A Review of Condition Metrics Used in Biodiversity Offsetting.

Biodiversity offsets are commonly used to compensate for environmental impacts, but their effectiveness is often questioned. Estimations of expected losses and gains often rely on what we called condition metrics, which measure a site's quality or condition using certain ecological attributes. Condition metrics are central to most offset policies, but their attributes and calculations vary substantially. We reviewed the academic literature to draw a profile of existing condition metrics used in the offsetting context. We found 17 metrics that differed in how they included attributes from the three "dimensions of equivalence": biodiversity (present in 15 metrics), landscape (in 10 metrics) and ecosystem services (in 5 metrics). Most metrics included many ecological attributes and required fieldwork and GIS data to be calculated, but few used modeling and expert opinion. Generally, metrics aggregated the attributes into a single final value and were created in Global North countries. To favor more transparent and ecologically equivalent offset trades worldwide, we suggest condition metrics should include the three dimensions of equivalence in a disaggregated way, i.e. measurements done separately and analyzed in parallel. The use of modeling, expert opinion and GIS may facilitate the inclusion of the dimensions and reduce the need for intensive (and expensive) fieldwork. Testing synergies and trade-offs among attributes could indicate if metrics can be simplified without losing information. Finally, development of fit-for-purpose condition metrics is especially important in Global South countries, where few such metrics exist.

Native forest cover safeguards stream water quality under a changing climate.

Ensuring a sufficient and adequate supply of water for humans and ecosystems is a pressing environmental challenge. The expansion of agricultural and urban lands has jeopardized watershed ecosystem services and a changing climate poses additional risks for regional water supply. We used stream water quality data collected between 2000 and 2014, coupled with detailed precipitation and land cover information, to investigate the effects of landscape composition and short-term precipitation variability on the quality of water resources in the state of São Paulo, Brazil. The state is home to over 45 million people and has a long history of human landscape modification. A severe drought in 2014-2015 led to a major water crisis and highlighted the fragility of the regional water supply system. We found that human-dominated watersheds had lower overall water quality when compared to forested watersheds, with urban cover showing the most detrimental impacts on water quality. Forest cover was associated with a better overall water quality across the studied watersheds, with forested watersheds having low turbidity and high dissolved oxygen. High precipitation led to increased turbidity and fecal coliforms levels and lower dissolved oxygen in streams but these effects depended on watershed land cover. High precipitation diluted concentrations of nitrogen and dissolved solids in highly urbanized watersheds but exacerbated turbidity in pasture-dominated watersheds. Given the high costs of water treatment in densely populated regions, there is a pressing need to plan and manage landscapes in order to ensure adequate water resources. In tropical regions, maintaining or restoring native vegetation cover is a promising intervention to sustain adequate water quality.

ATLANTIC BIRDS: a data set of bird species from the Brazilian Atlantic Forest.

South America holds 30% of the world's avifauna, with the Atlantic Forest representing one of the richest regions of the Neotropics. Here we have compiled a data set on Brazilian Atlantic Forest bird occurrence (150,423) and abundance samples (N = 832 bird species; 33,119 bird individuals) using multiple methods, including qualitative surveys, mist nets, point counts, and line transects). We used four main sources of data: museum collections, on-line databases, literature sources, and unpublished reports. The data set comprises 4,122 localities and data from 1815 to 2017. Most studies were conducted in the Florestas de Interior (1,510 localities) and Serra do Mar (1,280 localities) biogeographic sub-regions. Considering the three main quantitative methods (mist net, point count, and line transect), we compiled abundance data for 745 species in 576 communities. In the data set, the most frequent species were Basileuterus culicivorus, Cyclaris gujanensis, and Conophaga lineata. There were 71 singletons, such as Lipaugus conditus and Calyptura cristata. We suggest that this small number of records reinforces the critical situation of these taxa in the Atlantic Forest. The information provided in this data set can be used for macroecological studies and to foster conservation strategies in this biodiversity hotspot. No copyright restrictions are associated with the data set. Please cite this Data Paper if data are used in publications and teaching events.

Landscape-level effects on aboveground biomass of tropical forests: A conceptual framework.

