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Seasonal acclimation in the epiphytic lichen Parmelia sulcata is influenced by change in photobiont population density

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Abstract

CO2 gas exchange, radial growth, chlorophyll (Chl) content and photobiont density of an epiphytic population of Parmelia sulcata were monitored every 2 months during 1 year in a temperate deciduous forest of Central Italy, to verify possible seasonal variations. Light response curves of south-exposed thalli, built up in the laboratory at 6 and 27°C at optimal thallus hydration, showed that CO2 gas exchange changed significantly during the year, with a maximum for gross photosynthesis in December at both temperatures. Photoinhibition phenomena occurred in early spring, immediately before tree leaves sprouted. The principal component analysis of CO2 gas exchange parameters clearly separated the months with from the months without tree canopy cover. Radial growth, measured on marginal lobes of north- and south-exposed thalli, was the highest in December, and the lowest in April. Photobiont density, measured in lobes of south- and north-exposed thalli with a sedimentation chamber, also changed during the year: the number of photobionts was highest in June and December, and lowest in April, although no significant change in cell size and Chl content per cell was evident throughout the year. South-exposed thalli had slightly, but constantly higher photobiont density both on a weight and an area basis. The acclimation of lichen photosynthesis and Chl content to seasonal temperature and light changes should partially be re-visited on the basis of the significant variation in photobiont population density. This phenomenon still awaits, however, a satisfactory explanation, although it is probably related to the seasonal change in nutrient availability.

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References

  • Armstrong RA (1974) Growth phases in the life of a lichen thallus. New Phytol 73:913–918

    Article  Google Scholar 

  • Arrigoni PV, Nardi E (1975) Documenti per la carta della vegetazione del Monte Amiata. Webbia 29:717–785

    Article  Google Scholar 

  • Bennett J (2002) Algal layer ratios as indicators of air pollution effects in Parmelia sulcata. Bryologist 105:104–110

    Article  Google Scholar 

  • Brown D, Kershaw KA (1985) Electrophoretic and gas exchange patterns of two populations of Peltigera rufescens. In: Brown DH (ed) Lichen physiology and cell biology. Plenum, New York, pp 111–128

    Chapter  Google Scholar 

  • Casano LM, del Campo EM, García-Breijo FJ, Reig-Armiñana J, Gasulla F, del Hoyo A, Guéra A, Barreno E (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environ Microb 13:806–818

    Article  CAS  Google Scholar 

  • Coxson DS, Kershaw KA (1983) The ecology of Rhizocarpon superficiale. II. The seasonal response of net photosynthesis and respiration to temperature, moisture, and light. Can J Bot 61:3019–3030

    Article  Google Scholar 

  • Coxson DS, Kershaw KA (1984) Low-temperature acclimation of net photosynthesis in the crustaceous lichen Caloplaca trachyphylla. Can J Bot 62:86–95

    Article  Google Scholar 

  • Del Valle Tascón S, Sanz MJ, Calatayud A, Barreno E (1994) Coeficientes de extinction de clorofilas y feofitinas (a y b) en DMSO y ecuaciones para el cálculo de sus concentraciones. Stud Bot 13:115–121

    Google Scholar 

  • Eaton JS, Likens GE, Bormann HF (1973) Throughfall and stemflow chemistry in a northern hardwood forest. J Ecol 61:495–508

    Article  CAS  Google Scholar 

  • Farrar JF (1976) The lichen as an ecosystem: observation and experiment. In: Brown DH, Hawksworth DL, Bailey RH (eds) Lichenology: progress and problems. Academic Press, London, pp 385–406

    Google Scholar 

  • Fiechter E (1990) Thallusdifferenzierung und intrathalline Sekundärstoffverteilung bei Parmeliaceae (Lecanorales, Lichenisierte Ascomyceten). Inaugural dissertation, Philosophische Fakultät II, University of Zürich, Zürich

  • Fiechter E, Honegger R (1988) Seasonal variations in the fine structure of Hypogymnia physodes (lichenized Ascomycetes) and its Trebouxia photobiont. Plant Syst Evol 158:249–263

    Article  Google Scholar 

  • Friedl T (1989) Systematik und Biologie von Trebouxia (Microthamniales, Chlorophyta) als Phycobiont der Parmeliaceae (lichenisierte Ascomyceten). Inaugural-Dissertation, Fakultät Biologie, Universität Bayreuth

  • Gauslaa Y, McEvoy M (2005) Seasonal changes in solar radiation drive acclimation of the sun-screening compound parietin in the lichen Xanthoria parietina. Basic Appl Ecol 6:75–82

