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1.  Prioritizing Tiger Conservation through Landscape Genetics and Habitat Linkages 
PLoS ONE  2014;9(11):e111207.
Even with global support for tiger (Panthera tigris) conservation their survival is threatened by poaching, habitat loss and isolation. Currently about 3,000 wild tigers persist in small fragmented populations within seven percent of their historic range. Identifying and securing habitat linkages that connect source populations for maintaining landscape-level gene flow is an important long-term conservation strategy for endangered carnivores. However, habitat corridors that link regional tiger populations are often lost to development projects due to lack of objective evidence on their importance. Here, we use individual based genetic analysis in combination with landscape permeability models to identify and prioritize movement corridors across seven tiger populations within the Central Indian Landscape. By using a panel of 11 microsatellites we identified 169 individual tigers from 587 scat and 17 tissue samples. We detected four genetic clusters within Central India with limited gene flow among three of them. Bayesian and likelihood analyses identified 17 tigers as having recent immigrant ancestry. Spatially explicit tiger occupancy obtained from extensive landscape-scale surveys across 76,913 km2 of forest habitat was found to be only 21,290 km2. After accounting for detection bias, the covariates that best explained tiger occupancy were large, remote, dense forest patches; large ungulate abundance, and low human footprint. We used tiger occupancy probability to parameterize habitat permeability for modeling habitat linkages using least-cost and circuit theory pathway analyses. Pairwise genetic differences (FST) between populations were better explained by modeled linkage costs (r>0.5, p<0.05) compared to Euclidean distances, which was in consonance with observed habitat fragmentation. The results of our study highlight that many corridors may still be functional as there is evidence of contemporary migration. Conservation efforts should provide legal status to corridors, use smart green infrastructure to mitigate development impacts, and restore habitats where connectivity has been lost.
doi:10.1371/journal.pone.0111207
PMCID: PMC4230928  PMID: 25393234
2.  Population Status of a Cryptic Top Predator: An Island-Wide Assessment of Tigers in Sumatran Rainforests 
PLoS ONE  2011;6(11):e25931.
Large carnivores living in tropical rainforests are under immense pressure from the rapid conversion of their habitat. In response, millions of dollars are spent on conserving these species. However, the cost-effectiveness of such investments is poorly understood and this is largely because the requisite population estimates are difficult to achieve at appropriate spatial scales for these secretive species. Here, we apply a robust detection/non-detection sampling technique to produce the first reliable population metric (occupancy) for a critically endangered large carnivore; the Sumatran tiger (Panthera tigris sumatrae). From 2007–2009, seven landscapes were surveyed through 13,511 km of transects in 394 grid cells (17×17 km). Tiger sign was detected in 206 cells, producing a naive estimate of 0.52. However, after controlling for an unequal detection probability (where p = 0.13±0.017; ±S.E.), the estimated tiger occupancy was 0.72±0.048. Whilst the Sumatra-wide survey results gives cause for optimism, a significant negative correlation between occupancy and recent deforestation was found. For example, the Northern Riau landscape had an average deforestation rate of 9.8%/yr and by far the lowest occupancy (0.33±0.055). Our results highlight the key tiger areas in need of protection and have led to one area (Leuser-Ulu Masen) being upgraded as a ‘global priority’ for wild tiger conservation. However, Sumatra has one of the highest global deforestation rates and the two largest tiger landscapes identified in this study will become highly fragmented if their respective proposed roads networks are approved. Thus, it is vital that the Indonesian government tackles these threats, e.g. through improved land-use planning, if it is to succeed in meeting its ambitious National Tiger Recovery Plan targets of doubling the number of Sumatran tigers by 2022.
doi:10.1371/journal.pone.0025931
PMCID: PMC3206793  PMID: 22087218
3.  Influence of Connectivity, Wild Prey and Disturbance on Occupancy of Tigers in the Human-Dominated Western Terai Arc Landscape 
PLoS ONE  2012;7(7):e40105.
Occupying only 7% of their historical range and confined to forested habitats interspersed in a matrix of human dominated landscapes, tigers (Panthera tigris) typify the problems faced by most large carnivores worldwide. With heads of governments of tiger range countries pledging to reverse the extinction process and setting a goal of doubling wild tiger numbers by 2022, achieving this target would require identifying existing breeding cores, potential breeding habitats and opportunities for dispersal. The Terai Arc Landscape (TAL) represents one region which has recently witnessed recovery of tiger populations following conservation efforts. In this study, we develop a spatially explicit tiger occupancy model with survey data from 2009–10 based on a priori knowledge of tiger biology and specific issues plaguing the western TAL (6,979 km2), which occurs in two disjunct units (Tiger Habitat Blocks; THBs). Although the overall occupancy of tigers was 0.588 (SE 0.071), our results clearly indicate that loss in functionality of a regional corridor has resulted in tigers now occupying 17.58% of the available habitat in THB I in comparison to 88.5% in THB II. The current patterns of occupancy were best explained by models incorporating the interactive effect of habitat blocks (AIC w = 0.883) on wild prey availability (AIC w = 0.742) and anthropogenic disturbances (AIC w = 0.143). Our analysis has helped identify areas of high tiger occupancy both within and outside existing protected areas, which highlights the need for a unified control of the landscape under a single conservation unit with the primary focus of managing tigers and associated wildlife. Finally, in the light of global conservation targets and recent legislations in India, our study assumes significance as we identify opportunities to secure (e.g. THB II) and increase (e.g. THB I) tiger populations in the landscape.
doi:10.1371/journal.pone.0040105
PMCID: PMC3390357  PMID: 22792220
4.  Opportunities of Habitat Connectivity for Tiger (Panthera tigris) between Kanha and Pench National Parks in Madhya Pradesh, India 
PLoS ONE  2012;7(7):e39996.