Despite the general recognition that fragmentation can reduce forest biomass through edge effects, a systematic review of the literature does not reveal a clear role of edges in modulating biomass loss. Additionally, the edge effects appear to be constrained by matrix type, suggesting that landscape composition has an influence on biomass stocks. The lack of empirical evidence of pervasive edge-related biomass losses across tropical forests highlights the necessity for a general framework linking landscape structure with aboveground biomass. Here, we propose a conceptual model in which landscape composition and configuration mediate the magnitude of edge effects and seed-flux among forest patches, which ultimately has an influence on biomass. Our model hypothesizes that a rapid reduction of biomass can occur below a threshold of forest cover loss. Just below this threshold, we predict that changes in landscape configuration can strongly influence the patch's isolation, thus enhancing biomass loss. Moreover, we expect a synergism between landscape composition and patch attributes, where matrix type mediates the effects of edges on species decline, particularly for shade-tolerant species. To test our conceptual framework, we propose a sampling protocol where the effects of edges, forest amount, forest isolation, fragment size, and matrix type on biomass stocks can be assessed both collectively and individually. The proposed model unifies the combined effects of landscape and patch structure on biomass into a single framework, providing a new set of main drivers of biomass loss in human-modified landscapes. We argue that carbon trading agendas (e.g., REDD+) and carbon-conservation initiatives must go beyond the effects of forest loss and edges on biomass, considering the whole set of effects on biomass related to changes in landscape composition and configuration.

Atlantic forest bird communities provide different but not fewer functions after habitat loss.

Habitat loss often reduces the number of species as well as functional diversity. Dramatic effects to species composition have also been shown, but changes to functional composition have so far been poorly documented, partly owing to a lack of appropriate indices. We here develop three new community indices (i.e. functional integrity, community integrity of ecological groups and community specialization) to investigate how habitat loss affects the diversity and composition of functional traits and species. We used data from more than 5000 individuals of 137 bird species captured in 57 sites in the Brazilian Atlantic Forest, a highly endangered biodiversity hotspot.Results indicate that habitat loss leads to a decrease in functional integrity while measures of functional diversity remain unchanged or are even positively affected. Changes to functional integrity were caused by (i) a decrease in the provisioning of some functions, and an increase in others; (ii) strong within-guild species turnover; and (iii) a replacement of specialists by generalists. Hence, communities from more deforested sites seem to provide different but not fewer functions. We show the importance of investigating changes to both diversity and composition of functional traits and species, as the effects of habitat loss on ecosystem functioning may be more complex than previously thought. Crucially, when only functional diversity is assessed, important changes to ecological functions may remain undetected and negative effects of habitat loss underestimated, thereby imperiling the application of effective conservation actions.

Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives.

The Brazilian Atlantic Forest hosts one of the world's most diverse and threatened tropical forest biota. In many ways, its history of degradation describes the fate experienced by tropical forests around the world. After five centuries of human expansion, most Atlantic Forest landscapes are archipelagos of small forest fragments surrounded by open-habitat matrices. This 'natural laboratory' has contributed to a better understanding of the evolutionary history and ecology of tropical forests and to determining the extent to which this irreplaceable biota is susceptible to major human disturbances. We share some of the major findings with respect to the responses of tropical forests to human disturbances across multiple biological levels and spatial scales and discuss some of the conservation initiatives adopted in the past decade. First, we provide a short description of the Atlantic Forest biota and its historical degradation. Secondly, we offer conceptual models describing major shifts experienced by tree assemblages at local scales and discuss landscape ecological processes that can help to maintain this biota at larger scales. We also examine potential plant responses to climate change. Finally, we propose a research agenda to improve the conservation value of human-modified landscapes and safeguard the biological heritage of tropical forests.

Habitat split as a driver of disease in amphibians.

Anthropogenic habitat disturbance is fundamentally altering patterns of disease transmission and immunity across the vertebrate tree of life. Most studies linking anthropogenic habitat change and disease focus on habitat loss and fragmentation, but these processes often lead to a third process that is equally important: habitat split. Defined as spatial separation between the multiple classes of natural habitat that many vertebrate species require to complete their life cycles, habitat split has been linked to population declines in vertebrates, e.g. amphibians breeding in lowland aquatic habitats and overwintering in fragments of upland terrestrial vegetation. Here, we link habitat split to enhanced disease risk in amphibians (i) by reviewing the biotic and abiotic forces shaping elements of immunity and (ii) through a spatially oriented field study focused on tropical frogs. We propose a framework to investigate mechanisms by which habitat split influences disease risk in amphibians, focusing on three broad host factors linked to immunity: (i) composition of symbiotic microbial communities, (ii) immunogenetic variation, and (iii) stress hormone levels. Our review highlights the potential for habitat split to contribute to host-associated microbiome dysbiosis, reductions in immunogenetic repertoire, and chronic stress, that often facilitate pathogenic infections and disease in amphibians and other classes of vertebrates. We highlight that targeted habitat-restoration strategies aiming to connect multiple classes of natural habitats (e.g. terrestrial-freshwater, terrestrial-marine, marine-freshwater) could enhance priming of the vertebrate immune system through repeated low-load exposure to enzootic pathogens and reduced stress-induced immunosuppression.

