Hematological and biochemical parameters of giant pandas (Ailuropoda melanoleuca) in captive and semi-natural environments.

Physiological indexes like blood parameters have been widely used to monitor the health of free-roaming animals. Attempts to reintroduce one of China's most endangered species, the giant panda (Ailuropoda melanoleuca), have been hampered by a lack of data on its ecology and physiology. We examined three giant pandas' hematological and blood chemistry parameters in a soft release program and 30 captive giant pandas as controls and determined the reference intervals (RIs) for those blood parameters in the captive animals. Elevation, captivity status and the interaction of those factors were statistically significant for hematologic measures. Release pandas had significantly higher hemoglobin and hematocrit values after they moved to high elevation locations. We also found significant difference in the enzyme parameters between high and low elevation pandas such as higher aspartate aminotransferase, alanine aminotransferase, creatinine kinase, amylase and lower lactate dehydrogenase and alkaline phosphatase. Release pandas also had higher nutrition parameter values such as higher albumin, globulin and creatinine. The RI for blood parameters in our study provides a baseline to monitor the health of captive animals and forms the basis for assessing the health of free-roaming giant pandas in future reintroduction efforts.

Matrilinear hierarchy in the American black bear (Ursus americanus).

The American black bear (Ursus americanus) was long thought to be solitary and its social organization has not been well described. Here, we present new data on black bear social structure. The objectives of the study were to make detailed observations of the behavior of wild black bears to determine their social interactions and structure. We tested whether black bears interacted socially beyond mating and competing for resources, if black bears tracked relationships and interacted regularly even when resources were not limited, and whether the social structure of a population of black bears was based on a matrilinear hierarchy. We collected data by direct observation of bears from 1993 to 2014. Observations of 1210 social interactions at a provisioning site indicated that females compete and form matrilinear hierarchies. Dominant bears established a hierarchy for food, control of space, and control of younger bears. Post interaction scent marking took place, which suggested that dominant females were conditioning subordinates to their scent marks. Affiliative behavior occurred between related and unrelated bears and helped to establish the social structure of the bear community. Based on our data, human-bear conflicts can be reduced by behavioral modifications by humans when they encounter bears. Knowledge of bear behavior and the matrilinear hierarchy provide a basis for non-lethal management of bears that find themselves in a bear-human conflict situation.

Field metabolic rates of giant pandas reveal energetic adaptations.

Knowledge of energy expenditure informs conservation managers for long term plans for endangered species health and habitat suitability. We measured field metabolic rate (FMR) of free-roaming giant pandas in large enclosures in a nature reserve using the doubly labeled water method. Giant pandas in zoo like enclosures had a similar FMR (14,182 kJ/day) to giant pandas in larger field enclosures (13,280 kJ/day). In winter, giant pandas raised their metabolic rates when living at - 2.4 °C (36,108 kJ/day) indicating that they were below their thermal neutral zone. The lower critical temperature for thermoregulation was about 8.0 °C and the upper critical temperature was about 28 °C. Giant panda FMRs were somewhat lower than active metabolic rates of sloth bears, lower than FMRs of grizzly bears and polar bears and 69 and 81% of predicted values based on a regression of FMR versus body mass of mammals. That is probably due to their lower levels of activity since other bears actively forage for food over a larger home range and pandas often sit in a patch of bamboo and eat bamboo for hours at a time. The low metabolic rates of giant pandas in summer, their inability to acquire fat stores to hibernate in winter, and their ability to raise their metabolic rate to thermoregulate in winter are energetic adaptations related to eating a diet composed almost exclusively of bamboo. Differences in FMR of giant pandas between our study and previous studies (one similar and one lower) appear to be due to differences in activity of the giant pandas in those studies.

Temperature-Dependent Sex Determination in Sea Turtles in the Context of Climate Change: Uncovering the Adaptive Significance.

