Abstract
Studies on biodiversity–ecosystem functioning (BEF) in highly controlled experiments often yield results incompatible with observations from natural systems: experimental results often reveal positive relationships between diversity and productivity, while for natural systems, zero or even negative relationships have been reported. The discrepancy may arise due to a limited or closed local species pool in experiments, while natural systems in meta-community contexts experience dynamic processes, i.e., colonization and extinctions. In our study, we analysed plant community properties and above-ground biomass within a semi-natural (i.e., not weeded) experiment in an agricultural landscape. Eleven replicates with four different diversity levels were created from a species pool of 20 wildflower species. We found an overall significant negative relationship between total diversity and productivity. This relationship likely resulted from invasion resistance: in plots sown with low species numbers, we observed colonization by low-performing species; colonization increased species richness but did not contribute substantially to productivity. Interestingly, when analysing the biomass of the sown and the colonizer species separately, we observed in both cases positive BEF relationships, while this relationship was negative for the whole system. A structural equation modelling approach revealed that higher biomass of the sown species was linked to higher species richness, while the positive BEF relationship of the colonizers was indirect and constrained by the sown species biomass. Our results suggest that, in semi-natural conditions common in extensive agroecosystems, the negative BEF relationship results from the interplay between local dominant species and colonization from the regional species pool by subordinate species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Assaf TA, Beyschlag W, Isselstein J (2011) The relationship between plant diversity and productivity in natural and in managed grasslands. Appl Ecol Environ Res 9:157–166. https://doi.org/10.15666/aeer/0902_157166
Bartón K (2015) MuMIn: multi-model inference. R package version 1.9.13. 1:18
Bracken MES, Williams SL (2017) The underappreciated role of life history in mediating the functional consequences of biodiversity change. Oikos 126:488–496. https://doi.org/10.1111/oik.03884
Bruggisser OT, Sandau N, Blandenier G, Fabian Y, Kehrli P, Aebi A, Naisbit RE, Bersier L-F (2012) Direct and indirect bottom-up and top-down forces shape the abundance of the orb-web spider Argiope bruennichi. Basic Appl Ecol 13:706–714. https://doi.org/10.1016/j.baae.2012.10.001
Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. Proc Natl Acad Sci USA 105:17012–17017. https://doi.org/10.1073/pnas.0805962105
Cadotte MW, Hamilton MA, Murray BR (2009) Phylogenetic relatedness and plant invader success across two spatial scales. Divers Distrib 15:481–488. https://doi.org/10.1111/j.1472-4642.2009.00560.x
Cardinale BJ, Nelson K, Palmer MA (2000) Linking species diversity to the functioning of ecosystems: on the importance of environmental context. Oikos 91:175–183. https://doi.org/10.1034/j.1600-0706.2000.910117.x
Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992. https://doi.org/10.1038/nature05202
Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS, Loreau M, Weis JJ (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. Proc Natl Acad Sci 104:18123–18128. https://doi.org/10.1073/pnas.0709069104
Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecol Lett 12:693–715. https://doi.org/10.1111/j.1461-0248.2009.01314.x
Chapin FS III, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277:500–504. https://doi.org/10.1126/science.277.5325.500
Díaz S, Lavorel S, de Bello F, Quétier F, Grigulis K, Robson TM (2007) Incorporating plant functional diversity effects in ecosystem service assessments. Proc Natl Acad Sci USA 104:20684–20689. https://doi.org/10.1073/pnas.0704716104