The Tiger (Panthera tigris) population in India has undergone a sharp decline during the last few years. Of the number of factors attributed to this decline, habitat fragmentation has been the most worrisome. Wildlife corridors have long been a subject of discussion amongst wildlife biologists and conservationists with contrasting schools of thought arguing their merits and demerits. However, it is largely believed that wildlife corridors can help minimize genetic isolation, offset fragmentation problems, improve animal dispersal, restore ecological processes and reduce man animal conflict. This study attempted to evaluate the possibilities of identifying a suitable wildlife corridor between two very important wildlife areas of central India – the Kanha National Park and the Pench National Park – with tiger as the focal species. Geographic Information System (GIS) centric Least Cost Path modeling was used to identify likely routes for movement of tigers. Habitat suitability, perennial water bodies, road density, railway tracks, human settlement density and total forest edge were considered as key variables influencing tiger movement across the Kanha-Pench landscape. Each of these variables was weighted in terms of relative importance through an expert consultation process. Using different importance scenarios, three alternate corridor routes were generated of which one was identified as the most promising for tiger dispersal. Weak links – where cover and habitat conditions are currently sub-optimal – were flagged on the corridor route. Interventions aimed at augmenting the identified corridor route have been suggested using accepted wildlife corridor design principles. The involvement of local communities through initiatives such as ecotourism has been stressed as a crucial long term strategy for conservation of the Kanha-Pench wildlife corridor. The results of the study indicate that restoration of the identified wildlife corridors between the two protected areas is technically feasible.
doi:10.1371/journal.pone.0039996
PMCID: PMC3398000  PMID: 22815720
5.  Forest corridors maintain historical gene flow in a tiger metapopulation in the highlands of central India 
Understanding the patterns of gene flow of an endangered species metapopulation occupying a fragmented habitat is crucial for landscape-level conservation planning and devising effective conservation strategies. Tigers (Panthera tigris) are globally endangered and their populations are highly fragmented and exist in a few isolated metapopulations across their range. We used multi-locus genotypic data from 273 individual tigers (Panthera tigris tigris) from four tiger populations of the Satpura–Maikal landscape of central India to determine whether the corridors in this landscape are functional. This 45 000 km2 landscape contains 17% of India's tiger population and 12% of its tiger habitat. We applied Bayesian and coalescent-based analyses to estimate contemporary and historical gene flow among these populations and to infer their evolutionary history. We found that the tiger metapopulation in central India has high rates of historical and contemporary gene flow. The tests for population history reveal that tigers populated central India about 10 000 years ago. Their population subdivision began about 1000 years ago and accelerated about 200 years ago owing to habitat fragmentation, leading to four spatially separated populations. These four populations have been in migration–drift equilibrium maintained by high gene flow. We found the highest rates of contemporary gene flow in populations that are connected by forest corridors. This information is highly relevant to conservation practitioners and policy makers, because deforestation, road widening and mining are imminent threats to these corridors.
doi:10.1098/rspb.2013.1506
PMCID: PMC3735263  PMID: 23902910
Panthera tigris; central India; gene flow; connectivity; landscape genetics; non-invasive genetic analysis
6.  Phylogeography and Genetic Ancestry of Tigers (Panthera tigris) 
PLoS Biology  2004;2(12):e442.
Eight traditional subspecies of tiger (Panthera tigris), of which three recently became extinct, are commonly recognized on the basis of geographic isolation and morphological characteristics. To investigate the species' evolutionary history and to establish objective methods for subspecies recognition, voucher specimens of blood, skin, hair, and/or skin biopsies from 134 tigers with verified geographic origins or heritage across the whole distribution range were examined for three molecular markers: (1) 4.0 kb of mitochondrial DNA (mtDNA) sequence; (2) allele variation in the nuclear major histocompatibility complex class II DRB gene; and (3) composite nuclear microsatellite genotypes based on 30 loci. Relatively low genetic variation with mtDNA, DRB, and microsatellite loci was found, but significant population subdivision was nonetheless apparent among five living subspecies. In addition, a distinct partition of the Indochinese subspecies P. t. corbetti into northern Indochinese and Malayan Peninsula populations was discovered. Population genetic structure would suggest recognition of six taxonomic units or subspecies: (1) Amur tiger P. t. altaica; (2) northern Indochinese tiger P. t. corbetti; (3) South China tiger P. t. amoyensis; (4) Malayan tiger P. t. jacksoni, named for the tiger conservationist Peter Jackson; (5) Sumatran tiger P. t. sumatrae; and (6) Bengal tiger P. t. tigris. The proposed South China tiger lineage is tentative due to limited sampling. The age of the most recent common ancestor for tiger mtDNA was estimated to be 72,000–108,000 y, relatively younger than some other Panthera species. A combination of population expansions, reduced gene flow, and genetic drift following the last genetic diminution, and the recent anthropogenic range contraction, have led to the distinct genetic partitions. These results provide an explicit basis for subspecies recognition and will lead to the improved management and conservation of these recently isolated but distinct geographic populations of tigers.
Genetic analysis provides the basis for subspecies recognition among tigers, and will lead to improved conservation strategies for these endangered animals
doi:10.1371/journal.pbio.0020442
PMCID: PMC534810  PMID: 15583716
7.  Panel of polymorphic heterologous microsatellite loci to genotype critically endangered Bengal tiger: a pilot study 
SpringerPlus  2014;3:4.
