What factors influence the rediscovery of lost tetrapod species?

We created a database of lost and rediscovered tetrapod species, identified patterns in their distribution and factors influencing rediscovery. Tetrapod species are being lost at a faster rate than they are being rediscovered, due to slowing rates of rediscovery for amphibians, birds and mammals, and rapid rates of loss for reptiles. Finding lost species and preventing future losses should therefore be a conservation priority. By comparing the taxonomic and spatial distribution of lost and rediscovered tetrapod species, we have identified regions and taxa with many lost species in comparison to those that have been rediscovered-our results may help to prioritise search effort to find them. By identifying factors that influence rediscovery, we have improved our ability to broadly distinguish the types of species that are likely to be found from those that are not (because they are likely to be extinct). Some lost species, particularly those that are small and perceived to be uncharismatic, may have been neglected in terms of conservation effort, and other lost species may be hard to find due to their intrinsic characteristics and the characteristics of the environments they occupy (e.g. nocturnal species, fossorial species and species occupying habitats that are more difficult to survey such as wetlands). These lost species may genuinely await rediscovery. However, other lost species that possess characteristics associated with rediscovery (e.g. large species) and that are also associated with factors that negatively influence rediscovery (e.g. those occupying small islands) are more likely to be extinct. Our results may foster pragmatic search protocols that prioritise lost species likely to still exist.

Unwrapping broken tails: Biological and environmental correlates of predation pressure in limbless reptiles.

Studying species interactions in nature often requires elaborated logistics and intense fieldwork. The difficulties in such task might hinder our ability to answer questions on how biotic interactions change with the environment. Fortunately, a workaround to this problem lies within scientific collections. For some animals, the inspection of preserved specimens can reveal the scars of past antagonistic encounters, such as predation attempts. A common defensive behaviour that leaves scars on animals is autotomy, the loss of a body appendage to escape predation. By knowing the collection site of preserved specimens, it is possible to assess the influence of organismal biology and the surrounding environment in the occurrence of autotomy. We gathered data on tail loss for 8189 preserved specimens of 33 snake and 11 amphisbaenian species to investigate biological and environmental correlates of autotomy in reptiles. We applied generalized linear mixed effect models to evaluate whether body size, sex, life-stage, habitat use, activity pattern, biome, tropicality, temperature and precipitation affect the probability of tail loss in limbless reptiles. We observed autotomy in 23.6% of examined specimens, with 18.7% of amphisbaenian and 33.4% of snake specimens showing tail loss. The probability of tail loss did not differ between snakes and amphisbaenians, but it was higher among large-sized specimens, particularly in adults and females. Chance of tail loss was higher for diurnal and arboreal species, and among specimens collected in warmer regions, but it was unaffected by biome, precipitation, and tropicality. Autotomy in limbless reptiles was affected by size-dependent factors that interplay with ontogeny and sexual dimorphism, although size-independent effects of life-stage and sex also shaped behavioural responses to predators. The increase in probability of tail loss with verticality and diurnality suggests a risk-balance mechanism between species habitat use and activity pattern. Although autotomy is more likely in warmer regions, it seems unrelated to seasonal differences in snakes and amphisbaenians activity. Our findings reveal several processes related to predator-prey interactions involving limbless reptiles, demonstrating the importance of scientific collections to unveil ecological mechanisms at different spatio-temporal scales.

When the tail shakes the snake: phylogenetic affinities and morphology of Atractus badius (Serpentes: Dipsadidae), reveals some current pitfalls on the snake's genomic age.

Atractus badius has a long and controversial nomenclatural history due to both its antiquity and the brevity of its original description. This species was described based on two syntypes from Java. Later, a lectotype was designated and the distribution range restricted to the Guiana Shield. Although this species has been repeatedly recorded throughout Amazonia and the Andes, these records have been erroneously assigned to A. badius because of a considerable level of confusion in the literature. We found 13 additional specimens of this poorly known snake, expanding our knowledge on its morphological variability, phylogenetic relationships and distribution. In this paper, we report new localities and data on meristic, morphometric, coloration, scales micro-ornamentation, osteology and hemipenial morphology to A. badius. We also determine the phylogenetic position of A. badius as nested in a composite Guiana Shield clade. In addition, we discuss recent advances on the systematics of Atractus and comment on some 'new arrangements' with respect to previously recognized species groups and available morphological evidence. Finally, we highlight the importance of accurate voucher identification before promoting taxonomic changes or implementing nomenclatural acts derived from new phylogenetic hypotheses, and notably propose the synonymy of the recently described A. pyroni with A. roulei.

