Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Population genetics, demographics and implications for conservation of Brachychiton sp. Ormeau, a Critically Endangered rainforest tree

R. Roberts A , R. W. Lamont A , C. L. Simmons A B , G. Leiper C , G. P. Guymer B and A. Shapcott https://orcid.org/0000-0003-3734-052X A D
+ Author Affiliations
- Author Affiliations

A Genecology Research Centre, School of Science Technology and Engineering, University of the Sunshine Coast, Maroochydore, Qld 4558, Australia.

B Queensland Herbarium, Department of Environment and Science, Brisbane Botanic Gardens, Mt Coot-tha Road, Toowong, Qld 4066, Australia.

C Retired. Beenleigh, Qld 4207, Australia.

D Corresponding author. Email: ashapcot@usc.edu.au

Australian Journal of Botany 69(5) 259-273 https://doi.org/10.1071/BT21005
Submitted: 14 January 2021  Accepted: 8 April 2021   Published: 15 June 2021

Abstract

Brachychiton sp. Ormeau (L.H. Bird AQ435851), commonly known as the Ormeau bottle tree, is listed as Critically Endangered under the Environment Protection and Biodiversity Conservation Act 1999. Undescribed and extremely rare, it is known only from several sites within a very small geographic range near Ormeau in south-east Queensland. Using microsatellite markers developed for this study, we found Brachychiton sp. Ormeau to be genetically distinct from several closely related species, confirming unique specific status. We also assessed levels of genetic variation found within B. sp. Ormeau subpopulations to provide recommendations for recovery projects. The species exhibited low levels of variation (He = 0.065); however, no evidence of inbreeding (F = –0.290). We infer that the species’ current restricted range and low genetic diversity is due to a combination of the effects of well documented climate shifts across the Plio-Pleistocene, exacerbated by extensive rates of relatively recent and ongoing human-mediated habitat loss. Our results suggest that, to enhance the long-term viability of B. sp. Ormeau, the most effective recovery strategies include the protection and restoration of the existing remnant habitat, as well as enhancement of local subpopulations and existing isolated plants, with additional plants to increase the genetic diversity.

Keywords: Ormeau bottle tree, Brachychiton ‘sp. Ormeau’, conservation, demographics, endangered species, fragmentation, regeneration, rainforest, extinction, habitat patches.


References

Accad A, Neldner VJ (2015) ‘Remnant regional ecosystem vegetation in Queensland. Analysis 1997–2013.’ (Queensland Department of Science, Information Technology and Innovation: Brisbane, Qld, Australia)

Arroyo-Rodríguez V, Fahrig L, Tabarelli M, Watling JI, Tischendorf L, Benchimol M, Cazetta E, Faria D, Leal IR, Melo FPL, Morante-Filho JC, Santos BA, Arasa-Gisbert R, Arce-Pena N, Cervantes-Lopez MJ, Cudney-Valenzuela S, Galan-Acedo C, San-Jose M, Vieira ICG, Slik JWF, Nowakowski AJ, Tscharntke T (2020) Designing optimal human-modified landscapes for forest biodiversity conservation. Ecology Letters
Designing optimal human-modified landscapes for forest biodiversity conservation.Crossref | GoogleScholarGoogle Scholar | 32537896PubMed |

Bate PJ, Franklin DC (2015) Limited impact of irrigation on the phenology of Brachychiton megaphyllus: a deciduous shrub that flowers while leafless during the tropical dry season. Journal of Tropical Ecology 31, 459–467.
Limited impact of irrigation on the phenology of Brachychiton megaphyllus: a deciduous shrub that flowers while leafless during the tropical dry season.Crossref | GoogleScholarGoogle Scholar |

Buist M, Yates CJ, Ladd PG (2000) Ecological characteristics of Brachychiton populneus (Sterculiaceae) (kurrajong) in relation to the invasion of urban bushland in south-western Australia Austral Ecology 25, 487–496.
Ecological characteristics of Brachychiton populneus (Sterculiaceae) (kurrajong) in relation to the invasion of urban bushland in south-western AustraliaCrossref | GoogleScholarGoogle Scholar |

Buza L, Young A, Thrall P (2000) Genetic erosion, inbreeding and reduced fitness in fragmented populations of the endangered tetraploid pea Swainsona recta. Biological Conservation 93, 177–186.
Genetic erosion, inbreeding and reduced fitness in fragmented populations of the endangered tetraploid pea Swainsona recta.Crossref | GoogleScholarGoogle Scholar |

