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.

Historical climatic instability predicts the inverse latitudinal pattern in speciation rate of modern mammalian biota.

Evolutionary rate explanations for latitudinal diversity gradients predict faster speciation and diversification rates in richer, older and more stable tropical regions (climatic stability hypothesis). Numerous modern lineages have emerged in high latitudes, however, suggesting that climatic oscillations can drive population divergence, at least among extratropical species (glacial refugia hypothesis). This conflicting evidence suggests that geographical patterns of evolutionary rates are more complicated than previously thought. Here, we reconstructed the complex evolutionary dynamics of a comprehensive data set of modern mammals, both terrestrial and marine. We performed global and regional regression analyses to investigate how climatic instability could have indirectly influenced contemporary diversity gradients through its effects on evolutionary rates. In particular, we explored global and regional patterns of the relationships between species richness and assemblage-level evolutionary rates and between evolutionary rates and climatic instability. We found an inverse relationship between evolutionary rates and species richness, especially in the terrestrial domain. Additionally, climatic instability was strongly associated with the highest evolutionary rates at high terrestrial latitudes, supporting the glacial refugia hypothesis there. At low latitudes, evolutionary rates were unrelated to climatic stability. The inverse relationship between evolutionary rates and the modern latitudinal diversity gradient casts doubt on the idea that higher evolutionary rates in the tropics underlie the current diversity patterns of modern mammals. Alternatively, the longer time spans for diversity to accumulate in the older and more stable tropics (and not high diversification rates) may explain the latitudinal diversity gradient.

Sampling effort and the drivers of plant species richness in the Brazilian coastal regions.

The causes of the gradients in species richness remain contentious because of multiple competing hypotheses, significant knowledge gaps, and regional effects of environmental and historical factors on species pools. Coastal zones are subject to particular sets of environmental constraints, thus identifying the drivers of species richness therein should shed light on the regional gradients of species diversity. Here, we investigate the geographic patterns and drivers of plant diversity across coastal regions while allowing for pervasive sampling deficiencies. Based on 142708 records of flowering plant occurrences, we mapped species richness and estimated the level of knowledge across the coastal zone of Brazil. Based on inventory completeness, we used linear regression models to test the predictive power of environmental variables that represent different environmental hypotheses. Few cells (25%) were well-surveyed, reflecting little knowledge about the distribution and diversity of flowering plants on the highly-populated Brazilian coast. Still, we found support for the habitat heterogeneity hypothesis as the best explanation of the variation in species richness of flowering plants in this region. Soil properties and water constraints are also important factors. Although our work emphasises the paucity of information on plant diversity in tropical and human-dominated areas, we show that knowledge limitations should not curb our capability of addressing hypotheses about species diversity.

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.

Biophysical Modeling of Water Economy Can Explain Geographic Gradient of Body Size in Anurans.

Geographical gradients of body size express climate-driven constraints on animals, but whether they exist and what causes them in ectotherms remains contentious. For amphibians, the water conservation hypothesis posits that larger bodies reduce evaporative water loss (EWL) along dehydrating gradients. To address this hypothesis mechanistically, we build on well-established biophysical equations of water exchange in anurans to propose a state-transition model that predicts an increase of either body size or resistance to EWL as alternative specialization along dehydrating gradients. The model predicts that species whose water economy is more sensitive to variation in body size than to variation in resistance to EWL should increase in size in response to increasing potential evapotranspiration (PET). To evaluate the model predictions, we combine physiological measurements of resistance to EWL with geographic data of body size for four different anuran species. Only one species, Dendropsophus minutus, was predicted to exhibit a positive body size-PET relationship. Results were as predicted for all cases, with one species-Boana faber-showing a negative relationship. Based on an empirically verified mathematical model, we show that clines of body size among anurans depend on the current values of those traits and emerge as an advantage for water conservation. Our model offers a mechanistic and compelling explanation for the cause and variation of gradients of body size in anurans.

Functional planning units for the management of an endangered Brazilian titi monkey.

Conservation practices in the tropics often rely on the data available for a few, better-known species and the adoption of an appropriate spatial scale. By defining a set of landscape units that account for critical aspects of the focal species, the information available on these conservation targets can support regional conservation policies. Here, we define and classify adjacent landscapes, termed planning units, to orientate management decisions within and among these landscapes, which are occupied by an endangered flagship primate species (Coimbra-Filho's titi monkey, Callicebus coimbrai) from eastern Brazil. We use landscape boundaries (highways and river systems), and a high-resolution map of forest remnants to identify continuous and manageable landscapes. We employed functional landscape metrics based on the species' dispersal ability and home range size to characterize and classify these landscapes. We classified planning units by scoring them according to a suite of selected metrics through a Principal Component Analysis. We propose 31 planning units, containing one to six C. coimbrai populations, most with low values of habitat availability, functional connectivity and carrying capacity, and a high degree of degradation. Due to this poor landscape configuration, basic management practices are recommendable. However, additional aspects of the landscapes and the populations they contain (e.g., matrix type and genetic variability) should improve the scheme, which will require a closer integration of research aims with socio-political strategies. Even so, our scheme should prove useful for the combination of information on conservation targets (i.e., focal species) with management strategies on an administrative scale.

