Intensified agriculture, a driver of biodiversity loss, can diminish ecosystem functions and their stability. Biodiversity can increase functional redundancy and is expected to stabilize ecosystem functions. Few studies, however, have explored how agricultural intensity affects functional redundancy and its link with ecosystem function stability. Here, within a continental-wide study, we assess how functional redundancy of seed predation is affected by agricultural intensity and landscape simplification. By combining carabid abundances with molecular gut content data, functional redundancy of seed predation was quantified for 65 weed genera across 60 fields in four European countries. Across weed genera, functional redundancy was reduced with high field management intensity and simplified crop rotations. Moreover, functional redundancy increased the spatial stability of weed seed predation at the field scale. We found that ecosystem functions are vulnerable to disturbances in intensively managed agroecosystems, providing empirical evidence of the importance of biodiversity for stable ecosystem functions across space.

Agroécologie INRAE Institut Agro Université de Bourgogne Franche Comté Dijon France

Applied Animal Ecology Department of Zoology University of Innsbruck Innsbruck Austria

Centre for Crop Systems Analysis Department of Plant Sciences Wageningen University Wageningen The Netherlands

Department of Crop Production Ecology Swedish University of Agricultural Sciences Uppsala Sweden

Department of Ecology Swedish University of Agricultural Sciences Uppsala Sweden

Functional Diversity in Agro Ecosystems Crop Research Institute Praha 6 Ruzyně Czech Republic

IGEPP INRAE Institut Agro Univ Rennes Angers France

Zobrazit více v PubMed

Batáry, P., Holzschuh, A., Orci, K.M., Samu, F. & Tscharntke, T. (2012) Responses of plant, insect and spider biodiversity to local and landscape scale management intensity in cereal crops and grasslands. Agriculture, Ecosystems & Environment, 146, 130–136.

Biggs, C.R., Yeager, L.A., Bolser, D.G., Bonsell, C., Dichiera, A.M., Hou, Z. et al. (2020) Does functional redundancy affect ecological stability and resilience? A review and meta‐analysis. Ecosphere, 11, e03184.

Boussard, H. & Baudry, J. (2017) Chloe 4.0: a software for landscape pattern analysis.

Brose, U., Ehnes, R.B., Rall, B.C., Vucic‐Pestic, O., Berlow, E.L. & Scheu, S. (2008) Foraging theory predicts predator–prey energy fluxes. Journal of Animal Ecology, 77, 1072–1078.

Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M. & West, G.B. (2004) Toward a metabolic theory of ecology. Ecology, 85, 1771–1789.

Carbonne, B., Bohan, D.A., Foffová, H., Daouti, E., Frei, B., Neidel, V. et al. (2022) Direct and indirect effects of landscape and field management intensity on carabids through trophic resources and weeds. Journal of Applied Ecology, 59, 176–187.

Carbonne, B., Petit, S., Neidel, V., Foffova, H., Daouti, E., Frei, B. et al. (2020) The resilience of weed seedbank regulation by carabid beetles, at continental scales, to alternative prey. Scientific Reports, 10, 19315.

Cardinale, B. (2012) Impacts of biodiversity loss. Science, 336, 552–553.

Cariveau, D.P., Williams, N.M., Benjamin, F.E. & Winfree, R. (2013) Response diversity to land use occurs but does not consistently stabilise ecosystem services provided by native pollinators. Ecology Letters, 16, 903–911.

Chaplin‐Kramer, R., O'Rourke, M.E., Blitzer, E.J. & Kremen, C. (2011) A meta‐analysis of crop pest and natural enemy response to landscape complexity. Ecology Letters, 14, 922–932.

Comont, D., Hicks, H., Crook, L., Hull, R., Cocciantelli, E., Hadfield, J. et al. (2019) Evolutionary epidemiology predicts the emergence of glyphosate resistance in a major agricultural weed. New Phytologist, 223, 1584–1594.

Daedlow, D., Westerman, P.R., Baraibar, B., Rouphael, S. & Gerowitt, B. (2014) Weed seed predation rate in cereals as a function of seed density and patch size, under high predation pressure by rodents. Weed Research, 54, 186–195.

Dainese, M., Martin, E.A., Aizen, M.A., Albrecht, M., Bartomeus, I., Bommarco, R. et al. (2019) A global synthesis reveals biodiversity‐mediated benefits for crop production. Science Advances, 5, eaax0121.

