Jeannine Cavender-Bares (University of Minnesota, Minneapolis, USA), Miklós Dombos (Hungarian Academy of Sciences, Budapest, Hungary), Susanne Dunker (Helmholtz Centre for Environmental Research (UFZ), Leipzig, Germany), Forest Isbell (University of Minnesota, Minneapolis, USA), Birgitta König-Ries (Friedrich Schiller University Jena, Jena, Germany), Liesje Mommer (Wageningen University, Wageningen, The Netherlands), Kevin Mueller (Cleveland State University, Cleveland, USA), Koen Verhoeven (NIOO, Wageningen, The Netherlands), Michael Vohland (Leipzig University, Leipzig, Germany), Nils Wagemaker (Radboud University, Nijmegen, The Netherlands)

Temporal changes of biodiversity effects on ecosystem functions

A plethora of experimental studies has shown that the magnitude and stability of ecosystem functions increase with biodiversity (Cardinale et al. 2012, Isbell et al. 2015). Short-term experiments mostly predict a saturating relationship between biodiversity and ecosystem functions, implying that biodiversity effects are stronger at low biodiversity, and the loss of species at higher biodiversity levels has little effect (Cardinale et al. 2011, Cardinale et al. 2012). However, the few existing long-term experiments have challenged this view by demonstrating the strength of the biodiversity effect to increase with time, i.e., the saturating BEF relationship to become (more) linear (Reich et al. 2012, Guerrero-Ramírez et al. 2017). In fact, biodiversity effects seem to become increasingly important when more environmental contexts, functions, and experimental years are considered (Isbell et al. 2011, Eisenhauer et al. 2018 These findings contrast with the notion of saturating biodiversity effects, and thus have fundamentally different implications for the consequences of biodiversity change as well as the many related functions and services for humankind. Long-term biodiversity experiments are, therefore, not only key to understand mechanisms underlying BEF relationships at ecological equilibrium (Eisenhauer et al. 2012a, Eisenhauer et al. 2012b), but also to provide better-informed recommendations for land managers and policy makers (Hungate et al. 2017, Isbell et al. 2017). The Jena Experiment is one of the few existing long-term experiments that allows scientists to assess whether short-term and long-term biodiversity effects are indeed qualitatively different and to uncover the mechanistic basis of divergence of short- versus long-term effects.

While the diverging trends are apparent, it is currently unclear whether strengthening biodiversity effects are attributable to

1. deteriorating performance of low diversity communities,
2. improving performance of high diversity communities, or
3. both (Meyer et al. 2016, Guerrero-Ramírez et al. 2017, Eisenhauer et al. 2012b).

Since low-diversity plant communities are widely used in landscapes managed for production, such as agricultural systems and tree plantations (Isbell et al. 2017), deteriorating low-diversity communities over time may have important implications for the long-term provisioning of vital ecosystem services in managed ecosystems. A recent meta-analysis of 26 long-term grassland and forest biodiversity experiments shows that biodiversity–ecosystem functioning relationships strengthen mainly by greater increases in functioning in high-diversity communities in grasslands and forests (Guerrero-Ramírez et al. 2017). In grasslands, however, biodiversity effects also strengthen due to decreases in functioning in low-diversity communities. The synthesis of multiple ecosystem functions in the Jena Experiment also suggests that both deteriorating performance at low diversity and improving performance at high diversity contribute to strengthening BEF relationships over time (Meyer et al. 2016). The generality of those findings and the paucity of experiments that capture long-term effects puts long-term studies in the unique position to unravel the mechanisms that are responsible for increasing biodiversity effects over time (Eisenhauer 2018). Moreover, in order to derive such a mechanistic understanding, potential confounding influences of calendar year have to be ruled out by comparing ecosystems of different age in the same calendar years, as we do in the Field Experiment that we set up in preparation of the requested Research Unit (see below). Thus, the Jena Experiment in particular allows in-depth understanding of the full range of biotic interactions and eco-evolutionary dynamics and how they interactively influence ecosystem functioning in the short- and in the long-term.

Potential mechanisms underlying temporal changes of biodiversity effects

There are several possible causes that may explain the declining performance of low-diversity plant communities over time. Many of those are related to the assembly of plant community-specific above- and belowground microbial and animal communities (Lange et al. 2015, Ebeling et al. 2018, Schmid et al. 2019, Schuldt et al. 2019) that feed back to plant community composition and performance through different biotic interactions (Bever et al. 1997, Bever 2003, Eisenhauer 2012). Accumulation of specific plant antagonists and imbalanced use of resources can generate ‘negative feedback effects’ on plants at low plant diversity (Schnitzer et al. 2011, Eisenhauer et al. 2012a, Kulmatiski et al. 2012, Mommer et al. 2018). On the other side of the spectrum, improving high-diversity communities have been associated with diversity-dependent increases in soil fertility from greater storage of carbon and nitrogen (Fornara and Tilman 2008, Reich et al. 2012, Leimer et al. 2016), increase in plant complementarity effects (Cardinale et al. 2007, Marquard et al. 2009, Reich et al. 2012), accumulation of plant growth facilitators at high plant diversity (‘positive feedback effects’ by e.g., mycorrhizal fungi, biocontrol bacteria; Eisenhauer et al. 2012a, Latz et al. 2012), and, more recently, increasing niche differentiation by co-evolutionary adaptation (Zuppinger-Dingley et al. 2014). Both types of feedback effects may ultimately co-determine an increase in the strength of positive plant diversity effects in the long term (Eisenhauer 2012, Eisenhauer 2018). However, the relative importance of positive and negative feedbacks as well as the main agents of varying community assembly effects, their eco-evolutionary implications, and their context-dependency remain poorly understood.

