Abstract
The Alps played an important role in the biogeography of European plants and acted as a refugium for numerous species during the interglacial cycles. We investigated Nuphar pumila, one of the most emblematic glacial relicts of the Alps, by carrying out exhaustive literature and field surveys to collect relevant data on its distribution and threats. We further evaluated the level of introgression with the closely related N. lutea based on microsatellite data from natural populations across the Alps as well as from all ex situ collections and reintroductions in Switzerland. According to our results, more than 60% of the known N. pumila populations went extinct, and the species currently presents 37 natural populations in the investigated area. A large number of populations were affected by eutrophication (69%) and hybridization with N. lutea (53%). Priority should be given to the in situ conservation of genetically pure populations, while ex situ cultures should be applied to nearly extinct populations and the genetically pure individuals still present in hybrid populations. N. pumila is an excellent representative of the wetland/aquatic glacial relicts that are particularly affected by the combination of climate change and habitat degradation. International integration of research and conservation programs is needed to limit the decline of such rare species in the Alps.
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References
Aeschimann D, Luber K, Moser DM, Theurillat J-P (2004) Flora alpina, vol 1–3. Haupt Verlag, Bern
Allendorf F, Leary R, Spruell P, Wenburg J (2001) The problems with hybrids: setting conservation guidelines. Trend Ecol Evol 16:613–622
Anamthawat-Jonsson K, Thorsson AT (2003) Natural hybridisation in birch: triploid hybrids between Betula nana and B. pubescens. Plant Cell Tissue Org Cult 75:99–107
Arrigo N, Bétrisey S, Graf L, Bilat J, Gerber E, Kozlowski G (2016) Hybridization as a threat in climate relict Nuphar pumila (Nymphaeaceae). Biodivers Conserv 25:1863–1877
Bornand C, Gygax A, Juillerat P, Jutzi M, Möhl A, Rometsch S, Sager L, Santiago H, Eggenberg S (2016) Rote Liste Gefässpflanzen. Gefährdete Arten der Schweiz. Bundesamt für Umwelt, Bern und Info Flora, Genf. Umwelt-Vollzug Nr. 1621
Brochmann C, Gabrielsen TM, Nordal I, Landvik JY, Elven R (2003) Glacial survival or tabula rasa? The history of North Atlantic biota revisited. Taxon 52:417–450
Buerkle CA (2005) Maximum-likelihood estimation of a hybrid index based on molecular markers. Mol Ecol Notes 5:684–687
Cayouette J, Cattling PM (1992) Hybridization in the genus Carex with special reference to North America. Bot Rev 58:351–440
Chase WM, Hills HG (1991) Silica gel: an ideal material for field preservation of leaf samples for DNA studies. Taxon 40:215–220
Eidesen PB, Ehrich D, Bakkestuen V, Alsos IG, Gilg O, Taberlet P, Brochmann C (2013) Genetic roadmap of the Arctic: plant dispersal highways, traffic barriers and capitals of diversity. New Phytol 200:898–910
Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467
Hampe A, Jump AS (2011) Climate relicts: past, present, future. Annu Rev Ecol Evol 42:313–333
Heslop-Harrison Y (1953) Nuphar intermedia Lebed., a presumed relict hybrid in Britain. Watsonia 3:7–25
Heslop-Harrison Y (1955) Nuphar Sm. J Ecol 43:342–364
Holderegger R, Thiel-Egenter C (2009) A discussion of different types of glacial refugia used in mountain biogeography and phylogeography. J Biogeogr 36:476–480
Jadwiszczak KA, Jablonska E, Klosowski S, Banaszek A (2011) Aneuploids in the shrub birch Betula humilis populations in Poland. Acta Soc Bot Pol 80:233–235
Jadwiszczak KA, Drzymulska D, Banaszek A, Jadwiszczak P (2012) Population history, genetic variation and conservation status of the endangered birch species Betula nana L. in Poland. Silva Fenn 46:465–477
Käsermann CH, Moser DM (1999) Merkblätter Artenschutz, Blütenpflanzen und Farne. Bundesamt für Umwelt, Wald und Landschaft (BUWAL), Bern, Switzerland
Kozlowski G (2001) Une plante rarissime dans le canton de Fribourg: le Nénuphar nain [N. pumila (Timm.) DC.]. Bull Soc Frib Sc Nat 90:60–71
Kozlowski G, Eggenberg S (2005) Vorkommen der Kleinen Teichrose Nuphar pumila und des Hybrids N. × intermedia in der Schweiz. Bot Helv 115:125–136
Kulczynski S (1924) Das boreale und arktisch-alpine Element in der mitteleuropäischen Flora. Bull de l’Ac Pol d Sc Série B 3:127–214
