Centenary Symposium Special Feature: Paper Summaries

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Introduction Journal of Ecology was the first ecological journal in the world. It was established as the official publication of the newly formed British Ecological Society in 1913 under the leadership and guidance of the Society’s first President, Sir Arthur Tansley FRS (1871–1955). The pages of Journal of Ecology have hosted many of the most influential papers in plant ecology. In celebration of the Journal’s 100th anniversary, a Centenary Symposium was held during the British Ecological Society’s Annual Meeting in Sheffield, UK, in September 2011. A group of internationally-renowned researchers were invited to talk on topics in which the Journal has published major contributions over the last century, and in which significant progress is currently being made. The contributors to the Centenary Symposium produced written versions of their papers for publication in the Journal of Ecology’s Centenary Special Issue. The papers in this Centenary Symposium Special Feature cover a wide range of topics, so there is something to interest every reader. Some of the topics and ideas dealt with in this set of papers were not even remotely within Tansley’s sphere of thought when Journal of Ecology was being launched by the British Ecological Society in 1913. The Journal editors are confident that the ten papers presented in this Special Feature are significant contributions to the literature, and that they will be widely-read for many years to come

Editorial Tansley’s vision for Journal of Ecology, and a Centenary Celebration Michael J. Hutchings, David J. Gibson, Richard D. Bardgett, Mark Rees, Erika Newton, Andrea Baier & Lauren Sandhu

Root responses to nutrients and soil biota: drivers of species coexistence and ecosystem productivity de Kroon, Hans; Hendriks, Marloes; van Ruijven, Jasper; Ravenek, Janneke; Padilla, Francisco; Jongejans, Eelke; Visser, Eric; Mommer, Liesje Summary 1. Although a major part of plant biomass is underground, we know little about the contribution of different species to root biomass in multispecies communities. We summarize studies on root distributions and plant responses to species-specific soil biota, and formulate three hypotheses to explain how root responses may drive species coexistence and ecosystem productivity. 2. Recent studies suggest that root growth of some species may be stimulated in species mixtures compared to monocultures without hampering the growth of other species, leading to belowground overyielding. Further studies suggest that these responses are the result of reduced impairment of growth by species-specific plant pathogens that accumulate in monocultures. 3. First, we hypothesize that due to pathogen-constrained growth, monocultures are ‘underrooted’, i.e. they do not have enough roots for optimal acquisition of nutrients. Although elevated root production in mixtures represents a cost to the plant, improved nutrition will eventually result in improved plant performance. 4. Second, due to the plant species specificity of the soil biotic communities, we suggest that plant species in mixtures develop an intransitive competitive network in which none of the species is competitively superior to all other species. Competitive intransitivity is proposed as a mechanism of species coexistence. 5. As a final hypothesis we suggest that pathogen-mediated root overproduction in species mixtures determines patterns of community productivity and overyielding, both directly, by improving plant performance, and indirectly, by releasing more carbon into the soil, resulting in enhanced availability of nutrients. 6. Synthesis. Recent evidence suggests that species coexistence and ecosystem productivity may be the result of an interplay between pathogen-driven plant responses and nutritional consequences. We suggest that responses of the roots are an important yet mostly overlooked intermediary between soil biota and plant community responses to biodiversity.

