Physical constraints on thermoregulation and flight drive morphological evolution in bats.

Body size and shape fundamentally determine organismal energy requirements by modulating heat and mass exchange with the environment and the costs of locomotion, thermoregulation, and maintenance. Ecologists have long used the physical linkage between morphology and energy balance to explain why the body size and shape of many organisms vary across climatic gradients, e.g., why larger endotherms are more common in colder regions. However, few modeling exercises have aimed at investigating this link from first principles. Body size evolution in bats contrasts with the patterns observed in other endotherms, probably because physical constraints on flight limit morphological adaptations. Here, we develop a biophysical model based on heat transfer and aerodynamic principles to investigate energy constraints on morphological evolution in bats. Our biophysical model predicts that the energy costs of thermoregulation and flight, respectively, impose upper and lower limits on the relationship of wing surface area to body mass (S-MR), giving rise to an optimal S-MR at which both energy costs are minimized. A comparative analysis of 278 species of bats supports the model's prediction that S-MR evolves toward an optimal shape and that the strength of selection is higher among species experiencing greater energy demands for thermoregulation in cold climates. Our study suggests that energy costs modulate the mode of morphological evolution in bats­hence shedding light on a long-standing debate over bats' conformity to ecogeographical patterns observed in other mammals­and offers a procedure for investigating complex macroecological patterns from first principles.

The biogeography of thermal risk for terrestrial ectotherms: Scaling of thermal tolerance with body size and latitude.

Many organisms are shrinking in size in response to global warming. However, we still lack a comprehensive understanding of the mechanisms linking body size and temperature of organisms across their geographical ranges. Here we investigate the biophysical mechanisms determining the scaling of body temperature with size across latitudes in terrestrial ectotherms. Using biophysical models, we simulated operative temperatures experienced by lizard-like ectotherms as a function of microclimatic variables, body mass and latitude and used them to generate null predictions for the effect of size on temperature across geographical gradients. We then compared model predictions against empirical data on lizards' field body temperature (Tb ) and thermal tolerance limits (CTmax and CTmin ). Our biophysical models predict that the allometric scaling of operative temperatures with body size varies with latitude, with a positive relationship at low latitudes that vanishes with increasing latitude. The analyses of thermal traits of lizards show a significant interaction of body size and latitude on Tb and CTmax and no effect of body mass on CTmin , consistent with model's predictions. The estimated scaling coefficients are within the ranges predicted by the biophysical model. The effect of body mass, however, becomes non-significant after controlling for the phylogenetic relatedness between species. We propose that large-bodied terrestrial ectotherms exhibit higher risk of overheating at low latitudes, while size differences in thermal sensitivity vanish towards higher latitudes. Our work highlights the potential of combining mechanistic models with empirical data to investigate the mechanisms underpinning broad-scale patterns and ultimately provide a null model to develop baseline expectations for further empirical research.

Upscaling Microclimatic Conditions into Body Temperature Distributions of Ectotherms.

Realistic projections of the biological impacts of climate change require predicting fitness responses to variations in environmental conditions. For ectotherms, this challenge requires methods to scale-up microclimatic information into actual body temperatures, Tb, while dealing with uncertainty regarding individual behaviors and physiological constraints. Here, we propose an information-theoretical model to derive microhabitat selection and Tb distributions of ectotherm populations from microclimatic data. The model infers the most probable allocation of individuals among the available microenvironments and the associated population-level Tb distribution. Using empirical Tb data of 41 species of desert lizards from three independently evolved systems-Western North America, Kalahari Desert, and Western Australia-we show that the model accurately predicts empirical Tb distributions across the three systems. Moreover, the framework naturally provides a way to quantify the importance of thermoregulation in a thermal environment and thereby a measurement for the constraint imposed by the climatic conditions. By predicting Tb distributions of ectotherm populations even without exhaustive information on the underpinning mechanisms, our approach forms a solid theoretical basis for upscaling microclimatic and physiological information into a population-level fitness trait. This scaling process is a first step to reliably project the biological impacts of climate change to broad temporal and spatial scales.

Human-mediated dispersal of terrestrial species between Antarctic biogeographic regions: A preliminary risk assessment.

