The global biodiversity crisis demands targeted conservation strategies that maximize impact despite limited resources. Surrogate species approaches, particularly using umbrella, keystone, and flagship species, offer practical targets for conservation planning that may indirectly benefit ecosystems. However, selecting target species is often hindered by conceptual ambiguities and inconsistent methodologies. To address these challenges, we present an integrative framework that systematically identifies effective surrogate species through MultiCriteria Decision Analysis (MCDA) combined with big data. Our framework quantifies each species' conservation potential using three indices: an Umbrella index, a Keystone index, and a Flagship index. The Umbrella index assesses habitat overlap using Area of Habitat (AOH) data, the Keystone index is calculated through a network analysis of predator-prey relationships, and the Flagship index analyzes public interest via Google Trends and Baidu Index. These indices are integrated into a composite Effectiveness index using the Multi-Attribute Utility Theory (MAUT) model, with sensitivity analysis to evaluate the robustness of species rankings. We applied this framework to Three-River-Source National Park in the Qinghai-Tibetan Plateau. Our results identified the snow leopard (Panthera uncia) as the most effective surrogate species among mammals, ranking first in both the Flagship and Keystone indices, and tenth in the Umbrella index, leading to its top position in the composite Effectiveness index. This data-driven, transparent approach enhances objectivity in surrogate species selection, promising more strategic and impactful biodiversity conservation efforts worldwide.
Infanticide and adoption have been attributed to sexual selection, where an individual later reproduces with the parent whose offspring it killed or adopted. While sexually selected infanticide is well known, evidence for sexually selected adoption is anecdotal. We report on both behaviors at 346 nests over 27 y in green-rumped parrotlets ( Forpus passerinus ) in Venezuela. Parrotlets are monogamous with long-term pair bonds, exhibit a strongly male-biased adult sex ratio, and nest in cavities that are in short supply, creating intense competition for nest sites and mates. Infanticide attacks occurred at 256 nests in two distinct contexts: 1) Attacks were primarily committed by nonbreeding pairs (69%) attempting to evict parents from the cavity. Infanticide attacks per nest were positively correlated with population size and evicting pairs never adopted abandoned offspring. Competition for limited nest sites was a primary cause of eviction-driven infanticide, and 2) attacks occurred less frequently at nests where one mate died (31%), was perpetrated primarily by stepparents of both sexes, and was independent of population size. Thus, within a single species and mating system, infanticide occurred in multiple contexts due to multiple drivers. Nevertheless, 48% of stepparents of both sexes adopted offspring, and another 23% of stepfathers exhibited both infanticide and long-term care. Stepfathers were often young males who subsequently nested with widows, reaching earlier ages of first breeding than competitors and demonstrating sexually selected adoption. Adoption and infanticide conferred similar fitness benefits to stepfathers and appeared to be equivalent strategies driven by limited breeding opportunities, male-biased sex ratios, and long-term monogamy.
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.
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.
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.
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.
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.
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.
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. A detailed Review across animal and human societies provides insight on the causes and consequences of adult sex ratio skew.
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.
ABSTRACT 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.
We examine the evidence linking species' traits to contemporary range shifts and find they are poor predictors of range shifts that have occurred over decades to a century. We then discuss reasons for the poor performance of traits for describing interspecific variation in range shifts from two perspectives: (a) factors associated with species' traits that degrade range-shift signals stemming from the measures used for species' traits, traits that are typically not analyzed, and the influence of phylogeny on range-shift potential and (b) issues in quantifying range shifts and relating them to species' traits due to imperfect detection of species, differences in the responses of altitudinal and latitudinal ranges, and emphasis on testing linear relationships between traits and range shifts instead of nonlinear responses. Improving trait-based approaches requires a recognition that traits within individuals interact in unexpected ways and that different combinations of traits may be functionally equivalent.
Theory posits that resilience of ecosystems increases when there is a diversity of agents (e.g., species) and linkages between them. If ecosystems are conceptualized as components of coupled human and natural systems, then a corollary would be that novel types of human-induced diversity may also foster resilience. We explored this hypothesis by studying how socially created diversity mediated the impact of a historically severe drought on a network of wetlands in the foothills of the California Sierra Nevada containing a metapopulation of the threatened California Black Rail (Laterallus jamaicensis coturniculus). We examined how (1) diversity in motivations for land ownership affected use of irrigation water and response to drought; (2) differences in natural and irrigated water sources affected wetland drying in response to drought; and (3) these processes affected the persistence of rails and the transmission risk of West Nile virus (WNV), an emerging infectious disease that threatens people and rails. Wetlands were mostly fed by inefficiencies and leaks from the irrigation system. Wetlands with both natural and irrigated water sources were larger, wetter, and likelier to persist through drought because these two sources showed response diversity by drying at different times. Wetlands with diverse water sources also provided the best habitat for the California Black Rail, and irrigation appeared responsible for its persistence through the drought. Irrigation increased WNV transmission risk by increasing the quantity, but not the quality, of wetland habitats for mosquitoes. The impacts of social diversity were more ambiguous, with redundancy prevalent. However, profit-motivated landowners provided wetlands more irrigation during nondrought conditions, whereas other landowner types were more likely to continue providing irrigation during drought. Our results highlight that conservation in social-ecological systems requires assessing not only the value of historic ecological diversity, but also how novel types of socially induced diversity may benefit ecosystems.