Ecological processes, such as changes in the competitive environment as well as antagonistic and beneficial multitrophic interaction partners above and below the ground impose selective pressures on members of the community and thereby create ‘eco-to-evo’ feedbacks (Hendry 2016). The subsequent evolutionary changes, in turn, will alter the conditions for other members of the community via ‘evo-to-eco’ feedbacks (Whitham et al. 2006, Lipowsky et al. 2011, van Moorsel et al. 2018), giving rise to complex eco-evolutionary dynamics (Fig. 1). Some changes in plant traits will be plastic responses, while others are genetic or epigenetic in origin, and lead to adaptation and differences along the diversity gradient (Whitham et al. 2006, Lipowsky et al. 2011, van Moorsel et al. 2018). Understanding the relative role of these components is of importance, because the mechanisms determine how reversible the changes are and how much they contribute to long-term BEF relationships. Open-ended questions are if variation in trait expression is related to micro-evolutionary changes as well as the role of traits that may be relevant for biotic interactions and feedback effects, such as defense traits at the physiological level. Evolutionary changes, such as increased niche differentiation (Zuppinger-Dingley et al. 2014), and increased resource-use complementarity due to community assembly processes (Reich et al. 2012, Roscher et al. 2013), will slowly build up and can thus produce increasing biodiversity effects over time (Fig. 1). Yet, it remains unexplored whether short-term and long-term biodiversity effects are qualitatively different, such that short-term effects may be dominated by phenotypic plasticity and community assembly, while long-term effects may be co-determined by eco-evolutionary dynamics that may continue to produce divergence in plant community performance in the long-term. Ultimately, ecological and evolutionary processes are intertwined, and long-term experiments are needed not only to gain basic understanding of the relative importance as well as interactions of these processes, but also to apply these concepts to better provisioning of ecosystem functions and stability (Tilman and Snell-Rood 2014).

Figure 1.  

A. Conceptual diagram of the mechanistic approach of the planned Research Unit. B. Conceptual scheme of the proposed evolutionary niche shifts in plant monocultures and mixtures. This idea feeds into our understanding of how evolutionary history influences the ecological interactions of species that compete for growth factors, ultimately defining biotope space (gray rectangle; Hutchinson 1978). Graphically depicted, species (ellipses) in mixture will show increasing niche differentiation over time due to competition (niche overlap). Thus, history of selection in diverse communities is expected to result in greater interspecific differences (less overlap of ellipses) and more specialization (smaller ellipses) than a history of isolation (monocultures). In monocultures, species will experience strong selection pressure by accumulating soil-borne pathogens, and species may invest energy in chemical and morphological defense traits (depicted by ellipses shifting towards the same corner of the habitat space). Plants in mixtures together may exploit more available biotope space than single monocultures, causing increasing diversity effects on ecosystem functions over time. However, there is limited support for this assumption for traits related to light (e.g., Lipowsky et al. 2015, Roscher et al. 2015) and resource use (Jesch et al. 2018) so far.

The proposed Research Unit will address this knowledge gap by asking the overarching question: Are increasing biodiversity–ecosystem functioning relationships with time caused by changing biotic interactions due to the interplay between multitrophic community assembly processes and eco-evolutionary dynamics? As community assembly, biotic interactions, and eco-evolutionary processes strongly interact in influencing plant traits and signals in space and time, collaboration across the proposed subprojects in targeted and unique plant history and soil history experiments using cutting-edge technology will produce significant synergies and novel mechanistic insights into BEF relationships.

Spokesperson and principle investigators highlighted.

