Abstract
Key message
Ancestral halophytic traits such as salt glands and leaf deciduousness have facilitated the adaptation of Myricaria germanica to non-saline calcium-rich soils.
Abstract
Myricaria germanica is a scale-leaved, deciduous shrub from the Tamaricaceae, a salt gland family of halophytes, xerophytes and rheophytes usually from xeric, saline areas. Atypically, the genus Myricaria is usually from mesic, non-saline areas. In this study, we describe the shoot morphology and anatomy of seedlings and adult plants of Myricaria germanica in order to explore its adaptation to the environment. It is a species of montane to subalpine-flooded riverine areas on non-saline limestone and dolomite soils. The adult leaves show strong leaf reduction but no other significant xeromorphic or scleromorphic features. While the salt glands of most Tamaricaceae secrete NaCl, our SEM EDS investigations show that Myricaria germanica secretes large amounts of Ca and Mg, probably as CaSO4 and as Mg-containing CaCO3, rather than NaCl. This suggests that the evolution of salt glands in a halophytic ancestor may have been an enabling trait that facilitated the adaptation of Myricaria germanica to non-saline Ca-rich soils. Because leaf deciduousness can also be an adaptation for reduction of plant NaCl content, the same may apply to this Myricaria germanica trait. Similarly, leaf reduction can evolve as a response to osmotic stress in saline areas. Its persistence in Myricaria germanica may no longer have any adaptational significance. Our work highlights the dichotomy of the stress-tolerant family Tamaricaceae into two types of stressful habitats, one lowland (e.g. Tamarix) and one montane to alpine (Myricaria). Similar range fragmentation is known in Mediterranean taxa like Armeria and Astragalus.
Similar content being viewed by others
References
Albert R (1975) Salt regulation in halophytes. Oecologia 21:57–71
Bachmann J (1997) Ökologie und Verbreitung der Deutschen Tamariske (Myricaria germanica Desv.) in Südtirol und deren pflanzensoziologische Stellung. Diploma-thesis, University of Vienna
Beadle NCW (1966) Soil phosphate and its role in molding segments of the Australian flora and vegetation with special reference to xeromorphy and sclerophylly. Ecology 47:992–1007
Berry WL (1970) Characteristics of salts secreted by Tamarix aphylla. Am J Bot 57: 1226–1230
Bill HC, Spahn P, Reich M (1997) Bestandsveränderung und Besiedlungsdynamik der Deutschen Tamariske, Myricaria germanica (L.) Desv., an der oberen Isar (Bayern). Z Ökol Naturschutz 6: 137–150
Blondel J, Aronson J, Bodiou J-Y, Boeuf G (2010) Biological diversity in space and time, 2nd edn. Oxford University Press, Oxford
Blum A (1996) Crop responses to drought and the interpretation of adaptation. Plant Growth Regul 20:135–148
Blum A, Arkin GF (1984) Sorghum root growth and water use as affected by water supply and growth duration. Field Crop Res 9:131–142
Bosabalidis AM, Kofidis G (2002) Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci 163: 375–379
Brunswik H (1920) Über das Vorkommen von Gipskristallen bei Tamaricaceae. Sitzungsberichte der Akademie d wiss math-naturw Klasse Abt I 129:115–139
Carlquist S (2010) Caryophyllales: a key group for understanding wood anatomy character states and their evolution. Bot J Linn Soc 164:342–393
Clode PL, Marshall AT (2003) Skeletal microstructure of Galaxea fascicularis: a high resolution SEM study. Biol Bull 204:146–154
Conti E, Soltis DE, Hardig TM, Schneider J (1999) Phylogenetic relationships of Silver Saxifrages (Saxifraga, Sect. Ligulatae): implications for the evolution of substrate, specification, life histories, and biogeography. Mol Phylogen Evol 13:536–555
De Laubenfels DJ (1953) The external morphology of coniferous leaves. Phytomorphology 3:1–20