In India, six landscapes and source populations that are important for long-term conservation of Bengal tigers (Panthera tigris tigris) have been identified. Except for a few studies, nothing is known regarding the genetic structure and extent of gene flow among most of the tiger populations across India as the majority of them are small, fragmented and isolated. Thus, individual-based relationships are required to understand the species ecology and biology for planning effective conservation and genetics-based individual identification has been widely used. But this needs screening and describing characteristics of microsatellite loci from DNA from good-quality sources so that the required number of loci can be selected and the genotyping error rate minimized. In the studies so far conducted on the Bengal tiger, a very small number of loci (n = 35) have been tested with high-quality source of DNA, and information on locus-specific characteristics is lacking. The use of such characteristics has been strongly recommended in the literature to minimize the error rate and by the International Society for Forensic Genetics (ISFG) for forensic purposes. Therefore, we describe for the first time locus-specific genetic and genotyping profile characteristics, crucial for population genetic studies, using high-quality source of DNA of the Bengal tiger. We screened 39 heterologous microsatellite loci (Sumatran tiger, domestic cat, Asiatic lion and snow leopard) in captive individuals (n = 8), of which 21 loci are being reported for the first time in the Bengal tiger, providing an additional choice for selection. The mean relatedness coefficient (R = −0.143) indicates that the selected tigers were unrelated. Thirty-four loci were polymorphic, with the number of alleles ranging from 2 to 7 per locus, and the remaining five loci were monomorphic. Based on the PIC values (> 0.500), and other characteristics, we suggest that 16 loci (3 to 7 alleles) be used for genetic and forensic study purposes. The probabilities of matching genotypes of unrelated individuals (3.692 × 10-19) and siblings (4.003 × 10-6) are within the values needed for undertaking studies in population genetics, relatedness, sociobiology and forensics.
doi:10.1186/2193-1801-3-4
PMCID: PMC3895153  PMID: 24455462
Bengal tiger; Panthera tigris tigris; Heterologous microsatellite loci; Genotyping panel
8.  Identifying Conservation Successes, Failures and Future Opportunities; Assessing Recovery Potential of Wild Ungulates and Tigers in Eastern Cambodia 
PLoS ONE  2012;7(10):e40482.
Conservation investment, particularly for charismatic and wide-ranging large mammal species, needs to be evidence-based. Despite the prevalence of this theme within the literature, examples of robust data being generated to guide conservation policy and funding decisions are rare. We present the first published case-study of tiger conservation in Indochina, from a site where an evidence-based approach has been implemented for this iconic predator and its prey. Despite the persistence of extensive areas of habitat, Indochina's tiger and ungulate prey populations are widely supposed to have precipitously declined in recent decades. The Seima Protection Forest (SPF), and broader Eastern Plains Landscape, was identified in 2000 as representing Cambodia's best hope for tiger recovery; reflected in its designation as a Global Priority Tiger Conservation Landscape. Since 2005 distance sampling, camera-trapping and detection-dog surveys have been employed to assess the recovery potential of ungulate and tiger populations in SPF. Our results show that while conservation efforts have ensured that small but regionally significant populations of larger ungulates persist, and density trends in smaller ungulates are stable, overall ungulate populations remain well below theoretical carrying capacity. Extensive field surveys failed to yield any evidence of tiger, and we contend that there is no longer a resident population within the SPF. This local extirpation is believed to be primarily attributable to two decades of intensive hunting; but importantly, prey densities are also currently below the level necessary to support a viable tiger population. Based on these results and similar findings from neighbouring sites, Eastern Cambodia does not currently constitute a Tiger Source Site nor meet the criteria of a Global Priority Tiger Landscape. However, SPF retains global importance for many other elements of biodiversity. It retains high regional importance for ungulate populations and potentially in the future for Indochinese tigers, given adequate prey and protection.
doi:10.1371/journal.pone.0040482
PMCID: PMC3471919  PMID: 23077476
9.  Apes in Space: Saving an Imperilled Orangutan Population in Sumatra 
PLoS ONE  2011;6(2):e17210.
Deforestation rates in Sumatra are amongst the highest in the tropics. Lowland forests, which support the highest densities of orangutans, are particularly vulnerable to clearance and fragmentation because they are highly accessible. Consequently, many orangutans will, in the future, live in strictly or partially isolated populations. Whilst orangutans have been extensively studied in primary forests, their response to living in human-dominated landscapes remains poorly known, despite it being essential for their future management. Here, we focus on an isolated group of critically endangered Sumatran orangutans (Pongo abelii) that co-exist with farmers in a mixed agroforest system consisting of degraded natural forest, smallholder (predominantly rubber) farms and oil palm plantations. Over 24 months we conducted the first ever spatial assessment of orangutan habitat use in the human-transformed landscape of Batang Serangan, North Sumatra. From 1,204 independent crop-raiding incidents recorded, orangutans showed strong foraging preference for mixed farmland/degraded forest habitat over oil palm patches. The core home range areas of the eight adult orangutans encompassed only 14% of the available study area. Monthly home range sizes averaged 423 ha (±139, SD) for males, and 131±46 ha for females, and were positively influenced by wild and cultivated fruit presence, and by crop consumption. The average daily distance travelled was similar for both adult males (868 m±350, SD) and females (866 m±195), but increased when orangutans raided crops. These findings show that orangutans can survive, demographically, in certain types of degraded landscapes, foraging on a mixture of crops and wild fruits. However, the poor quality habitat offered to orangutans by oil palm plantations, in terms of low food availability and as a barrier to female movements, is cause for concern since this is the land use type that is most rapidly replacing the preferred forest habitat across both Sumatran and Bornean orangutan ranges.
doi:10.1371/journal.pone.0017210
PMCID: PMC3040220  PMID: 21364732
10.  Canine Distemper Virus: an Emerging Disease in Wild Endangered Amur Tigers (Panthera tigris altaica) 
mBio  2013;4(4):e00410-13.
