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Nitrogen cycling and storage in Gagea spathacea (Liliaceae): ecological insights for protecting a rare woodland species

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Abstract

Strategies to globally protect biological diversity are often hampered by an insufficient ecological knowledge about target species. This also applies to Gagea spathacea (Liliaceae), a ‘vulnerable’ woodland spring geophyte with a distribution largely restricted to the lowlands of Central Europe. We studied whether the species’ linkage to highly fertile forest soils is related to its high nitrogen (N) demands during its short developmental cycle. We hypothesized that the species exhibits a highly efficient N (re)cycling strategy, characterized by efficient resorption of N from the leaves and reallocation to bulbs at the end of the growing season. To test this assumption, we conducted a 15N tracer experiment and quantified 15N flows between soil, leaves, bulbs, and roots. Our findings support our hypothesis that G. spathacea is exceptionally efficient in recycling N, shown by the resorption of 68% of leaf N and its reallocation to bulbs at the end of the growing season. After 6 weeks of growth the plant showed a distinct shift in its N metabolism: The C:N ratio of leaves strongly increased and those of bulbs decreased, leaf 15N enrichment and recovery started to decrease, while total plant 15N recovery remained constant, indicating no further N uptake from the soil. Leaf N reallocation to bulbs was accompanied by a twofold increase of the bulbs’ biomass. Because of the stenoecious behaviour of G. spathacea, a careful protection and sustainable management of G. spathacea forest habitats is necessary, particularly in its Central European core area.

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References

  • Aerts R (1990) Nutrient use efficiency in evergreen and deciduous species from heathlands. Oecologia 84:391–397

    Article  PubMed  Google Scholar 

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Aerts R (1999) Interspecific competition in natural plant communities: mechanisms, trade-offs and plant-soil feedbacks. J Exp Bot 50:29–37

    Article  CAS  Google Scholar 

  • Bähring A, Fichtner A, Friedrich U, von Oheimb G, Härdtle W (2017) Bryophytes and organic layers control uptake of airborne nitrogen in low-N environments. Front Plant Sci 8:2080

    Article  PubMed  PubMed Central  Google Scholar 

  • Balmford A, Bennun L, ten Brink B, Cooper D, Cote IM, Crane P, Dobson A, Dudley N, Dutton I, Green RE, Gregory RD, Harrison J, Kennedy ET, Kremen C, Leader-Williams N, Lovejoy TE, Mace G, May R, Mayaux P, Morling P, Phillips J, Redford K, Ricketts TH, Rodriguez JP, Sanjayan M, Schei PJ, van Jaarsveld AS, Walther BA (2005) The convention on biological diversity’s 2010 target. Science 307:212–213

    Article  CAS  PubMed  Google Scholar 

  • Beisenova S, Peterson A, Peterson J, Bersimbaev RI, Klahr A, Schnittler M (2015) On the limits of drought—life history of Gagea bulbifera (Liliaceae). Flora 210:72–79

    Article  Google Scholar 

  • Betts MG, Wolf C, Ripple WJ, Phalan B, Millers KA, Duarte A, Butchart SHM, Levi T (2017) Global forest loss disproportionately erodes biodiversity in intact landscapes. Nature 547:441–444

    Article  CAS  PubMed  Google Scholar 

  • Bilgin A, Guzel S (2017) Foliar resorption and nutrient changes in leaves of Tilia rubra ssp. caucasica (Linden) along an altitudinal gradient during the growing season. Fresenius Environ Bull 26:1607–1621

    CAS  Google Scholar 

  • Boerner REJ (1984) Foliar nutrient dynamics and nutrient use efficiency of four deciduous tree species in relation to soil fertility. J Appl Ecol 21:1029–1040

    Article  Google Scholar 

  • Chandra A, Idrisova A (2011) Convention on Biological Diversity: a review of national challenges and opportunities for implementation. Biodivers Conserv 20:3295–3316