1. Craven, D. Eisenhauer N, Pearse W D, Hautier Y, Isbell F, Roscher C, Bahn M, Beierkuhnlein C, Bönisch G, Buchmann N, Byun C, Catford JA, Cerabolini BE L, Cornelissen JHC, Craine JM, De Luca E, Ebeling A, Griffin JN, Hector A, Hines J, Jentsch A, Kattge J, Kreyling J, Lanta V, Lemoine N, Meyer ST, Minden V, Onipchenko V, Polley WH, Reich PB, van Ruijven J, Schamp B, Smith MD, Soudzilovskaia NA, Tilman D, Weigelt A, Wilsey B, Manning P (2018) Multiple facets of biodiversity drive the diversity-stability relationship. Nature Ecology & Evolution 2: 1579-1587.
2. Eisenhauer N, Dobies T, Cesarz S, Hobbie SE, Meyer RJ, Worm K, Reich PB (2013) Plant diversity effects on soil food webs are stronger than those of elevated CO₂ and N deposition in a long-term grassland experiment. Proceedings of the National Academy of Sciences USA 110: 6889-6894.
3. Eisenhauer N , Herrmann S, Hines J, Buscot F, Siebert J, Thakur MP (2018b) The dark side of animal phenology. Trends in Ecology and Evolution 33: 898-901.
4. Guerrero-Ramirez NR, Craven D, Reich PB, Ewel JJ, Isbell F, Koricheva J, Parrotta JA, Auge H, Erickson HE, Forrester DI, Hector H, Joshi J, Montagnini F, Palmborg C, Piotto D, Potvin C, Roscher C, van Ruijven J, Tilman D, Wilsey B and Eisenhauer N (2017) Diversity-dependent temporal divergence of ecosystem functioning in experimental ecosystems. Nature Ecology & Evolution 1: 1639-1642.
5. Isbell F, Craven D, Connolly J, Loreau M, Schmid B, Beierkuhnlein H, Bezemer TM, Bonin C, Bruelheide H, de Luca E, Ebeling A, Griffin J, Guo Q, Hautier Y, Hector A, Jentsch A, Kreyling J, Lanta V, Manning P, Meyer ST, Mori AS, Naeem S, Niklaus PA, Polley HW, Reich PB, Roscher C, Seabloom EW, Smith MD, Thakur MP, Tilman D, Tracy BF, van der Putten WH, van Ruijven J, Weigelt A, Weisser WW, Wilsey B, Eisenhauer N (2015) Biodiversity increases the resistance of ecosystem productivity to climate extremes. Nature 526: 574-577.
6. Lange M, Eisenhauer N, Sierra CA, Bessler H, Engels C, Griffiths RI, Mellado-Vázquez PG, Malik A, Roy J, Scheu S, Steinbeiss S, Thomson BC, Trumbore SE, Gleixner G (2015) Plant diversity drives soil carbon storage by increased soil microbial activity. Nature Communications 6: 6707.
7. Reich PB, Tilman D, Isbell F, Mueller K, Hobbie SE, Flynn DFB and Eisenhauer N (2012) Impacts of biodiversity loss escalate through time as redundancy fades. Science 336: 589-592.
8. Scherber C, Eisenhauer N, Weisser WW, Schmid B, Voigt W, Schulze E-D, Roscher C, Weigelt A, Allan E, Beßler H, Bonkowski M, Buchmann N, Buscot F, Clement LW, Ebeling A, Engels C, Fischer M, Halle S, Kertscher I, Klein A-M, Koller R, König S, Kowalski E, Kummer V, Kuu A, Lange M, Lauterbach D, Middelhoff C, Migunova VD, Milcu A, Müller R, Partsch S, Petermann JS, Renker C, Rottstock T, Sabais ACW, Scheu S, Schumacher J, Temperton VM and Tscharnke T (2010) Bottom-up effects of plant diversity on biotic interactions in a biodiversity experiment. Nature 468: 553-556.
9. Schuldt A, Ebeling A, Kunz M, Staab M, Guimarães-Steinicke C, Bachmann D, Buchmann N, Durka W, 10, Fichtner A, Fornoff F, Härdtle W, Hertzog L, Klein A-M, Roscher C, Schaller J, von Oheimb G, Weigelt A, Weisser WW, Wirth C, Zhang J, Bruelheide H, Eisenhauer N (2019) Multiple plant diversity components drive consumer communities across ecosystems. Nature Communications 10: 1460.
10. Schwarz B, Barnes AD, Thakur MP, Brose U, Ciobanu M, Reich PB, Rich RL, Rosenbaum B, Stefanski A and Eisenhauer N (2017) Warming alters energetic structure and function but not resilience of soil food webs. Nature Climate Change 7: 895-900.

New objectives based on a strong research history

The previous Research Units within the Jena Experiment have yielded unique insights into the role of plant diversity for multiple ecosystem functions and trophic levels (e.g., Scherber et al. 2010, Allan et al. 2013, Lange et al. 2015, Lefcheck et al. 2015, Schuldt et al. 2019), stability of ecosystem functions (e.g., Isbell et al. 2015, Wright et al. 2015, Craven et al. 2018), as well as first insights into the role of eco-evolutionary dynamics (e.g., Zuppinger-Dingley et al. 2014, Zuppinger-Dingley et al. 2016, van Moorsel et al. 2018). However, our understanding of the ecological mechanisms (Laforest-Lapointe et al. 2017, Guerrero-Ramírez et al. 2017) and eco-evolutionary feedbacks (van Moorsel et al. 2018, Schmid et al. 2019) underlying changes in BEF relationships over time is still in its infancy. Considering multitrophic community assembly and exploring subsequent biotic interaction variation as determinant of long-term BEF relationships will be key to advance this field of research (Hines et al. 2015, Barnes et al. 2018). Specifically, the combination of the unique research infrastructure of the Jena Experiment and novel experimental approaches with cutting-edge technology in microbiology, chemical ecology, proximal sensing, genomics, and food web modelling will allow the proposed Research Unit to take a leading role in BEF research. We propose to zoom in on the underlying mechanisms of long-term BEF by investigating the different influences that plants experience in their interactions with plant and consumer communities.

The subprojects (SPs) of the proposed Research Unit fall into two main categories and four tightly linked research areas (RA) (Fig. 2). Subprojects under “Microbial community assembly” (RA1) and “Assembly and functions of animal communities” (RA2) mostly focus on plant diversity effects on the assembly of consumer communities and subsequent feedback effects on plant and consumer communities and ecosystem functions. Resulting biotic interactions drive the expression of growth and defense traits, as well as micro-evolutionary processes. Thus, subprojects under “Mediators of plant-biotic interactions” (RA3) and “Intraspecific diversity and micro-evolutionary changes” (RA4) mostly focus on plant diversity effects on plant trait expression and micro-evolutionary adaptation, how this is fueled by phenotypic plasticity, genetic and/or epigenetic differentiation, and how this influences ecosystem functions. In RA1, the assembly of plant and soil microbiomes will be explored because of their crucial role as part of the plant’s extended phenotype (Schnitzer et al. 2011, Laforest-Lapointe et al. 2017, Schmid et al. 2019). In RA2, taking a multitrophic perspective on BEF (Hines et al. 2015, Soliveres et al. 2016, Barnes et al. 2018), above- and belowground animal community assembly and activity patterns (Eisenhauer et al. 2018a) as well as their feedback effects on plants and ecosystem functions will be studied. In RA3, the mechanisms behind plant responses to and effects on biotic interactions and complex food webs will be studied by focusing on plant growth and defense traits and the chemical signaling with interaction partners above and below the ground with their knock-on effects on higher trophic levels. In RA4, trait changes, micro-evolutionary adaptation, and population genetics will be investigated by studying the intraspecific diversity of plant communities. As a consortium, we will thus be able to study the assembly of above-belowground communities and subsequent feedback effects, as well as plant trait expression and micro-evolutionary processes. Notably, these two main categories are closely linked as plastic micro-evolutionary responses of plants are supposed to be strongly influenced by above-belowground community assembly and their feedback effects, and vice versa (Fig. 1). These conceptual links are exemplified by the many collaborations of subprojects across categories and research fields (Fig. 2).

