Increasing plant functional diversity is not the key for supporting pollinators in wildflower strips

Uyttenbroeck, Roel; Piqueray, Julien; Hatt, Séverin; Mahy, Grégory; Monty, Arnaud

doi:10.1016/j.agee.2017.08.014

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Increasing plant functional diversity is not the key for supporting pollinators in wildflower strips

Uyttenbroeck, Roel; Piqueray, Julien; Hatt, Séverin et al.

2017 • In Agriculture, Ecosystems and Environment, 249, p. 144-155

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https://hdl.handle.net/2268/213931

DOI
10.1016/j.agee.2017.08.014

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Keywords :

functional diversity; wildflower strips; plant-pollinator networks; niche overlap; agri-environment schemes; redundancy

Abstract :

[en] Intensification of agriculture has been one of the major drivers for biodiversity loss in recent decades. Pollinators, which serve an important role in pollinating crops as well as wild plants, have shown a decline in species richness. Flower strips can be used to support pollinators in agro-ecosystems, however the question remains as to how their design can be optimized in order to best benefit pollinators. Increasing plant species diversity has been shown to be beneficial for pollinators, and it is often suggested that functional traits are driving this relationship. Therefore, increasing plant functional diversity could be a tool to support pollinator abundance and diversity. As experimental evidence on this relationship is scarce, we developed a field study with experimental sown flower strips with four functional diversity levels, based on multiple flower traits and with equal plant species richness. We monitored vegetation development, as well as the flower-visiting pollinator community and their interaction networks with flowers. We were able to create a functional diversity gradient while controlling for plant species richness and evenness. However, in contrast to our expectations, pollinator species richness and evenness were not influenced by functional diversity, and increasing functional diversity even resulted in lower flower visitation rates. Network stability metrics showed no effect or negative relationships with functional diversity. We conclude that increasing functional diversity was not the key for supporting pollinators in wildflower strips. Our results also suggest that, for a constant amount of flower resources, increasing plant functional diversity and thus decreasing redundancy of potential pollinator feeding niches, decreases the amount of flower resources present per feeding niche. As pollinator species tended to have less overlap in their feeding niches in flower strips with increased functional diversity, this may lead to a reduction of flower resources available for pollinator species with a more specialized feeding niche.

Research Center/Unit :

TERRA Teaching and Research Centre - TERRA
BIOSE - Ingénierie des Bio‐Systèmes - ULiège

Disciplines :

Environmental sciences & ecology
Agriculture & agronomy

Author, co-author :

Uyttenbroeck, Roel ; Université de Liège > Ingénierie des biosystèmes (Biose) > Biodiversité et Paysage

Piqueray, Julien

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

Mahy, Grégory ; Université de Liège > Ingénierie des biosystèmes (Biose) > Biodiversité et Paysage

Monty, Arnaud ; Université de Liège > Ingénierie des biosystèmes (Biose) > Biodiversité et Paysage

Language :

English

Title :

Increasing plant functional diversity is not the key for supporting pollinators in wildflower strips

Publication date :

01 November 2017

Journal title :

Agriculture, Ecosystems and Environment

ISSN :

0167-8809

eISSN :

1873-2305

Publisher :

Elsevier Science, Amsterdam, Netherlands

Volume :

249

Pages :

144-155

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

CARE AgricultureIsLife

Available on ORBi :