Daouti, E., Jonsson, M., Vico, G. & Menegat, A. (2022) Seed predation is key to preventing population growth of the weed Alopecurus myosuroides. Journal of Applied Ecology, 59, 471–482.

de Bello, F., Lavorel, S., Hallett, L.M., Valencia, E., Garnier, E., Roscher, C. et al. (2021) Functional trait effects on ecosystem stability: assembling the jigsaw puzzle. Trends in Ecology & Evolution, 36, 822–836.

de Castro‐Arrazola, I., Andrew, N.R., Berg, M.P., Curtsdotter, A., Lumaret, J.P., Menéndez, R. et al. (2023) A trait‐based framework for dung beetle functional ecology. Journal of Animal Ecology, 92, 44–65.

Ehnes, R.B., Rall, B.C. & Brose, U. (2011) Phylogenetic grouping, curvature and metabolic scaling in terrestrial invertebrates. Ecology Letters, 14, 993–1000.

Elmqvist, T., Folke, C., Nyström, M., Peterson, G., Bengtsson, J., Walker, B. et al. (2003) Response diversity, ecosystem change, and resilience. Frontiers in Ecology and the Environment, 1, 488–494.

Eyre, M.D., Luff, M.L., Atlihan, R. & Leifert, C. (2012) Ground beetle species (Carabidae, Coleoptera) activity and richness in relation to crop type, fertility management and crop protection in a farm management comparison trial. Annals of Applied Biology, 161, 169–179.

Feit, B., Blüthgen, N., Daouti, E., Straub, C., Traugott, M. & Jonsson, M. (2021) Landscape complexity promotes resilience of biological pest control to climate change. Proceedings of the Royal Society B: Biological Sciences, 288, 20210547.

Feit, B., Blüthgen, N., Traugott, M. & Jonsson, M. (2019) Resilience of ecosystem processes: a new approach shows that functional redundancy of biological control services is reduced by landscape simplification. Ecology Letters, 22, 1568–1577.

Frei, B., Guenay, Y., Bohan, D.A., Traugott, M. & Wallinger, C. (2019) Molecular analysis indicates high levels of carabid weed seed consumption in cereal fields across Central Europe. Journal of Pest Science, 92, 935–942.

Gagic, V., Holding, M., Venables, W.N., Hulthen, A.D. & Schellhorn, N.A. (2021) Better outcomes for pest pressure, insecticide use, and yield in less intensive agricultural landscapes. Proceedings of the National Academy of Sciences, 118, e2018100118.

Geiger, F., Bengtsson, J., Berendse, F., Weisser, W.W., Emmerson, M., Morales, M.B. et al. (2010) Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic and Applied Ecology, 11, 97–105.

Guenay‐Greunke, Y., Bohan, D.A., Traugott, M. & Wallinger, C. (2021) Handling of targeted amplicon sequencing data focusing on index hopping and demultiplexing using a nested metabarcoding approach in ecology. Scientific Reports, 11, 19510.

Hallett, A.C., Mitchell, R.J., Chamberlain, E.R. & Karron, J.D. (2017) Pollination success following loss of a frequent pollinator: the role of compensatory visitation by other effective pollinators. AoB Plants, 9, plx020.

Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S. et al. (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs, 75, 3–35.

Isbell, F., Cowles, J., Dee, L.E., Loreau, M., Reich, P.B., Gonzalez, A. et al. (2018) Quantifying effects of biodiversity on ecosystem functioning across times and places. Ecology Letters, 21, 763–778.

Jarošík, V. (1989) Mass vs. length relationship for carabid beetles (Col., Carabidae). Pedobiologia (Jena), 33, 87–90.

King, R.A., Read, D.S., Traugott, M. & Symondson, W.O.C. (2008) Invited Review: Molecular analysis of predation: a review of best practice for DNA‐based approaches. Molecular Ecology, 17, 947–963.

Kitson, J.J.N., Hahn, C., Sands, R.J., Straw, N.A., Evans, D.M. & Lunt, D.H. (2019) Detecting host–parasitoid interactions in an invasive Lepidopteran using nested tagging DNA metabarcoding. Molecular Ecology, 28, 471–483.

Knapp, M., Seidl, M., Knappová, J., Macek, M. & Saska, P. (2019) Temporal changes in the spatial distribution of carabid beetles around arable field‐woodlot boundaries. Scientific Reports, 9, 1–11.

Kotze, D.J. & O'Hara, R.B. (2003) Species decline: but why? Explanations of carabid beetle (Coleoptera, Carabidae) declines in Europe. Oecologia, 135, 138–148.

Laliberté, E., Wells, J.A., DeClerck, F., Metcalfe, D.J., Catterall, C.P., Queiroz, C. et al. (2010) Land‐use intensification reduces functional redundancy and response diversity in plant communities. Ecology Letters, 13, 76–86.