The adaptive significance of temperature-dependent sex determination (TSD) in reptiles remains unknown decades after TSD was first identified in this group. Concurrently, there is growing concern about the effect that rising temperatures may have on species with TSD, potentially producing extremely biased sex ratios or offspring of only one sex. The current state-of the-art in TSD research on sea turtles is reviewed here and, against current paradigm, it is proposed that TSD provides an advantage under warming climates. By means of coadaptation between early survival and sex ratios, sea turtles are able to maintain populations. When offspring survival declines at high temperatures, the sex that increases future fecundity (females) is produced, increasing resilience to climate warming. TSD could have helped reptiles to survive mass extinctions in the past via this model. Flaws in research on sex determination in sea turtles are also identified and it is suggested that the development of new techniques will revolutionize the field.

Free-roaming dogs limit habitat use of giant pandas in nature reserves.

Giant pandas (Ailuropoda melanoleuca) were historically hunted using dogs and are currently threatened by free-roaming dogs and their associated diseases. To better understand the spatial magnitude of this threat, we used a GIS approach to investigate edge effects of dogs on giant panda habitat. We first examined two nature reserves with contrasting free-roaming dog populations: Liziping, with many dogs (~0.44/km2), and Daxiangling, with few dogs (~0.14/km2). Spatial analysis indicated that giant pandas at Liziping (but not Daxiangling) showed a shift in habitat use away from populated areas consistent with a risk response to the foray distance of free-roaming dogs (10.9 km path-distance). Most giant panda locations (86%) from the 2014 census in Liziping were clustered around remote "dog-free zones." Expanding this analysis across the entire giant panda range revealed that 40% of panda habitat is within the foray distance of dogs. Our assessment will inform dog control programs including monitoring, education, veterinary care, and other measures. We recommend that reserves designated for the release of translocated pandas receive priority consideration for dog control efforts. Only by understanding and managing complex interactions between humans, domestic animals, and wild animals can we sustain natural systems in a world increasingly dominated by humans.

Physiological determinants of the internesting interval in sea turtles: a novel 'water-limitation' hypothesis.

The internesting interval separates successive clutches of sea turtle eggs, and its duration varies both among and within species. Here, we review the potential physiological limits to this interval, and develop the hypothesis that desalination capacity limits the internesting interval owing to the requirement for water deposition in eggs. Sea turtles deposit 1-4 kg of water per clutch in egg albumen; for most species, this represents about 2% of adult body mass. We calculate how quickly turtles can recover this water by estimating maximal salt excretion rates, metabolic water production and urinary losses. From this water balance perspective, the 'water-limitation' hypothesis is plausible for green turtles but not for leatherbacks. Some plasma biochemistry studies indicate dehydration in sea turtles during the nesting season, although this is not a universal finding and these data have rarely been collected during the internesting interval itself. There is mixed support for a trade-off between clutch size and the length of the interval. We conclude that the 'water-limitation' hypothesis is plausible for most sea turtle species, but requires direct experimentation.

Are thermal barriers "higher" in deep sea turtle nests?

Thermal tolerances are affected by the range of temperatures that species encounter in their habitat. Daniel Janzen hypothesized in his "Why mountain passes are higher in the tropics" that temperature gradients were effective barriers to animal movements where climatic uniformity was high. Sea turtles bury their eggs providing some thermal stability that varies with depth. We assessed the relationship between thermal uniformity and thermal tolerance in nests of three species of sea turtles. We considered that barriers were "high" when small thermal changes had comparatively large effects and "low" when the effects were small. Mean temperature was lower and fluctuated less in species that dig deeper nests. Thermal barriers were comparatively "higher" in leatherback turtle (Dermochelys coriacea) nests, which were the deepest, as embryo mortality increased at lower "high" temperatures than in olive ridley (Lepidochelys olivacea) and green turtle (Chelonia mydas) nests. Sea turtles have temperature-dependent sex determination (TSD) and embryo mortality increased as temperature approached the upper end of the transitional range of temperatures (TRT) that produces both sexes (temperature producing 100% female offspring) in leatherback and olive ridley turtles. As thermal barriers are "higher" in some species than in others, the effects of climate warming on embryo mortality is likely to vary among sea turtles. Population resilience to climate warming may also depend on the balance between temperatures that produce female offspring and those that reduce embryo survival.