Fabian Y, Sandau N, Bruggisser OT, Kehrli P, Aebi A, Rohr RP, Naisbit RE, Bersier L-F (2012) Diversity protects plant communities against generalist molluscan herbivores. Ecol Evol 2:2460–2473. https://doi.org/10.1002/ece3.359
Fabian Y, Sandau N, Bruggisser OT, Aebi A, Kehrli P, Rohr RP, Naisbit RE, Bersier L-F (2013) The importance of landscape and spatial structure for hymenopteran-based food webs in an agro-ecosystem. J Anim Ecol 82:1203–1214. https://doi.org/10.1111/1365-2656.12103
Fabian Y, Sandau N, Bruggisser OT, Aebi A, Kehrli P, Rohr RP, Naisbit RE, Bersier L-F (2014) Plant diversity in a nutshell: testing for small-scale effects on trap nesting wild bees and wasps. Ecosphere 5:art18. https://doi.org/10.1890/es13-00375.1
Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, Thousand Oaks
Funk JL, Cleland EE, Suding KN, Zavaleta ES (2008) Restoration through reassembly: plant traits and invasion resistance. Trends Ecol Evol 23:695–703. https://doi.org/10.1016/j.tree.2008.07.013
Grace JB, Anderson TM, Smith MD, Seabloom E, Andelman SJ, Meche G, Weiher E, Allain LK, Jutila H, Sankaran M, Knops J, Ritchie M, Willig MR (2007) Does species diversity limit productivity in natural grassland communities? Ecol Lett 10:680–689. https://doi.org/10.1111/j.1461-0248.2007.01058.x
Günter M (2000) Establishment and care of perennial wildflower strips under specific conditions for arable farming in the Swiss midlands. Agrarökologie 37:1–154
Haaland C, Naisbit RE, Bersier L-F (2011) Sown wildflower strips for insect conservation: a review. Insect Conserv Divers 4:60–80. https://doi.org/10.1111/j.1752-4598.2010.00098.x
Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324:636–638. https://doi.org/10.1126/science.1169640
Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Högberg P, Huss-Danell K, Joshi J, Jumpponen A, Körner C, Leadley PW, Loreau M, Minns A, Mulder CPH, O’Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, Scherer-Lorenzen M, Schulze E-D, Siamantziouras A-SD, Spehn EM, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127. https://doi.org/10.1126/science.286.5442.1123
Hector A, Dobson K, Minns A, Bazeley-White E, Lawton JH (2001) Community diversity and invasion resistance: an experimental test in a grassland ecosystem and a review of comparable studies. Ecol Res 16:819–831. https://doi.org/10.1046/j.1440-1703.2001.00443.x
Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432. https://doi.org/10.2307/1934352
Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’Connor MI (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108. https://doi.org/10.1038/nature11118
Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110:449–460. https://doi.org/10.1007/s004420050180
Jain M, Flynn DFB, Prager CM, Hart GM, DeVan CM, Ahrestani FS, Palmer MI, Bunker DE, Knops JMH, Jouseau CF, Naeem S (2014) The importance of rare species: a trait-based assessment of rare species contributions to functional diversity and possible ecosystem function in tall-grass prairies. Ecol Evol 4:104–112. https://doi.org/10.1002/ece3.915
Jørgensen SE (2004) Model selection and multimodel inference. Ecol Modell 172:96–97. https://doi.org/10.1016/j.ecolmodel.2003.11.004
Kahmen A, Perner J, Audorff V, Weisser W, Buchmann N (2005) Effects of plant diversity, community composition and environmental parameters on productivity in montane European grasslands. Oecologia 142:601–615. https://doi.org/10.1007/s00442-004-1749-2
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: r tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Kleyer M, Bekker RM, Knevel IC, Bakker JP, Thompson K, Sonnenschein M, Poschlod P, Van Groenendael JM, Klimeš L, Klimešová J, Klotz S, Rusch GM, Hermy M, Adriaens D, Boedeltje G, Bossuyt B, Dannemann A, Endels P, Götzenberger L, Hodgson JG, Jackel A-K, Kühn I, Kunzmann D, Ozinga WA, Römermann C, Stadler M, Schlegelmilch J, Steendam HJ, Tackenberg O, Wilmann B, Cornelissen JHC, Eriksson O, Garnier E, Peco B (2008) The LEDA traitbase: a database of life-history traits of the Northwest European flora. J Ecol 96:1266–1274. https://doi.org/10.1111/j.1365-2745.2008.01430.x
Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579. https://doi.org/10.1111/2041-210X.12512
Legendre P, Legendre L (1998) Numerical ecology, 2 english edn. Elsevier, Amsterdam
Lepš J (2004) What do the biodiversity experiments tell us about consequences of plant species loss in the real world? Basic Appl Ecol 5:529–534. https://doi.org/10.1016/j.baae.2004.06.003
Lepŝ J, Doleẑal J, Bezemer TM, Brown VK, Hedlund K, Arroyo MI, Bracht Jörgensen H, Lawson CS, Mortimer SR, Peix Geldart A, Rodríguez Barrueco C, Santa Regina I, Ŝmilauer P, van der Putten WH (2007) Long-term effectiveness of sowing high and low diversity seed mixtures to enhance plant community development on ex-arable fields. Appl Veg Sci 10:97–110. https://doi.org/10.1111/j.1654-109X.2007.tb00508.x
Levine JM, D’Antonio CM (1999) Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87:15. https://doi.org/10.2307/3546992
Loreau M (1998) Biodiversity and ecosystem functioning: a mechanistic model. Proc Natl Acad Sci USA 95:5632–5636. https://doi.org/10.1073/Pnas.95.10.5632
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. https://doi.org/10.1038/35083573
Loreau M, Mouquet N (1999) Immigration and the maintenance of local species diversity. Am Nat 154:427–440. https://doi.org/10.1086/303252
Milbau A, Nijs I, De Raedemaecker F, Reheul D, De Cauwer B (2005) Invasion in grassland gaps: the role of neighbourhood richness, light availability and species complementarity during two successive years. Funct Ecol 19:27–37. https://doi.org/10.1111/j.0269-8463.2005.00939.x
Minchin PRR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69:89–107. https://doi.org/10.1007/BF00038690
Mouquet N, Moore JL, Loreau M (2002) Plant species richness and community productivity: why the mechanism that promotes coexistence matters. Ecol Lett 5:56–65. https://doi.org/10.1046/j.1461-0248.2002.00281.x
Narwani A, Matthews B, Fox JW, Venail PA (2015) Using phylogenetics in community assembly and ecosystem functioning research. Funct Ecol 29:589–591. https://doi.org/10.1111/1365-2435.12431
Nentwig W (2000) Streifenförmige ökologische Ausgleichsflächen in der Kulturlandschaft: Ackerkrautstreifen, Buntbrachem, Feldränder. vaö - Verlag Agrarökologie, Bern, Hannover
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner HH (2015) Vegan: community ecology package. R packag. version 2.2-1
Parain E, Rohr RP, Gray SM, Bersier L-F (2019) Global warming disrupts biodiversity-ecosystem functioning relationships. Am Nat (in press)
Pärtel M, Szava-Kovats RC, Zobel M (2011) Dark diversity: shedding light on absent species. Trends Ecol Evol 26:124–128. https://doi.org/10.1016/j.tree.2010.12.004
Petchey OL (2004) On the statistical significance of functional diversity effects. Funct Ecol 18:297–303. https://doi.org/10.1111/j.0269-8463.2004.00852.x
Petermann JS, Fergus AJF, Roscher C, Turnbull LA, Weigelt A, Schmid B (2010) Biology, chance, or history? The predictable reassembly of temperate grassland communities. Ecology 91:408–421. https://doi.org/10.1890/08-2304.1
Pfisterer AB, Joshi J, Schmid B, Fischer M (2004) Rapid decay of diversity-productivity relationships after invasion of experimental plant communities. Basic Appl Ecol 5:5–14. https://doi.org/10.1078/1439-1791-00215
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 1–86
R Core Team (2015). R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org/
Richards SA (2005) Testing ecological theory using the information-theoretic approach: examples and cautionary results. Ecology 86:2805–2814. https://doi.org/10.1890/05-0074
Richards SA (2008) Dealing with overdispersed count data in applied ecology. J Appl Ecol 45:218–227. https://doi.org/10.1111/j.1365-2664.2007.01377.x
Rohr RP, Saavedra S, Peralta G, Frost CM, Bersier L-F, Bascompte J, Tylianakis JM (2016) Persist or produce: a community trade-off tuned by species evenness. Am Nat 188:411–422. https://doi.org/10.1086/688046
Rösch V, Tscharntke T, Scherber C, Batáry P (2015) Biodiversity conservation across taxa and landscapes requires many small as well as single large habitat fragments. Oecologia 179:209–222. https://doi.org/10.1007/s00442-015-3315-5