Linking Vegetation Change, Carbon Sequestration and Biodiversity: Insights from Island Ecosystems in a Long-Term Natural Experiment Wardle, David; Jonsson, Micael; Bansal, Sheel; Bardgett, Richard; Gundale, Michael; Metcalfe, Daniel Summary 1. Despite recent interest in linkages between above- and below-ground communities and their consequences for ecosystem processes, much remains unknown about their responses to long-term ecosystem change. We synthesize multiple lines of evidence from a long-term ‘natural experiment’ to illustrate how ecosystem retrogression (the decline in ecosystem process rates due to long-term absence of major disturbance) drives vegetation change, and thus above-ground and below-ground carbon (C) sequestration, and communities of consumer biota. 2. Our study system involves 30 islands in Swedish boreal forest that form a 5000 year firedriven retrogressive chronosequence. Here, retrogression leads to lower plant productivity and slower decomposition, and a community shift from plants with traits associated with resource acquisition to those linked with resource conservation. 3. We present consistent evidence that above-ground ecosystem C sequestration declines, while below-ground and total C storage increases linearly for at least 5000 years following fire absence. This increase is driven primarily by changes in vegetation characteristics, impairment of decomposer organisms and absence of humus combustion. 4. Data from contrasting trophic groups show that during retrogression, biomass or abundance of plants and decomposer biota decreases, while that of above-ground invertebrates and birds increases, due to different organisms accessing resources via distinct energy channels. Meanwhile, diversity measures of vascular plants and above-ground (but not below-ground) consumers respond positively to retrogression. 5. We show that taxonomic richness of plants and above-ground consumers are positively correlated with total ecosystem C storage, suggesting that conserving old growth forests simultaneously maximizes biodiversity and C sequestration. However, we find little observational or experimental evidence that plant diversity is a major driver of ecosystem C storage on the islands relative to other biotic and abiotic factors. 6. Synthesis. Our study reveals that across contrasting islands differing in exposure to a key extrinsic driver (historical disturbance regime and resulting retrogression), there are coordinated responses of soil fertility, vegetation, consumer communities, and ecosystem C sequestration, which all feed back to one another. It also highlights the value of well replicated natural experiments for tackling questions about above-ground–below-ground linkages over temporal and spatial scales that are otherwise unachievable.

Ecosystem CO2 starvation and terrestrial silicate rock weathering: mechanisms and global-scale quantification during the late Miocene Beerling, David; Taylor, Lyla; Bradshaw, Catherine; Lunt, Dan; Valdes, Paul; Banwart, Steve; Pagani, Mark; Leake, Jonathan Summary 1. The relative constancy of the lower limit on Earth’s atmospheric CO2 concentration ([CO2]a) during major tectonic episodes over the final 24 million years of the Cenozoic is surprising because they are expected to draw-down [CO2]a by enhancing chemical weathering and carbonate deposition in the seafloor. That [CO2]a did not drop to extremely low values suggests the existence of feedback mechanisms that slow silicate weathering as [CO2]a declines. One proposed mechanism is a negative feedback mediated through CO2 starvation of land plants in active orogenic regions compromising the efficiency of the primary carboxylating enzyme in C3 plants (Rubisco) and diminishing productivity and terrestrial weathering. 2. The CO2 starvation hypothesis is developed further by identifying four key related mechanisms: decreasing net primary production (NPP) leading to (1) decreasing belowground C allocation, reducing the surface area of contact between minerals and roots and mycorrhizal fungi and (2) reduced demand for soil nutrients decreasing the active exudation of protons and organic acids by fine roots and mycorrhizas; (3) lower carbon cost-fornutrient benefits of arbuscular mycorrhizas (AM) favouring AM over ectomycorrhizal (EM) root-fungal symbioses, which are less effective at mineral weathering, and (4) conversion of forest to C3 and C4 grassland arresting Ca leaching from soils. 3. We evaluated the global importance of mechanisms 1 and 2 in silicate weathering under a changing late Miocene [CO2]a[CO2]a and climate using a process-based model of soil chemistry describing the effects of plants and mycorrhizal fungi on the biological proton cycle. The model captures what we believe are the key processes controlling the pH of the mycorrhizosphere, and includes numerical routines for calculating weathering rates on basalt and granite using simple yet rigorous equilibrium chemistry and rate laws. 4. Our simulations indicate a reduction in the capacity of the terrestrial biosphere to weather continental silicate rocks by a factor of four in response to successively decreasing [CO2]a values (400 ppm, 280 ppm, 180 ppm and 100 ppm) and associated late Miocene (11.6-5.3 Ma) cooling. Marked reductions in terrestrial weathering could effectively limit biologically mediated long-term carbon sequestration in marine sediments. 5. Synthesis. These results support the idea of terrestrial vegetation acting as a negative feedback mechanism that counteracts substantial declines in [CO2]a linked to increased production of fresh weatherable minerals in warm, low latitude, active orogenic regions.