Unraveling the drivers of community dissimilarity and species extinction in fragmented landscapes.

Communities in fragmented landscapes are often assumed to be structured by species extinction due to habitat loss, which has led to extensive use of the species-area relationship (SAR) in fragmentation studies. However, the use of the SAR presupposes that habitat loss leads species to extinction but does not allow for extinction to be offset by colonization of disturbed-habitat specialists. Moreover, the use of SAR assumes that species richness is a good proxy of community changes in fragmented landscapes. Here, we assessed how communities dwelling in fragmented landscapes are influenced by habitat loss at multiple scales; then we estimated the ability of models ruled by SAR and by species turnover in successfully predicting changes in community composition, and asked whether species richness is indeed an informative community metric. To address these issues, we used a data set consisting of 140 bird species sampled in 65 patches, from six landscapes with different proportions of forest cover in the Atlantic Forest of Brazil. We compared empirical patterns against simulations of over 8 million communities structured by different magnitudes of the power-law SAR and with species-specific rules to assign species to sites. Empirical results showed that, while bird community composition was strongly influenced by habitat loss at the patch and landscape scale, species richness remained largely unaffected. Modeling results revealed that the compositional changes observed in the Atlantic Forest bird metacommunity were only matched by models with either unrealistic magnitudes of the SAR or by models ruled by species turnover, akin to what would be observed along natural gradients. We show that, in the presence of such compositional turnover, species richness is poorly correlated with species extinction, and z values of the SAR strongly underestimate the effects of habitat loss. We suggest that the observed compositional changes are driven by each species reaching its individual extinction threshold: either a threshold of forest cover for species that disappear with habitat loss, or of matrix cover for species that benefit from habitat loss.

Associations of forest cover, fragment area, and connectivity with neotropical understory bird species richness and abundance.

Theoretical and empirical studies demonstrate that the total amount of forest and the size and connectivity of fragments have nonlinear effects on species survival. We tested how habitat amount and configuration affect understory bird species richness and abundance. We used mist nets (almost 34,000 net hours) to sample birds in 53 Atlantic Forest fragments in southeastern Brazil. Fragments were distributed among 3 10,800-ha landscapes. The remaining forest in these landscapes was below (10% forest cover), similar to (30%), and above (50%) the theoretical fragmentation threshold (approximately 30%) below which the effects of fragmentation should be intensified. Species-richness estimates were significantly higher (F= 3715, p = 0.00) where 50% of the forest remained, which suggests a species occurrence threshold of 30-50% forest, which is higher than usually occurs (<30%). Relations between forest cover and species richness differed depending on species sensitivity to forest conversion and fragmentation. For less sensitive species, species richness decreased as forest cover increased, whereas for highly sensitive species the opposite occurred. For sensitive species, species richness and the amount of forest cover were positively related, particularly when forest cover was 30-50%. Fragment size and connectivity were related to species richness and abundance in all landscapes, not just below the 30% threshold. Where 10% of the forest remained, fragment size was more related to species richness and abundance than connectivity. However, the relation between connectivity and species richness and abundance was stronger where 30% of the landscape was forested. Where 50% of the landscape was forested, fragment size and connectivity were both related to species richness and abundance. Our results demonstrated a rapid loss of species at relatively high levels of forest cover (30-50%). Highly sensitive species were 3-4 times more common above the 30-50% threshold than below it; however, our results do not support a unique fragmentation threshold.

Moving to healthier landscapes: Forest restoration decreases the abundance of Hantavirus reservoir rodents in tropical forests.