Lami, F., Boscutti, F., Masin, R., Sigura, M. & Marini, L. (2020) Seed predation intensity and stability in agro‐ecosystems: role of predator diversity and soil disturbance. Agriculture, Ecosystems & Environment, 288, 106720.

Larsen, A.E. & Noack, F. (2021) Impact of local and landscape complexity on the stability of field‐level pest control. Nature Sustainability, 4, 120–128.

Lemerle, D., Verbeek, B. & Coombes, N. (1995) Losses in grain yield of winter crops from Lolium rigidum competition depend on crop species, cultivar and season. Weed Research, 35, 503–509.

Lindroth, C. (1985) The Carabidae (Coleoptera) of Fennoscandia and Denmark. Leiden, Copenhagen: E.J. Brill/Scandinavia Science Press Ltd.

Löbl, I. & Smetana, A. (2003) Catalogue of Palaearctic Coleoptera. Stenstrup, Denmark: Apollo Books.

Loreau, M. & de Mazancourt, C. (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecology Letters, 16, 106–115.

Lutman, P.J.W., Moss, S.R., Cook, S. & Welham, S.J. (2013) A review of the effects of crop agronomy on the management of Alopecurus myosuroides. Weed Research, 53, 299–313.

MacArthur, R. (1955) Fluctuations of animal populations and a measure of community stability. Ecology, 36, 533–536.

MacGregor‐Fors, I. & Payton, M.E. (2013) Contrasting diversity values: statistical inferences based on overlapping confidence intervals. PLoS One, 8, e56794.

Maity, A., Singh, V., Jessup, R. & Bagavathiannan, M. (2021) Seed traits correlate with herbicide resistance in Italian ryegrass (Lolium perenne ssp. multiflorum). Pest Management Science, 77, 2756–2765.

Martin, E.A., Feit, B., Requier, F., Friberg, H. & Jonsson, M. (2019) Chapter Three—Assessing the resilience of biodiversity‐driven functions in agroecosystems under environmental change. In: Bohan, D.A. & Dumbrell, A.J. (Eds.) Advances in ecological research, Resilience in complex socio‐ecological systems. Cambridge: Academic Press, pp. 59–123.

Matson, P.A., Parton, W.J., Power, A.G. & Swift, M.J. (1997) Agricultural intensification and ecosystem properties. Science, 277(5325), 504–509.

May, R.M. (1973) Stability and complexity in model ecosystems. Princeton, New Jersey: Princeton University Press.

Menalled, F.D., Smith, R.G., Dauer, J.T. & Fox, T.B. (2007) Impact of agricultural management on carabid communities and weed seed predation. Agriculture, Ecosystems & Environment, 118, 49–54.

Moorhouse‐Gann, R.J., Dunn, J.C., de Vere, N., Goder, M., Cole, N., Hipperson, H. et al. (2018) New universal ITS2 primers for high‐resolution herbivory analyses using DNA metabarcoding in both tropical and temperate zones. Scientific Reports, 8, 8542.

Moss, S. (2017) Black‐grass (Alopecurus myosuroides): why has this weed become such a problem in Western Europe and what are the solutions? Outlooks on Pest Management, 28, 207–212.

Naeem, S. & Li, S. (1997) Biodiversity enhances ecosystem reliability. Nature, 390, 507–509.

O'Rourke, M.E., Liebman, M. & Rice, M.E. (2008) Ground beetle (Coleoptera: Carabidae) assemblages in conventional and diversified crop rotation systems. Environmental Entomology, 37, 121–130.

Outhwaite, C.L., McCann, P. & Newbold, T. (2022) Agriculture and climate change are reshaping insect biodiversity worldwide. Nature, 605, 97–102.

Ovaskainen, O. & Abrego, N. (2020) Joint species distribution modelling: with applications in R. Ecology, biodiversity and conservation. Cambridge: Cambridge University Press.

Ovaskainen, O., Tikhonov, G., Norberg, A., Blanchet, F.G., Duan, L., Dunson, D. et al. (2017) How to make more out of community data? A conceptual framework and its implementation as models and software. Ecology Letters, 20, 561–576.

Peralta, G., Frost, C.M., Rand, T.A., Didham, R.K. & Tylianakis, J.M. (2014) Complementarity and redundancy of interactions enhance attack rates and spatial stability in host–parasitoid food webs. Ecology, 95, 1888–1896.

Petit, S., Boursault, A. & Bohan, D.A. (2014) Weed seed choice by carabid beetles (Coleoptera: Carabidae): linking field measurements with laboratory diet assessments. European Journal of Entomology, 111, 615–620.

