Living on the edge: Opportunities for Amur tiger recovery in China

Abstract Sporadic sightings of the endangered Amur tiger Panthera tigris altaica along the China-Russia border during the late 1990s sparked efforts to expand this subspecies distribution and abundance by restoring potentially suitable habitats in the Changbai Mountains. To guide science-based recovery efforts and provide a baseline for future monitoring of this border population, empirical, quantitative information is needed on what resources and management practices promote or limit the occurrence of tigers in the region. We established a large-scale field camera-trapping network to estimate tiger density, survival and recruitment in the Hunchun Nature Reserve and the surrounding area using an open population spatially explicit capture-recapture model. We then fitted an occupancy model that accounted for detectability and spatial autocorrelation to assess the relative influence of habitat, major prey, disturbance and management on tiger habitat use patterns. Our results show that the ranges of most tigers abut the border with Russia. Tiger densities ranged between 0.20 and 0.27 individuals/100 km2 over the study area; in the Hunchun Nature Reserve, the tiger density was three times higher than that in the surrounding inland forested area. Tiger occupancy was strongly negatively related to heavy cattle grazing, human settlements and roads and was positively associated with sika deer abundance and vegetation cover. These findings can help to identify the drivers of tiger declines and dispersal limits and refine strategies for tiger conservation in the human-dominated transboundary landscape. Progressively alleviating the impacts of cattle and human disturbances on the forest, and simultaneously addressing the economic needs of local communities, should be key priority actions to increase tiger populations. The long-term goal is to expand tiger distribution by improving habitats for large ungulates.

[1]  D. Macmillan,et al.  Identifying realistic recovery targets and conservation actions for tigers in a human‐dominated landscape using spatially explicit densities of wild prey and their determinants , 2014 .

[2]  Murray G Efford,et al.  Population density estimated from locations of individuals on a passive detector array. , 2009, Ecology.

[3]  Qamar Qureshi,et al.  Evaluating the status of the Endangered tiger Panthera tigris and its prey in Panna Tiger Reserve, Madhya Pradesh, India , 2010, Oryx.

[4]  Clare Duncan,et al.  How do we want Satellite Remote Sensing to support biodiversity conservation globally? , 2016 .

[5]  Olivier Gimenez,et al.  Wildlife in a Politically Divided World: Insularism Inflates Estimates of Brown Bear Abundance , 2016 .

[6]  Sheng Li,et al.  Shared resources between giant panda and sympatric wild and domestic mammals , 2015 .

[7]  N. Leader‐Williams,et al.  Assessing the viability of tiger subpopulations in a fragmented landscape , 2006 .

[8]  Philippe De Maeyer,et al.  Application of the topographic position index to heterogeneous landscapes , 2013 .

[9]  G. Jolly.  EXPLICIT ESTIMATES FROM CAPTURE-RECAPTURE DATA WITH BOTH DEATH AND IMMIGRATION-STOCHASTIC MODEL. , 1965, Biometrika.

[10]  Kathleen Mclaughlin.  Tiger land. , 2016, Science.

[11]  U. Ramakrishnan,et al.  Connectivity of Tiger (Panthera tigris) Populations in the Human-Influenced Forest Mosaic of Central India , 2013, PloS one.

[12]  Carlos Carroll,et al.  Chapter 32 – Science-Based Conservation of Amur Tigers in the Russian Far East and Northeast China , 2010 .

[13]  T. McDonald,et al.  Survival rates and causes of mortality of Amur tigers on and near the Sikhote‐Alin Biosphere Zapovednik , 2008 .

[14]  Tong Liu,et al.  Human-carnivore conflict in China: a review of current approaches with recommendations for improved management. , 2012, Integrative zoology.

[15]  James L. D. Smith,et al.  Landscape Analysis of Tiger Distribution and Habitat Quality in Nepal , 1998 .

[16]  J. Andrew Royle,et al.  Spatial capture–recapture models allowing Markovian transience or dispersal , 2015, Population Ecology.

[17]  S. Naidenko,et al.  Genetic structure of the Amur tiger (Panthera tigris altaica) population: Are tigers in Sikhote-Alin and southwest Primorye truly isolated? , 2016, Integrative zoology.

[18]  Tianming Wang,et al.  Estimating the Population Size and Genetic Diversity of Amur Tigers in Northeast China , 2016, PloS one.

[19]  G. Seber.  A NOTE ON THE MULTIPLE-RECAPTURE CENSUS. , 1965, Biometrika.

[20]  Yu Tian,et al.  Amur tigers and leopards returning to China: direct evidence and a landscape conservation plan , 2016, Landscape Ecology.

[21]  K. U. Karanth,et al.  A tiger cannot change its stripes: using a three-dimensional model to match images of living tigers and tiger skins , 2009, Biology Letters.

[22]  K. U. Karanth,et al.  Dynamics of a low‐density tiger population in Southeast Asia in the context of improved law enforcement , 2016, Conservation biology : the journal of the Society for Conservation Biology.

[23]  Mevin B. Hooten,et al.  Spatial occupancy models for large data sets , 2013 .