A general integrative framework for modelling woody biomass production and carbon sequestration rates in forests Coomes, David; Holdaway, Robert; Kobe, Richard; Lines, Emily; Allen, Robert

Summary 1. Forests are an important, yet poorly understood, component of the global carbon cycle. We develop a general integrative framework for modelling the influences of stand age, environmental conditions, climate change and disturbance on woody biomass production and carbon sequestration. We use this framework to explore drivers of carbon cycling in New Zealand mountain beech forests, using a 30-year sequence of data from 246 permanent inventory plots. 2. A series of disturbance events (wind, snow storms, earthquakes and beetle outbreaks) had major effects on carbon fluxes: by killing large trees they removed significant quantities of carbon from the woody biomass pool, and by creating canopy gaps they reduced the Crown Area Index of stands (i.e. canopy area per unit ground area) and woody biomass production. A patch-dynamics model, which we parameterised using permanent plot data, predicts that episodic disturbance events can create long-term (~100-year) oscillations in carbon stocks at the regional scale. 3. Productivity declined with stand age, as shown in many other studies, but the effect was hard to detect because of canopy disturbance. Individual trees can increase productivity by adjusting the positioning, nutrient content and angle of leaves within canopies. We show that such optimization is most effective when trees are large, and suggest it reduces the impact of water and nutrient limitation in old stands. 4. We found no evidence that forests were responding to changing climatic conditions, although strong altitudinal trends in biomass production indicate that global warming could alter carbon fluxes in the future. 5. Synthesis. Our study emphasizes the critical role of disturbance in driving forest carbon fluxes. Losses of biomass arising from tree death (particularly in older stands) exceeded gains arising from growth for most of the 30-year study, moving 0.3 Mg C ha-1 yr-1 from biomass to detritus and atmospheric pools. Large-scale disturbance events are prevalent in many forests worldwide, and these events are likely to be a driving factor in determining forest carbon sequestration patterns over the next century.

The Productivity, Metabolism and Carbon Cycle of Tropical Forest Vegetation Malhi, Yadvinder

Summary 1. Tropical forests account for one third of the total metabolic activity of the Earth’s land surface. Hence understanding the controls on tropical forest photosynthesis and respiration, and the allocation of the products of photosynthesis to canopy, woody tissue and rhizosphere, is important in order to understand global ecosystem functioning. 2. I review how studies in tropical ecosystem ecology have progressed since their inception in the 1960s towards developing a quantitative, mechanistic and global description of the carbon cycle of tropical vegetation. 3. I present a synthesis of studies in tropical forest sites in the Americas and Asia for which gross primary productivity (GPP) has been reported, and a subset of these sites for which net primary productivity (NPP) and ecosystem carbon use efficiency (CUE) have been estimated. GPP ranges between 30 and 40 Mg C ha-1 year-1 in lowland moist tropical forests, and declines with elevation. CUE in tropical forests is at the low end of the global range reported for forests. 4. A pathway and framework are presented to explain the link between photosynthesis and tropical forest biomass, and in explain differences in carbon cycling and biomass between forests. Variation in CUE and allocation of NPP can be as important as variation in GPP in explaining differences in tropical forest growth rates between sites. 5. Finally, I explore some of the key questions surrounding the functioning and future of tropical forests in the rapidly changing conditions of the early Anthropocene. 6. Synthesis. There have been significant recent advances in quantifying the carbon cycle of tropical forests, but our understanding of causes of variation among forests is still poor. Moreover, we should expect all tropical forests in the 21st century, whether intact or disturbed, to be undergoing rapid change in function and composition; the key challenge for tropical ecosystem ecologists is to determine and understand the major and most fundamental aspects of this change.