Figure 2.  

Structure of the proposed Research Unit. Three complementary experimental approaches are envisaged to study long-term biodiversity-ecosystem function (BEF) relationships, and how these are influenced by plant history and soil history. BEF patterns are studied in the Field Experiment with long-term plant diversity plots and manipulations of soil-history effects. BEF mechanisms are studied in the Ecotron Experiment and in Microcosm Experiments. In the Ecotron Experiment, plant history and soil history are independently crossed and detailed process measurements are possible. The Microcosm Experiments zoom in on focal interactions. In the Field Experiment and in the Ecotron Experiment, studies are conducted at the community level as well as at the plant individual level (magnifier; see detailed design of studies in the Appendices). Subprojects’ (SPs’) participation in experiments are illustrated with lines. The SPs of the proposed Research Unit fall into two tightly linked main categories (in gray) with two research areas each that aim at exploring variation in community assembly processes, micro-evolutionary changes, and resulting differences in biotic interactions as determinants of the long-term BEF relationship. Subprojects under “Microbial community assembly” (blue) and “Assembly and functions of animal communities” (red) mostly focus on plant diversity effects on the assembly of communities and their feedback effects on biotic interactions and ecosystem functions, while subprojects under “Mediators of plant-biotic interactions” (orange) and “Intraspecific diversity and micro-evolutionary changes” (green) mostly focus on plant diversity effects on plant trait expression and micro-evolution. PIs with requested personnel are underlined.

All of the proposed subprojects will utilize common experimental setups that explore the eco-evolutionary history of plant and soil communities. Community-level studies will explore BEF relationships as affected by plant history and/or soil history. Plant history refers to the abiotic and biotic selection pressures that plants have experienced in their respective communities since the start of the Jena Experiment, while soil history encompasses abiotic and biotic soil properties that have emerged from plant-soil interactions (Bever 2003, Schmid et al. 2019). Plant individual-specific studies will advance the mechanistic understanding of community-level responses and processes by exploring plants’ investments into growth and/or defense, interactions with microorganisms and animals above and below the ground, and how plant diversity-induced alterations in genetic diversity and trait expression change the performance of the plants and the interactions with their abiotic and biotic environment.

Novel tools to study temporal changes in biotic interactions and BEF effects

The exploration of biotic interactions within and across trophic levels is one key research frontier to mechanistically understand BEF relationships (Ives et al. 2005, Thébault and Loreau 2006, Thompson et al. 2012, Hines et al. 2015, Barnes et al. 2018). Although this research direction has been advocated for more than a decade, it is only now that we have the appropriate tools in hand to explore biotic interactions in more complexity. Recent progress in molecular and proximal sensing techniques now allow scientists to identify and quantify the microbial players in plants’ aboveground-belowground interactions (e.g., Laforest-Lapointe et al. 2017, Schmid et al. 2019) as well as to explore the temporal dynamics of biotic interactions (e.g., Dell et al. 2014, Eisenhauer et al. 2018a, Schuldt et al. 2019). At the same time, molecular sequencing techniques have been refined, such as cost-effective exploration and comparative analysis of DNA methylation and genetic variation in hundreds of samples de novo (van Gurp et al. 2016), and network analyses have emerged as tools to identify hub taxa and community-wide shifts in plant-microbe interactions (e.g., Morriën et al. 2017) as well as energy fluxes through food webs (Schwarz et al. 2017, Barnes et al. 2018). These novel methods allow us to characterize plant history and soil history effects on aboveground-belowground interactions, phenotypic and molecular adaptations (Berg and Coop 2014), and the distribution and maintenance of standing genetic variation (Vellend et al. 2014). Furthermore, we are now able to explore the chemical communication of plants above- and belowground determining interactions with mutualists and antagonists (van Dam and Bouwmeester 2016).

Notably, addressing the main objectives of the proposed Research Unit with these novel techniques requires a stepwise approach. In the proposed first phase of the Research Unit, we plan to build on recently established (Field Experiment; see below) and envisaged experiments (Ecotron Experiment and Microcosm Experiments; see below and individual SP’s proposals, respectively) to study the effects of plant history and soil history on BEF relationships and to separate those from potentially confounding climate effects. These experiments have sophisticated designs and provide the unique framework to describe microbial and animal community assembly patterns, morphological and chemical mediators of plant-biotic interactions, intraspecific plant diversity and micro-evolutionary changes, as well as the linkages to ecosystem functioning. Many novel tools will for the first time be employed in a BEF context and will thus contribute to describing new BEF patterns and develop hypotheses inspiring future experimental work that will build the basis for the second phase of the proposed Research Unit. For instance, the detailed investigation of microbial communities, comprising plant antagonists and mutualists, is an important first step to identify and cultivate potential key taxa that may then be manipulated in future experiments in the second phase. Similarly, the identification of important chemical traits and signals in the first phase of the Research Unit could allow us testing their role in biotic interactions and BEF relationships by targeted manipulations and/or lab experiments. The exploration of energy fluxes through food webs may enable us to detect key nodes that could be manipulated in subsequent experiments. Moreover, the discovery of key biological activity periods may guide the timing of future sampling campaigns. Taken together, we see the proposed research in the first phase of the Research Units as the prerequisite for future mechanistic studies, an approach that is already exemplified by the Microcosm Experiments.

