatter, B., 2021.The World of Organic Agriculture, 2021.
Wojcik, V.A., Morandin, L.A., Davies Adams, L., Rourke, K.E., Floral resource competition between honey bees and wild bees: is there clear evidence and can we guide management and conservation?. Environ. Entomol. 47 (2018), 822–833, 10.1093/ee/nvy077.
Wood, T.J., Michez, D., Paxton, R.J., Drossart, M., Neumann, P., Gérard, M., Vanderplanck, M., Barraud, A., Martinet, B., Leclercq, N., Vereecken, N.J., Managed honey bees as a radar for wild bee decline?. Apidologie, 2020, 1–17, 10.1007/s13592-020-00788-9.
Woodcock, B.A., Garratt, M.P.D., Powney, G.D., Shaw, R.F., Osborne, J.L., Soroka, J., Lindström, S.A.M., Stanley, D., Ouvrard, P., Edwards, M.E., Jauker, F., McCracken, M.E., Zou, Y., Potts, S.G., Rundlöf, M., Noriega, J.A., Greenop, A., Smith, H.G., Bommarco, R., van der Werf, W., Stout, J.C., Steffan-Dewenter, I., Morandin, L., Bullock, J.M., Pywell, R.F., Meta-analysis reveals that pollinator functional diversity and abundance enhance crop pollination and yield. Nat. Commun. 10 (2019), 1–10, 10.1038/s41467-019-09393-6.
Zurbuchen, A., Landert, L., Klaiber, J., Müller, A., Hein, S., Dorn, S., Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol. Conserv. 143 (2010), 669–676, 10.1016/j.biocon.2009.12.003.