Integrating design and ecological theory to achieve adaptive diverse pastures.

Increasing plant diversity is often suggested as a way of overcoming some of the challenges faced by managers of intensive pasture systems, but it is unclear how to design the most suitable plant mixtures. Using innovative design theory, we identify two conceptual shifts that foster potentially beneficial design approaches. Firstly, reframing the goal of mixture design to supporting ecological integrity, rather than delivering lists of desired outcomes, leads to flexible design approaches that support context-specific solutions that should operate within identifiable ecological limits. Secondly, embracing, rather than minimising uncertainty in performance leads to adaptive approaches that could enhance current and future benefits of diversifying pasture. These two fundamental shifts could therefore accelerate the successful redesign of intensive pastures.

Environmental and plant community drivers of plant pathogen composition and richness.

Interactions between individual plant pathogens and their environment have been described many times. However, the relative contribution of different environmental parameters as controls of pathogen communities remains largely unknown. Here we investigate the importance of environmental factors, including geomorphology, climate, land use, soil and plant community composition, for a broad range of aboveground and belowground fungal, oomycete and bacterial plant pathogens. We found that plant community composition is the main driver of the composition and richness of plant pathogens after taking into account all other tested parameters, especially those related to climate and soil. In the face of future changes in climate and land use, our results suggest that changes in plant pathogen community composition and richness will primarily be mediated through changes in plant communities, rather than the direct effects of climate or soils.

Land use, but not distance, drives fungal beta diversity.

Fungi are one of the most diverse taxonomic groups on the planet, but much of their diversity and community organization remains unknown, especially at local scales. Indeed, a consensus on how fungal communities change across spatial or temporal gradients-beta diversity-remains nascent. Here, we use a data set of plant-associated fungal communities (leaf, root, and soil) across multiple land uses from a New Zealand-wide study to look at fungal community turnover at small spatial scales (<1 km). Using hierarchical Bayesian beta regressions and Hill-number-based diversity profiles, we show that fungal communities are often markedly dissimilar at even small distances, regardless of land use. Moreover, diversity profile plots indicate that leaf, root, and soil-associated communities show different patterns in the dominance or rarity of dissimilar species. Leaf-associated communities differed from site to site in their low-abundance species, whereas root-associated communities differed between sites in the dominant species; soil-associated communities were intermediate. Land-use differences were largely driven by the lower turnover between high-productivity grassland sites. Further, we discuss the implications and benefits of using diversity profile plots of turnover to draw inferences into the mechanisms of how communities are structured across spatial gradients.

Resource-use efficiency drives overyielding via enhanced complementarity.

Overyielding, the primary metric for assessing biodiversity effects on ecosystem functions, is often partitioned into "complementarity" and "selection" components, but this reveals nothing about the role of increased resource use, resource-use efficiency, or trait plasticity. We obtained multiple overyielding values by comparing productivity in a five-species mixture to expected values from its component monocultures at a) six levels of nitrogen addition (spanning 0-500 kg N ha-1 year-1) and b) across four seasons. We also measured light, water, and nitrogen use, resource-use efficiency, and three functional traits-leaf nitrogen content, specific leaf area, and leaf area ratio-n mixtures and monocultures. We found strong evidence for non-transgressive overyielding. This was strongest in spring, with mixture productivity exceeding expected values by 20 kg dry matter ha-1 day-1. Peak overyielding was driven by enhanced complementarity, with the two non-N2-fixing forb species far exceeding expected productivity in mixtures. Peak overyielding also coincided with higher water use in the mixture than for any monoculture, and enhanced mixture-resource-use efficiency. There was only weak evidence that trait plasticity influenced overyielding or resource use. Our findings suggest that when complementarity drives overyielding in grassland mixtures, and this is made possible both by increased water use and enhanced efficiency in water, nitrogen, and light use. Our results also suggest that mixtures offer a viable compromise between productivity, resource-use efficiency, and reduced environmental impacts (i.e., nitrate leaching) from intensive agriculture.

Rarity is a more reliable indicator of land-use impacts on soil invertebrate communities than other diversity metrics.

