[en] The reintroduction of plant species is a technique increasingly used to restore extirpated populations. Although most often used to improve the conservation status of endangered species, it can also be considered for species extinct in the wild. The process of resurrecting extinct plant species is however still in its infancy, and it entails additional challenges compared to the reintroduction of locally extinct populations. This study proposes a framework to analyse constraints to post-extinction recovery based on the case of Bromus bromoideus, a species endemic to southern Belgium and northern France, extinct in the wild since 1935. The plant still exists in ex situ collections, and seeds stored for decades at 5% moisture content and -20 °C have shown a good viability. We initiated a feasibility study to assess the risks associated to a programme aiming at reviving this long-extinct species. Several constraints were identified. Biological constraints are related to the fuzzy taxonomy of the species, the unknown origin of the seeds and undocumented ex situ cultivation, and the likely low genetic diversity of the material available for reintroduction. Ecological constraints are linked to the habitat of the species. B. bromoideus has no known natural habitat and is only found in cultivated fields, which are by definition highly anthropized unprotected areas. This study shows the importance of undertaking a preliminary study that addresses all aspects of technical feasibility, scientific justification, biological and societal risks. Based on this exercise and inspired by international standards, we developed a decision tool to assist conservationists to resurrect a plant species in the best possible way.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Godefroid, Sandrine
Piqueray, Julien
Delescaille, Louis-Marie
Monty, Arnaud ; Université de Liège - ULiège > Département GxABT > Biodiversité et Paysage
Mahy, Grégory ; Université de Liège - ULiège > Département GxABT > Biodiversité et Paysage
Language :
English
Title :
A framework to identify constraints to post-extinction recovery of plant species—Application to the case of Bromus bromoideus
Publication date :
2020
Journal title :
Journal for Nature Conservation
ISSN :
1617-1381
eISSN :
1618-1093
Publisher :
Elsevier, Netherlands
Special issue title :
Frankenstein's work or everyday conservation? Examining plant de-extinction in practice
Abeli, T., Dalrymple, S., Godefroid, S., Mondoni, A., Müller, J., Rossi, G., et al. Ex situ plant collections and their potential for restoration of genetic diversity back to the wild. Conservation Biology, 2020, 10.1111/cobi.13391 Early view.
Ainouche, M.L., Bayer, R.J., On the origins of the tetraploid Bromus species (section Bromus, Poaceae): Insights from internal transcribed spacer sequences of nuclear ribosomal DNA. Genome 40 (1997), 730–743.
Akeroyd, J., Wyse Jackson, P., A handbook for botanic gardens on the reintroduction of plants to the wild. 1995, BGCI, Richmond.
Albrecht, H., Cambecèdes, J., Lang, M., Wagner, M., Management options for the conservation of rare arable plants in Europe. Botany Letters 8107 (2016), 1–27.
Barrett, S.C.H., Kohn, J.R., Genetic and evolutionary consequences of small population size in plants: Implications for conservation. Falk, D.A., Holsinger, K.E., (eds.) Genetics and conservation of rare plants, 1991, Oxford University Press, New York, 3–30.
Brütting, C., Hensen, I., Wesche, K., Ex situ cultivation affects genetic structure and diversity in arable plants. Plant Biology 15 (2013), 505–513.
Commander, L.E., Coates, D., Broadhurst, L., Offord, C.A., Makinson, R.O., Matthes, M., Guidelines for the translocation of threatened plants in Australia. 3rd ed., 2018, Australian Network for Plant Conservation., Canberra.
Dalrymple, S.E., Banks, E., Stewart, G.B., Pullin, A.S., A meta-analysis of threatened plant reintroductions from across the globe. Maschinski, J., Haskins, K.E., (eds.) Plant reintroduction in a changing climate – Promises and perils, 2012, Island Press, Washington, 31–52.
de Cugnac, A., Les Jardins botaniques et la conservation des espèces rares. A propos de Bromus arduennensis Dmrt., Liste de 35 jardins où B. arduennensis (= f. arduennensis) a été cultivé. Bulletin du Muséum national d'histoire naturelle 2 (1936), 286–289.
de Cugnac, A., Le brome des Ardennes – l’étonnante carrière d'une espèce rare des confins ardennais. Bulletin de la Société des Naturalistes luxembourgeois 58 (1954), 38–75.
Delescaille, L.M., Piqueray, J., Godefroid, S., Le statut du brome épais (Bromus grossus) en Région Wallonne. Adoxa 69:70 (2011), 1–14.
Ensslin, A., Sandner, T.M., Matthies, D., Consequences of ex situ cultivation of plants: Genetic diversity, fitness and adaptation of the monocarpic Cynoglossum officinale L. in botanic gardens. Biological Conservation 144 (2011), 272–278.
Ensslin, A., Tschöpe, O., Burkart, M., Joshi, J., Fitness decline and adaptation to novel environments in ex situ plant collections: Current knowledge and future perspectives. Biological Conservation, 192(394), 2015, 401.