Molecular phylogeny of Neotropical Parrot Snakes (Serpentes: Colubrinae: Leptophis) supports underestimated species richness.

Tetrapod taxa with broad geographic distributions across the Neotropics are often composed of multiple evolutionary lineages. In this paper, we present the most complete phylogeny of Leptophis to date and assess morphology-based species limits within the broadly distributed green parrot snake Leptophis ahaetulla sensu lato, which occurs from Mexico to Argentina. Although L. ahaetulla sensu stricto, L. nigromarginatus and L. occidentalis were recovered as paraphyletic, tree topology tests failed to reject their monophyly. Monophyly of L. bocourti, L. coeruleodorsus, L. cupreus, L. depressirostris, L. marginatus, L. riveti and L. sp. nov. was strongly supported. Our phylogenetic trees support recognition of multiple species within Leptophis ahaetulla sensu lato and suggest that color evolution and the uplift of the Andes played an important role in the diversification of parrot snakes.

Hidden diversity in two widespread snake species (Serpentes: Xenodontini: Erythrolamprus) from South America.

The spatial distribution of genetic diversity of widely distributed Neotropical tetrapods has been an active research field during the last decade, although it has focused on lowland (mostly Amazonian) taxa. In this paper we use phylogenetic analyses to explore the diversity within two widely distributed snake species, Erythrolamprus epinephelus and E. reginae. Specifically, we focus on Andean populations of the former and lowland samples of the latter. Our results show that Erythrolamprus epinephelus is paraphyletic and support recognition of the subspecies albiventris, fraseri and lamonae as distinct species. Regarding E. reginae, our results are in conflict with recent taxonomic proposals in that (1) E. reginae is paraphyletic, and (2) E. zweifeli from Trinidad and E. reginae from Amazonian Ecuador are not reciprocally monophyletic. Finally, we recommend caution when proposing taxonomic changes based on incomplete geographic and/or character sampling of widespread Neotropical taxa.

Phylogeny, diversity and biogeography of Neotropical sipo snakes (Serpentes: Colubrinae: Chironius).

Neotropical sipo snakes (Chironius) are large diurnal snakes with a long tail and big eyes that differ from other Neotropical snakes in having 10 or 12 dorsal scale rows at midbody. The 22 currently recognized species occur from Central America south to Uruguay and northeastern Argentina. Based on the largest geographical sampling to date including ∼90% of all species, we analyzed one nuclear and three mitochondrial genes using phylogenetic methods to (1) test the monophyly of Chironius and some of its widely distributed species; (2) identify lineages that could represent undescribed species; and (3) reconstruct ancestral distributions. Our best hypothesis placed C. grandisquamis (Chocoan Rainforest) + C. challenger (Pantepui) as sister to all other species. Based on phylogeny and geographic distribution, we identified 14 subclades as putative species within Chironius fuscus, C. multiventris (including C. foveatus and C. laurenti), C. monticola, and C. exoletus. Under current taxonomy, these species show nearly twice as much genetic diversity as other species of Chironius for ND4. Biogeographical analyses using BioGeoBEARS suggest that current distribution patterns of Chironius species across South America resulted from multiple range expansions. The MRCA of the clade C. challenger + C. grandisquamis was most likely distributed over the Pantepui region, the Andes, and the Chocoan Rainforest, whereas the remaining lineages probably evolved from an Amazonian ancestor.

Comparative Evolution of an Archetypal Adaptive Radiation: Innovation and Opportunity in Anolis Lizards.

