Benno I. Simmons

Has land use pushed terrestrial biodiversity beyond the planetary boundary? A global assessment.

Crossing “safe” limits for biodiversity loss The planetary boundaries framework attempts to set limits for biodiversity loss within which ecological function is relatively unaffected. Newbold et al. present a quantitative global analysis of the extent to which the proposed planetary boundary has been crossed (see the Perspective by Oliver). Using over 2 million records for nearly 40,000 terrestrial species, they modeled the response of biodiversity to land use and related pressures and then estimated, at a spatial resolution of ∼1 km2, the extent and spatial patterns of changes in local biodiversity. Across 65% of the terrestrial surface, land use and related pressures have caused biotic intactness to decline beyond 10%, the proposed “safe” planetary boundary. Changes have been most pronounced in grassland biomes and biodiversity hotspots. Science, this issue p. 288; see also p. 220 Land use has reduced biosphere intactness below safe limits across 65% of Earth’s terrestrial surface, especially in grasslands. Land use and related pressures have reduced local terrestrial biodiversity, but it is unclear how the magnitude of change relates to the recently proposed planetary boundary (“safe limit”). We estimate that land use and related pressures have already reduced local biodiversity intactness—the average proportion of natural biodiversity remaining in local ecosystems—beyond its recently proposed planetary boundary across 58.1% of the world’s land surface, where 71.4% of the human population live. Biodiversity intactness within most biomes (especially grassland biomes), most biodiversity hotspots, and even some wilderness areas is inferred to be beyond the boundary. Such widespread transgression of safe limits suggests that biodiversity loss, if unchecked, will undermine efforts toward long-term sustainable development.

Policy windows for the environment: Tips for improving the uptake of scientific knowledge

(1) EU’s Seventh Framework Programme withinnthe EU Biodiversity Observation Network (No. 308454) (2) Post-doctoralnfellowship from Fondation Wiener Anspach, Belgium and the Scrivennfellowship, (3) Cambridge Earth System Science NERC DTPn[NE/L002507/1], (4) Austrian Science Fund (FWF), (5) Arcadia.

Trait evolution, resource specialization and vulnerability to plant extinctions among Antillean hummingbirds

Species traits are thought to predict feeding specialization and the vulnerability of a species to extinctions of interaction partners, but the context in which a species evolved and currently inhabits may also matter. Notably, the predictive power of traits may require that traits evolved to fit interaction partners. Furthermore, local abiotic and biotic conditions may be important. On islands, for instance, specialized and vulnerable species are predicted to be found mainly in mountains, whereas species in lowlands should be generalized and less vulnerable. We evaluated these predictions for hummingbirds and their nectar-food plants on Antillean islands. Our results suggest that the rates of hummingbird trait divergence were higher among ancestral mainland forms before the colonization of the Antilles. In correspondence with the limited trait evolution that occurred within the Antilles, local abiotic and biotic conditions—not species traits—correlate with hummingbird resource specialization and the vulnerability of hummingbirds to extinctions of their floral resources. Specifically, hummingbirds were more specialized and vulnerable in conditions with high topographical complexity, high rainfall, low temperatures and high floral resource richness, which characterize the Antillean Mountains. These findings show that resource specialization and species vulnerability to extinctions of interaction partners are highly context-dependent.

Moving from frugivory to seed dispersal: Incorporating the functional outcomes of interactions in plant–frugivore networks