since 31 August 2017

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Bibliography

Albrecht, M., Duelli, P., Müller, C., Kleijn, D., Schmid, B., The Swiss agri-environment scheme enhances pollinator diversity and plant reproductive success in nearby intensively managed farmland. J. Appl. Ecol. 44 (2007), 813–822, 10.1111/j.1365-2664.2007.01306.x.
Balzan, M.V., Bocci, G., Moonen, A.-C., Augmenting flower trait diversity in wildflower strips to optimise the conservation of arthropod functional groups for multiple agroecosystem services. J. Insect Conserv. 18 (2014), 713–728, 10.1007/s10841-014-9680-2.
Balzan, M.V., Bocci, G., Moonen, A.-C., Utilisation of plant functional diversity in wildflower strips for the delivery of multiple agroecosystem services. Entomol. Exp. Appl. 158 (2016), 304–319, 10.1111/eea.12403.
Bascompte, J., Jordano, P., Melián, C.J., Olesen, J.M., The nested assembly of plant–animal mutualistic networks. Proc. Natl. Acad. Sci. 100 (2003), 9383–9387, 10.1073/pnas.1633576100.
Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J., Kunin, W.E., Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313 (2006), 351–354, 10.1126/science.1127863.
Blüthgen, N., Klein, A.-M., Functional complementarity and specialisation: the role of biodiversity in plant–pollinator interactions. Basic Appl. Ecol. 12 (2011), 282–291, 10.1016/j.baae.2010.11.001.
Blüthgen, N., Menzel, F., Blüthgen, N., Measuring specialization in species interaction networks. BMC Ecol., 6, 2006, 9, 10.1186/1472-6785-6-9.
Botta-Dukát, Z., Rao's quadratic entropy as a measure of functional diversity based on multiple traits. J. Veg. Sci. 16 (2005), 533–540.
Campbell, A.J., Biesmeijer, J.C., Varma, V., Wäckers, F.L., Realising multiple ecosystem services based on the response of three beneficial insect groups to floral traits and trait diversity. Basic Appl. Ecol. 13 (2012), 363–370, 10.1016/j.baae.2012.04.003.
Chittka, L., Gumbert, A., Kunze, J., Foraging dynamics of bumble bees: correlates of movements within and between plant species. Behav. Ecol. 8 (1997), 239–249, 10.1093/beheco/8.3.239.
De Cauwer, B., Reheul, D., D'hooghe, K., Nijs, I., Milbau, A., Evolution of the vegetation of mown field margins over their first 3 years. Agric. Ecosyst. Environ. 109 (2005), 87–96.
Devoto, M., Bailey, S., Craze, P., Memmott, J., Understanding and planning ecological restoration of plant–pollinator networks. Ecol. Lett. 15 (2012), 319–328, 10.1111/j. 1461-0248.2012.01740.x.
Dormann, C.F., Fründ, J., Blüthgen, N., Gruber, B., Indices, graphs and null models: analyzing bipartite ecological networks. Open Ecol. J. 2 (2009), 7–24, 10.2174/1874213000902010007.
Ebeling, A., Klein, A.-M., Schumacher, J., Weisser, W.W., Tscharntke, T., How does plant richness affect pollinator richness and temporal stability of flower visits?. Oikos 117 (2008), 1808–1815, 10.1111/j.1600-0706.2008.16819.x.
Ebeling, A., Klein, A.-M., Tscharntke, T., Plant–flower visitor interaction webs: temporal stability and pollinator specialization increases along an experimental plant diversity gradient. Basic Appl. Ecol. 12 (2011), 300–309, 10.1016/j.baae.2011.04.005.
Fontaine, C., Dajoz, I., Meriguet, J., Loreau, M., Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol., 4, 2006, e1, 10.1371/journal.pbio.0040001.
Gibson, R.H., Nelson, I.L., Hopkins, G.W., Hamlett, B.J., Memmott, J., Pollinator webs, plant communities and the conservation of rare plants: arable weeds as a case study. J. Appl. Ecol. 43 (2006), 246–257, 10.1111/j.1365-2664.2006.01130.x.