    Article  CAS  Google Scholar 

  • Gauslaa Y, Ohlson M, Solhaug KA, Bilger W, Nybakken L (2001) Aspect-dependent high-irradiance damage in two transplanted foliose forest lichens, Lobaria pulmonaria and Parmelia sulcata. Can J For Res 31:1639–1649

    Google Scholar 

  • Green TGA, Nash TH III, Lange OL (2008) Physiological ecology of carbon dioxide exchange. In: Nash TH III (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 152–181

    Chapter  Google Scholar 

  • Harris GP (1971) The ecology of corticolous lichens. II. The relationship between physiology and the environment. J Ecol 59:441–452

    Article  Google Scholar 

  • Harris GP (1972) The ecology of corticolous lichens. III. A simulation model of productivity as a function of light intensity and water availability. J Ecol 60:19–40

    Article  Google Scholar 

  • Hill DH (1985) Changes in photobiont dimensions and numbers during co-development of lichen symbionts. In: Brown DH (ed) Lichen physiology and cell biology. Plenum Press, New York, pp 303–317

    Chapter  Google Scholar 

  • Hill DH (1994) The cell cycle of the photobiont of the lichen Parmelia sulcata (Lecanorales, Ascomycotina) during development of the thallus lobes. Cryptog Bot 4:270–273

    Google Scholar 

  • Honegger R (1998) The lichen symbiosis—what is so spectacular about it? Lichenologist 30:193–212

    Google Scholar 

  • Kershaw KA (1985) Photosynthetic capacity changes in lichens and their potential ecological significance. In: Brown DH (ed) Lichen physiology and cell biology. Plenum, New York, pp 93–109

    Chapter  Google Scholar 

  • Kinoshita Y, Hayase S, Higuchi M, Ahmadijan V, Yoshimura I, Yamada Y (1991) Improvement of protoplast isolation from lichen mycobionts. Agric Biol Chem 55:1891–1892

    Article  CAS  Google Scholar 

  • Lange OL (2002) Photosynthetic productivity of the epilithic lichen Lecanora muralis: long-term field monitoring of CO2 exchange and its physiological interpretation. I. Dependence of photosynthesis on water content, light, temperature, and CO2 concentration from laboratory measurements. Flora 197:233–249

    Article  Google Scholar 

  • Lange OL, Green TGA (2005) Lichens show that fungi can acclimate their respiration to seasonal change in temperature. Oecologia 142:11–19

    Article  PubMed  Google Scholar 

  • Levia DF Jr, Frost EE (2003) A review and evaluation of stemflow literature in the hydrologic and biogeochemical cycles of forested and agricultural ecosystems. J Hydrol 274:1–29

    Article  CAS  Google Scholar 

  • Louwhoff SHJJ, Purvis OW, James PW (2009) Parmelia Ach. (1803). In: Smith CW, Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley PA (eds) The lichens of Great Britain and Ireland. British Lichen Society, London, pp 651–654

    Google Scholar 

  • MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38

    Article  Google Scholar 

  • MacKenzie TDB, MacDonald TM, Dubois LA, Campbell DA (2001) Seasonal changes in temperature and light drive acclimation of photosynthetic physiology and macromolecular content in Lobaria pulmonaria. Planta 214:57–66

    Article  PubMed  CAS  Google Scholar 

  • MacKenzie TDB, Johnson J, Campbell DA (2004) Environmental change provokes rapid macromolecular reallocations within the photosynthetic system in a static population of photobionts in the lichen Lobaria pulmonaria. Lichenologist 36:425–433

    Article  Google Scholar 

  • Martínez Moreno MI (1999) Taxonomía del género Peltigera Willd. (Ascomycetes Liquenizados) en la Península Ibérica y estudio de sus hongos liquenícolas. Ruizia. Monografías del Real Jardín Botánico, 15, Real Jardín Botánico, CSIC, Madrid

  • McEvoy M, Gauslaa Y, Solhaug KA (2007) Changes in pools of depsidones and melanins, and their function, during growth and acclimation under contrasting natural light in the lichen Lobaria pulmonaria. New Phytol 175:271–282

    Article  PubMed  CAS  Google Scholar 

  • Nash TH III (ed) (2008) Lichen biology, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Palmqvist K, Dahlman L, Jonsson A, Nash TH III (2008) The carbon economy of lichens. In: Nash TH III (ed) Lichen biology, 2nd edn. Cambridge University Press, Cambridge, pp 182–215

    Chapter  Google Scholar 

  • Piccotto M, Tretiach M (2010) Photosynthesis in chlorolichens: the influence of the habitat light regime. J Plant Res 123:763–775

    Article  PubMed  CAS  Google Scholar 

  • Pintado A (1996) Estudio ecofisiológico del grupo Ramalina polymorpha en la Sierra de Guadarrama. PhD dissertation, Universidad Complutense de Madrid, Madrid

