Managing sun bears in a changing tropical landscape

Aim

Across the tropics, large‐bodied mammal species are threatened by rapid and widespread forest habitat conversion by either commercial logging or agricultural expansion. How such species use these habitats is an important area of research for guiding their future management. The tropical forest‐dwelling sun bear, Helarctos malayanus, is the least known of the eight bear species. Consequently, the IUCN/SSC Bear Specialist Group ranks research on this species as a top priority. This study aims to investigate landscape variables that influence sun bear habitat use in forests under varying levels of degradation and protection.

Location

A 20,998 km² Sumatra forest landscape covering Kerinci Seblat National Park (KSNP), Batang Hari Protection Forest (BHPF) and neighbouring logging and agricultural concessions.

Methods

An occupancy‐based sampling technique using detection/non‐detection data with 10 landscape covariates was applied in six study areas that operated a total of 125 camera traps. The potential differences between habitat use (ψ) of sun bears were first modelled with broad‐scale covariates of study area, land‐use types and forest type. Sun bear habitat use was then investigated with the finer‐scale landscape features associated within these areas.

Results

From 10,935 trap nights, sun bears were recorded at altitudes ranging from 365 to 1791 m. At a broad‐scale, habitat use increased with protection status, being highest in KSNP (0.688 ± 0.092, ± SE) and BHPF (0.621 ± 0.110) compared to production (0.418 ± 0.121) and convertible (0.286 ± 0.122) forests. Within these areas, sun bears showed a preference for forest that was further from public roads and villages and at a lower elevation.

Main conclusions

The habitat suitability model identified several high‐quality habitat patches outside of the priority conservation areas for immediate protection. Consequently, conservation management strategies should emphasize the importance of high conservation value forests and prohibit further conversion of threatened lowland forests.

     

The impact of fossil stratigraphic ranges on tip-calibration,and the accuracy and precision of divergence time estimates

The molecular clock provides the only viable means of establishing realistic evolutionary timescales but it remains unclear how best to calibrate divergence time analyses. Calibrations can be applied to the tips and/or to the nodes of a phylogeny. Tip-calibration is an attractive approach since it allows fossil species to be included alongside extant relatives in molecular clock analyses. However, most fossil species are known from multiple stratigraphical horizons and it remains unclear how such age ranges should be interpreted to codify tip-calibrations. We use simulations and empirical data to explore the impact on precision and accuracy of different approaches to informing tip-calibrations. In particular, we focus on the effect of using tip-calibrations defined using the oldest vs youngest stratigraphic occurrences, the full stratigraphical range, as well as confidence intervals on these data points. The results of our simulations show that using different calibration approaches leads to different divergence-time estimates and demonstrate that concentrating tip-calibrations near the root of the dated phylogeny improves both precision and accuracy of estimated divergence times. Finally, our results indicate that the highest levels of accuracy and precision are achieved when fossil tips are calibrated based on the fossil occurrence from which the morphological data were derived. These trends were corroborated by analysis of an empirical dataset for Ursidae. Overall, we conclude that tip-dating analyses should, in particular, employ tip calibrations close to the root of the tree and they should be calibrated based on the age of the fossil used to inform the morphological data used in Total Evidence Dating.     

Tooth root morphology as an indicator for dietary specialization in carnivores (Mammalia: Carnivora)

The Carnivora occupy a wide range of feeding niches in concordance with the enormous diversity in their skull and dental form. It is well established that differences in crown morphology are linked to variations in the material properties of the foods ingested and masticated. However, how tooth root form is related to dietary specialization is less well known. In the present study, we investigate the relationship between tooth root morphology and dietary specialization in terrestrial carnivores (canids, felids, hyaenids, and ursids). We specifically address the question of how variation in tooth root surface area is related to bite force potentials as one of the crucial masticatory performance parameters in feeding ecology. We applied computed tomography imaging to reconstruct and quantify dental root surface area in 17 extant carnivore species. Moreover, we computed maximal bite force at several tooth positions based on a dry skull model and assessed the relationship of root surface area to skull size, maximal bite force, food properties, and prey size. We found that postcanine tooth root surface areas corrected for skull size serve as a proxy for bite force potentials and, by extension, dietary specialization in carnivores. Irrespective of taxonomic affinity, species that feed on hard food objects have larger tooth roots than those that eat soft or tough foods. Moreover, carnivores that prey on large animals have larger tooth root surface areas. Our results show that tooth root morphology is a useful indicator of bite force production and allows inferences to be made about dietary ecology in both extant and extinct mammals. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105, 456–471.     