High exposure to warming from climate change is expected to threaten biodiversity by pushing many species toward extinction. Such exposure is often assessed for all taxa at a location from climate projections, yet species have diverse strategies for buffering against temperature extremes. We compared changes in species occupancy and site-level richness of small mammal and bird communities in protected areas of the Mojave Desert using surveys spanning a century. Small mammal communities remained remarkably stable, whereas birds declined markedly in response to warming and drying. Simulations of heat flux identified different exposure to warming for birds and mammals, which we attribute to microhabitat use. Estimates from climate projections are unlikely to accurately reflect species' exposure without accounting for the effects of microhabitat buffering on heat flux.
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.
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.
Endotherms dissipate heat to the environment to maintain a stable body temperature at high ambient temperatures, which requires them to maintain a balance between heat dissipation and water conservation. Birds are relatively small, contain a large amount of metabolically expensive tissue, and are mostly diurnal, making them susceptible to physiological challenges related to water balance and heat dissipation. We compiled total evaporative water loss (TEWL) measurements for 174 species of birds exposed to different temperatures and used comparative methods to examine their relationships with body size, ambient temperature, precipitation, diet, and diel activity cycle. TEWL in the thermoneutral zone (TNZ) was associated primarily with body mass and activity phase. Larger and more active-phase birds, with their higher metabolic rates, lost more water through evaporation than smaller, resting-phase birds, particularly at higher thermal exposures. However, maximum temperature of the natural habitat became an important determinant of TEWL when birds were exposed to temperatures exceeding the TNZ. Species from hotter climates exhibited higher TEWL. Adaptation to arid climates did not restrict evaporative water loss at thermal conditions within the TNZ, but promoted evaporative water loss at exposures above the TNZ. The TEWL of granivores, which ingest food with low water content, differed little from species with other food habitats under all thermal conditions. The effects of environmental covariates of TEWL were dissimilar across thermal exposures, suggesting no evidence for a tradeoff between water conservation in the TNZ and heat dissipation at exposure to higher temperatures. Thus, birds may be able to acclimate when climate change results in the need to increase heat dissipation due to warming, except perhaps in hot, arid environments where species will need to depend heavily upon evaporative cooling to maintain homeothermy.
We studied growth in the Green-rumped Parrotlet (Forpus passerinus), a small Neotropical parrotlet that has an unusually long nestling period (28-35 days) and feeds nestlings nutritionally poor seeds. We asked why nestlings grow slowly even though nest predation is their main mortality factor. We examined nutrient accretion and the development of thermoregulation and computed an energy budget until fledging. We described three periods of growth: (1) days 1-13, when peak accretion for sodium, lipids, and energy occurred; (2) days 14-22, when nestlings became endothermic and accretion for proteins, calcium, and phosphorus peaked; and (3) days 23-30, when nestlings reached 90% of the asymptotic values of body components. The deposition rate of lipids (logistic constant K = 0.33) was higher than that of protein (K = 0.19), ash and calcium (K = 0.20), and, particularly, phosphorus (K = 0.14). In concordance with their slow growth, nestlings became endothermic only 10 days before fledging, considerably later than expected from asymptotic mass. Total metabolized energy during the nestling period was 1,133.3 kJ, of which 59.2% accounted for resting metabolic rate and 26.2% for activity. Growth efficiency, the proportion of total metabolized energy allocated to tissue deposition, was 14.5%, one of the lowest reported for altricial nestlings. We argue that nestling growth was not energy-limited and that limiting nutrients were deposited slowly as a result of restrictions imposed by low availability of protein and phosphorus in the diet. We propose that slow growth and poor diets are interrelated in Green-rumped Parrotlets and other Psittaciformes, but the direction of the causal relationship between them is unclear. Received 24 June 2009, accepted 12 December 2009.
The field metabolic rate (FMR) of an endothermic animal represents its energy expenditure in a natural environment, or its energy budget, and its field water flux (FWF) reflects the animal's water requirements. We examined FMR of 103 species and FWF of 75 species of adult birds from direct field measurements using the doubly labelled water method, and used the phylogenetic generalized least squares method to conduct a phylogenetically informed, comprehensive analysis of the relationship between FMR, FWF and multiple environmental and biological variables. Field metabolic rate was strongly positively associated with body mass with an allometric exponent of 0.66, and seabirds had lower FMR than terrestrial species. Birds consuming plant matter had lower FMR compared to omnivores, carnivores or nectarivores and low ambient temperature was associated with higher FMR. There was little evidence for phylogenetic covariance in FMR, even though previous studies identified a phylogenetic signal for basal metabolic rate. Life-history traits, such as fecundity and migration, were also not strongly associated with FMR. Field water flux was strongly positively associated with body mass with an allometric exponent of 0.61, and was strongly related to precipitation but not to temperature. Diet and habitat use had significant effects on FWF, with nectarivores and marine species exhibiting higher values than granivores and forest birds. Thus, FMR and FWF are affected similarly by body size and differently by environmental temperature and precipitation, while the roles of diet, life-history traits and habitat are more nuanced and generalities remain elusive. A free Plain Language Summary can be found within the Supporting Information of this article.