Anthropogenic pressures increase extinction risk of an isolated Asian elephant (Elephas maximus) population in southwestern China, as revealed by a combination of molecular- and landscape-scale approaches.
fragmentation
inbreeding
isolation
land-use change
population viability
Journal
Integrative zoology
ISSN: 1749-4877
Titre abrégé: Integr Zool
Pays: Australia
ID NLM: 101492420
Informations de publication
Date de publication:
Nov 2022
Nov 2022
Historique:
pubmed:
18
3
2021
medline:
15
11
2022
entrez:
17
3
2021
Statut:
ppublish
Résumé
Identification of the effect of anthropogenic threats on ecosystem is crucial. We used molecular tools and remote sensing to evaluate the population status of an isolated Asian elephant population in southwestern China in response to changes in habitat suitability between 1989 and 2019. A total of 22 unique genotypes were identified from 117 dung samples collected between March and June 2018 using microsatellite DNA analysis, including 13 males and 9 females. Based on the size of fecal boli, 1 animal was a juvenile, 9 were subadults, and 12 were adults, indicating that recruitment was limited. The effective population size was small (15.3) but there was no signature of a recent population bottleneck. We observed a low genetic diversity (H
Identifiants
pubmed: 33728791
doi: 10.1111/1749-4877.12534
doi:
Substances chimiques
Rubber
9006-04-6
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1078-1094Subventions
Organisme : Second national survey of terrestrial wildlife project, National Forestry and Grassland Administration of China
ID : 20080131
Informations de copyright
© 2021 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.
Références
Ahlering MA, Hailer F, Roberts MT et al. (2011a). A simple and accurate method to sex savannah, forest and asian elephants using noninvasive sampling techniques. Molecular Ecology Resources 11, 831-4.
Ahlering MA, Hedges S, Johnson A et al. (2011b). Genetic diversity, social structure, and conservation value of the elephants of the Nakai Plateau, Lao PDR, based on non-invasive sampling. Conservation Genetics 12, 413-22.
Alfred R, Ahmad AH, Payne J et al. (2012). Home range and ranging behaviour of Bornean elephant (Elephas maximus borneensis) females. PLoS ONE 7, e31400.
Atzeni L, Cushman S, Bai D et al. (2020). Meta-replication, sampling bias and multi-scale model selection: A case study on snow leopard (Panthera uncia) in western China. Ecology and Evolution 10, 7686-712.
Bastian M, Heymann S, Jacomy M, eds (2009). Gephi: an open source software for exploring and manipulating networks. International AAAI Conference on Weblogs and Social Media, 17-20 May 2009, San Jose, California.
Bohnett E, Riordan P, Kun S (2015). Initial assessment on large and medium sized terrestrial mammal assemblage using camera trapping in Nangunhe Nature Reserve in Yunnan, China. Journal of Resources and Ecology 6, 331-45.
Bourgeois S, Kaden J, Senn H et al. (2019). Improving cost-efficiency of faecal genotyping: New tools for elephant species. PLoS ONE 14, e0210811.
Bryant J, Gottelli D, Zeng X et al. (2016). Assessing current genetic status of the Hainan gibbon using historical and demographic baselines: Implications for conservation management of species of extreme rarity. Molecular Ecology 25, 3540-56.
Campos-Arceiz A, Blake S (2011). Megagardeners of the forest - the role of elephants in seed dispersal. Acta Oecologica 37, 542-53.
Chakraborty S, Boominathan D, Desai AA et al. (2014). Using genetic analysis to estimate population size, sex ratio, and social organization in an Asian elephant population in conflict with humans in Alur, southern India. Conservation Genetics 15, 897-907.
Chang ZF, Luo MF, Liu ZJ et al. (2012). Human influence on the population decline and loss of genetic diversity in a small and isolated population of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Genetica 140, 105-14.
Charlesworth B (2009). Effective population size and patterns of molecular evolution and variation. Nature Reviews Genetics 10, 195-205.
Choudhury A, Choudhury D, Desai A et al. (2008). Elephas maximus. IUCN Red List of Threatened Species. Available from URL: https://www.iucnredlist.org/species/7140/45818198
Do C, Waples RS, Peel D et al. (2014). NeEstimator v2: Reimplementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Molecular Ecology Resources 14, 209-14.