The effects of land use on soil invertebrates - an important ecosystem component - are poorly understood. We investigated land-use impacts on a comprehensive range of soil invertebrates across New Zealand, measured using DNA metabarcoding and six biodiversity metrics. Rarity and phylogenetic rarity - direct measures of the number of species or the portion of a phylogeny unique to a site - showed stronger, more consistent responses across taxa to land use than widely used metrics of species richness, effective species numbers, and phylogenetic diversity. Overall, phylogenetic rarity explained the highest proportion of land use-related variance. Rarity declined from natural forest to planted forest, grassland, and perennial cropland for most soil invertebrate taxa, demonstrating pervasive impacts of agricultural land use on soil invertebrate communities. Commonly used diversity metrics may underestimate the impacts of land use on soil invertebrates, whereas rarity provides clearer and more consistent evidence of these impacts.

Living within the Earth's soil are millions of insects, worms and other invertebrates, which help keep the ground healthy and fertile. There is a growing concern that changing land-use habits, such as agriculture and urban development, are causing these populations of invertebrates to decline. However, to what extent different types of land use negatively impact soil invertebrates is not clear. Healthy habitats often have a greater variety of species. This biodiversity can be measured in a number of ways, ranging from counting the number of species, to more complex approaches that calculate a species' role in an ecosystem or how close it is to extinction. Finding a way to sensitively measure the biodiversity of soil invertebrates could further researcher's understanding of how different types of land use are affecting these communities. A new method known as DNA metabarcoding has made it easier to distinguish between different species and calculate the biodiversity of entire populations. Now, Dopheide et al. have used this technique to study invertebrate communities from 75 sites across New Zealand which have been impacted by different land-use habits. This revealed that the most reliable and consistent way to uncover how land use affects soil invertebrates was to measure the rarity of species (i.e. the number of unique species present at each site). Dopheide et al. found that agriculture negatively affected soil invertebrates and that most types of invertebrates responded in a similar way. Horticulture ­ such as orchards and vineyards ­ had the most severe impact, with the lowest variety of species compared to grassland or forest. Other measurements of biodiversity, such as the number of different species, may underestimate the negative impact agriculture is having on invertebrate communities. The findings of Dopheide et al. highlight why developing strategies to preserve and restore these communities is so important. However, more work is needed to understand what specifically is causing biodiversity to decline and how this effect can be reversed.

Land use is a determinant of plant pathogen alpha- but not beta-diversity.

Little is known about the diversity patterns of plant pathogens and how they change with land use at a broad scale. We employed DNA metabarcoding to describe the diversity and composition of putative plant pathogen communities in three substrates (soil, roots, and leaves) across five major land uses at a national scale. Almost all plant pathogen communities (fungi, oomycetes, and bacteria) showed strong responses to land use and substrate type. Land use category could explain up to 24% of the variance in composition between communities. Alpha-diversity (richness) of plant pathogens was consistently lower in natural forests than in agricultural systems. In planted forests, there was also generally low pathogen alpha-diversity in soil and roots, but alpha-diversity in leaves was high compared with most other land uses. In contrast to alpha-diversity, differences in within-land use beta-diversity of plant pathogens (the predictability of plant pathogen communities within land use) were subtle. Our results show that large-scale patterns and distributions of putative plant pathogens can be determined using metabarcoding, allowing some of the first landscape level insights into these critically important communities.

Contrasting responses of soil nematode communities to native and non-native woody plant expansion.

Woody plant expansion into grasslands is widespread, driven by both successions to dominance by native woody species or invasion by non-native woody species. These shifts from grass- to woody-dominated systems also have profound effects on both above- and belowground communities and ecosystem processes. Woody-plant expansion should also alter the functional composition of the soil biota, including that of nematodes, which are major drivers of soil food-web structure and belowground processes, but such belowground impacts are poorly understood. We determined whether succession by a widespread native (Kunzea ericoides) and invasion by a non-native woody species (Pinus nigra) into tussock grasslands affect the composition of nematode functional guilds and the structure of nematode-based food webs. Although increasing dominance by woody species in both systems altered the functional guild composition of the nematode community, we found contrasting responses of nematode functional guilds to the different dominant plant species. Specifically, nematode communities reflected conditions of resource enrichment with increasing K. ericoides tree cover, whereas communities became structurally simplified and dominated by stress-tolerant nematode families with increasing P. nigra tree cover. Because nematodes regulate both bacterial- and fungal-dominated food webs in soils, these shifts could in turn alter multiple ecosystem processes belowground such as nutrient cycling. Incorporating species' functional traits into the assessment of habitat-change impacts on communities can greatly improve our understanding of species responses to environmental changes and their consequences in ecosystems.