The distribution of terrestrial biodiversity within Antarctica is complex, with 16 distinct biogeographic regions (Antarctic Conservation Biogeographic Regions) currently recognised within the Antarctic continent, Peninsula and Scotia Arc archipelagos of the Antarctic Treaty area. Much of this diversity is endemic not only to Antarctica as a whole, but to specific regions within it. Further complexity is added by inclusion of the biodiversity found on the islands located in the Southern Ocean north of the Treaty area. Within Antarctica, scientific, logistic and tourism activities may inadvertently move organisms over potentially long distances, far beyond natural dispersal ranges. Such translocation can disrupt natural species distribution patterns and biogeography through: (1) movement of spatially restricted indigenous species to other areas of Antarctica; (2) movement of distinct populations of more generally distributed species from one area of Antarctica to another, leading to genetic homogenisation and loss of assumed local patterns of adaptation; and (3) further dispersal of introduced non-native species from one area of Antarctica to another. Species can be moved between regions in association with people and cargo, by ship, aircraft and overland travel. Movement of cargo and personnel by ship between stations located in different biogeographic regions is likely to present one of the greatest risks, particularly as coastal stations may experience similar climatic conditions, making establishment more likely. Recognising that reducing the risk of inter-regional transfer of species is a priority issue for the Antarctic Treaty Consultative Meeting, we make practical recommendations aimed at reducing this risk, including the implementation of appropriate biosecurity procedures.

Untangling human and environmental effects on geographical gradients of mammal species richness: a global and regional evaluation.

Different hypotheses (geographical, ecological, evolutionary or a combination of them) have been suggested to account for the spatial variation in species richness. However, the relative importance of environment and human impacts in explaining these patterns, either globally or at the biogeographical region level, remains largely unexplored. Here, we jointly evaluate how current environmental conditions and human impacts shape global and regional gradients of species richness in terrestrial mammals. We processed IUCN global distributional data for 3939 mammal species and a set of seven environmental and two human impact variables at a spatial resolution of 96.5 × 96.5 km. We used simple, multiple and partial regression techniques to evaluate environmental and human effects on species richness. Actual evapotranspiration (AET) is the main driver of mammal species richness globally. Together with our results at the biogeographical realm level, this lends strong support for the water-energy hypothesis (i.e. global diversity gradients are best explained by the interaction of water and energy, with a latitudinal shift in the relative importance of ambient energy vs. water availability as we move from the poles to the equator). While human effects on species richness are not easily detected at a global scale due to the large proportion of shared variance with the environment, these effects significantly emerge at the regional level. In the Nearctic, Palearctic and Oriental regions, the independent contribution of human impacts is almost as important as current environmental conditions in explaining richness patterns. The intersection of human impacts with climate drives the geographical variation in mammal species richness in the Palearctic, Nearctic and Oriental regions. Using a human accessibility variable, we show, for the first time, that the zones most accessible to humans are often those where we find lower mammal species richness.

Correlated evolution between body size and echolocation in bats (order Chiroptera).

BACKGROUND: Body size and echolocation call frequencies are related in bats. However, it is unclear if this allometry applies to the entire clade. Differences have been suggested between nasal and oral emitting bats, as well as between some taxonomic families. Additionally, the scaling of other echolocation parameters, such as bandwidth and call duration, needs further testing. Moreover, it would be also interesting to test whether changes in body size have been coupled with changes in these echolocation parameters throughout bat evolution. Here, we test the scaling of peak frequency, bandwidth, and call duration with body mass using phylogenetically informed analyses for 314 bat species. We specifically tested whether all these scaling patterns differ between nasal and oral emitting bats. Then, we applied recently developed Bayesian statistical techniques based on large-scale simulations to test for the existence of correlated evolution between body mass and echolocation. RESULTS: Our results showed that echolocation peak frequencies, bandwidth, and duration follow significant allometric patterns in both nasal and oral emitting bats. Changes in these traits seem to have been coupled across the laryngeal echolocation bats diversification. Scaling and correlated evolution analyses revealed that body mass is more related to peak frequency and call duration than to bandwidth. We exposed two non-exclusive kinds of mechanisms to explain the link between size and each of the echolocation parameters. CONCLUSIONS: The incorporation of Bayesian statistics based on large-scale simulations could be helpful for answering macroevolutionary patterns related to the coevolution of traits in bats and other taxonomic groups.