    Article  Google Scholar 

  • Chaytor B, Gerster R, Herzog T (2002) The Convention on Biological Diversity—exploring the creation of a mediation mechanisms. J World Intellect Prop 5:157–180

    Article  Google Scholar 

  • Coplen TB, Krouse HR, Böhlke JK (1992) Reporting of nitrogen-isotope abundances. Pure Appl Chem 64:907–908

    Article  Google Scholar 

  • Diekmann M, Härdtle W, Stoltenberg K (2014) Verbreitung und Ökologie des Scheiden-Gelbsterns (Gagea spathacea). Abhandlungen des Naturwissenschaftlichen Vereins zu Bremen 47:355–365

    Google Scholar 

  • Ellenberg H, Weber HE, Düll R, Wirth V, Werner W, Paulissen D (1992) Zeigerwerte von Pflanzen in Mitteleuropa. Scr Geobot 18:1–248

    Google Scholar 

  • Estiarte M, Peñuelas J (2015) Alteration of the phenology of leaf senescence and fall in winter deciduous species by climate change: effects on nutrient proficiency. Glob Change Biol 21:1005–1017

    Article  Google Scholar 

  • Fang YT, Koba K, Makabe A, Takahashi C, Zhu WX, Hayashi T, Hokari AA, Urakawa R, Bai E, Houlton BZ, Xi D, Zhang SS, Matsushita K, Tu Y, Liu DW, Zhu FF, Wang ZY, Zhou GY, Chen DX, Makita T, Toda H, Liu XY, Chen QS, Zhang DQ, Li YD, Yoh M (2015) Microbial denitrification dominates nitrate losses from forest ecosystems. Proc Natl Acad Sci USA 112:1470–1474

    Article  CAS  PubMed  Google Scholar 

  • Friedrich U, Falk K, Bahlmann E, Marquardt T, Meyer H, Niemeyer T, Schemmel S, von Oheimb G, Hardtle W (2011) Fate of airborne nitrogen in heathland ecosystems: a 15 N tracer study. Glob Change Biol 17:1549–1559

    Article  Google Scholar 

  • Friedrich U, von Oheimb G, Kriebitzsch WU, Schlesselmann K, Weber MS, Hardtle W (2012) Nitrogen deposition increases susceptibility to drought—experimental evidence with the perennial grass Molinia caerulea (L.) Moench. Plant Soil 353:59–71

    Article  CAS  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • Goberville E, Hautekeete NC, Kirby RR, Piquot Y, Luczak C, Beaugrand G (2016) Climate change and the ash dieback crisis. Sci Rep 6:35303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Martinez SC, Krutovsky KV, Neale DB (2006) Forest-tree population genomics and adaptive evolution. New Phytol 170:227–238

    Article  PubMed  Google Scholar 

  • Gove B, Power SA, Buckley GP, Ghazoul J (2007) Effects of herbicide spray drift and fertilizer overspread on selected species of woodland ground flora: comparison between short-term and long-term impact assessments and field surveys. J Appl Ecol 44:374–384

    Article  CAS  Google Scholar 

  • Haeupler H, Muer T (2000) Bildatlas der Farn- und Blütenpflanzen Deutschlands. Ulmer, Stuttgart

    Google Scholar 

  • Härdtle W, von Oheimb G, Westphal C (2003) The effects of light and soil conditions on the species richness of the ground vegetation of deciduous forests in northern Germany (Schleswig-Holstein). For Ecol Manag 182:327–338

    Article  Google Scholar 

  • Hofmeister J, Hosek J, Brabec M, Dvorak D, Beran M, Deckerova H, Burel J, Kriz M, Borovicka J, Betak J, Vasutova M (2014) Richness of ancient forest plant species indicates suitable habitats for macrofungi. Biodiv Conserv 23:2015–2031

    Article  Google Scholar 

  • Joppa LN, Visconti P, Jenkins CN, Pimm SL (2013) Achieving the Convention on Biological Diversity’s goals for plant conservation. Science 341:1100–1103

