A cloudy forecast for species distribution models: Predictive uncertainties abound for California birds after a century of climate and land-use change.

Correlative species distribution models are widely used to quantify past shifts in ranges or communities, and to predict future outcomes under ongoing global change. Practitioners confront a wide range of potentially plausible models for ecological dynamics, but most specific applications only consider a narrow set. Here, we clarify that certain model structures can embed restrictive assumptions about key sources of forecast uncertainty into an analysis. To evaluate forecast uncertainties and our ability to explain community change, we fit and compared 39 candidate multi- or joint species occupancy models to avian incidence data collected at 320 sites across California during the early 20th century and resurveyed a century later. We found massive (>20,000 LOOIC) differences in within-time information criterion across models. Poorer fitting models omitting multivariate random effects predicted less variation in species richness changes and smaller contemporary communities, with considerable variation in predicted spatial patterns in richness changes across models. The top models suggested avian environmental associations changed across time, contemporary avian occupancy was influenced by previous site-specific occupancy states, and that both latent site variables and species associations with these variables also varied over time. Collectively, our results recapitulate that simplified model assumptions not only impact predictive fit but may mask important sources of forecast uncertainty and mischaracterize the current state of system understanding when seeking to describe or project community responses to global change. We recommend that researchers seeking to make long-term forecasts prioritize characterizing forecast uncertainty over seeking to present a single best guess. To do so reliably, we urge practitioners to employ models capable of characterizing the key sources of forecast uncertainty, where predictors, parameters and random effects may vary over time or further interact with previous occurrence states.

Reference genome of the Virginia rail, Rallus limicola.

The Virginia rail, Rallus limicola, is a member of the family Rallidae, which also includes many other species of secretive and poorly studied wetland birds. It is recognized as a single species throughout its broad distribution in North America where it is exploited as a game bird, often with generous harvest limits, despite a lack of systematic population surveys and evidence of declines in many areas due to wetland loss and degradation. To help advance understanding of the phylogeography, biology, and ecology of this elusive species, we report the first reference genome assembly for the Virginia rail, produced as part of the California Conservation Genomics Project (CCGP). We produced a de novo genome assembly using Pacific Biosciences HiFi long reads and Hi-C chromatin-proximity sequencing technology with an estimated sequencing error rate of 0.191%. The assembly consists of 1,102 scaffolds spanning 1.39 Gb, with a contig N50 of 11.0 Mb, scaffold N50 of 25.3 Mb, largest contig of 45 Mb, and largest scaffold of 128.4 Mb. It has a high BUSCO completeness score of 96.9% and represents the first genome assembly available for the genus Rallus. This genome assembly will help resolve questions about the complex evolutionary history of rails and evaluate the potential of rails for adaptive evolution in the face of growing threats from climate change and habitat loss and fragmentation. It will also provide a valuable resource for rail conservation efforts by quantifying Virginia rail vagility, population connectivity, and effective population sizes.

Reference genome of the black rail, Laterallus jamaicensis.

The black rail, Laterallus jamaicensis, is one of the most secretive and poorly understood birds in the Americas. Two of its five subspecies breed in North America: the Eastern black rail (L. j. jamaicensis), found primarily in the southern and mid-Atlantic states, and the California black rail (L. j. coturniculus), inhabiting California and Arizona, are recognized across the highly disjunct distribution. Population declines, due primarily to wetland loss and degradation, have resulted in conservation status listings for both subspecies. To help advance understanding of the phylogeography, biology, and ecology of this elusive species, we report the first reference genome assembly for the black rail, produced as part of the California Conservation Genomics Project (CCGP). We produced a de novo genome assembly using Pacific Biosciences HiFi long reads and Hi-C chromatin-proximity sequencing technology with an estimated sequencing error rate of 0.182%. The assembly consists of 964 scaffolds spanning 1.39 Gb, with a contig N50 of 7.4 Mb, scaffold N50 of 21.4 Mb, largest contig of 44.8 Mb, and largest scaffold of 101.2 Mb. The assembly has a high BUSCO completeness score of 96.8% and represents the first genome assembly available for the genus Laterallus. This genome assembly can help resolve questions about the complex evolutionary history of rails, assess black rail vagility and population connectivity, estimate effective population sizes, and evaluate the potential of rails for adaptive evolution in the face of growing threats from climate change, habitat loss and fragmentation, and disease.

Concordant and opposing effects of climate and land-use change on avian assemblages in California's most transformed landscapes.

