Hostname: page-component-77c89778f8-9q27g Total loading time: 0 Render date: 2024-07-21T20:14:51.389Z Has data issue: false hasContentIssue false

Preference of lichens for shady habitats is correlated with intolerance to high nitrogen levels

Published online by Cambridge University Press:  03 June 2010

Markus HAUCK
Affiliation:
Albrecht von Haller Institute of Plant Sciences, Department of Plant Ecology, Georg August University of Göttingen, Untere Karspüle 2, D-37073 Göttingen, Germany. Email: mhauck@gwdg.de
Volkmar WIRTH
Affiliation:
Staatliches Museum für Naturkunde Karlsruhe, Erbprinzenstraße 13, D-76133 Karlsruhe, Germany.

Abstract

Based on findings in vascular plants showing that the capacity to provide enough carbon skeletons for rapid ammonium assimilation into amino acids is a prerequisite for tolerance to eutrophication, we tested the hypothesis that lichens from shady habitats are particularly sensitive to nitrogen pollution. We tested this hypothesis using published ecological indicator values (estimates of eutrophication tolerance and light preferences on an ordinal scale) for more than 500 central European lichen species. Our results show that shade-adapted lichens are indeed at the same time intolerant to eutrophication. However, not all eutrophication-sensitive lichens inhabit shady environments, suggesting the existence of several independent mechanisms causing intolerance of high nitrogen levels in lichens. The correlation of shade adaptation with nitrogen intolerance is limited to epiphytic and saxicolous species, since terricolous lichens are out-competed by vascular plants in dense vegetation. Our results suggest that lichen communities of shady bark, wood and rock are particularly sensitive to eutrophication.

