Detecting extinction risk from climate change by IUCN Red List criteria.

Anthropogenic climate change is a key threat to global biodiversity. To inform strategic actions aimed at conserving biodiversity as climate changes, conservation planners need early warning of the risks faced by different species. The IUCN Red List criteria for threatened species are widely acknowledged as useful risk assessment tools for informing conservation under constraints imposed by limited data. However, doubts have been expressed about the ability of the criteria to detect risks imposed by potentially slow-acting threats such as climate change, particularly because criteria addressing rates of population decline are assessed over time scales as short as 10 years. We used spatially explicit stochastic population models and dynamic species distribution models projected to future climates to determine how long before extinction a species would become eligible for listing as threatened based on the IUCN Red List criteria. We focused on a short-lived frog species (Assa darlingtoni) chosen specifically to represent potential weaknesses in the criteria to allow detailed consideration of the analytical issues and to develop an approach for wider application. The criteria were more sensitive to climate change than previously anticipated; lead times between initial listing in a threatened category and predicted extinction varied from 40 to 80 years, depending on data availability. We attributed this sensitivity primarily to the ensemble properties of the criteria that assess contrasting symptoms of extinction risk. Nevertheless, we recommend the robustness of the criteria warrants further investigation across species with contrasting life histories and patterns of decline. The adequacy of these lead times for early warning depends on practicalities of environmental policy and management, bureaucratic or political inertia, and the anticipated species response times to management actions.

Physiological control of water exchange in anurans.

Research on water exchange in frogs has historically assumed that blood osmotic potential drives water exchange between a frog and its environment, but here we show that the "seat patch" (the primary site of water exchange in many anurans), or other sites of cutaneous water uptake, act as an anatomic "compartment" with a water potential controlled separately from water potential of the blood, and the water potential of that compartment can be the driver of water exchange between the animal and its environment. We studied six frog species (Xenopus laevis, Rana pipiens, R. catesbeiana, Bufo boreas, Pseudacris cadaverina, and P. regilla) differing in ecological relationships to environmental water. We inferred the water potentials of seat patches from water exchanges by frogs in sucrose solutions ranging in water potential from 0 to 1000-kPa. Terrestrial and arboreal species had seat patch water potentials that were more negative than the water potentials of more aquatic species, and their seat patch water potentials were similar to the water potential of their blood, but the water potentials of venters of the more aquatic species were different from (and less negative than) the water potentials of their blood. These findings indicate that there are physiological mechanisms among frog species that can be used to control water potential at the sites of cutaneous water uptake, and that some frogs may be able to adjust the hydric conductance of their skin when they are absorbing water from very dilute solutions. Largely unexplored mechanisms involving aquaporins are likely responsible for adjustments in hydric conductance, which in turn, allow control of water potential at sites of cutaneous water uptake among species differing in ecological habit and the observed disequilibrium between sites of cutaneous water uptake and blood water potential in more aquatic species.

Condensation onto the skin as a means for water gain by tree frogs in tropical Australia.

Green tree frogs, Litoria caerulea, in the wet-dry tropics of northern Australia remain active during the dry season with apparently no available water and temperatures that approach their lower critical temperature. We hypothesized that this surprising activity might be because frogs that are cooled during nighttime activity gain water from condensation by returning to a warm, humid tree hollow. We measured the mass gained when a cool frog moved into either a natural or an artificial hollow. In both hollows, water condensed on cool L. caerulea, resulting in water gains of up to 0.93% of body mass. We estimated that the water gained was more than the water that would be lost to evaporation during activity. The use of condensation as a means for water gain may be a significant source of water uptake for species like L. caerulea that occur in areas where free water is unavailable over extended periods.

Removing the rubbish: frogs eliminate foreign objects from the body cavity through the bladder.

During the course of a telemetry study on three species of Australian frogs (Litoria caerulea, Litoria dahlii and Cyclorana australis), we found that many of the surgically implanted transmitters had migrated into the bladder. We subsequently implanted small beads into L. caerulea and they were expelled from the body in 10-23 days. Beads implanted into cane toads (Rhinella marina) to document the process were either expelled or were enveloped into the bladder. This appears to be a unique pathway for expulsion of foreign objects from the body, and suggests that caution should be employed in telemetry studies when interpreting the separation of some animals from their transmitters as a mortality event.