Climate and land-use change could exhibit concordant effects that favor or disfavor the same species, which would amplify their impacts, or species may respond to each threat in a divergent manner, causing opposing effects that moderate their impacts in isolation. We used early 20th century surveys of birds conducted by Joseph Grinnell paired with modern resurveys and land-use change reconstructed from historic maps to examine avian change in Los Angeles and California's Central Valley (and their surrounding foothills). Occupancy and species richness declined greatly in Los Angeles from urbanization, strong warming (+1.8°C), and drying (-77.2 millimeters) but remained stable in the Central Valley, despite large-scale agricultural development, average warming (+0.9°C), and increased precipitation (+11.2 millimeters). While climate was the main driver of species distributions a century ago, the combined impacts of land-use and climate change drove temporal changes in occupancy, with similar numbers of species experiencing concordant and opposing effects.

Adult sex ratios: causes of variation and implications for animal and human societies.

Converging lines of inquiry from across the social and biological sciences target the adult sex ratio (ASR; the proportion of males in the adult population) as a fundamental population-level determinant of behavior. The ASR, which indicates the relative number of potential mates to competitors in a population, frames the selective arena for competition, mate choice, and social interactions. Here we review a growing literature, focusing on methodological developments that sharpen knowledge of the demographic variables underlying ASR variation, experiments that enhance understanding of the consequences of ASR imbalance across societies, and phylogenetic analyses that provide novel insights into social evolution. We additionally highlight areas where research advances are expected to make accelerating contributions across the social sciences, evolutionary biology, and biodiversity conservation.

Stability of patch-turnover relationships under equilibrium and nonequilibrium metapopulation dynamics driven by biogeography.

Two controversial tenets of metapopulation biology are whether patch quality and the surrounding matrix are more important to turnover (colonisation and extinction) than biogeography (patch area and isolation) and whether factors governing turnover during equilibrium also dominate nonequilibrium dynamics. We tested both tenets using 18 years of surveys for two secretive wetland birds, black and Virginia rails, during (1) a period of equilibrium with stable occupancy and (2) after drought and arrival of West Nile Virus (WNV), which resulted in WNV infections in rails, increased extinction and decreased colonisation probabilities modified by WNV, nonequilibrium dynamics for both species and occupancy decline for black rails. Area (primarily) and isolation (secondarily) drove turnover during both stable and unstable metapopulation dynamics, greatly exceeding the effects of patch quality and matrix conditions. Moreover, slopes between turnover and patch characteristics changed little between equilibrium and nonequilibrium, confirming the overriding influences of biogeographic factors on turnover.

Thermal adaptation of pelage in desert rodents balances cooling and insulation.

Phenotypic convergence across distantly related taxa can be driven by similar selective pressures from the environment or intrinsic constraints. The roles of these processes on physiological strategies, such as homeothermy, are poorly understood. We studied the evolution of thermal properties of mammalian pelage in a diverse community of rodents inhabiting the Mojave Desert, USA. We used a heat flux device to measure the thermal insulation of museum specimens and determined whether thermal properties were associated with habitat preferences while assessing phylogenetic dependence. Species that prefer arid habitats exhibited lower conductivity and thinner pelage relative to species with other habitat preferences. Despite being thinner, the pelage of arid species exhibited comparable insulation to the pelage of the other species due to its lower conductivity. Thus, arid species have insulative pelage while simultaneously benefitting from thin pelage that promotes convective cooling. We found no evidence of intrinsic constraints or phylogenetic dependence, indicating pelage readily evolves to environmental pressures. Thermoregulatory simulations demonstrated that arid specialists reduced energetic costs required for homeothermy by 14.5% by evolving lower conductivity, providing support for adaptive evolution of pelage. Our study indicates that selection for lower energetic requirements of homeothermy has shaped evolution of pelage thermal properties.

Hardship at birth alters the impact of climate change on a long-lived predator.

Climate change is increasing the frequency of extreme events, such as droughts or hurricanes, with substantial impacts on human and wildlife communities. Extreme events can affect individuals through two pathways: by altering the fitness of adults encountering a current extreme, and by affecting the development of individuals born during a natal extreme, a largely overlooked process. Here, we show that the impact of natal drought on an avian predator overrode the effect of current drought for decades, so that individuals born during drought were disadvantaged throughout life. Incorporation of natal effects caused a 40% decline in forecasted population size and a 21% shortening of time to extinction. These results imply that climate change may erode populations more quickly and severely than currently appreciated, suggesting the urgency to incorporate "penalties" for natal legacies in the analytical toolkit of impact forecasts. Similar double impacts may apply to other drivers of global change.

