Multiple morphophysiological responses of a tropical frog to urbanization conform to the pace-of-life syndrome.

The Pace-of-Life syndrome proposes that behavioural, physiological and immune characteristics vary along a slow-fast gradient. Urbanization poses several physiological challenges to organisms. However, little is known about how the health status of frogs is affected by urbanization in the Tropics, which have a faster and more recent urbanization than the northern hemisphere. Here, we analysed a suite of physiological variables that reflect whole organism health, reproduction, metabolic and circulatory physiology and leukocyte responses in Leptodactylus podicipinus. Specifically, we tested how leukocyte profile, erythrocyte morphometrics and germ cell density, as well as somatic indices and erythrocyte nuclear abnormalities differ throughout the adult life span between urban and rural populations. We used Phenotypic Trajectory Analysis to test the effect of age and site on each of the multivariate data sets; and a Generalised Linear Model to test the effect of site and age on nuclear abnormalities. Somatic indices, erythrocyte nuclear abnormalities, erythrocyte morphometrics and leukocyte profile differed between populations, but less so for germ cell density. We found a large effect of site on nuclear abnormalities, with urban frogs having twice as many abnormalities as rural frogs. Our results suggest that urban frogs have a faster pace of life, but the response of phenotypic compartments is not fully concerted.

Reproducibility in ecology and evolution: Minimum standards for data and code.

We call for journals to commit to requiring open data be archived in a format that will be simple and clear for readers to understand and use. If applied consistently, these requirements will allow contributors to be acknowledged for their work through citation of open data, and facilitate scientific progress.

Combined effects of landscape composition and agrochemicals on frog communities amid sugarcane-dominated agroecosystems.

Global demand for crops will continue increasing over the next few decades to cover both food and biofuel needs. This demand will put further pressure to expand arable land and replace natural habitats. However, we are only beginning to understand the combined effects of agrochemicals and land-use change on tropical freshwater biodiversity. In this study, we analyzed how pond-dwelling anuran larvae responded to pond characteristics, landscape composition, and agrochemical contamination in a sugarcane-dominated agroecosystem in Brazil. Then we used an information theoretical approach with generalized linear models to relate species richness and abundance to predictor variables. The variation in tadpole abundance was associated with both agrochemical concentration (e.g., ametryn, diuron, and malathion) and landscape variables (e.g., percentage of forest, percentage of agriculture, and distance to closest forest). The relationship between species abundance and agrochemicals was species-specific. For example, the abundances of Scinax fuscovarius and Physalaemus nattereri were negatively associated with ametryn, and Dendropsophus nanus was negatively associated with tebuthiuron, whereas that of Leptodactylus fuscus was positively associated with malathion. Conversely, species richness was associated with distance to forest fragments and aquatic vegetation heterogeneity, but not agrochemicals. Although we were unable to assign a specific mechanism to the variation in tadpole abundance based on field observations, the lower abundance of three species in ponds with high concentrations of agrochemicals suggest they negatively impact some frog species inhabiting agroecosystems. We recommend conserving ponds near forest fragments, with abundant stratified vegetation, and far from agrochemical runoffs to safeguard more sensitive pond-breeding species.

Hematological parameters of a Neotropical wild frog population, with a phylogenetic perspective on blood cell composition in Anura.

Hematological parameters can provide key information to an animal health status. However, this information is usually hard to obtain. Here, we described the hematological parameters of Leptodactylus podicipinus in the Brazilian Pantanal. We measured red blood cell morphometrics, erythrogram, and leukogram. We also tested for phylogenetic signal in the erythrogram and leukogram of 48 frog species from 15 families, testing if body size explains their variation. Lymphocytes were the most abundant leukocytes (>60%) in L. podicipinus, followed by neutrophils (∼10%). Given that L. podicipinus is an abundant and widely distributed species in central Brazil, knowing its hematological pattern can help establish a baseline and improve its use as a bioindicator of environmental degradation. Mean corpuscular hemoglobin and value contributed more to the phylomorphospace of erythrogram, in which Leptodactylus spp. and Hypsiboas raniceps had lower values of these variables, whereas Bufotes viridis and Hyla arborea had high values. The phylogenetic signal was spread throughout the dimensions of the leukogram phylomorphospace. The variables that most contributed to it were total leukocytes counts, lymphocytes, and neutrophils. We also found a moderate phylogenetic signal for both the erythrogram and leukogram. Accordingly, body size accounted for a low proportion of variation in both the leukogram (4.7%) and erythrogram (0.57%). By applying phylogenetic comparative methods to hematological parameters, our results add a new perspective on the evolution of blood cell physiology in frogs.

