Stephen A. Wood

Functional traits in agriculture: agrobiodiversity and ecosystem services.

Functional trait research has led to greater understanding of the impacts of biodiversity in ecosystems. Yet, functional trait approaches have not been widely applied to agroecosystems and understanding of the importance of agrobiodiversity remains limited to a few ecosystem processes and services. To improve this understanding, we argue here for a functional trait approach to agroecology that adopts recent advances in trait research for multitrophic and spatially heterogeneous ecosystems. We suggest that trait values should be measured across environmental conditions and agricultural management regimes to predict how ecosystem services vary with farm practices and environment. This knowledge should be used to develop management strategies that can be easily implemented by farmers to manage agriculture to provide multiple ecosystem services.

Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition

Significance Ecosystem functioning is more strongly affected by biodiversity loss when multiple functions are considered because different species affect different functions. To quantify these biodiversity-functioning relationships, the emerging multifunctionality framework advocates calculation of indices that aggregate responses of individual functions. Data aggregation, however, is notorious for providing misleading information by obscuring true relationships between explanatory and response variables. We test the ability of common multifunctionality indices to reveal effects on key ecosystem functions of changes in soil communities. The multifunctionality indices all decrease with soil animal loss, but the responses of individual functions diverge markedly from these aggregated metrics. Application of the multifunctionality framework for landscape provision of multiple ecosystem services should therefore emphasize understanding relationships between communities and individual functions. Ecosystem management policies increasingly emphasize provision of multiple, as opposed to single, ecosystem services. Management for such “multifunctionality” has stimulated research into the role that biodiversity plays in providing desired rates of multiple ecosystem processes. Positive effects of biodiversity on indices of multifunctionality are consistently found, primarily because species that are redundant for one ecosystem process under a given set of environmental conditions play a distinct role under different conditions or in the provision of another ecosystem process. Here we show that the positive effects of diversity (specifically community composition) on multifunctionality indices can also arise from a statistical fallacy analogous to Simpson’s paradox (where aggregating data obscures causal relationships). We manipulated soil faunal community composition in combination with nitrogen fertilization of model grassland ecosystems and repeatedly measured five ecosystem processes related to plant productivity, carbon storage, and nutrient turnover. We calculated three common multifunctionality indices based on these processes and found that the functional complexity of the soil communities had a consistent positive effect on the indices. However, only two of the five ecosystem processes also responded positively to increasing complexity, whereas the other three responded neutrally or negatively. Furthermore, none of the individual processes responded to both the complexity and the nitrogen manipulations in a manner consistent with the indices. Our data show that multifunctionality indices can obscure relationships that exist between communities and key ecosystem processes, leading us to question their use in advancing theoretical understanding—and in management decisions—about how biodiversity is related to the provision of multiple ecosystem services.

Understanding the dominant controls on litter decomposition

Summary 1. Litter decomposition is a biogeochemical process fundamental to element cycling within ecosystems, influencing plant productivity, species composition and carbon storage. 2. Climate has long been considered the primary broad-scale control on litter decomposition rates, yet recent work suggests that plant litter traits may predominate. Both decomposition paradigms, however, rely on inferences from cross-biome litter decomposition studies that analyse site-level means. 3. We re-analyse data from a classical cross-biome study to demonstrate that previous research may falsely inflate the regulatory role of climate on decomposition and mask the influence of unmeasured local-scale factors. 4. Using the re-analysis as a platform, we advocate experimental designs of litter decomposition studies that involve high within-site replication, measurements of regulatory factors and processes at the same local spatial grain, analysis of individual observations and biome-scale gradients. 5. Synthesis. We question the assumption that climate is the predominant regulator of decomposition rates at broad spatial scales. We propose a framework for a new generation of studies focused on factoring local-scale variation into the measurement and analysis of soil processes across broad scales. Such efforts may suggest a revised decomposition paradigm and ultimately improve confidence in the structure, parameter estimates and hence projections of biogeochemical models.

Metrics for land-scarce agriculture

Nutrient content must be better integrated into planning Over the past half-century, the paradigm for agricultural development has been to maximize yields through intensifying production, particularly for cereal crops (1). Increasing production of high-yielding cereals—wheat, rice, and maize—has replaced more nutrient-rich cereals, which has eroded the content of essential dietary nutrients in the worlds cereal supply. New approaches are needed to produce healthy foods, rich in essential nutrients, with efficient use of land. Standard yield metrics that measure the quantity of production are inadequate to assess progress toward this goal; thus, we propose alternative metrics of nutritional yields.

