What factors influence the rediscovery of lost tetrapod species?

We created a database of lost and rediscovered tetrapod species, identified patterns in their distribution and factors influencing rediscovery. Tetrapod species are being lost at a faster rate than they are being rediscovered, due to slowing rates of rediscovery for amphibians, birds and mammals, and rapid rates of loss for reptiles. Finding lost species and preventing future losses should therefore be a conservation priority. By comparing the taxonomic and spatial distribution of lost and rediscovered tetrapod species, we have identified regions and taxa with many lost species in comparison to those that have been rediscovered-our results may help to prioritise search effort to find them. By identifying factors that influence rediscovery, we have improved our ability to broadly distinguish the types of species that are likely to be found from those that are not (because they are likely to be extinct). Some lost species, particularly those that are small and perceived to be uncharismatic, may have been neglected in terms of conservation effort, and other lost species may be hard to find due to their intrinsic characteristics and the characteristics of the environments they occupy (e.g. nocturnal species, fossorial species and species occupying habitats that are more difficult to survey such as wetlands). These lost species may genuinely await rediscovery. However, other lost species that possess characteristics associated with rediscovery (e.g. large species) and that are also associated with factors that negatively influence rediscovery (e.g. those occupying small islands) are more likely to be extinct. Our results may foster pragmatic search protocols that prioritise lost species likely to still exist.

Turtles and Tortoises Are in Trouble.

Turtles and tortoises (chelonians) have been integral components of global ecosystems for about 220 million years and have played important roles in human culture for at least 400,000 years. The chelonian shell is a remarkable evolutionary adaptation, facilitating success in terrestrial, freshwater and marine ecosystems. Today, more than half of the 360 living species and 482 total taxa (species and subspecies combined) are threatened with extinction. This places chelonians among the groups with the highest extinction risk of any sizeable vertebrate group. Turtle populations are declining rapidly due to habitat loss, consumption by humans for food and traditional medicines and collection for the international pet trade. Many taxa could become extinct in this century. Here, we examine survival threats to turtles and tortoises and discuss the interventions that will be needed to prevent widespread extinction in this group in coming decades.

Home range variation of two different-sized groups of golden snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia, China: implications for feeding competition.

Knowledge on the home range size of a species or population is important for understanding its behavioral and social ecology and improving the effectiveness of conservation strategies. We studied the home range size of two different-sized groups of golden snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia, China. The larger group (236 individuals) had a home range of 22.5 km2 from September 2007 to July 2008, whereas the smaller group (62 individuals) occupied a home range of 12.4 km2 from November 2008 to July 2009. Both groups exhibited considerable seasonal variation in their home range size, which was likely due to seasonal changes in food availability and distribution. The home range in any given season (winter, spring, summer, or winter+spring+summer) of the larger group was larger than that of the smaller group. As the two groups were studied in the same area, with the confounding effects of food availability thus minimized, the positive relationship between home range size and group size suggested that scramble feeding competition increased within the larger group.

Genetic analysis suggests dispersal among chimpanzees in a fragmented forest landscape in Uganda.

Habitat fragmentation is a leading threat to global biodiversity. Dispersal plays a key role in gene flow and population viability, but the impact of fragmentation on dispersal patterns remains poorly understood. Among chimpanzees, males typically remain in their natal communities while females often disperse. However, habitat loss and fragmentation may cause severe ecological disruptions, potentially resulting in decreased fitness benefits of male philopatry and limited female dispersal ability. To investigate this issue, we genotyped nearly 900 non-invasively collected chimpanzee fecal samples across a fragmented forest habitat that may function as a corridor between two large continuous forests in Uganda, and used the spatial associations among co-sampled genotypes to attribute a total of 229 individuals to 10 distinct communities, including 9 communities in the corridor habitat and 1 in continuous forest. We then used parentage analyses to infer instances of between-community dispersal. Of the 115 parent-offspring dyads detected with confidence, members of 39% (N = 26) of mother-daughter dyads were found in different communities, while members of 10% (N = 5) of father-son dyads were found in different communities. We also found direct evidence for one dispersal event that occurred during the study period, as a female's sample found first in one community was found multiple times in another community 19 months later. These findings suggest that even in fragmented habitats, chimpanzee males remain in their natal communities while females tend to disperse. Corridor enhancement in unprotected forest fragments could help maintain gene flow in chimpanzees and other species amid anthropogenic pressures.