Differences in prey availability across space and time lead to interaction rewiring and reshape a predator-prey metaweb.

Space and time promote variation in network structure by affecting the likelihood of potential interactions. However, little is known about the relative roles of ecological and biogeographical processes in determining how species interactions vary across space and time. Here we study the spatiotemporal variation in predator-prey interaction networks formed by anurans and arthropods and test for the effects of prey availability in determining interaction patterns, information that is often absent and limits the understanding of the determinants of network structure. We found that network dissimilarity between ecoregions and seasons was high and primarily driven by interaction rewiring.We also found that species turnover was positively related to geographical distance. Using a null model approach to disentangle the effect of prey availability on the spatial and temporal variation, we show that differences in prey availability were important in determining the variation in network structure between seasons and among areas. Our study reveals that fluctuations in prey abundance, alongside the limited dispersal abilities of anurans and their prey, may be responsible for the spatial patterns that emerged in our predator-prey metaweb. These findings contribute to our understanding of the assembly rules that maintain biotic processes in metacommunities and highlight the importance of prey availability to the structure of these systems.

The evolution of red blood cell shape in fishes.

The size and shape of red blood cells (RBCs) provide key information on life-history strategies in vertebrates. However, little is known about how RBC shape evolved in response to environmental factors, body size and the role of evolutionary rate. Here, we analysed RBC morphometrics in a set of Teleostei (bony fishes) and Elasmobranchii (sharks and rays) species testing the hypothesis that phylogenetic relationship explains species occupation of morphospace. We collected data on cell and nucleus area and volume, nucleus:cytoplasm ratio and shape factor for 65 species belonging to 28 orders. Then, we built phylomorphospaces separately for bony fish and sharks and rays. To test whether phylogenetic relationships predicted phenotypic similarity, we calculated multivariate phylogenetic signal. We also estimated the evolutionary rate of RBC shape for each node and tip using ridge regression. Finally, we tested whether habitat and body size influenced RBC shape using a PGLS. We found a significant phylogenetic signal in RBC shape for bony fish, but not sharks and rays. Saltwater teleost species were more clustered than freshwater ones in the phylomorphospace, suggesting clade disparity. Accordingly, the rate of evolution was highly heterogeneous, with significant decrease in Acanthopterygii. Neither habitat nor body size influenced RBC shape. In conclusion, RBC shape seems to have evolved in fishes in response to multiple selective pressures independent of life-history characters.

Idiosyncratic liver pigment alterations of five frog species in response to contrasting land use patterns in the Brazilian Cerrado.

BACKGROUND: Changes in land use trigger environmental changes that can lead to decreased biodiversity and species loss. The liver is an essential detoxification organ that reflects systemic physiological responses to environmental changes. Here, we tested whether contrasting land use patterns influence the amount of substances from the hepatic cellular catabolism and melanomacrophages (MMs) of five anuran species in the Brazilian Cerrado. METHODS: We collected the same five species of pond-dwelling frogs in one protected area and in an area with intense agricultural activity. We used routine histological and histochemical techniques to quantify the area occupied by lipofuscin, melanin, and hemosiderin in the liver of two frogs Leptodactylus fuscus, Physalaemus cuvieri, and three tree-frogs Dendropsophus minutus, Scinax fuscomarginatus, and Boana albopunctata. We classified land use types in a buffer around each pond based on satellite images. We then used a double-constrained Correspondence Analysis, a recently developed ecological method to relate functional traits to environmental variables, to test the effect of each land use type on the area of each liver pigment. RESULTS: There was an increase in the amount of melanin in environments with high proportion of agriculture, as well as variation in the amount of lipofuscin and hemosiderin. Liver pigments of P. cuvieri and B. albopunctata varied more strongly in response to land use types, suggesting they could be good indicator species. Therefore, the area of MMs in the liver and the metabolic products in their cytoplasm can be used as biomarkers of environmental changes in regions with intense agricultural activities. Our results add a new perspective to the influence of land use patterns on environmental health by highlighting the effect of environmental changes on internal morphological aspects of animals.

