Protected areas slow declines unevenly across the tetrapod tree of life.

Protected areas (PAs) are the primary strategy for slowing terrestrial biodiversity loss. Although expansion of PA coverage is prioritized under the Convention on Biological Diversity, it remains unknown whether PAs mitigate declines across the tetrapod tree of life and to what extent land cover and climate change modify PA effectiveness1,2. Here we analysed rates of change in abundance of 2,239 terrestrial vertebrate populations across the globe. On average, vertebrate populations declined five times more slowly within PAs (-0.4% per year) than at similar sites lacking protection (-1.8% per year). The mitigating effects of PAs varied both within and across vertebrate classes, with amphibians and birds experiencing the greatest benefits. The benefits of PAs were lower for amphibians in areas with converted land cover and lower for reptiles in areas with rapid climate warming. By contrast, the mitigating impacts of PAs were consistently augmented by effective national governance. This study provides evidence for the effectiveness of PAs as a strategy for slowing tetrapod declines. However, optimizing the growing PA network requires targeted protection of sensitive clades and mitigation of threats beyond PA boundaries. Provided the conditions of targeted protection, adequate governance and well-managed landscapes are met, PAs can serve a critical role in safeguarding tetrapod biodiversity.

Publisher Correction: Intensive farming drives long-term shifts in avian community composition.

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

Intensive farming drives long-term shifts in avian community composition.

Agricultural practices constitute both the greatest cause of biodiversity loss and the greatest opportunity for conservation1,2, given the shrinking scope of protected areas in many regions. Recent studies have documented the high levels of biodiversity-across many taxa and biomes-that agricultural landscapes can support over the short term1,3,4. However, little is known about the long-term effects of alternative agricultural practices on ecological communities4,5 Here we document changes in bird communities in intensive-agriculture, diversified-agriculture and natural-forest habitats in 4 regions of Costa Rica over a period of 18 years. Long-term directional shifts in bird communities were evident in intensive- and diversified-agricultural habitats, but were strongest in intensive-agricultural habitats, where the number of endemic and International Union for Conservation of Nature (IUCN) Red List species fell over time. All major guilds, including those involved in pest control, pollination and seed dispersal, were affected. Bird communities in intensive-agricultural habitats proved more susceptible to changes in climate, with hotter and drier periods associated with greater changes in community composition in these settings. These findings demonstrate that diversified agriculture can help to alleviate the long-term loss of biodiversity outside natural protected areas1.

Diversified farms bolster forest-bird populations despite ongoing declines in tropical forests.

While some agricultural landscapes can support wildlife in the short term, it is uncertain how well they can truly sustain wildlife populations. To compare population trends in different production systems, we sampled birds along 48 transects in mature forests, diversified farms, and intensive farms across Costa Rica from 2000 to 2017. To assess how land use influenced population trends in the 349 resident and 80 migratory species with sufficient data, we developed population models. We found, first, that 23% of species were stable in all three land use types, with the rest almost evenly split between increasing and decreasing populations. Second, in forest habitats, a slightly higher fraction was declining: 62% of the 164 species undergoing long-term population changes; nearly half of these declines occurred in forest-affiliated invertivores. Third, in diversified farms, 49% of the 230 species with population changes were declining, with 60% of these declines occurring in agriculture-affiliated species. In contrast, 51% of the species with population changes on diversified farms showed increases, primarily in forest-affiliated invertivores and frugivores. In intensive farms, 153 species showed population changes, also with similar proportions of species increasing (50%) and decreasing (50%). Declines were concentrated in agriculture-affiliated invertivores and forest-affiliated frugivores; increases occurred in many large, omnivorous species. Our findings paint a complex picture but clearly indicate that diversified farming helps sustain populations of diverse, forest-affiliated species. Despite not fully offsetting losses in forest habitats, diversified farming practices help sustain wildlife in a critical time, before possible transformation to nature-positive policies and practices.

Land-use change interacts with island biogeography to alter bird community assembly.

