Understanding the responses of biodiversity to drivers of change and the effects of biodiversity on ecosystem properties and ecosystem services is a key challenge in the context of global environmental change. We performed a systematic review and meta-analysis of the scientific literature linking direct drivers of change and ecosystem services via functional traits of three taxonomic groups (vegetation, invertebrates, and vertebrates) to: (1) uncover trends and research biases in this field; and (2) synthesize existing empirical evidence. Our results show the existence of important biases in published studies related to ecosystem types, taxonomic groups, direct drivers of change, ecosystem services, geographical range, and the spatial scale of analysis. We found multiple evidence of links between drivers and services mediated by functional traits, particularly between land-use changes and regulating services in vegetation and invertebrates. Seventy-five functional traits were recorded in our sample. However, few of these functional traits were repeatedly found to be associated with both the species responses to direct drivers of change (response traits) and the species effects on the provision of ecosystem services (effect traits). Our results highlight the existence of potential "key functional traits," understood as those that have the capacity to influence the provision of multiple ecosystem services, while responding to specific drivers of change, across a variety of systems and organisms. Identifying "key functional traits" would help to develop robust indicator systems to monitor changes in biodiversity and their effects on ecosystem functioning and ecosystem services supply.

Faculty of Sustainability Institute of Ethics and Transdisciplinary Sustainability Research Leuphana University of Lüneburg Lüneburg Germany

Institute of Botany Academy of Sciences of the Czech Republic Trebon Czech Republic

Social ecological Systems Laboratory Department of Ecology Universidad Autónoma de Madrid Madrid Spain

Social ecological Systems Laboratory Department of Ecology Universidad Autónoma de Madrid Madrid Spain; Applied Research and Agricultural Extension Department Madrid Institute for Rural Agricultural and Food Research and Development Alcalá De Henares Madrid Spain

Zobrazit více v PubMed

Abelleira‐Martínez, O. J. , Fremier, A. K. , Günter, S. , Ramos Bendaña, Z. , Vierling, L. , Galbraith, S. M. , … Ordoñez, J. C. (2016). Scaling up functional traits for ecosystem services with remote sensing: Concepts and methods. Ecology and Evolution, 6(13), 4359–4371. PubMed PMC

Abson, D. J. , Von Wehrden, H. , Baumgärtner, S. , Fischer, J. , Hanspach, J. , Härdtle, W. , … Walmsley, D. (2014). Ecosystem services as a boundary object for sustainability. Ecological Economics, 103, 29–37.

Balvanera, P. , Pfisterer, A. B. , Buchmann, N. , He, J. S. , Nakashizuka, T. , Raffaelli, D. , & Schmid, B. (2006). Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters, 9, 1146–1156. PubMed

Balvanera, P. , Siddique, I. , Dee, L. , Paquette, A. , Isbell, F. , González, A. , … Griffin, J. N. (2014). Linking biodiversity and ecosystem services: Current uncertainties and the necessary next steps. BioScience, 64, 49–57.

Bennett, E. M. , Cramer, W. , Begossi, A. , Cundill, G. , Díaz, S. , Egoh, B. , … Tscharntke, T. (2015). Linking biodiversity, ecosystem services and human well‐being: Three challenges for designing research for sustainability. Current Opinion in Environmental Sustainability, 14, 76–85.

Biggs, R. , Schlüter, M. , Biggs, D. , Bohensky, E. L. , BurnSilver, S. , Cundill, G. , … West, P. C. (2012). Toward principles for enhancing the resilience of ecosystem services. Annual Review of Environment and Resources, 37, 421–448.

Biggs, R. , Schlüter, M. , & Schoon, M. L. (2015). Principles for Building Resilience. UK: Cambridge University Press.

Brown, K. A. , Johnson, S. E. , Parks, K. E. , Holmes, S. M. , Ivoandry, T. , Abram, N. K. , … Wright, P. C. (2013). Use of provisioning ecosystem services drives loss of functional traits across land use intensification gradients in tropical forests in Madagascar. Biological Conservation, 161, 118–127.