Ensslin, A., Van de Vyver, A., Vanderborght, T., Godefroid, S., Ex situ cultivation entails high risk of seed dormancy loss on short-lived wild plant species. The Journal of Applied Ecology 55 (2018), 1145–1154.
Falk, D.A., Millar, C., The influence of climate variability and change on the science and practice of restoration ecology. Palmer, M.A., Zedler, J.B., Falk, D.A., (eds.) Foundations of restoration ecology, 2016, Island Press, Washington, 484–513.
Falk, D.A., Constance, I., Millar, C.I., Olwell, M., Guidelines for developing a rare plant reintroduction plan. Falk, D.A., Millar, C.I., Olwell, M., (eds.) Restoring diversity: Strategies for reintroduction of endangered plants, 1996, Island Press, Washington, 453–490.
Glémin, S., Mating systems and the efficacy of selection at the molecular level. Genetics 177 (2007), 905–916.
Godefroid, S., Van de Vyver, A., Stoffelen, P., Robbrecht, E., Vanderborght, T., et al. Testing the viability of seeds from old herbarium specimens for conservation purposes. Taxon 60 (2011), 565–569.
Godefroid, S., Vanderborght, T., Plant reintroductions: The need for a global database. Biodiversity and Conservation 20 (2011), 3683–3688.
Godefroid, S., Piazza, C., Rossi, G., Buord, S., Stevens, A.D., Aguraiuja, R., et al. How successful are plant species reintroductions?. Biological Conservation 144 (2011), 672–682.
Gorbunov, Y.N., Dzybov, D.S., Kuzmin, Z.E., Smirnov, I.A., Methodological recommendations for botanic gardens on the reintroduction of rare and threatened plants. 2008, Grif & Co, Tula.
GPPC, Plant conservation report. A review of progress in implementing the global strategy for plant conservation (GSPC)., 2008, Global Partnership for Plant Conservation, Dublin.
Grime, J.P., Brown, V.K., Thompson, K., Masters, G.J., Hiller, S.H., Clarke, I.P., et al. The response of two contrasting limestone grasslands to simulated climate change. Science 289 (2000), 762–765.
Havens, K., Guerrant, E.O., Maunder, M., Vitt, P., Guidelines for ex situ conservation collection management. Minimizing risks. Guerrant, E.O., Havens, K., Maunder, M., (eds.) Ex situ plant conservation: Supporting species survival in the wild, 2004, Island Press, Washington, 454–473.
Husband, B.C., Schemske, D.W., Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50 (1996), 54–70.
IUCN/SSC, Guidelines for reintroductions and other conservation translocations. Version 1.0. 2013, IUCN/SSC, Gland.
IUCN/SSC, IUCN SSC guiding principles on creating proxies of extinct species for conservation benefit. Version 1.0. 2016, IUCN Species Survival Commission, Gland.
Jauzein, P., Flore des champs cultivés. 1995, INRA, Paris.
Kennedy, K.L., The role of federal guidance and state and federal partnership in ex situ plant conservation in the United States. Guerrant, E.O., Havens, K., Maunder, M., (eds.) Ex situ plant conservation: Supporting species survival in the wild, 2004, Island Press, Washington, 67–83.
Koch, M.A., Meyer, N., Engelhardt, M., Thiv, M., Morphological and genetic variation of highly endangered Bromus species and the status of these Neolithic weeds in Central Europe. Plant Systematics and Evolution 302 (2016), 515–525.
Lambinon, J., Verloove, F., Nouvelle Flore de la Belgique, du Grand-Duché de Luxembourg, du Nord de la France et des Régions voisines (Ptéridophytes et Spermatophytes). 6th ed., 2012, Jardin botanique national de Belgique, Meise.
Lang, M., Prestele, J., Fischer, C., Kollmann, J., Albrecht, H., Reintroduction of rare arable plants by seed transfer. What are the optimal sowing rates?. Ecology and Evolution 6 (2016), 5506–5516.
Lauterbach, D., Burkart, M., Gemeinholzer, B., 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 (2012), 64–75.
Lawrence, M.J., A comprehensive collection and regeneration strategy for ex situ conservation. Genetic Resources and Crop Evolution 49 (2002), 199–209.
Lawrence, B.A., Kaye, T.N., Reintroduction of Castilleja levisecta: Effects of ecological similarity, source population genetics, and habitat quality. Restoration Ecology 19 (2011), 166–176.
Leimu, R., Mutikainen, P., Koricheva, J., Fischer, M., How general are positive relationships between plant population size, fitness and genetic variation?. The Journal of Ecology 94 (2006), 942–952.
Lemoine, C., Sérusiaux, E., Mahy, G., Piqueray, J., Agro-environmental scheme for segetal plant conservation in Wallonia (Belgium): An assessment in conventional and organic fields. Biotechnology, Agronomy, Society and Environment 22 (2018), 35–44.