Intra and interspecific differences in desiccation tolerance in native and alien Antarctic springtails in geothermal grounds.

The extreme low humidity and temperatures in Antarctica make it one of the harsher areas for life on our planet. In a global change context, environmental barriers that prevented the arrival of alien species in Antarctica are weakening. Deception Island, one of the four active volcanoes of Antarctica, is especially vulnerable to the impacts of alien species. Geothermal areas (GA) in this Island offer unique microclimatic conditions that could differentially affect native and alien soil arthropods. Here we explore the desiccation tolerance of a native (Cryptopygus antarcticus) and an alien (Proisotoma minuta) springtail (Collembola) species to these extreme environmental conditions. GA and non-geothermal areas (NGA) were selected to evaluate intra- and interspecific variation in desiccation tolerance. Populations of P. minuta from GA had greater desiccation tolerance than populations from NGA. However, desiccation tolerance of C. antarcticus did not differ between GA and NGA. This native species had greater desiccation tolerance than the alien P. minuta, but also greater body size. Our findings show that the alien P. minuta responds differently to environmental conditions than the native C. antarcticus. Furthermore, body size may influence desiccation tolerance in these two springtail species.

TerrANTALife 1.0 Biodiversity data checklist of known Antarctic terrestrial and freshwater life forms.

Background: Incomplete species inventories for Antarctica represent a key challenge for comprehensive ecological research and conservation in the region. Additionally, data required to understand population dynamics, rates of evolution, spatial ranges, functional traits, physiological tolerances and species interactions, all of which are fundamental to disentangle the different functional elements of Antarctic biodiversity, are mostly missing. However, much of the fauna, flora and microbiota in the emerged ice-free land of the continent have an uncertain presence and/or unresolved status, with entire biodiversity compendia of prokaryotic groups (e.g. bacteria) being missing. All the available biodiversity information requires consolidation, cross-validation, re-assessment and steady systematic inclusion in order to create a robust catalogue of biodiversity for the continent. New information: We compiled, completed and revised eukaryotic species inventories present in terrestrial and freshwater ecosystems in Antarctica in a new living database: terrANTALife (version 1.0). The database includes the first integration in a compendium for many groups of eukaryotic microorganisms. We also introduce a first catalogue of amplicon sequence variants (ASVs) of prokaryotic biodiversity. Available compendia and literature to date were searched for Antarctic terrestrial and freshwater species, integrated, taxonomically harmonised and curated by experts to create comprehensive checklists of Antarctic organisms. The final inventories comprises 470 animal species (including vertebrates, free-living invertebrates and parasites), 306 plants (including all Viridiplantae: embryophytes and green algae), 997 fungal species and 434 protists (sensu lato). We also provide a first account for many groups of microorganisms, including non-lichenised fungi and multiple groups of eukaryotic unicellular species (Stramenophila, Alveolata and Rhizaria (SAR), Chromists and Amoeba), jointly referred to as "protists". In addition, we identify 1753 bacterial (obtained from 348117 ASVs) and 34 archaeal genera (from 1848 ASVs), as well as, at least, 14 virus families. We formulate a basic tree of life in Antarctica with the main lineages listed in the region and their "known-accepted-species" numbers.

Climate drives global functional trait variation in lizards.

A major challenge in ecology and evolution is to disentangle the mechanisms driving broad-scale variation in biological traits such as body size, colour, thermal physiology traits and behaviour. Climate has long been thought to drive trait evolution and abiotic filtering of trait variation in ectotherms because their thermal performance and fitness are closely related to environmental conditions. However, previous studies investigating climatic variables associated with trait variation have lacked a mechanistic description of the underpinning processes. Here, we use a mechanistic model to predict how climate affects thermal performance of ectotherms and thereby the direction and strength of the effect of selection on different functional traits. We show that climate drives macro-evolutionary patterns in body size, cold tolerance and preferred body temperatures among lizards, and that trait variation is more constrained in regions where selection is predicted to be stronger. These findings provide a mechanistic explanation for observations on how climate drives trait variation in ectotherms through its effect on thermal performance. By connecting physical, physiological and macro-evolutionary principles, the model and results provide an integrative, mechanistic framework for predicting organismal responses to present climates and climate change.