Byrne M, Steane DA, Joseph L, Yeates DK, Jordan GJ, Crayn D, Aplin K, Cantrill DJ, Cook LG, Crisp MD, Keogh JS, Melville J, Moritz C, Porch N, Sniderman JMK, Sunnucks P, Weston PH (2011a) Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota. Journal of Biogeography 38, 1635–1656.
Decline of a biome: evolution, contraction, fragmentation, extinction and invasion of the Australian mesic zone biota.Crossref | GoogleScholarGoogle Scholar |

Byrne M, Stone L, Millar M (2011b) Assessing genetic risk in revegetation. Journal of Applied Ecology 48, 1365–1373.
Assessing genetic risk in revegetation.Crossref | GoogleScholarGoogle Scholar |

Carter RJ (2011) Diversification of the Malvales, Sterculioideae and Brachychiton. PhD thesis, Australian National University, Canberra, ACT, Australia.

Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigour. Trends in Plant Science 15, 57–71.
Molecular mechanisms of polyploidy and hybrid vigour.Crossref | GoogleScholarGoogle Scholar | 20080432PubMed |

Cho L-H, Yoon J, An G (2017) The control of flowering time by environmental factors. The Plant Journal 90, 708–719.
The control of flowering time by environmental factors.Crossref | GoogleScholarGoogle Scholar | 27995671PubMed |

Chung MY, Nason JD, Sun B-Y, Moon M-O, Chung JM, Park C-W, Chung MG (2010) Extremely low levels of genetic variation in the critically endangered monotypic fern genus Mankyua chejuense (Ophioglossaceae) from Korea: implications for conservation. Biochemical Systematics and Ecology 38, 888–896.
Extremely low levels of genetic variation in the critically endangered monotypic fern genus Mankyua chejuense (Ophioglossaceae) from Korea: implications for conservation.Crossref | GoogleScholarGoogle Scholar |

Coates DJ, Sampson JF, Yates CJ (2007) Plant mating systems and assessing population persistence in fragmented landscapes. Australian Journal of Botany 55, 239–249.
Plant mating systems and assessing population persistence in fragmented landscapes.Crossref | GoogleScholarGoogle Scholar |

Cowie ID, Guymer GP (2014) A new, rare species of Brachychiton from Fish River Station, Northern Territory. Australian Systematic Botany 27, 462–468.
A new, rare species of Brachychiton from Fish River Station, Northern Territory.Crossref | GoogleScholarGoogle Scholar |

Da Silva J, Donaldson D, Reeves G, Hedderson TA (2012) Population genetics and conservation of critically small cycad populations: a case study of the Albany Cycad, Encephalartos latifrons (Lehmann). Biological Journal of the Linnean Society. Linnean Society of London 105, 293–308.
Population genetics and conservation of critically small cycad populations: a case study of the Albany Cycad, Encephalartos latifrons (Lehmann).Crossref | GoogleScholarGoogle Scholar |

Dardengo JFE, Rossi AAB, Silva BM, Silva IV, Silva CJ, Sebbenn AM (2016) Diversity and spatial genetic structure of a natural population of Theobroma speciosum (Malvaceae) in the Brazilian Amazon. Revista de Biología Tropical 64, 1091–1099.
Diversity and spatial genetic structure of a natural population of Theobroma speciosum (Malvaceae) in the Brazilian Amazon.Crossref | GoogleScholarGoogle Scholar | 29461785PubMed |

Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |

Ellstrand NC, Elam DR (1993) Population genetic conseqences of small population size: implications for plant conservation. Annual Review of Ecology and Systematics 24, 217–242.
Population genetic conseqences of small population size: implications for plant conservation.Crossref | GoogleScholarGoogle Scholar |

Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software Structure: a simulation study.Crossref | GoogleScholarGoogle Scholar | 15969739PubMed |

Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.
Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data.Crossref | GoogleScholarGoogle Scholar | 1644282PubMed |

Fensham RJ, Beveridge JA, Forster PI (2019) Brachychiton guymeri J.A.Bever., Fensham & P.I.Forst. (Sterculiaceae), a new species from north Queensland Austrobaileya 10, 443–457.

Franklin DC, Bate PJ (2013) Brachychiton megaphyllus, the red-flowered kurrajong species profile. Northern Territory Naturalist 24, 81–88.

