Olga Ferlian

Methods to identify the prey of invertebrate predators in terrestrial field studies

Abstract Predation is an interaction during which an organism kills and feeds on another organism. Past and current interest in studying predation in terrestrial habitats has yielded a number of methods to assess invertebrate predation events in terrestrial ecosystems. We provide a decision tree to select appropriate methods for individual studies. For each method, we then present a short introduction, key examples for applications, advantages and disadvantages, and an outlook to future refinements. Video and, to a lesser extent, live observations are recommended in studies that address behavioral aspects of predator–prey interactions or focus on per capita predation rates. Cage studies are only appropriate for small predator species, but often suffer from a bias via cage effects. The use of prey baits or analyses of prey remains are cheaper than other methods and have the potential to provide per capita predation estimates. These advantages often come at the cost of low taxonomic specificity. Molecular methods provide reliable estimates at a fine level of taxonomic resolution and are free of observer bias for predator species of any size. However, the current PCR‐based methods lack the ability to estimate predation rates for individual predators and are more expensive than other methods. Molecular and stable isotope analyses are best suited to address systems that include a range of predator and prey species. Our review of methods strongly suggests that while in many cases individual methods are sufficient to study specific questions, combinations of methods hold a high potential to provide more holistic insights into predation events. This review presents an overview of methods to researchers that are new to the field or to particular aspects of predation ecology and provides recommendations toward the subset of suitable methods to identify the prey of invertebrate predators in terrestrial field research.

Land-use type and intensity differentially filter traits in above- and below-ground arthropod communities

Along with the global decline of species richness goes a loss of ecological traits. Associated biotic homogenization of animal communities and narrowing of trait diversity threaten ecosystem functioning and human well-being. High management intensity is regarded as an important ecological filter, eliminating species that lack suitable adaptations. Below-ground arthropods are assumed to be less sensitive to such effects than above-ground arthropods. Here, we compared the impact of management intensity between (grassland vs. forest) and within land-use types (local management intensity) on the trait diversity and composition in below- and above-ground arthropod communities. We used data on 722 arthropod species living above-ground (Auchenorrhyncha and Heteroptera), primarily in soil (Chilopoda and Oribatida) or at the interface (Araneae and Carabidae). Our results show that trait diversity of arthropod communities is not primarily reduced by intense local land use, but is rather affected by differences between land-use types. Communities of Auchenorrhyncha and Chilopoda had significantly lower trait diversity in grassland habitats as compared to forests. Carabidae showed the opposite pattern with higher trait diversity in grasslands. Grasslands had a lower proportion of large Auchenorrhyncha and Carabidae individuals, whereas Chilopoda and Heteroptera individuals were larger in grasslands. Body size decreased with land-use intensity across taxa, but only in grasslands. The proportion of individuals with low mobility declined with land-use intensity in Araneae and Auchenorrhyncha, but increased in Chilopoda and grassland Heteroptera. The proportion of carnivorous individuals increased with land-use intensity in Heteroptera in forests and in Oribatida and Carabidae in grasslands. Our results suggest that gradients in management intensity across land-use types will not generally reduce trait diversity in multiple taxa, but will exert strong trait filtering within individual taxa. The observed patterns for trait filtering in individual taxa are not related to major classifications into above- and below-ground species. Instead, ecologically different taxa resembled each other in their trait diversity and compositional responses to land-use differences. These previously undescribed patterns offer an opportunity to develop management strategies for the conservation of trait diversity across taxonomic groups in permanent grassland and forest habitats.

Invasive earthworms erode soil biodiversity: a meta-analysis.

Biological invasions pose a serious threat to biodiversity and ecosystem functioning across ecosystems. Invasions by ecosystem engineers, in particular, have been shown to have dramatic effects in recipient ecosystems. For instance, invasion by earthworms, a below-ground invertebrate ecosystem engineer, in previously earthworm-free ecosystems alters the physico-chemical characteristics of the soil. Studies have shown that such alterations in the soil can have far-reaching impacts on soil organisms, which form a major portion of terrestrial biodiversity. Here, we present the first quantitative synthesis of earthworm invasion effects on soil micro-organisms and soil invertebrates based on 430 observations from 30 independent studies. Our meta-analysis shows a significant decline of the diversity and density of soil invertebrates in response to earthworm invasion with anecic and endogeic earthworms causing the strongest effects. Earthworm invasion effects on soil micro-organisms were context-dependent, such as depending on functional group richness of invasive earthworms and soil depth. Microbial biomass and diversity increased in mineral soil layers, with a weak negative effect in organic soil layers, indicating that the mixing of soil layers by earthworms (bioturbation) may homogenize microbial communities across soil layers. Our meta-analysis provides a compelling evidence for negative effects of a common invasive below-ground ecosystem engineer on below-ground biodiversity of recipient ecosystems, which could potentially alter the ecosystem functions and services linked to soil biota.