Type
Research Article
Copyright
Copyright © British Lichen Society 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Cruz, C., Bio, A. F. M., Domínguez-Valdivia, M. D., Aparicio-Tejo, P. M., Lamsfus, C. & Martins-Loução, M. A. (2006) How does glutamine synthetase activity determine plant tolerance to ammonium? Planta 223: 10681080.CrossRefGoogle ScholarPubMed
Dahlman, L., Persson, J., Näsholm, T. & Palmqvist, K. (2003) Carbon and nitrogen distribution in the green-algal lichens Hypogymnia physodes and Platismatia glauca in relation to nutrient supply. Planta 217: 4148.Google Scholar
Dahlman, L., Persson, J., Palmqvist, K. & Näsholm, T. (2004) Organic and inorganic nitrogen uptake in lichens. Planta 219: 459467.Google Scholar
Ellenberg, H. (1974) Zeigerwerte der Gefäßpflanzen Mitteleuropas. Scripta Geobotanica 9: 197.Google Scholar
Ellenberg, H. (1992) Zeigerwerte der Gefäßpflanzen Mitteleuropas (ohne Rubus). Scripta Geobotanica 18: 9166.Google Scholar
Gaio-Oliveira, G., Branquinho, C., Máguas, C. & Martins-Loução, M. A. (2001) The concentration of nitrogen in nitrophilous and non-nitrophilous lichen species. Symbiosis 31: 187199.Google Scholar
Gaio-Oliveira, G., Dahlman, L., Palmqvist, K. & Máguas, C. (2004) Ammonium uptake in the nitrophytic lichen Xanthoria parietina and its effects on vitality and balance between symbionts. Lichenologist 36: 7586.Google Scholar
Gaio-Oliveira, G., Dahlman, L., Palmqvist, K., Martins-Loução, M. A. & Máguas, C. (2005a) Nitrogen uptake in relation to excess supply and its effects on the lichen Evernia prunastri (L.) Ach. and Xanthoria parietina (L.) Th. Fr. Planta 220: 794803.Google Scholar
Gaio-Oliveira, G., Dahlman, L., Palmqvist, K. & Máguas, C. (2005b) Responses of the lichen Xanthoria parietina (L.) Th. Fr. to varying thallus nitrogen concentrations. Lichenologist 37: 171179.Google Scholar
Green, T. G. A., Büdel, B., Meyer, A., Zellner, H. & Lange, O. L. (1997) Temperate rainforest lichens in New Zealand: light response of photosynthesis. New Zealand Journal of Botany 35: 493504.CrossRefGoogle Scholar
Hauck, M. (2010) Ammonium and nitrate tolerance in lichens. Environmental Pollution 158: 11271133.Google Scholar
Hauck, M., Willenbruch, K. & Leuschner, C. (2009a) Lichen substances prevent lichens from nutrient deficiency. Journal of Chemical Ecology 35: 7173.Google Scholar
Hauck, M., Jürgens, S.-R., Willenbruch, K., Huneck, S. & Leuschner, C. (2009b) Dissociation and metal-binding characteristics of yellow lichen substances suggest a relationship with site preferences of lichens. Annals of Botany 103: 1322.Google Scholar
Johnson, N. C., Rowland, D. L., Corkidi, L. & Allen, E. B. (2008) Plant winners and losers during grassland N-eutrophication differ in biomass allocation and mycorrhizas. Ecology 89: 28682878.Google Scholar
Krupa, S. V. (2003) Effects of atmospheric ammonia (NH3) on terrestrial vegetation: a review. Environmental Pollution 124: 179221.Google Scholar
Lageard, J. G. A., Wilson, D. B., Cresswell, N., Cawley, L. E., Jones, H. E. & Caporn, S. J. M. (2005) Wood growth response of Calluna vulgaris (L.) Hull to elevated N deposition and drought. Dendrochronologia 23: 7581.Google Scholar
Lakatos, M., Rascher, U. & Büdel, B. (2006) Functional characteristics of corticolous lichens in the understorey of a tropical lowland rain forest. New Phytologist 172: 679695.Google Scholar
Munzi, S., Pisani, T. & Loppi, S. (2009) The integrity of lichen cell membrane as a suitable parameter for monitoring biological effects of acute nitrogen pollution. Ecotoxicology and Environmental Safety 72: 20092012.Google Scholar
Neuhäuser, B., Dynowksi, M., Mayer, M. & Ludewig, U. (2007) Regulation of NH4+transport by essential cross talk between AMT monomers through the carboxyl tails. Plant Physiology 143: 16511659.CrossRefGoogle ScholarPubMed
Nimis, P. L. & Martellos, S. (2003) On the ecology of sorediate lichens in Italy. Bibliotheca Lichenologica 86: 393406.Google Scholar
Olivier, J. G. J., Bouwman, A. F., van der Hook, K. W. & Berdowski, J. J. M. (1998) Global air emission inventories for anthropogenic sources of NOX, NH3 and N2O in 1990. Environmental Pollution 102(S1): 135148.Google Scholar
Palmqvist, K. & Dahlman, L. (2006) Responses of the green algal foliose lichen Platismatia glauca to increased nitrogen supply. New Phytologist 171: 343356.Google Scholar
Palmqvist, K., Campbell, D., Ekblad, A. & Johansson, H. (1998) Photosynthetic capacity in relation to nitrogen content and its partitioning in lichens with different photobionts. Plant, Cell and Environment 21: 361372.CrossRefGoogle Scholar
Paul, A., Hauck, M. & Leuschner, C. (2009a) Iron and phosphate uptake explains the calcifuge-calcicole behavior of the terricolous lichens Cladonia furcata subsp. furcata and C. rangiformis. Plant and Soil 319: 4956.Google Scholar
Paul, A., Hauck, M. & Leuschner, C. (2009b) Iron and phosphate uptake in epiphytic and saxicolous lichens differing in their pH requirements. Environmental and Experimental Botany 67: 133138.Google Scholar
Pirintsos, S. A., Munzi, S., Loppi, S. & Kotzabasis, K. (2009) Do polyamines alter the sensitivity of lichens to nitrogen stress? Ecotoxicology and Environmental Safety 72: 13311336.CrossRefGoogle ScholarPubMed
Riddell, J., Nash, T. H. & Padgett, P. (2008) The effect of HNO3 gas on the lichen Ramalina menziesii. Flora 203: 4754.Google Scholar
Schmull, M., Hauck, M., Vann, D. R., Johnson, A. H. & Runge, M. (2002) Site factors determining epiphytic lichen distribution in a dieback-affected spruce-fir forest on Whiteface Mountain, New York: stemflow chemistry. Canadian Journal of Botany 80: 11311140.CrossRefGoogle Scholar
Schortemeyer, M., Stamp, P. & Feil, B. (1997) Ammonium tolerance and carbohydrate status in maize cultivars. Annals of Botany 79: 2530.Google Scholar
Sparrius, L. B. (2007) Response of epiphytic lichen communities to decreasing ammonia air concentrations in a moderately polluted area of the Netherlands. Environmental Pollution 146: 375379.Google Scholar
Tretiach, M. & Geletti, A. (1997) CO2 exchange of the endolithic lichen Verrucaria baldensis from karst habitats in northern Italy. Oecologia 111: 515522.Google Scholar
van Dobben, H. F. & de Bakker, A. J. (1996) Re-mapping epiphytic lichen biodiversity in the Netherlands: effects of decreasing SO2 and increasing NH3. Acta Botanica Neerlandica 45: 5571.CrossRefGoogle Scholar
van Herk, C. M. (1999) Mapping ammonia pollution with epiphytic lichens in the Netherlands. Lichenologist 31: 920.CrossRefGoogle Scholar
van Herk, C. M. (2001) Bark pH and susceptibility to toxic air pollutants as independent causes of changes in epiphytic lichen composition in space and time. Lichenologist 33: 419441.Google Scholar
van Herk, C. M., Aptroot, A., van Dobben, H. F. (2002) Long-term monitoring in the Netherlands suggests that lichens respond to global warming. Lichenologist 34: 141154.Google Scholar
van Herk, C. M., Mathijssen-Spiekman, E. A. M. & de Zwart, D. (2003) Long distance nitrogen air pollution effect on lichens in Europe. Lichenologist 35: 413415.CrossRefGoogle Scholar
Weber, B., Scherr, C., Reichenberger, H. & Büdel, B. (2007) Fast reactivation by high air humidity and photosynthetic performance of alpine lichens growing endolithically in limestone. Arctic, Antarctic, and Alpine Research 39: 309317.CrossRefGoogle Scholar
Wirth, V. (1972) Die Silikatflechten-Gemeinschaften im außeralpinen Zentraleuropa. Dissertationes Botanicae 17: 1306.Google Scholar
Wirth, V. (1985) Zur Ausbreitung, Herkunft und Ökologie anthropogen geforderter Rinden- und Holzflechten. Tuexenia 5: 523535.Google Scholar
Wirth, V. (1995) Die Flechten Baden-Württembergs. Stuttgart: Ulmer.Google Scholar
Wirth, V. (2010) Ökologische Zeigerwerte von Flechtenerweiterte und aktualisierte Fassung. Herzogia 23 (in press).Google Scholar