State-dependent movement choices of desert lizards: The role of behavioural thermoregulation during summer and winter.

Environmental temperatures are increasing worldwide, threatening desert ectotherms already living at their thermal limits. Organisms with flexible thermoregulatory behaviours may be able to mitigate the effects of extreme temperatures by moving among microhabitats, yet little work has tracked movement patterns of desert ectotherms in the wild over diurnal scales or compared behaviour among seasons. Here, we used camera traps to track the thermoregulatory behaviour and microhabitat choices of 30 desert lizards (Messalina bahaldini) in custom, outdoor arenas that provided access to open, rock, and bush microhabitats. We found that in the summer, lizards preferred to move to the shaded microhabitats and remain there under warmer conditions. During winter, however, lizards' activity was not related to temperature, and lizards mostly chose to remain in the open habitat. Interestingly, in both seasons, lizards tended to remain in their current microhabitat and moved infrequently between certain combinations of microhabitats. Our study shows that thermoregulation (shade-seeking behaviour) is a major factor during summer, helping lizards to avoid extreme temperatures, but not during winter, and shows a novel effect of current microhabitat on movement, suggesting that other biotic or abiotic factors may also drive microhabitat choice. Understanding the complex factors at play in microhabitat choice is critical for developing conservation programs that effectively mitigate the negative impacts of climate change on desert animals.

Cool shade and not-so-cool shade: How habitat loss may accelerate thermal stress under current and future climate.

Worldwide habitat loss, land-use changes, and climate change threaten biodiversity, and we urgently need models that predict the combined impacts of these threats on organisms. Current models, however, overlook microhabitat diversity within landscapes and so do not accurately inform conservation efforts, particularly for ectotherms. Here, we built and field-parameterized a model to examine the effects of habitat loss and climate change on activity and microhabitat selection by a diurnal desert lizard. Our model predicted that lizards in rock-free areas would reduce summer activity levels (e.g. foraging, basking) and that future warming will gradually decrease summer activity in rocky areas, as even large rocks become thermally stressful. Warmer winters will enable more activity but will require bushes and small rocks as shade retreats. Hence, microhabitats that may seem unimportant today will become important under climate change. Modelling frameworks should consider the microhabitat requirements of organisms to improve conservation outcomes.

Behavioural thermoregulation by the endangered crocodile lizard (Shinisaurus crocodilurus) in captivity.

Understanding the factors that may affect behavioural thermoregulation of endangered reptiles is important for their conservation because thermoregulation determines body temperatures and in turn physiological functions of these ectotherms. Here we measured seasonal variation in operative environmental temperature (Te), body temperature (Tb), and microhabitat use of endangered crocodile lizards (Shinisaurus crocodilurus) from a captive population, within open and shaded enclosures, to understand how they respond to thermally challenging environments. Te was higher in open enclosures than in shaded enclosures. The Tb of lizards differed between the open and shaded enclosures in summer and autumn, but not in spring. In summer, crocodile lizards stayed in the water to avoid overheating, whereas in autumn, crocodile lizards perched on branches seeking optimal thermal environments. Crocodile lizards showed higher thermoregulatory effectiveness in open enclosures (with low thermal quality) than in shaded enclosures. Our study suggests that the crocodile lizard is capable of behavioural thermoregulation via microhabitat selection, although overall, it is not an effective thermoregulator. Therefore, maintaining diverse thermal environments in natural habitats for behavioural thermoregulation is an essential measure to conserve this endangered species both in the field and captivity.

Thermal dependence of feeding performance and resting metabolic expenditure in different altitudinal populations of toad-headed lizards.

Inter-population variations in growth rate can result from independent or interactive effects of genetic and environmental factors, and be induced by some physiological differences as well. Toad-headed lizards (Phrynocephalus vlangalii) from a higher-elevation population were shown to have a higher growth rate than those from a lower-elevation population. The physiological basis of growth rate variation in this species is not well understood. Here, we investigated the feeding performance and resting metabolic rate (RMR) of lower- and higher-elevation individuals at different test ambient temperatures to evaluate the role of differences in energy intake, assimilation efficiency and metabolic expenditure on growth rate variations. Within the range of 25-35 °C, lizard RMR increased with increasing test ambient temperature, but food intake, apparent digestive coefficient (ADC, food energy minus faecal energy divided by food energy), and assimilation efficiency (AE, food energy minus faecal and urinary energy divided by food energy) were less thermally sensitive in both populations. Higher-elevation lizards tended to eat more food and have a lower RMR than lower-elevation ones, despite the lack of differences in ADC and AE. Our result showed that more energy intake and reduced maintenance cost may be associated with the higher growth rate of higher-elevation lizards. Accordingly, inter-population differences in energy acquisition and expenditure could act as potential sources for geographic variation in growth rate.

Environmental causes of between-population difference in growth rate of a high-altitude lizard.