Synergies and tradeoffs between cash crop production and food security: a case study in rural Ghana

Despite dramatic improvements in global crop yields over the past half-century, chronic food insecurity persists in many parts of the world. Farming crops for sale (cash cropping) has been recommended as a way to increase income that can, in turn, improve food security for smallholder farmers. Despite long-term efforts by development agencies and government to promote cash cropping, there is limited evidence documenting a relationship between these crops and the food security of households cultivating them. We used a mixed methods approach to build a case study to assess these relationships by collecting quantitative and qualitative data from cacao and oil palm farmers in the Ashanti region of Ghana. Three dimensions of food security were considered: food availability, measured by the months in a year households reported inadequate food; food access, indicated by the coping strategies they employed to secure sufficient food; and food utilization, gauged by the diversity of household diets and anthropometric measurements of child nutritional status. We found significant negative relationships between each of these pillars of food security and a household’s intensity of cash crop production, measured by both quantity and area. A qualitative assessment indicated community perception of these tradeoffs and identified potential mechanisms, including increasing food prices and competing activities for land use, as underlying causes. The adverse relationship between cash crop production and household food security observed in this paper calls for caution; results suggest that positive relationships cannot be assumed, and that further empirical evidence is needed to better understand these tradeoffs.

Biodiversity as a multidimensional construct: a review, framework and case study of herbivory's impact on plant biodiversity

Biodiversity is inherently multidimensional, encompassing taxonomic, functional, phylogenetic, genetic, landscape and many other elements of variability of life on the Earth. However, this fundamental principle of multidimensionality is rarely applied in research aimed at understanding biodiversitys value to ecosystem functions and the services they provide. This oversight means that our current understanding of the ecological and environmental consequences of biodiversity loss is limited primarily to what unidimensional studies have revealed. To address this issue, we review the literature, develop a conceptual framework for multidimensional biodiversity research based on this review and provide a case study to explore the framework. Our case study specifically examines how herbivory by whitetail deer (Odocoileus virginianus) alters the multidimensional influence of biodiversity on understory plant cover at Black Rock Forest, New York. Using three biodiversity dimensions (taxonomic, functional and phylogenetic diversity) to explore our framework, we found that herbivory alters biodiversitys multidimensional influence on plant cover; an effect not observable through a unidimensional approach. Although our review, framework and case study illustrate the advantages of multidimensional over unidimensional approaches, they also illustrate the statistical and empirical challenges such work entails. Meeting these challenges, however, where data and resources permit, will be important if we are to better understand and manage the consequences we face as biodiversity continues to decline in the foreseeable future.

Agricultural intensification and the functional capacity of soil microbes on smallholder African farms

Summary 1. Fertilization may impact ecosystem processes that sustain agriculture, such as nutrient cycling, by altering the composition of soil microbial communities that regulate such processes. These processes are crucial to low-input, smallholder tropical agriculture, which supports 900 million of the world’s poorest people. Yet little is known about how efforts to increase crop yield on such farms will affect the capacity of soil microbial communities to carry out ecosystem processes. 2. We studied the diversity and functional capacity of microbial communities on smallholder farms in western Kenya. We measured functional capacity as the abundance of functional genes involved in several components of nutrient cycling as well as catabolism of multiple carbon substrates; taxonomic diversity was measured using metagenomic sequencing. Diversity and functional capacity were measured on short-term, experimental mineral fertilizer addition plots and on actively managed farms that have maintained for at least seven years a management strategy of low mineral fertilization, high mineral fertilization, or high fertilization combined with legume rotations. 3. Soil bacterial diversity decreased with mineral fertilizer addition, with a community shift towards taxa that thrive in high-resource conditions. This taxonomic response did not correspond with decreased microbial functional capacity. Instead, functional capacity was increased, along with yields, when fertilizers were combined with legume rotations that add organic matter to soil. 4. Policy implications. Mineral fertilizer use is associated with lower soil microbial diversity on smallholder farms, but not associated with changes in microbial functional capacity. Functional capacity is highest, along with yields, when mineral fertilizers are paired with legume rotations. Our findings suggest that this type of agroforestry can be an important strategy for maintaining the long-term functional capacity of soil microbes as well as increasing crop yields on smallholder farms. These observations support proposals to achieve long-term food production targets in sub-Saharan Africa by combining mineral fertilizers with organic inputs.