Changes in body fluids of the cocooning fossorial frog Cyclorana australis in a seasonally dry environment.

We investigated changes in the lymph (equivalent to plasma) and urine of the cocooning frog Cyclorana australis during the dry season in monsoonal northern Australia. Frogs in moist soil for two days were fully hydrated (lymph 220 mOsm kg(-1), urine 49 mOsm kg(-1)). From five weeks onwards the soil was dry (matric potential <-8000 kPa). Aestivating frogs at three and five months formed cocoons in shallow (<20 cm) burrows and retained bladder fluid (25-80% of standard mass). After three months, urine but not lymph osmolality was elevated. After five months, lymph (314 mOsm kg(-1)) and urine (294 mOsm kg(-1)) osmolality and urea concentrations were elevated. Urea was a major contributing osmolyte in urine and accumulated in lymph after five months. Lymph sodium concentration did not change with time, whereas potassium increased in urine after five months. Active animals had moderate lymph osmolality (252 mOsm kg(-1)), but urea concentrations remained low. Urine was highly variable in active frogs, suggesting that they tolerate variation in hydration state. Despite prolonged periods in dry soil, osmolality increase in C. australis was not severe. Aestivation in a cocoon facilitates survival in shallow burrows, but such a strategy may only be effective in environments with seasonally reliable rainfall.

Microclimate and limits to photosynthesis in a diverse community of hypolithic cyanobacteria in northern Australia.

Hypolithic microbes, primarily cyanobacteria, inhabit the highly specialized microhabitats under translucent rocks in extreme environments. Here we report findings from hypolithic cyanobacteria found under three types of translucent rocks (quartz, prehnite, agate) in a semiarid region of tropical Australia. We investigated the photosynthetic responses of the cyanobacterial communities to light, temperature and moisture in the laboratory, and we measured the microclimatic variables of temperature and soil moisture under rocks in the field over an annual cycle. We also used molecular techniques to explore the diversity of hypolithic cyanobacteria in this community and their phylogenetic relationships within the context of hypolithic cyanobacteria from other continents. Based on the laboratory experiments, photosynthetic activity required a minimum soil moisture of 15% (by mass). Peak photosynthetic activity occurred between approximately 8 degrees C and 42 degrees C, though some photosynthesis occurred between -1 degrees C and 51 degrees C. Maximum photosynthesis rates also occurred at light levels of approximately 150-550 micromol m(-2) s(-1). We used the field microclimatic data in conjunction with these measurements of photosynthetic efficiency to estimate the amount of time the hypolithic cyanobacteria could be photosynthetically active in the field. Based on these data, we estimated that conditions were appropriate for photosynthetic activity for approximately 942 h (approximately 75 days) during the year. The hypolithic cyanobacteria community under quartz, prehnite and agate rocks was quite diverse both within and between rock types. We identified 115 operational taxonomic units (OTUs), with each rock hosting 8-24 OTUs. A third of the cyanobacteria OTUs from northern Australia grouped with Chroococcidiopsis, a genus that has been identified from hypolithic and endolithic communities from the Gobi, Mojave, Atacama and Antarctic deserts. Several OTUs identified from northern Australia have not been reported to be associated with hypolithic communities previously.

Not just small, wet, and cold: effects of body size and skin resistance on thermoregulation and arboreality of frogs.

We used simulations from a biophysical model that integrates interlinked exchanges of energy and water between frogs and their environments to address questions about the limits to thermoregulation and about adaptations for arboreality. Body size and cutaneous resistance (Rc) both significantly affected body temperature (Tb) and the time to desiccate to 70% of standard mass (an ecologically relevant metric of desiccation). Cutaneous resistances < 25 s/cm allow basking frogs to elevate their Tb several degrees above ambient, but Rc above 25 had little additional effect on Tb. Small frogs (<10 g) are able to elevate their Tb above ambient while basking, even with small Rc. Large frogs must have greater skin resistances to be able to elevate body temperatures above ambient, yet large frogs take longer to desiccate to 70% of their standard mass. Frogs can avoid rapid desiccation with high Rc, a large body size, or some combination of these traits. Our literature survey indicates that frogs with a combination of Rc and body size that would result in long times to desiccate to 70% of standard mass tend to be arboreal, suggesting that those species may be selectively favored in a niche that often requires frogs to be away from water sources for extended periods of time.