BACKGROUND: Ectothermic animals living in cold (high latitude or high elevation) regions are predicted to grow slower due to limited thermal opportunities for activity and food resources than those living in warm regions. However, the Qinghai toad-headed lizards (Phrynocephalus vlangalii) grow faster and reach a larger adult size at a high-elevation site than at a low-elevation site. In this study, we aimed to identify the genetic and environmental causes of this between-population difference in growth rate by conducting mark-recapture and common garden experiments on juvenile growth rate, and investigating the thermal environment, lizard body temperature, potential prey availability at the two elevation sites. RESULTS: Compared with low-elevation individuals, high-elevation juvenile lizards had higher growth rates in the field, but grew at similar rates in the laboratory. High-elevation lizards had higher active body temperatures than low-elevation lizards despite similar air temperatures in the period of field investigation. The high-elevation site had relatively more and larger preys than the low-elevation site. CONCLUSIONS: Inter-population difference in growth rate of P. vlangalii may primarily result from developmental plasticity in response to the difference in environmental resources, rather than genetic differentiation. The higher growth rate of high-elevation lizards is likely associated with higher potential food availability and higher active body temperatures.

Low precipitation aggravates the impact of extreme high temperatures on lizard reproduction.

Extreme high temperatures are occurring more frequently with ongoing anthropogenic climate warming, but the experimental tests of the effects of high temperatures on terrestrial vertebrates in natural conditions are rare. In this study, we investigated the effects of extreme high temperatures on female reproduction and offspring traits of multi-ocellated racerunners (Eremias multiocellata) kept in field enclosures in the desert steppe of Inner Mongolia. Our studies indicate that high temperatures significantly affect the gestation period and reproductive output of females and the offspring sex ratio, but have little impact on offspring body size and mass. More interestingly, we found that the effect of extreme high temperatures on female reproductive output was not consistent between two consecutive years that differed in precipitation. Low precipitation may aggravate the impact of climate warming on lizards and negatively affect the survival of lizards in the desert steppe. Our results provide evidence that temperature interacts with precipitation to determine the life history of lizards, and they suggest that a drier and hotter environment, such as the future climate in arid mid-latitude areas, will likely impose severe pressure on lizard populations, which are an important component of the food web in desert areas around the world.

Rocks and Vegetation Cover Improve Body Condition of Desert Lizards during Both Summer and Winter.

Microhabitats provide ecological and physiological benefits to animals, sheltering them from predation and extreme temperatures and offering an additional supply of water and food. However, most studies have assumed no energetic costs of searching for microhabitats or moving between them, or considered how the availability of microhabitats may affect the energy reserves of animals and how such effects may differ between seasons. To fill these gaps, we studied how the body condition of lizards is affected by microhabitat availability in the extreme environment of the Judean Desert. In particular, we quantified how vegetation and rock cover in the vicinity of these lizards affect their body condition during summer and winter. First, we used aerial imagery to map the vegetation/rock cover at two study sites. Next, we collected 68 adult lizards and examined how their body condition varies across seasons and availability of vegetation and rock cover. In addition, we examined how vegetation and rock cover may differ in their effective distance (i.e., the distance that best explains body condition of lizards). We found that lizards body condition was better if they were collected closer to a higher availability of vegetation or rocks. However, while close proximity (within 10 m) was the best predictor for the positive effect of rocks, a greater distance (up to 90 m) was the best predictor for the effect of the vegetation cover. Moreover, the positive effect of vegetation was 12-fold higher than the effect of rocks. Interestingly, although the lizards' body condition during winter was poorer than during summer, the positive effects of rock and vegetation cover remained constant between the seasons. This similarity of benefits across seasons suggests that shaded microhabitats have important additional ecological roles regardless of climate, and that they may provide thermoregulatory benefits in winter too. We also found a synergic effect of vegetation and rock cover on the lizards' body condition, suggesting that their roles are complementary rather than overlapping. Our research has revealed the importance of shade- and shelter-providing microhabitats in both summer and winter. We suggest that proximity to microhabitat diversity may contribute to better body condition in lizards or, alternatively, facilitates competition and attracts lizards with better body condition. Comprehending the complex interactions between animals and different microhabitats is critical for developing better conservation plans, understanding the risks of climate change, and suggesting mitigation strategies.

The extract of aquatic macrophyte Carex cinerascens induced colony formation in bloom-forming cyanobacterium Microcystis aeruginosa.