Vocal babbling in a wild parrot shows life history and endocrine affinities with human infants.

Prelinguistic babbling is a critical phase in infant language development and is best understood in temperate songbirds where it occurs primarily in males at reproductive maturity and is modulated by sex steroids. Parrots of both sexes are icons of tropical vocal plasticity, but vocal babbling is unreported in this group and whether the endocrine system is involved is unknown. Here we show that vocal babbling is widespread in a wild parrot population in Venezuela, ensues in both sexes during the nestling stage, occurs amidst a captive audience of mixed-aged siblings, and is modulated by corticosteroids. Spectrographic analysis and machine learning found phoneme diversity and combinatorial capacity increased precipitously for the first week, thereafter, crystalizing into a smaller repertoire, consistent with the selective attrition model of language development. Corticosterone-treated nestlings differed from unmanipulated birds and sham controls in several acoustic properties and crystallized a larger repertoire post-treatment. Our findings indicate babbling occurs during an early life-history stage in which corticosteroids help catalyse the transition from a universal learning programme to one finely tuned for the prevailing ecological environment, a potentially convergent scenario in human prelinguistic development.

Keeping your cool: thermoregulatory performance and plasticity in desert cricetid rodents.

Small mammals in hot deserts often avoid heat via nocturnality and fossoriality, and are thought to have a limited capacity to dissipate heat using evaporative cooling. Research to date has focused on thermoregulatory responses to air temperatures (Ta) below body temperature (Tb). Consequently, the thermoregulatory performance of small mammals exposed to high Ta is poorly understood, particularly responses across geographic and seasonal scales. We quantified the seasonal thermoregulatory performance of four cricetid rodents (Neotoma albigula, Neotoma lepida, Peromyscus eremicus, Peromyscus crinitus) exposed to high Ta, at four sites in the Mojave Desert. We measured metabolism, evaporative water loss and Tb using flow-through respirometry. When exposed to Ta≥Tb, rodents showed steep increases in Tb, copious salivation and limited evaporative heat dissipation. Most individuals were only capable of maintaining Ta-Tb gradients of ∼1°, resulting in heat tolerance limits (HTLs) in the range Ta=43-45°C. All species exhibited a thermoneutral Tb of ∼35-36°C, and Tb increased to maximal levels of ∼43°C. Metabolic rates and rates of evaporative water loss increased steeply in all species as Ta approached Tb. We also observed significant increases in resting metabolism and evaporative water loss from summer to winter at Ta within and above the thermoneutral zone. In contrast, we found few differences in the thermoregulatory performance within species across sites. Our results suggest that cricetid rodents have a limited physiological capacity to cope with environmental temperatures that exceed Tb and that a rapidly warming environment may increasingly constrain their nocturnal activity.

In transition: Avian biogeographic responses to a century of climate change across desert biomes.

Transition zones between biomes, also known as ecotones, are areas of pronounced ecological change. They are primarily maintained by abiotic factors and disturbance regimes that could hinder or promote species range shifts in response to climate change. We evaluated how climate change has affected metacommunity dynamics in two adjacent biomes and across their ecotone by resurveying 106 sites that were originally surveyed for avian diversity in the early 20th century by Joseph Grinnell and colleagues. The Mojave, a warm desert, and the Great Basin, a cold desert, have distinct assemblages and meet along a contiguous, east-west boundary. Both deserts substantially warmed over the past century, but the Mojave dried while the Great Basin became wetter. We examined whether the distinctiveness and composition of desert avifaunas have changed, if species distributions shifted, and how the transition zone impacted turnover patterns. Avifauna change was characterized by (a) reduced occupancy, range contractions, and idiosyncratic species redistributions; (b) degradation of historic community structure, and increased taxonomic and climatic differentiation of the species inhabiting the two deserts; and (c) high levels of turnover at the transition zone but little range expansion of species from the warm, dry Mojave into the cooler, wetter Great Basin. Although both deserts now support more drier and warmer tolerant species, their bird communities still occupy distinct climatological space and differ significantly in climatic composition. Our results suggest a persistent transition zone between biomes contributes to limiting the redistribution of birds, and highlight the importance of understanding how transition zone dynamics impact responses to climate change.

The rescue effect and inference from isolation-extinction relationships.