Liu, H., Ren, H., Liu, Q., Wen, X.Y., Maunder, M., Gao, J.Y., Translocation of threatened plants as a conservation measure in China. Conservation Biology 29 (2015), 1537–1551.
Maréchal, A., Note sur Bromus arduennensis Dmrt. et sur le rôle des jardins botaniques dans la conservation des espèces rares. Bulletin de la Société royale de Botanique de Belgique 70 (1937), 51–58.
Maschinski, J., Albrecht, M.A., Center for plant conservation's best practice guidelines for the reintroduction of rare plants. Plant Diversity 39 (2017), 390–395.
Maschinski, J., Haskins, K.E., Plant reintroduction in a changing climate. Promises and perils. 2012, Island Press, Washington.
Maslovat, C., Guidelines for translocation of plant species at risk in British Columbia. 2009, Ministry of Environment, Victoria.
Maunder, M., Culham, A., Bordeu, A., Allainguillaume, J., Wilkinson, M., Genetic diversity and pedigree for Sophora toromiro (Leguminosae): A tree extinct in the wild. Molecular Ecology 8 (1999), 725–738.
Morgan, M.T., Consequences of life history for inbreeding depression and mating system evolution in plants. Proceedings of the Royal Society of London Series B-Biological Sciences 268 (2001), 1817–1824.
Piqueray, J., Gilliaux, V., Gaillard, T., Mahy, G., Delescaille, L.M., Uncleaned crop seed sowing as a tool to conserve Bromus grossus and restore species-rich arable-dependent plant communities. Conservation Evidence, 15, 2018, 26.32.
Prasse, R., Kunzmann, D., Schröder, R., Entwicklung und praktische Umsetzung naturschutzfachlicher Mindestanforderungen an einen Herkunftsnachweis für gebietseigenes Wildpflanzensaatgut krautiger Pflanzen Abschlussbericht. 2010, Institut für Umweltplanung, Hannover.
Püschel, T.A., Espejo, J., Sanzana, M.J., Benítez, H.A., Analysing the floral elements of the lost tree of Easter Island: A morphometric comparison between the remaining ex-situ lines of the endemic extinct species Sophora toromiro. PloS One, 9(12), 2014, e115548, 10.1371/journal.pone.0115548.
Reed, D.H., Relationship between population size and fitness. Conservation Biology 19 (2005), 563–568.
Royal Botanic Gardens Kew, Seed information database (SID). Version 7.1. 2019 http://data.kew.org/sid/.
Rucińska, A., Puchalski, J., 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 (2011), 401–413.
Schoen, D.J., Brown, A.H.D., The conservation of wild plant species in seed banks. BioScience 51 (2001), 960–966.
Scholz, H., Zur Systematik der Gatung Bromus L. subg. Bromus (Graminae). Willdenowia 6 (1970), 139–160.
Sharrock, S., Jones, M., Conserving Europe's threatened plants: Progress towards target 8 of the global strategy for plant conservation. 2009, Botanic Gardens Conservation International, Richmond.
Smith, P.M., Observations on some critical Brome grasses. Watsonia 9 (1973), 319–332.
SPW, Evolution de l’économie agricole et horticole de la Région wallonne 2008-2009. 2009, Service Public de Wallonie, Département de l'Etude du Milieu naturel et agricole, Jambes.
SPW, Evolution de l’économie agricole et horticole de la Wallonie. 2019, Service Public de Wallonie, Département de l'Etude du Milieu naturel et agricole, Jambes.
Storkey, J., Meyer, S., Still, K.S., Leuschner, C., The impact of agricultural intensification and land-use change on the European arable flora. Proceedings of the Royal Society B Biological Sciences 279 (2012), 1421–1429.
Thompson, K., Bakker, J., Bekker, R., The soil seed bank of North West Europe: Methodology, density and longevity. 1997, Cambridge University Press, Cambridge.
Thomson, F.J., Moles, A.T., Auld, T.D., Kingsford, R.T., Seed dispersal distance is more strongly correlated with plant height than with seed mass. The Journal of Ecology 99 (2011), 1299–1307.
Tournay, R., Le Brome des Ardennes, “Bromus arduennensis” et ses proches, B. secalinus et B. grossus. Bulletin du Jardin botanique national de Belgique 38 (1968), 295–379.
Vergeer, P., van den Berg, L.J.L., Roelofs, J.G.M., Ouborg, N.J., Single-family versus multi-family introductions. Plant Biology 7 (2005), 509–515.
Walker, K.J., Hodder, K.H., Bullock, J.B., Pywell, R.F., A review of the potential effects of seed sowing for habitat re-creation on the conservation of intraspecific biodiversity. Defra Contract BD1447. 2004, Centre for Ecology and Hydrology, Monks Wood.