Colony formation in Microcystis aeruginosa played important roles in blooms formation. To study the effects of plant allelopathy on colony formation in M. aruginosa, unicellular M. aeruginosa was cultivated under laboratory conditions treated with various extract concentration of Carex cinerascens. The growth of M. aeruginosa in the treatments with 0.05 and 0.1 mg L-1 extract of C. cinerascens was promoted but the growth in the treatments with 1.5, 3.0, and 6.0 mg L-1 C. cinerascens extract was inhibited. Obvious colony formation in M. aeruginosa was observed in all treatments while no colony formation was detected in the control. The cell number per colony at the first day was the largest and decreased along with culture time. The cell number per colony in the control ranged from 3.0 to 4.0 during the experiment. However, the values in the five treatments at the first day were 33, 80, 58, 41, and 30, respectively. A positive exponential relationship between cell number per colony of M. aeruginosa and extracellular polysaccharides (EPS) content was found as well. Compared the fold-increase in cell number per colony and the fold-increase in total biomass of M. aeruginosa at various day, it was found that colony formation induced by extract of C. cinerascens was primarily dependent on promotion of cell adhesion during the first 2 days. The cell number per colony decreased afterward was due to the increasing proportion of single cells in the culture because single cells had a great higher growth rate than M. aeruginosa colonies under culture condition. Our results suggested that plant allelopathy be one of the major factor contributing to colony formation in M. aeruginosa.

Different elevational patterns of rodent species richness between the southern and northern slopes of a mountain.

Studies on elevational gradients in biodiversity have accumulated in recent decades. However, few studies have compared the elevational patterns of diversity between the different slopes of a single mountain. We investigated the elevational distribution of rodent diversity (alpha and beta diversity) and its underlying mechanisms along the southern and northern slopes of Mt. Taibai, the highest mountain in the Qinling Mountains, China. The species richness of rodents on the two slopes showed distinct distribution patterns, with a monotonically decreasing pattern found along the southern slope and a hump-shaped elevational pattern evident along the northern slope. Multi-model inference suggested that temperature was an important explanatory factor for the richness pattern along the southern slope, and the mid-domain effect (MDE) was important in explaining the richness pattern along the northern slope. The two slopes also greatly differed in the elevational patterns of species turnover, with the southern slope demonstrating a U-shaped curve and the northern slope possessing a roughly hump-shaped pattern. Our results suggest that even within the same mountain, organisms inhabiting different slopes may possess distinct diversity patterns, and the underlying mechanisms may also differ. The potential role of the factors associated with slope aspect in shaping diversity, therefore, cannot be ignored.

Phylogeographical structure and demographic expansion in the endemic alpine stream salamander (Hynobiidae: Batrachuperus) of the Qinling Mountains.

The Qinling Mountains of China provide an excellent study area for assessing the effect of Pleistocene climatic oscillations and paleogeological events on intraspecific diversification. To assess genetic diversity of an endemic stream salamander, Batrachuperus tibetanus, for its conservation, a phylogeographical survey was performed based on mitochondrial DNA and morphological data. The mitochondrial data revealed three lineages of B. tibetanus in the Qinling Mountains. A lineage present in the northwestern Qinling Mountains groups with the Tibet lineage of B. tibetanus, and the remaining Qinling populations are eastern and western lineages that separated ~3-4 million years ago (Ma). The eastern and western Qinling lineage delineation is supported by three morphological variables (snout length, eye diameter and axilla-groin length). The divergence of the two major lineages was likely caused by orogenesis of the Qinling Mountains during the late Cenozoic, and the two lineages were subsequently affected at different levels by Pleistocene climatic oscillations showing different signals of demographic expansion. A large suitable area of B. tibetanus through the Qinling Mountains since the last glacial maximum (LGM) indicated the adaptation of this species to the climatic changes. However, low genetic diversity within populations indicate the urgency of preserving the vulnerable populations and endemic lineages.

Food restriction affects maternal investment but not neonate phenotypes in a viviparous lizard.

Food availability significantly affects an animal's energy metabolism, and thus its phenotype, survival, and reproduction. Maternal and offspring responses to food conditions are critical for understanding population dynamics and life-history evolution of a species. In this study, we conducted food manipulation experiments in field enclosures to identify the effect of food restriction on female reproductive traits and postpartum body condition, as well as on hatchling phenotypes, in a lacertid viviparous lizard from the Inner Mongolian desert steppe of China. Females under low-food availability treatment (LFT) had poorer immune function and body condition compared with those under high-food availability treatment (HFT). The food availability treatments significantly affected the litter size and litter mass of the females, but not their gestation period in captivity or brood success, or the body size, sprint speed, and sex ratio of the neonates. Females from the LFT group had smaller litter sizes and, therefore, lower litter mass than those from the HFT group. These results suggest that female racerunners facing food restriction lay fewer offspring with unchanged body size and locomotor performance, and incur a cost in the form of poor postpartum body condition and immune function. The flexibility of maternal responses to variable food availability represents an important life strategy that could enhance the resistance of lizards to unpredictable environmental change.

Thermal ecology of three coexistent desert lizards: Implications for habitat divergence and thermal vulnerability.