Dörken VM (2013) Leaf dimorphism in Thuja plicata and Platycladus orientalis (thujoid Cupressaceae s. str., Coniferales): the changes in morphology and anatomy from juvenile needle leaves to mature scale leaves. Plant Syst Evol 299:1991–2001
Dörken VM (2014) Leaf-morphology and leaf-anatomy in Ephedra altissima Desf. (Ephedraceae, Gnetales) and their evolutionary relevance. Feddes Repert 123: 243–255
Dörken VM, Jagel A (2014) Pinus sylvestris—Wald-Kiefer (Pinaceae), Baum des Jahres 2007. Jahrb Bochumer Bot Ver 5: 246–254
Dörken VM, Parsons R (2016) Morpho-anatomical studies on the change in the foliage of two imbricate-leaved New Zealand podocarps: Dacrycarpus dacrydioides and Dacrydium cupressinum. Plant Syst Evol 302:41–54
Dörken, VM, Parsons R (2017) Morpho-anatomical studies on the leaf reduction in Casuarina: the ecology of xeromorphy. Trees (in press)
Dörken VM, Stützel T (2011) Morphology and anatomy of anomalous cladodes in Sciadopitys verticillata Siebold & Zucc. (Sciadopityaceae). Trees (Berlin) 25: 199–213
Düll R, Kutzelnigg H (2011) Taschenlexikon der Pflanzen Deutschlands und angrenzender Länder, 7th edn. Quelle and Meyer, Wiebelsheim
Eckenwalder JE (2009) Conifers of the world. Timber Press, Portland
eFloras (2008) Missouri botanical garden, Harvard University Herbaria, Cambridge. http://www.efloras.org (cited 08.09.2016)
Egger G, Steineder R, Angermann K (2014) Erhebung und Bewertung der Deutschen Tamariske (FFH Lebensraumtyp 3230 Alpine Flüsse mit Ufergehölzen von Myricaria germanica) an der Isel und deren Zubringern Tauernbach, Schwarzach und Kalserbach Teil I. eb&p Umweltbüro GmbH, Klagenfurt. pp. 1–57
Endress PK (1975) Der Verbreitungsrückgang von Myricaria germanica Desv. und Typha minima Hoppe auf der Alpennordseite Graubündens. Vierteljahrsschr Naturforsch Ges Zürich 120: 1–14
Evert RF (2006) Esau’s plant anatomy, 3rd edn. Wiley, New York
Fahn A, Cutler D (1992) Xerophytes. Bornträger, Berlin
Faraday CD, Thomson WW (1986) Functional aspects of the salt glands of the Plumbaginaceae. J Exp Bot 37:1129–1135
Farjon A (2005) A monograph of Cupressaceae and Sciadopitys. Royal Botanic Gardens, Kew
Farjon A (2010a) A handbook of the world´s conifers, vol. I. Brill, Leiden
Farjon A (2010b) A handbook of the world´s conifers, vol. II. Brill, Leiden
Feustel H (1921) Anatomie und Biologie der Gymnospermenblätter. Beih Bot Centralbl 38: 177–253
Fitting H (1950) Weitere Beobachtungen über die Induktion der Dorsiventralität in den blattartigen Zweigsystemen von Cupressaceen. Planta 37:676–696
Foster AS, Gifford EM (1974) Comparative morphology of vascular plants, 2nd edn. Freeman, San Francisco
Gaskin JF (2003) Tamaricaceae. In: Kubitzki K, Bayer C (eds) The families and genera of vascular plants, vol 5. Springer, Berlin, pp 336–338
Gerlach D (1984) Botanische Mikrotomtechnik, eine Einführung, 2nd edn. Thieme, Stuttgart
Gladfelter EH (1983) Skeletal development in Acropora cervicornis. II. Diel patterns of calcium carbonate accretion. Coral Reefs 2:91–100
Hanson AD, Rathinasabapathi B, Rivoal J, Burnet M, Dillon MO, Douglas AG (1994) Osmoprotective compounds in the Plumbaginaceae: a natural experiment in metabolic engineering of stress tolerance. Proc Natl Acad Sci USA 91:306–310
Hardion L, Dumas PJ, Abdel-Samad F, Kharrat MBD, Surina B, Affre L, Medail F, Bacchetta G, Baumel A (2016) Geographical isolation caused diversification in the Mediterranean thorny cushion-like Astragalus L. sect. Tragacantha DC (Fabaceae) Mol Phylogen Evol 97: 187–195
Hegi G (1975) Illustrierte Flora von Mittel-Europa. vol 5(1). Carl Hanser-Verlag, München
Heywood VH (1982) Blütenpflanzen der Welt. Birkhäuser, Basel
Hidaka M (1991) Deposition of fusiform crystals without apparent diurnal rhythm at the growing edge of septa of the coral Galaxea fascicularis. Coral Reefs 10:41–45
Hill RS (1998) Fossil evidence for the onset of xeromorphy and scleromorphy in Australian Proteaceae. Aust Syst Bot 11: 391–400
