Thermal niches and activity periods in syntopic Phymaturus and Liolaemus lizards from the Andes, Argentina.

Explanations for differences in thermal biology within and between species of lizards employ concepts of phylogenetic inertia and plasticity. We compared the thermal biology of three liolaemid species in the Andean highlands in Argentina: two allopatric congeners (Phymaturus williamsi and P. aguanegra) each in syntopy with Liolaemus parvus. We predicted intra and inter-generic differences in ecophysiological traits and periods of activity at both sites, ecotypic differences between the (labile) Liolaemus populations, but predicted no interspecific differences between the (putatively conservative) Phymaturus. We determined the operative temperatures (T e), field body temperatures (T b), preferred temperatures (T pref), effectiveness of thermoregulation (E), and activity periods. As expected, P. williamsi differed from L. parvus in T b, T pref, and activity periods, likely as result of niche segregation. Contrary to predictions, the Phymaturus populations exhibited differentiation in T b and T pref, while L. parvus populations differed in T pref and E. Accordingly, Phymaturus species tend to be effective thermoregulators whereas L. parvus populations behave as good thermoregulators or thermoconformers depending on thermal conditions in fluctuating habitats. Phymaturus may be less evolutionarily conservative than previously suggested. The suite of co-evolving traits affecting thermal ecology may not be collectively conservative nor labile but rather a continuum between both evolutionary paths.

High reproductive effort in a vulnerable lizard from high altitudes in Argentina: Reproductive biology and sexual dimorphism in Phymaturus extrilidus.

Reproductive biology is fundamental to understanding the ecology and evolution of lizards which, in turn, is essential for the definition of the species´ conservation status. We studied life-history traits related to the reproduction of the Phymaturus extrilidus lizard, including the male and female reproductive cycles, litter size, mean annual reproductive output, reproductive effort, sexual maturity size and sexual dimorphism, body condition, and fat body cycles. We found sexual dimorphism in size and shape, supporting the hypotheses of sexual and fecundity selection. Females exhibited biennial reproductive cycles synchronous with the annual prenuptial male cycle, adjusted for the maturation of the vitellogenic follicles of females. Females of P. extrilidus have the highest mean annual reproductive output (MARO=1.14) recorded in Phymaturus, and this is accompanied by the highest reproductive effort (C=0.28, C energetic =0.31). Births occur from late summer to early autumn. The female reproductive cycle, strictly biennial, like all species of the P. palluma group, and the vitellogenesis in particular, appear to be limited by body condition and the amount of fat body stored. This study presents the fundamental reproductive traits of P. extrilidus that can provide valuable information to be used in the evaluation of the conservation status of this species.

Could plasticity mediate highlands lizards' resilience to climate change? A case study of the leopard iguana (Diplolaemus leopardinus) in Central Andes of Argentina.

The predicted rise of global temperatures is of major concern for ectotherms because of its direct impact on their behavior and physiology. As physiological performance mediates a species' resilience to warming exposure, physiological plasticity could greatly reduce the susceptibility to climate change. We studied the degree to which Diplolaemus leopardinus lizards are able to adjust behavioral and physiological traits in response to short periods of temperature change. We used a split cross design to measure the acclimation response of preferred body temperature (Tp), and the thermal performance curve of resting metabolic rate (RMR) and evaporative water loss (EWL). Our results showed that plasticity differs among traits: whereas Tp and EWL showed lower values in warm conditions, the body temperature at which RMR was highest increased. Moreover, RMR was affected by thermal history, showing a large increase in response to cold exposure in the group initially acclimated to warm temperatures. The reduction of EWL and the increase in optimal temperature will give lizards the potential to partially mitigate the impact of rising temperatures in the energy cost and water balance. However, the decrease in Tp and the sensitivity to the warm thermal history of RMR could be detrimental to the energy net gain, increasing the species' vulnerability, especially considering the increase of heat waves predicted for the next 50 years. The integration of acclimation responses in behavioral and physiological traits provides a better understanding of the range of possible responses of lizards to cope with the upcoming climatic and environmental modifications expected as a result of climate change.

Looking at the past to infer into the future: Thermal traits track environmental change in Liolaemidae.

The diversity of habitats generated by the Andes uplift resulted a mosaic of heterogeneous environments in South America for species to evolve a variety of ecological and physiological specializations. Species in the lizard family Liolaemidae occupy a myriad of habitats in the Andes. Here, we analyze the tempo and mode of evolution in the thermal biology of liolaemids. We assessed whether there is evidence of local adaptation (lability) or conservatism (stasis) in thermal traits. We tested the hypothesis that abiotic factors (e.g., geography, climate) rather than intrinsic factors (egg-laying [oviparous] or live-bearing [viviparous], substrate affinity) explain variation in field active body temperature (Tb ), preferred temperature (Tp ), hours of restriction of activity, and potential hours of activity. Although most traits exhibited high phylogenetic signal, we found variation in thermal biology was shaped by geography, climate, and ecological diversity. Ancestral character reconstruction showed shifts in Tb tracked environmental change in the past ∼20,000 years. Thermal preference is 3°C higher than Tb , yet exhibited a lower rate of evolution than Tb and air temperature. Viviparous Liolaemus have lower Tb s than oviparous species, whereas Tp is high for both modes of reproduction, a key difference that results in a thermal buffer for viviparous species to cope with global warming. The rapid increase in environmental temperatures expected in the next 50-80 years in combination with anthropogenic loss of habitats are projected to cause extirpations and extinctions in oviparous species.

