Closing the knowledge gap: Helminth parasites of freshwater turtles from the Chaco-Pampa Plain, Southern South America.

Six species of freshwater turtles dominate the Chaco-Pampa Plain in southern South America and their parasites have been relatively understudied, with most records concentrated in Brazil. Particularly in Argentina, there are only scattered records of parasites for most of the turtles that inhabit the region, leaving a large knowledge gap. The purpose of the present contribution is to increase the knowledge of the internal parasites of six species of freshwater turtles from Argentina, after 15 years of fieldwork, by providing new hosts and additional geographic records for many host-parasite relationships. Some molecular sequences of the studied parasites were provided as a tool for better species identification. We processed 433 stomach and fecal samples from live individuals and visceral and soft tissue samples from 54 dissected turtles collected from a wide range and different ecoregions. We found 6230 helminths belonging to 18 taxa (one cestode, 11 digeneans and six nematodes). Fourteen new parasite-host associations are reported here, and for the first time parasites are recorded for Phrynops williamsi. This work contributes significantly to the knowledge of the parasitofauna in freshwater turtles in Argentina, providing a detailed list of parasites present in each turtle species and reporting molecular characters for future studies.

Does temperature at local scale explain thermal biology patterns of temperate tadpoles?

Most of the literature on temperature-organism interactions rely on mean temperature (mostly air), disregarding the real complexity of this variable. There is a growing consensus about the importance of considering the temperature fluctuations as a mechanism improving organism's performance. Tadpoles are small body size ectotherm organisms that behave isothermally with their environment. As such, are good models for studying their thermal biology relative to their immediate environment. We studied six anuran tadpole species in North Patagonia, Alsodes gargola, Hylorina sylvatica, Batrachyla taeniata, Pleurodema thaul, P. bufoninum and Rhinella spinulosa, distributed in a West-East altitudinal cline with different environments and thermal conditions. We evaluated the relationship between thermal descriptors at a local scale and the thermal biology patterns of these temperate tadpoles. We estimated thermal tolerance limits and thermal sensitivity of locomotion of each species. The different aquatic environments showed important differences in local thermal conditions, associated with observed differences in the thermal traits in these tadpoles. Species exposed to lower temperature fluctuations and lower environmental mean temperatures showed lower swimming optimal temperatures and narrower thermal tolerance ranges. We found greater variability in the upper than in the lower critical limits in these Patagonian anuran tadpoles. Minimum critical temperatures were close to freezing temperature, possibly in detriment of their tolerance to high temperatures. Overall, our results suggest that these species are adapted to low temperatures. Finally, warming tolerances and predicted thermal safety margins, show that none of the studied species appear to be under thermal stress that may compromise their survival at the present time or in the near future, under a moderate climate change scenario.

Early ontogeny and sequence heterochronies in Leiuperinae frogs (Anura: Leptodactylidae).

The study of early development in Neotropical Leiuperinae frogs (Anura, Leptodactylidae) has been addressed by several works in recent times. However, a comparative developmental approach under a phylogenetic context was not available. Herein we analyzed the morphological and ontogenetic diversity of embryos belonging to 22 species of the three largest genera in Leiuperinae. We find that in most cases, variations fit with the phylogeny at the inter- and intrageneric levels. Embryo kyphosis and whitish color are synapomorphies for the clade grouping Physalaemus and Engystomops. The presence of a third lower tooth row on the oral disc is plesiomorphic for Leiuperinae, only changing in derived clades. The configurations and developmental trajectories of the lower lip are exceptionally diverse. The developmental sequences optimized on the phylogenetic tree recover an early differentiated first lower tooth row a synapomorphy of Pseudopaludicola and Physalaemus, and an early differentiated second row as synapomorphy of Pleurodema. On the other hand, few features are highly conserved in the subfamily, such as the adhesive glands universally present in a type-C configuration. Our results also suggest that the morphology and ontogeny of embryos is in some cases associated to the environment where they develop. A large body size, poorly developed transient respiratory structures, large yolk provision and delayed development of the digestive tract occur convergently in embryos inhabiting cold, oxygenated environments. Embryos that develop in warmer water bodies in xeric environments show more complex and persistent transient respiratory structures and an early onset of hind limbs development. Our survey highlights that morphology and early development of anurans can be a valuable source of information for phylogenetic studies, and provide fundamental bases to explore and discuss how evolutionary changes can be shaped by environmental conditions.

How sensitive are temperate tadpoles to climate change? The use of thermal physiology and niche model tools to assess vulnerability.

Ectotherms are vulnerable to climate change, given their dependence on temperature, and amphibians are particularly interesting because of their complex life cycle. Tadpoles may regulate their body temperature by using suitable thermal microhabitats. Thus, their physiological responses are the result of adjustment to the local thermal limits experienced in their ponds. We studied three anuran tadpole species present in Argentina and Chile: Pleurodema thaul and Pleurodema bufoninum that are seasonal and have broad geographic ranges, and Batrachyla taeniata, a geographically restricted species with overwintering tadpoles. Species with restricted distribution are more susceptible to climate change than species with broader distribution that may cope with potential climatic changes in the environments in which they occur. We aim to test whether these species can buffer the potential effects of climate warming. We used ecological niche models and the outcomes of their thermal attributes (critical thermal limits, optimal temperature, and locomotor performance breadth) as empirical evidence of their capacity. We found that Pleurodema species show broader performance curves, related to their occurrence, while the geographically restricted B. taeniata shows a narrower thermal breadth, but is faster in warmer conditions. The modeled distributions and empirical physiological results suggest no severe threats for these three anurans. However, the risk level is increasing and a retraction of their distribution range might be possible for Pleurodema species, and some local population extinctions may happen, particularly for the narrowly distributed B. taeniata.