Hill RS, Merrifield HE (1993) An early Tertiary macroflora from West Dale, southwestern Australia. Alcheringa 17:285–326
Imamura SL (1937) Über die aitiogene Dorsiventralität der Assimilationsorgane bei höheren Pflanzen. Bot Mag (Tokyo) 61: 308–316
Kadukova J, Manousaki E, Kalogerakis N (2008) Pb and Cd accumulation and phyto-excretion by salt cedar (Tamarix smyrnensis Bunge). Int J Phytoremed 10:31–46
Kammerer H (2003) Artenschutzprojekt Deutsche Tamariske: Möglichkeiten und Aussichten einer Wiederansiedelung von Myricaria germanica im Gesäuse. Stipa-Technisches Büro für Ökologie (Auftraggeber: Nationalpark Gesäuse GmbH). Graz, pp. 1–29
Kiermeier P (1993) Wildgehölze des mitteleuropäischen Raums, BdB Handbuch Teil VIII. Fördergesellschaft “Grün ist Leben” Baumschulen mbH, Pinneberg
Köhlein F (1980) Saxifragen und andere Steinbrechgewächse. Ulmer, Stuttgart
Korner C (2003) Alpine plant life, 2nd edn. Springer, Berlin
Krüssmann G (1976) Handbuch der Laubgehölze, vol. 1, 2nd edn. Parey, Berlin
Krüssmann G (1977) Handbuch der Laubgehölze, vol 2, 2nd edn. Parey, Berlin
Krüssmann G (1978) Handbuch der Laubgehölze, vol. 3, 2nd edn. Parey, Berlin
Krüssmann G (1983) Handbuch der Nadelgehölze, 2nd edn. Parey, Berlin
Kubitzki K (2004) The families and genera of vascular plants. vol 6, flowering plants, Dicotyledons: Celastrales, Oxidales, Rosales, Cornales, Ericales. Springer, Berlin
Kubitzki K, Rohwer JG, Bittrich V (1993) The families and genera of vascular plants. vol 2, flowering plants, Dicotyledons: Magnoliid, Hamamelid and Caryophylloid families. Springer, Berlin
Kudrnovsky H (2002) Die Deutsche Tamariske an der Isle. Ergebnisse der Kartierung im Auftrag des österreichischen Alpenvereins, Fachabteilung Raumplanung und Naturschutz. Innsbruck. pp. 1–25
Langner W (1963) Die Entstehung sogenannter Jugendformen bei Chamaecyparis. Silvae Genet 13: 57–63
Lener FP (2011) Etablierung und Entwicklung der Deutschen Tamariske (Myricaria germanica) an der oberen Drau in Kärnten. Diploma-thesis, University of Vienna
Liu Y, Wang Y, Huang H (2009) Species-level phylogeographical history of Myricaria plants in the mountain ranges of western China and the origin of M. laxiflora in Three Gorges mountain region. Mol Ecol 18: 2700–2712
Loveless AR (1961) A nutritional interpretation of sclerophylly based on differences in the chemical composition of sclerophyllous and mesophytic leaves. Ann Bot (Oxford) 25: 168–184
Loveless AR (1962) Further evidence to support a nutritional interpretation of sclerophylly. Ann Bot (Oxford) 26: 551–561
Mabberley DJ (2008) Mabberley’s plant book, 3rd edn. University Press, Cambridge
Marschner H, Marschner P (2012) Marschner´s mineral nutrition of higher plants, 3rd edn. Academic Press, London
Moor M (1958) Pflanzengesellschaften Schweizer Flussauen. Mitt Schweiz Anstalt Forstl Versuchswesen 34: 221–360
Moray C, Goolsby EW, Bromham L (2016) The phylogenetic association between salt tolerance and heavy metal hyperaccumulation in angiosperms. Evol Biol 43:119–130
Müller N (1988) Zur Flora und Vegetation des Lechs bei Forchach (Reutte-Tirol)—letzte Reste nordalpiner Wildflußlandschaften. Natur Landschaft 63: 263–269
Müller N (1991) Exkursionsführer Lechtal. Hoppea 50: 685–700
Müller N (1993) Biotopbrücke Lech. Gart Landschaft 103: 45–48
Müller N (1995a) River dynamics and floodplain vegetation and their alterations due to human impact. Arch Hydrobiol Suppl 101. Large Rivers 9:477–512
Müller N (1995b) Wandel von Flora und Vegetation nordalpiner Wildflusslandschaften unter dem Einfluss des Menschen. Ber ANL 19: 125–187
Müller N, Bürger A (1990) Flußmorphologie und Auenvegetation des Lechs im Bereich der Forchacher Wildflußlandschaft (Oberes Lechtal, Tirol). Jahrb d Ver zum Schutz der Bergwelt 55: 123–154
Napp-Zinn K (1966) Anatomie des Blattes. I. Blattanatomie der Gymnospermen. Bornträger, Berlin
Parsons RF (2010) Whipcord plants: a comparison of south-eastern Australia with New Zealand. Cunninghamia 11:277–281