Contrasting patterns in phylogenetic and biogeographic factories of invasive grasses (Poaceae) across the globe.

Grasses (Family Poaceae) are among the most successful invasive plants in the world. Here we evaluate phylogenetic and biogeographic patterns of emergence of naturalized and invasive species among grasses globally. In our data, circa 19% of the grasses are currently catalogued as invasive and almost 38% are listed as naturalized; these are among the highest ratios for single families of organisms. Remarkably, most tribes of grasses contain numerous naturalized and invasive species, suggesting that the invasion success is rooted broadly in ancestral traits in the Poaceae. Moreover, the probability of invasiveness is positively related to the diversification rates in the family also suggesting a link with recent radiation events. The phylogenetic distribution of the invasive condition is neither strongly conserved nor purely random. Phylogenetic clumping levels also vary between Poaceae subclades. We postulate that this diffuse clumping could be partially attributed to the expression of labile traits that contribute to species invasiveness. In addition, floristic regions (biomes and biogeographic realms) have different proportions of invasive species, with the temperate Palearctic region having the highest ratio of invasive vs. non-invasive species. The phylodiversity of aliens across regions is also variable in space. Comparison of alien phylodiversity levels across biogeographic realms and biomes reveals regions producing highly restricted invasive lineages and others where the diversity of aliens exported is no different from global mean diversity levels in grasses. Elucidating the evolutionary patterns and drivers of invasiveness is useful for understanding and managing invasions, with the low phylogenetic structure of alien grasses warning of their overall high invasiveness potential.

The imprint of Cenozoic migrations and evolutionary history on the biogeographic gradient of body size in New World mammals.

Ecology, evolution, and historical events all contribute to biogeographic patterns, but studies that integrate them are scarce. Here we focus on how biotic exchanges of mammals during the Late Cenozoic have contributed to current geographic body size patterns. We explore differences in the environmental correlates and phylogenetic patterning of body size between groups of mammals participating and not participating in past biotic exchanges. Both the association of body size with environmental predictors and its phylogenetic signal were stronger for groups that immigrated into North or South America than for indigenous groups. This pattern, which held when extinct clades were included in the analyses, can be interpreted on the basis of the length of time that clades have had to diversify and occupy niche space. Moreover, we identify a role for historical events, such as Cenozoic migrations, in configuring contemporary mammal body size patterns and illustrate where these influences have been strongest for New World mammals.

Half a century of thermal tolerance studies in springtails (Collembola): A review of metrics, spatial and temporal trends.

Global changes in soil surface temperatures are altering the abundances and distribution ranges of invertebrate species worldwide, including effects on soil microarthropods such as springtails (Collembola), which are vital for maintaining soil health and providing ecosystem services. Studies of thermal tolerance limits in soil invertebrates have the potential to provide information on demographic responses to climate change and guide assessments of possible impacts on the structure and functioning of ecosystems. Here, we review the state of knowledge of thermal tolerance limits in Collembola. Thermal tolerance metrics have diversified over time, which should be taken into account when conducting large-scale comparative studies. A temporal trend shows that the estimation of 'Critical Thermal Limits' (CTL) is becoming more common than investigations of 'Supercooling Point' (SCP), despite the latter being the most widely used metric. Indeed, most studies (66%) in Collembola have focused on cold tolerance; fewer have assessed heat tolerance. The majority of thermal tolerance data are from temperate and polar regions, with fewer assessments from tropical and subtropical latitudes. While the hemiedaphic life form represents the majority of records at low latitudes, euedaphic and epedaphic groups remain largely unsampled in these regions compared to the situation in temperate and high latitude regions, where sampling records show a more balanced distribution among the different life forms. Most CTL data are obtained during the warmest period of the year, whereas SCP and 'Lethal Temperature' (LT) show more variation in terms of the season when the data were collected. We conclude that more attention should be given to understudied zoogeographical regions across the tropics, as well as certain less-studied clades such as the family Neanuridae, to identify the role of thermal tolerance limits in the redistribution of species under changing climates.

Water constraints drive allometric patterns in the body shape of tree frogs.