Characterization of seasonal reproductive and stress steroid hormones in wild Radiated Tortoises, Astrochelys radiata.

The critically endangered Radiated Tortoise (Astrochelys radiata) is endemic to the southern coastlines of Madagascar. Once common, wild populations of this tortoise have undergone dramatic declines in recent years. Although there have been studies documenting reproductive activities, reproductive physiological parameters are unknown yet may be crucial in the recovery of the species. Over four research seasons in remote field locations native to A. radiata, we surveyed for, radio-tracked, and sampled wild, free ranging tortoises. We sampled and measured stress and reproductive parameters (corticosterone [CORT], testosterone [T], estradiol-17ß [E2], and progesterone [P]) in 311 plasma samples from 203 wild A. radiata, capturing their active period. Generally, hormone concentrations were associated with body condition, temperature, and humidity. There was wide variation in CORT that varied monthly and by group. Juvenile tortoises maintained more than twice the mean basal CORT concentrations than either adult sex, with the most dramatic distinctions in the middle of the wet season. For adult sex hormones, the last months of the dry season and into the wet season when ground humidities are low and just begin to rise prior to temperature declines, male T concentrations gradually increased to a peak before returning to near undetectable values into the dry season. We had limited data for T concentrations in females, but found average T concentrations were much lower than in males and positively correlated with larger female home range sizes. For female hormone cycles, E2 also peaked in the early 1/3 of the wet season along with male T, and was followed by an uptick in P which correlates to the putative ovulatory cycle. Females tracked over four years showed variation in patterns of P, indicating that number and frequency of clutches vary. Our results suggest that 1) there is high species plasticity in response to stress; 2) A. radiata reproductive cycling is somewhat dissociated with courtship timing and is instead triggered by environmental cues; and 3) individual female reproductive output is irregular. This study is oone of the first to document and describe multi-year seasonal stress and reproductive hormones in a free-ranging Malagasy chelonian. These data may be used to identify key high-production habitats for conservation, and aide in captive management and reproduction in assurance colonies for species health and survival.

Comparative ecophysiology of a critically endangered (CR) ectotherm: Implications for conservation management.

Captive breeding is a vital conservation tool for many endangered species programs. It is often a last resort when wild animal population numbers drop to below critical minimums for natural reproduction. However, critical ecophysiological information of wild counterparts may not be well documented or understood, leading to years of minimal breeding successes. We collected endocrine and associated ecological data on a critically endangered ectotherm concurrently in the wild and in captivity over several years. We tracked plasma concentrations of steroid stress and reproductive hormones, body condition, activity, and environmental parameters in three populations (one wild and two geographically distinct captive) of ploughshare tortoise (Astrochelys yniphora). Hormone profiles along with environmental and behavioral data are presented and compared. We show that animals have particular seasonal environmental requirements that can affect annual reproduction, captivity affects reproductive state, and sociality may be required at certain times of the year for breeding to be successful. Our data suggest that changes in climatic conditions experienced by individuals, either due to decades-long shifts or hemispheric differences when translocated from their native range, can stifle breeding success for several years while the animals physiologically acclimatize. We also found that captivity affects stress (plasma corticosterone) and body condition of adults and juveniles differently and seasonally. Our results indicate that phenotypic plasticity in reproduction and behavior is related to environmental cues in long-lived ectotherms, and detailed ecophysiological data should be used when establishing and improving captive husbandry conditions for conservation breeding programs. Further, considering the recent revelation of this tortoises' possible extirpation from the wild, these data are critically opportune and may be key to the survival of this species.