The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts.

Anecdotal evidence suggests that birds have smaller intestines than mammals. In the present analysis, we show that small birds and bats have significantly shorter small intestines and less small intestine nominal (smooth bore tube) surface area than similarly sized nonflying mammals. The corresponding >50% reduction in intestinal volume and hence mass of digesta carried is advantageous because the energetic costs of flight increase with load carried. But, a central dilemma is how birds and bats satisfy relatively high energy needs with less absorptive surface area. Here, we further show that an enhanced paracellular pathway for intestinal absorption of water-soluble nutrients such as glucose and amino acids may compensate for reduced small intestines in volant vertebrates. The evidence is that l-rhamnose and other similarly sized, metabolically inert, nonactively transported monosaccharides are absorbed significantly more in small birds and bats than in nonflying mammals. To broaden our comparison and test the veracity of our finding we surveyed the literature for other similar studies of paracellular absorption. The patterns found in our focal species held up when we included other species surveyed in our analysis. Significantly greater amplification of digestive surface area by villi in small birds, also uncovered by our analysis, may provide one mechanistic explanation for the observation of higher paracellular absorption relative to nonflying mammals. It appears that reduced intestinal size and relatively enhanced intestinal paracellular absorption can be added to the suite of adaptations that have evolved in actively flying vertebrates.

Body temperature and resistance to evaporative water loss in tropical Australian frogs.

Although the skin of most amphibians measured to date offers no resistance to evaporative water loss (EWL), some species, primarily arboreal frogs, produce skin secretions that increase resistance to EWL. At high air temperatures, it may be advantageous for amphibians to increase EWL as a means to decrease body temperature. In Australian hylid frogs, most species do not decrease their resistance at high air temperature, but some species with moderate resistance (at moderate air temperatures) gradually decrease resistance with increasing air temperature, and some species with high resistance (at moderate air temperatures) abruptly decrease resistance at high air temperatures. Lower skin resistance at high air temperatures decreases the time to desiccation, but the lower body temperatures allow the species to avoid their critical thermal maximum (CT(Max)) body temperatures. The body temperatures of species with low to moderate resistances to EWL that do not adjust resistance at high air temperatures do not warm to their CT(Max), although for some species, this is because they have high CT(Max) values. As has been reported previously for resistance to EWL generally, the response pattern of change of EWL at high air temperatures has apparently evolved independently among Australian hylids. The mechanisms involved in causing resistance and changes in resistance are unknown.

Ontogenetic comparisons of standard metabolism in three species of crocodilians.

Due in part to their large size, aggressive temperament, and difficulty in handling, there are few physiological studies of adult crocodilians in the literature. As a result, studies comparing individuals across an ontogenetic series and comparisons among species are also lacking. We addressed this gap in knowledge by measuring standard metabolic rates (SMR) of three species of crocodilians (Crocodylus porosus, C. johnsoni, and Alligator mississippiensis), and included individuals that ranged from 0.22 to 114 kg. Allometric scaling of SMR with body mass was similar among the species, but C. porosus had significantly higher SMR than did C. johnsoni or A. mississippiensis. Differences in SMR among species are potentially related to behavioural differences in levels of aggression; C. porosus are the most aggressive of the crocodilians measured, and have rates of standard metabolism that are approximately 36% higher at the grand mean body size than those measured for C. johnsoni or A. mississippiensis, which are among the least aggressive crocodilians.

Evaluating thermoregulation in reptiles: an appropriate null model.