Biases in the metabarcoding of plant pathogens using rust fungi as a model system.

Plant pathogens such as rust fungi (Pucciniales) are of global economic and ecological importance. This means there is a critical need to reliably and cost-effectively detect, identify, and monitor these fungi at large scales. We investigated and analyzed the causes of differences between next-generation sequencing (NGS) metabarcoding approaches and traditional DNA cloning in the detection and quantification of recognized species of rust fungi from environmental samples. We found significant differences between observed and expected numbers of shared rust fungal operational taxonomic units (OTUs) among different methods. However, there was no significant difference in relative abundance of OTUs that all methods were capable of detecting. Differences among the methods were mainly driven by the method's ability to detect specific OTUs, likely caused by mismatches with the NGS metabarcoding primers to some Puccinia species. Furthermore, detection ability did not seem to be influenced by differences in sequence lengths among methods, the most appropriate bioinformatic pipeline used for each method, or the ability to detect rare species. Our findings are important to future metabarcoding studies, because they highlight the main sources of difference among methods, and rule out several mechanisms that could drive these differences. Furthermore, strong congruity among three fundamentally different and independent methods demonstrates the promising potential of NGS metabarcoding for tracking important taxa such as rust fungi from within larger NGS metabarcoding communities. Our results support the use of NGS metabarcoding for the large-scale detection and quantification of rust fungi, but not for confirming the absence of species.

Biogeographic differences in soil biota promote invasive grass response to nutrient addition relative to co-occurring species despite lack of belowground enemy release.

Multiple plant species invasions and increases in nutrient availability are pervasive drivers of global environmental change that often co-occur. Many plant invasion studies, however, focus on single-species or single-mechanism invasions, risking an oversimplification of a multifaceted process. Here, we test how biogeographic differences in soil biota, such as belowground enemy release, interact with increases in nutrient availability to influence invasive plant growth. We conducted a greenhouse experiment using three co-occurring invasive grasses and one native grass. We grew species in live and sterilized soil from the invader's native (United Kingdom) and introduced (New Zealand) ranges with a nutrient addition treatment. We found no evidence for belowground enemy release. However, species' responses to nutrients varied, and this depended on soil origin and sterilization. In live soil from the introduced range, the invasive species Lolium perenne L. responded more positively to nutrient addition than co-occurring invasive and native species. In contrast, in live soil from the native range and in sterilized soils, there were no differences in species' responses to nutrients. This suggests that the presence of soil biota from the introduced range allowed L. perenne to capture additional nutrients better than co-occurring species. Considering the globally widespread nature of anthropogenic nutrient additions to ecosystems, this effect could be contributing to a global homogenization of flora and the associated losses in native species diversity.

Belowground competition drives invasive plant impact on native species regardless of nitrogen availability.

Plant invasions and eutrophication are pervasive drivers of global change that cause biodiversity loss. Yet, how invasive plant impacts on native species, and the mechanisms underpinning these impacts, vary in relation to increasing nitrogen (N) availability remains unclear. Competition is often invoked as a likely mechanism, but the relative importance of the above and belowground components of this is poorly understood, particularly under differing levels of N availability. To help resolve these issues, we quantified the impact of a globally invasive grass species, Agrostis capillaris, on two co-occurring native New Zealand grasses, and vice versa. We explicitly separated above- and belowground interactions amongst these species experimentally and incorporated an N addition treatment. We found that competition with the invader had large negative impacts on native species growth (biomass decreased by half), resource capture (total N content decreased by up to 75%) and even nutrient stoichiometry (native species tissue C:N ratios increased). Surprisingly, these impacts were driven directly and indirectly by belowground competition, regardless of N availability. Higher root biomass likely enhanced the invasive grass's competitive superiority belowground, indicating that root traits may be useful tools for understanding invasive plant impacts. Our study shows that belowground competition can be more important in driving invasive plant impacts than aboveground competition in both low and high fertility ecosystems, including those experiencing N enrichment due to global change. This can help to improve predictions of how two key drivers of global change, plant species invasions and eutrophication, impact native species diversity.