Climatic variables influence the temporal dynamics of an anuran metacommunity in a nonstationary way.

Understanding the temporal dynamics of communities is crucial to predict how communities respond to climate change. Several factors can promote variation in phenology among species, including tracking of seasonal resources, adaptive responses to other species, demographic stochasticity, and physiological constraints. The activities of ectothermic vertebrates are sensitive to climatic variations due to the effect of temperature and humidity on species physiology. However, most studies on temporal dynamics have analyzed multi-year data and do not have resolution to discriminate within-year patterns that can determine community assembly cycles. Here, we tested the temporal stability and synchrony of calling activity and also how climatic variables influence anuran species composition throughout the year in a metacommunity in the Atlantic Forest of southern Brazil. Using a multivariate method, we described how the relationship between species composition and climatic variables changes through time. The metacommunity showed a weak synchronous spatial pattern, meaning that species responded independently to environmental variation. Interestingly, species composition exhibited a nonstationary response to climate, suggesting that climate affects species composition differently depending on the season. The species-climate relationship was stronger during the spring, summer, and winter, mainly influenced by temperature, rainfall, and humidity. Thus, temporal community dynamics seem to be mediated by species life-history traits, in which independent fluctuations promote community stability in temporally varying environments.

Allometric escape from acoustic constraints is rare for frog calls.

Allometric constraint is a product of natural selection and physical laws, particularly with respect to body size and traits constrained by properties thereof, such as metabolism, longevity, and vocal frequency. Allometric relationships are often conserved across lineages, indicating that physical constraints dictate scaling patterns in deep time, despite substantial genetic and ecological divergence among organisms. In particular, acoustic allometry (sound frequency ~ body size) is conserved across frogs, in defiance of massive variation in both body size and frequency. Here, we ask how many instances of allometric escape have occurred across the frog tree of life using a Bayesian framework that estimates the location, number, and magnitude of shifts in the adaptive landscape of acoustic allometry. Moreover, we test whether ecology in terms of calling site could affect these relationships. We find that calling site has a major influence on acoustic allometry. Despite this, we identify only four major instances of allometric escape, potentially deriving from ecomorphological adaptations to new signal modalities. In these instances of allometric escape, the optima and strength of the scaling relationship are different than expected for most other frog species, representing new adaptive regimes of body size ~ call frequency. Allometric constraints on frog calls are highly conserved and have rarely allowed escape, despite frequent invasions of new adaptive regimes and dramatic ecomorphological divergence. Our results highlight the rare instances in which natural and sexual selection combined can overcome physical constraints on sound production.

Predators regulate prey species sorting and spatial distribution in microbial landscapes.

The role of predation in determining the metacommunity assembly model of prey communities is understudied relative to that of interspecific competition among prey. Previous work on metacommunity dynamics of competing species has shown that sorting by habitat patch type and spatial patterning can be affected by disturbances. Microcosms offer a useful model system to test the effect of multi-trophic interactions and disturbance on metacommunity dynamics. Here, we investigated the potential role of predators in enhancing or disrupting sorting and spatial pattern among prey in experimental landscapes. We exposed multi-trophic protist microcosm landscapes with one predator, two competing prey, two patch resource types, and localized dispersal to three disturbance regimes (none, low, and high). Then, we used variation partitioning and spatial clustering analysis to analyse the results. In contrast with previous experiments that did not manipulate predators, we found that patch type did not structure prey communities very well. Instead, we found that it was the distribution of the predator that most strongly predicted the composition of the prey community. The predator impacted species sorting by (1) preferentially consuming one prey, thereby acting as a strong local environmental driver, and by (2) indirectly magnifying the impact of patch food resources on the less preferred prey. The predator also enhanced spatial signal in the prey community because of its limited dispersal. Our results indicate that predators can strongly influence prey species sorting and spatial patterning in metacommunities in ways that would otherwise be attributed to stochastic effects, such as dispersal limitation or demographic drift. Therefore, whenever possible, predators should be explicitly included as separate explanatory factors in variation partitioning analyses.

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.