Maiz-Tome L (2016) Nuphar pumila. The IUCN red list of threatened species 2016: e.T167888A1179645
Metzing D, Garve E, Matzke-Hajek G (2018) Rote Liste und Gesamtartenliste der Farn- und Blütenpflanzen (Trachaeophyta) Deutschlands. Bundesamt für Naturschutz. Naturschutz und Biologische Vielfalt 70:13–358
Meusel H, Mühlberg H, Fuchs HP (1965) Nymphaeaceae. In: Hegi G (ed) Illustrierte Flora von Mitteleuropa. Band III. Teil 3. Carl Hanser, München
Mikolajczak A, Ferrez Y (2005) Connaissance de la flore rare ou menacée de Franche-Comté, Nuphar pumila (Timm) DC., Conservatoire Botanique de Franche-Comté
Muller S (2006) Les plantes protégées de Lorraine. Distribution, écologie, conservation. Biotope, Mèze (collection Parthénope)
Natho G (1959) Variationsbreite und Bastardbildung bei mitteleuropäischen Birkensippen. Feddes Repert 61:211–273
Niklfeld H (1999) Rote Liste gefährdeter Pflanzen Österreichs. Grüne Reihe des Bundesministeriums für Umwelt Jugend und Familie. Band 10. Graz, Austria
Oberdorfer E (1977) Süddeutsche Pflanzengesellschaften Teil I. Zweite Auflage. Gustav Fischer, Stuttgart
Padgett DJ (1998) Phenetic distinction between the dwarf yellow water-lilies: Nuphar microphylla and N. pumila (Nymphaeaceae). Can J Bot 76:1755–1762
Padgett DJ (2007) A monograph of Nuphar (Nympheaceae). Rhodora 109:1–95
Padgett DJ, Les DH, Crow GE (1998) Evidence for the hybrid origin of Nuphar × rubrodisca (Nymphaeaceae). Am J Bot 85:1468–1476
Padgett DJ, Les DH, Crow GE (1999) Phylogenetic relationships in Nuphar (Nymphaeaceae): evidence from morphology, chloroplast DNA, and nuclear ribosomal DNA. Am J Bot 86:1316–1324
Padgett DJ, Shimoda M, Horky LA, Les DH (2002) Natural hybridization and the imperiled Nuphar of Western Japan. Aquat Bot 72:161–174
Paun O, Schönswetter P, Winkler M, Consortium I, Tribsch A (2008) Historical divergence vs. contemporary gene flow: evolutionary history of the calcicole Ranunculus alpestris group (Ranunculaceae) in the European Alps and the Carpathians. Mol Ecol 17:4263–4275
Reisch C (2001) Climatic oscillations and the fragmentation of plant populations—genetic diversity within and among populations of the glacial relict plants Saxifraga paniculata (Saxifragaceae) and Sesleria albicans (Poaceae). Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften der Naturwissenschaftlichen Fakultät III, Biologie und Vorklinische Medizin der Universität Regensburg
Ronikier M, Schneeweis GM, Schönswetter P (2012) The extreme disjunction between Beringia and Europe in Ranunculus glacialis sl. (Ranunculaceae) does not coincide with the deepest genetic split—a story of the importance of temperate mountain ranges in arctic-alpine phylogeography. Mol Ecol 21:5561–5578
Roweck H (1988) Ökologische Untersuchungen an Teichrosen. Archiv für Hydrobiologie. Schweizerbart'sche Verlagsbuchhandlung, Supplementband. 81 Heft 2/3. Nägele u. Obermiller. Stuttgart, Germany
Roweck H, Reinöhl H (1986) Zur Verbreitung und systematischen Abgrenzung der Teichrosen Nuphar pumila und N. × intermedia in Baden-Württemberg. Veröffentlichungen Landesstelle Naturschutz Baden-Württemberg 61:81–151
Schmitt T, Muster C, Schönswetter P (2010) Are disjunct alpine and arctic-alpine animal and plant species in the western Palearctic really “relics of the cold past”? In: Habel JC, Assman T (eds) Relict species: phylogeny and conservation biology. Springer, Berlin, pp 239–252
Schroeter C (1926) das Pflanzenleben der Alpen. Eine Schilderung der Hochgebirgsflora. Verlag Albert Raustein, Zürich
Shiga T, Kadono Y (2007) Natural hybridization of the two Nuphar species in northern Japan: homoploid hybrid speciation in progress? Aquat Bot 86:123–131
Shiga T, Kadono Y (2008) Genetic relationships of Nuphar in central to western Japan as revealed by allozyme analysis. Aquat Bot 88:105–112
Stehlik I (2003) Resistance or emigration? Response of alpine plants to the ice ages. Taxon 52:499–510
Stehlik I, Blattner FR, Holderegger R, Bachmann K (2002) Nunatak survival of the high Alpine plant Eritrichium nanum (L.) Gaudin in the central Alps during the ice ages. Mol Ecol 11:2027–2036
Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464
Thorn K (1960) Bemerkungen zu einer Übersichtskarte vermutlicher Glazialreliktpflanzen Deutschlands. Mitteilungen der Floristisch-Soziologischen Arbeitsgemeinschaft 8:81–85
Tribsch A, Schönswetter P (2003) Patterns of endemism and comparative phylogeography confirm palaeoenvironmental evidence for Pleistocene refugia in the eastern Alps. Taxon 52:477–497
