Abstract
Botanic gardens and arboreta, particularly in regions where iconic relict trees naturally occur, play a vital role in the conservation of these species. Maintaining well-managed living ex situ collections of rare and threatened relict tree species provides an immediate insurance policy for the future species conservation. The aim of this research was to investigate the origin, representativeness and genetic diversity of relict trees kept in botanic gardens and arboreta. We used as a model two ecologically and biogeographically distinct members of the prominent relict genus Zelkova (Ulmaceae), which survived the last glaciation in disjunct and isolated refugial regions: Z. carpinifolia in Transcaucasia and Z. abelicea endemic to Crete (Greece) in the Mediterranean. Our study revealed substantial differences in the genetic diversity and the origin of living ex situ collections of the two investigated taxa. The living ex situ collections of Z. carpinifolia have relatively high representativeness compared with the global genetic variability of natural stands identified in a previous study. In contrast, Z. abelicea, which possesses an extraordinarily high genetic variability in natural populations, is clearly underrepresented in botanic garden collections. Moreover, all Z. abelicea trees investigated in this study most probably originated from a single region, the Levka Ori in western Crete. Thus, the ex situ conservation of Z. abelicea requires major planning and coordination efforts, including the establishment of well-documented collections in botanic gardens in Greece and especially on Crete. New living ex situ collections should be created using plant material collected from all of the mountain regions where Z. abelicea still occurs. Our study highlights the need for re-evaluating the existing living ex situ collections of trees and the development of new strategies for future conservation efforts in botanic gardens and arboreta. The coordination of conservation efforts between gardens must be enhanced to prioritize actions for the most threatened relict tree species.
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References
Bandelt HJ, Foster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Barriel V (1994) Phylogénies moléculaires et insertions-délétions de nucléotides. C R Acad Sci Paris 317:693–701
BGCI (Botanic Gardens Conservation International) (2010) Global survey of ex situ Zelkova collections. http://www.bgci.org/files/survey-zelkova.pdf. Accessed 28 Nov 2013
Bosque M, Adamogianni MI, Bariotakis M, Fazan L, Stoffel M, Garfì G, Gratzfeld J, Kozlowski G, Pirintsos S (2014) Fine-scale spatial patterns of the Tertiary relict Zelkova abelicea (Ulmaceae) indicate possible processes contributing to its persistence to climate changes. Reg Environ Change 14:835–849
Browicz K, Zielinski J (1982) Chorology of trees and shrubs in south-west Asia and adjacent regions. Polish Academy of Sciences, Institute of Dendrology, Bogucki Wydawnictwo Naukowe, Poznan
Brown AHD, Marshall DR (1995) A basic sampling strategy: theory and practice. In: Gaurino L, Gaurino L, Ramanatha Rao V, Reid R, Reid R (eds) Collecting plant genetic diversity: technical guidelines. CAB International, Wallingford, pp 75–91
Burnham RJ (1986) Foliar morphological analysis of the Ulmoideae (Ulmaceae) from the early Tertiary of western North America. Palaeontogr Abt B 201:135–167
Caetano S, Naciri Y, Naciri Y (2011) The biogeography of seasonally dry tropical forests in South America. In: Dirzo R, Young HS, Mooney HA, Mooney HA, Ceballos G (eds) Seasonally dry tropical forests: ecology and conservation. Island Press, Stanford, pp 23–44
CBD (Convention on Biological Diversity) (2011) Updated global strategy for plant conservation 2011–2020. http://www.cbd.int. Accessed 15 Dec 2013
Chaw S-M, Parkinson CL, Cheng Y, Vincent TM, Palmer DJ (2000) Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms, and origin of Gnetales from conifers. Proc Nat Acad Sci USA 97:4086–4091
Christe C, Kozlowski G, Frey D, Bétrisey S, Maharramova E, Garfì G, Pirintsos S, Naciri Y (2014) Footprints of past intensive diversification and structuring in the genus Zelkova (Ulmaceae) in south-western Eurasia. J Biogeogr 41:1081–1093
Cohen JI, Williams JT, Plucknett DL, Shands H (1991) Ex situ conservation of plant genetic resources: global development and environmental concerns. Science 253:866–872
Connor SE (2009) Human impact—the last nail in the coffin for ancient plants? J Biogeogr 36:485–486
Del Tredici J, Ling H, Yang G (1992) The Ginkgos of Tian Mu Shan. Conserv Biol 6:202–209
Denk T, Grimm GW (2005) Phylogeny and biogeography of Zelkova (Ulmaceae sensu stricto) as inferred from leaf morphology, ITS sequence data and the fossil record. Bot J Linn Soc 147:129–157
Di Pasquale G, Garfì G, Quezél P (1992) Sur la présence d’un Zelkova nouveau en Sicile sudorientale (Ulmaceae). Biocosme Mésogéen 8–9:401–409