Anthropogenic activities have reshaped biodiversity on islands worldwide. However, it remains unclear how island attributes and land-use change interactively shape multiple facets of island biodiversity through community assembly processes. To answer this, we conducted bird surveys in various land-use types (mainly forest and farmland) using transects on 34 oceanic land-bridge islands in the largest archipelago of China. We found that bird species richness increased with island area and decreased with isolation, regardless of the intensity of land-use change. However, forest-dominated habitats exhibited lower richness than farmland-dominated habitats. Island bird assemblages generally comprised species that share more similar traits or evolutionary histories (i.e. functional and/or phylogenetic clustering) than expected if assemblages were randomly assembled. Contrary to our expectations, we observed that bird assemblages in forest-dominated habitats were more clustered on large and close islands, whereas assemblages in farmland-dominated habitats were more clustered on small islands. These contrasting results indicate that land-use change interacts with island biogeography to alter the community assembly of birds on inhabited islands. Our findings emphasize the importance of incorporating human-modified habitats when examining the community assembly of island biota, and further suggest that agricultural landscapes on large islands may play essential roles in protecting countryside island biodiversity.

3D printed models are an accurate, cost-effective, and reproducible tool for quantifying terrestrial thermal environments.

Predicting ecological responses to rapid environmental change has become one of the greatest challenges of modern biology. One of the major hurdles in forecasting these responses is accurately quantifying the thermal environments that organisms experience. The distribution of temperatures available within an organism's habitat is typically measured using data loggers called operative temperature models (OTMs) that are designed to mimic certain properties of heat exchange in the focal organism. The gold standard for OTM construction in studies of terrestrial ectotherms has been the use of copper electroforming which creates anatomically accurate models that equilibrate quickly to ambient thermal conditions. However, electroformed models require the use of caustic chemicals, are often brittle, and their production is expensive and time intensive. This has resulted in many researchers resorting to the use of simplified OTMs that can yield substantial measurement errors. 3D printing offers the prospect of robust, easily replicated, morphologically accurate, and cost-effective OTMs that capture the benefits but alleviate the problems associated with electroforming. Here, we validate the use of OTMs that were 3D printed using several materials across eight lizard species of different body sizes and living in habitats ranging from deserts to tropical forests. We show that 3D printed OTMs have low thermal inertia and predict the live animal's equilibration temperature with high accuracy across a wide range of body sizes and microhabitats. Finally, we developed a free online repository and database of 3D scans (https://www.3dotm.org/) to increase the accessibility of this tool to researchers around the world and facilitate ease of production of 3D printed models. 3D printing of OTMs is generalizable to taxa beyond lizards. If widely adopted, this approach promises greater accuracy and reproducibility in studies of terrestrial thermal ecology and should lead to improved forecasts of the biological impacts of climate change.

A hierarchical N-mixture model to estimate behavioral variation and a case study of Neotropical birds.

Understanding how and why animals use the environments where they occur is both foundational to behavioral ecology and essential to identify critical habitats for species conservation. However, some behaviors are more difficult to observe than others, which can bias analyses of raw observational data. To our knowledge, no method currently exists to model how animals use different environments while accounting for imperfect behavior-specific detection probability. We developed an extension of a binomial N-mixture model (hereafter the behavior N-mixture model) to estimate the probability of a given behavior occurring in a particular environment while accounting for imperfect detection. We then conducted a simulation to validate the model's ability to estimate the effects of environmental covariates on the probabilities of individuals performing different behaviors. We compared our model to a naïve model that does not account for imperfect detection, as well as a traditional N-mixture model. Finally, we applied the model to a bird observation data set in northwest Costa Rica to quantify how three species behave in forests and farms. Simulations and sensitivity analyses demonstrated that the behavior N-mixture model produced unbiased estimates of behaviors and their relationships with predictor variables (e.g., forest cover, habitat type). Importantly, the behavior N-mixture model accurately characterized uncertainty, unlike the naïve model, which often suggested erroneous effects of covariates on behaviors. When applied to field data, the behavior N-mixture model suggested that Hoffmann's woodpecker (Melanerpes hoffmanii) and Inca dove (Columbina inca) behaved differently in forested versus agricultural habitats, while turquoise-browed motmot (Eumomota superciliosa) did not. Thus, the behavior N-mixture model can help identify habitats that are essential to a species' life cycle (e.g., where individuals nest, forage) that nonbehavioral models would miss. Our model can greatly improve the appropriate use of behavioral survey data and conclusions drawn from them. In doing so, it provides a valuable path forward for assessing the conservation value of alternative habitat types.