Metabolic rate of the red panda, Ailurus fulgens, a dietary bamboo specialist.

The red panda (Ailurus fulgens) has a similar diet, primarily bamboo, and shares the same habitat as the giant panda, Ailuropoda melanoleuca. There are considerable efforts underway to understand the ecology of the red panda and to increase its populations in natural reserves. Yet it is difficult to design an effective strategy for red panda reintroduction if we do not understand its basic biology. Here we report the resting metabolic rate of the red panda and find that it is higher than previously measured on animals from a zoo. The resting metabolic rate was 0.290 ml/g/h (range 0.204-0.342) in summer and 0.361 ml/g/h in winter (range 0.331-0.406), with a statistically significant difference due to season and test temperature. Temperatures in summer were probably within the thermal neutral zone for metabolism but winter temperatures were below the thermal neutral zone. There was no difference in metabolic rate between male and female red pandas and no difference due to mass. Our values for metabolic rate were much higher than those measured by McNab for 2 red pandas from a zoo. The larger sample size (17), more natural conditions at the Panda Base and improved accuracy of the metabolic instruments provided more accurate metabolism measurements. Contrary to our expectations based on their low quality bamboo diet, the metabolic rates of red pandas were similar to mammals of the same size. Based on their metabolic rates red pandas would not be limited by their food supply in natural reserves.

Climate Impacts on Sea Turtle Breeding Phenology in Greece and Associated Foraging Habitats in the Wider Mediterranean Region.

Sea turtles are vulnerable to climate change impacts in both their terrestrial (nesting beach) and oceanic habitats. From 1982 to 2012, air and sea surface temperatures at major high use foraging and nesting regions (n = 5) of loggerhead turtles (Caretta caretta) nesting in Greece have steadily increased. Here, we update the established relationships between sea surface temperature and nesting data from Zakynthos (latitude: 37.7°N), a major nesting beach, while also expanding these analyses to include precipitation and air temperature and additional nesting data from two other key beaches in Greece: Kyparissia Bay (latitude: 37.3°N) and Rethymno, Crete (latitude: 35.4°N). We confirmed that nesting phenology at Zakynthos has continued to be impacted by breeding season temperature; however, temperature has no consistent relationship with nest numbers, which are declining on Zakynthos and Crete but increasing at Kyparissia. Then using statistically downscaled outputs of 14 climate models assessed by the Intergovernmental Panel on Climate Change (IPCC), we projected future shifts in nesting for these populations. Based on the climate models, we projected that temperature at the key foraging and breeding sites (Adriatic Sea, Aegean Sea, Crete, Gulf of Gabès and Zakynthos/Kyparissia Bay; overall latitudinal range: 33.0°-45.8°N) for loggerhead turtles nesting in Greece will rise by 3-5°C by 2100. Our calculations indicate that the projected rise in air and ocean temperature at Zakynthos could cause the nesting season in this major rookery to shift to an earlier date by as much as 50-74 days by 2100. Although an earlier onset of the nesting season may provide minor relief for nest success as temperatures rise, the overall climatic changes to the various important habitats will most likely have an overall negative impact on this population.

Metabolic rates of giant pandas inform conservation strategies.

The giant panda is an icon of conservation and survived a large-scale bamboo die off in the 1980s in China. Captive breeding programs have produced a large population in zoos and efforts continue to reintroduce those animals into the wild. However, we lack sufficient knowledge of their physiological ecology to determine requirements for survival now and in the face of climate change. We measured resting and active metabolic rates of giant pandas in order to determine if current bamboo resources were sufficient for adding additional animals to populations in natural reserves. Resting metabolic rates were somewhat below average for a panda sized mammal and active metabolic rates were in the normal range. Pandas do not have exceptionally low metabolic rates. Nevertheless, there is enough bamboo in natural reserves to support both natural populations and large numbers of reintroduced pandas. Bamboo will not be the limiting factor in successful reintroduction.

