Forest cover reduces thermally suitable habitats and affects responses to a warmer climate predicted in a high-elevation lizard.

Warmer climates have affected animal distribution ranges, but how they may interact with vegetation patterns to affect habitat use, an important consideration for future wildlife management, has received little attention. Here, we use a biophysical model to investigate the potential thermal impact of vegetation pattern on the habitat quality of a high-elevation grassland lizard, Takydromus hsuehshanensis, and to predict the thermal suitability of vegetation for this species in a future warmer climate (assuming 3 °C air temperature increase). We assess the thermal quality of vegetation types in our study area (Taroko National Park in areas >1,800 m) using three ecologically relevant estimates of reptiles: body temperature (T b), maximum active time, and maximum digestive time. The results show that increasing forest canopy gradually cools the microclimates, hence decreasing these estimates. In the current landscape, sunny mountain-top grasslands are predicted to serve as high quality thermal habitat, whereas the dense forests that are dominant as a result of forest protection are too cold to provide suitable habitat. In simulated warmer climates, the thermal quality of dense forests increases slightly but remains inferior to that of grasslands. We note that the impact of warmer climates on this reptile will be greatly affected by future vegetation patterns, and we suggest that the current trend of upslope forest movement found in many other mountain systems could cause disadvantages to some heliothermic lizard species.

Can reptile embryos influence their own rates of heating and cooling?

Previous investigations have assumed that embryos lack the capacity of physiological thermoregulation until they are large enough for their own metabolic heat production to influence nest temperatures. Contrary to intuition, reptile embryos may be capable of physiological thermoregulation. In our experiments, egg-sized objects (dead or infertile eggs, water-filled balloons, glass jars) cooled down more rapidly than they heated up, whereas live snake eggs heated more rapidly than they cooled. In a nest with diel thermal fluctuations, that hysteresis could increase the embryo's effective incubation temperature. The mechanisms for controlling rates of thermal exchange are unclear, but may involve facultative adjustment of blood flow. Heart rates of snake embryos were higher during cooling than during heating, the opposite pattern to that seen in adult reptiles. Our data challenge the view of reptile eggs as thermally passive, and suggest that embryos of reptile species with large eggs can influence their own rates of heating and cooling.

Synergistic limits to the altitudinal distribution of a high-altitude lizard, Takydromus hsuehshanensis.

The geographic distribution of species can be affected by environmental factors. The adult highaltitude lizard Takydromus hsuehshanensis (altitude > 1800 m) has been shown to tolerate summer lowland air temperature; its absence in lowland areas may therefore be caused by other factors. We employed a transplant experiment to monitor survival in different life stages and female reproduction in lowland areas. We maintained the T. hsuehshanensis adults in semi-natural outdoor enclosures with sufficient food, water, and the exclusion of potential predators. The results showed that (1) the survival rates of adults gradually decreased to 23.4% from one summer to the next, (2) illness occurred in adults during the winter, and (3) reproductive capacity (2 eggs/female), hatching success (31.7%), and hatchling survival rate (0% at the end of 11 weeks) were very low during the active season. We suggest that environmental factors synergistically caused these impairments in T. hsuehshanensis across different life stages and different seasons. This may partially explain its current altitudinal distribution.

Comparison of freshwater discrimination ability in three species of sea kraits (Laticauda semifasciata, L. laticaudata and L. colubrina).

Three species of amphibious sea kraits (Laticauda spp.) require drinking freshwater to regulate water balance. The extent of terrestriality is known to differ among them. Species with higher extent of terrestriality would drink freshwater accumulated on land, whereas less terrestrial species would rely totally on freshwater that runs into the sea. Consequently, we predicted that the latter species might have a better ability to follow the flow of freshwater or lower salinity water in the sea than the former. We investigated the freshwater discrimination ability of three sea krait species, using a Y-maze apparatus. We found that Laticauda semifasciata and Laticauda laticaudata, less terrestrial species, followed freshwater significantly more frequently than seawater, whereas Laticauda colubrina, more terrestrial species, unbiasedly selected freshwater and seawater. This result supports our prediction and suggests that less terrestrial sea kraits more efficiently access freshwater sources in the sea than highly terrestrial sea kraits. It is likely that behavioral rehydration systems vary among sea kraits in relation to their terrestrial tendency.