Cadotte, M. W. , Carscadden, K. , & Mirotchnick, N. (2011). Beyond species: Functional diversity and the maintenance of ecological processes and services. Journal of Applied Ecology, 48(5), 1079–1087.

Cardinale, B. J. , Duffy, J. E. , Gonzalez, A. , Hooper, D. U. , Perrings, C. , Venail, P. , … Naeem, S. (2012). Biodiversity loss and its impact on humanity. Nature, 486, 59–67. PubMed

Daniel, T. C. , Muhar, A. , Arnberger, A. , Aznar, O. , Boyd, J. W. , Chan, K. M. , … von der Dunk, A. (2012). Contributions of cultural services to the ecosystem services agenda. Proceedings of the National Academy of Sciences, 109(23), 8812–8819. PubMed PMC

De Bello, F. , Lavorel, S. , Diaz, S. , Harrington, R. , Cornelissen, J. H. C. , Bardgett, R. D. , … Harrison, P. A. (2010). Towards an assessment of multiple ecosystem processes and services via functional traits. Biodiversity and Conservation, 19, 2873–2893.

De Lima, R. F. , Dallimer, M. , Atkinson, P. W. , & Barlow, J. (2013). Biodiversity and land‐use change: Understanding the complex responses of an endemic‐rich bird assemblage. Diversity and Distribution, 19, 411–422.

Díaz, S. , Demissew, S. , Carabias, J. , Joly, C. , Lonsdale, M. , Ash, N. , … Zlatanova, D. (2015). The IPBES conceptual framework—Connecting nature and people. Current Opinion in Environmental Sustainability, 14, 1–16.

Díaz, S. , Lavorel, S. , De Bello, F. , Quétier, F. , Grigulis, K. , & Robson, T. M. (2007). Incorporating plant functional diversity effects in ecosystem service assessments. Proceedings of the National Academy of Sciences, 104, 20684–20689. PubMed PMC

Díaz, S. , Purvis, A. , Cornelissen, J. H. C. , Mace, G. M. , Donoghue, M. J. , Ewers, R. M. , … Pearse, W. D. (2013). Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecology and Evolution, 3, 2958–2975. PubMed PMC

Dirzo, R. , Young, H. S. , Galetti, M. , Ceballos, G. , Isaac, N. J. B. , & Collen, B. (2014). Defaunation in the Anthropocene. Science, 345(6195), 401–406. PubMed

Dukes, J. S. (2001). Biodiversity and invasibility in grassland microcosms. Oecologia, 126(4), 563–568. PubMed

Fazey, I. , Fischer, J. , & Lindenmayer, D. (2005). What do conservation biologists publish? Biological Conservation, 124, 63–73.

Frimpong, E. A. , & Angermeier, P. L. (2009). FishTraits: A database of ecological and life‐history traits of freshwater fishes of the United States. Fisheries, 34, 487–493.

García‐Llorente, M. , Iniesta‐Arandia, I. , Willaarts, B. , Harrison, P. A. , Berry, P. , Bayo, M. M. , … Martín‐López, B. (2015). Biophysical and socio‐cultural factors underlying spatial tradeoffs of ecosystem services in semiarid watersheds. Ecology & Society, 20(3), 39.

Gilroy, J. J. , Medina‐Uribe, C. A. , Haugaasen, T. , & Edwards, D. P. (2015). Effect of scale on trait predictors of species responses to agriculture. Conservation Biology, 29(2), 463–472. PubMed

Goodness, J. , Andersson, E. , Anderson, P. M. , & Elmqvist, T. (2016). Exploring the links between functional traits and cultural ecosystem services to enhance urban ecosystem management. Ecological Indicators, 70, 597–605.

Gossner, M. M. , Simons, N. K. , Achtziger, R. , Blick, T. , Dorow, W. , Dziock, F. , … Weisser, W. W. (2015). A summary of eight traits of Coleoptera, Hemiptera, Orthoptera and Araneae, occurring in grasslands in Germany. Scientific Data, 2, 150013. PubMed PMC

Grigulis, K. , Lavorel, S. , Krainer, U. , Legay, N. , Baxendale, C. , Dumont, M. , … Clèment, J. C. (2013). Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services. Journal of Ecology, 101, 47–57.