Chimpanzees (Pan troglodytes) Flexibly Use Introduced Species for Nesting and Bark Feeding in a Human-Dominated Habitat.

As habitat loss and fragmentation place growing pressure on endangered nonhuman primate populations, researchers find increasing evidence for novel responses in behavior. In western Uganda between the Budongo and Bugoma Forests, chimpanzees (Pan troglodytes schweinfurthii) inhabit a mosaic landscape comprising forest fragments, human settlements, and agricultural land. We recorded nests and feeding evidence of unhabituated chimpanzees in this region over a 12-mo period. We found extensive evidence of nesting in introduced tree species, including eucalyptus (Eucalyptus grandis), guava (Psidium guajava), cocoa (Theobroma cacao), and Caribbean pine (Pinus caribaea). In addition, we found instances of ground nesting, nest reuse, and composite nests constructed from branches of multiple trees. This evidence may indicate a lack of suitable nesting trees or attempts by chimpanzees to nest in areas of riparian forest that allow them to avoid human detection. We also found new evidence for eucalyptus bark feeding by chimpanzees. Such evidence suggests chimpanzees respond flexibly to mitigate anthropogenic pressures in human-dominated landscapes. The limits of such flexibility remain unknown. Further research is needed to examine systematically the factors influencing the use of such resources and to understand better the extent to which chimpanzees can persist while relying on them.

Genetic censusing identifies an unexpectedly sizeable population of an endangered large mammal in a fragmented forest landscape.

BACKGROUND: As habitat degradation and fragmentation continue to impact wildlife populations around the world, it is critical to understand the behavioral flexibility of species in these environments. In Uganda, the mostly unprotected forest fragment landscape between the Budongo and Bugoma Forests is a potential corridor for chimpanzees, yet little is known about the status of chimpanzee populations in these fragments. RESULTS: From 2011 through 2013, we noninvasively collected 865 chimpanzee fecal samples across 633 km(2) and successfully genotyped 662 (77%) at up to 14 microsatellite loci. These genotypes corresponded to 182 chimpanzees, with a mean of 3.5 captures per individual. We obtained population size estimates of 256 (95% confidence interval 246-321) and 319 (288-357) chimpanzees using capture-with-replacement and spatially explicit capture-recapture models, respectively. The spatial clustering of associated genotypes suggests the presence of at least nine communities containing a minimum of 8-33 individuals each. Putative community distributions defined by the locations of associated genotypes correspond well with the distribution of 14 Y-chromosome haplotypes. CONCLUSIONS: These census figures are more than three times greater than a previous estimate based on an extrapolation from small-scale nest count surveys that tend to underestimate population size. The distribution of genotype clusters and Y-chromosome haplotypes together indicate the presence of numerous male philopatric chimpanzee communities throughout the corridor habitat. Our findings demonstrate that, despite extensive habitat loss and fragmentation, chimpanzees remain widely distributed and exhibit distinct community home ranges. Our results further imply that elusive and rare species may adapt to degraded habitats more successfully than previously believed. Their long-term persistence is unlikely, however, if protection is not afforded to them and habitat loss continues unabated.

Chimpanzee nesting patterns in savanna habitat: environmental influences and preferences.

Data on chimpanzee (Pan troglodytes) nesting patterns were collected in Issa, Ugalla, western Tanzania. Ugalla is one of the driest, most open, and seasonal habitats inhabited by chimpanzees. We investigated the physical characteristics of nests and trees used for nesting to understand environmental influences on nest building and identify the characteristics preferred by the chimpanzees and the basis for such preferences. We analyzed 2,167 nests and 1,523 nesting trees. Most nests were built in the middle section of the tree crown and close to the tree trunk, and used a single tree in construction. Some physical characteristics of nests (e.g., distance from tree trunk) seemed to be the result of constraints imposed by tree structure. Issa chimpanzees preferred tall trees with high first branches for nesting supporting the hypothesis that elevated height of a sleeping place is a predator defense strategy. The height from the ground to the first branch showed less variation than either tree height or crown height and correlated weakly with tree height, suggesting that height from the ground to the first branch may be a more important factor than tree height alone in selecting a tree in which to nest. As in other study sites, the chimpanzees used tree species in proportions that did not correspond to their abundance suggesting tree species preference. We report for the first time that chimpanzees directionally oriented their nests and propose that this may be to maximize sunlight. We compare our data to those of other chimpanzee study sites.