Endocrine indicators of a stress response in nesting diamondback terrapins to shoreline barriers in Barnegat Bay, NJ.

Anthropogenic stressors such as habitat loss are a global problem for wildlife. Coastal development in the United States has replaced estuary shorelines with hard erosion barriers. In Barnegat Bay, New Jersey, the diamondback terrapin (Malaclemys terrapin) encounters these barriers when approaching upland beaches for nesting. To determine the effects of shoreline barriers on this threatened species' nesting abilities, we measured adrenocortical response (i.e., stress response) by comparing natural corticosterone and testosterone levels of 91 terrapins following in situ exposure to either an experimentally blocked, or open nesting beach. In addition, we exposed 15 individuals, from various nesting beaches, to handling stress to identify acute corticosterone secretion, finding a significant increase over 60min to 8ng/ml. Corticosterone did not reach this level in terrapins exposed to barriers. Corticosterone and testosterone levels were not significantly higher among terrapins exposed to barriers compared to those at open reference beaches. This lack of a stress response suggests that terrapins do not physiologically respond to barriers when they approach nesting beaches and thus are not stressed. This may be due to an adaptive trait to help female turtles complete the nesting process despite the natural stresses inherent to coming on land. Our study suggests that this lack of stress response is also applied to non-natural, human made nesting barriers. If terrapins are not physiologically capable of adapting to shoreline barriers, future erosion control structures could support terrapin nesting with periodic upland access points. This endocrinological study provides a more quantitative approach to guiding management of anthropogenic stressors upon wildlife.

Global analysis of the effect of local climate on the hatchling output of leatherback turtles.

The most recent climate change projections show a global increase in temperatures along with precipitation changes throughout the 21(st) century. However, regional projections do not always match global projections and species with global distributions may exhibit varying regional susceptibility to climate change. Here we show the effect of local climatic conditions on the hatchling output of leatherback turtles (Dermochelys coriacea) at four nesting sites encompassing the Pacific, Atlantic and Indian Oceans. We found a heterogeneous effect of climate. Hatchling output increased with long-term precipitation in areas with dry climatic conditions (Playa Grande, Pacific Ocean and Sandy Point, Caribbean Sea), but the effect varied in areas where precipitation was high (Pacuare, Caribbean Sea) and was not detected at the temperate site (Maputaland, Indian Ocean). High air temperature reduced hatchling output only at the area experiencing seasonal droughts (Playa Grande). Climatic projections showed a drastic increase in air temperature and a mild decrease in precipitation at all sites by 2100. The most unfavorable conditions were projected for Sandy Point where hatching success has already declined over time along with precipitation levels. The heterogeneous effect of climate may lead to local extinctions of leatherback turtles in some areas but survival in others by 2100.

A simple, physiologically-based model of sea turtle remigration intervals and nesting population dynamics: Effects of temperature.

Variation in the yearly number of sea turtles nesting at rookeries can interfere with population estimates and obscure real population dynamics. Previous theoretical models suggested that this variation in nesting numbers may be driven by changes in resources at the foraging grounds. We developed a physiologically-based model that uses temperatures at foraging sites to predict foraging conditions, resource accumulation, remigration probabilities, and, ultimately, nesting numbers for a stable population of sea turtles. We used this model to explore several scenarios of temperature variation at the foraging grounds, including one-year perturbations and cyclical temperature oscillations. We found that thermally driven resource variation can indeed synchronize nesting in groups of turtles, creating cohorts, but that these cohorts tend to break down over 5-10 years unless regenerated by environmental conditions. Cohorts were broken down faster at lower temperatures. One-year perturbations of low temperature had a synchronizing effect on nesting the following year, while high temperature perturbations tended to delay nesting in a less synchronized way. Cyclical temperatures lead to cyclical responses both in nesting numbers and remigration intervals, with the amplitude and lag of the response depending on the duration of the cycle. Overall, model behavior is consistent with observations at nesting beaches. Future work should focus on refining the model to fit particular nesting populations and testing further whether or not it may be used to predict observed nesting numbers and remigration intervals.