Gross, K. L. , Willig, M. R. , Gough, L. , Inouye, R. , & Cox, S. B. (2000). Patterns of species density and productivity at different spatial scales in herbaceous plant communities. Oikos, 89, 417–427.

Hanski, I. , Von Hertzen, L. , Fyhrquist, N. , Koskinen, K. , Torppa, K. , Laatikainen, T. , … Haahtela, T. (2012). Environmental biodiversity, human microbiota, and allergy are interrelated. Proceedings of the National Academy of Sciences, 109, 8334–8339. PubMed PMC

Harrison, P. A. , Berry, P. M. , Simpson, G. , Haslett, J. R. , Blicharska, M. , Bucur, M. , … Turkelboom, F. (2014). Linkages between biodiversity attributes and ecosystem services: A systematic review. Ecosystem Services, 9, 191–203.

Hevia, V. , Carmona, C. P. , Azcárate, F. M. , Torralba, M. , Alcorlo, P. , Ariño, R. , … González, J. A. (2016). Effects of land use on taxonomic and functional diversity: A cross‐taxon analysis in a Mediterranean landscape. Oecologia, 181(4), 959–970. PubMed

Homburg, K. , Homburg, N. , Schäfer, F. , Schuldt, A. , & Assmann, T. (2014). Carabids.org – A dynamic online database of ground beetle species traits (Coleoptera, Carabidae). Insect Conservation and Diversity, 7, 195–205.

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

Isbell, F. , Calcagno, V. , Hector, A. , Connolly, J. , Harpole, W. S. , Reich, P. B. , … Loreau, M. (2011). High plant diversity is needed to maintain ecosystem services. Nature, 477, 199–203. PubMed

Kattge, J. , Lavorel, S. , Prentice, I. C. , Leadley, P. , Bönisch, G. , Garnier, E. , … Wirth, C. (2011). TRY – a global database of plant traits. Global Change Biology, 17, 2905–2935.

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

Larsen, T. H. , Williams, N. M. , & Kremen, C. (2005). Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecology Letters, 8(5), 538–547. PubMed

Lavorel, S. (2013). Plant functional effects on ecosystem services. Journal of Ecology, 101, 4–8.

Lavorel, S. , Díaz, S. , Cornelissen, J. H. C. , Garnier, E. , Harrison, S. P. , McIntyre, S. , … Urcey, C. (2007). Plant functional types: Are we getting any closer to the Holy Grail? In Canadell J., Pitelka L. F., & Pataki D. (Eds.), Terrestrial ecosystems in a changing world (pp. 149–164). Berlin Heidelberg: Springer.

Lavorel, S. , & Garnier, E. (2002). Predicting changes in community composition and ecosystem functioning from plant traits: Revisiting the Holy Grail. Functional Ecology, 16, 545–556.

Lavorel, S. , Grigulis, K. , Lamarque, P. , Colace, M. P. , Garden, D. , Girel, J. , … Douzet, R. (2011). Using plant functional traits to understand the landscape distribution of multiple ecosystem services. Journal of Ecology, 99, 135–147.

Lavorel, S. , Storkey, J. , Bardgett, R. D. , de Bello, F. , Berg, M. P. , Le Roux, X. , … Harrington, R. (2013). A novel framework for linking functional diversity of plants with other trophic levels for the quantification of ecosystem services. Journal of Vegetation Science, 24, 942–948.

Mace, G. M. , Norris, K. , & Fitter, A. H. (2012). Biodiversity and ecosystem services: A multilayered relationship. Trends in Ecology & Evolution, 27, 19–26. PubMed

Mitchell, M. G. , Bennett, E. M. , & Gonzalez, A. (2013). Linking landscape connectivity and ecosystem service provision: Current knowledge and research gaps. Ecosystems, 16(5), 894–908.