Evolutionary changes in plant reproductive traits following habitat fragmentation and their consequences for population fitness Jacquemyn, Hans; De Meester, Luc; Jongejans, Eelke; Honnay, Olivier

Summary 1. The effects of habitat fragmentation on plant population genetic structure and diversity are relatively well studied. Yet, most of these studies used molecular tools focusing on neutral genetic markers, and much less is known about the potential evolutionary consequences of habitat fragmentation on ecologically relevant plant traits. 2. It can be expected that the altered biotic and abiotic conditions and limited gene flow following habitat fragmentation may impose strong selection pressures on traits important for plant fitness. Responses to these selection pressures may, however, be hampered by reduced genetic diversity through genetic drift. Conversely, evolutionary changes in flower or dispersal traits may itself impact the strength of inbreeding and genetic drift. 3. In this review, we highlight different reproductive plant traits that may be under selection following habitat fragmentation, and we examine studies that have shown indications for micro-evolutionary responses. 4. There are still relatively few studies that have convincingly shown that habitat fragmentation has generated strong micro-evolutionary responses. Separating genetic from plastic trait responses, and quantifying the long term fitness consequences of microevolutionary changes in plant traits also remain major challenges. 5. Synthesis. Many plant traits may be subject to selection following habitat fragmentation, but up till now studies that quantified micro-evolutionary responses to habitat fragmentation are limited. To study the consequences of changing plant traits for population fitness, we advocate applying population models that link demographic vital rates, the responding plant traits and their heritability.

Metapopulations and metacommunities: combining spatial and temporal perspectives in plant ecology Alexander, Helen; Foster, Bryan; Ballantyne IV, Ford; Collins, Cathy; Antonovics, Janis; Holt, Robert Summary 1. Metapopulation and metacommunity theories occupy a central role in ecology, but can be difficult to apply to plants. Challenges include whether seed dispersal is sufficient for population connectivity, the role of seed banks, and problems with studying colonization and extinction in long-lived and clonal plants. Further, populations often do not occupy discrete habitat patches. Despite these difficulties, we present case studies to illustrate explicit integration of spatial and temporal data in plant ecology. 2. First, on the population level, we focused on two early successional species that lack discrete habitat patches. Multiyear data sets taken with a grid approach and simple models permit the analysis of landscape dynamics that reflect regional as well as local processes. Using Silene latifolia, we examined colonization. We found evidence for seed dispersal and connectivity among populations across a large landscape. With Helianthus annuus, a species with seed banks, we determined the degree to which landscape-level patterns of abundance were predicted by local processes (previous year recruitment at a site plus seed banks) versus seed dispersal. Local processes dominated dynamics. 3. Second, at the community level, we utilized a landscape-level experiment to examine the influence of environmental gradients and spatial processes (dispersal limitation) on community composition during 18 years of succession. Throughout succession environmental and spatial factors both contributed significantly to spatial variation in species composition (beta diversity). When connectivity was disrupted, space was the dominant factor underlying beta diversity and this did not change over time. Across more connected communities, spatial effects diminished over succession as the importance of environmental factors increased, consistent with species-sorting metacommunity models. 4. Synthesis. Metapopulation/metacommunity concepts emphasize the interaction between space and time in ecological processes. Spatial processes, such as long-distance dispersal, play a crucial role in creating new populations. Temporal processes, including seed banks, may dominate dynamics at both local and regional scales. The relative importance of spatial versus temporal processes changes as populations persist and communities assemble over time; these patterns may only emerge after many years. Integrating long-term data with spatial data is thus essential for understanding spatio-temporal patterns inherent in metapopulation and metacommunity theories.

Modelling spread of British wind-dispersed plants under future wind speeds in a changing climate Bullock, James; White, Steven; Prudhomme, Christel; Tansey, Christine; Perea, Ramon; Hooftman, Danny Summary 1. Climate change impacts on habitat suitability and demography are often studied, but direct effects on plant dispersal are rarely considered. To address this lack we analysed climate model projections of future wind speeds and modelled their possible impacts on dispersal and spread of wind-dispersed plants. 2. Projections for 17 Global Climate Models and three emission scenarios suggested great uncertainty about wind speeds in southern England by the period 2070-2099. Projections ranged from -90% to +100% change in the mean wind speed, although the average projection was for large falls in both summer and winter wind speeds. 3. Using a novel method for converting projected changes in mean wind speed to new seasonal wind speed distributions, we parameterised a mechanistic model of seed dispersal by wind using baseline and changes in mean wind speed from -80% to +80%. 4. The mechanistic seed dispersal model was combined with demographic data in an analytical model of plant spread. This was done for three British native and three non-native species, which represented a range of life forms. 5. Dispersal kernels and population spread rates were affected disproportionately by changes in wind speed, demonstrating non-linear propagation of uncertainty in wind speed projections through to modelled plant spread rates. 6. Sensitivity analyses showed differences among the plant species in which demographic transitions were most important in determining spread rates. By contrast, sensitivity of spread rates to dispersal parameters showed great consistency among species, with seed release height being more important than seed terminal velocity. 7. Synthesis. Plant populations will need to shift their geographic ranges to keep pace with climate change-driven habitat loss. This paper shows that climate change may affect that ability by decreasing the dispersal distances of wind-dispersed plants and thus their potential spread rates. However, the modelling approach presented here illustrates that uncertainty in climate models leads to an even greater uncertainty about how dispersal and spread will change in future climates. Caution should therefore be exercised in making predictions as to how fast plant species may spread in response to climate change.