Complementary expertise facilitates the “Research Unit’s functioning”

The previous Research Units in the framework of the Jena Experiment have had a unique role in BEF research by exploring whole-ecosystem responses to changes in biodiversity. Thus, the Jena Experiment is internationally widely known and respected as a key pillar in BEF research as well as one of the few running long-term biodiversity experiments in grassland. The proposed Research Unit will build on the unique strengths of the Jena Experiment, yet taking a novel approach in studying BEF relationships. The interdisciplinary approach (collaboration between animal ecologists, biochemists, plant ecologists, soil ecologists, soil microbiologists, evolutionary ecologists, and food web modelers) is highly innovative and world-leading. In order to address some of the most pressing challenges in BEF research, novel experimental, theoretical, and analytical approaches, expertise, and a completely realigned group of PIs is necessary. The consortium for the proposed Research Unit comprises scientists that were already involved in earlier phases of the Jena Experiment and many new ones that were selected in the past years to bring new expertise into the group, in particular in chemical ecology, soil microbiology, proximate sensing, evolutionary ecology, and ecological modeling. A particular strength of the consortium is a very close cooperation among the different subprojects (Fig. 2). This collaboration is indicated by collaborative work in the two main experiments, complementary analyses on the same plant individuals, and joint sampling campaigns. The proposed Research Unit includes scientists and collaborators from various universities and research institutes in Germany and Switzerland. German participation includes the universities of Göttingen, Halle, Jena, Köln, Leipzig, Frankfurt, TU and LMU Munich, the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, the Max Planck Institutes for Biogeochemistry and Chemical Ecology (both in Jena), as well as the Helmholtz-Centres for Environmental Research in Halle/Leipzig and for Health and Environment Munich, and we propose to strengthen this team through close collaborations with Mercator Fellows (Prof. Dr. Jeannine Cavender-Bares, Prof. Dr. Forest Isbell, Prof. Dr. Liesje Mommer, Prof Dr. Kevin Mueller) that will complement our expertise and connect us with international scientists and experimental infrastructures.

Joint work programme including proposed research methods

Cutting-edge techniques meet novel experimental approaches

We propose to use a set of three complementary experimental approaches (see Table 1 for the core experimental infrastructures) to advance the mechanistic understanding of BEF relationships by focusing on trait variation and biotic interaction variation caused by multitrophic community assembly as well as eco-evolutionary feedbacks as determinants of long-term plant diversity effects on ecosystem functioning (Fig. 1). While the Field Experiment allows to test important patterns in BEF relationships and the role of soil history, the Ecotron Experiment and Microcosm Experiments enable zooming in on the underlying mechanisms and to study effects of plant history and soil history (Fig. 2). The unifying rationale of the planned Research Unit is that plant interactions and interactions of plants with higher trophic levels (including microorganisms and animals) determine phenotypic plasticity and micro-evolutionary processes that together trigger ecosystem functioning. The planned Research Unit will embrace this plasticity of traits and their multitrophic interaction environment as well as their long-term evolutionary changes. In all experimental approaches, studying plant and soil eco-evolutionary history effects and their interactions will be the main ingredients to better understand why diverse plant communities function better than low-diversity plant communities and why this difference increases over time (Reich et al. 2012, Guerrero-Ramírez et al. 2017).

Table 1. Download as CSV 

Unique features of the Field Experiment and the Ecotron Experiment that will build the core experimental infrastructures of the proposed Research Unit. The complementary Microcosm Experiments are explained in the respective subprojects’ proposals (not shown here).

Field Experiment	Ecotron Experiment
• Study of biodiversity-ecosystem function patterns	• Study of biodiversity-ecosystem function mechanisms
• Long-term soil history effects (17 years)	• Orthogonal cross of soil history and plant history treatments
• Random species compositions for species-independent conclusions	• Possibility to study species-specific effects and two-species interactions along the plant diversity gradient
• Realistic field conditions and separation of community age from time effects	• Controlled environmental conditions for detailed process and behavioral measurements
• Age-structured communities	• Plant individuals of the same age/development stage
• Plant diversity levels: 1, 2, 4, 8, 16, 60	• Plant diversity levels: 1, 2, 3, 6
• Plant species richness and plant functional group effects	• Plant species richness and dissimilarity effects in temporal resoruce use
• Large, undisturbed plots allowing for repeated measurements of many subprojects and the continuation of unique time series	• Intact soil monoliths in lysimeters with the respective soil communities that can be destructively harvested
• Biodiversity-induced variations in plant density	• Equal plant densities across plant diversity levels and limited weeding effects

In the Field Experiment (for hypotheses see Fig. 3; Vogel et al. 2019; Suppl. materials 1, 2) long-term soil history effects can be studied under field conditions, where random combinations of plant species from a large species pool (Table 1; Suppl. material 3) form the longest running plant diversity gradient in the world (Lefcheck et al. 2015). In the iDiv Ecotron (Ecotron Experiment; Suppl. materials 4, 5), intact soil monoliths can be studied, environmental conditions and plant density can be controlled, plants with different community histories (i.e., community-selected plants) can be crossed with soils that have different histories, and individual plant species that differ in temporal resource use traits can be followed through the diversity gradient (Table 1). In the Ecotron Experiment (Fig. 4; Suppl. material 4), plant communities are proposed to be planted in equal densities, and weeding disturbances will not co-vary with the plant diversity gradient, addressing some concerns expressed regarding BEF studies in grasslands (Weisser et al. 2017). The controlled Ecotron environment will allow to study species interactions and perform sophisticated process measurements that currently are impossible under field conditions. Further Microcosm Experiments will focus on isolating mechanisms underlying focal interactions. While all planned subprojects will work in the Field Experiment and Ecotron Experiment, allowing for collaborations and synergies among subprojects, Microcosm Experiments will have more subproject-specific foci (Fig. 2). Common phytometer species and plant species-specific analyses will further link the research activities of all subprojects across experimental set-ups (Fig. 2).