Moretti, M. , de Bello, F. , Ibanez, S. , Fontana, S. , Pezzatti, G. B. , Dziock, F. , … Lavorel, S. (2013). Linking traits between plants and invertebrate herbivores to track functional effects of land‐use changes. Journal of Vegetation Science, 24, 949–962.

Mori, A. S. , Furukawa, T. , & Sasaki, T. (2013). Response diversity determines the resilience of ecosystems to environmental change. Biological Reviews, 88(2), 349–364. PubMed

Mouchet, M. A. , Lamarque, P. , Martín‐López, B. , Crouzat, E. , Gos, P. , Byczek, C. , & Lavorel, S. (2014). An interdisciplinary methodological guide for quantifying associations between ecosystem services. Global Environmental Change, 28, 298–308.

Myers, N. , Mittermeier, R. A. , Mittermeier, C. G. , da Fonseca, G. A. B. , & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–858. PubMed

Nagendra, H. , Reyers, B. , & Lavorel, S. (2013). Impacts of land change on biodiversity : Making the link to ecosystem services. Current Opinion in Environmental Sustainability, 5, 1–6.

Nahlik, A. M. , Kentula, M. E. , Fennessy, M. S. , & Landers, D. H. (2012). Where is the consensus? A proposed foundation for moving ecosystem service concepts into practice. Ecological Economics, 77, 27–35.

Newbold, T. , Scharlemann, J. P. , Butchart, S. H. , Şekercioğlu, Ç. H. , Joppa, L. , Alkemade, R. , & Purves, D. W. (2014). Functional traits, land‐use change and the structure of present and future bird communities in tropical forests. Global Ecology and Biogeography, 23(10), 1073–1084.

Nieto‐Romero, M. , Oteros‐Rozas, E. , González, J. A. , & Martín‐López, B. (2014). Exploring the knowledge landscape of ecosystem services assessments in Mediterranean agroecosystems: Insights for future research. Environmental Science & Policy, 37, 121–133.

Nimmo, D. G. , Mac Nally, R. , Cunningham, S. C. , Haslem, A. , & Bennett, A. F. (2015). Vive la résistance: Reviving resistance for 21st century conservation. Trends in Ecology & Evolution, 30(9), 516–523. PubMed

Oliver, T. H. , Heard, M. , Isaac, N. J. B. , Roy, D. B. , Procter, D. , Eigenbrod, F. , … Bullock, J. M. (2015). Biodiversity and resilience of ecosystem functions. Trends in Ecology & Evolution, 30, 673–684. PubMed

Pereira, H. M. , Ferrier, S. , Walters, M. , Geller, G. N. , Jongman, R. H. G. , Scholes, R. J. , … Wegmann, M. (2013). Essential biodiversity variables. Science, 339, 277–278. PubMed

Pereira, H. M. , Navarro, L. M. , & Martins, I. S. (2012). Global biodiversity change: The bad, the good, and the unknown. Annual Review of Environment and Resources, 37, 25–50.

Peterson, G. D. , Allen, C. R. , & Holling, C. S. (1998). Ecological resilience, biodiversity, and scale. Ecosystems, 1, 6–18.

Quétier, F. , Lavorel, S. , Thuiller, W. , & Davies, I. (2007). Plant‐trait based modeling assessment of ecosystem‐service sensitivity to land‐use change. Ecological Applications, 17, 2377–2386. PubMed

Radchuk, V. , Laender, F. , Brink, P. J. , & Grimm, V. (2015). Biodiversity and ecosystem functioning decoupled: Invariant ecosystem functioning despite non‐random reductions in consumer diversity. Oikos, 125, 424–433.

Ricketts, T. H. , Watson, K. B. , Koh, I. , Ellis, A. M. , Nicholson, C. C. , Posner, S. , … Sonter, L. J. (2016). Disaggregating the evidence linking biodiversity and ecosystem services. Nature Communications, 7, 13106. PubMed PMC

Seidl, R. , Spies, T. A. , Peterson, D. L. , Stephens, S. L. , & Hicke, J. A. (2015). Searching for resilience: Addressing the impacts of changing disturbance regimes on forest ecosystem services. Journal of Applied Ecology, 53, 120–129. PubMed PMC

Seppelt, R. , Dormann, C. F. , Eppink, F. V. , Lautenbach, S. , & Schmidt, S. (2011). A quantitative review of ecosystem service studies: Approaches, shortcomings and the road ahead. Journal of Applied Ecology, 48(3), 630–636.