Dobelmann J, Alexander A, Baty JW et al. (2019). The association between mitochondrial genetic variation and reduced colony fitness in an invasive wasp. Molecular Ecology 28, 3324-38.
Dormann CF, Elith J, Bacher S et al. (2013). Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography 36, 27-46.
Eggert L, Eggert J, Woodruff D (2003). Estimating population sizes for elusive animals: The forest elephants of Kakum National Park, Ghana. Molecular Ecology 12, 1389-402.
ESRI A (2012). ArcGIS 10.1. Redlands, CA, USA: Environmental Systems Research Institute.
Feng L, Wang Z, Lin L et al. (2010). Habitat selection in dry season of Asian elephant (Elephas maximus) and conservation strategies in Nangunhe National Nature Reserve,Yunnan, China. Acta Theriologica Sinica 30, 1-10.
Fernando P, Leimgruber P, Prasad T et al. (2012). Problem-elephant translocation: Translocating the problem and the elephant? PLoS ONE 7, e50917.
Fernando P, Pastorini J (2011). Range-wide status of Asian elephants. Gajah 35, 15-20.
Fernando P, Vidya T, Rajapakse C et al. (2003). Reliable noninvasive genotyping: Fantasy or reality? Journal of Heredity 94, 115-23.
Frankham R (1995). Effective population size/adult population size ratios in wildlife: A review. Genetics Research 66, 95-107.
Galpern P, Manseau M, Hettinga P et al. (2012). Allelematch: An R package for identifying unique multilocus genotypes where genotyping error and missing data may be present. Molecular Ecology Resources 12, 771-8.
Goossens B, Sharma R, Othman N et al. (2016). Habitat fragmentation and genetic diversity in natural populations of the Bornean elephant: Implications for conservation. Biological Conservation 196, 80-92.
Gray TNE, Vidya TNC, Potdar S et al. (2014). Population size estimation of an Asian elephant population in eastern Cambodia through non-invasive mark-recapture sampling. Conservation Genetics 15, 803-10.
Habel JC, Schmitt T (2018). Vanishing of the common species: Empty habitats and the role of genetic diversity. Biological Conservation 218, 211-6.
Hale LJ, Shi K, Gilbert TC, Peh KS-H, Riordan P (2020). Social structure and demography of a remnant Asian elephant (Elephas maximus) population and the implications for survival. Oryx 55, 473-8.
He C, Du J, Zhu D, Zhang L (2020). Population viability analysis of small population: A case study for Asian elephant in China. Integrative Zoology 15, 350-62.
Hedges S, Johnson A, Ahlering M et al. (2013). Accuracy, precision, and cost-effectiveness of conventional dung density and fecal DNA based survey methods to estimate Asian elephant (Elephas maximus) population size and structure. Biological Conservation 159, 101-8.
Hedges S, Lawson D (2006). Dung Survey Standards for the MIKE Programme. CITES MIKE Programme, Nairobi, Kenya. Available from URL: https://cites.org/eng/prog/mike/index.php/portal
Hoffmann AA, Sgrò CM, Kristensen TN (2017). Revisiting adaptive potential, population size, and conservation. Trends in Ecology & Evolution 32, 506-17.
Hollenbeck C, Portnoy D, Gold J (2016). A method for detecting recent changes in contemporary effective population size from linkage disequilibrium at linked and unlinked loci. Heredity 117, 207.
Huang C, Li X, Khanal L, Jiang X (2019). Habitat suitability and connectivity inform a co-management policy of protected area network for Asian elephants in China. PeerJ 7, e6791.
Huisman J, Kruuk LE, Ellis PA et al. (2016). Inbreeding depression across the lifespan in a wild mammal population. PNAS 113, 3585-90.
Huyan J, Xiao J, Yu B et al. (2014). Research progress in function zoning of nature reserves in China. Acta Ecologica Sinica 34, 6391-6.
Johnson JA, Tingay RE, Culver M et al. (2009). Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle. Molecular Ecology 18, 54-63.
Johnson MB, Parker LD, Vanthomme H et al. (2019). Patterns of genetic diversity in African forest elephants living in a human-modified landscape in southwest Gabon. Conservation Science and Practice 1, e76.