The rescue effect in metapopulations hypothesises that less isolated patches are unlikely to go extinct because recolonisation may occur between breeding seasons ('recolonisation rescue'), or immigrants may sufficiently bolster population size to prevent extinction altogether ('demographic rescue'). These mechanisms have rarely been demonstrated directly, and most evidence of the rescue effect is from relationships between isolation and extinction. We determined the frequency of recolonisation rescue for metapopulations of black rails (Laterallus jamaicensis) and Virginia rails (Rallus limicola) from occupancy surveys conducted during and between breeding seasons, and assessed the reliability of inferences about the occurrence of rescue drawn from isolation-extinction relationships, including autologistic isolation measures that corrected for unsurveyed patches and imperfect detection. Recolonisation rescue occurred at expected rates, but was elevated during periods of disturbance that resulted in non-equilibrium metapopulation dynamics. Inferences from extinction-isolation relationships were unreliable, particularly for autologistic measures and for the more vagile Virginia rail.

Cooling requirements fueled the collapse of a desert bird community from climate change.

Climate change threatens global biodiversity by increasing extinction risk, yet few studies have uncovered a physiological basis of climate-driven species declines. Maintaining a stable body temperature is a fundamental requirement for homeothermic animals, and water is a vital resource that facilitates thermoregulation through evaporative cooling, especially in hot environments. Here, we explore the potential for thermoregulatory costs to underlie the community collapse of birds in the Mojave Desert over the past century in response to climate change. The probability of persistence was lowest for species occupying the warmest and driest sites, which imposed the greatest cooling costs. We developed a general model of heat flux to evaluate whether water requirements for evaporative cooling contributed to species' declines by simulating thermoregulatory costs in the Mojave Desert for 50 bird species representing the range of observed declines. Bird species' declines were positively associated with climate-driven increases in water requirements for evaporative cooling and exacerbated by large body size, especially for species with animal-based diets. Species exhibiting reductions in body size across their range saved up to 14% in cooling costs and experienced less decline than species without size reductions, suggesting total cooling costs as a mechanism underlying Bergmann's rule. Reductions in body size, however, are unlikely to offset the 50 to 78% increase in cooling costs threatening desert birds from future climate change. As climate change spreads warm, dry conditions across the planet, water requirements are increasingly likely to drive population declines, providing a physiological basis for climate-driven extinctions.

Ontogeny of the adrenocortical response in an extremely altricial bird.

Life history theory predicts that physiological and behavioral responsiveness to stress should be delayed in development until the benefits of heightened reactivity outweigh the costs of potentially chronic glucocorticoid levels. Birds often acquire stress-responsiveness at locomotor independence, however, both stress-responsiveness and locomotor ability are delayed in birds with altricial developmental strategies. Parrots (Psittacidae) are extremely altricial, but it is not known whether they also postpone physiological responsiveness to stress until locomotor independence. We quantified individual variation in baseline and stress-induced plasma corticosterone (CORT) concentrations, the main avian glucocorticoid, in wild green-rumped parrotlets (Forpus passerinus) of Venezuela at four stages of nestling development. Parrotlet neonates are very underdeveloped and compete for parental care among extreme sibling size hierarchies, a competitive scenario that might benefit from early hypothalamic-pituitary-adrenal (HPA) functionality. Nestlings that underwent a standardized restraint stress-treatment showed higher average CORT concentrations compared to baseline in all age groups sampled, and exhibited no evidence of age-related changes in the stress response. This is 2 weeks before locomotor independence and earlier than previously documented for altricial species. Results suggest that precocity of HPA function may be advantageous to growth and survivorship in extremely altricial birds.

Integrating social and ecological data to model metapopulation dynamics in coupled human and natural systems.

Understanding how metapopulations persist in dynamic working landscapes requires assessing the behaviors of key actors that change patches as well as intrinsic factors driving turnover. Coupled human and natural systems (CHANS) research uses a multidisciplinary approach to identify the key actors, processes, and feedbacks that drive metapopulation and landscape dynamics. We describe a framework for modeling metapopulations in CHANS that integrates ecological and social data by coupling stochastic patch occupancy models of metapopulation dynamics with agent-based models of land-use change. We then apply this framework to metapopulations of the threatened black rail (Laterallus jamaicensis) and widespread Virginia rail (Rallus limicola) that inhabit patchy, irrigation-fed wetlands in the rangelands of the California Sierra Nevada foothills. We collected data from five diverse sources (rail occupancy surveys, land-use change mapping, a survey of landowner decision making, climate and reservoir databases, and mosquito trapping and West Nile virus testing) and integrated them into an agent-based stochastic patch occupancy model. We used the model to (1) quantify the drivers of metapopulation dynamics, and the potential interactions and feedbacks among them; (2) test predictions of the behavior of metapopulations in dynamic working landscapes; and (3) evaluate the impact of three policy options on metapopulation persistence (irrigation district water cutbacks during drought, incentives for landowners to create wetlands, and incentives for landowners to protect wetlands). Complex metapopulation dynamics emerged when landscapes functioned as CHANS, highlighting the importance of integrating human activities and other ecological processes into metapopulation models. Rail metapopulations were strongly top-down regulated by precipitation, and the black rail's decade-long decline was caused by the combination of West Nile virus and drought. Theoretical predictions of the two metapopulations' responses to dynamic landscapes and incentive programs were complicated by heterogeneity in patch quality and CHANS couplings, respectively. Irrigation cutbacks during drought posed a serious extinction risk that neither incentive policy effectively ameliorated.