Foods eaten by the Sichuan snub-nosed monkey (Rhinopithecus roxellana) in Shennongjia National Nature Reserve, China, in relation to nutritional chemistry.

The diet of Rhinopithecus roxellana is characterized by lichens, which are available year-round and an uncommon food source for nonhuman primates, supplemented by seasonal plant foods. We present the first study of foods eaten by R. roxellana in relation to nutritional chemistry in Shennongjia National Nature Reserve, Hubei Province, China. We analyzed the nutrients (crude protein, crude fat, and water soluble carbohydrate [WSC]) and feeding deterrents (crude fiber, condensed tannin [CT], and total phenolic [TP]) of 111 parts from 53 plant species and of 6 lichen species. Results showed that lichens were a good choice for R. roxellana living in habitats with limited and seasonally available plant foods. They contained higher concentrations of WSC than foliage, fat concentrations equivalent to those in plant parts (except fruits/seeds), and lower concentrations of fiber than mature leaves, flowers, and fruits. Although lichens were lower in protein than plant parts (except fruits), the monkeys could likely meet their protein requirement by eating seasonal plant foods rich in protein, including foliage, flowers, buds, and seeds. The monkeys were not observed to select foliage higher in protein, but appeared to select mature leaves higher in WSC and lower in fiber. Fruits were a good source of WSC and fat, and seeds were a good source of fat. Neither CT nor TP content showed negative effects on the selection of mature leaves or lichens.

Characteristics of a group of Hubei Golden Snub-nosed Monkeys (Rhinopithecus roxellana hubeiensis) before and after major snow storms.

Natural disasters can negatively affect primate population demography and social group structure. A clear understanding of these effects has important implications for wildlife conservation. The worst snow storms in nearly five decades hit portions of southern and central China between January 10 and February 6, 2008, presenting a unique opportunity to observe their immediate effects on a previously studied group of Hubei Golden Snub-nosed Monkeys (Rhinopithecus roxellana hubeiensis) in temperate forests in Shennongjia Nature Reserve, Hubei Province, China. We recorded social and demographic characteristics of the group before and after the snow storms. The average group size decreased from 270 individuals before the storms to 197 individuals after the storms, a reduction of 27.2%. Adult females (30.1%), juveniles (38.1%) and infants (55.4%) suffered higher mortality than did adult males (15.7%). Despite age and sex-based differences in mortality, the ratios of adult males to adult females, adults to immatures and adult females to immatures remained similar before and after the storms. However, higher mortality among females, juveniles and infants may reduce the group's long-term potential for growth.

Sleeping tree choice by Bwindi chimpanzees.

Unlike nearly all other nonhuman primates, great apes build sleeping nests. In Bwindi Impenetrable National Park, Uganda, chimpanzees build nests nightly and also build day nests. We investigated patterns of nest tree use by Bwindi chimpanzees to understand ecological influences on nest tree selection. We analyzed data on 3,414 chimpanzee nests located from 2000 to 2004. Chimpanzees at Bwindi were selective in their use of nest trees. Of at least 163 tree species known to occur in Bwindi [Butynski, Ecological survey of the Impenetrable (Bwindi) Forest, Uganda, and recommendations for its conservation and management. Report to the Government of Uganda, 1984], chimpanzees utilized only 38 species for nesting. Of these, four tree species (Cassipourea sp., Chrysophyllum gorungosanum, Drypetes gerrardii, and Teclea nobilis) accounted for 72.1% of all nest trees. There was considerable variation in nesting frequencies among the top four species between and within years. However, these species were used significantly more often for nesting than other species in 70.9% (39 of 55) of the months of this study. A Spearman rank correlation found no significant relationship between tree abundance and tree species preference. Ninety-three percent of all nests were constructed in food tree species, although not necessarily at the same time the trees bore food items used by chimpanzees. The results indicate that nesting tree species preferences exist. Bwindi chimpanzees' choice of nesting tree species does not appear to be dependent on tree species density or use of the tree for food. We discuss possible reasons for the selectivity in nest trees by the Bwindi population.