Varga ZS, Schmitt T (2008) Types of oreal and oreotundral disjunctions in the western Palearctic. Biol J Linn Soc 93:415–430
Volkova PA, Arutyunyan NG, Schanzer IA, Chemeris EV, Bobrov AA (2018) Genetic variability of Eurasian Nuphar species unravels possible routes in which freshwater plants could fill their wide areas. Aquat Bot 145:49–57
Walter H, Straka H (1970) Arealkunde. Floristisch-historische Geobotanik. Verlag Eugen Ulmer, Stuttgart
Wangerin W (1932) Florenelemente und Arealtypen. Beih Bot Zentralbl 49:515–566
Welk E (2001) Arealkundliche Analyse und Bewertung der Schutzrelevanz seltener und gefährdeter Gefässpflanzen Deutschlands. Dissertation zur Erlangung des Doktorgrades vorgelegt an der Mathematisch-Naturwissenschaftlich-Technischen Fakultät der Martin-Luther-Universität Halle-Wittenberg
Windmaisser T, Kattari S, Heubl G, Reisch C (2016) Glacial refugia and postglacial expansion of the alpine-prealpine plant species Polygala chamaebuxus. Ecol Evol 6:7809–7819
Winkler M, Tribsch A, Schneeweis GM, Brodbeck S, Gugerli F, Holderegger R, Abbott RJ, Schönswetter P (2012) Tales of the unexpected: phylogeography of the arctic-alpine model plant Saxifraga oppositifolia (Saxifragaceae) revisited. Mol Ecol 21:4618–4630
Woolbright SA, Whitham TG, Gering CA, Allan GJ, Bailey JK (2014) Climate relicts and their associated communities as natural ecology and evolution laboratories. Trends Ecol Evol 29:406–416
Zimmermann M, Vischer-Leopold M, Ellwanger G, Ssymak A, Schröder E (2010) The EU habitat directive and the German Natura 200 network of protected areas as tool for implementing the conservation of relict species. In: Habel JC, Assman T (eds) Relict species: phylogeny and conservation biology. Springer, Berlin, pp 323–340
Acknowledgements
We are grateful to the following persons and institutions for their precious help, collaboration and/or issue of permissions: Switzerland—Botanical Gardens of St-Gall, Zürich, Geneva, Lausanne and Fribourg; Benoît Clément, Botanical Garden of the University of Fribourg; Marius Achermann and Francesca Cheda, Service de la Nature et du paysage de l’Etat de Fribourg; Dr. Andreas Keel, Amt für Landschaft- und Naturschutz, Kanton Zürich; Claudia Huber, UNA, Bern; Rolf Heeb and Christian Peisker, Kantonsschule Wattwil; Luca Champoud and Valentine Kam, Collège du Sud, La Frasse; François Genoud, Auberge du Lac des Joncs, Les Paccots; Coordination régionale pour la protection de la flore (FR-GE-NE-VD); Dr. Stephan Eggenberg, Info Flora. France—Eric Brugel and Julien Guyonneau, Conservatoire botanique national de Franche-Comté; Sophie Daucourt, Direction Régionale de l’Environnement, de l’Aménagement et du Logement de Franche-Comté (DREAL); Alain David, Office National de l’Eau et des Milieux Aquatiques (ONEMA); Alain Piot, Hôtel et lac de l’Abbaye, Grande-Rivière; owners of the pond Bachetey, Haute-Saône. Austria—Michaela Messner, Bezirkshauptmannschaft Reutte; municipalities of Grän and Nesselwängle, Tirol. Germany—Günter Riegel, Regierungsbezirk Schwaben; Dr. Klaus Neugebauer, Regierungsbezirk Oberbayern; Hans Lampartner, Regierungspräsidium Tübingen; Bertrand Schmidt, Landratsamt Ravensburg; Dr. Ulrich Weiland, Zweckverband Allgäuer Moorallianz; Dr. Stephanie Socher, Bayerischen Landesamt für Umwelt in Augsburg; Naturpark Südschwarzwald; Sigrid Rossiwal, Regierung von Oberbayern, Uwe Grabner, Starnberg; Josef Kunsler, Bad Endorf; NSG Eggstätt-Hemhofer Seenplatte; Bernadette Zimmermann, Regierungspräsidium Freiburg. We thank the Natural History Museum Fribourg (Switzerland) and the Fonds de recherche of the University of Fribourg (Switzerland, Project number 516) for their logistic and financial support. Nils Arrigo was funded by an SNSF Ambizione research Grant (PZ00P3_148224).
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GK and SB developed the research ideas; SB, LG, and EG collected the data and samples; NA and JB carried out molecular analyses; SB, NA, and GK analyzed the data and led the writing of the manuscript.
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Bétrisey, S., Arrigo, N., Graf, L. et al. Glacial relicts in the Alps: the decline and conservation strategy for Nuphar pumila (Nymphaeaceae). Alp Botany 130, 89–99 (2020). https://doi.org/10.1007/s00035-020-00232-9
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DOI: https://doi.org/10.1007/s00035-020-00232-9