Effect of body mass and melanism on heat balance in Liolaemus lizards of the goetschi clade.

The body temperature of ectotherms depends on the environmental temperatures and behavioral adjustments, but morphology may also have an effect. For example, in colder environments, animals tend to be larger and to show higher thermal inertia, as proposed by Bergmann's rule and the heat balance hypothesis (HBH). Additionally, dark coloration increases solar radiation absorption and should accelerate heat gain (thermal melanism hypothesis, TMH). We tested Bergmann's rule, the HBH and the TMH within the ITALIC! Liolaemus goetschilizard clade, which shows variability in body size and melanic coloration. We measured heating and cooling rates of live and euthanized animals, and tested how morphology and color affect these rates. Live organisms show less variable and faster heating rates compared with cooling rates, suggesting behavioral and/or physiological adjustments. Our results support Bergmann's rule and the HBH, as larger species show slower heating and cooling rates. However, we did not find a clear pattern to support the TMH. The influence of dorsal melanism on heating by radiation was masked by the body size effect in live animals, and results from euthanized individuals also showed no clear effects of melanism on heating rates. Comparison among three groups of live individuals with different degrees of melanism did not clarify the influence of melanism on heating rates. However, when euthanized animals from the same three groups were compared, we observed that darker euthanized animals actually heat faster than lighter ones, favoring the TMH. Although unresolved aspects remain, body size and coloration influenced heat exchange, suggesting complex thermoregulatory strategies in these lizards, probably regulated through physiology and behavior, which may allow these small lizards to inhabit harsh weather environments.

Thermal sensitivity of cold climate lizards and the importance of distributional ranges.

One of the fundamental goals in macroecology is to understand the relationship among species' geographic ranges, ecophysiology, and climate; however, the mechanisms underlying the distributional geographic patterns observed remain unknown for most organisms. In the case of ectotherms this is particularly important because the knowledge of these interactions may provide a robust framework for predicting the potential consequences of climate change in these organisms. Here we studied the relationship of thermal sensitivity and thermal tolerance in Patagonian lizards and their geographic ranges, proposing that species with wider distributions have broader plasticity and thermal tolerance. We predicted that lizard thermal physiology is related to the thermal characteristics of the environment. We also explored the presence of trade-offs of some thermal traits and evaluated the potential effects of a predicted scenario of climate change for these species. We examined sixteen species of Liolaemini lizards from Patagonia representing species with different geographic range sizes. We obtained thermal tolerance data and performance curves for each species in laboratory trials. We found evidence supporting the idea that higher physiological plasticity allows species to achieve broader distribution ranges compared to species with restricted distributions. We also found a trade-off between broad levels of plasticity and higher optimum temperatures of performance. Finally, results from contrasting performance curves against the highest environmental temperatures that lizards may face in a future scenario (year 2080) suggest that the activity of species occurring at high latitudes may be unaffected by predicted climatic changes.

Chasing the Patagonian sun: comparative thermal biology of Liolaemus lizards.

The importance of the thermal environment for ectotherms and its relationship with thermal physiology and ecology is widely recognized. Several models have been proposed to explain the evolution of the thermal biology of ectotherms, but experimental studies have provided mixed support. Lizards from the Liolaemus goetschi group can be found along a wide latitudinal range across Argentina. The group is monophyletic and widely distributed, and therefore provides excellent opportunities to study the evolution of thermal biology. We studied thermal variables of 13 species of the L. goetschi group, in order to answer three questions. First, are aspects of the thermal biology of the L. goetschi group modelled by the environment or are they evolutionarily conservative? Second, have thermal characteristics of these animals co-evolved? And third, how do the patterns of co-evolution observed within the L. goetschi group compare to those in a taxonomically wider selection of species of Liolaemus? We collected data on 13 focal species and used species information of Liolaemus lizards available in the literature and additional data obtained by the authors. We tackled these questions using both conventional and phylogenetically based analyses. Our results show that lizards from the L. goetschi group and the genus Liolaemus in general vary in critical thermal minimum in relation to mean air temperature, and particularly the L. goetschi group shows that air temperature is associated with critical thermal range, as well as with body temperature. Although the effect of phylogeny cannot be ignored, our results indicate that these thermal biology aspects are modelled by cold environments of Patagonia, while other aspects (preferred body temperature and critical thermal maximum) are more conservative. We found evidence of co-evolutionary patterns between critical thermal minimum and preferred body temperature at both phylogenetic scales (the L. goetschi group and the extended sample of 68 Liolaemus species).

Running in cold weather: morphology, thermal biology, and performance in the southernmost lizard clade in the world (Liolaemus lineomaculatus section: Liolaemini: Iguania).

The integration or coadaptation of morphological, physiological, and behavioral traits is represented by whole-organism performance traits such as locomotion or bite force. Additionally, maximum sprint speed is a good indicator of whole-organism performance capacity as variation in sprinting ability can affect survival. We studied thermal biology, morphology, and locomotor performance in a clade of Liolaemus lizards that occurs in the Patagonian steppe and plateaus, a type of habitat characterized by its harsh cold climate. Liolaemus of the lineomaculatus section display a complex mixture of conservative and flexible traits. The phylogenetically informed analyses of these ten Liolaemus species show little coevolution of their thermal traits (only preferred and optimum temperatures were correlated). With regard to performance, maximum speed was positively correlated with optimum temperature. Body size and morphology influenced locomotor performance. Hindlimbs are key for maximal speed, but forelimb length was a better predictor for sustained speed (i.e. average speed over a total distance of 1.2 m). Finally, sustained speed differed among species with different diets, with herbivores running on average faster over a long distance than omnivores.