Ex situ conservation in botanical gardens – challenges and scientific potential preserving plant biodiversity

  • Zsófia KOVÁCS Hungarian University of Agriculture and Life Sciences, Institute of Agronomy, Department of Botany, Ménesi street 44, Budapest 1118, (HU)
  • Anna Mária CSERGŐ Hungarian University of Agriculture and Life Sciences, Institute of Agronomy, Department of Botany, Ménesi street 44, Budapest 1118, (HU)
  • Péter CSONTOS Institute for Soil Sciences, Centre for Agricultural Research, Herman Ottó street 15, Budapest 1022 (HU)
  • Mária HÖHN Hungarian University of Agriculture and Life Sciences, Institute of Agronomy, Department of Botany, Ménesi street 44, Budapest 1118, (HU)
Keywords: biodiversity conservation, ex situ, functional traits, genetic diversity, living collections, review

Abstract

In the Anthropocene, the world’s plant diversity is threatened with extinction and the erosion of the genetic diversity of natural populations. According to the State of the World’s Plants and Fungi 2020 of the Royal Botanic Gardens, Kew, two out of five of the ~350,000 known vascular plant species are at risk of extinction. Despite the considerable toolkit of biodiversity conservation practices, usually it is hard to choose the best option to stop biodiversity loss. Ex situ conservation has seen massive development due to radical losses of natural ecosystems, and its incrementing necessity has been underscored by Target 8 of the 2011-2020 Global Strategy for Plant Conservation. As we crossed the finish line of this strategy in 2020, a review of the accumulated knowledge on the ex situ living collections has become particularly important. Despite the increasing attention received by ex situ conservation, studies on the sustainability, quality, and usability of the plant material prior to establishing the garden collections are few, leaving major gaps unfilled in terms of best ex situ conservation practices. Here we present an overview of the results and experiences in ex situ conservation focusing on living plant collections, with the aim of guiding conservation practitioners towards the most efficient working methods. We evaluate the future needs and perspectives of this conservation technique, based on case studies on both woody and herb species. Possible conservation applications and priorities suggested for future works are summarized.

Metrics

Metrics Loading ...

References

Aguiar BI, Freitas MLM, Zannato AS, Tambarussi EV, Moraes MLT, Ambrosano MN, … Sebbenn AM (2020). The effects of pollen dispersal and mating pattern on inbreeding depression and hybrid vigor in Balfourodendron riedelianum (Engl.) Engl. (Rutaceae). Conservation Genetics 21:305-317.

https://doi.org/10.1007/s10592-020-01250-0

Allendorf FW, Luikart G, Aitken SN (2013). Genetics and the conservation of populations. Wiley-Blackwell Publishing (2nd ed), Oxford, UK.

Asgher M, Verma S, Khan NA, Vyas D, Kumari P, Rashid S, … Ahmad P (2020). Physiological, biochemical and reproductive studies on Valeriana wallichii, a critically endangered medicinal plant of the Himalayan region grown under in-situ and ex-situ conditions. Plants 9(2):131. https://doi.org/10.3390/plants9020131

Basey AC, Fant JB, Kramer AT (2015). Producing native plant materials for restoration: 10 rules to collect and maintain genetic diversity. Native Plants Journal 16(1):37-53. http://npj.uwpress.org/cgi/doi/10.3368/npj.16.1.37

Bennie J, Davies TW, Cruse D, Gaston KJ (2016). Ecological effects of artificial light at night on wild plants. Journal of Ecology 104:611-620. https://doi.org/10.1111/1365-2745.12551

Biesmeijer JC (2006). Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313(5785):351-354. https://doi.org/10.1126/science.1127863

Brown ADH, Briggs JD (1991). Sampling strategies for genetic variation in ex situ collections of endangered plant species. In: Falk DA, Holsinger KE (Eds). Genetics and Conservation of Rare Plants. Oxford University Press, New York pp 99-122.

