Luke O. Frishkoff

Loss of avian phylogenetic diversity in neotropical agricultural systems

Costa Rican birds of a feather lost together Evolutionary history is lost when land is converted for farming, and recently evolved species may cope better with changing land use. Frishkoff et al. compared bird diversity over 12 years in three different kinds of landscape in tropical Central America. They mapped their data onto the bird evolutionary tree and found that more evolutionary branches were lost in intensive agricultural landscapes than in mixed landscapes. In turn, mixed landscapes lost more evolutionary branches than forest reserves. This is not just because of species loss; in fact, mixed agricultural landscapes contained similar numbers of species to those in forest reserves. Evolutionary history is lost because the more evolutionarily distinct species—those with fewer extant relatives and a longer evolutionary history—are more likely to become extinct in agricultural land. Science, this issue p. 1343 Longer branches of the avian phylogenetic tree are disproportionately lost in agricultural landscapes in Costa Rica. Habitat conversion is the primary driver of biodiversity loss, yet little is known about how it is restructuring the tree of life by favoring some lineages over others. We combined a complete avian phylogeny with 12 years of Costa Rican bird surveys (118,127 detections across 487 species) sampled in three land uses: forest reserves, diversified agricultural systems, and intensive monocultures. Diversified agricultural systems supported 600 million more years of evolutionary history than intensive monocultures but 300 million fewer years than forests. Compared with species with many extant relatives, evolutionarily distinct species were extirpated at higher rates in both diversified and intensive agricultural systems. Forests are therefore essential for maintaining diversity across the tree of life, but diversified agricultural systems may help buffer against extreme loss of phylogenetic diversity.

Confronting and resolving competing values behind conservation objectives

Significance Conservationists have become embroiled in debates over different motivations for conserving nature. One path forward is to acknowledge that nature is valued for many reasons and that managing for one objective can fail to achieve others. We categorize conservation objectives and provide a framework for comparing trade-offs between alternative strategies for conserving Costa Rican birds. Specifically, we focus on mitigating species extinction risk, preventing population extirpations, restoring historic assemblages, and conserving evolutionarily unique, culturally significant, and ecosystem-service providing species. Our approach pinpoints strategies for resolving trade-offs and achieving multiple conservation objectives; for example, by maintaining forest cover surrounding tropical farms. These insights demonstrate the advances needed in conservation strategy to design multifunctional interventions. 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.

Agriculture erases climate‐driven β‐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 β-diversity-differences among sites in their species compositions-is critical to forecast communities in the Anthropocene. Here, we study patterns in bird β-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 β-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.

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.

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.

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

Significance Widespread conversion of natural habitats to human land use creates evolutionarily novel environments and causes declines of native species. Stemming biodiversity loss requires an understanding of why some species persist while others decline in these novel habitats. We analyzed survey data of amphibian species from around the globe to determine whether closely related species respond similarly to habitat conversion. We find that species that persist in converted habitats tend to come from the same clades within the amphibian tree of life and that by favoring these widely distributed clades, habitat conversion leads to nonrandom extirpations and loss of evolutionary history. Our results show that the identity of winners and losers during the Anthropocene can be tightly linked to their evolutionary history. 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.

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.

Integrating Over Uncertainty In Spatial Scale Of Response Within Multispecies Occupancy Models Yields More Accurate Assessments Of Community Composition

Species abundance and community composition are affected not only by the local environment, but also by broader landscape and regional context. Yet determining the spatial scale at which landscapes affect species remains a persistent challenge that hinders ecologists’ abilities to understand how environmental gradients influence species presence and shape entire communities, especially in the face of data deficient species and imperfect species detection. Here we present a Bayesian framework that allows uncertainty surrounding the ‘true’ spatial scale of species’ responses (i.e., changes in presence/absence) to be integrated directly into a community hierarchical model. This scale selecting multi-species occupancy model (ssMSOM) estimates the scale of response, and shows high accuracy and correct type I error rates across a broad range of simulation conditions. In contrast, ensembles of single species GLMs frequently fail to detect the correct spatial scale of response, and are often falsely confident in favoring the incorrect spatial scale, especially as species’ detection probabilities deviate from perfect. Integrating spatial scale selection directly into hierarchical community models provides a means of formally testing hypotheses regarding spatial scales of response, and more accurately determining the environmental drivers that shape communities.

Reply to Kirchhoff: Homogenous and mutually exclusive conservation typologies are neither possible nor desirable

Kirchhoff (1) highlights inherent difficulties in organizing the rationales that motivate conservation. The author provides two critiques: first, that our conservation objective typology aggregates conflicting subgoals, and second that the objectives are not mutually exclusive (2). We contend that homogenous and mutually exclusive typologies are neither feasible nor desirable for improving awareness of trade-offs in conservation decisions.