Maarten B. Eppinga

Empirical and theoretical challenges in aboveground–belowground ecology

A growing body of evidence shows that aboveground and belowground communities and processes are intrinsically linked, and that feedbacks between these subsystems have important implications for community structure and ecosystem functioning. Almost all studies on this topic have been carried out from an empirical perspective and in specific ecological settings or contexts. Belowground interactions operate at different spatial and temporal scales. Due to the relatively low mobility and high survival of organisms in the soil, plants have longer lasting legacy effects belowground than aboveground. Our current challenge is to understand how aboveground–belowground biotic interactions operate across spatial and temporal scales, and how they depend on, as well as influence, the abiotic environment. Because empirical capacities are too limited to explore all possible combinations of interactions and environmental settings, we explore where and how they can be supported by theoretical approaches to develop testable predictions and to generalise empirical results. We review four key areas where a combined aboveground–belowground approach offers perspectives for enhancing ecological understanding, namely succession, agro-ecosystems, biological invasions and global change impacts on ecosystems. In plant succession, differences in scales between aboveground and belowground biota, as well as between species interactions and ecosystem processes, have important implications for the rate and direction of community change. Aboveground as well as belowground interactions either enhance or reduce rates of plant species replacement. Moreover, the outcomes of the interactions depend on abiotic conditions and plant life history characteristics, which may vary with successional position. We exemplify where translation of the current conceptual succession models into more predictive models can help targeting empirical studies and generalising their results. Then, we discuss how understanding succession may help to enhance managing arable crops, grasslands and invasive plants, as well as provide insights into the effects of global change on community re-organisation and ecosystem processes.

Nutrients and hydrology indicate the driving mechanisms of peatland surface patterning.

Peatland surface patterning motivates studies that identify underlying structuring mechanisms. Theoretical studies so far suggest that different mechanisms may drive similar types of patterning. The long time span associated with peatland surface pattern formation, however, limits possibilities for empirically testing model predictions by field manipulations. Here, we present a model that describes spatial interactions between vegetation, nutrients, hydrology, and peat. We used this model to study pattern formation as driven by three different mechanisms: peat accumulation, water ponding, and nutrient accumulation. By on‐and‐off switching of each mechanism, we created a full‐factorial design to see how these mechanisms affected surface patterning (pattern of vegetation and peat height) and underlying patterns in nutrients and hydrology. Results revealed that different combinations of structuring mechanisms lead to similar types of peatland surface patterning but contrasting underlying patterns in nutrients and hydrology. These contrasting underlying patterns suggest that the presence or absence of the structuring mechanisms can be identified by relatively simple short‐term field measurements of nutrients and hydrology, meaning that longer‐term field manipulations can be circumvented. Therefore, this study provides promising avenues for future empirical studies on peatland patterning.

Regular Surface Patterning of Peatlands: Confronting Theory with Field Data

Regular spatial patterns of sharply bounded ridges and hollows are frequently observed in peatlands and ask for an explanation in terms of underlying structuring processes. Simulation models suggest that spatial regularity of peatland patterns could be driven by an evapotranspiration-induced scale-dependent feedback (locally positive, longer-range negative) between ridge vegetation and nutrient availability. The sharp boundaries between ridges and hollows could be induced by a positive feedback between net rate of peat formation and acrotelm thickness. Theory also predicts how scale-dependent and positive feedbacks drive underlying patterns in nutrients, hydrology, and hydrochemistry, but these predictions have not yet been tested empirically. The aim of this study was to provide an empirical test for the theoretical predictions; therefore, we measured underlying patterns in nutrients, hydrology, and hydrochemistry across a maze-patterned peatland in the Great Vasyugan Bog, Siberia. The field data corroborated predicted patterns as induced by scale-dependent feedback; nutrient concentrations were higher on ridges than in hollows. Moreover, diurnal dynamics in water table level clearly corresponded to evapotranspiration and showed that water levels in two ridges were lower than in the hollow in between. Also, the data on hydrochemistry suggested that evapotranspiration rates were higher on ridges. The bimodal frequency distribution in acrotelm thickness indicated sharp boundaries between ridges and hollows, supporting the occurrence of a positive feedback. Moreover, nutrient content in plant tissue was most strongly associated with acrotelm thickness, supporting the view that positive feedback further amplifies ridge–hollow differences in nutrient status. Our measurements are consistent with the hypothesis that the combination of scale-dependent and positive feedback induces peatland patterning.