[24]  J. M. Sappington,et al.  Quantifying Landscape Ruggedness for Animal Habitat Analysis: A Case Study Using Bighorn Sheep in the Mojave Desert , 2007 .

[25]  John M. Goodrich,et al.  Effects of Roads and Human Disturbance on Amur Tigers , 2002, Conservation biology : the journal of the Society for Conservation Biology.

[26]  Res Altwegg,et al.  Spatial occupancy models applied to atlas data show Southern Ground Hornbills strongly depend on protected areas. , 2014, Ecological applications : a publication of the Ecological Society of America.

[27]  Todd W. Arnold.  Uninformative Parameters and Model Selection Using Akaike's Information Criterion , 2010 .

[28]  Spatially explicit capture-recapture method (SECR, SPACECAP): A new approach to determination of the Amur tiger (Panthera tigris altaica) population density by means of camera-traps , 2013, Doklady Biological Sciences.

[29]  John Geweke,et al.  Evaluating the accuracy of sampling-based approaches to the calculation of posterior moments , 1991 .

[30]  J Andrew Royle,et al.  Spatially explicit inference for open populations: estimating demographic parameters from camera-trap studies. , 2010, Ecology.

[31]  John Power,et al.  Cats, connectivity and conservation: incorporating data sets and integrating scales for wildlife management , 2017 .

[32]  Richard Schuster,et al.  Using bird species community occurrence to prioritize forests for old growth restoration , 2013 .

[33]  J. Nichols,et al.  ESTIMATION OF TIGER DENSITIES IN INDIA USING PHOTOGRAPHIC CAPTURES AND RECAPTURES , 1998 .

[34]  Matthew C. Hansen,et al.  Tracking changes and preventing loss in critical tiger habitat , 2016, Science Advances.

[35]  Darryl I. MacKenzie,et al.  Designing occupancy studies: general advice and allocating survey effort , 2005 .

[36]  M. Linkie,et al.  Estimating overlap of daily activity patterns from camera trap data , 2009 .

[37]  B. Bhattarai,et al.  Effect of human disturbance on the prey of tiger in the Chitwan National Park--implications for park management. , 2013, Journal of environmental management.

[38]  Richard B. Chandler,et al.  unmarked: An R Package for Fitting Hierarchical Models of Wildlife Occurrence and Abundance , 2011 .

[39]  J. Nichols,et al.  Tigers and their prey: Predicting carnivore densities from prey abundance. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[40]  D. Macdonald,et al.  Spatial variation in the density and vulnerability of preferred prey in the landscape shape patterns of Amur tiger habitat use , 2016 .

[41]  A. S. Mukhacheva,et al.  A comparison of food habits and prey preference of Amur tiger (Panthera tigris altaica) at three sites in the Russian Far East. , 2015, Integrative zoology.

[42]  Jianguo Wu,et al.  Population viability of the Siberian Tiger in a changing landscape: Going, going and gone? , 2011 .

[43]  S. Goyal,et al.  Responses of tiger (Panthera tigris) and their prey to removal of anthropogenic influences in Rajaji National Park, India , 2009, European Journal of Wildlife Research.

[44]  Wenhong Xiao,et al.  A science-based approach to guide Amur leopard recovery in China , 2017 .

[45]  Margaret F. Kinnaird,et al.  Crouching tigers, hidden prey: Sumatran tiger and prey populations in a tropical forest landscape , 2003 .

[46]  Siberian tiger's recent population bottleneck in the Russian Far East revealed by microsatellite markers , 2011 .

[47]  Alan E. Gelfand,et al.  Model choice: A minimum posterior predictive loss approach , 1998, AISTATS.

[48]  James L. D. Smith,et al.  Phylogeography and Genetic Ancestry of Tigers (Panthera tigris) , 2004, PLoS biology.

[49]  Wu Jianguo,et al.  Spatiotemporal pattern and major causes of the Amur tiger population dynamics , 2009 .

[50]  J. Andrew Royle,et al.  ESTIMATING SITE OCCUPANCY RATES WHEN DETECTION PROBABILITIES ARE LESS THAN ONE , 2002, Ecology.

[51]  M. Efford.  Density estimation in live‐trapping studies , 2004 .

[52]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[53]  Xiao-Li Meng,et al.  POSTERIOR PREDICTIVE ASSESSMENT OF MODEL FITNESS VIA REALIZED DISCREPANCIES , 1996 .

[54]  J. Andrew Royle,et al.  Parameter-expanded data augmentation for Bayesian analysis of capture–recapture models , 2010, Journal of Ornithology.

[55]  M. Linkie,et al.  Conserving tigers in Malaysia: A science-driven approach for eliciting conservation policy change , 2015 .

[56]  D. McCullough,et al.  In situ population structure and ex situ representation of the endangered Amur tiger , 2009, Molecular ecology.

[57]  E. Wikramanayake,et al.  Influence of prey depletion and human disturbance on tiger occupancy in Nepal , 2013 .