A century of climate and land-use change cause species turnover without loss of beta diversity in California's Central Valley.

Climate and land-use changes are thought to be the greatest threats to biodiversity, but few studies have directly measured their simultaneous impacts on species distributions. We used a unique historic resource-early 20th-century bird surveys conducted by Joseph Grinnell and colleagues-paired with contemporary resurveys a century later to examine changes in bird distributions in California's Central Valley, one of the most intensively modified agricultural zones in the world and a region of heterogeneous climate change. We analyzed species- and community-level occupancy using multispecies occupancy models that explicitly accounted for imperfect detection probability, and developed a novel, simulation-based method to compare the relative influences of climate and land-use covariates on site-level species richness and beta diversity (measured by Jaccard similarity). Surprisingly, we show that mean occupancy, species richness and between-site similarity have remained remarkably stable over the past century. Stability in community-level metrics masked substantial changes in species composition; occupancy declines of some species were equally matched by increases in others, predominantly species with generalist or human-associated habitat preferences. Bird occupancy, richness and diversity within each era were driven most strongly by water availability (precipitation and percent water cover), indicating that both climate and land-use are important drivers of species distributions. Water availability had much stronger effects than temperature, urbanization and agricultural cover, which are typically thought to drive biodiversity decline.

Collapse of a desert bird community over the past century driven by climate change.

Climate change has caused deserts, already defined by climatic extremes, to warm and dry more rapidly than other ecoregions in the contiguous United States over the last 50 years. Desert birds persist near the edge of their physiological limits, and climate change could cause lethal dehydration and hyperthermia, leading to decline or extirpation of some species. We evaluated how desert birds have responded to climate and habitat change by resurveying historic sites throughout the Mojave Desert that were originally surveyed for avian diversity during the early 20th century by Joseph Grinnell and colleagues. We found strong evidence of an avian community in collapse. Sites lost on average 43% of their species, and occupancy probability declined significantly for 39 of 135 breeding birds. The common raven was the only native species to substantially increase across survey sites. Climate change, particularly decline in precipitation, was the most important driver of site-level persistence, while habitat change had a secondary influence. Habitat preference and diet were the two most important species traits associated with occupancy change. The presence of surface water reduced the loss of site-level richness, creating refugia. The collapse of the avian community over the past century may indicate a larger imbalance in the Mojave and provide an early warning of future ecosystem disintegration, given climate models unanimously predict an increasingly dry and hot future.

Validating dispersal distances inferred from autoregressive occupancy models with genetic parentage assignments.

Dispersal distances are commonly inferred from occupancy data but have rarely been validated. Estimating dispersal from occupancy data is further complicated by imperfect detection and the presence of unsurveyed patches. We compared dispersal distances inferred from seven years of occupancy data for 212 wetlands in a metapopulation of the secretive and threatened California black rail (Laterallus jamaicensis coturniculus) to distances between parent-offspring dyads identified with 16 microsatellites. We used a novel autoregressive multi-season occupancy model that accounted for both unsurveyed patches and imperfect detection to quantify patch isolation using buffer radius (BRM) and incidence function (IFM) connectivity measures at 15 scales (1-10, 15, 20, 25, and 30 km). Connectivity measures were then fit as colonization covariates in occupancy models to estimate a model-averaged dispersal distance. As predicted, colonization was more strongly related to connectivity at small spatial scales (<10 km). AIC weights were greatest at 7 km for BRM and at 4 km for IFM. Model-averaged dispersal distances (BRM = 7.46 km; IFM = 5.48 km) showed good agreement with the mean M(±SE) dispersal distance from 23 parent-offspring dyads (5.58 ± 1.92 km), indicating reasonably accurate mean dispersal distances can be inferred from occupancy data when isolation strongly affects colonization.