Jombart T (2008). adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403-5.
Joshi R, Singh R, Dixit A et al. (2010). Is isolation of protected habitats the prime conservation concern for endangered Asian elephants in Shivalik landscape. GJESM 4, 113-26.
Kalinowski ST, Taper ML, Marshall TC (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16, 1099-106.
Kalinowski ST, Wagner AP, Taper ML (2006). ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Resources 6, 576-9.
Kanagaraj R, Araujo MB, Barman R et al. (2019). Predicting range shifts of Asian elephants under global change. Diversity and Distributions 25, 822-38.
Kongrit C, Siripunkaw C, Brockelman W et al. (2008). Isolation and characterization of dinucleotide microsatellite loci in the Asian elephant (Elephas maximus). Molecular Ecology Resources 8, 175-7.
Krishnan V, Kumar MA, Raghunathan G et al. (2019). Distribution and habitat use by Asian Elephants (Elephas maximus) in a coffee-dominated landscape of Southern India. Tropical Conservation Science 12, 1-12.
Lacy RC, Pollak JP (2019). Vortex: A stochastic simulation of the extinction process. Illinois, USA: Chicago Zoological Society, Brookfield.
Lan H, Zhou T, Wan Q-H et al. (2019). Genetic diversity and differentiation at structurally varying MHC haplotypes and microsatellites in bottlenecked populations of endangered crested ibis. Cells 8, 377.
Li X, Jiang G, Tian H et al. (2015). Human impact and climate cooling caused range contraction of large mammals in China over the past two millennia. Ecography 38, 74-82.
Liang S, Chen J, Wu B et al. (2015). Extracting rubber plantation with decision tree model based on object-oriented method. Journal of Remote Sensing 19, 485-94.
Lin L, Jin Y, Yang H et al. (2015). Evaluation of habitat for Asian elephants (Elephas maximus) in Xishuangbanna, Yunnan, China. Acta Theriologica Sinica 35, 1-13.
Liu L, Yanfei J, Dekun C et al. (2014). Population and habitat status of Asian elephants (Elephas maximus) in Mengla Sub-reserve of Xishuangbanna National Nature Reserve,Yunnan of China. Acta Ecologica Sinica 34, 1725-35.
Liu P, Wen H, Harich FK et al. (2017). Conflict between conservation and development: cash forest encroachment in Asian elephant distributions. Scientific Reports 7, 6404.
Liu P, Wen H, Lin L et al. (2016). Habitat evaluation for Asian elephants (Elephas maximus) in Lincang: Conservation planning for an extremely small population of elephants in China. Biological Conservation 198, 113-21.
Liu X, Feng Z, Jiang L et al. (2013). Rubber plantation and its relationship with topographical factors in the border region of China, Laos and Myanmar. Journal of Geographical Sciences 23, 1019-40.
Luikart G, Sherwin W, Steele B et al. (1998). Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Molecular Ecology 7, 963-74.
Ma L (2004). Study of Asian elephant community structure with conservation genetics (Master thesis). Beijing Normal University, Beijing.
Menon V, Tiwari SK (2019). Population status of Asian elephants (Elephas maximus) and key threats. International Zoo Yearbook 53, 17-30.
Merola M (1994). A reassessment of homozygosity and the case for inbreeding depression in the cheetah, Acinonyx jubatus: implications for conservation. Conservation Biology 8, 961-71.
Merz G (1986). The status of the forest elephant Loxodonta africana cyclotis, Matschie, 1900, in the Gola Forest reserves, Sierra Leone. Biological Conservation 36, 83-94.
Mondol S, Mailand CR, Wasser SK (2014). Male biased sex ratio of poached elephants is negatively related to poaching intensity over time. Conservation Genetics 15, 1259-63.
Moßbrucker AM, Apriyana I, Fickel J et al. (2015). Non-invasive genotyping of Sumatran elephants: Implications for conservation. Tropical Conservation Science 8, 745-59.
Muscarella R, Galante PJ, Soley-Guardia M et al. (2014). ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution 5, 1198-205.