Pillar, V.D., Blanco, C.C., Müller, S.C., Sosinski, E.E., Joner, F. & Duarte, L.D.S. (2013) Functional redundancy and stability in plant communities. Journal of Vegetation Science, 24, 963–974.

Pimm, S.L. & Lawton, J.H. (1978) On feeding on more than one trophic level. Nature, 275, 542–544.

Pocock, M.J.O., Schmucki, R. & Bohan, D.A. (2021) Inferring species interactions from ecological survey data: a mechanistic approach to predict quantitative food webs of seed feeding by carabid beetles. Ecology and Evolution, 11, 12858–12871.

Pompanon, F., Deagle, B.E., Symondson, W.O.C., Brown, D.S., Jarman, S.N. & Taberlet, P. (2012) Who is eating what: diet assessment using next generation sequencing. Molecular Ecology, 21, 1931–1950.

Purtauf, T., Roschewitz, I., Dauber, J., Thies, C., Tscharntke, T. & Wolters, V. (2005) Landscape context of organic and conventional farms: influences on carabid beetle diversity. Agriculture, Ecosystems & Environment, 108, 165–174.

R Core Team. (2022) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Rosenfeld, J.S. (2002) Functional redundancy in ecology and conservation. Oikos, 98, 156–162.

Rusch, A., Binet, D., Delbac, L. & Thiéry, D. (2016) Local and landscape effects of agricultural intensification on Carabid community structure and weed seed predation in a perennial cropping system. Landscape Ecology, 31, 2163–2174.

Rusch, A., Bommarco, R., Jonsson, M., Smith, H.G. & Ekbom, B. (2013) Flow and stability of natural pest control services depend on complexity and crop rotation at the landscape scale. Journal of Applied Ecology, 50, 345–354.

Rusch, A., Chaplin‐Kramer, R., Gardiner, M.M., Hawro, V., Holland, J., Landis, D. et al. (2016) Agricultural landscape simplification reduces natural pest control: a quantitative synthesis. Agriculture, Ecosystems & Environment, 221, 198–204.

Sanders, D., Thébault, E., Kehoe, R. & Frank van Veen, F.J. (2018) Trophic redundancy reduces vulnerability to extinction cascades. Proceedings of the National Academy of Sciences, 115, 2419–2424.

Saska, P., van der Werf, W., de Vries, E. & Westerman, P.R. (2008) Spatial and temporal patterns of carabid activity‐density in cereals do not explain levels of predation on weed seeds. Bulletin of Entomological Research, 98, 169–181.

Thibaut, L.M. & Connolly, S.R. (2013) Understanding diversity–stability relationships: towards a unified model of portfolio effects. Ecology Letters, 16, 140–150.

Thiele, H.U. (2012) Carabid beetles in their environments: a study on habitat selection by adaptations in physiology and behaviour. Berlin: Springer Science & Business Media.

Tiemann, L.K., Grandy, A.S., Atkinson, E.E., Marin‐Spiotta, E. & McDaniel, M.D. (2015) Crop rotational diversity enhances belowground communities and functions in an agroecosystem. Ecology Letters, 18, 761–771.

Tikhonov, G., Opedal, Ø.H., Abrego, N., Lehikoinen, A., de Jonge, M.M.J., Oksanen, J. et al. (2020) Joint species distribution modelling with the R‐package Hmsc. Methods in Ecology and Evolution, 11, 442–447.

Varah, A., Ahodo, K., Coutts, S.R., Hicks, H.L., Comont, D., Crook, L. et al. (2020) The costs of human‐induced evolution in an agricultural system. Nature Sustainability, 3, 63–71.

Wallinger, C., Sint, D., Baier, F., Schmid, C., Mayer, R. & Traugott, M. (2015) Detection of seed DNA in regurgitates of granivorous carabid beetles. Bulletin of Entomological Research, 105, 728–735.

Weibull, A.‐C., Östman, Ö. & Granqvist, Å. (2003) Species richness in agroecosystems: the effect of landscape, habitat and farm management. Biodiversity and Conservation, 12, 1335–1355.

Weigelt, A., Schumacher, J., Roscher, C. & Schmid, B. (2008) Does biodiversity increase spatial stability in plant community biomass? Ecology Letters, 11, 338–347.

Westerman, P.R., Wes, J.S., Kropff, M.J. & Werf, W.V.D. (2003) Annual losses of weed seeds due to predation in organic cereal fields. Journal of Applied Ecology, 40, 824–836.

Yachi, S. & Loreau, M. (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proceedings of the National Academy of Sciences, 96, 1463–1468.