Fuchs EJ, Hamrick JL (2011) Mating system and pollen flow between remnant populations of the endangered tropical tree, Guaiacum sanctum (Zygophyllaceae). Conservation Genetics 12, 175–185.
Mating system and pollen flow between remnant populations of the endangered tropical tree, Guaiacum sanctum (Zygophyllaceae).Crossref | GoogleScholarGoogle Scholar |

Ghazoul J (2005) Pollen and seed dispersal among dispersed plants. Biological Reviews of the Cambridge Philosophical Society 80, 413–433.
Pollen and seed dispersal among dispersed plants.Crossref | GoogleScholarGoogle Scholar | 16094807PubMed |

Gitzendanner MA, Soltis P (2000) Patterns of genetic variation in rare and widespread plant congeners. American Journal of Botany 87, 783–792.
Patterns of genetic variation in rare and widespread plant congeners.Crossref | GoogleScholarGoogle Scholar | 10860909PubMed |

Giustina LD, Luz LN, Vieira FS, Rossi FS, Soares-Lopes CRA, Pereira TNS, Rossi AAB (2014) Population structure and genetic diversity in natural populations of Theobroma speciosum Willd. ex Spreng (Malvaceae). Genetics and Molecular Research 13, 3510–3519.
Population structure and genetic diversity in natural populations of Theobroma speciosum Willd. ex Spreng (Malvaceae).Crossref | GoogleScholarGoogle Scholar | 24615108PubMed |

Godefroid S, Piazza C, Rossi G, Buord S, Stevens A-D, Aguraiuja R, Cowell C, Weekley CW, Vogg G, Iriondo JM, Johnson I, Dixon B, Gordon D, Magnanon S, Valentin B, Bjureke K, Koopman R, Vicens M, Virevaire M, Vanderborght T (2011) How successful are plant species reintroductions? Biological Conservation 144, 672–682.
How successful are plant species reintroductions?Crossref | GoogleScholarGoogle Scholar |

Guymer GP (1988) A taxonomic revision of Brachychiton (Sterculiaceae). Australian Systematic Botany 1, 199–323.
A taxonomic revision of Brachychiton (Sterculiaceae).Crossref | GoogleScholarGoogle Scholar |

Hamrick JL, Trapnell DW (2011) Using population genetic analyses to understand seed dispersal patterns. Acta Oecologica 37, 641–649.
Using population genetic analyses to understand seed dispersal patterns.Crossref | GoogleScholarGoogle Scholar |

Heywood VH (2019) Conserving plants within and beyond protected areas – still problematic and future uncertain. Plant Diversity 41, 36–49.
Conserving plants within and beyond protected areas – still problematic and future uncertain.Crossref | GoogleScholarGoogle Scholar | 31193163PubMed |

Hiscock SJ, Kües U (1999) Cellular and molecular mechanisms of sexual incompatibility in plants and fungi. International Review of Cytology 193, 165–295.
Cellular and molecular mechanisms of sexual incompatibility in plants and fungi.Crossref | GoogleScholarGoogle Scholar | 10494623PubMed |

Hudson QJ, Wilkins RJ, Waas JR, Hogg ID (2000) Low genetic variability in small populations of New Zealand kokako Callaeas cinerea wilsoni. Biological Conservation 96, 105–112.
Low genetic variability in small populations of New Zealand kokako Callaeas cinerea wilsoni.Crossref | GoogleScholarGoogle Scholar |

Humphreys AM, Govaerts R, Fininski SZ, Lughadha EN, Vorontsova MS (2019) Global dataset shows geography and life form predict modern plant extinction and rediscovery. Nature Ecology & Evolution 3, 1043–1047.
Global dataset shows geography and life form predict modern plant extinction and rediscovery.Crossref | GoogleScholarGoogle Scholar |

Jump AS, Peñuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecology Letters 8, 1010–1020.
Running to stand still: adaptation and the response of plants to rapid climate change.Crossref | GoogleScholarGoogle Scholar |

Kang Y, Lanchier N (2011) Expansion or extinction: deterministic and stochastic two-patch models with Allee effects. Mathematical Biology 62, 925–973.
Expansion or extinction: deterministic and stochastic two-patch models with Allee effects.Crossref | GoogleScholarGoogle Scholar |

Koenig J, Griffiths A (2012) The population ecology of two tropical trees, Brachychiton diversifolius (Malvaceae) and Bombax ceiba (Bombaceae), harvested by indigenous woodcarvers in Arnhem Land, Australia Environmental Management 50, 555–565.
The population ecology of two tropical trees, Brachychiton diversifolius (Malvaceae) and Bombax ceiba (Bombaceae), harvested by indigenous woodcarvers in Arnhem Land, AustraliaCrossref | GoogleScholarGoogle Scholar | 22829220PubMed |

Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15, 1179–1191.
Clumpak: a program for identifying clustering modes and packaging population structure inferences across K.Crossref | GoogleScholarGoogle Scholar | 25684545PubMed |