    Article  CAS  PubMed  Google Scholar 

  • Keith DA (1998) An evaluation and modification of World Conservation Union Red List criteria for classification of extinction risk in vascular plants. Conserv Biol 12:1076–1090

    Article  Google Scholar 

  • Keith DA, Akcakaya HR, Thuiller W, Midgley GF, Pearson RG, Phillips SJ, Regan HM, Araujo MB, Rebelo TG (2008) Predicting extinction risks under climate change: coupling stochastic population models with dynamic bioclimatic habitat models. Biol Lett 4:560–563

    Article  PubMed  PubMed Central  Google Scholar 

  • Kjaer ED (2017) Introduction Part 2. Consequences of ash dieback: damage level, resistance and resilience of European ash forests. Baltic For 23:141–143

    Google Scholar 

  • Krause EHL (1889) Geographische Übersicht der Flora von Schleswig-Holstein. Petermanns Geogr Mitt 6:114–115

    Google Scholar 

  • Leuschner C, Ellenberg H (2017) Ecology of central European forests (vegetation ecology of central Europe), vol 1. Springer, Berlin

    Book  Google Scholar 

  • Levichev IG, Tuniyev BS, Timukhin IN (2010) On the origin of Gagea spathacea (Liliaceae) in the Flora of the Caucasus. Bot Zh 95:464–482

    Google Scholar 

  • McNeill AM, Hood RC, Wood M (1994) Direct measurement of nitrogen fixation by Trifolium repens L. and Alnus glutinosa L. using 15N. J Exp Bot 45:749–755

    Article  CAS  Google Scholar 

  • Meusel H, Jäger E, Weinert E (1965) Vergleichende Chorologie der zentraleuropäischen Flora. Fischer, Jena

    Google Scholar 

  • Millard P (1996) Ecophysiology of the internal cycling of nitrogen for tree growth. Z Pflanzen Bodenk 159:1–10

    Article  CAS  Google Scholar 

  • Millard P, Proe MF (1992) Storage and internal cycling of nitrogen in relation to seasonal growth of sitka spruce. Tree Physiol 10:33–43

    Article  CAS  PubMed  Google Scholar 

  • Mitchell RJ, Beaton JK, Bellamy PE, Broome A, Chetcuti J, Eaton S, Ellis CJ, Gimona A, Harmer R, Hester AJ, Hewison RL, Hodgetts NG, Iason GR, Kerr G, Littlewood NA, Newey S, Potts JM, Pozsgai G, Ray D, Sim DA, Stockan JA, Taylor AFS, Woodward S (2014) Ash dieback in the UK: a review of the ecological and conservation implications and potential management options. Biol Conserv 175:95–109

    Article  Google Scholar 

  • Mölder A, Schmidt M, Schönfelder E, Engel F, Schulz F (2015) Bryophytes as indicators of ancient woodlands in Schleswig-Holstein (Northern Germany). Ecol Indic 54:12–30

    Article  Google Scholar 

  • Nadelhoffer KJ, Colman BP, Currie WS, Magill A, Aber JD (2004) Decadal-scale fates of 15N tracers added to oak and pine stands under ambient and elevated N inputs at the Harvard Forest (USA). For Ecol Manag 196:89–107

    Article  Google Scholar 

  • Niinemets U, Tamm U (2005) Species differences in timing of leaf fall and foliage chemistry modify nutrient resorption efficiency in deciduous temperate forest stands. Tree Physiol 25:1001–1014

    Article  PubMed  Google Scholar 

  • Pautasso M, Aas G, Queloz V, Holdenrieder O (2013a) Dieback of European ash: let’s avoid this kind of opportunities for nature conservation. Biol Conserv 167:452–453

    Article  Google Scholar 

  • Pautasso M, Aas G, Queloz V, Holdenrieder O (2013b) European ash (Fraxinus excelsior) dieback—a conservation biology challenge. Biol Conserv 158:37–49