The behavioral ecology of sympatric African apes: implications for understanding fossil hominoid ecology.

The behavioral ecology of the great apes is key evidence used in the reconstruction of the behavior of extinct ape and hominid taxa. Chimpanzees and gorillas have been studied in detail in the wild, and some studies of their behavioral ecology in sympatry have also been been carried out. Although the two ape species have divergent behavior and ecology in important respects, recent studies have shown that the interspecific differences are not as stark as previously thought and subsequently urge new consideration of how they share forest resources when sympatric. These new data require re-examination of assumptions about key aspects of chimpanzee-gorilla ecological divergence, such as diet, ranging and nesting patterns, and the mating system. Diet is a key component of the species' adaptive complexes that facilitates avoidance of direct competition from the other. While the nutritional basis for chimpanzee food choice remains unclear and no doubt varies from site to site, this species is a ripe fruit specialist and ranges farther during periods of ripe fruit scarcity. Gorillas in the same habitat also feed on ripe fruit when widely available, but fall back onto fibrous plant foods during lean periods. The inclusion of animal protein in the diet of the chimpanzees and its absence in that of the gorillas also distinguish the species ecologically. It may also offer clues to aspects of ecological divergence among early members of the hominid phylogeny. The paper concludes by suggesting likely characteristics of sympatric associations of Pliocene hominids, based on field data from extant sympatric apes.

Arboreal bipedalism in wild chimpanzees: implications for the evolution of hominid posture and locomotion.

Field observations of bipedal posture and locomotion in wild chimpanzees (Pan troglodytes) can serve as key evidence for reconstructing the likely origins of bipedalism in the last prehominid human ancestor. This paper reports on a sample of bipedal bouts, recorded ad libitum, in wild chimpanzees in Bwindi Impenetrable National Park in southwestern Uganda. The Ruhija community of chimpanzees in Bwindi displays a high rate of bipedal posture. In 246.7 hr of observation from 2001-2003, 179 instances of bipedal posture lasting 5 sec or longer were recorded, for a rate of 0.73 bouts per observation hour. Bipedalism was observed only on arboreal substrates, and was almost all postural, and not locomotor. Bipedalism was part of a complex series of positional behaviors related to feeding, which included two-legged standing, one-legged standing with arm support, and other intermediate postures. Ninety-six percent of bipedal bouts occurred in a foraging context, always as a chimpanzee reached to pluck fruit from tree limbs. Bipedalism was seen in both male and female adults, less frequently among juveniles, and rarely in infants. Both the frequency and duration of bipedal bouts showed a significant positive correlation with estimated substrate diameter. Neither fruit size nor nearest-neighbor association patterns were significantly correlated with the occurrence of bipedalism. Bipedalism is seen frequently in the Bwindi chimpanzee community, in part because of the unusual observer conditions at Bwindi. Most observations of bipedalism were made when the animals were in treetops and the observer at eye-level across narrow ravines. This suggests that wild chimpanzees may engage in bipedal behavior more often than is generally appreciated. Models of the likely evolutionary origins of bipedalism are considered in the light of Bwindi bipedalism data. Bipedalism among Bwindi chimpanzees suggests the origin of bipedal posture in hominids to be related to foraging advantages in fruit trees. It suggests important arboreal advantages in upright posture. The origin of postural bipedalism may have preceded and been causally disconnected from locomotor bipedalism.

Meat-adaptive genes and the evolution of slower aging in humans.

