A decision methodology for site-level ecosystem accounting.

The United Nations System of Environmental-Economic Accounting Ecosystem Accounting (SEEA EA) framework is the international standard for ecosystem accounting. To date, application of SEEA EA has been predominantly at large scales, usually at landscape and national levels. However, many environmental management decisions are taken locally, in site-specific contexts. While the use of SEEA EA continues to develop at all scales, there is currently no widely endorsed methodology for employing SEEA EA at local scales, such as the site level. We present a methodology for developing site-level ecosystem accounts, describing the important decisions at each step of the process. We also provide two case studies that demonstrate the context-dependent nature of the decision-making process of ecosystem accounting at small scales. The two major challenges for site-level accounting are stakeholder engagement and data availability. As the use of SEEA EA continues to increase in policy and decision-making processes worldwide, there is a need for local-scale case studies that adapt this methodology across a broad range of contexts. Our case studies provide some of the first published examples of the application of SEEA EA at the site level and are intended to promote consistent implementation of ecosystem accounting across scales.

When function, not origin, matters.

Native and introduced megaherbivores similarly affect plant diversity and abundance.

Functional traits of fossil plants.

A minuscule fraction of the Earth's paleobiological diversity is preserved in the geological record as fossils. What plant remnants have withstood taphonomic filtering, fragmentation, and alteration in their journey to become part of the fossil record provide unique information on how plants functioned in paleo-ecosystems through their traits. Plant traits are measurable morphological, anatomical, physiological, biochemical, or phenological characteristics that potentially affect their environment and fitness. Here, we review the rich literature of paleobotany, through the lens of contemporary trait-based ecology, to evaluate which well-established extant plant traits hold the greatest promise for application to fossils. In particular, we focus on fossil plant functional traits, those measurable properties of leaf, stem, reproductive, or whole plant fossils that offer insights into the functioning of the plant when alive. The limitations of a trait-based approach in paleobotany are considerable. However, in our critical assessment of over 30 extant traits we present an initial, semi-quantitative ranking of 26 paleo-functional traits based on taphonomic and methodological criteria on the potential of those traits to impact Earth system processes, and for that impact to be quantifiable. We demonstrate how valuable inferences on paleo-ecosystem processes (pollination biology, herbivory), past nutrient cycles, paleobiogeography, paleo-demography (life history), and Earth system history can be derived through the application of paleo-functional traits to fossil plants.

Multidimensional responses of grassland stability to eutrophication.

Eutrophication usually impacts grassland biodiversity, community composition, and biomass production, but its impact on the stability of these community aspects is unclear. One challenge is that stability has many facets that can be tightly correlated (low dimensionality) or highly disparate (high dimensionality). Using standardized experiments in 55 grassland sites from a globally distributed experiment (NutNet), we quantify the effects of nutrient addition on five facets of stability (temporal invariability, resistance during dry and wet growing seasons, recovery after dry and wet growing seasons), measured on three community aspects (aboveground biomass, community composition, and species richness). Nutrient addition reduces the temporal invariability and resistance of species richness and community composition during dry and wet growing seasons, but does not affect those of biomass. Different stability measures are largely uncorrelated under both ambient and eutrophic conditions, indicating consistently high dimensionality. Harnessing the dimensionality of ecological stability provides insights for predicting grassland responses to global environmental change.

Maximizing the potential for living cell banks to contribute to global conservation priorities.

Although cryobanking represents a powerful conservation tool, a lack of standardized information on the species represented in global cryobanks, and inconsistent prioritization of species for future sampling, hinder the conservation potential of cryobanking, resulting in missed conservation opportunities. We analyze the representation of amphibian, bird, mammal, and reptile species within the San Diego Zoo Wildlife Alliance Frozen Zoo® living cell collection (as of April 2019) and implement a qualitative framework for the prioritization of species for future sampling. We use global conservation assessment schemes (including the International Union for Conservation of Nature (IUCN) Red List of Threatened Species™, the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), the Alliance for Zero Extinction, the EDGE of Existence, and Climate Change Vulnerability), and opportunities for sample acquisition from the global zoo and aquarium community, to identify priority species for cryobanking. We show that 965 species, including 5% of all IUCN Red List "Threatened" amphibians, birds, mammals, and reptiles, were represented in the collection and that sampling from within existing zoo and aquarium collections could increase representation to 16.6% (by sampling an additional 707 "Threatened" species). High-priority species for future cryobanking efforts include the whooping crane (Grus americana), crested ibis (Nipponia nippon), and Siberian crane (Leucogeranus leucogeranus). Each of these species are listed under every conservation assessment scheme and have ex situ populations available for sampling. We also provide species prioritizations based on subsets of these assessment schemes together with sampling opportunities from the global zoo and aquarium community. We highlight the difficulties in obtaining in situ samples, and encourage the formation of a global cryobanking database together with the establishment of new cryobanks in biodiversity-rich regions.