Kyndt T, Assogbadjo AE, Hardy OJ, Kakaï RG, Sinsin B, Van Damme P, Gheysen G (2009) Spatial genetic structuring of baobab (Adansonia digitata, Malvaceae) in the traditional agroforestry systems of West Africa. American Journal of Botany 96, 950–957.
Spatial genetic structuring of baobab (Adansonia digitata, Malvaceae) in the traditional agroforestry systems of West Africa.Crossref | GoogleScholarGoogle Scholar | 21628247PubMed |

Leimu R, Mutiikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? Journal of Ecology 94, 942–952.
How general are positive relationships between plant population size, fitness and genetic variation?Crossref | GoogleScholarGoogle Scholar |

Leimu R, Vergeer P, Angeloni F, Ouborg NJ (2010) Habitat fragmentation, climate change, and inbreeding in plants. Annals of the New York Academy of Sciences 1195, 84–98.
Habitat fragmentation, climate change, and inbreeding in plants.Crossref | GoogleScholarGoogle Scholar | 20536818PubMed |

Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95, 255–273.
Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees.Crossref | GoogleScholarGoogle Scholar | 16094300PubMed |

MacPhail M, Pillans B, Hope G, Clark D (2020) Extirpations and extinctions: a plant microfossil-based history of the demise of rainforest and wet sclerophyll communities in the Lake George Basin, Southern Tablelands of NSW, south-east Australia Australian Journal of Botany 68, 208–228.
Extirpations and extinctions: a plant microfossil-based history of the demise of rainforest and wet sclerophyll communities in the Lake George Basin, Southern Tablelands of NSW, south-east AustraliaCrossref | GoogleScholarGoogle Scholar |

Matocq MD, Villablanca FX (2001) Low genetic diversity in an endangered species: recent or historic pattern? Biological Conservation 98, 61–68.
Low genetic diversity in an endangered species: recent or historic pattern?Crossref | GoogleScholarGoogle Scholar |

McKay JK, Christian CE, Harrison S, Rice KJ (2005) ‘How local is local?’ – a review of practical conceptual issues in the genetics of restoration. Restoration Ecology 13, 432–440.
‘How local is local?’ – a review of practical conceptual issues in the genetics of restoration.Crossref | GoogleScholarGoogle Scholar |

Meglécz E, Costedoat C, Dubut V, Gilles A, Malausa T, Pech N, Martin J-F (2010) QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects. Bioinformatics 26, 403–404.
QDD: a user-friendly program to select microsatellite markers and design primers from large sequencing projects.Crossref | GoogleScholarGoogle Scholar | 20007741PubMed |

Melo Júnior AF, Carvalho D, Brandão MM, Sousa LA, de Almeida Vieira F, Menezes EV, Royo VA, Dario Alves Oliveira DA (2015) Spatial genetic structure of Cavanillesia arborea K.Schum.(Malvaceae) in seasonally dry tropical forest: Implications for conservation. Biochemical Systematics and Ecology 58, 114–119.
Spatial genetic structure of Cavanillesia arborea K.Schum.(Malvaceae) in seasonally dry tropical forest: Implications for conservation.Crossref | GoogleScholarGoogle Scholar |

Neel MC (2008) Patch connectivity and genetic diversity conservation in the federally endangered and narrowly endemic plant species Astragalus albens (Fabaceae). Biological Conservation 141, 938–955.
Patch connectivity and genetic diversity conservation in the federally endangered and narrowly endemic plant species Astragalus albens (Fabaceae).Crossref | GoogleScholarGoogle Scholar |

Neldner VJ, Laidlaw MJ, McDonald KR, Mathieson MT, Melzer RI, Seaton R, McDonald WJF, Hobson R, Limpus CJ (2017) ‘Scientific Review of the Impacts of Land Clearing on Threatened Species in Queensland.’ (Queensland Government: Brisbane, Qld, Australia)

Peakall ROD, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
Inference of population structure using multilocus genotype data.Crossref | GoogleScholarGoogle Scholar | 10835412PubMed |

Queensland Herbarium (2019) ‘Regional Ecosystem Description Database (REDD). Ver. 11.1.’ (Queensland Department of Environment and Science: Brisbane, Qld, Australia)

Reynolds VA, Anderegg LDL, Loy X, Hille R, Lambers J, Mayfield MM (2018) Unexpected drought resistance strategies in seedlings of four Brachychiton species. Tree Physiology 38, 664–677.
Unexpected drought resistance strategies in seedlings of four Brachychiton species.Crossref | GoogleScholarGoogle Scholar | 29190366PubMed |

Ridley M (1996) ‘Evolution.’ (Blackwell Science: Cambridge, UK)