The chimpanzee life span is shorter than that of humans, which is consistent with a faster schedule of aging. We consider aspects of diet that may have selected for genes that allowed the evolution of longer human life spans with slower aging. Diet has changed remarkably during human evolution. All direct human ancestors are believed to have been largely herbivorous. Chimpanzees eat more meat than other great apes, but in captivity are sensitive to hypercholesterolemia and vascular disease. We argue that this dietary shift to increased regular consumption of fatty animal tissues in the course of hominid evolution was mediated by selection for "meat-adaptive" genes. This selection conferred resistance to disease risks associated with meat eating also increased life expectancy. One candidate gene is apolipoprotein E (apoE), with the E3 allele evolved in the genus Homo that reduces the risks for Alzheimer's and vascular disease, as well as influencing inflammation, infection, and neuronal growth. Other evolved genes mediate lipid metabolism and host defense. The timing of the evolution of apoE and other candidates for meat-adaptive genes is discussed in relation to key events in human evolution.

Brief communication: arboreal bipedalism in Bwindi chimpanzees.

Evidence of the form and function of bipedal behavior in nonhuman primates provides critical evidence to test theories about the origins of hominid bipedalism. Bipedalism has long been considered an evolutionarily interesting but rare behavior in wild chimpanzees. During May 2001, chimpanzees of the Ruhija community in the Bwindi Impenetrable National Park, Uganda, engaged in an exceptional frequency of arboreal bipedalism when feeding in large Ficus trees. Seventy-eight bipedal bouts of at least 5 sec duration were recorded for the entire community (0.49 bouts/hr), with a mean duration of 13.7 sec (+/-1.6 sec). The animals employed many variations on the bipedal postural theme, ranging from erect standing on the largest substrates while grasping overhead limbs for support, to standing on one leg while suspending the other leg in space, to extended-lean standing, in which bipedal standing transitioned into horizontal arm-leg suspension as the animal reached for more distant fruits. Bipedalism was used as part of a behavioral repertoire that integrated brachiation, four-limbed suspension, and forelimb-supported standing for effective small-fruit foraging. These observations suggest that under certain ecological conditions, arboreal bipedalism can be an important posture for wild chimpanzees, and may have been an important behavioral precursor to full terrestrial bipedalism.

Chimpanzees in Bwindi-Impenetrable National Park, Uganda, use different tools to obtain different types of honey.

Evidence of tool use for foraging for honey by chimpanzees in Bwindi-Impenetrable National Park, Uganda, is reported. These are the first records of tool use by chimpanzees in this region of the Albertine Rift. Tools of two types were found at sites of bee activity. Chimpanzees apparently use small stick tools to forage for the honey of a stingless bee [Meliponula bocandei (Trigonidae)] that nests in tree cavities and also in subterranean holes. They use significantly larger, thicker tools to assist in foraging for honey of African honeybees (Apis mellifera).

Social dynamics of intergroup encounters in the capped langur (Presbytis pileata).

Data from a 15-month field study of the capped langur (Presbytis pileata) in moist deciduous forest in Bangladesh show that during intergroup encounters males respond more aggressively to extra-group males and to the resident males of unfamiliar one-male groups than they do toward familiar males. Lone males followed established one-male groups and attempted to interact with group females. During intergroup encounters males responded to the approach of unfamiliar males with significantly more displays than were given to familiar (frequently encountered) males. The frequency of displays given to approaching groups showed a negative correlation with the frequency of encounters with those groups. In 50% of intergroup encounters males pushed and bit their group females if the females strayed from the immediate proximity of the group male. Further observations suggest that males obtain females that have emigrated from established groups or attempt to interact with them in established onemale groups. Males had a tenure from at least 13 months to at least 26 months, and between 1986 and 1988 no male changes were seen. Capped langur males defended females from other males, but females did not defend resources or participate in intergroup encounters. The implications of this sex difference in behavior during encounters is discussed with regard to ecological models of female-bonded primate groups.