Impact of temperature on bite force and bite endurance in the leopard iguana (Diplolaemus leopardinus) in the Andes Mountains.

In ectotherms, temperature exerts a strong influence on the performance of physiological and ecological traits. One approach to understanding the impact of rising temperatures on animals and their ability to cope with climate change is to quantify variation in thermal-sensitive traits. Here, we examined the thermal biology, temperature dependence and thermal plasticity of bite force (endurance and magnitude) in Diplolaemus leopardinus, an aggressive and territorial lizard endemic to Mendoza province, Argentina. Our results indicate that this lizard behaves like a moderate thermoregulator that uses the rocks of its environment as the main heat source. Bite endurance was not influenced by head morphometry and body temperature, whereas bite force was influenced by head length and jaw length, and exhibited thermal dependence. Before thermal acclimation treatments, the maximum bite force for D. leopardinus occurred at the lowest body temperature and fell sharply with increasing body temperature. After acclimation treatments, lizards acclimated at higher temperatures exhibited greater bite force. Bite force showed phenotypic plasticity, which reveals that leopard iguanas are able to maintain (and even improve) their bite force under a rising-temperature scenario.

An updated phylogeny and morphological study of the Phymaturus vociferator clade (Iguania: Liolaemidae).

Species delimitation in Phymaturus has been a difficult task due to the highly conserved morphological and ecological features present in this genus. Almost all species of Phymaturus have been described without DNA data or lacking statistical analyses which makes even more difficult to compare species. Although two molecular phylogenetic studies have been recently published, here we provide the first multilocus phylogenetic reconstruction including all Chilean species, with samples from all type localities and some previously unsampled populations. We also estimate pairwise distances among the Chilean species of Phymaturus (P. vociferator and P. mallimaccii clades) and compare our results with the P. payuniae clade, where previous studies have used multiple lines of evidence. Additionally, we performed univariate and multivariate morphological analyses and skeletal comparisons (clavicle) for the species of the P. vociferator clade. As a result of this integrative approach, we describe a new species.

Thermal biology in two syntopic lizards, Phymaturus extrilidus and Liolaemus parvus, in the Puna region of Argentina.

Body temperature is the most important ecophysiological variable affecting reptiles' life history. Moreover, thermoregulation in ectotherms implies a struggle to reach preferred temperatures in natural conditions due to the influence of biotic and abiotic factors. Our objective was to evaluate and compare the thermal biology of two syntopic species, Phymaturus extrilidus and Liolaemus parvus, in the Puna region of San Juan, Argentina. We determined body temperature (Tb), micro-environmental temperatures (Ta and Ts) and operative temperatures (Te) in the field. In the laboratory, we measured preferred temperatures (Tpref) and calculated the index of thermoregulatory efficiency (E). Neither body temperatures in the field nor preferred temperatures varied between seasons and sexes. Body temperatures were lower than preferred temperatures for both species. Nevertheless, regardless of the low thermal offer available in habitat, both species did achieve body temperatures higher than operative temperatures during activity. Thermoregulatory effectiveness was moderate in P. extrilidus (E=0.65), while L. parvus presented greater thermoregulatory efficiency (E=0.78). We conclude that under the rigorous climate conditions of the Puna, Phymaturus extrilidus and Liolaemus parvus are able to actively and efficiently thermoregulate, maintaining body temperatures close to the preferred and higher than those of its habitat. Differences in thermal characteristics between Phymaturus extrilidus and Liolaemus parvus are a consequence of differential limitations imposed on each species by the environment and of forces inherent to their life histories.

Gut microbial ecology of lizards: insights into diversity in the wild, effects of captivity, variation across gut regions and transmission.

Animals maintain complex associations with a diverse microbiota living in their guts. Our understanding of the ecology of these associations is extremely limited in reptiles. Here, we report an in-depth study into the microbial ecology of gut communities in three syntopic and viviparous lizard species (two omnivores: Liolaemus parvus and Liolaemus ruibali and an herbivore: Phymaturus williamsi). Using 16S rRNA gene sequencing to inventory various bacterial communities, we elucidate four major findings: (i) closely related lizard species harbour distinct gut bacterial microbiota that remain distinguishable in captivity; a considerable portion of gut bacterial diversity (39.1%) in nature overlap with that found on plant material, (ii) captivity changes bacterial community composition, although host-specific communities are retained, (iii) faecal samples are largely representative of the hindgut bacterial community and thus represent acceptable sources for nondestructive sampling, and (iv) lizards born in captivity and separated from their mothers within 24 h shared 34.3% of their gut bacterial diversity with their mothers, suggestive of maternal or environmental transmission. Each of these findings represents the first time such a topic has been investigated in lizard hosts. Taken together, our findings provide a foundation for comparative analyses of the faecal and gastrointestinal microbiota of reptile hosts.