Donaldson JS (2009) Botanic gardens science for conservation and global change. Trends Plant Sci 14:608–613
Egli B (1995) Zelkova abelicea (Lam.) Boiss. In: Phitos D, Strid A, Snogerup S, Greuter W (eds) The red data book of rare and threatened plants of Greece. Michalas K, WWF Greece, Athens, pp 526–527
Egli B (1997) A project for the preservation of Zelkova abelicea (Ulmaceae), a threatened endemic tree species from the mountains of Crete. Bocconea 5:505–510
Ensslin A, Sandner TM, Matthies D (2011) Consequences of ex situ cultivation of plants: genetic diversity, fitness and adaptation of the monocarpic Cynoglossum officinale L. in botanic gardens. Biol Conserv 144:272–278
Etisham-Ul-Haq M, Allnutt TR, Smith-Ramirez C, Gardner MF, Armesto JJ, Newton AC (2001) Patterns of genetic variation in and ex situ populations of the threatened Chilean vine Berberidopsis carollina, detected using RAPD markers. Ann Bot 87:813–821
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Fazan L, Stoffel M, Frey D, Pirintsos S, Kozlowski G (2012) Small does not mean young: age estimation of severely browsed trees in anthropogenic Mediterranean landscapes. Biol Conserv 153:97–100
Garfì G (2006) Zelkova sicula. IUCN red list of threatened species. Version 2013.2. http://www.iucnredlist.org. Accessed 28 Nov 2013
Garfì G, Carimi F, Pasta S, Rühl J, Trigila S (2011) Additional insights on the ecology of the relic tree Zelkova sicula di Pasquale, Garfì et Quézel (Ulmaceae) after the finding of new population. Flora 206:407–417
Güner A, Zielinski J (1998) Zelkova carpinifolia. IUCN red list of threatened species. Version 2013.2. http://www.iucnredlist.org. Accessed Nov 2013
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Kozlowski G, Gratzfeld J (2013) Zelkova—an ancient tree. Global status and conservation action. Natural History Museum Fribourg, Switzerland
Kozlowski G, Gibbs D, Fun H, Frey D, Gratzfeld J (2012a) Conservation of threatened relict trees through living ex situ collections: lessons from the global survey of the genus Zelkova (Ulmaceae). Biodivers Conserv 21:671–685
Kozlowski G, Frey D, Fazan L, Egli B, Pirintsos S (2012b) Zelkova abelicea. IUCN red list of threatened species. Version 2013.2. http://www.iucnredlist.org. Accessed 28 Nov 2013
Kozlowski G, Frey D, Fazan L, Egli B, Bétrisey S, Gratzfeld J, Garfì G, Pirintsos S (2014) Tertiary relict tree Zelkova abelicea (Ulmaceae): distribution, population structure and conservation status. Oryx 48:80–87
Kvavadze EV, Connor SE (2005) Zelkova carpinifolia (Pallas) K. Koch in Holocene sediments of Georgia—an indicator of climatic optima. Rev Palaeobot Palynol 133:69–89
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). Bot J Linn Soc 168:64–75
Ledig FT (1988) The conservation of diversity in forest trees. Why and how should genes be conserved? Bioscience 38:471–479
Li YY, Chen XY, Zhang X, Wu TY, Lu HP, Cai YW (2005) Genetic differences between wild and artificial populations of Metasequoia glyptostroboides: implications for species recovery. Conserv Biol 19:224–231
Magri D, Fineschi S, Bellarosa R, Buonamici A, Sebastiani F, Schirone B, Simeone MC, Vendramin CC (2007) The distribution of Quercus suber chloroplast haplotypes matches the paleogeographical history of the western Mediterranean. Mol Ecol 16:5259–5266
Mai DH (1995) Tertiäre vegetationsgeschichte Europas. Methoden und Ergebnisse, Gustav Fischer
Maunder M, Havens K, Guerrant EO Jr, Falk DA, Falk DA (2004) Ex situ methods: a vital but underused set of conservation resources. In: Guerrant EO Jr, Havens K, Maunder M (eds) Ex situ plant conservation. Supporting species survival in the wild. Island Press, Covelo, pp 3–20
Milne RI (2006) Northern Hemisphere plant disjunctions: a window on Tertiary land bridges and climate change? Ann Bot 98:465–472
Milne RI, Abbott RJ (2002) The origin and evolution of tertiary relict floras. Adv Bot Res 38:281–314
Namoff S, Husby CE, Francisco-Ortega J, Noblick LR, Lewis CE, Griffith MP (2010) How well does a botanic garden collection of rare palm capture the genetic variation in a wild population? Biol Conserv 143:1110–1117
Nei M (1973) Analysis of gene diversities in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323
Oldfield SF (2009) Botanic gardens and the conservation of tree species. Trends Plant Sci 14:581–583
Petit RJ, El-Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855
Petit RJ, Hampe A, Cheddadi R (2005) Climate change and tree phylogeography in the Mediterranean. Taxon 54:877–885
Phitos D, Strid A, Snogerup S, Greuter W (eds) (1995) The Red Data Book of rare and threatened plants of Greece. Michalas K, WWF Greece, Athens
Primack RB (2004) A primer of conservation biology, 3rd edn. Sinauer Associates, Inc Publishers, Sunderland