Adaptive radiation is a widely recognized pattern of evolution wherein substantial phenotypic change accompanies rapid speciation. Adaptive radiation may be triggered by environmental opportunities resulting from dispersal to new areas or via the evolution of traits, called key innovations, that allow for invasion of new niches. Species sampling is a known source of bias in many comparative analyses, yet classic adaptive radiations have not been studied comparatively with comprehensively sampled phylogenies. In this study, we use unprecedented comprehensive phylogenetic sampling of Anolis lizard species to examine comparative evolution in this well-studied adaptive radiation. We compare adaptive radiation models within Anolis and in the Anolis clade and a potential sister lineage, the Corytophanidae. We find evidence for island (i.e., opportunity) effects and no evidence for trait (i.e., key innovation) effects causing accelerated body size evolution within Anolis. However, island effects are scale dependent: when Anolis and Corytophanidae are analyzed together, no island effect is evident. We find no evidence for an island effect on speciation rate and tenuous evidence for greater speciation rate due to trait effects. These results suggest the need for precision in treatments of classic adaptive radiations such as Anolis and further refinement of the concept of adaptive radiation.

A Phylogenetic, Biogeographic, and Taxonomic study of all Extant Species of Anolis (Squamata; Iguanidae).

Anolis lizards (anoles) are textbook study organisms in evolution and ecology. Although several topics in evolutionary biology have been elucidated by the study of anoles, progress in some areas has been hampered by limited phylogenetic information on this group. Here, we present a phylogenetic analysis of all 379 extant species of Anolis, with new phylogenetic data for 139 species including new DNA data for 101 species. We use the resulting estimates as a basis for defining anole clade names under the principles of phylogenetic nomenclature and to examine the biogeographic history of anoles. Our new taxonomic treatment achieves the supposed advantages of recent subdivisions of anoles that employed ranked Linnaean-based nomenclature while avoiding the pitfalls of those approaches regarding artificial constraints imposed by ranks. Our biogeographic analyses demonstrate complexity in the dispersal history of anoles, including multiple crossings of the Isthmus of Panama, two invasions of the Caribbean, single invasions to Jamaica and Cuba, and a single evolutionary dispersal from the Caribbean to the mainland that resulted in substantial anole diversity. Our comprehensive phylogenetic estimate of anoles should prove useful for rigorous testing of many comparative evolutionary hypotheses. [Anoles; biogeography; lizards; Neotropics; phylogeny; taxonomy].

Phylogeny of Riama (Squamata: Gymnophthalmidae), impact of phenotypic evidence on molecular datasets, and the origin of the Sierra Nevada de Santa Marta endemic fauna.

Riama is the most speciose genus of the Neotropical lizard family Gymnophthalmidae. Its more than 30 montane species occur throughout the northern Andes, the Cordillera de la Costa (CC) in Venezuela, and Trinidad. We present the most comprehensive phylogenetic analysis of Riama to date based on a total evidence (TE) approach and direct optimization of molecular and morphological evidence. Analyses use DNA sequences from four loci and 35 phenotypic characters. The dataset consists of 55 ingroup terminals representing 25 of the 30 currently recognized species of Riama plus five undescribed taxa, including an endemic species from the Sierra Nevada de Santa Marta (SNSM) in Colombia, and 66 outgroup terminals of 47 species. Analysis results in a well-supported hypothesis in which Riama is polyphyletic, with its species falling into three clades. The Tepuian Anadia mcdiarmidi nests within one clade of Riama, and the recently resurrected Pantodactylus nests within Cercosaura. Accordingly, we propose a monophyletic taxonomy that reflects historical relationships. Analysis of character evolution indicates that the presence/absence of prefrontals-a cornerstone of the early genus-level taxonomy of cercosaurines-is optimally explained as having been plesiomorphically present in the most recent common ancestor of Cercosaurinae and lost in that of the immediately less inclusive clade. Multiple independent reversals to present and subsequent returns to absent occur within this clade. To evaluate the impact of phenotypic evidence on our results, we compare our TE results with results obtained from analyses using only molecular data. Although phenotypic evidence comprises only 1.2% of the TE matrix, its inclusion alters both the topology and support values of the clades that do not differ. Finally, current phylogenetic evidence reveals a SNSM-CC-Trinidad-tepuis biogeographical link. We hypothesize that an ancient connection facilitated the exchange of species between the SNSM and the CC.

Present diversity of Galápagos leaf-toed geckos (Phyllodactylidae: Phyllodactylus) stems from three independent colonization events.