Climate and land use changes will degrade the configuration of the landscape for titi monkeys in eastern Brazil.

Land use changes have profound effects on populations of Neotropical primates, and ongoing climate change is expected to aggravate this scenario. The titi monkeys from eastern Brazil (Callicebus personatus group) have been particularly affected by this process, with four of the five species now allocated to threatened conservation status categories. Here, we estimate the changes in the distribution of these titi monkeys caused by changes in both climate and land use. We also use demographic-based, functional landscape metrics to assess the magnitude of the change in landscape conditions for the distribution predicted for each species. We built species distribution models (SDMs) based on maximum entropy for current and future conditions (2070), allowing for different global circulation models and contrasting scenarios of glasshouse gas concentrations. We refined the SDMs using a high-resolution map of habitat remnants. We then calculated habitat availability and connectivity based on home-range size and the dispersal limitations of the individual, in the context of a predicted loss of 10% of forest cover in the future. The landscape configuration is predicted to be degraded for all species, regardless of the climatic settings. This include reductions in the total cover of forest remnants, patch size and functional connectivity. As the landscape configuration should deteriorate severely in the future for all species, the prevention of further loss of populations will only be achieved through habitat restoration and reconnection to counteract the negative effects for these and several other co-occurring species.

Forest structure drives global diversity of primates.

Geographic gradients in the species richness of non-human primates have traditionally been attributed to the variation in forest productivity (related to precipitation levels), although an all-inclusive, global-scale analysis has never been conducted. We perform a more comprehensive test on the role of precipitation and biomass production and propose an alternative hypothesis - the variation in vertical structure of forest habitats as measured by forest canopy height - in determining primate species richness on a global scale. Considering the potential causal relationships among precipitation, productivity and forest structure, we arranged these variables within a path framework to assess their direct and indirect associations with the pattern of primate species richness using structural equation modelling. The analysis also accounted for the influence of spatial autocorrelation in the relationships and assessed possible historical differences among biogeographical regions. The path coefficients indicate that forest canopy height (used as a proxy for vertical forest structure) is a better predictor of primate species richness than either precipitation or productivity on both global and continental scales. The only exception was Asia, where precipitation prevailed, albeit independently from productivity or forest structure. The influence of spatially structured processes varied markedly among biogeographical regions. Our results challenge the traditional rainfall-based viewpoint in favour of forest distribution and structure as primary drivers of primate species richness, which aggregate potential effects from both climatic factors and habitat complexity. These findings may support predictions of the impact of forest removal on primate species richness.

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.

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.

Amphibian responses in experimental thermal gradients: Concepts and limits for inference.

The interpretation of thermal-gradient data depends on the behavioral drives reported or assumed, and on the underlying behavioral models explaining how such drives operate. The best-known example is positive thermotaxis, a thermoregulatory behavioral drive frequently linked to a dual set-point model of thermoregulation around a target range. This behavioral drive is often assumed as dominant among 'ectotherms', including amphibians. However, we argue that, because amphibians are extremely diverse, they may exhibit alternative behavioral drives in thermal gradients, and tackle this idea from two perspectives. First, we provide a historical review of original definitions and proposed limits for inference. Second, although caveats apply, we propose that a cross-study analysis of data of temperature settings of gradients and the temperatures selected by amphibians would corroborate alternative behavioral drives, including negative thermotaxis. Therefore, we analyzed published data focusing on such relationships and show that gradient temperature settings influence the temperatures selected by amphibians, with further effects of phylogeny and ontogeny. We conclude that thermal gradient experiments are outstanding tools to investigate behavioral drives, but no given drive can be assumed a priori unless additional information about thermoregulation is available. Based on the historical debate, we propose using selected temperatures and preferred temperatures as different concepts, the former merely operational and the second explicitly linked to positive thermotaxis (and thus compatible with dual set-point thermoregulation). Under this view, thermal preferences would stand for a hypothesis of a behavioral drive (positive thermotaxis) requiring formal testing. These considerations impact the scope for inference based on thermal gradient experiments, particularly ecological modeling and emerging disease.

Is rich and rare the common share? Describing biodiversity patterns to inform conservation practices for South American anurans.

Species richness and range size are key features of biogeographic and macroecological analyses, which can yield a first assessment tool to define conservation priorities. Here we combined both features in a simultaneous analysis, based on range-diversity plots, to identify sets of rich-rare (high species richness with restricted ranges) and poor-rare cells (low species richness with restricted ranges). We applied this analysis to the anurans of South America and evaluated the representation of those sets of cells within the protected area system. South American anurans showed high species richness in the Brazilian Atlantic Forest and East Tropical Andes, while regions harboring most of the rare species were concentrated in the Andes and Atlantic Coast from North-Eastern Brazil to River Plate. Based on such patterns, we identified as rich-rare cells the Brazilian Atlantic Forest and Tropical Andes and as poor-rare cells the southern part of Andes and Uruguay. A low fraction of both sets of cells was represented within the protected area system. We show that a simultaneous consideration of species richness and rarity provides a rapid assessment of large-scale biodiversity patterns and may contribute to the definition of conservation priorities.