Grass, I., Albrecht, J., Jauker, F., Diekötter, T., Warzecha, D., Wolters, V., Farwig, N., Much more than bees—Wildflower plantings support highly diverse flower-visitor communities from complex to structurally simple agricultural landscapes. Agric. Ecosyst. Environ. 225 (2016), 45–53, 10.1016/j.agee.2016.04.001.
Haaland, C., Naisbit, R.E., Bersier, L.-F., Sown wildflower strips for insect conservation: a review. Insect Conserv. Divers. 4 (2011), 60–80, 10.1111/j.1752-4598.2010.00098.x.
Hegland, S.J., Boeke, L., Relationships between the density and diversity of floral resources and flower visitor activity in a temperate grassland community. Ecol. Entomol. 31 (2006), 532–538, 10.1111/j.1365-2311.2006.00812.x.
Hegland, S.J., Totland, Ø., Relationships between species’ floral traits and pollinator visitation in a temperate grassland. Oecologia 145 (2005), 586–594, 10.1007/s00442-005-0165-6.
Hicks, D.M., Ouvrard, P., Baldock, K.C.R., Baude, M., Goddard, M.A., Kunin, W.E., Mitschunas, N., Memmott, J., Morse, H., Nikolitsi, M., Osgathorpe, L.M., Potts, S.G., Robertson, K.M., Scott, A.V., Sinclair, F., Westbury, D.B., Stone, G.N., Food for pollinators: quantifying the nectar and pollen resources of urban flower meadows. PLoS One, 11, 2016, e0158117, 10.1371/journal.pone.0158117.
Hoehn, P., Tscharntke, T., Tylianakis, J.M., Steffan-Dewenter, I., Functional group diversity of bee pollinators increases crop yield. Proc. R. Soc. Lond. B Biol. Sci. 275 (2008), 2283–2291, 10.1098/rspb.2008.0405.
Holzschuh, A., Steffan-Dewenter, I., Kleijn, D., Tscharntke, T., Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context. J. Appl. Ecol. 44 (2007), 41–49, 10.1111/j.1365-2664.2006.01259.x.
Hothorn, T., Bretz, F., Westfall, P., Simultaneous inference in general parametric models. Biom. J. 50 (2008), 346–363, 10.1002/bimj.200810425.
Hudewenz, A., Klein, A.-M., Scherber, C., Stanke, L., Tscharntke, T., Vogel, A., Weigelt, A., Weisser, W.W., Ebeling, A., Herbivore and pollinator responses to grassland management intensity along experimental changes in plant species richness. Biol. Conserv. 150 (2012), 42–52, 10.1016/j.biocon.2012.02.024.
Junker, R.R., Blüthgen, N., Brehm, T., Binkenstein, J., Paulus, J., Martin Schaefer, H., Stang, M., Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Funct. Ecol. 27 (2013), 329–341, 10.1111/1365-2435.12005.
Kattge, J., Díaz, S., Lavorel, S., Prentice, I.C., Leadley, P., Bönisch, G., Garnier, E., Westoby, M., Reich, P.B., Wright, I.J., Cornelissen, J.H.C., Violle, C., Harrison, S.P., Van Bodegom, P.M., Reichstein, M., Enquist, B.J., Soudzilovskaia, N.A., Ackerly, D.D., Anand, M., Atkin, O., Bahn, M., Baker, T.R., Baldocchi, D., Bekker, R., Blanco, C.C., Blonder, B., Bond, W.J., Bradstock, R., Bunker, D.E., Casanoves, F., Cavender-Bares, J., Chambers, J.Q., Chapin Iii, F.S., Chave, J., Coomes, D., Cornwell, W.K., Craine, J.M., Dobrin, B.H., Duarte, L., Durka, W., Elser, J., Esser, G., Estiarte, M., Fagan, W.F., Fang, J., Fernández-Méndez, F., Fidelis, A., Finegan, B., Flores, O., Ford, H., Frank, D., Freschet, G.T., Fyllas, N.M., Gallagher, R.V., Green, W.A., Gutierrez, A.G., Hickler, T., Higgins, S.I., Hodgson, J.G., Jalili, A., Jansen, S., Joly, C.A., Kerkhoff, A.J., Kirkup, D., Kitajima, K., Kleyer, M., Klotz, S., Knops, J.M.H., Kramer, K., Kühn, I., Kurokawa, H., Laughlin, D., Lee, T.D., Leishman, M., Lens, F., Lenz, T., Lewis, S.L., Lloyd, J., Llusià, J., Louault, F., Ma, S., Mahecha, M.D., Manning, P., Massad, T., Medlyn, B.E., Messier, J., Moles, A.T., Müller, S.C., Nadrowski, K., Naeem, S., Niinemets, U., Nöllert, S., Nüske, A., Ogaya, R., Oleksyn, J., Onipchenko, V.G., Onoda, Y., Ordoñez, J., Overbeck, G., Ozinga, W.A., et al. TRY-a global database of plant traits. Global Change Biol. 17 (2011), 2905–2935, 10.1111/j.1365-2486.2011.02451.x.