Rosas F, Quesada M, Lobo JA, Sork VL (2011) Effects of habitat fragmentation on pollen flow and genetic diversity of the endangered tropical tree Swietenia humilis (Meliaceae). Biological Conservation 144, 3082–3088.
Effects of habitat fragmentation on pollen flow and genetic diversity of the endangered tropical tree Swietenia humilis (Meliaceae).Crossref | GoogleScholarGoogle Scholar |

Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics Methods and Protocols: Methods in Molecular Biology’. (Eds S Krawetz, S Misener) pp. 365–386. (Humana Press: Totowa, NJ, USA)

Sattler PS (1999) ‘The Conservation Status of Queensland’s bioregional Ecosystems.’ (Environmental Protection Agency, Queensland Government: Brisbane, Qld, Australia)

Shapcott A, Forster PI, Guymer GP, McDonald WJF, Faith DP, Erickson DL, Kress WJ (2015a) Mapping biodiversity and setting conservation priorities for SE Queensland’s rainforests using DNA Barcoding. PLoS One 10, e0122164
Mapping biodiversity and setting conservation priorities for SE Queensland’s rainforests using DNA Barcoding.Crossref | GoogleScholarGoogle Scholar | 25803607PubMed |

Shapcott A, Lamont RW, O’Connor K, James HE, Conroy G (2015b) Population genetics of Philotheca sporadica (Rutaceae) to advise an offset translocation program. Conservation Genetics 16, 687–702.
Population genetics of Philotheca sporadica (Rutaceae) to advise an offset translocation program.Crossref | GoogleScholarGoogle Scholar |

Shapcott A, Liu Y, Howard M, Forster PI, Kress WJ, Erickson DL, Faith DP, Shimizu Y, McDonald WJ (2017) Comparing floristic diversity and conservation priorities across South East Queensland regional rain forest ecosystems using phylodiversity indexes. International Journal of Plant Sciences 178, 211–229.
Comparing floristic diversity and conservation priorities across South East Queensland regional rain forest ecosystems using phylodiversity indexes.Crossref | GoogleScholarGoogle Scholar |

Silcock JL, Simmons CL, Monks L, Dillon R, Reiter N, Jusaitis M, Vesk PA, Byrne M, Coates DJ (2019) Threatened plant translocation in Australia: a review. Biological Conservation 236, 211–222.
Threatened plant translocation in Australia: a review.Crossref | GoogleScholarGoogle Scholar |

Silva JL, Brennan AC, Mejıas JA (2016) Population genetics of self-incompatibility in a clade of relict cliff-dwelling plant species. AoB Plants 8, plw029
Population genetics of self-incompatibility in a clade of relict cliff-dwelling plant species.Crossref | GoogleScholarGoogle Scholar | 27154621PubMed |

Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batáry P, Bengtsson J, Clough Y, Cris TO, Dormann CF, Ewers RM, Fründ J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes – eight hypotheses. Biological Reviews of the Cambridge Philosophical Society 87, 661–685.
Landscape moderation of biodiversity patterns and processes – eight hypotheses.Crossref | GoogleScholarGoogle Scholar | 22272640PubMed |

Weeks A, Sgro C, Young A, Frankham R, Mitchell M, Miller K, Byrne M, Coates D, Eldridge M, Sunnucks P, Breed M, James E, Hoffman A (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evolutionary Applications 4, 709–725.
Assessing the benefits and risks of translocations in changing environments: a genetic perspective.Crossref | GoogleScholarGoogle Scholar | 22287981PubMed |

Wilkie P, Clark A, Pennington RT, Cheek M, Bayer C, Wilcock CC (2006) Phylogenetic relationships within the subfamily Sterculioideae (Malvaceae/Sterculiaceae Sterculieae) using the chloroplast gene ndhF. Systematic Botany 31, 160–170.
Phylogenetic relationships within the subfamily Sterculioideae (Malvaceae/Sterculiaceae Sterculieae) using the chloroplast gene ndhF.Crossref | GoogleScholarGoogle Scholar |

Wilkie JD, Sedgley M, Olesen T (2008) Regulation of floral initiation in horticultural trees Journal of Experimental Botany 59, 3215–3228.
Regulation of floral initiation in horticultural treesCrossref | GoogleScholarGoogle Scholar | 18653697PubMed |

Zhang J, Ye Q, Gao P, Yao X (2012) Genetic footprints of habitat fragmentation in the extant populations of Sinojackia (Styracaceae): implications for conservation. Botanical Journal of the Linnean Society 170, 232–242.
Genetic footprints of habitat fragmentation in the extant populations of Sinojackia (Styracaceae): implications for conservation.Crossref | GoogleScholarGoogle Scholar |