We re-examined the biogeography of the leaf-toed geckos (Phyllodactylus) endemic to the Galápagos Islands by analyzing for the first time samples of P. gilberti, a species endemic to Wolf island, in a phylogenetic framework. Our aim was to test the three-colonizations scenario previously proposed for these lizards and estimate the age of each colonization event. To achieve this we estimated simultaneously a species tree and divergence times with Bayesian methods. Our results supported the three-colonizations scenario. Similar to a previous hypothesis, the species tree obtained here showed that most species of Phyllodactylus are nested in a single clade with an age between 5.49 and 13.8Ma, whereas a second independent colonization corresponding to P. darwini from San Cristóbal island occurred 3.03Ma ago. The species from Wolf island, P. gilberti, stems from a more recent colonization event (0.69Ma). Thus, present diversity of Galápagos leaf-toed geckos stems from three independent, asynchronous colonization events. As with other Galápagos organisms, the Pacific coast of South America seems to be the source for the founders of P. gilberti.

Phylogeny and biogeography of the most diverse clade of South American gymnophthalmid lizards (Squamata, Gymnophthalmidae, Cercosaurinae).

Nearly 50% of the diversity of the speciose Neotropical lizard clade Gymnophthalmidae is nested within the subclade Cercosaurinae. The taxonomy of Cercosaurinae lizards has been historically confusing because many diagnostic characters of those clades traditionally ranked as genera do not represent true diagnostic apomorphies. Even though molecular phylogenies of several 'genera' have been presented in the last few years, some of them remain poorly sampled (e.g., Anadia, Echinosaura, Potamites, Riama). In this paper we present a more comprehensive phylogeny of Cercosaurinae lizards with emphasis on Andean taxa from Ecuador and Peru, as well as a time-calibrated phylogeny with reconstruction of ancestral areas. Our analysis includes 52% of all recognized species of Cercosaurinae (67 species) and 1914 characters including three mitochondrial and one nuclear gene. We find that Anadia, Echinosaura, Euspondylus, Potamites, Proctoporus, and Riama are not monophyletic: the Tepuian Anadia mcdiarmidi is not sister to Andean species of Anadia; Echinosaura sulcarostrum is not included in the same clade formed by other species of Echinosaura and their more recent common ancestor; Teuchocercus is nested within Echinosaura; species of Euspondylus included in this study are nested within Proctoporus; Riama laudahnae is included in Proctoporus; and Potamites is paraphyletic and split in two separate clades, one of which we name Gelanesaurus, also a new genus-group name. Within Potamites, P. ecpleopus is paraphyletic, and P. strangulatus strangulatus and P. strangulatus trachodus are recognized as two distinct species. We also identify three unnamed clades (i.e., not nested within any of the recognized 'genera') from Andean populations in Ecuador and Peru. The estimated age of the clade Cercosaurinae (∼60Ma) corresponds to the early stages of the northern Andes. Even though the distribution of the most recent common ancestor of Cercosaurinae remains equivocal, our analysis shows that these lizards colonized and radiated along the northern Andes before reaching the central Andes in Peru. Finally, we present phylogenetic definitions for some of the recovered clades to promote a clear and precise classification of Cercosaurinae lizards.

Short-term predicted extinction of Andean populations of the lizard Stenocercus guentheri (Iguanidae: Tropidurinae).

We studied the thermal physiology of the Andean lizard Stenocercus guentheri in order to evaluate the possible effects of global warming on this species. We determined the preferred body temperature (Tpref), critical thermals (CTmin, CTmax), and hours of restriction and activity. Tpref was 32.14±1.83°C; CTmin was 8.31°C in adults and 9.14°C in juveniles, whereas CTmax was 43.28°C in adults and 41.68°C in juveniles. To assess extinction risk, we used the model created by Sinervo et al. (2010) and predicted that 16.7% of populations will have a high risk of extinction by 2020, with an increase to 26.7% by 2050. These results suggest that this species, despite being able to maintain its Tpref through behavioral thermoregulation and habitat selection, could be physiologically sensitive to climate warming; thus, the potential for local adaptation may be limited under a warmer climate. Further studies focusing on the ability of S. guentheri to evolve higher Tpref and thermal tolerances are needed to understand the ability of this species to respond to climate change.