How ectotherms exploit thermal resources has important implications for their habitat utilization and thermal vulnerability to climate warming. To address this issue, we investigated thermal relations of three sympatric lizard species (Eremias argus, Eremias multiocellata, and Phrynocephalus przewalskii) in the desert steppe of Inner Mongolia, China. We determined the thermoregulatory behavior, body temperature (T b), operative temperature (T e), selected body temperature (T sel), and critical thermal maximum (CTmax) of adult lizards. Based on these physiological parameters, we quantified the accuracy and effectiveness of thermoregulation as well as thermal-safety margin for these species. The three species were accurate and effective thermoregulators. The P. przewalskii preferred open habitats, and had a higher T b than the two Eremias lizards, which preferred shade habitats and shuttled more frequently between the shade and sun. This indicated that the three sympatric lizards have different thermoregulatory behavior and thermal physiology, which might facilitate their coexistence in the desert steppe ecosystem. In addition, the P. przewalskii had higher T sel and CTmax, and a wider thermal-safety margin than the two Eremias lizards, suggesting that the two Eremias lizards would be more vulnerable to climate warming than P. przewalskii.

Effects of cattle grazing on small mammal communities in the Hulunber meadow steppe.

Small mammals play important roles in many ecosystems, and understanding their response to disturbances such as cattle grazing is fundamental for developing sustainable land use strategies. However, how small mammals respond to cattle grazing remains controversial. A potential cause is that most of previous studies adopt rather simple experimental designs based solely on the presence/absence of grazing, and are thus unable to detect any complex relationships between diversity and grazing intensity. In this study, we conducted manipulated experiments in the Hulunber meadow steppe to survey small mammal community structures under four levels of grazing intensities. We found dramatic changes in species composition in native small mammal communities when grazing intensity reached intermediate levels (0.46 animal unit/ha). As grazing intensity increased, Spermophilus dauricus gradually became the single dominant species. Species richness and diversity of small mammals in ungrazed and lightly grazed (0.23 animal unit/ha) area were much higher than in intermediately and heavily grazed area. We did not detect a humped relationship between small mammal diversity and disturbance levels predicted by the intermediate disturbance hypothesis (IDH). Our study highlighted the necessity of conducting manipulated experiments under multiple grazing intensities.

Temperature-dependent sex determination ruled out in the Chinese soft-shelled turtle (Pelodiscus sinensis) via molecular cytogenetics and incubation experiments across populations.

The sex determination mechanism for the Chinese soft-shelled turtle (Pelodiscus sinensis) is subject to controversy. Some populations have been shown to possess sex chromosomes and thus genotypic sex determination (GSD), while others were reported to exhibit temperature-dependent sex determination (TSD). To test whether TSD and GSD coexist in this species or whether populations differ in their sex-determining system, we conducted egg incubation experiments to investigate how temperature influences hatchling sex in a wide range of populations of this species in China. In parallel, we used comparative genome hybridization (CGH) to study the micro-sex chromosomes of adult P. sinensis in the 2 populations that were previously identified to be TSD. The incubation experiments showed that temperature did not affect hatchling sex in any of the studied populations. CGH indicated that turtles have micro-sex chromosomes of the female heterogametic (ZZ/ZW) system in the 2 disputed populations. These results indicate that P. sinensis is a GSD rather than a TSD species. Thus, the apparent coexistence of TSD and GSD in this species is the result of previous misdiagnosis in purportedly TSD populations.

Habitat selection by Eld's deer following relocation to a patchy landscape.

An emerging issue in wildlife conservation is the re-establishment of viable populations of endangered species in suitable habitats. Here, we studied habitat selection by a population of Hainan Eld's deer (Cervus eldi) relocated to a patchy landscape of farmland and forest. Hainan Eld's deer were pushed to the brink of extinction in the 1970s, but their population expanded rapidly from 26 to more than 1000 individuals by 2003 through effective reserve protection. As part of a wider relocation and population management strategy, 131 deer were removed from the reserve and reintroduced into a farmland-forest landscape in 2005. Habitat use under a context of human disturbance was surveyed by monitoring 19 radio-collared animals. The majority of deer locations (77%) were within 0.6-2 km of villages. Annual home ranges of these collared deer averaged 725 ha (SD 436), which was 55% of the size of the reserve from which they had originated. The annual home ranges contained 54% shrub-grassland, 26% forest and 15% farmland. The relocated deer population selected landscape comprising slash-and-burn agriculture and forest, and avoided both intensively farmed areas and areas containing only forest. Within the selected landscape, deer preferred swiddens and shrub-grasslands. Forests above 300 m in elevation were avoided, whereas forests below 300 m in elevation were overrepresented during the dry season and randomly used during the wet season. Our findings show that reintroduced deer can utilize disturbed habitats, and further demonstrate that subsistence agroforest ecosystems have the capacity to sustain endangered ungulates.