Roscher C, Schumacher J, Baade J (2004) The role of biodiversity for element cycling and trophic interactions: an experimental approach in a grassland community. Basic Appl Ecol 5:107–121. https://doi.org/10.1078/1439-1791-00216
Roscher C, Temperton VM, Scherer-Lorenzen M et al (2005) Overyielding in experimental grassland communities—irrespective of species pool or spatial scale. Ecol Lett 8:419–429. https://doi.org/10.1111/j.1461-0248.2005.00736.x
Roscher C, Temperton VM, Buchmann N, Schulze E-D (2009) Community assembly and biomass production in regularly and never weeded experimental grasslands. Acta Oecol 35:206–217. https://doi.org/10.1016/j.actao.2008.10.003
Roscher C, Fergus AJF, Petermann JS, Buchmann N, Schmid B, Schulze E-D (2013) What happens to the sown species if a biodiversity experiment is not weeded? Basic Appl Ecol 14:187–198. https://doi.org/10.1016/j.baae.2013.01.003
Rose L, Leuschner C (2012) The diversity–productivity relationship in a permanent temperate grassland: negative diversity effect, dominant influence of management regime. Plant Ecol Divers 874:1–10. https://doi.org/10.1080/17550874.2012.723763
Rychtecká T, Lanta V, Weiterová I, Lepš J (2014) Sown species richness and realized diversity can influence functioning of plant communities differently. Naturwissenschaften 101:637–644. https://doi.org/10.1007/s00114-014-1198-7
Sandau N, Rohr RP, Naisbit RE, Fabian Y, Bruggisser OT, Kehrli P, Aebi A, Bersier L-F (2014) Including community composition in biodiversity-productivity models. Methods Ecol Evol 5:815–823. https://doi.org/10.1111/2041-210X.12215
Thompson K, Askew AP, Grime JP, Dunnett NP, Willis AJ (2005) Biodiversity, ecosystem function and plant traits in mature and immature plant communities. Funct Ecol 19:355–358. https://doi.org/10.1111/j.0269-8463.2005.00936.x
Tilman DG (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845. https://doi.org/10.1126/science.1060391
Tilman DG, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720. https://doi.org/10.1038/379718a0
Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Fründ J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev 87:661–685. https://doi.org/10.1111/j.1469-185X.2011.00216.x
Van Ruijven J, Berendse F (2003) Positive effects of plant species diversity on productivity in the absence of legumes. Ecol Lett 6:170–175. https://doi.org/10.1046/j.1461-0248.2003.00427.x
Venail PA, Gross K, Oakley TH, Narwani A, Allan E, Flombaum P, Isbell F, Joshi J, Reich PB, Tilman D, van Ruijven J, Cardinale BJ (2015) Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct Ecol 29:615–626. https://doi.org/10.1111/1365-2435.12432
Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183. https://doi.org/10.1111/j.1471-8286.2004.00829.x
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Acknowledgements
We thank Jan Lepš, Loïc Pellissier and Sarah M. Gray for helpful suggestions on an earlier version of the manuscript, and Sven Bacher for help with model averaging. We are grateful for the participation of Jacques Studer and of the farmers from Grandcour and all the valuable help provided by friends and family members.
Funding
This study was supported by the Swiss National Science Foundation (Grant 31003A_138489 to LFB).
Author information
Authors and Affiliations
Contributions
NS, PK and LFB planned the experiment, NS, AA, YF and OTB conducted the experiment, NS, RPR and LFB conducted the analyses; NS, REN and LFB wrote the article.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Data accessibility
Data will be available in Dryad.
Additional information
Communicated by Sarah M. Emery.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sandau, N., Naisbit, R.E., Fabian, Y. et al. Understanding negative biodiversity–ecosystem functioning relationship in semi-natural wildflower strips. Oecologia 189, 185–197 (2019). https://doi.org/10.1007/s00442-018-4305-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-018-4305-1