A trait-based framework for predicting foodborne pathogen risk from wild birds.

Recent foodborne illness outbreaks have heightened pressures on growers to deter wildlife from farms, jeopardizing conservation efforts. However, it remains unclear which species, particularly birds, pose the greatest risk to food safety. Using >11,000 pathogen tests and 1565 bird surveys covering 139 bird species from across the western United States, we examined the importance of 11 traits in mediating wild bird risk to food safety. We tested whether traits associated with pathogen exposure (e.g., habitat associations, movement, and foraging strategy) and pace-of-life (clutch size and generation length) mediated foodborne pathogen prevalence and proclivities to enter farm fields and defecate on crops. Campylobacter spp. were the most prevalent enteric pathogen (8.0%), while Salmonella and Shiga-toxin producing Escherichia coli (STEC) were rare (0.46% and 0.22% prevalence, respectively). We found that several traits related to pathogen exposure predicted pathogen prevalence. Specifically, Campylobacter and STEC-associated virulence genes were more often detected in species associated with cattle feedlots and bird feeders, respectively. Campylobacter was also more prevalent in species that consumed plants and had longer generation lengths. We found that species associated with feedlots were more likely to enter fields and defecate on crops. Our results indicated that canopy-foraging insectivores were less likely to deposit foodborne pathogens on crops, suggesting growers may be able to promote pest-eating birds and birds of conservation concern (e.g., via nest boxes) without necessarily compromising food safety. As such, promoting insectivorous birds may represent a win-win-win for bird conservation, crop production, and food safety. Collectively, our results suggest that separating crop production from livestock farming may be the best way to lower food safety risks from birds. More broadly, our trait-based framework suggests a path forward for co-managing wildlife conservation and food safety risks in farmlands by providing a strategy for holistically evaluating the food safety risks of wild animals, including under-studied species.

Genetic variation reveals individual-level climate tracking across the annual cycle of a migratory bird.

For migratory species, seasonal movements complicate local climate adaptation, as it is unclear whether individuals track climate niches across the annual cycle. In the migratory songbird yellow warbler (Setophaga petechia), we find a correlation between individual-level wintering and breeding precipitation, but not temperature. Birds wintering in the driest regions of the Neotropics breed in the driest regions of North America. Individuals from drier regions also possess distinct morphologies and population responses to varying rainfall. We find a positive association between bill size and breeding season precipitation which, given documented climate-associated genomic variation, might reflect adaptation to local precipitation regimes. Relative abundance in the breeding range is linked to interannual fluctuations in precipitation, but the directionality of this response varies across geography. Together, our results suggest that variation in climate optima may exist across the breeding range of yellow warblers and provide a mechanism for selection across the annual cycle.

Phylogenetic homogenization of amphibian assemblages in human-altered habitats across the globe.

Habitat conversion is driving biodiversity loss and restructuring species assemblages across the globe. Responses to habitat conversion vary widely, however, and little is known about the degree to which shared evolutionary history underlies changes in species richness and composition. We analyzed data from 48 studies, comprising 438 species on five continents, to understand how taxonomic and phylogenetic diversity of amphibian assemblages shifts in response to habitat conversion. We found that evolutionary history explains the majority of variation in species' responses to habitat conversion, with specific clades scattered across the amphibian tree of life being favored by human land uses. Habitat conversion led to an average loss of 139 million years of amphibian evolutionary history within assemblages, high species and lineage turnover at landscape scales, and phylogenetic homogenization at the global scale (despite minimal taxonomic homogenization). Lineage turnover across habitats was greatest in lowland tropical regions where large species pools and stable climates have perhaps given rise to many microclimatically specialized species. Together, our results indicate that strong phylogenetic clustering of species' responses to habitat conversion mediates nonrandom structuring of local assemblages and loss of global phylogenetic diversity. In an age of rapid global change, identifying clades that are most sensitive to habitat conversion will help prioritize use of limited conservation resources.

Temporally varying disruptive selection in the medium ground finch (Geospiza fortis).