Shading and watering as a tool to mitigate the impacts of climate change in sea turtle nests.

Increasing sand temperatures resulting from climate change may negatively impact sea turtle nests by altering sex ratios and decreasing reproductive output. We analyzed the effect of nest shading and watering on sand temperatures as climate mitigation strategies in a beach hatchery at Playa Grande, Costa Rica. We set up plots and placed thermocouples at depths of 45 cm and 75 cm. Half of the plots were shaded and half were exposed to the sun. Within these exposure treatments, we applied three watering treatments over one month, replicating local climatic conditions experienced in this area. We also examined gravimetric water content of sand by collecting sand samples the day before watering began, the day after watering was complete, and one month after completion. Shading had the largest impact on sand temperature, followed by watering and depth. All watering treatments lowered sand temperature, but the effect varied with depth. Temperatures in plots that received water returned to control levels within 10 days after watering stopped. Water content increased at both depths in the two highest water treatments, and 30 days after the end of water application remained higher than plots with low water. While the impacts of watering on sand temperature dissipate rapidly after the end of application, the impacts on water content are much more lasting. Although less effective at lowering sand temperatures than shading, watering may benefit sea turtle clutches by offsetting negative impacts of low levels of rain in particularly dry areas. Prior to implementing such strategies, the natural conditions at the location of interest (e.g. clutch depth, environmental conditions, and beach characteristics) and natural hatchling sex ratios should be taken into consideration. These results provide insight into the effectiveness of nest shading and watering as climate mitigation techniques and illustrate important points of consideration in the crafting of such strategies.

Climate change overruns resilience conferred by temperature-dependent sex determination in sea turtles and threatens their survival.

Temperature-dependent sex determination (TSD) is the predominant form of environmental sex determination (ESD) in reptiles, but the adaptive significance of TSD in this group remains unclear. Additionally, the viability of species with TSD may be compromised as climate gets warmer. We simulated population responses in a turtle with TSD to increasing nest temperatures and compared the results to those of a virtual population with genotypic sex determination (GSD) and fixed sex ratios. Then, we assessed the effectiveness of TSD as a mechanism to maintain populations under climate change scenarios. TSD populations were more resilient to increased nest temperatures and mitigated the negative effects of high temperatures by increasing production of female offspring and therefore, future fecundity. That buffered the negative effect of temperature on the population growth. TSD provides an evolutionary advantage to sea turtles. However, this mechanism was only effective over a range of temperatures and will become inefficient as temperatures rise to levels projected by current climate change models. Projected global warming threatens survival of sea turtles, and the IPCC high gas concentration scenario may result in extirpation of the studied population in 50 years.

Mojave desert tortoise (Gopherus agassizii) thermal ecology and reproductive success along a rainfall cline.

Desert resource environments (e.g. microclimates, food) are tied to limited, highly localized rainfall regimes which generate microgeographic variation in the life histories of inhabitants. Typically, enhanced growth rates, reproduction and survivorship are observed in response to increased resource availability in a variety of desert plants and short-lived animals. We examined the thermal ecology and reproduction of US federally threatened Mojave desert tortoises (Gopherus agassizii), long-lived and large-bodied ectotherms, at opposite ends of a 250-m elevation-related rainfall cline within Ivanpah Valley in the eastern Mojave Desert, California, USA. Biophysical operative environments in both the upper-elevation, "Cima," and the lower-elevation, "Pumphouse," plots corresponded with daily and seasonal patterns of incident solar radiation. Cima received 22% more rainfall and contained greater perennial vegetative cover, which conferred 5°C-cooler daytime shaded temperatures. In a monitored average rainfall year, Cima tortoises had longer potential activity periods by up to several hours and greater ephemeral forage. Enhanced resource availability in Cima was associated with larger-bodied females producing larger eggs, while still producing the same number of eggs as Pumphouse females. However, reproductive success was lower in Cima because 90% of eggs were depredated versus 11% in Pumphouse, indicating that predatory interactions produced counter-gradient variation in reproductive success across the rainfall cline. Land-use impacts on deserts (e.g. solar energy generation) are increasing rapidly, and conservation strategies designed to protect and recover threatened desert inhabitants, such as desert tortoises, should incorporate these strong ecosystem-level responses to regional resource variation in assessments of habitat for prospective development and mitigation efforts.