The origin of morphological diversity is a critical question in evolutionary biology. Interactions between the environment and developmental processes have determining roles in morphological diversity, creating patterns through space and over time. Also, the shape of organisms tends to vary with increasing size as a result of those developmental processes, known as allometry. Several studies have demonstrated that the body sizes of anurans are associated with hydric conditions in their environments and that localities with high water stress tend to select for larger individuals. However, how environmental conditions alter those patterns of covariance between size and shape is still elusive. We used 3D geometric morphometric analyses, associated with phylogenetic comparative methods, to determine if the morphological variations and allometric patterns found in Arboranae (Anura) is linked to water conservation mechanisms. We found effects of the hydric stress on the shape of Arboranae species, favouring globular shapes. Also, the allometric patterns varied in intensity according to the water stress gradient, being particularly relevant for smaller frogs, and more intense in environments with higher water deficits. Our study provides empirical evidence that more spherical body shapes, especially among smaller species, reflect an important adaptation of anurans to water conservation in water-constrained environments.

A global evaluation of metabolic theory as an explanation for terrestrial species richness gradients.

We compiled 46 broadscale data sets of species richness for a wide range of terrestrial plant, invertebrate, and ectothermic vertebrate groups in all parts of the world to test the ability of metabolic theory to account for observed diversity gradients. The theory makes two related predictions: (1) In-transformed richness is linearly associated with a linear, inverse transformation of annual temperature, and (2) the slope of the relationship is near -0.65. Of the 46 data sets, 14 had no significant relationship; of the remaining 32, nine were linear, meeting prediction 1. Model I (ordinary least squares, OLS) and model II (reduced major axis, RMA) regressions then tested the linear slopes against prediction 2. In the 23 data sets having nonlinear relationships between richness and temperature, split-line regression divided the data into linear components, and regressions were done on each component to test prediction 2 for subsets of the data. Of the 46 data sets analyzed in their entirety using OLS regression, one was consistent with metabolic theory (meeting both predictions), and one was possibly consistent. Using RMA regression, no data sets were consistent. Of 67 analyses of prediction 2 using OLS regression on all linear data sets and subsets, two were consistent with the prediction, and four were possibly consistent. Using RMA regression, one was consistent (albeit weakly), and four were possibly consistent. We also found that the relationship between richness and temperature is both taxonomically and geographically conditional, and there is no evidence for a universal response of diversity to temperature. Meta-analyses confirmed significant heterogeneity in slopes among data sets, and the combined slopes across studies were significantly lower than the range of slopes predicted by metabolic theory based on both OLS and RMA regressions. We conclude that metabolic theory, as currently formulated, is a poor predictor of observed diversity gradients in most terrestrial systems.

High Resolution Spatial Mapping of Human Footprint across Antarctica and Its Implications for the Strategic Conservation of Avifauna.

Human footprint models allow visualization of human spatial pressure across the globe. Up until now, Antarctica has been omitted from global footprint models, due possibly to the lack of a permanent human population and poor accessibility to necessary datasets. Yet Antarctic ecosystems face increasing cumulative impacts from the expanding tourism industry and national Antarctic operator activities, the management of which could be improved with footprint assessment tools. Moreover, Antarctic ecosystem dynamics could be modelled to incorporate human drivers. Here we present the first model of estimated human footprint across predominantly ice-free areas of Antarctica. To facilitate integration into global models, the Antarctic model was created using methodologies applied elsewhere with land use, density and accessibility features incorporated. Results showed that human pressure is clustered predominantly in the Antarctic Peninsula, southern Victoria Land and several areas of East Antarctica. To demonstrate the practical application of the footprint model, it was used to investigate the potential threat to Antarctica's avifauna by local human activities. Relative footprint values were recorded for all 204 of Antarctica's Important Bird Areas (IBAs) identified by BirdLife International and the Scientific Committee on Antarctic Research (SCAR). Results indicated that formal protection of avifauna under the Antarctic Treaty System has been unsystematic and is lacking for penguin and flying bird species in some of the IBAs most vulnerable to human activity and impact. More generally, it is hoped that use of this human footprint model may help Antarctic Treaty Consultative Meeting policy makers in their decision making concerning avifauna protection and other issues including cumulative impacts, environmental monitoring, non-native species and terrestrial area protection.

Correction: High Resolution Spatial Mapping of Human Footprint across Antarctica and Its Implications for the Strategic Conservation of Avifauna.

[This corrects the article DOI: 10.1371/journal.pone.0168280.].