Measuring the shape of mortality across animals and plants: Alternatives to H entropy metrics reveal hidden type IV survivorship curves and associations with parental care at macro-ecological scales.

The shape of mortality, or how mortality is spread across an organism's life course, is fundamental to a range of biological processes, with attempts to quantify it rooted in ecology, evolution, and demography. One approach to quantify the distribution of mortality over an organism's life is the use of entropy metrics whose values are interpreted within the classical framework of survivorship curves ranging from type I distributions, with mortality concentrated in late life stages, to type III survivorship curves associated with high early stage mortality. However, entropy metrics were originally developed using restricted taxonomic groups and the behavior of entropy metrics over larger scales of variation may make them unsuitable for wider-ranging contemporary comparative studies. Here, we revisit the classic survivorship framework and, using a combination of simulations and comparative analysis of demography data spanning the animal and plant kingdoms, we show that commonly used entropy metrics cannot distinguish between the most extreme survivorship curves, which in turn can mask important macroecological patterns. We show how using H entropy masks a macroecological pattern of how parental care is associated with type I and type II species and for macroecological studies recommend the use of metrics, such as measures of area under the curve. Using frameworks and metrics that capture the full range of variation of survivorship curves will aid in our understanding of the links between the shape of mortality, population dynamics, and life history traits.

Flock size and structure influence reproductive success in four species of flamingo in 540 captive populations worldwide.

As global wildlife populations continue to decline, the health and sustainability of ex situ populations in zoos and aquariums have become increasingly important. However, the majority of managed ex situ populations are not meeting sustainability criteria and are not viable in the long term. Historically, ex situ flamingo (Phoenicopteriformes) populations have shown low rates of reproductive success and improvements are needed for long-term viability. Both flock size and environmental suitability have previously been shown to be important determinants of ex situ flamingo reproductive success in a limited number of sites in some species. Here we combined current and historic globally shared zoological records for four of the six extant species of flamingo (Phoeniconaias minor, Phoenicopterus chilensis, Phoenicopterus roseus, and Phoenicopterus ruber) to analyze how flock size, structure, and climatic variables have influenced reproductive success in ex situ flamingo populations at 540 zoological institutions from 1990 to 2019. Flock size had a strong nonlinear relationship with reproductive success for all species, with flock sizes of 41-100 birds necessary to achieve ca. 50% probability of reproduction. Additionally, an even sex ratio and the introduction of new individuals to a flock both increased ex situ reproductive success in some cases, while climatic variables played a limited role. We demonstrate the conservation management potential from globally shared zoological data and provide species-specific management recommendations to increase the reproductive success of global ex situ flamingo populations: minimum flock sizes should be increased, and we encourage greater collaboration between individual institutions and regional associations in exchanging birds between flocks.

Reconciling climate action with the need for biodiversity protection, restoration and rehabilitation.

Globally, we are faced with a climate crisis that requires urgent transition to a low-carbon economy. Simultaneously, the biodiversity crisis demands equally urgent action to prevent further species loss and promote restoration and rehabilitation of ecosystems. Climate action itself must prevent further pressures on biodiversity and options for synergistic gains for both climate and biodiversity change mitigation and adaptation need to be explored and implemented. Here, we review the key potential impacts of climate mitigation measures in energy and land-use on biodiversity, including the development of renewable energy such as offshore and onshore wind, solar, and bioenergy. We also assess the potential impacts of climate action driven afforestation and native habitat rehabilitation and restoration. We apply our findings to Ireland as a unique case-study as the government develops a coordinated response to climate and biodiversity change through declaration of a joint climate and biodiversity emergency and inclusion of biodiversity in key climate change legislation and the national Climate Action Plan. However, acknowledgement of these intertwined crises is only a first step; implementation of synergistic solutions requires careful planning. We demonstrate how synergy between climate and biodiversity action can be gained through explicit consideration of the effects of climate change mitigation strategies, such as energy infrastructure development and land-use change, on biodiversity. We identify several potential "win-win" strategies for both climate mitigation and biodiversity conservation. For Ireland, these include increasing offshore wind capacity, rehabilitating natural areas surrounding onshore wind turbines, and limiting the development of solar photovoltaics to the built environment. Ultimately, climate mitigation should be implemented in a "Right Action, Right Place" framework to maximise positive biodiversity benefits. This review provides one of the first examples of how national climate actions can be implemented in a biodiversity-conscious way to initiate discussion about synergistic solutions for both climate and biodiversity.