Brütting C, Hensen I, Wesche K (2012). Ex situ cultivation affects genetic structure and diversity in arable plants. Plant Biology 15(3):505-513. https://doi.org/10.1111/j.1438-8677.2012.00655.x

Chacón-Vargas K, García-Merchán VH, Sanín MJ (2019). From keystone species to conservation: conservation genetics of wax palm Ceroxylon quindiuense in the largest wild populations of Colombia and selected neighbouring ex situ plant collections. Biodiversity and Conservation 29:283-302. https://doi.org/10.1007/s10531-019-01882-w

Chen XB, Tian Q, Zhang QX (2013). Genetic diversity and ex situ conservation of Sinocalycanthus chinensis. Acta Horticulturae 977:253-257. https://doi.org/10.17660/ActaHortic.2013.977.29

Christe C, Kozlowski G, Frey D, Fazan L, Bétrisey S, Pirintsos S, … Naciri Y (2014). Do living ex situ collections capture the genetic variation of wild populations? A molecular analysis of two relict tree species, Zelkova abelica and Zelkova carpinifolia. Biodiversity and Conservation 23(12):2945-2959. https://doi.org/10.1007/s10531-014-0756-9

Cochrane A (2004). Western Australia’s ex situ program for threatened species: a model integrated strategy for conservation. In: Guerrant EO, Havens K, Maunder M (Eds). Ex situ Plant Conservation: Supporting Species Survival in the Wild. Island Press, Washington, DC pp 231-285.

Corrêa GDC, Da Rocha MR, Naves RV (2000). Germinação de sementes e emergência de plântulas de baru (Dipteryx alata Vog.) nos cerrados do Estado de Goiás [Seed germination and emergence of baru seedlings (Dipteryx alata Vog.) close to the State of Goiás] Pesquisa Agropecuária Tropical 30:17-23. https://doi.org/10.5216/pat.v30i2.2580

Cristea V, Jarda L, Holobiuc I (2013). Ex situ conservation of three endemic and/or endangered Dianthus species. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 41(1):73-78. https://doi.org/10.15835/nbha4119110

Edesi J, Tolonen J, Ruotsalainen AL, Aspi J, Häggman H (2020). Cryopreservation enables long-term conservation of critically endangered species Rubus humulifolius. Biodiversity and Conservation 29:303-314 https://doi.org/10.1007/s10531-019-01883-9

Ellstrand NC (2014). Is gene flow the most important evolutionary force in plants? American Journal of Botany 101(5):737-753. https://doi.org/10.3732/ajb.1400024

Ellstrand NC, Elam DR (1993). Population genetic consequences of small population size: implications for plant conservation. Annual Review of Ecology and Systematics 24(1):217-242. https://doi.org/10.3732/ajb.1400024

Ensslin A, Sandner TM, Matthies SD (2011). Consequences of ex situ cultivation of plants: Genetic diversity, fitness and adaptation of the monocarpic Cynoglossum officinale L. in botanic gardens. Biological Conservation 144(1):272-278. https://doi.org/10.1016/j.biocon.2010.09.001

Ensslin A, Tschöpe O, Burkart M, Joshi J (2015). Fitness decline and adaptation to novel environments in ex situ plant collections: Current knowledge and future perspectives. Biological Conservation 192:394-401. https://doi.org/10.1016/j.biocon.2015.10.012

Ensslin A, Van de VyVer A, Vanderborght T, Godefroid S (2018). Ex situ cultivation entails high risk of seed dormancy loss on short-lived wild plant species. Journal of Applied Ecology 55(3):1145-1154. https://doi.org/10.1111/1365-2664.13057

Ensslinn A, Godefroid S (2019). How the cultivation of wild plants in botanic gardens can change their genetic and phenotypic status and what this means for their conservation value. Sibbaldia: The Journal of Botanic Garden Horticulture 17:51-69. https://doi.org/10.23823/Sibbaldia/2019.267

Ensslin A, Godefroid S (2020). Ex situ cultivation impacts on plant traits and drought stress response in a multi-species experiment. Biological Conservation 248:108630. https://doi.org/10.1016/j.biocon.2020.108630

Etisham-Ul-Haq M, Allnutt TR, Smith-Ramiarez C, Gardener MF, Armesto JJ, Newton AC (2001). Patterns of genetic variation in in and ex situ populations of the threatened Chilean vine Berberidopsis corallina, detected using RAPD Markers. Annals of Botany 87(6):813-821. https://doi.org/10.1006/anbo.2001.1420

Falk DA (1987). Integrated conservation strategies for endangered plants. Natural Areas Journal 7:118-123.