Burrowing seabird effects on invertebrate communities in soil and litter are dominated by ecosystem engineering rather than nutrient addition.

Vertebrate consumers can be important drivers of the structure and functioning of ecosystems, including the soil and litter invertebrate communities that drive many ecosystem processes. Burrowing seabirds, as prevalent vertebrate consumers, have the potential to impact consumptive effects via adding marine nutrients to soil (i.e. resource subsidies) and non-consumptive effects via soil disturbance associated with excavating burrows (i.e. ecosystem engineering). However, the exact mechanisms by which they influence invertebrates are poorly understood. We examined how soil chemistry and plant and invertebrate communities changed across a gradient of seabird burrow density on two islands in northern New Zealand. Increasing seabird burrow density was associated with increased soil nutrient availability and changes in plant community structure and the abundance of nearly all the measured invertebrate groups. Increasing seabird densities had a negative effect on invertebrates that were strongly influenced by soil-surface litter, a positive effect on fungal-feeding invertebrates, and variable effects on invertebrate groups with diverse feeding strategies. Gastropoda and Araneae species richness and composition were also influenced by seabird activity. Generalized multilevel path analysis revealed that invertebrate responses were strongly driven by seabird engineering effects, via increased soil disturbance, reduced soil-surface litter, and changes in trophic interactions. Almost no significant effects of resource subsidies were detected. Our results show that seabirds, and in particular their non-consumptive effects, were significant drivers of invertebrate food web structure. Reductions in seabird populations, due to predation and human activity, may therefore have far-reaching consequences for the functioning of these ecosystems.

Vegetation exerts a greater control on litter decomposition than climate warming in peatlands.

Historically, slow decomposition rates have resulted in the accumulation of large amounts of carbon in northern peatlands. Both climate warming and vegetation change can alter rates of decomposition, and hence affect rates of atmospheric CO2 exchange, with consequences for climate change feedbacks. Although warming and vegetation change are happening concurrently, little is known about their relative and interactive effects on decomposition processes. To test the effects of warming and vegetation change on decomposition rates, we placed litter of three dominant species (Calluna vulgaris, Eriophorum vaginatum, Hypnum jutlandicum) into a peatland field experiment that combined warming.with plant functional group removals, and measured mass loss over two years. To identify potential mechanisms behind effects, we also measured nutrient cycling and soil biota. We found that plant functional group removals exerted a stronger control over short-term litter decomposition than did approximately 1 degrees C warming, and that the plant removal effect depended on litter species identity. Specifically, rates of litter decomposition were faster when shrubs were removed from the plant community, and these effects were strongest for graminoid and bryophyte litter. Plant functional group removals also had strong effects on soil biota and nutrient cycling associated with decomposition, whereby shrub removal had cascading effects on soil fungal community composition, increased enchytraeid abundance, and increased rates of N mineralization. Our findings demonstrate that, in addition to litter quality, changes in vegetation composition play a significant role in regulating short-term litter decomposition and belowground communities in peatland, and that these impacts can be greater than moderate warming effects. Our findings, albeit from a relatively short-term study, highlight the need to consider both vegetation change and its impacts below ground alongside climatic effects when predicting future decomposition rates and carbon storage in peatlands.

Effects of climate change on the delivery of soil-mediated ecosystem services within the primary sector in temperate ecosystems: a review and New Zealand case study.