Linking habitat modification to catastrophic shifts and vegetation patterns in bogs

Paleoecological studies indicate that peatland ecosystems may exhibit bistability. This would mean that these systems are resilient to gradual changes in climate, until environmental thresholds are passed. Then, ecosystem stability is lost and rapid shifts in surface and vegetation structure at landscape scale occur. Another remarkable feature is the commonly observed self-organized spatial vegetation patterning, such as string-flark and maze patterns. Bistability and spatial self-organization may be mechanistically linked, the crucial mechanism being scale-dependent (locally positive and longer-range negative) feedback between vegetation and the peatland environment. Focusing on bogs, a previous model study shows that nutrient accumulation by vascular plants can induce such scale-dependent feedback driving pattern formation. However, stability of bog microforms such as hummocks and hollows has been attributed to different local interactions between Sphagnum, vascular plants, and the bog environment. Here we analyze both local and longer-range interactions in bogs to investigate the possible contribution of these different interactions to vegetation patterning and stability. This is done by a literature review, and subsequently these findings are incorporated in the original model. When Sphagnum and encompassing local interactions are included in this model, the boundaries between vegetation types become sharper and also the parameter region of bistability drastically increases. These results imply that vegetation patterning and stability of bogs could be synergistically governed by local and longer-range interactions. Studying the relative effect of these interactions is therefore suggested to be an important component of future predictions on the response of peatland ecosystems to climatic changes.

A critical transition in leaf evolution facilitated the Cretaceous angiosperm revolution

The revolutionary rise of broad-leaved (flowering) angiosperm plant species during the Cretaceous initiated a global ecological transformation towards modern biodiversity. Still, the mechanisms involved in this angiosperm radiation remain enigmatic. Here we show that the period of rapid angiosperm evolution initiated after the leaf interior (post venous) transport path length for water was reduced beyond the leaf interior transport path length for CO2 at a critical leaf vein density of 2.5–5 mm mm−2. Data and our modelling approaches indicate that surpassing this critical vein density was a pivotal moment in leaf evolution that enabled evolving angiosperms to profit from developing leaves with more and smaller stomata in terms of higher carbon returns from equal water loss. Surpassing the critical vein density may therefore have facilitated evolving angiosperms to develop leaves with higher gas exchange capacities required to adapt to the Cretaceous CO2 decline and outcompete previously dominant coniferous species in the upper canopy.

Spatial Self-Organization on Intertidal Mudflats through Biophysical Stress Divergence

In this study, we investigated the emergence of spatial self‐organized patterns on intertidal flats, resulting from the interaction between biological and geomorphological processes. Autocorrelation analysis of aerial photographs revealed that diatoms occur in regularly spaced patterns consisting of elevated hummocks alternating with water‐filled hollows. Hummocks were characterized by high diatom content and a high sediment erosion threshold, while both were low in hollows. These results highlight the interaction between diatom growth and sedimentary processes as a potential mechanism for spatial patterning. Several alternative mechanisms could be excluded as important mechanisms in the formation of spatial patterns. We developed a spatially explicit mathematical model that revealed that scale‐dependent interactions between sedimentation, diatom growth, and water redistribution explain the observed patterns. The model predicts that areas exhibiting spatially self‐organized patterns have increased sediment accretion and diatom biomass compared with areas lacking spatial patterns, a prediction confirmed by empirical evidence. Our study on intertidal mudflats provides a simple but clear‐cut example of how the interaction between biological and sedimentary processes, through the process of self‐organization, induces spatial patterns at a landscape level.

Bistability and regular spatial patterns in arid ecosystems

A variety of patterns observed in ecosystems can be explained by resource–concentration mechanisms. A resource–concentration mechanism occurs when organisms increase the lateral flow of a resource toward them, leading to a local concentration of this resource and to its depletion from areas farther away. In resource–concentration systems, it has been proposed that certain spatial patterns could indicate proximity to discontinuous transitions where an ecosystem abruptly shifts from one stable state to another. Here, we test this hypothesis using a model of vegetation dynamics in arid ecosystems. In this model, a resource–concentration mechanism drives a positive feedback between vegetation and soil water availability. We derived the conditions leading to bistability and pattern formation. Our analysis revealed that bistability and regular pattern formation are linked in our model. This means that, when regular vegetation patterns occur, they indicate that the system is along a discontinuous transition to desertification. Yet, in real systems, only observing regular vegetation patterns without identifying the pattern-driving mechanism might not be enough to conclude that an ecosystem is along a discontinuous transition because similar patterns can emerge from different ecological mechanisms.