Frankham R, Bradshaw CJA, Brook BW (2014). Genetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biological Conservation 170:56-63. https://doi.org/10.1016/j.biocon.2013.12.036

Gargiulo R, Saubin M, Rizzuto G, West B, Fay MF, Kallow S, Trivedi C (2019). Genetic diversity in British populations of Taxus baccata L.: Is the seedbank collection representative of the genetic variation in the wild? Biological Conservation 233:289-297. https://doi.org/10.1016/j.biocon.2019.01.014

Given DR (1987). What the conservationist requires of ex situ collections. In: Bramwell D, Hamann O, Heywood VH, Synge H (Eds). Botanic gardens and World Conservation Strategy. Academic Press, London pp 103-116.

Global strategy for plant conservation (GSPC) 2011-2020. Retrieved 2021 January 17 from https://www.cbd.int/gspc/targets.shtml

Gong X, Wu Q, Lu Y, Zhang Y (1998). Pollination biology of cultivated Magnolia delavayi. Acta Botanica Yunnanica 20(1):89-93.

Guerrant EOJ, Fiedler PL (2004). Accounting for sample decline during ex situ storage and reintroduction. In: Guerrant EOJ, Havens K, Maunder M (Eds). Ex situ Plant Conservation: Supporting Species Survival in the Wild. Island Press, Washington pp 365-386.

Guimarães RA, Corrêa MKM, Chaves LJ, Naves RV, de Campos Telles MP, Soares TN (2019). Mating system and pollen dispersal in Dipteryx alata Vogel (Leguminosae): comparing in situ and ex situ conditions. Tree Genetics & Genomes 15(28). https://doi.org/10.1007/s11295-019-1337-6

Hammer K (1984). Das domestikationssyndrom [The domestication syndrome]. Die Kulturpflanze 32(1):11-34.

Hampe A, Petit RJ (2005). Conserving biodiversity under climate change: the rear edge matters. Ecology Letters 8(5):461-467. https://doi.org/10.1111/j.1461-0248.2005.00739.x

Haskins KE, Pence V (2012). Transitioning plants to new environments: beneficial applications of soil microbes. In: Maschinski J, Haskins KE (Eds). Plant reintroductions in a changing climate: promises and perils. Society for Ecological Restoration, Center for Plant Restoration, Island Press, Washington pp 89-107.

Havens K, Guerrant EO, Maunder M, Vitt P (2004). Guidelines for ex situ conservation collection management: Minimizing risks. In: Guerrant EO, Havens K, Maunder M (Eds). Ex situ Plant Conservation: Supporting Species Survival in the Wild. Island Press, Washington pp 454-473.

Havens K, Vitt P, Maunder M, Guerrant EO, Dixon K (2006). Ex situ plant conservation and beyond. BioScience 56:525-532.

Hawkes JG, Maxted N, Ford-Lloyd BV (2012). The ex situ conservation of plant genetic resources. Springer Netherlands, Dordrecht pp 92-107.

Herbert R, Samuel S, Pattison G (1999). Using local stock for planting native trees and shrubs. In: Forestry Commission Practice Note 8. UK Forestry Commission, Edinburgh.