On the association of giant short-faced bear (Arctodus simus) and brown bear (Ursus arctos) in late Pleistocene North America

Climate change and human impacts are often implicated in Quaternary megafaunal extinctions. The discovery of associated remains of extinct giant short-faced bears (Arctodus simus) and invading brown bears (Ursus arctos) raises the possibility of competition as another potential factor. We describe fossil remains of both genera from Pellucidar Cave, Vancouver Island, Canada. Analyses of ancient mitochondrial DNA support the identifications of post-cranial brown bear specimens and assign these bears to Clade 4. Our results are consistent with the migration of brown bears from Eastern Beringia to the contiguous United States before the Last Glacial Maximum (LGM) and to Vancouver Island as environmental conditions became favorable after the LGM. Radiocarbon age estimates on these specimens indicate the presence of giant short-faced bears approximately 13.5 thousand calibrated years before present (cal. ka BP; uncalibrated 11,775 ± 30, 11,720 ± 50, and 11,615 ± 30 BP) and of brown bears immediately preceding (～14.5 cal. ka BP; 12,440 ± 35, 12,425 ± 30 BP) and following this time (～13 cal. ka BP; uncal. 11,100 ± 30 BP), suggesting niche partitioning to reduce competition among these species. We suggest that shifts in food availability or quality due to post-glacial vegetation and faunal changes were probably of primary importance in the arrival and the disappearance of giant short-faced bears on Vancouver Island. This study focuses on a key time period and geographic location that is useful in understanding Pleistocene extinctions in North America.     

A reliable, non-invasive PCR method for giant panda (Ailuropoda melanoleuca) sex identification

We developed an inexpensive, fast and reliable PCR method for sex identification of giant panda (Ailuropoda melanoleuca) by using one pair of primers to co-amplify homologous fragments with size polymorphism that located at amelogenin (AMEL) exon 5. In giant panda, a 63 bp deletion in exon 5 of Y-linked allele provides a significant discrimination between AMELX and AMELY, thus the amplification products can be distinguished simply by agarose gel electrophoresis, exhibiting sex-specific banding patterns (male: 237 bp, 174 bp; female: 237 bp). Both blood and feces samples from known-sex giant pandas were successfully amplified. Cross species test also revealed that this method could be applied to other Ursidae species. These authors contributed equally to this work.     

Tandemly repeated satellite DNA ofDolichopoda schiavazzii: A test for models on the evolution of highly repetitive DNA

The evolutionary relationships among the Carnivora were studied in a phylogenetic analysis based on the complete mitochondrial cytochromeb gene. The study, which addressed primarily the relationships among the Caniformia, included 4 feliform and 26 caniform species, with 9 pinnipeds. The analysis identified five caniform clades: Canidae, Ailuridae (with the monotypic lesser panda), Musteloidea (Mustelidae+Procyonidae), Ursidae (including the giant panda), and Pinnipedia. The closest relatives of the Pinnipedia among terrestrial caniforms were not identified conclusively. Our analysis shows that the skunks are only distantly related to remaining mustelids (Mustelidae sensu stricto) and that the family Mustelidae, including the skunks, is paraphyletic. The relationship among the five caniform clades was unresolved, suggesting an evolutionary separation within a relatively short period of time. Based on distance values, we propose that this primary diversification took place 45 million years ago.     

A reliable genetic technique for sex determination of giant panda (<Emphasis Type="Italic">Ailuropoda melanoleuca</Emphasis>) from non-invasively collected hair samples

Extractions from non-invasive hair samples usually yield low amounts of highly degraded DNA. Previously developed mammal molecular sexing methods were not designed with such sub-optimal conditions in mind. We developed a simple and reliable PCR-based sexing method aimed at degraded, low yield DNA extractions from the giant panda (Ailuropoda melanoleuca). Comparisons of this new primer set with others showed that the reliability of sex determination from low-yield, degraded DNA extractions was improved if; amplification products were short (<170 bp); and the Y-chromosome amplification product was shorter than the X-chromosome amplification product. The primers developed in this study appear useful for sex determination in other bear species.     

A system for sex determination from degraded DNA: a useful tool for palaeogenetics and conservation genetics of ursids

In this paper, we characterise three sex-specific genes (ZFX/Y, SRY, AMLX/Y) for all eight extant bear species and propose a new, robust and accurate molecular procedure to identify the sex of bears from non-invasive samples and fossil remains. These materials contain tiny amounts of poorly preserved deoxyribonucleic acid (DNA), leaving Polymerase Chain Reaction (PCR) amplification very prone to contamination and difficult to analyse. By taking into account the ancient DNA requirements, the duplex procedures that we developed are efficient not only on DNA extracted from bear faeces but also on ancient DNA extracted from a brown bear fossil 7,500 years old. Defined specifically for ursids, the procedure for faecal samples (co-amplification of ZFX/Y and SRY markers) appears more accurate than other published procedures, as it prevents cross-amplification of potential ingested prey and contamination (19 non-ursid species tested). This system can be applied to threatened bear populations to improve the reliability of sex-ratio and population-size estimates based on non-invasive samples. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorised users.