Figure 3.  

Hypothesized slope of BEF relationships in the different treatments of the Field Experiment (see main text for details). Note that the ‘with plant history, with soil history’ only serves as a control in the Field Experiment, and effects of plant history can only be tested in the planned Ecotron Experiment. Redrawn after Vogel et al. (2019). ‘+’, with; ‘-‘, without.

Figure 4.  

Experimental design and hypotheses of the Ecotron Experiment. Briefly, four treatments will be established based on monoliths from a selection of the 9-year old Trait-Based Experiment (TBE; Ebeling et al. 2014) and from bare ground plots of the Jena Experiment as well as two seed sources: the respective plots and the original seed material that was used for the set-up of the TBE. (1) With plot-specific plant history and with plot-specific soil history; (2) without plot-specific plant history and with plot-specific soil history; (3) with plot-specific plant history and without plot-specific soil history; and (4) without plot-specific plant history and without plot-specific soil history. We expect the biodiversity–ecosystem function relationships to differ among the four treatments (see main text for details).

The Field Experiment – objectives and hypotheses

Studies on changes in biodiversity effects with community age (years since the start of the experiment) all have the problem that time (calendar year) is confounded with age. The Field Experiment (established in 2016 in preparation of this proposal; for design see Suppl. material 1; for one-page summary [“Cheat Sheet”], see Suppl. material 2) for the first time allows to compare communities of different ages at the same point in time. We set up the same communities in 2016 as we had set up in 2002 and can now observe them at ages 5 and 19 in 2020, 6 and 20 in 2021, and so on. To make the comparison, the communities of the same species compositions but different ages are located on the same plots. The ‘with plant history, with soil history’ treatment is represented by the undisturbed soil and plant communities, which have been maintained since 2002 (Roscher et al. 2004). We also established a ‘without plant history, without soil history’ treatment in order to replicate the soil situation as in 2002. Therefore, we used soil from a nearby agricultural crop field (no plant and no soil history from the old experiment; very similar to the conditions before the Jena Experiment was sown on a former agricultural field in 2002). In addition, we set up a treatment where the soil of the old experimental plot was broken up and mixed before sowing the new experiment with new seed material (‘without plant history, with soil history’). The setup of this new experiment on the plots of the Main Experiment is a first significant step towards separating environmental correlates of time (such as climatic trends) from community age effects caused by plant–soil eco-evolutionary dynamics (Schnitzer et al. 2011, Eisenhauer et al. 2012a, Zuppinger-Dingley et al. 2014, Roscher et al. 2015, van Moorsel et al. 2018, Schmid et al. 2019). This allows us to experimentally explore community-age effects, such as eco-evolutionary soil history effects (plant community-specific soil history) and eco-evolutionary niche differentiation (plant community-specific plant history), on the strength of biodiversity effects independently of confounding temporal trends under the same climate conditions. In addition to the community-level analyses, we will employ a phytometer approach and plant species-specific assessments to study plant-specific eco-evolutionary responses to the experimental treatments in a standardized way and in concerted actions (Suppl. material 1).

According to the proposed mechanisms underlying strengthening BEF relationships in time (Eisenhauer et al. 2012a, Zuppinger-Dingley et al. 2014, Meyer et al. 2016), we expect the slope of the BEF relationship to differ among the treatments of the Field Experiment (Fig. 3): we hypothesize a steeper and more significant BEF relationship in the treatment ‘with plant history, with soil history’ than in the treatment ‘without plant history, with soil history’, because of increased niche differentiation in plants with eco-evolutionary history of coexistence. This means that low-diversity communities in the “with plant history, with soil history” treatment should perform worst in comparison to all other treatments, e.g., due to the accumulation of plant antagonists and nutrient limitation (due to one-sided nutrient use); and the high-diversity communities in this treatment should perform best, e.g., due to resource use complementarity and an accumulation of plant growth facilitators. The treatment ‘without plant history, without soil history’ is predicted to have the shallowest BEF slope, because of lower niche differentiation in plant mixtures and missing plant community-specific soil effects (Fig. 3).

Preliminary results from the Field Experiment provide support for the prediction of a steeper slope in the ‘with plant history, with soil history’ treatment for absolute and relative plant biomass production (Vogel et al. 2019). Moreover, soil nematode community composition and soil microbial functioning (carbon use efficiency) differed substantially among the experimental treatments (Vogel et al. 2019). Thus, already one year after establishment of the experiment, the BEF slopes of the treatments ‘without plant history, without soil history’ and ‘without plant history, with soil history’ differed significantly, suggesting that soil and plant history are both important, and motivating the complementary Ecotron Experiment (see below). This proposal for a new Research Unit will allow us to assess whether the effects consolidate and allows to probe the relevant mechanistic processes. Notably, the ‘with plant history, with soil history’ treatment can only serve as a reference in the Field Experiment, because the respective plots were not disturbed like in the other treatments, and because the plant history treatment cannot be studied independent of the soil history treatment. Thus, plant history versus soil history effects can only be studied in the planned Ecotron Experiment.

Since the establishment of the Field Experiment has already been successfully accomplished in preparation of this proposal, there are no establishment risks, and the new research questions can be addressed immediately . The Field Experiment provides the ideal infrastructure for large collaborative initiatives on the mechanisms underlying BEF relationships (Fig. 2) and allows testing our overarching hypothesis as well as SP-specific hypotheses (see individual SP proposals).