Predicting bycatch hotspots for endangered leatherback turtles on longlines in the Pacific Ocean.

Fisheries bycatch is a critical source of mortality for rapidly declining populations of leatherback turtles, Dermochelys coriacea. We integrated use-intensity distributions for 135 satellite-tracked adult turtles with longline fishing effort to estimate predicted bycatch risk over space and time in the Pacific Ocean. Areas of predicted bycatch risk did not overlap for eastern and western Pacific nesting populations, warranting their consideration as distinct management units with respect to fisheries bycatch. For western Pacific nesting populations, we identified several areas of high risk in the north and central Pacific, but greatest risk was adjacent to primary nesting beaches in tropical seas of Indo-Pacific islands, largely confined to several exclusive economic zones under the jurisdiction of national authorities. For eastern Pacific nesting populations, we identified moderate risk associated with migrations to nesting beaches, but the greatest risk was in the South Pacific Gyre, a broad pelagic zone outside national waters where management is currently lacking and may prove difficult to implement. Efforts should focus on these predicted hotspots to develop more targeted management approaches to alleviate leatherback bycatch.

Movements and diving behavior of internesting green turtles along Pacific Costa Rica.

Using satellite transmitters, we determined the internesting movements, spatial ecology and diving behavior of East Pacific green turtles (Chelonia mydas) nesting on Nombre de Jesús and Zapotillal beaches along the Pacific coast of northwestern Costa Rica. Kernel density analysis indicated that turtles spent most of their time in a particularly small area in the vicinity of the nesting beaches (50% utilization distribution was an area of 3 km(2) ). Minimum daily distance traveled during a 12 day internesting period was 4.6 ± 3.5 km. Dives were short and primarily occupied the upper 10 m of the water column. Turtles spent most of their time resting at the surface and conducting U-dives (ranging from 60 to 81% of the total tracking time involved in those activities). Turtles showed a strong diel pattern, U-dives mainly took place during the day and turtles spent a large amount of time resting at the surface at night. The lack of long-distance movements demonstrated that this area was heavily utilized by turtles during the nesting season and, therefore, was a crucial location for conservation of this highly endangered green turtle population. The unique behavior of these turtles in resting at the surface at night might make them particularly vulnerable to fishing activities near the nesting beaches.

Stable isotopes of C and N reveal habitat dependent dietary overlap between native and introduced turtles Pseudemys rubriventris and Trachemys scripta.

Habitat degradation and species introductions are two of the leading causes of species declines on a global scale. Invasive species negatively impact native species through predation and competition for limited resources. The impacts of invasive species may be increased in habitats where habitat degradation is higher due to reductions of prey abundance and distribution. Using stable isotope analyses and extensive measurements of resource availability we determined how resource availability impacts the long term carbon and nitrogen assimilation of the invasive red-eared slider turtle (Trachemys scripta elegans) and a native, threatened species, the red-bellied turtle (Pseudemys rubriventris) at two different freshwater wetland complexes in Pennsylvania, USA. At a larger wetland complex with greater vegetative species richness and diversity, our stable isotope analyses showed dietary niche partitioning between species, whereas analyses from a smaller wetland complex with lower vegetative species richness and diversity showed significant dietary niche overlap. Determining the potential for competition between these two turtle species is important to understanding the ecological impacts of red-eared slider turtles in wetland habitats. In smaller wetlands with increased potential for competition between native turtles and invasive red-eared slider turtles we expect that when shared resources become limited, red-eared slider turtles will negatively impact native turtle species leading to long term population declines. Protection of intact wetland complexes and the reduction of introduced species populations are paramount to preserving populations of native species.