Future human well-being under climate change depends on the ongoing delivery of food, fibre and wood from the land-based primary sector. The ability to deliver these provisioning services depends on soil-based ecosystem services (e.g. carbon, nutrient and water cycling and storage), yet we lack an in-depth understanding of the likely response of soil-based ecosystem services to climate change. We review the current knowledge on this topic for temperate ecosystems, focusing on mechanisms that are likely to underpin differences in climate change responses between four primary sector systems: cropping, intensive grazing, extensive grazing and plantation forestry. We then illustrate how our findings can be applied to assess service delivery under climate change in a specific region, using New Zealand as an example system. Differences in the climate change responses of carbon and nutrient-related services between systems will largely be driven by whether they are reliant on externally added or internally cycled nutrients, the extent to which plant communities could influence responses, and variation in vulnerability to erosion. The ability of soils to regulate water under climate change will mostly be driven by changes in rainfall, but can be influenced by different primary sector systems' vulnerability to soil water repellency and differences in evapotranspiration rates. These changes in regulating services resulted in different potentials for increased biomass production across systems, with intensively managed systems being the most likely to benefit from climate change. Quantitative prediction of net effects of climate change on soil ecosystem services remains a challenge, in part due to knowledge gaps, but also due to the complex interactions between different aspects of climate change. Despite this challenge, it is critical to gain the information required to make such predictions as robust as possible given the fundamental role of soils in supporting human well-being.

Are plant-soil feedback responses explained by plant traits?

Plant-soil feedbacks can influence plant growth and community structure by modifying soil biota and nutrients. Because most research has been performed at the species level and in monoculture, our ability to predict responses across species and in mixed communities is limited. As plant traits have been linked to both soil properties and plant growth, they may provide a useful approach for an understanding of feedbacks at a generic level. We measured how monocultures and mixtures of grassland plant species with differing traits responded to soil that had been conditioned by model grassland plant communities dominated by either slow- or fast-growing species. Soils conditioned by the fast-growing community had higher nitrogen availability than those conditioned by the slow-growing community; these changes influenced future plant growth. Effects were stronger, and plant traits had greater predictive power, in mixtures than in monocultures. In monoculture, all species produced more above-ground biomass in soil conditioned by the fast-growing community. In mixtures, slow-growing species produced more above-ground biomass, and fast-growing species produced more below-ground biomass, in soils conditioned by species with similar traits. The use of a plant trait-based approach may therefore improve our understanding of differential plant species responses to plant-soil feedbacks, especially in a mixed-species environment.

Effects of species evenness and dominant species identity on multiple ecosystem functions in model grassland communities.

Ecosystems provide multiple services upon which humans depend. Understanding the drivers of the ecosystem functions that support these services is therefore important. Much research has investigated how species richness influences functioning, but we lack knowledge of how other community attributes affect ecosystem functioning. Species evenness, species spatial arrangement, and the identity of dominant species are three attributes that could affect ecosystem functioning, by altering the relative abundance of functional traits and the probability of synergistic species interactions such as facilitation and complementary resource use. We tested the effect of these three community attributes and their interactions on ecosystem functions over a growing season, using model grassland communities consisting of three plant species from three functional groups: a grass (Anthoxanthum odoratum), a forb (Plantago lanceolata), and a N-fixing forb (Lotus corniculatus). We measured multiple ecosystem functions that support ecosystem services, including ecosystem gas exchange, water retention, C and N loss in leachates, and plant biomass production. Species evenness and dominant species identity strongly influenced the ecosystem functions measured, but spatial arrangement had few effects. By the end of the growing season, evenness consistently enhanced ecosystem functioning and this effect occurred regardless of dominant species identity. The identity of the dominant species under which the highest level of functioning was attained varied across the growing season. Spatial arrangement had the weakest effect on functioning, but interacted with dominant species identity to affect some functions. Our results highlight the importance of understanding the role of multiple community attributes in driving ecosystem functioning.

Herbivore species richness, composition and community structure mediate predator richness effects and top-down control of herbivore biomass.