Disruptive natural selection within populations exploiting different resources is considered to be a major driver of adaptive radiation and the production of biodiversity. Fitness functions, which describe the relationships between trait variation and fitness, can help to illuminate how this disruptive selection leads to population differentiation. However, a single fitness function represents only a particular selection regime over a single specified time period (often a single season or a year), and therefore might not capture longer-term dynamics. Here, we build a series of annual fitness functions that quantify the relationships between phenotype and apparent survival. These functions are based on a 9-year mark-recapture dataset of over 600 medium ground finches (Geospiza fortis) within a population bimodal for beak size. We then relate changes in the shape of these functions to climate variables. We find that disruptive selection between small and large beak morphotypes, as reported previously for 2 years, is present throughout the study period, but that the intensity of this selection varies in association with the harshness of environment. In particular, we find that disruptive selection was strongest when precipitation was high during the dry season of the previous year. Our results shed light on climatic factors associated with disruptive selection in Darwin's finches, and highlight the role of temporally varying fitness functions in modulating the extent of population differentiation.

Species-specific responses to habitat conversion across scales synergistically restructure Neotropical bird communities.

Ecologists are increasingly exploring methods for preserving biodiversity in agricultural landscapes. Yet because species vary in how they respond to habitat conversion, ecological communities in agriculture and more natural habitats are often distinct. Unpacking the heterogeneity in species responses to habitat conversion will be essential for predicting and mitigating community shifts. Here, we analyze two years of bird censuses at 150 sites across gradients of local land cover, landscape forest amount and configuration, and regional precipitation in Costa Rica to holistically characterize species responses to habitat conversion. Specifically, we used Poisson-binomial mixture models to (1) delineate groups of species that respond similarly to environmental gradients, (2) explore the relative importance of local vs. landscape-level habitat conversion, and (3) determine how landscape context influences species' local habitat preferences. We found that species fell into six groups: habitat generalists, abundant and rare forest specialists, and three groups of agricultural specialists that differed in their responses to landscape forest cover, fragmentation, and regional precipitation. Birds were most sensitive to local forest cover, but responses were contingent on landscape context. Specifically, forest specialists benefitted most when local forest cover increased in forested landscapes, while habitat generalists exhibited compensatory dynamics, peaking at sites with either local or landscape-level forest, but not both. Our study demonstrates that species responses to habitat conversion are complex but predictable. Characterizing species-level responses to environmental gradients represents a viable approach for forecasting the winners and losers of global change and designing interventions to minimize the ongoing restructuring of Earth's biota.

Agriculture erases climate-driven ß-diversity in Neotropical bird communities.

Earth is experiencing multiple global changes that will, together, determine the fate of many species. Yet, how biological communities respond to concurrent stressors at local-to-regional scales remains largely unknown. In particular, understanding how local habitat conversion interacts with regional climate change to shape patterns in ß-diversity-differences among sites in their species compositions-is critical to forecast communities in the Anthropocene. Here, we study patterns in bird ß-diversity across land-use and precipitation gradients in Costa Rica. We mapped forest cover, modeled regional precipitation, and collected data on bird community composition, vegetation structure, and tree diversity across 120 sites on 20 farms to answer three questions. First, do bird communities respond more strongly to changes in land use or climate in northwest Costa Rica? Second, does habitat conversion eliminate ß-diversity across climate gradients? Third, does regional climate control how communities respond to habitat conversion and, if so, how? After correcting for imperfect detection, we found that local land-use determined community shifts along the climate gradient. In forests, bird communities were distinct between sites that differed in vegetation structure or precipitation. In agriculture, however, vegetation structure was more uniform, contributing to 7%-11% less bird turnover than in forests. In addition, bird responses to agriculture and climate were linked: agricultural communities across the precipitation gradient shared more species with dry than wet forest communities. These findings suggest that habitat conversion and anticipated climate drying will act together to exacerbate biotic homogenization.

Confronting and resolving competing values behind conservation objectives.