Abstract There is growing interest in understanding the functional outcomes of species interactions in ecological networks. For many mutualistic networks, including pollination and seed dispersal networks, interactions are generally sampled by recording animal foraging visits to plants. However, these visits may not reflect actual pollination or seed dispersal events, despite these typically being the ecological processes of interest. Frugivorous animals can act as seed dispersers, by swallowing entire fruits and dispersing their seeds, or as pulp peckers or seed predators, by pecking fruits to consume pieces of pulp or seeds. These processes have opposing consequences for plant reproductive success. Therefore, equating visitation with seed dispersal could lead to biased inferences about the ecology, evolution and conservation of seed dispersal mutualisms. Here, we use natural history information on the functional outcomes of pairwise bird–plant interactions to examine changes in the structure of seven European plant–frugivore visitation networks after non‐mutualistic interactions (pulp pecking and seed predation) have been removed. Following existing knowledge of the contrasting structures of mutualistic and antagonistic networks, we hypothesized a number of changes following interaction removal, such as increased nestedness and lower specialization. Non‐mutualistic interactions with pulp peckers and seed predators occurred in all seven networks, accounting for 21%–48% of all interactions and 6%–24% of total interaction frequency. When non‐mutualistic interactions were removed, there were significant increases in network‐level metrics such as connectance and nestedness, while robustness decreased. These changes were generally small, homogenous and driven by decreases in network size. Conversely, changes in species‐level metrics were more variable and sometimes large, with significant decreases in plant degree, interaction frequency, specialization and resilience to animal extinctions and significant increases in frugivore species strength. Visitation data can overestimate the actual frequency of seed dispersal services in plant–frugivore networks. We show here that incorporating natural history information on the functions of species interactions can bring us closer to understanding the processes and functions operating in ecological communities. Our categorical approach lays the foundation for future work quantifying functional interaction outcomes along a mutualism–antagonism continuum, as documented in other frugivore faunas.

The major barriers to evidence-informed conservation policy and possible solutions

Abstract Conservation policy decisions can suffer from a lack of evidence, hindering effective decision‐making. In nature conservation, studies investigating why policy is often not evidence‐informed have tended to focus on Western democracies, with relatively small samples. To understand global variation and challenges better, we established a global survey aimed at identifying top barriers and solutions to the use of conservation science in policy. This obtained the views of 758 people in policy, practice, and research positions from 68 countries across six languages. Here we show that, contrary to popular belief, there is agreement between groups about how to incorporate conservation science into policy, and there is thus room for optimism. Barriers related to the low priority of conservation were considered to be important, while mainstreaming conservation was proposed as a key solution. Therefore, priorities should focus on convincing the public of the importance of conservation as an issue, which will then influence policy‐makers to adopt pro‐environmental long‐term policies.

Uncovering indirect interactions in bipartite ecological networks

Indirect interactions play an essential role in governing population, community and coevolutionary dynamics across a diverse range of ecological communities. Such communities are widely represented as bipartite networks: graphs depicting interactions between two groups of species, such as plants and pollinators or hosts and parasites. For over thirty years, studies have used indices, such as connectance and species degree, to characterise the structure of these networks and the roles of their constituent species. However, compressing a complex network into a single metric necessarily discards large amounts of information about indirect interactions. Given the large literature demonstrating the importance and ubiquity of indirect effects, many studies of network structure are likely missing a substantial piece of the ecological puzzle. Here we use the emerging concept of bipartite motifs to outline a new framework for bipartite networks that incorporates indirect interactions. While this framework is a significant departure from the current way of thinking about networks, we show that this shift is supported by quantitative analyses of simulated and empirical data. We use simulations to show how consideration of indirect interactions can highlight ecologically important differences missed by the current index paradigm. We extend this finding to empirical plant-pollinator communities, showing how two bee species, with similar direct interactions, differ in how specialised their competitors are. These examples underscore the need for a new paradigm for bipartite ecological networks: one incorporating indirect interactions.

bmotif: a package for counting motifs in bipartite networks

Bipartite networks are widely-used to represent a diverse range of species interactions, such as pollination, herbivory, parasitism and seed dispersal. The structure of these networks is usually characterised by calculating one or more metrics that capture different aspects of network architecture. While these metrics capture useful properties of networks, they only consider structure at the scale of the whole network (the macro-scale) or individual species (the micro-scale). ‘Meso-scale’ structure between these scales is usually ignored, despite representing ecologically-important interactions. Network motifs are a framework for capturing this meso-scale structure and are gaining in popularity. However, there is no software available in R, the most popular programming language among ecologists, for conducting motif analyses in bipartite networks. Similarly, no mathematical formalisation of bipartite motifs has been developed. Here we introduce bmotif: a package for counting motifs, and species positions within motifs, in bipartite networks. Our code is primarily an R package, but we also provide MATLAB and Python code of the core functionality. The software is based on a mathematical framework where, for the first time, we derive formal expressions for motif frequencies and the frequencies with which species occur in different positions within motifs. This framework means that analyses with bmotif are fast, making motif methods compatible with the permutational approaches often used in network studies, such as null model analyses. We describe the package and demonstrate how it can be used to conduct ecological analyses, using two examples of plant-pollinator networks. We first use motifs to examine the assembly and disassembly of an Arctic plant-pollinator community, and then use them to compare the roles of native and introduced plant species in an unrestored site in Mauritius. bmotif will enable motif analyses of a wide range of bipartite ecological networks, allowing future research to characterise these complex networks without discarding important meso-scale structural detail.