The Ecotron Experiment – objectives and hypotheses

The comprehensive study of plant history and soil history effects requires complementary approaches, e.g., for testing general relationships under field conditions (large species pool and random community mixtures in the Field Experiment), as well as more specific process and interaction assessments in highly-controlled setups (species- and interaction-specific effects and responses). The planned Ecotron Experiment allows us to do this along a well-established plant diversity gradient (for details on the design, see Suppl. material 4; for one-page summary [“Cheat Sheet”], see Suppl. material 5). It thus builds on the strengths of the Jena Experiment, while complementing the Field Experiment in several important aspects. While the Field Experiment and the Ecotron Experiment share the objectives provided above on the mechanisms of increasing BEF relationships over time, the unique objectives of the Ecotron Experiment are to (1) orthogonally separate plant history from soil history effects, (2) study plant species- and interaction-specific effects at all diversity levels, and (3) study the mechanisms underlying BEF relationships via sophisticated process measurements (see Table 1 for differences between the Field Experiment and the Ecotron Experiment). Thus, many SPs complement the assessments they also perform in the Field Experiment (mentioned above and in more detail in the SPs’ proposals) with more detailed analyses of certain processes and interactions in the Ecotron Experiment.

We expect the steepest BEF slope in the treatment ‘with plant history, with soil history’ (green, solid line in Fig. 4) due to increased plant complementarity at the high plant diversity (Fig. 1; van Moorsel et al. 2018) and specific plant-soil feedback effects (more detrimental ones at low plant diversity and more beneficial ones at high plant diversity; Eisenhauer et al. 2012a). In the treatment ‘without plant history, with soil history’, we expect generally lower levels of ecosystem functioning, as plants may be less well protected against plant antagonists at low plant diversity and may have higher levels of niche overlap at high plant diversity (Fig. 1; green, dashed line in Fig. 4). In the treatment ‘without plant history, without soil history’, we expect to find the shallowest BEF relationship (brown, solid line). While we hypothesize lower densities of plant-specific antagonists in the soil in this treatment (which is why EF might be higher than in the treatments with plot-specific soil history), plants at high plant diversity have not been selected towards elevated resource use complementarity (Fig. 1). Finally, we hypothesize slightly steeper BEF slopes in the treatment ‘with plant history, without soil history’ (brown, dashed line), because the selection of plants towards increased defense (Fig. 1) may not be of benefit in a soil with low pathogen pressure (plant growth-defense trade-off). At high plant diversity, however, ecosystem functioning might be higher because of reduced niche overlap (Fig. 1).

Anticipated total duration of the project

Research data and knowledge management

Database and international collaboration

Other information

Description of how joint objectives and the joint work programme will be implemented in the coordination project

As outlined above, the described scientific objectives will be achieved via a plethora of communication and interaction channels that have proven successful in facilitating integrative BEF research. Regular meetings (Jena Retreats) provide the basis for mutual trust and collaboration. We will use multiple communication channels to guarantee the highest level of transparency, including regular email updates, webpage, Twitter, and Google Scholar accounts, a common database, a clear data use policy, and a common project- and paper proposal system. These means as well as central coordination of experimental setups and sampling campaigns will be strongly supported by SP Z1 (see SP Z1 proposal). Accordingly, the spokesperson has made sure that all research plans proposed in this Research Unit are highly complementary and all contribute to the common goal to study biotic interactions, community assembly, and eco-evolutionary dynamics as drivers of long-term biodiversity–ecosystem functioning relationships.

Requested modules

Coordination module

As outlined above, there are multiple needs of the Research Unit that require a central and flexible budget. For instance, in the past funds from the Coordination Module were used to cover unforeseen repair or replacement of infrastructure and central equipment, additional workshops and analyses in exceptional circumstances, such as extreme climate events (e.g., Wright et al. 2015), and additional management and measurement campaigns, including repeated or additional measurements. A total of EUR 40,000.00 coordination funds are requested (standard rate of EUR 10,000.00 per year).

Total sum of requested funds in ‘Coordination Module’: EUR 40,000.00

Network Funds Module (Funding for Staff, Direct Project Costs and Instrumentation)

Notably, substantial financial support by the contributing institutions, particularly of the FSU Jena (funding the Scientific Coordinator, a technician, and gardeners) facilitates the scientific network. In addition to the database infrastructure support provided by iDiv, we request a data curator (50% E13), who will be responsible for data quality control and scientific computation help for PhD students, compliance with reproducible science principles, post-processing meta-data, Jena Experiment homepage, data policy implementation and checking, supervision of data transfer within and beyond the Research Unit, long-term time-series updates and publication, and preparation of synthesis datasets.

Gender Equality Measures in Research Networks Module

Similar to the previous phases of the Jena Experiment, the proportion of female PIs is relatively high (~35%), surpassing the proportion of female professors at German universities by far (~20% in 2015). Female researchers are involved in all proposed SPs, either as PIs or as key contributors, which shows that female researchers are well integrated into the network and also hold leading positions, e.g., as PIs in the Central Coordination (SPZ). Notably, the careers of several female researchers have benefited from the Jena Experiment as a Research Unit in the past. They now hold professorships or permanent positions at various universities or research institutes. In the last Research Unit, the proportion of female researchers was ~42% among postdocs and ~69% among PhD candidates. Obtaining a PhD is a critical phase in a scientific career towards a professorship as females often wish to start a family. If they do not receive any help to balance their time-consuming academic work when having their first child, and in addition receive support to explore future career options, they often drop out of science. With the proposed large group of young female scientists and more experienced PIs – with kids – there is great potential for role model interactions that will show that it is possible to combine career and family, also as a female scientist. In the proposed Research Unit, we explicitly aim to engage specific tools to support young female researchers to build up a successful academic career.