Diverse motivations for preserving nature both inspire and hinder its conservation. Optimal conservation strategies may differ radically depending on the objective. For example, creating nature reserves may prevent extinctions through protecting severely threatened species, whereas incentivizing farmland hedgerows may benefit people through bolstering pest-eating or pollinating species. Win-win interventions that satisfy multiple objectives are alluring, but can also be elusive. To achieve better outcomes, we developed and implemented a practical typology of nature conservation framed around seven common conservation objectives. Using an intensively studied bird assemblage in southern Costa Rica as a case study, we applied the typology in the context of biodiversity's most pervasive threat: habitat conversion. We found that rural habitats in a varied tropical landscape, comprising small farms, villages, forest fragments, and forest reserves, provided biodiversity-driven processes that benefit people, such as pollination, seed dispersal, and pest consumption. However, species valued for their rarity, endemism, and evolutionary distinctness declined in farmland. Conserving tropical forest on farmland increased species that international tourists value, but not species discussed in Costa Rican newspapers. Despite these observed trade-offs, our analyses also revealed promising synergies. For example, we found that maintaining forest cover surrounding farms in our study region would likely enhance most conservation objectives at minimal expense to others. Overall, our typology provides a framework for resolving the competing objectives of modern conservation.

Phylogeny, Traits, and Biodiversity of a Neotropical Bat Assemblage: Close Relatives Show Similar Responses to Local Deforestation.

If species' evolutionary pasts predetermine their responses to evolutionarily novel stressors, then phylogeny could predict species survival in an increasingly human-dominated world. To understand the role of phylogenetic relatedness in structuring responses to rapid environmental change, we focused on assemblages of Neotropical bats, an ecologically diverse and functionally important group. We examined how taxonomic and phylogenetic diversity shift between tropical forest and farmland. We then explored the importance of evolutionary history by ascertaining whether close relatives share similar responses to environmental change and which species traits might mediate these trends. We analyzed a 5-year data set (5,011 captures) from 18 sites in a countryside landscape in southern Costa Rica using statistical models that account and correct for imperfect detection of species across sites, spatial autocorrelation, and consideration of spatial scale. Taxonomic and phylogenetic diversity decreased with deforestation, and assemblages became more phylogenetically clustered. Species' responses to deforestation were strongly phylogenetically correlated. Body mass and absolute wing loading explained a substantial portion of species variation in species' habitat preferences, likely related to these traits' influence on maneuverability in cluttered forest environments. Our findings highlight the role that evolutionary history plays in determining which species will survive human impacts and the need to consider diversity metrics, evolutionary history, and traits together when making predictions about species persistence for conservation or ecosystem functioning.

Phylogenetic occupancy models integrate imperfect detection and phylogenetic signal to analyze community structure.

Biological communities are structured phylogenetically-closely related species are typically more likely to be found at the same sites. This may be, in part, because they respond similarly to environmental gradients. Accurately surveying biological communities is, however, made difficult by the fact that detection of species is not perfect. In recent years, numerous statistical methods have been developed that aim to overcome deficiencies in the species detection process. However, these methods do not allow investigators to assess phylogenetic community structure. Here, we introduce the phylogenetic occupancy model (POM), which accounts for imperfect species detection while assessing phylogenetic patterns in community structure. Using simulated data sets we show that the POM grants less biased estimates of phylogenetic structure than models without imperfect detection, and can correctly ascertain the effects of species traits on community composition while accounting for evolutionary non-independence of taxa. Integrating phylogenetic methods into widely used occupancy models will help clarify how evolutionary history influences modern day communities.

Climate change and habitat conversion favour the same species.

Land-use change and climate change are driving a global biodiversity crisis. Yet, how species' responses to climate change are correlated with their responses to land-use change is poorly understood. Here, we assess the linkages between climate and land-use change on birds in Neotropical forest and agriculture. Across > 300 species, we show that affiliation with drier climates is associated with an ability to persist in and colonise agriculture. Further, species shift their habitat use along a precipitation gradient: species prefer forest in drier regions, but use agriculture more in wetter zones. Finally, forest-dependent species that avoid agriculture are most likely to experience decreases in habitable range size if current drying trends in the Neotropics continue as predicted. This linkage suggests a synergy between the primary drivers of biodiversity loss. Because they favour the same species, climate and land-use change will likely homogenise biodiversity more severely than otherwise anticipated.

Thermal niche predicts tolerance to habitat conversion in tropical amphibians and reptiles.