Quézel P, Médail F (2003) Ecologie et biogeography des forêts du bassin méditerranéen. Elsevier, Paris
Rodríguez-Sánchez F, Guzmán B, Valido A, Vargas P, Arroyo J (2009) Late Neogene history of the laurel tree (Laurus L., Lauraceae) based on phylogeographical analyses of Mediterranean and Macaronesian populations. J Biogeogr 36:1270–1281
Rucinska 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. Biodivers Conserv 20:401–413
Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RK (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 921:142–166
Søndergaard P, Egli BR (2006) Zelkova abelicea (Ulmaceae) in Crete: floristics, ecology, propagation and threats. Willdenowia 36:317–322
Taberlet P, Gielly L, Patou G, Bouvet J (1991) Universal primers for amplification of three noncoding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109
Trueman SJ, Pegg GS, King J (2007) Domestication for conservation of an endangered species: the case of the Wollemi Pine. Tree For Sci Biotech 1:1–10
Whitlock BA, HaleAM, Groff PA (2010) Intraspecific inversions pose a challenge for the trnH-psbA plant DNA barcode. PloS One 5(7):e11533. doi:10.1371/journal.pone.0011533
Wiegrefe SJ, Sytsma KJ, Guries RP (1998) The Ulmaceae, one family or two? Evidence from chloroplast DNA restriction site mapping. Plant Syst Evol 210:249–270
Wyse Jackson P, Kennedy K (2009) The Global Strategy for Plant Conservation: a challenge and opportunity for the international community. Trends Plant Sci 14:578–580
Yang RC, Yeh FC (1992) Genetic consequences if in situ and ex situ conservation of forest trees. Forest Chron 68:720–729
Zheng-Yi W, Raven PH (eds) (2003) Zelkova. Flora of China, Vol. 5. Ulmaceae–Basellaceae. Missouri Botanical Garden Press, St. Louis
Acknowledgments
We would like to thank B. Clément and S. Bollinger from the Botanical Garden of the University of Fribourg (Switzerland); E. Gerber and A. Fasel from the Natural History Museum Fribourg (Switzerland); M. Jafari (University of Teheran, Iran) and Y. Marbach, B. Egli and R. Keller (Switzerland) for their assistance during the manuscript preparation. We are indebted to the Franklinia Foundation for its generous support provided to undertake this study and to the City of Geneva, the Société Académique de Genève and the Prof. R. Spichiger (University of Geneva) for the funds they provided to buy a new automated sequencer. Special thanks go to D. Gibbs from Botanic Gardens Conservation International (BGCI), who coordinated the data and sample exchange, and to V. Ali-zade, E. Alirzayeva, E. Maharramova (Azerbaijan National Academy of Sciences), H. Safarov (Hyrcanian National Park), M. Khutsishvili (National Botanic Garden of Georgia, Tbilisi) for the field work coordination and sampling in Azerbaijan and Georgia. The permission to collect Z. abelicea plant material was granted by the Ministry of the Environment, General Directorate of Forests, Department of Aesthetic Forests, National Parks and Wildlife Management, Athens, Greece (199076/1843). Many botanic gardens and arboreta around the world provided samples for the present survey—their contributions are gratefully acknowledged: Arboretum Kórnickie, Poland; Aristotle University of Thessaloniki, Greece; Botanic Garden of the University of Poznan, Poland; Botanic Gardens of Adelaide, Australia; Botanische Gärten der Universität Bonn, Germany; Botanischer Garten der Universität Zürich, Switzerland; Botanischer Garten der Universität Bern, Switzerland; Botanischer Garten der Universität Freiburg, Switzerland; Conservatoire et Jardin botaniques de la Ville de Genève, Switzerland; Parc Floraire, Switzerland; Botanischer Garten und Botanisches Museum Berlin Dahlem, Germany; Cambridge University Botanic Garden, United Kingdom; Chicago Botanic Garden, United States of America; Garten der Johannes Gutenberg Universität Mainz, Germany; Jardí Botànic de Barcelona, Spain; Jardin Botanique de la Ville de Paris, Ecole du Breuil, France; Jardin Botanique de l’Université de Strasbourg, France; Jardins des Plantes et Arboretum de Chevreloup, France; Kutaisi Botanical Garden, Georgia; Morris Arboretum, United States of America; National Botanic Gardens of Ireland, Ireland; Royal Botanic Gardens, Kew, United Kingdom; Royal Veterinary and Agricultural University Arboretum, Denmark; Stichting Arboretum Wespelaar, Belgium; Syon Park, United Kingdom; The Dawes Arboretum, United States of America; The Royal Horticultural Society’s Garden, Wisley, United Kingdom; The Sir Harold Hillier Garden and Arboretum, United Kingdom; and Westonbirt Arboretum, United Kingdom.
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Christe, C., Kozlowski, G., Frey, D. et al. 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 . Biodivers Conserv 23, 2945–2959 (2014). https://doi.org/10.1007/s10531-014-0756-9
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DOI: https://doi.org/10.1007/s10531-014-0756-9