Abundance drives generalisation in hummingbird-plant pollination networks

Abstract Abundant pollinators are often more generalised than rare pollinators. This could be because abundance drives generalisation: neutral effects suggest that more abundant species will be more generalised simply because they have more chance encounters with potential interaction partners. On the other hand, generalisation could drive abundance, as generalised species could have a competitive advantage over specialists, being able to exploit a wider range of resources and gain a more balanced nutrient intake. Determining the direction of the abundance-generalisation relationship is therefore a ‘chicken-and-egg’ dilemma. Here we determine the direction of the relationship between abundance and generalisation in plant-hummingbird pollination networks sampled from a variety of locations across the Americas. For the first time we resolve the direction of the abundance-generalisation relationship using independent data on animal abundance. We find evidence that hummingbird pollinators are generalised because they are abundant, and little evidence that hummingbirds are abundant because they are generalised. Additionally, a null model analysis suggests this pattern is due to neutral processes: most patterns of species-level abundance and generalisation were well explained by a null model that assumed interaction neutrality. These results suggest that neutral processes play a key role in driving broad patterns of generalisation in animal pollinators across large spatial scales. Declarations Funding – BIS is supported by the Natural Environment Research Council as part of the Cambridge Earth System Science NERC DTP [NE/L002507/1]. JVB was funded by CERL - Engineer Research and Development Center. PKM was funded by the Sao Paulo Research Foundation (FAPESP grant #2015/21457-4). PAC was funded by the David Lack studentship from the British Ornithologists’ Union and Wolfson College, University of Oxford. CL was funded by the ESDEPED-UAT grant. MAM acknowledges the Consejo Nacional para Investigaciones Cientificas y Tecnologicas (Costa Rica), German Academic Exchange Service and the research funding program ‘LOEWE-Landes-Offensive zur Entwicklung Wissenschaftlicho konomischer Exzellenz’ of Hesse’s Ministry of Higher Education, Research, and the Arts (Germany). ROP was funded by CONACyT (project 258364). MAR was supported by the State of Sao Paulo Research Foundation (FAPESP) within the BIOTA/FAPESP, The Biodiversity Institute Program (www.biota.org.br) and the ‘Parcelas Permanentes’ project, as well as by Coordenacao de Pessoal de Nivel Superior (CAPES), Fundo de Apoio ao Ensino e a Pesquisa (FAEP)/Funcamp/Unicamp and The Nature Conservancy (TNC) of Brazil. LCR was supported by CNPq and Capes. MS was funded by CNPq (grant #302781/2016-1). AMMG is supported through a Marie Sklodowska-Curie Individual Fellowship (H2020-MSCA-IF-2016-704409). LVD was supported by the Natural Environment Research Council (grants NE/K015419/1 and NE/N014472/1). AMMG, JS, CR and BD thank the Danish National Research Foundation for its support of the Center for Macroecology, Evolution and Climate (grant no. DNRF96). WJS is funded by Arcadia.Abundant pollinators are often more generalised than rare pollinators. This could be because abundance drives generalisation: neutral effects suggest that more abundant species will be more generalised simply because they have more chance encounters with potential partners. On the other hand, generalisation could drive abundance, as generalised species could have a competitive advantage over specialists, being able to exploit a wider range of resources and gain a more balanced nutrient intake. Determining the direction of the abundance-generalisation relationship is therefore a chicken-and-egg dilemma. Here we determine the direction of the relationship between abundance and generalisation in hummingbird-plant pollination networks sampled from a variety of locations across the Americas. We find evidence that hummingbirds are generalised because they are abundant, and little evidence that hummingbirds are abundant because they are generalised. Additionally, a null model analysis suggests this pattern is due to neutral processes: most patterns of species-level abundance and generalisation were well explained by a null model that assumed interaction neutrality. These results suggest that neutral processes play a key role in driving broad patterns of generalisation in hummingbird pollinators. Declarations Funding – BIS is supported by the Natural Environment Research Council as part of the Cambridge Earth System Science NERC DTP [NE/L002507/1]. JVB was funded by CERL - Engineer Research and Development Center. PKM was funded by the São Paulo Research Foundation (FAPESP grant #2015/21457-4). PAC was funded by the David Lack studentship from the British Ornithologists’ Union and Wolfson College, University of Oxford. CL was funded by the ESDEPED-UAT grant. MAM acknowledges the Consejo Nacional para Investigaciones Científicas y Tecnológicas (Costa Rica), German Academic Exchange Service and the research funding program ‘LOEWE-Landes-Offensive zur Entwicklung Wissenschaftlichö konomischer Exzellenz’ of Hesse’s Ministry of Higher Education, Research, and the Arts (Germany). ROP was funded by CONACyT (project 258364). LCR was supported by CNPq and Capes. MS was funded by CNPq (grant #302781/2016-1). AMMG is supported through a Marie Skłodowska-Curie Individual Fellowship (H2020-MSCA-IF-2016-704409). LVD was supported by the Natural Environment Research Council (grants NE/K015419/1 and NE/N014472/1). AMMG, CR and BD thank the Danish National Research Foundation for its support of the Center for Macroecology, Evolution and Climate (grant no. DNRF96). WJS is funded by Arcadia.