Klein, A.-M., Steffan-Dewenter, I., Tscharntke, T., Fruit set of highland coffee increases with the diversity of pollinating bees. Proc. R. Soc. Lond. B Biol. Sci. 270 (2003), 955–961.
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 Biol. Sci. 274 (2007), 303–313, 10.1098/rspb.2006.3721.
Laliberté, E., Legendre, P., Shipley, B., 2014. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1. 0–12.
Lambinon, J., De Langhe, J.-E., Delvosalle, L., Duvigneaud, J., Flora van België, het Groothertogdom Luxemburg, Noord-Frankrijk en de aangrenzende gebieden. 2008, Nationale Plantentuin van België, Meise.
Lavorel, S., Grigulis, K., McIntyre, S., Williams, N.S.G., Garden, D., Dorrough, J., Berman, S., Quétier, F., Thébault, A., Bonis, A., Assessing functional diversity in the field–methodology matters!. Funct. Ecol. 22 (2008), 134–147, 10.1111/j.1365-2435.2007.01339.x.
Lepŝ, J., Doleẑal, J., Bezemer, T.M., Brown, V.K., Hedlund, K., Igual Arroyo, M., Jörgensen, H.B., Lawson, C.S., Mortimer, S.R., Peix Geldart, A., Rodríguez Barrueco, C., Santa Regina, I., Ŝmilauer, P., vander Putten, W.H., Long-term effectiveness of sowing high and low diversity seed mixtures to enhance plant community development on ex-arable fields. Appl. Veg. Sci. 10 (2007), 97–110, 10.1111/j.1654-109X.2007.tb00508.x.
Müller, H., 1881. Alpenblumen, ihre Befruchtung durch insekten und ihre Anpassungen an dieselben. Leipzig.
Münzbergová, Z., Herben, T., Seed, dispersal, microsite, habitat and recruitment limitation: identification of terms and concepts in studies of limitations. Oecologia 145 (2005), 1–8, 10.1007/s00442-005-0052-1.
Microsoft Corporation, Microsoft Excel 2010. 2010, Microsoft Corporation.
Moles, A.T., Westoby, M., Seedling survival and seed size: a synthesis of the literature. J. Ecol. 92 (2004), 372–383, 10.1111/j.0022-0477.2004.00884.x.
Monty, A., Garré, S., Bindelle, J., Mahy, G., Deleu, M., Bodson, B., Haubruge, É., AgricultureIsLife or how to facilitate innovation in agriculture through multi-disciplinary research?. Biotechnol. Agron. Soc. Environ. 20 (2016), 211–214.
Morandin, L.A., Winston, M.L., Wild bee abundance and seed production in conventional, organic, and genetically modified canola. Ecol. Appl. 15 (2005), 871–881, 10.1890/03-5271.
Natagriwal asbl, 2017. Bande aménagée à fleurs des prés [WWW Document]. URL https://www.natagriwal.be/fr/mesures-agro-environnementales/liste-des-mae/fiches/details/342. (Accessed 5.10.17).
Nicholls, C.I., Altieri, M.A., Plant biodiversity enhances bees and other insect pollinators in agroecosystems. A review. Agron. Sustain. Dev. 33 (2012), 257–274, 10.1007/s13593-012-0092-y.
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., 2015. vegan: Community Ecology Package. R package version 2. 2-1.
Orford, K.A., Murray, P.J., Vaughan, I.P., Memmott, J., Modest enhancements to conventional grassland diversity improve the provision of pollination services. J. Appl. Ecol. 53 (2016), 906–915, 10.1111/1365-2664.12608.