Habitat conversion is a major driver of the biodiversity crisis, yet why some species undergo local extinction while others thrive under novel conditions remains unclear. We suggest that focusing on species' niches, rather than traits, may provide the predictive power needed to forecast biodiversity change. We first examine two Neotropical frog congeners with drastically different affinities to deforestation and document how thermal niche explains deforestation tolerance. The more deforestation-tolerant species is associated with warmer macroclimates across Costa Rica, and warmer microclimates within landscapes. Further, in laboratory experiments, the more deforestation-tolerant species has critical thermal limits, and a jumping performance optimum, shifted ~2 °C warmer than those of the more forest-affiliated species, corresponding to the ~3 °C difference in daytime maximum temperature that these species experience between habitats. Crucially, neither species strictly specializes on either habitat - instead habitat use is governed by regional environmental temperature. Both species track temperature along an elevational gradient, and shift their habitat use from cooler forest at lower elevations to warmer deforested pastures upslope. To generalize these conclusions, we expand our analysis to the entire mid-elevational herpetological community of southern Costa Rica. We assess the climatological affinities of 33 amphibian and reptile species, showing that across both taxonomic classes, thermal niche predicts presence in deforested habitat as well as or better than many commonly used traits. These data suggest that warm-adapted species carry a significant survival advantage amidst the synergistic impacts of land-use conversion and climate change.

Countryside biogeography of Neotropical reptiles and amphibians.

The future of biodiversity and ecosystem services depends largely on the capacity of human-dominated ecosystems to support them, yet this capacity remains largely unknown. Using the framework of countryside biogeography, and working in the Las Cruces system of Coto Brus, Costa Rica, we assessed reptile and amphibian assemblages within four habitats that typify much of the Neotropics: sun coffee plantations (12 sites), pasture (12 sites), remnant forest elements (12 sites), and a larger, contiguous protected forest (3 sites in one forest). Through analysis of 1678 captures of 67 species, we draw four primary conclusions. First, we found that the majority of reptile (60%) and amphibian (70%) species in this study used an array of habitat types, including coffee plantations and actively grazed pastures. Second, we found that coffee plantations and pastures hosted rich, albeit different and less dense, reptile and amphibian biodiversity relative to the 326-ha Las Cruces Forest Reserve and neighboring forest elements. Third, we found that the small ribbons of "countryside forest elements" weaving through farmland collectively increased the effective size of a 326-ha local forest reserve 16-fold for reptiles and 14-fold for amphibians within our 236-km2 study area. Therefore, countryside forest elements, often too small for most remote sensing techniques to identify, are contributing -95% of the available habitat for forest-dependent reptiles and amphibians in our largely human-dominated study region. Fourth, we found large and pond-reproducing amphibians to prefer human-made habitats, whereas small, stream-reproducing, and directly developing species are more dependent on forest elements. Our investigation demonstrates that tropical farming landscapes can support substantial reptile and amphibian biodiversity. Our approach provides a framework for estimating the conservation value of the complex working landscapes that constitute roughly half of the global land surface, and which are experiencing intensification pressure worldwide.

Nonrandom extinction patterns can modulate pest control service decline.

Changes in biodiversity will mediate the consequences of agricultural intensification and expansion for ecosystem services. Regulating services, like pollination and pest control, generally decline with species loss. In nature, however, relationships between service provision and species richness are not always strong, partially because anthropogenic disturbances purge species from communities in nonrandom orders. The same traits that make for effective service providers may also confer resistance or sensitivity to anthropogenic disturbances, which may either temper or accelerate declines in service provision with species loss. We modeled a community of predators interacting with insect pest prey, and identified the contexts in which pest control provision was most sensitive to species loss. We found pest populations increased rapidly when functionally unique and dietary-generalist predators were lost first, with up to 20% lower pest control provision than random loss. In general, pest abundance increased most in the scenarios that freed more pest species from predation. Species loss also decreased the likelihood that the most effective service providers were present. In communities composed of species with identical traits, predators were equally effective service providers and, when competing predators went extinct, remaining community members assumed their functional roles. In more realistic trait-diverse communities, predators differed in pest control efficacy, and remaining predators could not fully compensate for the loss of their competitors, causing steeper declines in pest control provision with predator species loss. These results highlight diet breadth in particular as a key predictor of service provision, as it affects both the way species respond to and alter their environments. More generally, our model provides testable hypotheses for predicting how nonrandom species loss alters relationships between biodiversity and pest control provision.