Phylogeny of Neotropical Cercosaura (Squamata: Gymnophthalmidae) lizards.

Among Neotropical lizards, the geographically widespread gymnophthalmid Cercosaura as currently defined includes lowland and highland taxa from Panama to Argentina, with some species occurring in the northern Andes. In this study we analyze three mitochondrial (12S, 16S, ND4) and one nuclear (c-mos) gene using Bayesian methods to clarify the phylogenetic relationships among most species of Cercosaura based on a well-supported phylogenetic hypothesis that also includes a large sample of other taxa within Cercosaurini. The phylogenetic tree obtained in this paper shows that Cercosaura as currently defined is not monophyletic. Two species from the northern Andes (C. dicra and C. vertebralis) are nested within Pholidobolus, which has been formerly recognized as a major radiation along the Andes of Ecuador and Colombia. Therefore, Cercosaura has probably not diversified in the northern Andes, although the phylogenetic position of C. hypnoides from the Andes of Colombia remains unknown. Tree topology and genetic distances support both recognition of C. ocellata bassleri as a distinct species, C. bassleri, and recognition of C. argula and C. oshaughnessyi as two different species. In the interest of promoting clarity and precision regarding the names of clades of gymnophthalmid lizards, we propose a phylogenetic definition of Cercosaura.

Cost-effectiveness of using small vertebrates as indicators of disturbance.

In species-rich tropical forests, effective biodiversity management demands measures of progress, yet budgetary limitations typically constrain capacity of decision makers to assess response of biological communities to habitat change. One approach is to identify ecological-disturbance indicator species (EDIS) whose monitoring is also monetarily cost-effective. These species can be identified by determining individual species' responses to disturbance across a gradient; however, such responses may be confounded by factors other than disturbance. For example, in mountain environments the effects of anthropogenic habitat alteration are commonly confounded by elevation. EDIS have been identified with the indicator value (IndVal) metric, but there are weaknesses in the application of this approach in complex montane systems. We surveyed birds, small mammals, bats, and leaf-litter lizards in differentially disturbed cloud forest of the Ecuadorian Andes. We then incorporated elevation in generalized linear (mixed) models (GL(M)M) to screen for EDIS in the data set. Finally, we used rarefaction of species accumulation data to compare relative monetary costs of identifying and monitoring EDIS at equal sampling effort, based on species richness. Our GL(M)M generated greater numbers of EDIS but fewer characteristic species relative to IndVal. In absolute terms birds were the most cost-effective of the 4 taxa surveyed. We found one low-cost bird EDIS. In terms of the number of indicators generated as a proportion of species richness, EDIS of small mammals were the most cost-effective. Our approach has the potential to be a useful tool for facilitating more sustainable management of Andean forest systems.

Evolutionary history of Andean Pholidobolus and Macropholidus (Squamata: Gymnophthalmidae) lizards.

Andean Pholidobolus and Macropholidus lizards contain seven and two species, respectively, as currently recognized. We analyze three mitochondrial loci (12S, 16S, ND4) using Bayesian methods to clarify the phylogenetic relationships between these genera based on a well-supported phylogenetic hypothesis. The phylogenetic tree obtained in this paper includes two main clades and shows that both Pholidobolus and Macropholidus are not monophyletic. A chronophylogenetic analysis indicates that the southernmost clade, occurring in the Huancabamba Depression, diversified earlier than the northern-Andes clade. Bayesian hypothesis tests reject previous phylogenetic hypotheses. We propose phylogenetic definitions for the main clades inferred herein.

Feeding ecology of the Terciopelo pit viper snake (Bothrops asper) in Ecuador.