Hantavirus Cardiopulmonary Syndrome (HCPS) is a disease with high human lethality rates, whose transmission risk is directly related to the abundance of reservoir rodents. In the Brazilian Atlantic forest, the main reservoirs species, Oligoryzomys nigripes and Necromys lasiurus, are thought to increase in abundance with deforestation. Therefore, forest restoration may contribute to decrease HCPS transmission risk, a topic still unexplored, especially in tropical regions. Aiming at filling this research gap, we quantified the potential of forest restoration, as required by the current environmental legislation, to reduce the abundance of Hantavirus reservoir rodents in the Brazilian Atlantic Forest. Using a dataset on small mammal communities sampled at 104 sites, we modeled how the abundance of these two rodent species change with the percentage of forest cover and forest edge density. From the best model, we extrapolated rodent abundance to the entire Atlantic Forest, considering two scenarios: current and restored forest cover. Comparing the estimated abundance between these two scenarios, we show that forest restoration can reduce the abundance of O. nigripes up to 89.29% in 43.43% of Atlantic forest territory. For N. lasiurus, abundance decreased up to 46% in 44% of the Atlantic forest. To our knowledge, this is the first study linking forest restoration and zoonotic diseases. Our results indicate that forest restoration would decrease the chance of HCPS transmission in ~45% of the Atlantic forest, making the landscape healthier to ~2,8 million people living within this area. This positive effect of restoration on disease regulation should be considered as an additional argument to encourage and promote forest restoration in tropical areas around the world.

Hidden destruction of older forests threatens Brazil's Atlantic Forest and challenges restoration programs.

Understanding the dynamics of native forest loss and gain is critical for biodiversity conservation and ecosystem services, especially in regions experiencing intense forest transformations. We quantified native forest cover dynamics on an annual basis from 1990 to 2017 in Brazil's Atlantic Forest. Despite the relative stability of native forest cover during this period (~28 Mha), the ongoing loss of older native forests, mostly on flatter terrains, have been hidden by the increasing gain of younger native forest cover, mostly on marginal lands for mechanized agriculture. Changes in native forest cover and its spatial distribution increased forest isolation in 36.4% of the landscapes. The clearance of older forests associated with the recut of 27% of younger forests has resulted in a progressive rejuvenation of the native forest cover. We highlight the need to include native forest spatiotemporal dynamics into restoration programs to better estimate their expected benefits and unexpected problems.

Considering landscape-level processes in ecosystem service assessments.

The provision of ecosystem services is inherently spatial. Landscape structure affects service provision through multiple landscape-level processes, such as fragmentation, edge and connectivity effects. These processes can affect areas of ecosystem service supply and demand, and the flows linking those areas. Despite the emergence of sophisticated spatial ecosystem service assessments in the last two decades, we show through a literature review that landscape-level processes are still rarely considered in a comprehensive way. Even when they are considered, landscape effects are mostly limited to landscape composition, and configuration effects are underrepresented. Furthermore, most studies infer ecosystem service provision by only evaluating supply, ignoring demand and flows. Here we present a simple conceptual framework that illustrates how to incorporate landscape-level processes in the assessment of the different components of the service provision chain (supply, demand and flows). Using simulations, we evaluated how estimations of ecosystem service provision change when considering different landscape processes and discussed the implications of disregarding landscape effects. However, to fully implement the framework, a series of challenges linked to mapping and quantifying supply and demand, defining adequate scales of analysis, measuring flows, and parameterizing models for different types of services, still need to be overcome. To promote an adequate use and management of ecosystem services, it is essential to better incorporate landscape processes in ecosystem service assessments. This will lead to more quantitatively accurate and spatially precise estimates.

Offsetting impacts of development on biodiversity and ecosystem services.

Offsetting-trading losses in one place for commensurate gains in another-is a tool used to mitigate environmental impacts of development. Biodiversity and carbon are the most widely used targets of offsets; however, other ecosystem services are increasingly traded, introducing new risks to the environment and people. Here, we provide guidance on how to "trade with minimal trade-offs"- i.e. how to offset impacts on biodiversity without negatively affecting ecosystem services and vice versa. We briefly survey the literature on offsetting biodiversity, carbon and other ecosystem services, revealing that each subfield addresses unique issues (often overlooking those raised by others) and rarely assesses potential trade-offs. We discuss key differences between offsets that trade biodiversity and those that trade ecosystem services, conceptualise links between these different targets in an offsetting context and describe three broad approaches to manage potential trade-offs. We conclude by proposing a research agenda to strengthen the outcomes of offsetting policies that are emerging internationally.

Author Correction: Strategic approaches to restoring ecosystems can triple conservation gains and halve costs.

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

Scenarios and Models to Support Global Conservation Targets.