  • Pintado A, Valladares F, Sancho LG (1997) Exploring phenotypic plasticity in the lichen Ramalina capitata: morphology, water relations and chlorophyll content in north- and south-facing populations. Ann Bot 80:345–353

    Article  Google Scholar 

  • Ra H-SY, Rubin L, Crang RFE (2004) Structural impacts on thallus and photobiont components of two lichen species in response to low-level air pollution in Pacific Northwest forests. Microsc Microanal 10:270–279

    Article  PubMed  CAS  Google Scholar 

  • Rosenqvist E (2001) Light acclimation maintains the redox state of the PSII electron acceptor QA within a narrow range over a broad range of light intensities. Photosynth Res 70:299–310

    Article  PubMed  CAS  Google Scholar 

  • Solhaug KA, Gauslaa Y (2004) Photosynthates stimulate the UV-B induced fungal anthraquinones synthesis in the foliose lichen Xanthoria parietina. Plant Cell Environ 27:167–176

    Article  CAS  Google Scholar 

  • Staelens J, De Schrijver A, Verheyen K (2007) Seasonal variation in throughfall and stemflow chemistry beneath a European beech (Fagus sylvatica) tree in relation to canopy phenology. Can J For Res 37:1359–1372

    Article  CAS  Google Scholar 

  • Strobl A, Türk R (1990) Untersuchungen zum Chlorophyllgehalt einiger subalpiner Flechtenarten. Phyton 30:247–264

    CAS  Google Scholar 

  • Tretiach M, Carpanelli A (1992) Morphology and chlorophyll content as factors influencing the photosynthetic rates of Parmelia caperata (L.) Ach. Lichenologist 24:81–90

    Google Scholar 

  • Tretiach M, Ganis P (1999) Effects of H2S on epiphytic lichen vegetation: a study case from M. Amiata (Central Italy). Lichenologist 31:163–181

    Article  Google Scholar 

  • Tretiach M, Geletti A (1997) CO2 exchange of the endolithic lichen Verrucaria baldensis from karst habitats in northern Italy. Oecologia 111:515–522

    Article  Google Scholar 

  • Tretiach M, Crisafulli P, Virgilio D, Baruffo L, Jensen M (2003) Seasonal variation of photoinhibition in an epiphytic population of the lichen Parmelia sulcata Taylor. Biblioth Lichenol 86:313–327

    Google Scholar 

  • Tretiach M, Crisafulli P, Pittao E, Rinino S, Roccotiello E, Modenesi P (2005) Isidia ontogeny and its effects on the CO2 gas exchanges of the epiphytic lichen Pseudevernia furfuracea (L.) Zopf. Lichenologist 37:445–462

    Article  Google Scholar 

  • Utermöhl A (1958) Zur Vervollkommung der quantitativen Phytoplankton Methodik. Mitt Int Verein Limnol 9:1–38

    Google Scholar 

  • Valladares F, Ascaso C, Sancho LG (1994) Intrathalline variability of some structural and physical parameters in the lichen genus Lasallia. Can J Bot 72:415–428

    Article  Google Scholar 

  • Valladares F, Sancho LG, Ascaso C (1996) Functional analysis of the intrathalline and intracellular chlorophyll concentrations in the lichen family Umbilicariaceae. Ann Bot 78:471–477

    Article  CAS  Google Scholar 

  • Vráblíková H, McEvoy M, Solhaug KA, Barták M, Gauslaa Y (2006) Annual variation in photoacclimation and photoprotection of the photobiont in the foliose lichen Xanthoria parietina. J Photochem Photobiol B Biol 83:151–162

    Article  Google Scholar 

  • Zingone A, Honsell G, Marino D, Montresor M, Socal G (1990) Fitoplancton. In: Innamorati M, Ferrari I, Marino D, Ribera D’Alcalà M (eds) Metodi nell’ecologia del plankton marino. Nova Thalassia 11:183–198

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Acknowledgments

We thank Paola Crisafulli and Laurence Baruffo (Trieste, Italy) for help in carrying out CO2 gas exchange measurements, Elena Pittao (Trieste) for assistance with the figures, Massimo Bidussi (Ås, Norway) and Paolo Giordani (Genova, Italy) for critical remarks on a first draft of the manuscript. We thank ENEL GreenPower for providing the meteorological data of Fig. 1. The study received D.T.N. (f.o.o.p.) funds from the junior author.

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Correspondence to Mauro Tretiach.

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Communicated by Hermann Heilmeier.

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Tretiach, M., Bertuzzi, S., Candotto Carniel, F. et al. Seasonal acclimation in the epiphytic lichen Parmelia sulcata is influenced by change in photobiont population density. Oecologia 173, 649–663 (2013). https://doi.org/10.1007/s00442-013-2654-3

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