Hoban S, Schlarbaum S (2014). Optimal sampling of seeds from plant populations for ex-situ conservation of genetic biodiversity, considering realistic population structure. Biological Conservation 177:90-99. https://doi.org/10.1016/j.biocon.2014.06.014

Hoban S, Strand A (2015). Ex situ seed collections will benefit from considering spatial sampling design and species' reproductive biology. Biological Conservation 187:182-191. https://doi.org/10.1016/j.biocon.2015.04.023

Hoban S (2019). New guidance for ex situ gene conservation: Sampling realistic population systems and accounting for collection attrition. Biological Conservation 235:199-208. https://doi.org/10.1016/j.biocon.2019.04.013

Hoban S, Callicrate T, Clark J, Deans S, Dosmann M, Fant J, … Griffith MP (2020). Taxonomic similarity does not predict necessary sample size for ex situ conservation: a comparison among five genera. Proceedings of the Royal Society B: Biological Sciences 287(1926):20200102 https://doi.org/10.1098/rspb.2020.0102

Husband BC, Campbell LG (2004). Population responses to novel environments: Implications for ex situ plant conservation. In: Guerrant EO, Havens K, Maunder M (Eds). Ex situ Plant Conservation: Supporting Species Survival in the Wild. Island Press, Washington pp 231-285.

Hyvärinen MT (2020). Rubus humulifolius rescued by narrowest possible margin, conserved ex situ, and reintroduced in the wild. Journal for Nature Conservation 55:125819. https://doi.org/10.1016/j.jnc.2020.125819

IUCN (2020). The IUCN red list of threatened species. Version 2020-1. Retrieved 2021 January 17 from https://www.iucnredlist.org

Kallow S, Trivedi C (2017). Collecting genetic variation on a small island. In: Sniezko RA, Man G, Hipkins V, Woeste K, Gwaze D, Kliejunas JT, McTeague BA (Eds). Proceedings of Workshop: Gene Conservation of Tree Species-Banking on the Future. May 16-19. Gen. Tech. Rep. PNW-GTR-963. US Department of Agriculture, Forest Service, Pacific Northwest Research Station, pp 129-136.

Kovács Zs, Barabás S, Csontos P, Höhn M, Honfi P (2019). Az óriás útifű (Plantago maxima Juss. ex Jacq.) ex situ védelembe vonása II. Élőhelypreferencia-vizsgálat [Ex situ protection of the giant plantain (Plantago maxima Juss. ex Jacq.) II. Habitat preference studies]. Botanikai Közlemények 106(2):157-172. http://doi.org/10.17716/BotKozlem.2019.106.2.157

Lande R (1994). Risk of population extinction from fixation of new deleterious mutations. Evolution 48:1460-1469. https://doi.org/10.1111/j.1558-5646.1994.tb02188.x

Lauterbach D, Burkart M, Gemeinholzer B (2012). Rapid genetic differentiation between ex situ and their in situ source populations: an example of the endangered Silene otites (Caryophyllaceae). Botanical Journal of the Linnean Society 168(1):64-75. https://doi.org/10.1111/j.1095-8339.2011.01185.x

Lesica P, Allendorf FW (1995). When are peripheral populations valuable for conservation? Conservation Biology 9(4):753-760. https://doi.org/10.1046/j.1523-1739.1995.09040753.x

Li BJ, Wang JY, Liu ZJ, Zhuang XY, Huang JX (2018). Genetic diversity and ex situ conservation of Loropetalum subcordatum, an endangered species endemic to China. BMC Genetics 19:12. https://doi.org/10.1186/s12863-018-0599-6

Li DZ, Pritchard HW (2009). The science and economics of ex situ plant conservation. Trends in Plant Science 14(11):614-621. https://doi.org/10.1016/j.tplants.2009.09.005

Li Q, Xu Z, He T (2002). Ex situ genetic conservation of endangered Vatica guangxiensis (Dipterocarpaceae) in China. Biological Conservation 106(2):151-156. https://doi.org/10.1016/S0006-3207(01)00240-3

Liu U, Cossu TA, Davies RM, Forest F, Dickie JB, Breman E (2020). Conserving orthodox seeds of globally threatened plants ex situ in the Millennium Seed Bank, Royal Botanic Gardens, Kew, UK: the status of seed collections. Biodiversity and Conservation 29:2901-2949. https://doi.org/10.1007/s10531-020-02005-6