Nangunhe N (2018). General introduction of Nangunhe National Nature Reserve, Cangyuan, Yunnan, National Forestry and Grassland Administration. Available from URL: http://www.forestry.gov.cn. Accessed May 12, 2018.
Peakall R, Smouse PE (2006). GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Resources 6, 288-95.
Phillips SJ, Dudík M (2008). Modeling of species distributions with Maxent: New extensions and a comprehensive evaluation. Ecography 31, 161-75.
Phillips SJ, Dudík M, Schapire RE (2019). Maxent software for modeling species niches and distributions (Version 3.4.0). Available from URL: http://biodiversityinformatics.amnh.org/open_source/maxent/
R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from URL: https://www.R-project.org/.
Sukumar R (2006). A brief review of the status, distribution and biology of wild Asian elephants Elephas maximus. International Zoo Yearbook 40, 1-8.
Schmidt-Küntzel A, Dalton DL, Menotti-Raymond M et al. (2018). Conservation genetics of the cheetah: Genetic history and implications for conservation. In: Cheetahs: Biology and Conservation. Elsevier, San Diego, CA, pp. 71-92.
Taberlet P, Griffin S, Goossens B et al. (1996). Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Research 24, 3189-94.
Tang Y, Wang Z, Jiang G et al. (2019). Population dynamics analysis of Asian elephant in Nangunhe river basin. Forestry Construction 6, 97-102.
Theuerkauf J, Ellenberg H, Guiro Y (2000). Group structure of forest elephants in the Bossematié Forest Reserve, Ivory Coast. African Journal of Ecology 38, 262-4.
Thitaram C, Dejchaisri S, Somgird C et al. (2015). Social group formation and genetic relatedness in reintroduced Asian elephants (Elephas maximus) in Thailand. Applied Animal Behaviour Science 172, 52-7.
Tyson M, Hedges S, Sitompul A (2002). WCS-Indonesia Sumatran Elephant Project: Six month report for January-June, 2002. Wildlife Conservation Society, Jakarta, Indonesia.
Valière N (2002). GIMLET: A computer program for analysing genetic individual identification data. Molecular Ecology Notes 2, 377-9.
Varma S, Dang NX, Van Thanh T et al. (2008). The Asian elephants Elephas maximus of Cat Tien National Park, Vietnam: Status and conservation of a vanishing population. Oryx 42, 92-9.
Vidya T, Varma S, Dang NX et al. (2007). Minimum population size, genetic diversity, and social structure of the Asian elephant in Cat Tien National Park and its adjoining areas, Vietnam, based on molecular genetic analyses. Conservation Genetics 8, 1471-8.
Wan X, Jiang G, Yan C et al. (2019). Historical records reveal the distinctive associations of human disturbance and extreme climate change with local extinction of mammals. PNAS 116, 19001-8.
Wang L, Li Z, Luo A et al. (2015). Preliminary study on strategies and measures on transboundary biodiversity conservation between China and Laos. Forest Inventory and Planning 40, 149-52.
Warren DL, Seifert SN (2011). Ecological niche modeling in Maxent: The importance of model complexity and the performance of model selection criteria. Ecological Applications 21, 335-42.
White GC, Burnham KP (1999). Program MARK: Survival estimation from populations of marked animals. Bird Study 46, S120-S39.
Xu J, Grumbine RE, Beckschäfer P (2014). Landscape transformation through the use of ecological and socioeconomic indicators in Xishuangbanna, Southwest China, Mekong Region. Ecological Indicators 36, 749-56.
Yu L, Shi Y, Gong P (2015). Land cover mapping and data availability in critical terrestrial ecoregions: A global perspective with Landsat thematic mapper and enhanced thematic mapper plus data. Biological Conservation 190, 34-42.
Zachos F, Althoff C, Steynitz Yv et al. (2007). Genetic analysis of an isolated red deer (Cervus elaphus) population showing signs of inbreeding depression. European Journal of Wildlife Research 53, 61-7.
Zhang B, Li M, Zhang Z et al. (2007). Genetic viability and population history of the giant panda, putting an end to the “evolutionary dead end”? Molecular Biology and Evolution 24, 1801-10.
Zhang L, Dong L, Lin L et al. (2015). Asian elephants in China: estimating population size and evaluating habitat suitability. PLoS ONE 10, e0124834.