Established indexes of thermoregulation in ectotherms compare body temperatures of real animals with a null distribution of operative temperatures from a physical or mathematical model with the same size, shape, and color as the actual animal but without mass. These indexes, however, do not account for thermal inertia or the effects of inertia when animals move through thermally heterogeneous environments. Some recent models have incorporated body mass, to account for thermal inertia and the physiological control of warming and cooling rates seen in most reptiles, and other models have incorporated movement through the environment, but none includes all pertinent variables explaining body temperature. We present a new technique for calculating the distribution of body temperatures available to ectotherms that have thermal inertia, random movements, and different rates of warming and cooling. The approach uses a biophysical model of heat exchange in ectotherms and a model of random interaction with thermal environments over the course of a day to create a null distribution of body temperatures that can be used with conventional thermoregulation indexes. This new technique provides an unbiased method for evaluating thermoregulation in large ectotherms that store heat while moving through complex environments, but it can also generate null models for ectotherms of all sizes.

Energy metabolism and evaporative water loss in the European free-tailed bat and Hemprich's long-eared bat (Microchiroptera): species sympatric in the Negev Desert.

We compared the thermoregulatory abilities of two insectivorous bat species, Tadarida teniotis (mean body mass 32 g) and Otonycteris hemprichii (mean body mass 25 g), that are of different phylogenetic origins and zoogeographic distributions but are sympatric in the Negev Desert. At night, both were normothermic. By day, both were torpid when exposed to ambient temperatures (T(a)) below 25 degrees Celsius, with concomitant adjustments in metabolic rate (MR). Otonycteris hemprichii entered torpor at higher T(a) than T. teniotis, and, when torpid, their body temperatures (T(b)) were 1 degrees -2 degrees Celsius and 5 degrees -8 degrees Celsius above T(a), respectively; MR was correspondingly reduced. At night, the lower critical temperature of T. teniotis was 31.5 degrees Celsius, and that of O. hemprichii was 33 degrees Celsius. Mean nocturnal thermoneutral MR of T. teniotis was 37% greater than that of O. hemprichii. At high T(a), evaporative water loss (EWL) increased markedly in both species, but it was significantly higher in T. teniotis above 38 degrees Celsius. In both species, the dry heat transfer coefficient (thermal conductance) followed the expected pattern for small mammals, by day and by night. Total EWL was notably low in normothermic and torpid animals of both species, much lower than values reported for other bats, indicating efficient water conservation mechanisms in the study species. Comparing thermoregulatory abilities suggests that O. hemprichii is better adapted to hot, arid environments than T. teniotis, which may explain its wider desert distribution. By both standard and phylogenetically informed ANCOVA, we found no differences in basal metabolic rate (BMR) between desert and nondesert species of insectivorous bats, substantiating previous studies suggesting that low BMR is a characteristic common to insectivorous bats in general.

Preferred temperature correlates with evaporative water loss in hylid frogs from northern Australia.

We measured temperature preferences of 12 species of hylid frogs (Litoria and Cyclorana) from northern Australia in a laboratory thermal gradient. These species represented a range of ecological habitat use (aquatic, terrestrial, arboreal), adult body size (0.5-60 g), and cutaneous resistance to water loss (Rc=0.6-63.1 s cm-1). We found significant differences among species in selected skin temperature and gradient temperature but not in the variances of these measures (an index of precision of temperature selection). The species' differences correlated significantly with cutaneous resistance to water loss, with more-resistant frogs selecting higher skin and substrate temperatures in the thermal gradient, even after phylogenetic relationships are taken into account. Because cutaneous resistance to water loss also correlates with ecological habit (arboreal>terrestrial>aquatic), we suggest that their higher resistance to water loss allows arboreal and terrestrial species better ability to tolerate high temperatures, where growth or locomotory speed may be higher, without the associated risk of desiccation.

Regulation of gut function varies with life-history traits in chuckwallas (Sauromalus obesus: Iguanidae).