Lozada-Gobilard S, Pánková H, Zhu J, Stojanova B, Münzbergová Z (2020). Potential risk of interspecific hybridization in ex situ collections. Journal for Nature Conservation 58:125912. https://doi.org/10.1016/j.jnc.2020.125912

Marler TE, Lindstrom AJ (2020). Leaf nutrients of two Cycas L. species contrast among in situ and ex situ locations. Journal of Threatened Taxa 12(13):16831-16839. https://doi.org/10.11609/jott.6205.12.13.16831-16839

Marshall DR, Brown AHD (1975). Optimum sampling strategies in genetic conservation. In: Frankel OH, Hawkes JG (Eds). Crop Genetic Resources for Today and Tomorrow. Cambridge University Press, Cambridge pp 53-80.

Marshall DR (1989). Limitations to the use of germplasm collections. In: Brown AHD, Frankel OH, Marshall DR, Williams JT (Eds). The Use of Plant Genetic Resources. Cambridge University Press, Cambridge pp 105-120.

Maunder M, Higgens S, Culham A (2001). The effectiveness of botanic garden collections in supporting plant conservation: a European case study. Biodiversity and Conservation 10:383-401. https://doi.org/10.1023/A:1016666526878

Maunder M, Havens K, Guerrant EO, Falk DA (2004). Ex situ methods: A vital but underused set of conservation resources. In: Guerrant EO, Havens K, Maunder M (Eds). Ex situ Plant Conservation: Supporting Species Survival in the Wild. Island Press, Washington pp 3-20.

Miao YC, Su JR, Zhang ZJ, Lang XD, Liu WD, Li SF (2015). Microsatellite markers indicate genetic differences between cultivated and natural populations of endangered Taxus yunnanensis. Botanical Journal of the Linnean Society 177(3):450-461. https://doi.org/10.1111/boj.12249

Mounce R, Smith P, Brockington S (2017). Ex situ conservation of plant diversity in the world’s botanic gardens. Nature Plants 3(10):795-802. http://doi:10.1038/s41477-017-0019-3

MSBP (2015). Seed Conservation Standards for ‘MSB Partnership Collections’. Retrieved 2021 May 08 from http://brahmsonline.kew.org/Content/Projects/msbp/resources/Training/MSBP-Seed-Conservation-Standards.pdf

Namoff S, Husby CE, Francisco-Ortega J, Noblick LR, Lewis CE, Griffith MP (2010). How well does a botanical garden collection of a rare palm capture the genetic variation in a wild population? Biological Conservation 143(5):1110-1117. https://doi.org/10.1016/j.biocon.2010.02.004

Németh A, Makra O (2011). A tartós szegfű (Dianthus diutinus) ex situ védelme - esettanulmány [Ex situ conservation of long-lasting pink (Dianthus diutinus) – case study] In: Verő Gy (Eds). Természetvédelem és kutatás a Duna-Tisza közi homokhátságon. Rosalia 6. kötet. Duna-Ipoly Nemzeti Park Igazgatóság, Budapest pp 353-380. https://fuveszkert.u-szeged.hu/images/kutatasok/dianthus_Rosaliacikk.pdf

Nonić M, Šijačić-Nikolić M (2019) Genetic diversity: sources, threats, and conservation. In: Leal Filho W, Azul A, Brandli L, Özuyar P, Wall T (Eds). Life on Land. Encyclopedia of the UN Sustainable Development Goals. Springer, Cham. https://doi.org/10.1007/978-3-319-71065-5_53-1

O’Donnell K, Sharrock S (2017). The contribution of botanic gardens to ex situ conservation through seed banking. Plant Diversity 39(6):373-378. https://doi.org/10.1016/j.pld.2017.11.005

Peregrym MM, Kónya EP, Bezsmertna O (2019). Artificial light at night as a new threat for the efficiency of ex situ plant conservation. Conference paper. Conference: 1st International Scientific Conference “Advances and Perspectives of Biodiversity Research and Conservation in Georgia” (May 20-22, 2019, Tbilisi, Georgia). https://doi.org/10.13140/RG.2.2.16500.19842