Invasions: the trail behind, the path ahead, and a test of a disturbing idea. Moles, Angela; Flores-Moreno, Habacuc; Bonser, Stephen; Warton, David; Helm, Aveliina; Warman, Laura; Eldridge, David; Jurado, Enrique

Summary 1. We provide a brief overview of progress in our understanding of introduced plant species. 2. Three main conclusions emerge from our review: (i) Many lines of research, including the search for traits that make species good invaders, or that make ecosystems susceptible to invasion, are yielding idiosyncratic results. To move forward, we advocate a more synthetic approach that incorporates a range of different types of information about the introduced species and the communities and habitats they are invading. (ii) Given the growing evidence for the adaptive capacity of both introduced species and recipient communities, we need to consider the implications of the long-term presence of introduced species in our ecosystems. (iii) Several foundational ideas in invasion biology have become widely accepted without appropriate testing, or despite equivocal evidence from empirical tests. One such idea is the suggestion that disturbance facilitates invasion. 3. We use data from 200 sites around the world to provide a broad test of the hypothesis that invasions are better predicted by a change in disturbance regime than by disturbance per se. Neither disturbance nor change in disturbance regime explained more than 7% of the variation in the % of cover or species richness contributed by introduced species. However, change in disturbance regime was a significantly better predictor than was disturbance per se, explaining approximately twice as much variation as did disturbance. 4. Synthesis. Disturbance is a weak predictor of invasion. To increase predictive power we need to consider multiple variables (both intrinsic and extrinsic to the site) simultaneously. Variables that describe the changes sites have undergone may be particularly informative.

How fundamental plant functional trait relationships scale up to trade-offs and synergies in ecosystem services Lavorel, Sandra; Grigulis, Karl

Summary 1. Ecosystem services lie at the core of the interactions among humans and ecosystems. Fundamental understanding of ecological mechanisms underlying the simultaneous provision of multiple ecosystem services has been lagging behind policy and management needs, and stands out as a research priority. In this paper we focus on interactions between ecosystem services that result from fundamental functional mechanisms. 2. Plant diversity contributes significantly to the delivery of ecosystem services. Specifically, functional composition strongly determines different ecosystem properties and services. There is now well established knowledge on associations and trade-offs among different plant traits, but their consequences for ecosystem functioning and the resulting ability for ecosystems to provide multiple services have only started to be explored. We present a conceptual framework linking environmental change to changes in ecosystem functioning, and to changes in ecosystem services through plant traits. We consider explicitly the leaf economics and size axes of plant functional variation, and how their responses to key environmental variables are expected to scale up to ecosystem properties and ecosystem services. 3. The framework was tested using a structural equation modelling formalism to understand the trait-based mechanisms driving ecosystem services trade-offs in mountain grasslands. Variations along the leaf economics spectrum (LES) towards more exploitative strategies in response to increasing fertility cascaded to the combined increase in several ecosystem services valued by local stakeholders, including agronomic value, cultural value and soil water retention. Surprisingly, and contrary to published hypotheses, soil carbon sequestration did not increase at lower fertility and with associated more conservative plant strategies. Independent variation in LES and height provided alternative pathways to biomass production. 4. Synthesis. A trait-based framework can support the understanding and aid the management of multiple ecosystem services. We recommend testing this framework in a variety of contexts and at larger scales, using additional trait axes such as wood density or seed size.

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