ABSTRACT
Fewer than 500 Amur tigers (Panthera tigris altaica) remain in the wild. Due to low numbers and their solitary and reclusive nature, tiger sightings across their range in the Russian Far East and China are rare; sightings of sick tigers are rarer still. Serious neurologic disease observed in several wild tigers since 2001 suggested disease emergence in this endangered species. To investigate this possibility, histology, immunohistochemistry (IHC), in situ hybridization (ISH), and reverse transcription-PCR (RT-PCR) were performed on tissues from 5 affected tigers that died or were destroyed in 2001, 2004, or 2010. Our results reveal canine distemper virus (CDV) infection as the cause of neurologic disease in two tigers and definitively establish infection in a third. Nonsuppurative encephalitis with demyelination, eosinophilic nuclear viral inclusions, and positive immunolabeling for CDV by IHC and ISH were present in the two tigers with available brain tissue. CDV phosphoprotein (P) and hemagglutinin (H) gene products were obtained from brains of these two tigers by RT-PCR, and a short fragment of CDV P gene sequence was detected in lymph node tissue of a third tiger. Phylogenetically, Amur tiger CDV groups with an Arctic-like strain in Baikal seals (Phoca siberica). Our results, which include mapping the location of positive tigers and recognition of a cluster of cases in 2010, coupled with a lack of reported CDV antibodies in Amur tigers prior to 2000 suggest wide geographic distribution of CDV across the tiger range and recent emergence of CDV as a significant infectious disease threat to endangered Amur tigers in the Russian Far East.
IMPORTANCE
Recognition of disease emergence in wildlife is a rare occurrence. Here, for the first time, we identify and characterize a canine distemper virus (CDV), the second most common cause of infectious disease death in domestic dogs and a viral disease of global importance in common and endangered carnivores, as the etiology of neurologic disease and fatal encephalitis in wild, endangered Amur tigers. We establish that in 2010 CDV directly or indirectly killed ~1% of Amur tigers. Location of positive cases over an expansive geographic area suggests that CDV is widely distributed across the tiger range. Interspecies interactions are increasing as human populations grow and expand into wildlife habitats. Identifying animal reservoirs for CDV and identifying the CDV strains that are transmissible to and among wildlife species, including Amur tigers and sympatric critically endangered Amur leopards (Panthera pardus orientalis), is essential for guiding conservation and mitigation efforts.
doi:10.1128/mBio.00410-13
PMCID: PMC3747579  PMID: 23943758
11.  Modelling the Species Distribution of Flat-Headed Cats (Prionailurus planiceps), an Endangered South-East Asian Small Felid 
PLoS ONE  2010;5(3):e9612.
Background
The flat-headed cat (Prionailurus planiceps) is one of the world's least known, highly threatened felids with a distribution restricted to tropical lowland rainforests in Peninsular Thailand/Malaysia, Borneo and Sumatra. Throughout its geographic range large-scale anthropogenic transformation processes, including the pollution of fresh-water river systems and landscape fragmentation, raise concerns regarding its conservation status. Despite an increasing number of camera-trapping field surveys for carnivores in South-East Asia during the past two decades, few of these studies recorded the flat-headed cat.
Methodology/Principal Findings
In this study, we designed a predictive species distribution model using the Maximum Entropy (MaxEnt) algorithm to reassess the potential current distribution and conservation status of the flat-headed cat. Eighty-eight independent species occurrence records were gathered from field surveys, literature records, and museum collections. These current and historical records were analysed in relation to bioclimatic variables (WorldClim), altitude (SRTM) and minimum distance to larger water resources (Digital Chart of the World). Distance to water was identified as the key predictor for the occurrence of flat-headed cats (>50% explanation). In addition, we used different land cover maps (GLC2000, GlobCover and SarVision LLC for Borneo), information on protected areas and regional human population density data to extract suitable habitats from the potential distribution predicted by the MaxEnt model. Between 54% and 68% of suitable habitat has already been converted to unsuitable land cover types (e.g. croplands, plantations), and only between 10% and 20% of suitable land cover is categorised as fully protected according to the IUCN criteria. The remaining habitats are highly fragmented and only a few larger forest patches remain.
Conclusion/Significance
Based on our findings, we recommend that future conservation efforts for the flat-headed cat should focus on the identified remaining key localities and be implemented through a continuous dialogue between local stakeholders, conservationists and scientists to ensure its long-term survival. The flat-headed cat can serve as a flagship species for the protection of several other endangered species associated with the threatened tropical lowland forests and surface fresh-water sources in this region.
doi:10.1371/journal.pone.0009612
PMCID: PMC2840020  PMID: 20305809
12.  Diversity patterns of ground beetles and understory vegetation in mature, secondary, and plantation forest regions of temperate northern China 
Ecology and Evolution  2015;5(3):531-542.
Plantation and secondary forests form increasingly important components of the global forest cover, but our current knowledge about their potential contribution to biodiversity conservation is limited. We surveyed understory plant and carabid species assemblages at three distinct regions in temperate northeastern China, dominated by mature forest (Changbaishan Nature Reserve, sampled in 2011 and 2012), secondary forest (Dongling Mountain, sampled in 2011 and 2012), and forest plantation habitats (Bashang Plateau, sampled in 2006 and 2007), respectively. The α-diversity of both taxonomic groups was highest in plantation forests of the Bashang Plateau. Beetle α-diversity was lowest, but plant and beetle species turnover peaked in the secondary forests of Dongling Mountain, while habitats in the Changbaishan Nature Reserve showed the lowest turnover rates for both taxa. Changbaishan Nature Reserve harbored the highest proportion of forest specialists. Our results suggest that in temperate regions of northern China, the protected larch plantation forest established over extensive areas might play a considerable role in maintaining a high biodiversity in relation to understory herbaceous plant species and carabid assemblages, which can be seen as indicators of forest disturbance. The high proportion of phytophagous carabids and the rarity of forest specialists reflect the relatively homogenous, immature status of the forest ecosystems on the Bashang Plateau. China's last remaining large old-growth forests like the ones on Changbaishan represent stable, mature ecosystems which require particular conservation attention.
doi:10.1002/ece3.1367
PMCID: PMC4328759  PMID: 25691978
α-Diversity; biodiversity conservation; carabids; herbaceous plants; mature forest; turnover
13.  Genetic Evidence of Tiger Population Structure and Migration within an Isolated and Fragmented Landscape in Northwest India 
PLoS ONE  2012;7(1):e29827.