Petit RJ, El Mousadik A, Pons O (1998). Identifying populations for conservation on the basis of genetic markers. Conservation Biology 12 (4):844-855. https://doi.org/10.1111/j.1523-1739.1998.96489.x

Pineda B, Hidalgo R, Debouck D, Mejía M (2007). Multi-institutional distance learning course on the ex situ conservation of plant genetic resources. Centro Internacional de Agricultura Tropical. CIAT. Cali, Colombia pp 205-216. ISBN 9789586940948 Retrieved 2021 January 09 from https://cgspace.cgiar.org/bitstream/handle/10568/54187/c_ex_situ.pdf?sequence=1&isAllowed=y

Pogorzelec M, Bronowicka-Mielniczuk U, Serafin A, Parzymies M (2020). The importance of habitat selection for the reintroduction of the endangered Salix lapponum L. in eastern Poland. Journal for Nature Conservation 54:125785. https://doi.org/10.1016/j.jnc.2020.125785

Prasse R, Kunzmann D, Schröder R (2010). Entwicklung und praktische umsetzung naturschutzfachlicher mindestanforderungen an einen herkunftsnachweis für gebietseigenes wildpflanzensaatgut krautiger pflanzen abschlussbericht. Deutsche bundesstiftung umwelt. [Development and practical implementation of nature conservation requirements for a certificate of origin for native wild plant seeds of herbaceous plants Final report. German Federal Foundation Environment] Retrieved 2021 January 09 from https://www.dbu.de/OPAC/ab/DBUAbschlussbericht-AZ-23931.pdf

Rauschkolb R, Szczeparska L, Kehl A, Bossdorf O, Scheepens JF (2019). Plant populations of three threatened species experience rapid evolution under ex situ cultivation. Biodiversity and Conservation 28:3951-3969. https://doi.org/10.1007/s10531-019-01859-9

Reyes-Valdés MH, Burgueño J, Singh S, Martínez O, Sansaloni CP (2018). An informational view of accession rarity and allele specificity in germplasm banks for management and conservation. PLoS One 13(2):e0193346 https://doi.org/10.1371/journal.pone.0193346

Rucińska A, Puchalski J (2011). Comparative molecular studies on the genetic diversity of an ex situ garden collection and its source population of the critically endangered polish endemic plant Cochlearia polonica E. Fröhlich. Biodiversity and Conservation 20(2):401-413. https://doi.org/10.1007/s10531-010-9965-z

Schaal B, Leverich WJ (2004). Population genetic issues in ex situ plant conservation. In: Guerrant EO, Havens K, Maunder M(Eds). Ex situ Plant Conservation: Supporting Species Survival in The Wild. Island Press, Washington pp 267-285.

Schoen DJ, Brown AHD (2001). The conservation of wild plant species in seed banks: attention to both taxonomic coverage and population biology will improve the role of seed banks as conservation tools. BioScience 51(11):960-966. https://doi.org/10.1641/0006-3568(2001)051[0960:TCOWPS]2.0.CO;2

Schröder R, Prasse R (2013). Cultivation and hybridization alter the germination behavior of native plants used in revegetation and restoration. Restoration Ecology 21(6):793-800. https://doi.org/10.1111/rec.12018

Silva AR, Resende-Moreira LC, Carvalho CS, Lanes ECM, Ortiz-Vera MP, Viana PL, Jaffé R (2020). Range-wide neutral and adaptive genetic structure of an endemic herb from Amazonian Savannas. AoB Plants 12(1). https://doi.org/10.1093/aobpla/plaa003

Solberg SO, Yndgaard F, Palmè A (2015). Morphological and phenological consequences of ex situ conservation of natural populations of red clover (Trifolium pratense L.). Plant Genetic Resources 15(02):97-108. https://doi.org/10.1017/S1479262115000416