    Article  Google Scholar 

  • Peruzzi L, Peterson A, Tison JM, Harpke D (2011) New light on phylogeny and taxonomy of the Eurasian Gagea villosa-G. fragifera complex (Liliaceae). Nord J Bot 29:722–733

    Article  Google Scholar 

  • Peterson A, John H, Koch E, Peterson J (2004) A molecular phylogeny of the genus Gagea (Liliaceae) in Germany inferred from non-coding chloroplast and nuclear DNA sequences. Plant Syst Evol 245:145–162

    Article  CAS  Google Scholar 

  • Peterson A, Harpke D, Peruzzi L, Levichev IG, Tison JM, Peterson J (2009) Hybridization drives speciation in Gagea (Liliaceae). Plant Syst Evol 278:133–148

    Article  CAS  Google Scholar 

  • Peterson A, Levichev IG, Peterson J, Harpke D, Schnittler M (2011) New insights into the phylogeny and taxonomy of Chinese species of Gagea (Liliaceae)-speciation through hybridization. Org Divers Evol 11:387–407

    Article  Google Scholar 

  • Petzold R, Schwärzel K, Feger KH (2011) Transpiration od a hybrid poplar plantation in Saxony (Germany) in response to climate and soil conditions. Eur J For Res 130:695–706

    Article  Google Scholar 

  • Pfeiffer T, Klahr A, Heinrich A, Schnittler M (2011) Does sex make a difference? Genetic diversity and spatial genetic structure in two co-occurring species of Gagea (Liliaceae) with contrasting reproductive strategies. Plant Syst Evol 292:189–201

    Article  Google Scholar 

  • Pfeiffer T, Klahr A, Peterson A, Levichev IG, Schnittler M (2012) No sex at all? Extremely low genetic diversity in Gagea spathacea (Liliaceae) across Europe. Flora 207:372–378

    Article  Google Scholar 

  • Romahn K (2015) Gefäßpflanzen der Wälder in Schleswig-Holstein—Steckbriefe ausgewählter Arten. Mitteilungen der Arbeitsgemeinschaft Geobotanik in Schleswig-Holstein und Hamburg 68:121–200

    Google Scholar 

  • Rothstein DE, Zak DR (2001) Relationships between plant nitrogen economy and life history in three deciduous-forest herbs. J Ecol 89:385–394

    Article  CAS  Google Scholar 

  • Schmidt M, Mölder A, Schönfelder E, Engel F, Schmiedel I, Culmsee H (2014) Determining ancient woodland indicator plants for practical use: a new approach developed in northwest Germany. For Ecol Manag 330:228–239

    Article  Google Scholar 

  • Schnittler M, Günther KF (1999) Central European vascular plants requiring priority conservation measures—an analysis from national Red Lists and distribution maps. Biodivers Conserv 8:891–925

    Article  Google Scholar 

  • Schnittler M, Pfeiffer T, Harter D, Hamann A (2009) Bulbils contra seeds: reproductive investment in two species of Gagea (Liliaceae). Plant Syst Evol 279:29–40

    Article  Google Scholar 

  • Schnittler M, Peterson A, Peterson J, Beisenova S, Bersimbaev RI, Pfeiffer T (2013) Minor differences with big consequences: reproductive patterns in the genus Gagea (Liliaceae). Flora 208:591–598

    Article  Google Scholar 

  • Schnittler M, Nursafina A, Peterson A, Peterson J, Barnick C, Klahr A (2017) Studies of life history of Gagea graeca (Liliaceae) based on morphological and molecular methods. Bot Stud 58:40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Šerá B (2008) Simple traits among diaspore weight/number, plant height and ability of vegetative propagation. J Integr Plant Biol 50:1563–1569

    Article  PubMed  Google Scholar 

  • Shaver GR, Melillo JM (1984) Nutrient budgets of marsh plants: efficiency concepts and relation to availability. Ecology 65:1491–1510