Background
Majority of the tiger habitat in Indian subcontinent lies within high human density landscapes and is highly sensitive to surrounding pressures. These forests are unable to sustain healthy tiger populations within a tiger-hostile matrix, despite considerable conservation efforts. Ranthambore Tiger Reserve (RTR) in Northwest India is one such isolated forest which is rapidly losing its links with other tiger territories in the Central Indian landscape. Non-invasive genetic sampling for individual identification is a potent technique to understand the relationships between threatened tiger populations in degraded habitats. This study is an attempt to establish tiger movement across a fragmented landscape between RTR and its neighboring forests, Kuno-Palpur Wildlife Sanctuary (KPWLS) and Madhav National Park (MNP) based on non-invasively obtained genetic data.
Methods
Data from twelve microsatellite loci was used to define population structure and also to identify first generation migrants and admixed individuals in the above forests.
Results
Population structure was consistent with the Central Indian landscape and we could determine significant gene flow between RTR and MNP. We could identify individuals of admixed ancestry in both these forests, as well as first generation migrants from RTR to KPWLS and MNP.
Conclusions
Our results indicate reproductive mixing between animals of RTR and MNP in the recent past and migration of animals even today, despite fragmentation and poaching risk, from RTR towards MNP. Substantial conservation efforts should be made to maintain connectivity between these two subpopulations and also higher protection status should be conferred on Madhav National Park.
doi:10.1371/journal.pone.0029827
PMCID: PMC3256177  PMID: 22253791
14.  Mitochondrial Phylogeography Illuminates the Origin of the Extinct Caspian Tiger and Its Relationship to the Amur Tiger 
PLoS ONE  2009;4(1):e4125.
The Caspian tiger (Panthera tigris virgata) flourished in Central Asian riverine forest systems in a range disjunct from that of other tigers, but was driven to extinction in 1970 prior to a modern molecular evaluation. For over a century naturalists puzzled over the taxonomic validity, placement, and biogeographic origin of this enigmatic animal. Using ancient-DNA (aDNA) methodology, we generated composite mtDNA haplotypes from twenty wild Caspian tigers from throughout their historic range sampled from museum collections. We found that Caspian tigers carry a major mtDNA haplotype differing by only a single nucleotide from the monomorphic haplotype found across all contemporary Amur tigers (P. t. altaica). Phylogeographic analysis with extant tiger subspecies suggests that less than 10,000 years ago the Caspian/Amur tiger ancestor colonized Central Asia via the Gansu Corridor (Silk Road) from eastern China then subsequently traversed Siberia eastward to establish the Amur tiger in the Russian Far East. The conservation implications of these findings are far reaching, as the observed genetic depletion characteristic of modern Amur tigers likely reflects these founder migrations and therefore predates human influence. Also, due to their evolutionary propinquity, living Amur tigers offer an appropriate genetic source should reintroductions to the former range of the Caspian tiger be implemented.
doi:10.1371/journal.pone.0004125
PMCID: PMC2624500  PMID: 19142238
15.  Understanding the Impacts of Land-Use Policies on a Threatened Species: Is There a Future for the Bornean Orang-utan? 
PLoS ONE  2012;7(11):e49142.
The geographic distribution of Bornean orang-utans and its overlap with existing land-use categories (protected areas, logging and plantation concessions) is a necessary foundation to prioritize conservation planning. Based on an extensive orang-utan survey dataset and a number of environmental variables, we modelled an orang-utan distribution map. The modelled orang-utan distribution map covers 155,106 km2 (21% of Borneo's landmass) and reveals four distinct distribution areas. The most important environmental predictors are annual rainfall and land cover. The overlap of the orang-utan distribution with land-use categories reveals that only 22% of the distribution lies in protected areas, but that 29% lies in natural forest concessions. A further 19% and 6% occurs in largely undeveloped oil palm and tree plantation concessions, respectively. The remaining 24% of the orang-utan distribution range occurs outside of protected areas and outside of concessions. An estimated 49% of the orang-utan distribution will be lost if all forest outside of protected areas and logging concessions is lost. To avoid this potential decline plantation development in orang-utan habitats must be halted because it infringes on national laws of species protection. Further growth of the plantation sector should be achieved through increasing yields in existing plantations and expansion of new plantations into areas that have already been deforested. To reach this goal a large scale island-wide land-use masterplan is needed that clarifies which possible land uses and managements are allowed in the landscape and provides new standardized strategic conservation policies. Such a process should make much better use of non-market values of ecosystem services of forests such as water provision, flood control, carbon sequestration, and sources of livelihood for rural communities. Presently land use planning is more driven by vested interests and direct and immediate economic gains, rather than by approaches that take into consideration social equity and environmental sustainability.
doi:10.1371/journal.pone.0049142
PMCID: PMC3492325  PMID: 23145100
16.  Predicting Summer Site Occupancy for an Invasive Species, the Common Brushtail Possum (Trichosurus vulpecula), in an Urban Environment 
PLoS ONE  2013;8(3):e58422.