Potts, S.G., Vulliamy, B., Dafni, A., Ne'eman, G., Willmer, P., Linking bees and flowers: how do floral communities structure pollinator communities?. Ecology 84 (2003), 2628–2642, 10.1890/02-0136.
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.
Core Team, R., R: A Language and Environment for Statistical Computing. 2013, R Foundation for Statistical Computing, Vienna, Austria.
Rees, M., Community structure in sand dune annuals: is seed weight a key quantity?. J. Ecol. 83 (1995), 857–863, 10.2307/2261422.
Scheper, J., Bommarco, R., Holzschuh, A., Potts, S.G., Riedinger, V., Roberts, S.P.M., Rundlöf, M., Smith, H.G., Steffan-Dewenter, I., Wickens, J.B., Wickens, V.J., Kleijn, D., Local and landscape-level floral resources explain effects of wildflower strips on wild bees across four European countries. J. Appl. Ecol. 52 (2015), 1165–1175, 10.1111/1365-2664.12479.
Service Public de la Wallonie, Navteq, AGDP, IGN, 2014. Carte des sols de Wallonie [WWW Document]. URL http://geoapps.wallonie.be/CigaleInter/.
Steffan-Dewenter, I., Tscharntke, T., Succession of bee communities on fallows. Ecography 24 (2001), 83–93, 10.1034/j.1600-0587.2001.240110.x.
Stoate, C., Boatman, N.D., Borralho, R.J., Carvalho, C.R., Snoo, G.R., de Eden, P., Ecological impacts of arable intensification in Europe. J. Environ. Manage. 63 (2001), 337–365, 10.1006/jema.2001.0473.
Thébault, E., Fontaine, C., Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329 (2010), 853–856, 10.1126/science.1188321.
Tilman, D., Fargione, J., Wolff, B., D'Antonio, C., Dobson, A., Howarth, R., Schindler, D., Schlesinger, W.H., Simberloff, D., Swackhamer, D., Forecasting agriculturally driven global environmental change. Science 292 (2001), 281–284, 10.1126/science.1057544.
Turnbull, L.A., Rees, M., Crawley, M.J., Seed mass and the competition/colonization trade-off: a sowing experiment. J. Ecol. 87 (1999), 899–912, 10.1046/j.1365-2745.1999.00405.x.
Tylianakis, J.M., Laliberté, E., Nielsen, A., Bascompte, J., Conservation of species interaction networks. Biol. Conserv. 143 (2010), 2270–2279, 10.1016/j.biocon.2009.12.004.
Uyttenbroeck, R., Hatt, S., Piqueray, J., Paul, A., Bodson, B., Francis, F., Monty, A., Creating perennial flower strips: think functional!. Agric. Agric. Sci. 6 (2015), 95–101, 10.1016/j.aaspro.2015.08.044.
Uyttenbroeck, R., Hatt, S., Paul, A., Boeraeve, F., Piqueray, J., Francis, F., Danthine, S., Frédérich, M., Dufrêne, M., Bodson, B., Monty, A., Pros and cons of flowers strips for farmers: a review. Biotechnol. Agron. Soc. Environ. 20 (2016), 225–235.
Venjakob, C., Klein, A.-M., Ebeling, A., Tscharntke, T., Scherber, C., Plant diversity increases spatio-temporal niche complementarity in plant-pollinator interactions. Ecol. Evol. 6 (2016), 2249–2261, 10.1002/ece3.2026.
Winfree, R., Aguilar, R., Vázquez, D.P., LeBuhn, G., Aizen, M.A., A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 90 (2009), 2068–2076, 10.1890/08-1245.1.
Woodcock, B.A., Savage, J., Bullock, J.M., Nowakowski, M., Orr, R., Tallowin, J.R.B., Pywell, R.F., Enhancing floral resources for pollinators in productive agricultural grasslands. Biol. Conserv. 171 (2014), 44–51, 10.1016/j.biocon.2014.01.023.
Wratten, S.D., Gillespie, M., Decourtye, A., Mader, E., Desneux, N., Pollinator habitat enhancement: benefits to other ecosystem services. Agric. Ecosyst. Environ. 159 (2012), 112–122, 10.1016/j.agee.2012.06.020.