During the past 17 years, we have gained experience with three important means to support female researchers (requested funds: EUR 60,000.00; Coordination; EUR 15,000.00 per year). First, we organized yearly scientific workshops only for the female researchers of the Research Unit. The female scientists attending rated those workshops as very important as they were organized particularly to meet their needs (e.g., time for data analysis and writing and discussions in female-only groups, professional training in specific statistical analyses with female trainers and experts, and organized child care during the workshop). The workshops have been extremely successful with several publications being initiated and written up and new projects developed with females as leading PIs. For these reasons, we plan to continue with those yearly workshops in the period as specified in the current proposal. The second important means is flexible support. The career-limiting issues that female researchers may experience due to pregnancy, maternity leave, and childcare duties, are very individual. These can only be addressed by having a flexible support system. For instance, some female researchers needed some family-friendly support, such as child-care during workshops, conferences, or school holidays. We will further support female researchers during pregnancy and maternity leave by, e.g., equipping home offices or giving field assistance by student helpers. We would like to keep this flexibility to provide individual support. Third, another measure that has been proven successful to empower females striving for a career in science, is the provision of mentoring programs to promote leadership qualities, improve work-life balance, or to support applications and interviews for professorships. We will set up mentoring groups, where peers support each other in an organized manner. Each year, female scientists in the group will be asked to specify which type of course or activity would be the most appropriate. Moreover, the more advanced female PIs will be asked to give role model talks, e.g., during lunch at Jena Retreats.

Total sum of requested funds in ‘Gender Equality Measures’: EUR 60,000.00

Project-Specific Workshop Module

We are planning to organize at least one synthesis workshop that brings together data from multiple experiments across ecosystems to study long-term BEF relationships and their context-dependency and to foster international collaboration and networking. This workshop will facilitate the synthesis work of the requested plant postdoc in SPZ (WP6) and will help consolidating the Jena Experiment as a global leader in BEF synthesis. We are not requesting any money in this proposal, but will apply to sDiv workshop funds or use coordination funds (Coordination Module).

Mercator Fellow Module

To foster scientific exchange with international colleagues and add complementary expertise to the consortium, we plan to invite four Mercator fellows with expertise in belowground plant-plant- and plant-fungal interactions (Dr. Liesje Mommer), soil biogeochemistry and element cycling (Dr. Kevin Mueller), data synthesis and strong link to long-term biodiversity experiments in Cedar Creek (Dr. Forest Isbell), and plant physiology and plant eco-evolutionary dynamics (Dr. Jeannine Cavender-Bares). For each of these international collaborators, we calculated with a four-week stay in Jena or Leipzig that can also be split into multiple visits. For each Mercator Fellow, we calculated with the monthly DFG standard salary for professors (EUR 8,675.00) and travel costs of EUR 2,500.00 per fellow. However, we are requesting money for only two of the four Mercator Fellows in this proposal and will apply to sDiv sabbatical funds and/or use coordination funds (Coordination Module).

Total sum of requested funds in ‘Mercator Fellow Module’: EUR 22,350.00

Public Relations Module

The efficient communication of scientific findings to the public and policy makers is essential for the broad appreciation of the consequences of biodiversity change. During the last years, there has been increasing interest in the research of the Jena Experiment by the public (e.g., at the yearly Open Day; requested funds: EUR 5,000.00) as well as print, radio, and TV press, also facilitated by the outstanding work of iDiv’s press office (>100 media coverages; reaching >15 million people between November 2014 and April 2019). During the running funding period, we regularly offered information for press releases and institutional newsletters. An exceptionally successful tool to communicate the rationale and results of the Jena Experiment is the new image movie that is available in English and German. Moreover, the Jena Experiment now has its own Twitter, and Google Scholar accounts. In the requested Research Unit, we plan to represent the Jena Experiment at important local public relations events, such as the MINT exhibition in Jena and the Long Night of Sciences in Leipzig. The Jena Experiment also serves as a teaching platform. We gave regular excursions for groups from the University of Bayreuth (course “Monitoring and Experiments in Ecology”), FSU Jena (“Ecological Excursion”, “Field Practical”), University of Koblenz, University of Bonn (module “Biodiversity and Ecosystem Functions”), the graduate school of iDiv (yDiv), the summer school of iDiv, and the graduate school of the MPIs (summer school IMPRS). We propose to follow up this active role in public relations and teaching in the proposed Research Unit and feel encouraged that the relevance of the results of the Jena Experiment is widely appreciated, such as exemplified by the recent speech at the iDiv Ecotron inauguration by Karl Eugen Huthmacher, Department Head at the German Federal Ministry of Education and Research (BMBF), who stated that “…biodiversity change is at least as important as climate change for humans”. Moreover, a new, up-to-date homepage is needed that will be developed with support from the FSU Jena.

Total sum of requested funds in ‘Public Relations Module’: EUR 5,000.00

Employment status information

First-time proposal data

Composition of the project group

Cooperation with other researchers

Scientific equipment

Overall budget and requested personnel

We thank the eight reviewers for their very helpful feedback on our research plan and the positive evaluation. We thank the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation) for financial support (FOR 456, FOR 1451, FOR 5000) as well as the Friedrich-Schiller-University Jena, Max-Planck-Institute for Biogeochemistry Jena, Leipzig University, and the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, funded by the German Research Foundation (FZT 118), for financial and logistical help with the set-up and maintenance of the Jena Experiment. We also thank the gardeners for their great help maintaining the experimental plots and Ernst-Detlef Schulze for initiating the Jena Experiment. Moreover, we thank Anja Vogel for coordinating the setup of the Field Experiment as well as Kathrin Greyer and Svenja Haenzel for her help preparing this proposal and the on-site evaluation.

Research Unit (Forschungsgruppe)

The authors have declared that no competing interests exist.