Impact of roadside burning on genetic diversity in a high-biomass invasive grass.

The invasive grass-fire cycle is a widely documented feedback phenomenon in which invasive grasses increase vegetation flammability and fire frequency, resulting in further invasion and compounded effects on fire regimes. Few studies have examined the role of short-term adaptation in driving the invasive grass-fire cycle, despite invasive species often thriving after introduction to new environments. We used a replicated (nine locations), paired sampling design (burn vs unburnt sites) to test the hypothesis that roadside burning increases genetic diversity and thus adaptive potential in the invasive, high-biomass grass Cenchrus ciliaris. Between four and five samples per site (n = 93) were genotyped using the DArTseq platform, and we filtered the data to produce panels of 15,965 neutral and 5030 non-neutral single nucleotide polymorphism (SNP) markers. Using fastSTRUCTURE, we detected three distinct genetic clusters with extremely high F ST values among them (0.94-0.97) suggesting three different cultivars. We found high rates of asexual reproduction, possibly related to clonality or apomixis common in this species. At three locations, burnt and unburnt sites were genetically different, but genetic structure was not consistently related to fire management across the study region. Burning was associated with high genetic diversity and sexual reproduction in one genetic cluster, but with low genetic diversity and clonality in another. Individual SNPs were associated with longitude and genetic clustering, but not with recent fire management. Overall, we found limited evidence that roadside burning consistently increased genetic diversity and adaptive potential in C. ciliaris; evolutionary and breeding history more strongly shaped genetic structure. Roadside burning could therefore continue to be used for managing biomass in this species, with continued monitoring. Our study provides a framework for detecting fire-related changes on a genetic level-a process that could be used as an early warning system to detect the invasive grass-fire cycle in future.

The macroecology of plant populations from local to global scales.

Population ecologists develop theoretical and pragmatic knowledge of how and why populations change or remain stable, how life histories evolve and devise management strategies for populations of concern. However, forecasting the effects of global change or recommending management strategies is often urgent, requiring ecologists to work without detailed local evidence while using data and models from outside the focal location or species. Here we explore how the comparative ecology of populations, population macroecology, can be used to develop generalisations within and between species across different scales, using available demographic, environmental, life history, occurrence and trait data. We outline the strengths and weaknesses of using broad climatic variables and suitability inferred from probability of occupancy models to represent environmental variation in comparative analyses. We evaluate the contributions of traits, environment and their interaction as drivers of life history strategy. We propose that insights from life history theory, together with the adaptive capacity of populations and individuals, can inform on 'persist in place' vs 'shift in space' responses to changing conditions. As demographic data accumulate at landscape and regional scales for single species, and throughout plant phylogenies, we will have new opportunities for testing macroecological generalities within and across species.

Fertilized graminoids intensify negative drought effects on grassland productivity.

Droughts can strongly affect grassland productivity and biodiversity, but responses differ widely. Nutrient availability may be a critical factor explaining this variation, but is often ignored in analyses of drought responses. Here, we used a standardized nutrient addition experiment covering 10 European grasslands to test if full-factorial nitrogen, phosphorus, and potassium addition affected plant community responses to inter-annual variation in drought stress and to the extreme summer drought of 2018 in Europe. We found that nutrient addition amplified detrimental drought effects on community aboveground biomass production. Drought effects also differed between functional groups, with a negative effect on graminoid but not forb biomass production. Our results imply that eutrophication in grasslands, which promotes dominance of drought-sensitive graminoids over forbs, amplifies detrimental drought effects. In terms of climate change adaptation, agricultural management would benefit from taking into account differential drought impacts on fertilized versus unfertilized grasslands, which differ in ecosystem services they provide to society.