Invasive species are often favoured in fragmented, highly-modified, human-dominated landscapes such as urban areas. Because successful invasive urban adapters can occupy habitat that is quite different from that in their original range, effective management programmes for invasive species in urban areas require an understanding of distribution, habitat and resource requirements at a local scale that is tailored to the fine-scale heterogeneity typical of urban landscapes. The common brushtail possum (Trichosurus vulpecula) is one of New Zealand’s most destructive invasive pest species. As brushtail possums traditionally occupy forest habitat, control in New Zealand has focussed on rural and forest habitats, and forest fragments in cities. However, as successful urban adapters, possums may be occupying a wider range of habitats. Here we use site occupancy methods to determine the distribution of brushtail possums across five distinguishable urban habitat types during summer, which is when possums have the greatest impacts on breeding birds. We collected data on possum presence/absence and habitat characteristics, including possible sources of supplementary food (fruit trees, vegetable gardens, compost heaps), and the availability of forest fragments from 150 survey locations. Predictive distribution models constructed using the programme PRESENCE revealed that while occupancy rates were highest in forest fragments, possums were still present across a large proportion of residential habitat with occupancy decreasing as housing density increased and green cover decreased. The presence of supplementary food sources was important in predicting possum occupancy, which may reflect the high nutritional value of these food types. Additionally, occupancy decreased as the proportion of forest fragment decreased, indicating the importance of forest fragments in determining possum distribution. Control operations to protect native birds from possum predation in cities should include well-vegetated residential areas; these modified habitats not only support possums but provide a source for reinvasion of fragments.
doi:10.1371/journal.pone.0058422
PMCID: PMC3587593  PMID: 23469277
17.  Tigers of Sundarbans in India: Is the Population a Separate Conservation Unit? 
PLoS ONE  2015;10(4):e0118846.
The Sundarbans tiger inhabits a unique mangrove habitat and are morphologically distinct from the recognized tiger subspecies in terms of skull morphometrics and body size. Thus, there is an urgent need to assess their ecological and genetic distinctiveness and determine if Sundarbans tigers should be defined and managed as separate conservation unit. We utilized nine microsatellites and 3 kb from four mitochondrial DNA (mtDNA) genes to estimate genetic variability, population structure, demographic parameters and visualize historic and contemporary connectivity among tiger populations from Sundarbans and mainland India. We also evaluated the traits that determine exchangeability or adaptive differences among tiger populations. Data from both markers suggest that Sundarbans tiger is not a separate tiger subspecies and should be regarded as Bengal tiger (P. t. tigris) subspecies. Maximum likelihood phylogenetic analyses of the mtDNA data revealed reciprocal monophyly. Genetic differentiation was found stronger for mtDNA than nuclear DNA. Microsatellite markers indicated low genetic variation in Sundarbans tigers (He= 0.58) as compared to other mainland populations, such as northern and Peninsular (Hebetween 0.67- 0.70). Molecular data supports migration between mainland and Sundarbans populations until very recent times. We attribute this reduction in gene flow to accelerated fragmentation and habitat alteration in the landscape over the past few centuries. Demographic analyses suggest that Sundarbans tigers have diverged recently from peninsular tiger population within last 2000 years. Sundarbans tigers are the most divergent group of Bengal tigers, and ecologically non-exchangeable with other tiger populations, and thus should be managed as a separate “evolutionarily significant unit” (ESU) following the adaptive evolutionary conservation (AEC) concept.
doi:10.1371/journal.pone.0118846
PMCID: PMC4412631  PMID: 25919139
18.  Why the Indian Subcontinent Holds the Key to Global Tiger Recovery 
PLoS Genetics  2009;5(8):e1000585.
With only ∼3,000 wild individuals surviving restricted to just 7% of their historical range, tigers are now a globally threatened species. Therefore, conservation efforts must prioritize regions that harbor more tigers, as well try to capture most of the remaining genetic variation and habitat diversity. Only such prioritization based on demographic, genetic, and ecological considerations can ensure species recovery and retention of evolutionary flexibility in the face of ongoing global changes. Although scientific understanding of ecological and demographic aspects of extant wild tiger populations has improved recently, little is known about their genetic composition and variability. We sampled 73 individual tigers from 28 reserves spread across a diversity of habitats in the Indian subcontinent to obtain 1,263 bp of mitochondrial DNA and 10 microsatellite loci. Our analyses reveals that Indian tigers retain more than half of the extant genetic diversity in the species. Coalescent simulations attribute this high genetic diversity to a historically large population size of about 58,200 tigers for peninsular India south of the Gangetic plains. Furthermore, our analyses indicate a precipitous, possibly human-induced population crash ∼200 years ago in India, which is in concordance with historical records. Our results suggest that only 1.7% (with an upper limit of 13% and a lower limit of 0.2%) of tiger numbers in historical times remain now. In the global conservation context our results suggest that, based on genetic, demographic, and ecological considerations, the Indian subcontinent holds the key to global survival and recovery of wild tigers.
Author Summary
Tiger range and numbers have collapsed globally despite substantial conservation efforts. Genetic data quantifying variation from 73 wild tigers in 28 reserves in the Indian subcontinent suggests historically high numbers for tigers, and simulations reveal a signature of a 200-year-old, possibly human-induced decline. Simulations suggest that only 1.7% of historical tiger numbers now persist in peninsular Indian. Our data also reveal that tigers of the Indian subcontinent retain most of the species' genetic diversity, besides this region harbouring maximum diversity of tiger habitats. Overall, the Indian subcontinent appears to be a global hotspot holding the key to any future recovery of wild tigers from both an ecological and genetic perspective.
doi:10.1371/journal.pgen.1000585
PMCID: PMC2716534  PMID: 19680439
19.  Depauperate Avifauna in Plantations Compared to Forests and Exurban Areas 
PLoS ONE  2006;1(1):e63.