Leaf and root C-to-N ratios are poor predictors of soil microbial biomass C and respiration across 32 tree species

Soil microorganisms are the main primary decomposers of plant material and drive biogeochemical processes like carbon and nitrogen cycles. Hence, knowledge of their nutritional demands and limitations for activity and growth is of particular importance. However, potential effects of the stoichiometry of soil and plant species on soil microbial activity and carbon use efficiency are poorly understood. Soil properties and plant traits are assumed to drive microbial carbon and community structure. We investigated the associations between C and N concentrations of leaf, root, and soil as well as their ratios and soil microbial biomass C and activity (microbial basal respiration and specific respiratory quotient) across 32 young native angiosperm tree species at two locations in Central Germany. Correlations between C:N ratios of leaves, roots, and soil were positive but overall weak. Only regressions between root and leaf C:N ratios as well as between root and soil C:N ratios were significant at one site. Soil microbial properties differed significantly between the two sites and were significantly correlated with soil C:N ratio across sites. Soil C concentrations rather than N concentrations drove significant effects of soil C:N ratio on soil microbial properties. No significant correlations between soil microbial properties and leaf as well as root C:N ratios were found. We found weak correlations of C:N ratios between plant aboveground and belowground tissues. Furthermore, microorganisms were not affected by the stoichiometry of plant tissues in the investigated young trees. The results suggest that soil stoichiometry represents a consistent determinant of soil microbial biomass and respiration. Our study indicates that stoichiometric relationships among tree organs can be weak and poor predictors of soil microbial properties in young tree stands. Further research in controlled experimental settings with a wide range of tree species is needed to study the role of plant chemical traits like the composition and stoichiometry of root exudates in determining interactions between above- and belowground compartments.

Red list of a black box

To the Editor — It has recently been announced that for the first time the Federal Agency for Nature Conservation (BfN) Red List (a regional red list of threatened species in Germany) includes groups of soil invertebrates, namely earthworms, millipedes and centipedes1. Although these taxa already appear in very small numbers on other regional red lists (http://www.nationalredlist.org/) and the global IUCN Red List (http:// www.iucnredlist.org/), the taxonomic bias towards more charismatic species means that these understudied soil invertebrates are under-represented2 (Fig. 1). However, more worrying is the lack of information regarding the threats faced by these species. Of the 47 earthworm species assessed for the BfN Red List based on occurrence data, the most common status was Least Concern (22; although 14 of the 47 earthworm species were assessed as Extremely Rare); however, there are virtually no data on longor short-term population trends or risks faced1. For example, very little is known about the effects of human impacts, such as land-use change and climate change, on below-ground communities3, especially compared with above-ground organisms, highlighting the urgent need for more information. The lack of available soil biodiversity data results in under-representation in many biodiversity databases and synthesis analyses4,5. Existing databases often (1) have few data on soil organisms (for example, the PREDICTS database contains just under 1% of all described annelids6, whereas BioTIME4 contains no soil invertebrate time-series data); (2) are not global7; or (3) concentrate on a small subset of soil taxa8. We strongly advocate for data-mobilization initiatives focused on soil biodiversity, in order to address large-scale questions9. Such synthetic analyses can be useful in answering key questions as to how soil biodiversity might respond to anthropogenic impacts2,3, and if the response differs from those seen in above-ground biodiversity10. Given the importance of local biodiversity for ecosystem services and function, determining whether local biodiversity is declining (a hotly debated topic11), both aboveand below-ground2, is crucial in sustaining human well-being12. Mobilizing the necessary information and data on the ‘black box’ of soil biodiversity will require large collaborative initiatives. In addition, increasing the representation of the hidden biota on national and global red lists will help raise the awareness of policymakers as well as the general public, ideally resulting in increased funding for assessments and research in order to better understand changes in this underexplored biodiversity that is so critical for human well-being. ❐

Growing Research Networks on Mycorrhizae for Mutual Benefits

Research on mycorrhizal interactions has traditionally developed into separate disciplines addressing different organizational levels. This separation has led to an incomplete understanding of mycorrhizal functioning. Integration of mycorrhiza research at different scales is needed to understand the mechanisms underlying the context dependency of mycorrhizal associations, and to use mycorrhizae for solving environmental issues. Here, we provide a road map for the integration of mycorrhiza research into a unique framework that spans genes to ecosystems. Using two key topics, we identify parallels in mycorrhiza research at different organizational levels. Based on two current projects, we show how scientific integration creates synergies, and discuss future directions. Only by overcoming disciplinary boundaries, we will achieve a more comprehensive understanding of the functioning of mycorrhizal associations.