[58]  S. Goyal,et al.  Responses of leopard Panthera pardus to the recovery of a tiger Panthera tigris population , 2011 .

[59]  S. Wieren,et al.  A theoretical analysis of competitive exclusion in a Trans‐Himalayan large‐herbivore assemblage , 2002 .

[60]  David R. Anderson,et al.  Model Selection and Multimodel Inference , 2003 .

[61]  Chittaranjan Dave,et al.  Is competition with livestock detrimental for native wild ungulates? A case study of chital (Axis axis) in Gir Forest, India , 2011, Journal of Tropical Ecology.

[62]  L. L. Bailey,et al.  Conserving tigers in working landscapes , 2016, Conservation biology : the journal of the Society for Conservation Biology.

[63]  E. Wikramanayake,et al.  The Fate of Wild Tigers , 2007 .

[64]  C. Hojnowski,et al.  Why do Amur tigers maintain exclusive home ranges? Relating ungulate seasonal movements to tiger spatial organization in the Russian Far East , 2012 .

[65]  M. Hebblewhite,et al.  Estimating abundance and density of Amur tigers along the Sino-Russian border. , 2016, Integrative zoology.

[66]  Zhao Xiaodan,et al.  Distribution and abundance of Amur tiger, Amur leopard and their un- gulate prey in Hunchun National Nature Reserve, Jilin , 2014 .

[67]  James L. D. Smith,et al.  How much gene flow is needed to avoid inbreeding depression in wild tiger populations? , 2014, Proceedings of the Royal Society B: Biological Sciences.

[68]  J Andrew Royle,et al.  Bayesian inference in camera trapping studies for a class of spatial capture-recapture models. , 2009, Ecology.

[69]  D. G. Pikunov,et al.  Including biotic interactions with ungulate prey and humans improves habitat conservation modeling for endangered Amur tigers in the Russian Far East , 2014 .

[70]  Kathy MacKinnon,et al.  Bringing the Tiger Back from the Brink—The Six Percent Solution , 2010, PLoS biology.

[71]  Andrew Gelman,et al.  General methods for monitoring convergence of iterative simulations , 1998 .

[72]  L. Boitani,et al.  Border Security Fencing and Wildlife: The End of the Transboundary Paradigm in Eurasia? , 2016, PLoS biology.

[73]  S. Cleaveland,et al.  Canine distemper virus as a threat to wild tigers in Russia and across their range. , 2015, Integrative zoology.

[74]  Jianguo Liu,et al.  Coexistence between wildlife and humans at fine spatial scales , 2012, Proceedings of the National Academy of Sciences.

[75]  M. D. Madhusudan,et al.  Recovery of wild large herbivores following livestock decline in a tropical Indian wildlife reserve , 2004 .

[76]  Murali Haran,et al.  Dimension reduction and alleviation of confounding for spatial generalized linear mixed models , 2010, 1011.6649.

[77]  Hua-Ru Wang,et al.  [Variation trends of the vegetations in distribution region of Amur tiger based on MODIS NDVI]. , 2012, Ying yong sheng tai xue bao = The journal of applied ecology.

[78]  M. Hebblewhite,et al.  Is there a future for Amur tigers in a restored tiger conservation landscape in Northeast China? , 2012 .

[79]  Robert C. Fleischer,et al.  Prioritizing Tiger Conservation through Landscape Genetics and Habitat Linkages , 2014, PloS one.

[80]  D. Miquelle,et al.  Identifying ecological corridors for Amur tigers (Panthera tigris altaica) and Amur leopards (Panthera pardus orientalis). , 2015, Integrative zoology.

[81]  Tianming Wang,et al.  Camera traps reveal Amur tiger breeding in NE China , 2014 .

[82]  Yu Tian,et al.  [Land use pattern and its dynamic changes in Amur tiger distribution region]. , 1983, Ying yong sheng tai xue bao = The journal of applied ecology.

[83]  Zhongbao Liu.  Livestock depredation by Amur tigers in Hunchun Nature Reserve,Jilin,China , 2009 .

[84]  James L. D. Smith,et al.  Long-distance dispersal of an Amur tiger indicates potential to restore the North-east China/Russian Tiger Landscape , 2015, Oryx.

[85]  S. Naidenko,et al.  Social structure and space use of Amur tigers (Panthera tigris altaica) in Southern Russian Far East based on GPS telemetry data. , 2015, Integrative zoology.

[86]  C. Carroll,et al.  Spatial viability analysis of Amur tiger Panthera tigris altaica in the Russian Far East: the role of protected areas and landscape matrix in population persistence , 2006 .

[87]  T. Wiegand,et al.  Assessing habitat suitability for tiger in the fragmented Terai Arc Landscape of India and Nepal , 2011 .

[88]  Luis Roman Carrasco,et al.  Spatial correlates of livestock depredation by Amur tigers in Hunchun, China: Relevance of prey density and implications for protected area management , 2014, Biological Conservation.

[89]  James L. D. Smith,et al.  Temporal Variation in Tiger (Panthera tigris) Populations and Its Implications for Monitoring , 2009 .