Native forests are shrinking worldwide, causing a loss of biological diversity. Our ability to prioritize forest conservation actions is hampered by a lack of information about the relative impacts of different types of forest loss on biodiversity. In particular, we lack rigorous comparisons of the effects of clearing forests for tree plantations and for human settlements, two leading causes of deforestation worldwide. We compared avian diversity in forests, plantations and exurban areas on the Cumberland Plateau, USA, an area of global importance for biodiversity. By combining field surveys with digital habitat databases, and then analyzing diversity at multiple scales, we found that plantations had lower diversity and fewer conservation priority species than did other habitats. Exurban areas had higher diversity than did native forests, but native forests outscored exurban areas for some measures of conservation priority. Overall therefore, pine plantations had impoverished avian communities relative to both native forests and to exurban areas. Thus, reports on the status of forests give misleading signals about biological diversity when they include plantations in their estimates of forest cover but exclude forested areas in which humans live. Likewise, forest conservation programs should downgrade incentives for plantations and should include settled areas within their purview.
doi:10.1371/journal.pone.0000063
PMCID: PMC1762314  PMID: 17183694
20.  Modelling Spatial and Temporal Forest Cover Change Patterns (1973-2020): A Case Study from South Western Ghats (India) 
Sensors (Basel, Switzerland)  2008;8(10):6132-6153.
This study used time series remote sensing data from 1973, 1990 and 2004 to assess spatial forest cover change patterns in the Kalakad-Mundanthurai Tiger Reserve (KMTR), South Western Ghats (India). Analysis of forest cover changes and its causes are the most challenging areas of landscape ecology, especially due to the absence of temporal ground data and comparable space platform based data. Comparing remotely sensed data from three different sources with sensors having different spatial and spectral resolution presented a technical challenge. Quantitative change analysis over a long period provided a valuable insight into forest cover dynamics in this area. Time-series maps were combined within a geographical information system (GIS) with biotic and abiotic factors for modelling its future change. The land-cover change has been modelled using GEOMOD and predicted for year 2020 using the current disturbance scenario. Comparison of the forest change maps over the 31-year period shows that evergreen forest being degraded (16%) primarily in the form of selective logging and clear felling to raise plantations of coffee, tea and cardamom. The natural disturbances such as forest fire, wildlife grazing, invasions after clearance and soil erosion induced by anthropogenic pressure over the decades are the reasons of forest cover change in KMTR. The study demonstrates the role of remote sensing and GIS in monitoring of large-coverage of forest area continuously for a given region over time more precisely and in cost-effective manner which will be ideal for conservation planning and prioritization.
doi:10.3390/s8106132
PMCID: PMC3707442
Forest cover change; tropical forest; GEOMOD; monitoring; Western Ghats
21.  Impact of Logging and Forest Conversion to Oil Palm Plantations on Soil Bacterial Communities in Borneo 
Applied and Environmental Microbiology  2013;79(23):7290-7297.
Tropical forests are being rapidly altered by logging and cleared for agriculture. Understanding the effects of these land use changes on soil bacteria, which constitute a large proportion of total biodiversity and perform important ecosystem functions, is a major conservation frontier. Here we studied the effects of logging history and forest conversion to oil palm plantations in Sabah, Borneo, on the soil bacterial community. We used paired-end Illumina sequencing of the 16S rRNA gene, V3 region, to compare the bacterial communities in primary, once-logged, and twice-logged forest and land converted to oil palm plantations. Bacteria were grouped into operational taxonomic units (OTUs) at the 97% similarity level, and OTU richness and local-scale α-diversity showed no difference between the various forest types and oil palm plantations. Focusing on the turnover of bacteria across space, true β-diversity was higher in oil palm plantation soil than in forest soil, whereas community dissimilarity-based metrics of β-diversity were only marginally different between habitats, suggesting that at large scales, oil palm plantation soil could have higher overall γ-diversity than forest soil, driven by a slightly more heterogeneous community across space. Clearance of primary and logged forest for oil palm plantations did, however, significantly impact the composition of soil bacterial communities, reflecting in part the loss of some forest bacteria, whereas primary and logged forests did not differ in composition. Overall, our results suggest that the soil bacteria of tropical forest are to some extent resilient or resistant to logging but that the impacts of forest conversion to oil palm plantations are more severe.
doi:10.1128/AEM.02541-13
PMCID: PMC3837752  PMID: 24056463
22.  Slipping through the Cracks: Rubber Plantation Is Unsuitable Breeding Habitat for Frogs in Xishuangbanna, China 
PLoS ONE  2013;8(9):e73688.