We examined the effects of hibernation and fasting on intestinal glucose and proline uptake rates of chuckwallas (Sauromalus obesus) and on the size of organs directly or indirectly related to digestion. These lizards show geographic variation in body size and growth rate that parallels an elevational gradient in our study area. At low elevation, food is available only for a short time during the spring; at high elevation, food may also be available during summer and autumn, depending on rainfall conditions in a given year. We hypothesized that low-elevation lizards with a short season of food availability would show more pronounced regulation of gut size and function than high-elevation lizards with prolonged or bimodal food availability. Hibernating lizards from both elevations had significantly lower uptake rates per milligram intestine for both nutrients, and lower small intestine mass, than active lizards. The combination of these two effects resulted in significantly lower total nutrient uptake in hibernating animals compared to active ones. The stomach, large intestine, and cecum showed lower masses in hibernators, but these results were not statistically significant. The heart, kidney, and liver showed no difference in mass between hibernating and nonhibernating animals. Lizards from low elevations with a short growing season also showed a greater increase in both uptake rates and small intestine mass from the hibernating to the active state, compared to those from high elevations with longer growing seasons. Thus, compared to those from long growing season areas, lizards from short growing season areas have equal uptake capacity during hibernation but much higher uptake capacity while active and feeding. This pattern of regulation of gut function may or may not be an adaptive response, but it is consistent with variation in life-history characteristics among populations. In areas with a short season, those lizards that can extract nutrients quickly and then reduce the gut will be favored; in areas where food may be available later in the year, those lizards that maintain an active gut would be favored. While other researchers have found much greater magnitudes of gut regulation when making comparisons among species, we find the different patterns of change in gut function between different populations of chuckwallas particularly intriguing because they occur within a single species.

Comparative analysis of cutaneous evaporative water loss in frogs demonstrates correlation with ecological habits.

Most frog species show little resistance to evaporative water loss (EWL), but some arboreal species are known to have very high resistances. We measured EWL and cutaneous resistance to evaporation (Rc) in 25 species of frogs from northern Australia, including 17 species in the family Hylidae, six species in the Myobatrachidae, and one each in the Bufonidae and the Microhylidae. These species display a variety of ecological habits, including aquatic, terrestrial, and arboreal specialisations, with the complete range of habits displayed within just the one hylid genus, Litoria. The 25 species measured in this study have resistances that range from Rc=0 to 63.1. These include low values indistinguishable from a free water surface to high values typical of "waterproof" anuran species. There was a strong correlation between ecological habit and Rc, even taking phylogenetic relationships into account; arboreal species had the highest resistance, aquatic species tended to have little or no resistance, and terrestrial species tended to have resistance between those of arboreal and aquatic frogs. For one species, Litoria rubella, we found no significant changes in EWL along a 1,500-km aridity gradient. This study represents the strongest evidence to date of a link between ecological habits and cutaneous resistance to water loss among species of frogs.

Alligators and Crocodiles Have High Paracellular Absorption of Nutrients, But Differ in Digestive Morphology and Physiology.

Much of what is known about crocodilian nutrition and growth has come from animals propagated in captivity, but captive animals from the families Crocodilidae and Alligatoridae respond differently to similar diets. Since there are few comparative studies of crocodilian digestive physiology to help explain these differences, we investigated young Alligator mississippiensis and Crocodylus porosus in terms of (1) gross and microscopic morphology of the intestine, (2) activity of the membrane-bound digestive enzymes aminopeptidase-N, maltase, and sucrase, and (3) nutrient absorption by carrier-mediated and paracellular pathways. We also measured gut morphology of animals over a larger range of body sizes. The two species showed different allometry of length and mass of the gut, with A. mississippiensis having a steeper increase in intestinal mass with body size, and C. porosus having a steeper increase in intestinal length with body size. Both species showed similar patterns of magnification of the intestinal surface area, with decreasing magnification from the proximal to distal ends of the intestine. Although A. mississippiensis had significantly greater surface-area magnification overall, a compensating significant difference in gut length between species meant that total surface area of the intestine was not significantly different from that of C. porosus. The species differed in enzyme activities, with A. mississippiensis having significantly greater ability to digest carbohydrates relative to protein than did C. porosus. These differences in enzyme activity may help explain the differences in performance between the crocodilian families when on artificial diets. Both A. mississippiensis and C. porosus showed high absorption of 3-O methyl d-glucose (absorbed via both carrier-mediated and paracellular transport), as expected. Both species also showed surprisingly high levels of l-glucose-uptake (absorbed paracellularly), with fractional absorptions as high as those previously seen only in small birds and bats. Analyses of absorption rates suggested a relatively high proportional contribution of paracellular (i.e., non-mediated) uptake to total uptake of nutrients in both species. Because we measured juveniles, and most paracellular studies to date have been on adults, it is unclear whether high paracellular absorption is generally high within crocodilians or whether these high values are specific to juveniles.