Climatic and evolutionary contexts are required to infer plant life history strategies from functional traits at a global scale.

Life history strategies are fundamental to the ecology and evolution of organisms and are important for understanding extinction risk and responses to global change. Using global datasets and a multiple response modelling framework we show that trait-climate interactions are associated with life history strategies for a diverse range of plant species at the global scale. Our modelling framework informs our understanding of trade-offs and positive correlations between elements of life history after accounting for environmental context and evolutionary and trait-based constraints. Interactions between plant traits and climatic context were needed to explain variation in age at maturity, distribution of mortality across the lifespan and generation times of species. Mean age at maturity and the distribution of mortality across plants' lifespan were under evolutionary constraints. These findings provide empirical support for the theoretical expectation that climatic context is key to understanding trait to life history relationships globally.

Opposing community assembly patterns for dominant and nondominant plant species in herbaceous ecosystems globally.

Biotic and abiotic factors interact with dominant plants-the locally most frequent or with the largest coverage-and nondominant plants differently, partially because dominant plants modify the environment where nondominant plants grow. For instance, if dominant plants compete strongly, they will deplete most resources, forcing nondominant plants into a narrower niche space. Conversely, if dominant plants are constrained by the environment, they might not exhaust available resources but instead may ameliorate environmental stressors that usually limit nondominants. Hence, the nature of interactions among nondominant species could be modified by dominant species. Furthermore, these differences could translate into a disparity in the phylogenetic relatedness among dominants compared to the relatedness among nondominants. By estimating phylogenetic dispersion in 78 grasslands across five continents, we found that dominant species were clustered (e.g., co-dominant grasses), suggesting dominant species are likely organized by environmental filtering, and that nondominant species were either randomly assembled or overdispersed. Traits showed similar trends for those sites (<50%) with sufficient trait data. Furthermore, several lineages scattered in the phylogeny had more nondominant species than expected at random, suggesting that traits common in nondominants are phylogenetically conserved and have evolved multiple times. We also explored environmental drivers of the dominant/nondominant disparity. We found different assembly patterns for dominants and nondominants, consistent with asymmetries in assembly mechanisms. Among the different postulated mechanisms, our results suggest two complementary hypotheses seldom explored: (1) Nondominant species include lineages adapted to thrive in the environment generated by dominant species. (2) Even when dominant species reduce resources to nondominant ones, dominant species could have a stronger positive effect on some nondominants by ameliorating environmental stressors affecting them, than by depleting resources and increasing the environmental stress to those nondominants. These results show that the dominant/nondominant asymmetry has ecological and evolutionary consequences fundamental to understand plant communities.

Increasing effects of chronic nutrient enrichment on plant diversity loss and ecosystem productivity over time.

Human activities are enriching many of Earth's ecosystems with biologically limiting mineral nutrients such as nitrogen (N) and phosphorus (P). In grasslands, this enrichment generally reduces plant diversity and increases productivity. The widely demonstrated positive effect of diversity on productivity suggests a potential negative feedback, whereby nutrient-induced declines in diversity reduce the initial gains in productivity arising from nutrient enrichment. In addition, plant productivity and diversity can be inhibited by accumulations of dead biomass, which may be altered by nutrient enrichment. Over longer time frames, nutrient addition may increase soil fertility by increasing soil organic matter and nutrient pools. We examined the effects of 5-11 yr of nutrient addition at 47 grasslands in 12 countries. Nutrient enrichment increased aboveground live biomass and reduced plant diversity at nearly all sites, and these effects became stronger over time. We did not find evidence that nutrient-induced losses of diversity reduced the positive effects of nutrients on biomass; however, nutrient effects on live biomass increased more slowly at sites where litter was also increasing, regardless of plant diversity. This work suggests that short-term experiments may underestimate the long-term nutrient enrichment effects on global grassland ecosystems.

Author Correction: Leaf nutrients, not specific leaf area, are consistent indicators of elevated nutrient inputs.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

A system wide approach to managing zoo collections for visitor attendance and in situ conservation.