    Article  Google Scholar 

  • Silla F, Escudero A (2003) Uptake, demand and internal cycling of nitrogen in saplings of Mediterranean Quercus species. Oecologia 136:28–36

    Article  PubMed  Google Scholar 

  • Stefańska-Krzaczek E, Kacki Z, Szypuła B (2016) Coexistence of ancient forest species as an indicator of high species richness. For Ecol Manag 365:12–21

    Article  Google Scholar 

  • Tang LY, Han WX, Chen YH, Fang JY (2013) Resorption proficiency and efficiency of leaf nutrients in woody plants in eastern China. J Plant Ecol 6:408–417

    Article  Google Scholar 

  • Thornton B, Millard P (1993) The effects of nitrogen supply and defoliation on the seasonal internal cycling of nitrogen in Molinia caerulea. J Exp Bot 44:531–536

    Article  Google Scholar 

  • Thornton B, Millard P, Duff EI, Buckland ST (1993) The relative contribution of remobilization and root uptake in supplying nitrogen after defoliation for regrowth of lamina in four grass species. New Phytol 124:689–694

    Article  CAS  Google Scholar 

  • von Schlechtendal DFL, Lengethal LE, Schenk E (eds) (1851) Flora von Deutschland, vol 2, 4th edn. Friedrich Mauke, Jena

    Google Scholar 

  • Wood SN (2006) Generalized Additive Models. An introduction with R. Chapman and Hall/CRC, Boca Raton

    Book  Google Scholar 

  • Wulf M (1997) Plant species as indicators of ancient woodland in northwestern Germany. J Veg Sci 8:635–642

    Article  Google Scholar 

  • Zhang JH, Tang ZY, Luo YK, Chi XL, Chen YH, Fang JY, Shen HH (2015) Resorption efficiency of leaf nutrients in woody plants on Mt. Dongling of Beijing, North China. J Plant Ecol 8:530–538

    Article  Google Scholar 

  • Zhou LL, Addo-Danso SD, Wu PF, Li SB, Zou XH, Zhang Y, Ma XQ (2016) Leaf resorption efficiency in relation to foliar and soil nutrient concentrations and stoichiometry of Cunninghamia lanceolata with stand development in southern China. J Soil Sediment 16:1448–1459

    Article  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

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Acknowledgements

We gratefully acknowledge funding by the Federal Ministry of Education and Research, Bonn, Germany (Funding No. 01LC1312A).

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Authors and Affiliations

  1. Institute of Ecology, Faculty of Sustainability, Leuphana University of Lüneburg, Universitätsallee 1, 21335, Lüneburg, Germany

    Andreas Fichtner, Malin Armbrust, David Walmsley & Werner Härdtle

  2. Department of Ecology, Faculty of Biology, Philipps-University Marburg, Karl von Frisch Str 8, 35043, Marburg, Germany

    Diethart Matthies

  3. Jansen & Rickert, Heinrich-Wittorf-Strasse 31, 24539, Neumünster, Germany

    Doris Jansen

  4. Community Forest Lübeck, Alt-Lauerhof 1, 23568, Lübeck, Germany

    Knut Sturm

  5. Institute of General Ecology and Environmental Protection, Technische Universität Dresden, Pienner Str. 7, 01735, Tharandt, Germany

    Goddert von Oheimb

  6. German Centre of Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5E, 04103, Leipzig, Germany

    Goddert von Oheimb

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  1. Andreas Fichtner
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  2. Diethart Matthies
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  3. Malin Armbrust
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  4. Doris Jansen
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Correspondence to Werner Härdtle.

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Communicated by Dafeng Hui.

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Fichtner, A., Matthies, D., Armbrust, M. et al. Nitrogen cycling and storage in Gagea spathacea (Liliaceae): ecological insights for protecting a rare woodland species. Plant Ecol 219, 1117–1126 (2018). https://doi.org/10.1007/s11258-018-0863-x

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