Field hydration state varies among tropical frog species with different habitat use.

We have previously shown that ecological habit (e.g., arboreal, terrestrial, amphibious) correlates with thermoregulatory behaviors and water balance physiology among species of hylid frogs in northern Australia. We hypothesized that these frogs would be different with respect to their field hydration states because of the challenges associated with the different ecological habits. There are very few data on the hydration levels that frogs maintain in the field, and the existing data are from disparate species and locations and do not relate hydration state to habit or changes in seasonal water availability. We measured the hydration state of 15 species of frogs from tropical northern Australia to determine the influences of ecological habit and season on the hydration state that these frogs maintain. As predicted, frogs were significantly less hydrated in the dry season than they were in the wet season and showed significantly higher variation among individuals, suggesting that maintaining hydration is more challenging in the dry season. In the wet season, terrestrial species were significantly less hydrated than arboreal or amphibious species. During the dry season, amphibious species that sought refuge in cracking mud after the pond dried were significantly less hydrated than terrestrial or arboreal species. These data suggest that hydration behaviors and voluntary tolerance of dehydration vary with habitat use, even within closely related species in the same family or genus. Terrestrial and arboreal species might be expected to be the most vulnerable to changes in water availability, because they are somewhat removed from water sources, but the physiological characteristics of arboreal frogs that result in significant cutaneous resistance to water loss allow them to reduce the effects of their dehydrating microenvironment.

Paracellular absorption is relatively low in the herbivorous Egyptian spiny-tailed lizard, Uromastyx aegyptia.

Absorption of small water-soluble nutrients in vertebrate intestines occurs both by specific, mediated transport and by non-specific, passive, paracellular transport. Although it is apparent that paracellular absorption represents a significant route for nutrient absorption in many birds and mammals, especially small, flying species, its importance in ectothermic vertebrates has not previously been explored. Therefore, we measured fractional absorption (ƒ) and absorption rate of three paracellular probes (arabinose, L-rhamnose, cellobiose) and of 3-O-methyl D-glucose (absorbed by both mediated and paracellular pathways) by the large herbivorous lizard, Uromastyx aegyptia, to explore the relative importance of paracellular and mediated transport in an ectothermic, terrestrial vertebrate. Fractional absorption of 3-O-methyl D-glucose was high (ƒâ€Š= 0.73±0.04) and similar to other vertebrates; ƒ of the paracellular probes was relatively low (arabinose ƒâ€Š= 0.31±0.03, L-rhamnose ƒâ€Š= 0.19±0.02, and cellobiose ƒâ€Š= 0.14±0.02), and decreased with molecular mass, a pattern consistent with other vertebrates. Paracellular absorption accounted for approximately 24% of total 3-O-methyl D-glucose uptake, indicating low reliance on this pathway for these herbivorous lizards, a pattern similar to that found in other terrestrial vertebrates, and different from small flying endotherms (both birds and bats).

Scaling of standard metabolic rate in estuarine crocodiles Crocodylus porosus.

Standard metabolic rate (SMR, ml O2 min(-1)) of captive Crocodylus porosus at 30 °C scales with body mass (kg) according to the equation, SMR = 1.01 M(0.829), in animals ranging in body mass of 3.3 orders of magnitude (0.19-389 kg). The exponent is significantly higher than 0.75, so does not conform to quarter-power scaling theory, but rather is likely an emergent property with no single explanation. SMR at 1 kg body mass is similar to the literature for C. porosus and for alligators. The high exponent is not related to feeding, growth, or obesity of captive animals. The log-transformed data appear slightly curved, mainly because SMR is somewhat low in many of the largest animals (291-389 kg). A 3-parameter model is scarcely different from the linear one, but reveals a declining exponent between 0.862 and 0.798. A non-linear model on arithmetic axes overestimates SMR in 70% of the smallest animals and does not satisfactorily represent the data.