Speight, M. C. D. , Castella, E. , & Sarthou, J. P. (2013). Syrph the Net: The database of European Syrphidae. Dublin: Syrph the Net Publications.

Srivastava, D. S. , & Vellend, M. (2005). Biodiversity‐ecosystem function research: Is it relevant to conservation? Annual Review of Ecology, Evolution, and Systematics, 36, 267–294.

Statzner, B. , Bonada, N. , & Dolédec, S. (2008). Conservation of taxonomic and biological trait diversity of European stream macroinvertebrate communities: A case for a collective public database. Biodiversity and Conservation, 16, 367–390.

Storkey, J. , Brooks, D. , Haughton, A. , Hawes, C. , Smith, B. M. , & Holland, J. M. (2013). Using functional traits to quantify the value of plant communities to invertebrate ecosystem service providers in arable landscapes. Journal of Ecology, 101, 38–46.

Suding, K. N. , Lavorel, S. , Chapin, F. S. III , Cornelissen, J. H. C. , Diaz, S. , Garnier, E. , … Navas, M. L. (2008). Scaling environmental change through the community level: A trait‐based response‐and‐effect framework for plants. Global Change Biology, 14, 1125–1140.

Thompson, P. L. , Davies, T. J. , & Gonzalez, A. (2015). Ecosystem functions across trophic levels are linked to functional and phylogenetic diversity. PLoS ONE, 10(2), e0117595. PubMed PMC

Valiente‐Banuet, A. , Aizen, M. A. , Alcántara, J. M. , Arroyo, J. , Cocucci, A. , Galetti, M. , … Zamora, R. (2015). Beyond species loss: The extinction of ecological interactions in a changing world. Functional Ecology, 29(3), 299–307.

Vandewalle, M. , Bello, F. , Berg, M. P. , Bolger, T. , Dolédec, S. , Dubs, F. , … Woodcock, B. A. (2010). Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodiversity and Conservation, 19, 2921–2947.

Velasco, D. , García‐Llorente, M. , Alonso, B. , Dolera, A. , Palomo, I. , Iniesta‐Arandia, I. , & Martín‐López, B. (2015). Biodiversity conservation research challenges in the 21st century: A review of publishing trends in 2000 and 2011. Environmental Science and Policy, 54, 90–96.

Verheyen, K. , Honnay, O. , Motzkin, G. , Hermy, M. , & Foster, D. R. (2003). Response of forest plant species to land‐use change: A life‐history trait‐based approach. Journal of Ecology, 91(4), 563–577.

Vieira, N. M. K. , Poff, N. L. , Carlisle, D. M. , Moulton, S. R. , Koski, M. L. , & Kondratieff, B. C. (2006). A database of lotic invertebrate traits for North America. Reston, VA: US Geological Survey.

Vihervaara, P. , Rönkä, M. , & Walls, M. (2010). Trends in ecosystem service research: Early steps and current drivers. Ambio, 39, 314–324. PubMed PMC

Violle, C. , Reich, P. B. , Pacala, S. W. , Enquist, B. J. , & Kattge, J. (2014). The emergence and promise of functional biogeography. Proceedings of the National Academy of Sciences, 111(38), 13690–13696. PubMed PMC

Vitousek, P. M. , Mooney, H. A. , Lubchenco, J. , & Melillo, J. M. (1997). Human domination of Earth's ecosystems. Science, 277(5325), 494–499.

Wood, S. A. , Karp, D. S. , DeClerck, F. , Kremen, C. , Naeem, S. , & Palm, C. A. (2015). Functional traits in agriculture: Agrobiodiversity and ecosystem services. Trends in ecology & evolution, 30(9), 531–539. PubMed