Exploratory modeling: Extracting causality from complexity

On 22 May 2011 a massive tornado tore through Joplin, Mo., killing 158 people. With winds blowing faster than 200 miles per hour, the tornado was the most deadly in the United States since modern record keeping began in the 1950s.

Resource contrast in patterned peatlands increases along a climatic gradient

Spatial patterning of ecosystems can be explained by several mechanisms. One approach to disentangling the influence of these mechanisms is to study a patterned ecosystem along a gradient of environmental conditions. This study focused on hummock-hollow patterning of peatlands. Previous models predicted that patterning in drainage-dominated peatlands is driven by a peat-accumulation mechanism, reflected by higher nutrient availability in hollows relative to hummocks. Alternatively, patterning in evapotranspiration (ET)-dominated peatlands may be driven by a nutrient-accumulation mechanism, reflected by reversed nutrient distribution, namely, higher nutrient availability in hummocks relative to hollows. Here, we tested these predictions by comparing nutrient distributions among patterned peatlands in maritime (Scotland), humid temperate (Sweden), and humid continental (Siberia) climates. The areas comprise a climatic gradient from very wet and drainage-dominated (Scotland) to less wet and ET-dominated (Siberia) peatlands. Nutrient distribution was quantified as resource contrast, a measure for hummock-hollow difference in nutrient availability. We tested the hypothesis that the climatic gradient shows a trend in the resource contrast; from negative (highest nutrient availability in hollows) in Scotland to positive (highest nutrient availability in hummocks) in Siberia. The resource contrasts as measured in vegetation indeed showed a trend along the climatic gradient: contrasts were negative to slightly positive in Scotland, positive in Sweden, and strongly positive in Siberia. This finding corroborates the main prediction of previous models. Our results, however, also provided indications for further model development. The low concentrations of nutrients in the water suggest that existing models could be improved by considering both the dissolved and adsorbed phase and explicit inclusion of both nutrient-uptake and nutrient-storage processes. Our study suggests that future climate change may affect the ecosystem functioning of patterned peatlands by altering the contribution of pattern-forming mechanisms to redistribution of water and nutrients within these systems.

Plant-soil feedbacks and the coexistence of competing plants

Plant–soil feedbacks can have important implications for the interactions among plants. Understanding these effects is a major challenge since it is inherently difficult to measure and manipulate highly diverse soil communities. Mathematical models may advance this understanding by making the interplay of the various processes affecting plant–soil interaction explicit and by quantifying the relative importance of the factors involved. The aim of this paper is to provide a complete analysis of a pioneering plant–soil feedback model developed by Bever and colleagues (J Ecol 85: 561–573, 1997; Ecol Lett 2: 52–62, 1999; New Phytol 157: 465–473, 2003) to fully understand the range of possible impacts of plant–soil feedbacks on plant communities within this framework. We analyze this model by means of a new graphical method that provides a complete classification of the potential effects of soil communities on plant competition. Due to the graphical character of the method, the results are relatively easy to obtain and understand. We show that plant diversity depends crucially on two key parameters that may be viewed as measures of the intensity of plant competition and the direction and strength of plant–soil feedback, respectively. Our analysis provides a formal underpinning of earlier claims that plant–soil feedbacks, especially when they are negative, may enhance the diversity of plant communities. In particular, negative plant–soil feedbacks can enhance the range of plant coexistence by inducing competitive oscillations. However, these oscillations can also destabilize plant coexistence, leading to low population densities and extinctions. In addition, positive feedbacks can allow locally stable forms of plant coexistence by inducing alternative stable states. Our findings highlight that the inclusion of plant–soil interactions may fundamentally alter the predictions on the structure and functioning of above-ground ecosystems. The scenarios presented in this study can be used to formulate hypotheses about the ways soil community effects may influence plant competition that can be tested with empirical studies. This will advance our understanding of the role of plant–soil feedback in ecological communities.