Conversion of tropical forests into agriculture may present a serious risk to amphibian diversity if amphibians are not able to use agricultural areas as habitat. Recently, in Xishuangbanna Prefecture, Yunnan Province – a hotspot of frog diversity within China – two-thirds of the native tropical rainforests have been converted into rubber plantation agriculture. We conducted surveys and experiments to quantify habitat use for breeding and non-breeding life history activities of the native frog species in rainforest, rubber plantation and other human impacted sites. Rubber plantation sites had the lowest species richness in our non-breeding habitat surveys and no species used rubber plantation sites as breeding habitat. The absence of breeding was likely not due to intrinsic properties of the rubber plantation pools, as our experiments indicated that rubber plantation pools were suitable for tadpole growth and development. Rather, the absence of breeding in the rubber plantation was likely due to a misalignment of breeding and non-breeding habitat preferences. Analyses of our breeding surveys showed that percent canopy cover over pools was the strongest environmental variable influencing breeding site selection, with species exhibiting preferences for pools under both high and low canopy cover. Although rubber plantation pools had high canopy cover, the only species that bred in high canopy cover sites used the rainforest for both non-breeding and breeding activities, completing their entire life cycle in the rainforest. Conversely, the species that did use the rubber plantation for non-breeding habitat preferred to breed in low canopy sites, also avoiding breeding in the rubber plantation. Rubber plantations are likely an intermediate habitat type that ‘slips through the cracks’ of species habitat preferences and is thus avoided for breeding. In summary, unlike the rainforests they replaced, rubber plantations alone may not be able to support frog populations.
doi:10.1371/journal.pone.0073688
PMCID: PMC3769397  PMID: 24040026
23.  Philopatry and Dispersal Patterns in Tiger (Panthera tigris) 
PLoS ONE  2013;8(7):e66956.
Background
Tiger populations are dwindling rapidly making it increasingly difficult to study their dispersal and mating behaviour in the wild, more so tiger being a secretive and solitary carnivore.
Methods
We used non-invasively obtained genetic data to establish the presence of 28 tigers, 22 females and 6 males, within the core area of Pench tiger reserve, Madhya Pradesh. This data was evaluated along with spatial autocorrelation and relatedness analyses to understand patterns of dispersal and philopatry in tigers within this well-managed and healthy tiger habitat in India.
Results
We established male-biased dispersal and female philopatry in tigers and reiterated this finding with multiple analyses. Females show positive correlation up to 7 kms (which corresponds to an area of approximately 160 km2) however this correlation is significantly positive only upto 4 kms, or 50 km2 (r  = 0.129, p<0.0125). Males do not exhibit any significant correlation in any of the distance classes within the forest (upto 300 km2). We also show evidence of female dispersal upto 26 kms in this landscape.
Conclusions
Animal movements are important for fitness, reproductive success, genetic diversity and gene exchange among populations. In light of the current endangered status of tigers in the world, this study will help us understand tiger behavior and movement. Our findings also have important implications for better management of habitats and interconnecting corridors to save this charismatic species.
doi:10.1371/journal.pone.0066956
PMCID: PMC3699573  PMID: 23843973
24.  Landscape-scale accessibility of livestock to tigers: implications of spatial grain for modeling predation risk to mitigate human–carnivore conflict 
Ecology and Evolution  2015;5(6):1354-1367.
Innovative conservation tools are greatly needed to reduce livelihood losses and wildlife declines resulting from human–carnivore conflict. Spatial risk modeling is an emerging method for assessing the spatial patterns of predator–prey interactions, with applications for mitigating carnivore attacks on livestock. Large carnivores that ambush prey attack and kill over small areas, requiring models at fine spatial grains to predict livestock depredation hot spots. To detect the best resolution for predicting where carnivores access livestock, we examined the spatial attributes associated with livestock killed by tigers in Kanha Tiger Reserve, India, using risk models generated at 20, 100, and 200-m spatial grains. We analyzed land-use, human presence, and vegetation structure variables at 138 kill sites and 439 random sites to identify key landscape attributes where livestock were vulnerable to tigers. Land-use and human presence variables contributed strongly to predation risk models, with most variables showing high relative importance (≥0.85) at all spatial grains. The risk of a tiger killing livestock increased near dense forests and near the boundary of the park core zone where human presence is restricted. Risk was nonlinearly related to human infrastructure and open vegetation, with the greatest risk occurring 1.2 km from roads, 1.1 km from villages, and 8.0 km from scrubland. Kill sites were characterized by denser, patchier, and more complex vegetation with lower visibility than random sites. Risk maps revealed high-risk hot spots inside of the core zone boundary and in several patches in the human-dominated buffer zone. Validation against known kills revealed predictive accuracy for only the 20 m model, the resolution best representing the kill stage of hunting for large carnivores that ambush prey, like the tiger. Results demonstrate that risk models developed at fine spatial grains can offer accurate guidance on landscape attributes livestock should avoid to minimize human–carnivore conflict.
doi:10.1002/ece3.1440
PMCID: PMC4377277  PMID: 25859339
Carnivore conservation; human–wildlife conflict; India; livestock depredation; predation risk modeling; resource selection function
25.  Poor Prospects for Avian Biodiversity in Amazonian Oil Palm 
PLoS ONE  2015;10(5):e0122432.
Expansion of oil palm plantations across the humid tropics has precipitated massive loss of tropical forest habitats and their associated speciose biotas. Oil palm plantation monocultures have been identified as an emerging threat to Amazonian biodiversity, but there are no quantitative studies exploring the impact of these plantations on the biome’s biota. Understanding these impacts is extremely important given the rapid projected expansion of oil palm cultivation in the basin. Here we investigate the biodiversity value of oil palm plantations in comparison with other dominant regional land-uses in Eastern Amazonia. We carried out bird surveys in oil palm plantations of varying ages, primary and secondary forests, and cattle pastures. We found that oil palm plantations retained impoverished avian communities with a similar species composition to pastures and agrarian land-uses and did not offer habitat for most forest-associated species, including restricted range species and species of conservation concern. On the other hand, the forests that the oil palm companies are legally obliged to protect hosted a relatively species-rich community including several globally-threatened bird species. We consider oil palm to be no less detrimental to regional biodiversity than other agricultural land-uses and that political pressure exerted by large landowners to allow oil palm to count as a substitute for native forest vegetation in private landholdings with forest restoration deficits would have dire consequences for regional biodiversity.
doi:10.1371/journal.pone.0122432
PMCID: PMC4425670  PMID: 25955243

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