Mycorrhiza in tree diversity–ecosystem function relationships: conceptual framework and experimental implementation

The widely observed positive relationship between plant diversity and ecosystem functioning is thought to be substantially driven by complementary resource use of plant species. Recent work suggests that biotic interactions among plants and between plants and soil organisms drive key aspects of resource use complementarity. Here, we provide a conceptual framework for integrating positive biotic interactions across guilds of organisms, more specifically between plants and mycorrhizal types, to explain resource use complementarity in plants and its consequences for plant competition. Our overarching hypothesis is that ecosystem functioning increases when more plant species associate with functionally dissimilar mycorrhizal fungi because differing mycorrhizal types will increase coverage of habitat space for and reduce competition among plants. We introduce a recently established field experiment (MyDiv) that uses different pools of tree species that associate with either arbuscular or ectomycorrhizal fungi to create orthogonal experimental gradients in tree species richness and mycorrhizal associations and present initial results. Finally, we discuss options for future mechanistic studies on resource use complementarity within MyDiv. We show how mycorrhizal types and biotic interactions in MyDiv can be used in the future to test novel questions regarding the mechanisms underlying biodiversity–ecosystem function relationships.

Global gaps in soil biodiversity data

To the Editor — Soil biodiversity represents a major terrestrial biodiversity pool, supports key ecosystem services and is under pressure from human activities1. Yet soil biodiversity has been neglected from many global biodiversity assessments and policies. This omission is undoubtedly related to the paucity of comprehensive information on soil biodiversity, particularly on larger spatial scales. Information on belowground species distributions, population trends, endemism and threats to belowground diversity is important for conservation prioritization, but is practically non-existent. As a consequence, much of our understanding of global macroecological patterns in biodiversity, as well as mapping of global biodiversity hotspots, has been based on aboveground taxa (such as plants2) and has not considered the functionally vital, but less visible, biodiversity found in soil. We mapped the study sites from existing global datasets on soil biodiversity (soil macrofauna3, fungi4 and bacteria5) to examine key data gaps (Fig. 1). Our map indicates significant gaps in soil biodiversity data across northern latitudes, including most of Russia and Canada. Data are also lacking from much of central Asia and central Africa (for example, the Sahara Desert), as well as many tropical regions. The higher density of soil biodiversity sampling sites in Europe and the United States is similar to patterns observed for data on terrestrial bird, mammal and amphibian species6, as well as plants7. Yet, in such aboveground datasets, the gaps in understudied regions are much less pronounced than in the soil biodiversity datasets shown here. The comparative lack of soil biodiversity data across these regions limits our ability to examine global macroecological patterns and to quantify potential mismatches between aboveground and soil biodiversity. The potential for such mismatches (areas with high aboveground diversity, but low soil biodiversity, or vice versa) may be substantial, as evidence suggests that plant species richness declines more rapidly towards the North Pole than fungal species richness, which reaches a plateau4. Soil ecologists are increasingly conducting their own large-scale assessments (such as the African Soil Microbiology Project8) and additional databases on soil biodiversity are beginning to be developed9, in part through the Global Soil Biodiversity Initiative. However, increased efforts to fill these gaps and to compile additional global datasets on other soil taxa (for example, mesofauna) are needed to allow more detailed analyses of soil biodiversity on broad spatial scales. Of major concern is the lack of a global consensus on sampling strategies and methodological approaches to assess soil biodiversity, which in many cases makes it challenging to compare datasets directly. Furthermore, greater cooperation with conservation biologists and policymakers is needed to better integrate soil biodiversity into global policies. For instance, soil biodiversity should be more explicitly considered in the post-2020 global biodiversity framework10 that will follow the Strategic Plan for Biodiversity 2011–2020 and in future assessments of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services11. These evident gaps in soil biodiversity data restrict our ability to develop policies to protect soil biodiversity. We argue that addressing these data gaps will ultimately benefit human well-being1 and provide an impetus for increased policy-relevant research on soil biodiversity. ❐