Habitat selection by sea kraits (Laticauda spp.) at coastal sites of Orchid Island, Taiwan.

Three species of amphibious sea kraits (Laticauda spp.) spend variable time at sea and require fresh water for water balance. Both the rate of cutaneous evaporative water loss and the extent of terrestriality are known to differ among them. Laticauda semifasciata has the greatest rate of water loss and the least extent of terrestriality, whereas L. colubrina exhibits the reverse and L. laticaudata is intermediate. These sea kraits tend to be more abundant at places where there are sources of fresh water, but other factors also influence their distribution. To further clarify the habitat requirements, we investigated the abundance of each species of sea krait at six different habitats and the availability of each type of habitat on Orchid Island, Taiwan. The six habitats were high coral reef without fresh water (HR) and with fresh water (HRF); low coral reef without fresh water (LR) and with fresh water (LRF); sand or gravel coast, which has no coral reef, without fresh water (NR) and with fresh water (NRF). The extent of safety judged from the relative availability of retreat sites, from high to low, was HR, LR, and NR among these habitats. More than 75% of individuals counted for each species were found in HRF. We found no sea kraits in NRF and NR. The most available habitat was LR, but no L. laticaudata or L. semifasciata were found in this habitat. We found 3.3% and 16.7% of L. colubrina in LR and HR, respectively. For L. colubrina, the second abundant habitat was HR, whereas for L. laticaudata and L. semifasciata, the second abundant habitat was LRF. We conclude that both safety (availability of retreat sites) and fresh water are important to the habitat selection of sea kraits. Compared with other species, L. colubrina is characterized by a greater extent of terrestrial habit and possibly greater variety of access to sources of fresh water.

Abundance of sea kraits correlates with precipitation.

Recent studies have shown that sea kraits (Laticauda spp.)--amphibious sea snakes--dehydrate without a source of fresh water, drink only fresh water or very dilute brackish water, and have a spatial distribution of abundance that correlates with freshwater sites in Taiwan. The spatial distribution correlates with sites where there is a source of fresh water in addition to local precipitation. Here we report six years of longitudinal data on the abundance of sea kraits related to precipitation at sites where these snakes are normally abundant in the coastal waters of Lanyu (Orchid Island), Taiwan. The number of observed sea kraits varies from year-to-year and correlates positively with previous 6-mo cumulative rainfall, which serves as an inverse index of drought. Grouped data for snake counts indicate that mean abundance in wet years is nearly 3-fold greater than in dry years, and this difference is significant. These data corroborate previous findings and suggest that freshwater dependence influences the abundance or activity of sea kraits on both spatial and temporal scales. The increasing evidence for freshwater dependence in these and other marine species have important implications for the possible impact of climate change on sea snake distributions.

Bioenergetic modeling reveals that Chinese green tree vipers select postprandial temperatures in laboratory thermal gradients that maximize net energy intake.

With bioenergetic modeling, we tested the hypothesis that reptiles maximize net energy gain by postprandial thermal selection. Previous studies have shown that Chinese green tree vipers (Trimeresurus s. stejnegeri) have postprandial thermophily (mean preferred temperature T(p) for males =27.8 degrees C) in a linear thigmothermal gradient when seclusion sites and water existed. With some published empirical models of digestion associated factors for this snake, we calculated the average rate (E(net)) and efficiency (K(net)) of net energy gain from possible combinations of meal size, activity level, and feeding frequency at each temperature. The simulations consistently revealed that E(net) maximizes at the T(p) of these snakes. Although the K(net) peaks at a lower temperature than E(net), the value of K(net) remains high (>=0.85 in ratio to maximum) at the peak temperature of E(net). This suggested that the demands of both E(net) and K(net) can be attained by postprandial thermal selection in this snake. In conclusion, the data support our prediction that postprandial thermal selection may maximize net energy gain.

Prey envenomation does not improve digestive performance in Taiwanese pit vipers (Trimeresurus gracilis and T. stejnegeri stejnegeri).