Tang R, Li Y, Xu Y, Schinnerl J, Sun W, Chen G (2019). In-situ and ex situ pollination biology of the four threatened plant species and the significance for conservation. Biodiversity and Conservation 29(2):381-391. https://doi.org/10.1007/s10531-019-01887-5

Thompson PA (1974). The use of seed-banks for conservation of populations of species and ecotypes. Biological Conservation 6(1):15-19. https://doi.org/10.1016/0006-3207(74)90036-6

Tong YW, Durka W, Zhou WM, Zhou L, Yu DP, Dai LM (2020). Ex situ conservation of Pinus koraiensis can preserve genetic diversity but homogenizes population structure. Forest Ecology and Management 465:117820. https://doi.org/10.1016/j.foreco.2019.117820

Vitt P, Havens K (2004). Integrating quantitative genetics into ex situ conservation and restoration practices. In: Guerrant EO, Havens K, Maunder M (Eds.). Ex situ Plant Conservation: Supporting Species Survival in the Wild. Island Press, Washington pp 286-305.

Volis S (2017). Conservation utility of botanic garden living collections: setting a strategy and appropriate methodology. Plant Diversity 39(6):365-372. https://doi.org/10.1016/j.pld.2017.11.006

Volis S, Blecher M (2010). Quasi in situ: a bridge between ex situ and in situ conservation of plants. Biodiversity and Conservation 19(9):2441-2454. https://doi.org/10.1007/s10531-010-9849-2

Vrieling K, Saumitou-Laprade P, Cuguen PJ, van Dijk H, de Jong TJ, Klinkhamer PGL (1999). Direct and indirect estimates of the selfing rate in small and large individuals of the bumblebee pollinated Cynoglossum officinale L. (Boraginaceae). Ecology Letters 2:331-337. https://doi.org/10.1046/j.1461-0248.1999.00093.x

Wei X, Jiang M (2020). Meta-analysis of genetic representativeness of plant populations under ex situ conservation in contrast to wild source populations. Conservation Biology 35(1):12-23. https://doi.org/10.1111/cobi.13617

Wilson WD, Hutchinson JT, Ostrand KG (2017). Genetic diversity assessment of in situ and ex situ Texas wild rice (Zizania texana) populations, an endangered plant. Aquatic Botany 136:212-219. https://doi.org/10.1016/j.aquabot.2015.12.005

World Conservation Monitoring Centre (1998). Dipteryx alata. The IUCN Red List of Threatened Species. e.T32984A9741012. Retrieved 2021 January 17 from https://dx.doi.org/10.2305/IUCN.UK.1998.RLTS.T32984A9741012.en

Xiao YE, Jin D, Jiang K, Hu YH, Tong X, Mazer SJ, Chen XY (2019). Pollinator limitation causes sexual reproductive failure in ex situ populations of self-compatible Iris ensata. Plant Ecology and Diversity 12(1):21-35. https://doi.org/10.1080/17550874.2019.1569170

Yao XH, Ye QG, Kang M, Huang HW (2005). Geographic distribution and current status of the endangered genera Sinojackia and Changiostyrax. Biodiversity Science 13:339-346. https://doi.org/10.1360/biodiv.050059

Zhang JJ, Ye QG, Yao XH, Huang HW (2010). Spontaneous interspecific hybridization and patterns of pollen dispersal in ex situ populations of a tree species (Sinojackia xylocarpa) that is extinct in the wild. Conservation Biology 24(1):246-55. https://doi.org/10.1111/j.1523-1739.2009.01357.x

Zhao Y, Noltie H, Mathew B (2000). Iridaceae. Flora of China 24:297-313.

Published
2021-06-21
How to Cite
KOVÁCS, Z., CSERGŐ, A. M., CSONTOS, P., & HÖHN, M. (2021). Ex situ conservation in botanical gardens – challenges and scientific potential preserving plant biodiversity . Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(2), 12334. https://doi.org/10.15835/nbha49212334
Section
Review Articles
CITATION
DOI: 10.15835/nbha49212334