The environmental costs and benefits of high-yield farming

How we manage farming and food systems to meet rising demand is pivotal to the future of biodiversity. Extensive field data suggest that impacts on wild populations would be greatly reduced through boosting yields on existing farmland so as to spare remaining natural habitats. High-yield farming raises other concerns because expressed per unit area it can generate high levels of externalities such as greenhouse gas emissions and nutrient losses. However, such metrics underestimate the overall impacts of lower-yield systems. Here we develop a framework that instead compares externality and land costs per unit production. We apply this framework to diverse data sets that describe the externalities of four major farm sectors and reveal that, rather than involving trade-offs, the externality and land costs of alternative production systems can covary positively: per unit production, land-efficient systems often produce lower externalities. For greenhouse gas emissions, these associations become more strongly positive once forgone sequestration is included. Our conclusions are limited: remarkably few studies report externalities alongside yields; many important externalities and farming systems are inadequately measured; and realizing the environmental benefits of high-yield systems typically requires additional measures to limit farmland expansion. Nevertheless, our results suggest that trade-offs among key cost metrics are not as ubiquitous as sometimes perceived.High-yield farming systems have the potential to spare non-farmed land for other uses (such as nature conservation), but raise concerns about their other environmental impacts (such as greenhouse gas emissions and soil erosion). This study argues such impacts should be measured per unit of production and shows that viewed this way, some land-efficient systems have less impact than lower-yielding alternatives.

Ten‐year assessment of the 100 priority questions for global biodiversity conservation

In 2008, a group of conservation scientists compiled a list of 100 priority questions for the conservation of the worlds biodiversity. However, now almost a decade later, no one has yet published a study gauging how much progress has been made in addressing these 100 high-priority questions in the peer-reviewed literature. We took a first step toward reexamining the 100 questions to identify key knowledge gaps that remain. Through a combination of a questionnaire and a literature review, we evaluated each question on the basis of 2 criteria: relevance and effort. We defined highly relevant questions as those that - if answered - would have the greatest impact on global biodiversity conservation and quantified effort based on the number of review publications addressing a particular question, which we used as a proxy for research effort. Using this approach, we identified a set of questions that, despite being perceived as highly relevant, have been the focus of relatively few review publications over the past 10 years. These questions covered a broad range of topics but predominantly tackled 3 major themes: conservation and management of freshwater ecosystems, role of societal structures in shaping interactions between people and the environment, and impacts of conservation interventions. We believe these questions represent important knowledge gaps that have received insufficient attention and may need to be prioritized in future research.