Changes in predator species richness can have important consequences for ecosystem functioning at multiple trophic levels, but these effects are variable and depend on the ecological context in addition to the properties of predators themselves. Here, we report an experimental study to test how species identity, community attributes, and community structure at the herbivore level moderate the effects of predator richness on ecosystem functioning. Using mesocosms containing predatory insects and aphid prey, we independently manipulated species richness at both predator and herbivore trophic levels. Community structure was also manipulated by changing the distribution of herbivore species across two plant species. Predator species richness and herbivore species richness were found to negatively interact to influence predator biomass accumulation, an effect which is hypothesised to be due to the breakdown of functional complementarity among predators in species-rich herbivore assemblages. The strength of predator suppression of herbivore biomass decreased as herbivore species richness and distribution across host plants increased, and positive predator richness effects on herbivore biomass suppression were only observed in herbivore assemblages of relatively low productivity. In summary, the study shows that the species richness, productivity and host plant distribution of prey communities can all moderate the general influence of predators and the emergence of predator species richness effects on ecosystem functioning.

Effects of plant species identity, diversity and soil fertility on biodegradation of phenanthrene in soil.

The work presented in this paper investigated the effects of plant species composition, species diversity and soil fertility on biodegradation of (14)C-phenanthrene in soil. The two soils used were of contrasting fertility, taken from long term unfertilised and fertilised grassland, showing differences in total nitrogen content (%N). Plant communities consisted of six different plant species: two grasses, two forbs, and two legume species, and ranged in species richness from 1 to 6. The degradation of (14)C-phenanthrene was evaluated by measuring indigenous catabolic activity following the addition of the contaminant to soil using respirometry. Soil fertility was a driving factor in all aspects of (14)C-phenanthrene degradation; lag phase, maximum rates and total extents of (14)C-phenanthrene mineralisation were higher in improved soils compared to unimproved soils. Plant identity had a significant effect on the lag phase and extents of mineralisation. Soil fertility was the major influence also on abundance of microbial communities.

Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment.

Understanding the factors that drive soil carbon (C) accumulation is of fundamental importance given their potential to mitigate climate change. Much research has focused on the relationship between plant traits and C sequestration, but no studies to date have quantitatively considered traits of their mycorrhizal symbionts. Here, we use a modelling approach to assess the contribution of an important mycorrhizal fungal trait, organic nutrient uptake, to soil C accumulation. We show that organic nutrient uptake can significantly increase soil C storage, and that it has a greater effect under nutrient-limited conditions. The main mechanism behind this was an increase in plant C fixation and subsequent increased C inputs to soil through mycorrhizal fungi. Reduced decomposition due to increased nutrient limitation of saprotrophs also played a role. Our results indicate that direct uptake of nutrients from organic pools by mycorrhizal fungi could have a significant effect on ecosystem C cycling and storage.

Ecological consequences of carbon substrate identity and diversity in a laboratory study.

Plants return a wide range of carbon (C) substrates to the soil system. The decomposition rate of these substrates is determined by their chemical nature, yet few studies have examined the relative ecological role of specific substrates (i.e., substrate identity) or mixtures of substrates. Carbon substrate identity and diversity may alter soil chemistry and soil community composition, resulting in changes in belowground ecosystem functions such as decomposition and nutrient transfer, creating feedbacks that may affect plant growth and the aboveground community. A laboratory experiment was set up in which eight C substrates of varying chemical complexity were added to a base soil singly, in pairs, fours, or with all eight together every four days over a 92-day period. After 92 days these soils were analyzed for changes in chemistry, microbial community structure, and components of ecosystem functioning. The identity of the added C substrates significantly affected soil chemistry, microbial basal and substrate-induced respiration, and soil microbial community structure measured by either the catabolic response profile (CRP) technique or phospholipid fatty acid composition. These belowground changes strongly affected the ability of the soil microflora to decompose cellulose paper, probably because of differential effects of the C substrates on soil energy supplies and enzyme activities. The addition of C substrates to soils also reduced plant growth compared to the unamended control soil, but less so in soils amended with a tannin than those amended with other substrates. Carbon substrate diversity effects saturated at low diversity levels, tended to have neutral or negative effects on ecosystem functions, and depended strongly on which C substrates were added. It increased CRP compound use but had little effect on other measures of the soil microbial community. Overall, results showed that the chemical nature of C substrates added to soil, and sometimes their diversity, can affect the soil microbial community and soil chemistry, which subsequently affect other ecosystem processes such as decomposition and plant growth. The identity and diversity of substrates that plants add to soil may therefore have important consequences for both above- and belowground ecosystem functions.