Zoos contribute substantial resources to in situ conservation projects in natural habitats using revenue from visitor attendance, as well as other sources. We use a global dataset of over 450 zoos to develop a model of how zoo composition and socio-economic factors directly and indirectly influence visitor attendance and in situ project activity. We find that zoos with many animals, large animals, high species richness (particularly of mammals), and which are dissimilar to other zoos achieve higher numbers of visitors and contribute to more in situ conservation projects. However, the model strongly supports a trade-off between number of animals and body mass indicating that alternative composition strategies, such as having many small animals, may also be effective. The evidence-base presented here can be used to help guide collection planning processes and increase the in situ contributions from zoos, helping to reduce global biodiversity loss.

Global gene flow releases invasive plants from environmental constraints on genetic diversity.

When plants establish outside their native range, their ability to adapt to the new environment is influenced by both demography and dispersal. However, the relative importance of these two factors is poorly understood. To quantify the influence of demography and dispersal on patterns of genetic diversity underlying adaptation, we used data from a globally distributed demographic research network comprising 35 native and 18 nonnative populations of Plantago lanceolata Species-specific simulation experiments showed that dispersal would dilute demographic influences on genetic diversity at local scales. Populations in the native European range had strong spatial genetic structure associated with geographic distance and precipitation seasonality. In contrast, nonnative populations had weaker spatial genetic structure that was not associated with environmental gradients but with higher within-population genetic diversity. Our findings show that dispersal caused by repeated, long-distance, human-mediated introductions has allowed invasive plant populations to overcome environmental constraints on genetic diversity, even without strong demographic changes. The impact of invasive plants may, therefore, increase with repeated introductions, highlighting the need to constrain future introductions of species even if they already exist in an area.

Managing uncertainty in movement knowledge for environmental decisions.

Species' movements affect their response to environmental change but movement knowledge is often highly uncertain. We now have well-established methods to integrate movement knowledge into conservation practice but still lack a framework to deal with uncertainty in movement knowledge for environmental decisions. We provide a framework that distinguishes two dimensions of species' movement that are heavily influenced by uncertainty: knowledge about movement and relevance of movement to environmental decisions. Management decisions can be informed by their position in this knowledge-relevance space. We then outline a framework to support decisions around (1) increasing understanding of the relevance of movement knowledge, (2) increasing robustness of decisions to uncertainties and (3) improving knowledge on species' movement. Our decision-support framework provides guidance for managing movement-related uncertainty in systematic conservation planning, agri-environment schemes, habitat restoration and international biodiversity policy. It caters to different resource levels (time and funding) so that species' movement knowledge can be more effectively integrated into environmental decisions.

Animal life history is shaped by the pace of life and the distribution of age-specific mortality and reproduction.

Animals exhibit an extraordinary diversity of life history strategies. These realized combinations of survival, development and reproduction are predicted to be constrained by physiological limitations and by trade-offs in resource allocation. However, our understanding of these patterns is restricted to a few taxonomic groups. Using demographic data from 121 species, ranging from humans to sponges, we test whether such trade-offs universally shape animal life history strategies. We show that, after accounting for body mass and phylogenetic relatedness, 71% of the variation in animal life history strategies can be explained by life history traits associated with the fast-slow continuum (pace of life) and with a second axis defined by the distribution of age-specific mortality hazards and the spread of reproduction. While we found that life history strategies are associated with metabolic rate and ecological modes of life, surprisingly similar life history strategies can be found across the phylogenetic and physiological diversity of animals.

Leaf nutrients, not specific leaf area, are consistent indicators of elevated nutrient inputs.

Leaf traits are frequently measured in ecology to provide a 'common currency' for predicting how anthropogenic pressures impact ecosystem function. Here, we test whether leaf traits consistently respond to experimental treatments across 27 globally distributed grassland sites across 4 continents. We find that specific leaf area (leaf area per unit mass)-a commonly measured morphological trait inferring shifts between plant growth strategies-did not respond to up to four years of soil nutrient additions. Leaf nitrogen, phosphorus and potassium concentrations increased in response to the addition of each respective soil nutrient. We found few significant changes in leaf traits when vertebrate herbivores were excluded in the short-term. Leaf nitrogen and potassium concentrations were positively correlated with species turnover, suggesting that interspecific trait variation was a significant predictor of leaf nitrogen and potassium, but not of leaf phosphorus concentration. Climatic conditions and pretreatment soil nutrient levels also accounted for significant amounts of variation in the leaf traits measured. Overall, we find that leaf morphological traits, such as specific leaf area, are not appropriate indicators of plant response to anthropogenic perturbations in grasslands.