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.

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.

Thermal biology and locomotor performance in Phymaturus calcogaster: are Patagonian lizards vulnerable to climate change?

Behavioral and physiological traits of ectotherms are especially sensitive to fluctuations of environmental temperature. In particular, niche-specialist lizards are dependent on their physiological plasticity to adjust to changing environmental conditions. Lizards of the genus Phymaturus are viviparous, mainly herbivorous, and inhabit only rock promontories in the steppe environments of Patagonia and the Andes. Herein, we examine the vulnerability of the southernmost Phymaturus species to global warming: the endemic Phymaturus calcogaster, which lives in a mesic environment in eastern Patagonia. We studied body temperatures in the field (Tb ), preferred body temperatures in a thermogradient (Tpref ), the operative (Te ) and environmental temperatures, and the dependence of running performance on body temperature. P. calcogaster had a mean Tb (27.04°C) and a mean Te (31.15°C) both lower than their preferred temperature (Tpref = 36.61°C) and the optimal temperature for running performance (To = 37.13°C). Lizard activity seems to be restraint during the early afternoon due high environmental temperatures. However, both, the high safety margin and warming tolerance suggest that the expected increase in environmental temperatures due to global warming (IPCC report in 2018) would not threaten, but indeed enhance locomotor performance in this population.

Impact of immunological state on eco-physiological variables in one of the southernmost lizards in the world.

The immune state is an essential component of survival as it directly influences physiological performance and health status. Variation in the leukocyte profile, a significantly increase in body temperature, and a detriment of the eco-physiological performance are among the possible consequences of an unhealthy state. In this study we analyse and discuss how field body temperature, preferred body temperature, the speed for sprint and long runs, locomotor stamina, and body condition can be affected by the immunological state (i.e. leukocyte profile) in a wild population of Liolaemus sarmentoi. Juveniles and adult males with a high percentage of eosinophils, basophils, and a low percentage of monocytes preferred higher body temperatures in a thermal gradient, while pregnant females maintained thermal preferences independently of leukocyte profile. Although juveniles with a high percentage of heterophils showed less locomotor stamina, adult males and pregnant females showed no differences in locomotor performance in relation to leukocyte profile. This study represents a starting point in eco-immunology of a wild lizard population of Liolaemus in cold and temperate environments of Patagonia where the southward shift in the geographic ranges of pathogen populations due to global warming represents a threat to resident host populations.

Behavioral and physiological polymorphism in males of the austral lizard Liolaemus sarmientoi.

Integrative behavioral studies show that the interplay between individual physiology and social behavior influences the ecology of the species, ultimately affecting individual fitness. Particularly in lizards, color polymorphism is associated with differential behaviors and reproductive strategies, which are evident in mature males during the mating season. Dominant males generally have greater endurance, higher body temperature, and larger bodies than submissive males, so they can acquire and defend larger territories and have greater access to females for mating. We studied whether the color morphs observed in males of one of the world's southernmost reptiles, Liolaemus sarmientoi, are related to behavioral variation during agonistic interactions, thermal physiology, morphology, and/or locomotor stamina. Liolaemus sarmientoi males exhibit three color morphs: red (RR), red-yellow (RY), and yellow (YY). These lizards exhibit subtle behavioral displays and we did not observe stamina differences among morphs. However, we found that RR males are more aggressive than YY males during agonistic encounters. In addition, greater body temperature change during trials, higher field body temperatures, and greater head sizes of RR males compared to RY or YY indicate that RR is a dominant morph, which may influence their ability to acquire and defend territory and tactics for achieving reproductive success.

Reproductive strategies in males of the world's southernmost lizards.

Reproductive and life history patterns in reptiles are tightly related to the environmental conditions, so male reproductive cycles have been historically characterized as continuous, for tropical lizards, or seasonal, for temperate lizards. However, males of Liolaemus and Phymaturus lizards (Liolaemidae), from cold temperate climates of high altitudes or latitudes in Argentina and Chile, have developed a variety of reproductive cycles to coordinate with the short female reproductive season and to deal with the low frequency of reproductive females in the population. Using gonadal histology and morphological analysis, we describe the male reproductive biology, fat storage and sexual dimorphism of the viviparous lizards Liolaemus sarmientoi and Liolaemus magellanicus that inhabit an austral grass steppe at 51°S, in the southern limit of the American continent. Males of L. sarmientoi and L. magellanicus are reproductively available during the entire activity season of approximately 5 months. In addition, males of both species exhibit greater body sizes than females in morphological variables relevant in sexual selection. Meanwhile, females of both species exhibit larger inter-limb length than conspecific males, which suggests fecundity selection to increase space for a larger litter size. The continuous sperm production throughout the activity season allows these liolaemids to mate at any time when females ovulate, representing a selective advantage to deal with the short activity season and the adversities of the cold environment they inhabit.

Vulnerability to climate change of Anolis allisoni in the mangrove habitats of Banco Chinchorro Islands, Mexico.

As niche specialist species, lizards from tropical environments are characterized by a low tolerance and high physiological sensitivity to temperature changes. The extent of vulnerability to thermal changes depends on the lizard's physiological plasticity to adjust the environmental changes. Herein we studied the thermal biology of Anolis allisoni, an endemic arboreal lizard from the tropical islands of the Banco Chinchorro Biosphere Reserve, Mexico, carried out during April and May 2012 and April 2014. We report field body (Tb) and preferred body temperatures in the laboratory (Tpref), operative temperatures (Te) and restriction of hours of activity. Anolis allisoni showed high and identical Tb and Tpref (33°C), not significantly different than the mean Te (32.15°C). The effectiveness of thermoregulation (E=-0.30) and the analysis of hours of restriction suggested that the high temperatures of Te (40-62.5°C) registered at midday (from 12:00 to 15:00) of A. allisoni habitat are hostile and force lizards to take refuge during a period of 3h of their daily time of activity. The scarcity of opportunities to find alternative refuges for thermoregulation in Banco Chinchorro point out the vulnerability of A. allisoni and the risk of local extinction when considering future predictions of increase in global environmental temperatures.