Global biodiversity targets have far-reaching implications for nature conservation worldwide. Scenarios and models hold unfulfilled promise for ensuring such targets are well founded and implemented; here, we review how they can and should inform the Aichi Targets of the Strategic Plan for Biodiversity and their reformulation. They offer two clear benefits: providing a scientific basis for the wording and quantitative elements of targets; and identifying synergies and trade-offs by accounting for interactions between targets and the actions needed to achieve them. The capacity of scenarios and models to address complexity makes them invaluable for developing meaningful targets and policy, and improving conservation outcomes.

Strategic approaches to restoring ecosystems can triple conservation gains and halve costs.

International commitments for ecosystem restoration add up to one-quarter of the world's arable land. Fulfilling them would ease global challenges such as climate change and biodiversity decline but could displace food production and impose financial costs on farmers. Here, we present a restoration prioritization approach capable of revealing these synergies and trade-offs, incorporating ecological and economic efficiencies of scale and modelling specific policy options. Using an actual large-scale restoration target of the Atlantic Forest hotspot, we show that our approach can deliver an eightfold increase in cost-effectiveness for biodiversity conservation compared with a baseline of non-systematic restoration. A compromise solution avoids 26% of the biome's current extinction debt of 2,864 plant and animal species (an increase of 257% compared with the baseline). Moreover, this solution sequesters 1 billion tonnes of CO2-equivalent (a 105% increase) while reducing costs by US$28 billion (a 57% decrease). Seizing similar opportunities elsewhere would offer substantial contributions to some of the greatest challenges for humankind.

ATLANTIC BIRD TRAITS: a data set of bird morphological traits from the Atlantic forests of South America.

Scientists have long been trying to understand why the Neotropical region holds the highest diversity of birds on Earth. Recently, there has been increased interest in morphological variation between and within species, and in how climate, topography, and anthropogenic pressures may explain and affect phenotypic variation. Because morphological data are not always available for many species at the local or regional scale, we are limited in our understanding of intra- and interspecies spatial morphological variation. Here, we present the ATLANTIC BIRD TRAITS, a data set that includes measurements of up to 44 morphological traits in 67,197 bird records from 2,790 populations distributed throughout the Atlantic forests of South America. This data set comprises information, compiled over two centuries (1820-2018), for 711 bird species, which represent 80% of all known bird diversity in the Atlantic Forest. Among the most commonly reported traits are sex (n = 65,717), age (n = 63,852), body mass (n = 58,768), flight molt presence (n = 44,941), molt presence (n = 44,847), body molt presence (n = 44,606), tail length (n = 43,005), reproductive stage (n = 42,588), bill length (n = 37,409), body length (n = 28,394), right wing length (n = 21,950), tarsus length (n = 20,342), and wing length (n = 18,071). The most frequently recorded species are Chiroxiphia caudata (n = 1,837), Turdus albicollis (n = 1,658), Trichothraupis melanops (n = 1,468), Turdus leucomelas (n = 1,436), and Basileuterus culicivorus (n = 1,384). The species recorded in the greatest number of sampling localities are Basileuterus culicivorus (n = 243), Trichothraupis melanops (n = 242), Chiroxiphia caudata (n = 210), Platyrinchus mystaceus (n = 208), and Turdus rufiventris (n = 191). ATLANTIC BIRD TRAITS (ABT) is the most comprehensive data set on measurements of bird morphological traits found in a biodiversity hotspot; it provides data for basic and applied research at multiple scales, from individual to community, and from the local to the macroecological perspectives. No copyright or proprietary restrictions are associated with the use of this data set. Please cite this data paper when the data are used in publications or teaching and educational activities.

Landscape, Climate and Hantavirus Cardiopulmonary Syndrome Outbreaks.

We performed a literature review in order to improve our understanding of how landscape and climate drivers affect HCPS outbreaks. Anthropogenic landscape changes such as forest loss, fragmentation and agricultural land uses are related with a boost in hantavirus reservoir species abundance and hantavirus prevalence in tropical areas, increasing HCPS risk. Additionally, higher precipitation, especially in arid regions, favors an increase in vegetational biomass, which augments the resources for reservoir rodents, also increasing HCPS risk. Although these relationships were observed, few studies described it so far, and the ones that did it are concentrated in few places. To guide future research on this issue, we build a conceptual model relating landscape and climate variables with HCPS outbreaks and identified research opportunities. We point out the need for studies addressing the effects of landscape configuration, temperature and the interaction between climate and landscape variables. Critical landscape thresholds are also highly relevant, once HCPS risk transmission can increase rapidly above a certain degree of landscape degradation. These studies could be relevant to implement preventive measures, creating landscapes that can mitigate disease spread risk.