Physiological and microbial adjustments to diet quality permit facultative herbivory in an omnivorous lizard.

While herbivory is a common feeding strategy in a number of vertebrate classes, less than 4% of squamate reptiles feed primarily on plant material. It has been hypothesized that physiological or microbial limitations may constrain the evolution of herbivory in lizards. Herbivorous lizards exhibit adaptations in digestive morphology and function that allow them to better assimilate plant material. However, it is unknown whether these traits are fixed or perhaps phenotypically flexible as a result of diet. Here, we maintained a naturally omnivorous lizard, Liolaemus ruibali, on a mixed diet of 50% insects and 50% plant material, or a plant-rich diet of 90% plant material. We compared parameters of digestive performance, gut morphology and function, and gut microbial community structure between the two groups. We found that lizards fed the plant-rich diet maintained nitrogen balance and exhibited low minimum nitrogen requirements. Additionally, lizards fed the plant-rich diet exhibited significantly longer small intestines and larger hindguts, demonstrating that gut morphology is phenotypically flexible. Lizards fed the plant-rich diet harbored small intestinal communities that were more diverse and enriched in Melainabacteria and Oscillospira compared with mixed diet-fed lizards. Additionally, the relative abundance of sulfate-reducing bacteria in the small intestine significantly correlated with whole-animal fiber digestibility. Thus, we suggest that physiological and microbial limitations do not sensu stricto constrain the evolution of herbivory in lizards. Rather, ecological context and fitness consequences may be more important in driving the evolution of this feeding strategy.

The rediscovery of Oplurus bibronii Guichenot, 1848 a valid species of the liolaemid genus Phymaturus (Iguania: Liolaemidae).

Oplurus bibronii was a species described more than 160 years ago from the highlands of Ovalle, Chile. The species was earlier synonymized with Phymaturus palluma and since then its taxonomic status has not been re-examined. In February of 2011, we were successful in capturing specimens of Phymaturus in the highlands of Ovalle and additionally we examined high quality digital pictures of the type series of O. bibronii. Our analysis shows that the type series is composed of two different species, one of which overlaps their diagnostic characters with the characters of the specimens collected in the highlands of Ovalle, and therefore they correspond to Phymaturus bibronii (new combination). In addition, our review of the holotype, and some paratypes and topotypes of the recently described P. paihuanense shows that this is a junior synonym of P. bibronii.

Description of new andean species of the genus Phymaturus (Iguania: Liolaemidae) from Northwestern Argentina.

As a result of several field trips and studies of collections of Phymaturus samples from Andean areas of central western Argentina (San Juan province), we discovered two populations that exhibit a particular character combination not seen in other species formally recognized in the literature. Based on a detailed analysis of an extended list of morphological characters (93), including scalation, color pattern, gular and nuchal folds, precloacal pores, and morphometric data, we conclude that these populations represent independent lineages that deserve to be considered as new species. According to the most recent revision of the genus and considering the descriptions made in another recent contribution, the taxonomic composition of the genus was increased to 38 species. In this study we provide the formal description of two additional new taxa, including their diagnosis and detailed comparisons with other members of their species group. The two new species belong to the palluma group, and can be assigned to the Puna subclade because they present the typical dorsal "spray" pattern. Other characters described in this study suggest their close phylogenetic relationship with other species of this subclade inhabiting the southern Puna region of Argentina, such as Phymaturus punae. Within the Puna subclade, Phymaturus aguanegra sp. nov. differs from all other members (P. antofagastensis, P. denotatus, P. laurenti, P punae, P extrilidus, P mallimaccii and P paihuanense) exhibiting the following combination of diagnostic characters: a complete melanism over the dorsum of neck, the presence of enlarged scales at the base of tail in males, having strongly keeled tarsal scales, lacking enlarged scales on the anterior margin of the antehumeral fold and centre of chest, females without flank coloration, a vertebral dark gray stripe usually present on the dorsum, females exhibiting a tricolor dorsal pattern, with two types of brown and scattered ferriferous oxide spots, and the absence of a scapular spot. Phymaturus williamsi sp. nov. differs from all other members of the Puna clade because: exhibits an "aggregate" dorsal pattern, unlike the homogeneous spray of most Puna species, lacks enlarged scales on the anterior margin of the antehumeral fold and in the centre of chest, flank coloration in females is absent, females of Phymaturus williamsi sp. nov. lack white transversal stripes on the dorsal pattern, preocular scale in contact with canthal scale in Phymaturus williamsi sp. nov., rostral scale can be divided in Phymaturus williamsi sp. nov. and shows the largest number of scales counted around midbody within the Puna subclade (x= 213.4; 186-235).

First record of partial albinism and scoliosis in Odontophrynus occidentalis tadpoles (Anura: Cycloramphidae)

Albinism has been widely reported for diverse group of vertebrates. However, scoliosis is a rare abnormality. In this work, the first record of partial albinism and scoliosis case in tadpole of the frog Odontophrynus occidentalis is being presented. The individual was captured in Quebrada de las Flores, Sierra Pie de Palo, Caucete Department, San Juan Province, Argentina.