A test of the hierarchical model of litter decomposition

Our basic understanding of plant litter decomposition informs the assumptions underlying widely applied soil biogeochemical models, including those embedded in Earth system models. Confidence in projected carbon cycle–climate feedbacks therefore depends on accurate knowledge about the controls regulating the rate at which plant biomass is decomposed into products such as CO2. Here we test underlying assumptions of the dominant conceptual model of litter decomposition. The model posits that a primary control on the rate of decomposition at regional to global scales is climate (temperature and moisture), with the controlling effects of decomposers negligible at such broad spatial scales. Using a regional-scale litter decomposition experiment at six sites spanning from northern Sweden to southern France—and capturing both within and among site variation in putative controls—we find that contrary to predictions from the hierarchical model, decomposer (microbial) biomass strongly regulates decomposition at regional scales. Furthermore, the size of the microbial biomass dictates the absolute change in decomposition rates with changing climate variables. Our findings suggest the need for revision of the hierarchical model, with decomposers acting as both local- and broad-scale controls on litter decomposition rates, necessitating their explicit consideration in global biogeochemical models.Accurate understanding of plant litter decomposition is vital to inform Earth system modelling. Here the dominant hierarchical model for plant litter decomposition is found to be wanting, and revisions are suggested.

Contingency in ecosystem but not plant community response to multiple global change factors

Community and ecosystem responses to global environmental change are contingent on the magnitude of change and interacting global change factors. To reveal whether responses are also contingent on the magnitude of each interacting factor, multifactor, multilevel experiments are required, but are rarely conducted. We exposed model grassland ecosystems to six levels of atmospheric CO2 and six levels of nitrogen enrichment, applying the latter both chronically (simulating deposition) and acutely (simulating fertilization). The 66 treatments were maintained for 6 months under controlled growing conditions, with biomass harvested every 28 d and sorted to species. Aboveground plant productivity responses to CO2 were contingent on nitrogen amount, and the responses to nitrogen amount were dependent on whether applications were chronic or acute. Specifically, productivity responses to increasing CO2 concentrations were accentuated with higher nitrogen enrichments, and productivity was greater when higher nitrogen enrichments were applied acutely. Plant community composition was influenced only by nitrogen enrichment, where the co-dominant grass species with the greatest leaf trait plasticity increasingly dominated with higher nitrogen amounts. Community processes are considered to be unpredictable, but our data suggest that the prediction of the impacts of simultaneous global changes is more complex for ecosystem processes, given that their responses are contingent on the levels of interacting factors.

Farm management, not soil microbial diversity, controls nutrient loss from smallholder tropical agriculture

Tropical smallholder agriculture is undergoing rapid transformation in nutrient cycling pathways as international development efforts strongly promote greater use of mineral fertilizers to increase crop yields. These changes in nutrient availability may alter the composition of microbial communities with consequences for rates of biogeochemical processes that control nutrient losses to the environment. Ecological theory suggests that altered microbial diversity will strongly influence processes performed by relatively few microbial taxa, such as denitrification and hence nitrogen losses as nitrous oxide, a powerful greenhouse gas. Whether this theory helps predict nutrient losses from agriculture depends on the relative effects of microbial community change and increased nutrient availability on ecosystem processes. We find that mineral and organic nutrient addition to smallholder farms in Kenya alters the taxonomic and functional diversity of soil microbes. However, we find that the direct effects of farm management on both denitrification and carbon mineralization are greater than indirect effects through changes in the taxonomic and functional diversity of microbial communities. Changes in functional diversity are strongly coupled to changes in specific functional genes involved in denitrification, suggesting that it is the expression, rather than abundance, of key functional genes that can serve as an indicator of ecosystem process rates. Our results thus suggest that widely used broad summary statistics of microbial diversity based on DNA may be inappropriate for linking microbial communities to ecosystem processes in certain applied settings. Our results also raise doubts about the relative control of microbial composition compared to direct effects of management on nutrient losses in applied settings such as tropical agriculture.