Thoroughly documenting prey items and diet composition is crucial for understanding a predator's role in the ecosystem. In gape restricted predators, such as snakes, documenting and analyzing the type and size of the prey is important to interpret their ecological role. We describe the diet patterns of a species of venomous snake, the Terciopelo pit viper (Bothrops asper), from its Ecuadorian populations. Examining the gastrointestinal contents of museum specimens collected over an extensive area of the Pacific lowlands of Ecuador, we encountered 69 identifiable prey items from four major taxonomic groups (amphibians, centipedes, mammals, and reptiles). We evaluated the observed composition of prey to check for differences between sexes and size-classes. To complement our observations of the Terciopelo species complex throughout their distribution, we carried out a systematic literature review. Our data show an ontogenetic shift in diet, with a transition from more diverse diet in juveniles towards a mammal-specialized diet in adults, and distinct proportion of prey taxa between the sexes in the juvenile size class.

Global Protected Areas as refuges for amphibians and reptiles under climate change.

Protected Areas (PAs) are the cornerstone of biodiversity conservation. Here, we collated distributional data for >14,000 (~70% of) species of amphibians and reptiles (herpetofauna) to perform a global assessment of the conservation effectiveness of PAs using species distribution models. Our analyses reveal that >91% of herpetofauna species are currently distributed in PAs, and that this proportion will remain unaltered under future climate change. Indeed, loss of species' distributional ranges will be lower inside PAs than outside them. Therefore, the proportion of effectively protected species is predicted to increase. However, over 7.8% of species currently occur outside PAs, and large spatial conservation gaps remain, mainly across tropical and subtropical moist broadleaf forests, and across non-high-income countries. We also predict that more than 300 amphibian and 500 reptile species may go extinct under climate change over the course of the ongoing century. Our study highlights the importance of PAs in providing herpetofauna with refuge from climate change, and suggests ways to optimize PAs to better conserve biodiversity worldwide.

A new and very spiny lizard (Gymnophthalmidae: Echinosaura) from the Andes in northwestern Ecuador.

We describe a new species of Neotropical spiny-lizard of the genus Echinosaura from the Imbabura and Carchi Provinces on the western slopes of the Andes in northwestern Ecuador. The new species mostly resembles E. horrida. However, it can be distinguished from all congeners by having keeled enlarged dorsal scales forming a paired vertebral row, two paravertebral series of short oblique rows of projecting scales, and a pair of spine-like scales on temporal and nuchal regions. We also provide a detailed description of the osteology of the skull and pectoral girdle of the new species and present a phylogenetic hypothesis for Echinosaura based on three mitochondrial genes (12S, 16S, ND4) and one nuclear gene (c-mos).

A new giant anole (Squamata: Iguanidae: Dactyloinae) from southwestern Ecuador.

We describe a new species of Anolis lizard from the Pacific slopes of the Andes of southwestern Ecuador at elevations between 3721,000 m. The new species belongs to the Dactyloa clade and may be distinguished from other Anolis by size, external anatomy, mitochondrial DNA divergence, and dewlap color. Based on phylogenetic analyses of mitochondrial and nuclear DNA sequence data, we found that the new species is sister to A. fraseri in a clade composed primarily of large Dactyloid species. The new species is known from a protected area in southern Ecuador, Buenaventura Reserve, which suggests that at least some its populations are well protected.

Systematics of Pholidobolus lizards (Squamata, Gymnophthalmidae) from southern Ecuador, with descriptions of four new species.

Four new species of Pholidobolus lizards are described from poorly explored areas in the Andes of southern Ecuador based on morphological and genetic evidence. Among other morphological characters, Pholidobolus samek sp. nov. and P. condor sp. nov. differ from their congeners in having green dorsolateral stripes on head. Males of P. condor sp. nov. differ from those of P. samek sp. nov. in having reddish flanks and venter. P. dolichoderes sp. nov. is distinguished by having a long neck, with more scales between orbit and tympanum, whereas P. fascinatus sp. nov. is distinguished by lacking enlarged medial scales on collar and a conspicuous vertebral stripe. In addition, the phylogenetic position of the new species is inferred using DNA sequences of mitochondrial and nuclear genes. The phylogeny supports strongly monophyly of each of the new species and renders P. macbrydei paraphyletic and split into six subclades. Available data suggest that the new species have restricted distribution ranges (< 100 km2 each), and it is proposed that their classification be as Data Deficient or Critically Endangered species. The results reveal unexpected levels of diversity within Pholidobolus in the Andes of southern Ecuador and highlight the importance of improving scientific collections and conservation efforts in this area.