It has been a common belief that snake venom may help in the digestion of its prey, although direct examples and supporting evidence have not been sufficient. To address this, the present study examined whether preinjecting natural amounts of pit viper venom into experimental mice may accelerate their digestion by the snakes or gain energy benefit as compared to the control without the envenomation. Live adults of two Asian pit viper species Trimeresurus gracilis and T. stejnegeri stejnegeri, which inhabit the cold and warm environment respectively, were the subjects studied herein. A natural dose of 1.2 mg of each of the pit viper venom in phosphate-buffered saline (PBS) was injected into the mouse (about 10% of the snake mass) before it was being fed to the same species of vipers, while the pit vipers in control group were given mouse injected with sterile PBS. The snakes were kept at 14 degrees C or 24 degrees C, and parameters of gut passage time, costs of digestion, and/or digestive efficiency were measured. The results did not support the hypotheses that envenomation facilitates prey digestion. The venom in fact caused longer first defecation time and lower assimilation energy at 14 degrees C. Besides, the time to reach the oxygen consumption peak, and the first defecation time of T. s. stejnegeri were longer than that of T. gracilis.

Sea snakes (Laticauda spp.) require fresh drinking water: implication for the distribution and persistence of populations.

Dehydration and procurement of water are key problems for vertebrates that have secondarily invaded marine environments. Sea snakes and other marine reptiles are thought to remain in water balance without consuming freshwater, owing to the ability of extrarenal salt glands to excrete excess salts obtained either from prey or from drinking seawater directly. Contrary to this long-standing dogma, we report that three species of sea snake actually dehydrate in marine environments. We investigated dehydration and drinking behaviors in three species of amphibious sea kraits (Laticauda spp.) representing a range of habits from semiterrestrial to very highly marine. Snakes that we dehydrated either in air or in seawater refused to drink seawater but drank freshwater or very dilute brackish water (10%-30% seawater) to remain in water balance. We further show that Laticauda spp. can dehydrate severely in the wild and are far more abundant at sites where there are sources of freshwater. A more global examination of all sea snakes demonstrates that species richness correlates positively with mean annual precipitation within the Indo-West Pacific tropical region. The dependence of Laticauda spp. on freshwater might explain the characteristically patchy distributions of these reptiles and is relevant to understanding patterns of extinctions and possible future responses to changes in precipitation related to global warming. In particular, metapopulation dynamics of the Laticauda group of sea snakes are expected to change in relation to projected reductions of tropical dry-season precipitation.

Venom phospholipases A2 of bamboo viper (Trimeresurus stejnegeri): molecular characterization, geographic variations and evidence of multiple ancestries.

Phospholipases A2 (PLA2s) were purified from the Trimeresurus stejnegeri venom obtained from various localities in Taiwan and three provinces in China, by gel filtration followed by reversed-phase HPLC. The precise molecular mass and N-terminal sequence of each PLA2 were determined. In addition to the six previously documented PLA2 isoforms of this species, we identified ten novel isoforms. The venom gland cDNAs of individual specimens of the viper from four localities were used for PCR and subsequent cloning of the PLA2s. The molecular masses and partial sequences of most of the purified PLA2s matched with those deduced from a total of 13 distinct cDNA sequences of these clones. Besides the commonly known Asp49 or Lys-49 PLA2s of crotalid venoms, a novel type of PLA2 with Asn-49 substitution at the Ca2+-binding site was discovered. This type of PLA2 is non-catalytic, but may cause local oedema and appears to be a venom marker of many tree vipers. In particular, we showed that T. stejnegeri displayed high geographic variations of the PLA2s within and between their Taiwanese and Chinese populations, which can be explained by geological isolation and prey ecology. A phylogenetic tree of the acidic venom PLA2s of this species and other related Asian vipers reveals that T. stejnegeri contains venom genes related to those from several sympatric pit vipers, including the genera Tropedolaemus and Gloydius besides the Trimeresurus itself. Taken together, these findings may explain the exceptionally high variations in the venom as well as the evolutionary advantage of this species.