Petutschnig W (1994) Die Deutsche Tamariske (Myricaria germanica (L.) Desv.) in Kärnten. Carinthia II 104:19–30
Ramadan T (1998) Ecophysiology of salt excretion in the xero-halophyte Reaumuria hirtella. New Phytol 139:273–281
Rozema J, Gude H, Pollak G (1981) An ecophysiological study of the salt secretion of four halophytes. New Phytol 89:201–217
Saenger P (2002) Mangrove ecology, silviculture and conservation. Kluwer, Dordrecht
Sakai WS (1974) Scanning electron microscopy and energy dispersive X-ray analysis of chalk secreting leaf glands of Plumbago capensis. Am J Bot 61: 94–99
Salama FM, El-Naggar SM, Ramadan T (1999) Salt glands of some halophytes in Egypt. Phyton 39: 91–105
Salleo S, Nardini A (2000) Sclerophylly: evolutionary advantage or mere epiphenomenon? Plant Biosyst 134: 247–259
Salmon JT (1986) A field guide to the native trees of New Zealand. Reed Methuen, Auckland
Scassellati G, Pasqua G, Valletta A, Abbate G (2016) Salt glands of Armeria canescens (Host.) Boiss.: morphological and functional aspects. Plant Biosyst 150: 1134–1139
Schälchli U, Abegg J, Hunziger L (2001) Fachbericht Trübung, Strömung, Geschiebetrieb und Kolmation. - in: Internationale Regierungskommission Alpenrhein, Projektgruppe Gewässer und Fischökologie: Trübung und Schwall Alpenrhein. Zürich. pp. 1–101
Schmidt H (1930) Zur Funktion der Hydathoden von Saxifraga. Planta 10:314–344
Schneider W (1913) Vergleichend-morphologische Untersuchung über die Kurztriebe einiger Arten von Pinus. Flora 105:30–40
Seddon G (1974) Xerophytes, xeromorphs and sclerophylls: the history of some concepts in ecology. Biol J Linn Soc 6: 65–87
Seidling W, Ziche D, Beck W (2012) Climate responses and interrelations of stem increment and crown transparency in Norway Spruce, Scots Pine and Common Beech. Forest Ecol Manag 284: 196–204
Storey R, Thomson WW (1994) An X-ray microanalysis study of the salt glands and intracellular calcium crystals ofTamarix. Ann Bot (Oxford) 73:307–313
Strasburger E (1872) Die Coniferen und Gnetaceen, Textband. Abel, Leipzig, pp. 382–390
Tetzlaf M (2005) Die Anatomie des Gymnospermenblattes unter funktionellen und evolutiven Gesichtspunkten. Diploma. Ruhr-University, Bochum
Webb DA, Gornall RJ (1989) Saxifrages of Europe. Helm, London
Zhang ML, Meng HH, Zhang HX, Vyacheslav BV, Sanderson SC (2014) Himalayan origin and evolution of Myricaria (Tamaricaeae) in the Neogene. PLoS One 9(6):e9758
Zohlen A, Tyler G (2004) Soluble inorganic tissue phosphorus and calcicole-calcifuge behaviour of plants. Ann Bot (Oxford) 94: 427–432
Acknowledgements
We are grateful to Mr. Otmar Ficht and Mrs. Anne Kern (Botanic Garden, University of Konstanz, Germany) for producing the seedlings. Furthermore, we thank the Botanic Garden of the Eberhard Karls Universität Tübingen (Germany) for providing research material; the “Amt für Natur, Jagd und Fischerei” (Kanton St. Gallen, Switzerland) for the special permission to collect material in the natural habitat; Dr. Michael Laumann and Mrs. Lauretta Nejedli (Electron Microscopy Center, Department of Biology, University of Konstanz, Germany) for technical support (paraffin technique and SEM). Finally, we thank Dr. Volker Hellmann for his helpful discussions and our field-trips to M. germanica in the northern Alps and Dr. N.C. Uren (Department of Animal, Plant and Soil Sciences, LaTrobe University, Australia) for helpful discussions and advice concerning soil properties.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by K. Masaka.
Rights and permissions
About this article
Cite this article
Dörken, V.M., Parsons, R.F. & Marshall, A.T. Studies on the foliage of Myricaria germanica (Tamaricaceae) and their evolutionary and ecological implications. Trees 31, 997–1013 (2017). https://doi.org/10.1007/s00468-017-1523-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-017-1523-9