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Lichens show that fungi can acclimate their respiration to seasonal changes in temperature

  • Ecophysiology
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Abstract

Five species of lichens, the majority members of a soil-crust community (Cladonia convoluta, Diploschistes muscorum, Fulgensia fulgens, Lecanora muralis, Squamarina lentigera) showed seasonal changes of temperature sensitivity of their dark respiration (DR) to such an extent that several substantially met the definition of full acclimation, i.e. near identical DR under different nocturnal temperature conditions during the course of the year. C. convoluta, for example, had maximal DR at 5°C of −0.42, −1.11 and −0.09 nmol CO2 g−1 s−1 in autumn, winter, and summer, respectively, a tenfold range. However, at the mean night temperatures for the same three seasons, 9.7°C, 4.2°C and 13.6°C, maximal DR were almost identical at −1.11, −0.93, and −1.45 nmol CO2 g−1 s−1. The information was extracted from measurements using automatic cuvettes that continuously recorded a sample lichen’s gas exchange every 30 min under near-natural conditions. The longest period (for L. muralis) covered 15 months and 22,000 data sets whilst, for the other species studied, data blocks were available throughout the calendar year. The acclimation of DR means that maximal net carbon fixation rates remain substantially similar throughout the year and are not depressed by increased carbon loss by respiration in warmer seasons. This is especially important for lichens because of their normally high rate of DR compared to net photosynthesis. We suggest that lichens, especially soil-crust species, could be a suitable model for fungi generally, a group of organisms for which little is known about temperature acclimation because of the great difficulty in separating the organism from its growth medium. Fungi, whether saprophytic, symbiotic or parasitic, including soil lichens, are important components of soil ecosystems and contribute much of the respired CO2 from these systems. Temperature acclimation by fungi would mean that expected increases in carbon losses caused by global climate warming from soil ecosystems might not be as extensive as first thought. This would ameliorate this positive feedback loop present in some climate models and might substantially lower the predicted warming.

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References

  • Addy HD, Boswell EP, Koide RT (1998) Low temperature acclimation and freezing resistance of extraradical VA mycorrhizal hyphae. Mycol Res 102:582–586

    Article  Google Scholar 

  • Ahmadjian V (1993) The lichen symbiosis. Wiley, New York

    Google Scholar 

  • Ahmadjian V (1995) Lichens are more important than you think. BioScience 45:124

    Google Scholar 

  • Arnone JA, Körner C (1997) Temperature adaptation and acclimation potential of leaf dark respiration in two species of Ranunculus from warm and cold habitats. Arct Alp Res 29:122–125

    Google Scholar 

  • Belnap J, Büdel B, Lange OL (2003) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function and management (Ecological studies 150). Springer, Berlin Heidelberg New York, pp 3–30

    Google Scholar 

  • Brown DH, Snelgar WP, Green TGA (1981) Effects of storage conditions on lichen respiration and desiccation sensitivity. Ann Bot 48:923–926

    Google Scholar 

  • Chapin FS III, Ruess RW (2001) The roots of the matter. Nature 411:749–752

    Article  CAS  PubMed  Google Scholar 

  • Cox PM, Betts RA, Jones CD, Spall SA, Toterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408:184–187

    Article  CAS  PubMed  Google Scholar 

  • Grace J, Raymont M (1999) Respiration in the balance. Nature 404:819–820

    Article  Google Scholar 

  • Green TGA, Lange OL (1994) Photosynthesis in poikilohydric plants: a comparison of lichens and bryophytes. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis (Ecological studies 100). Springer, Berlin Heidelberg New York, pp 319–342

    Google Scholar 

  • Hale ME (1973) Growth. In: Ahmadjian V, Hale ME (eds) The lichens. Academic Press, New York, pp 473–492

    Google Scholar 

  • Harley JL, Smith DC (1956) Sugar absorption and surface carbohydrate activity of Peltigera polydactyla (Neck.) Hoffm. Ann Bot 20:513–543

    CAS  Google Scholar 

  • Hepp P (1824) Lichenen-Flora von Würzburg, oder Aufzählung und Beschreibung der um Würzburg wachsenden Flechten. Florian Kupferberg, Mainz

    Google Scholar 

  • Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Xiaosu D (eds) (2001) Climate change 2001: the scientific basis. Cambridge University Press, Cambridge

    Google Scholar 

  • Kappen L, Lange OL (1972) Die Kälteresistenz einiger Makrolichenen. Flora 161:1–29

    Article  Google Scholar 

  • Kappen L, Valladares F (1999) Opportunistic growth and desiccation tolerance: the ecological success of poikilohydrous autotrophs. In: Pugnaire FI, Valladares F (eds) Handbook of functional plant ecology. Marcel Dekker, New York, pp 9–80

    Google Scholar 

  • Kershaw KA (1985) Physiological ecology of lichens. Cambridge University Press, Cambridge

    Google Scholar 

  • Kirk PM, Cannon PF, David JC, Stalpers JA (2001) Ainsworth and Bisby’s dictionary of the fungi, 9th edn. CAB International, Wallingford

    Google Scholar 

  • Klement O (1955) Prodromus der mitteleuropäischen Flechtengesellschaften. Feddes Reper 135:5–194

    Google Scholar 

  • Körner C (2003) Alpine plant life, 2nd edn. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Kutsch WL, Kappen L (1997) Aspects of carbon and nitrogen cycling in soils of the Bornhöved Lake district. II. Modelling the influence of temperature increase on soil respiration and organic carbon content in arable soils under different managements. Biogeochemistry 39:207–224

    Article  Google Scholar 

  • Lange OL (2000) Photosynthetic performance of a gelatinous lichen under temperate habitat conditions: long-term monitoring of CO2 exchange of Collema cristatum. Bibl Lichenol 75:307–332

    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

    Google Scholar 

  • Lange OL (2003a) Photosynthetic productivity of the epilithic lichen Lecanora muralis: long-term field monitoring of CO2 exchange and its physiological interpretation. II. Diel and seasonal patterns of net photosynthesis and respiration. Flora 198:233–249

    Google Scholar 

  • Lange OL (2003b) Photosynthetic productivity of the epilithic lichen Lecanora muralis: long-term field monitoring of CO2 exchange and its physiological interpretation. III. Diel, seasonal, and annual carbon budgets. Flora 198:277–292

    Google Scholar 

  • Lange OL, Green TGA (2003) Photosynthetic performance of a foliose lichen of biological soil-crust communities: long-term monitoring of the CO2 exchange of Cladonia convoluta under temperate habitat conditions. Bibl Lichenol 86:257–280

    Google Scholar 

  • Lange OL, Green TGA (2004) Photosynthetic performance of the squamulose soil-crust lichen Squamarina lentigera: laboratory measurements and long-term monitoring of CO2 exchange in the field. Bibl Lichenol 88:363–390

    Google Scholar 

  • Lange OL, Wagenitz G (2003) What is a ‘phycolichen’? Differences and changes in the meaning of an old lichenological term. Lichenologist 35:341–345

    Article  Google Scholar 

  • Lange OL, Reichenberger H, Walz H (1997) Continuous monitoring of CO2 exchange of lichens in the field: short-term enclosure with an automatically operating cuvette. Lichenologist 29:259–274

    Article  Google Scholar 

  • Lange OL, Büdel B, Meyer A, Zellner H, Zotz G (2000) Lichen carbon gain under tropical conditions: water relations and CO2 exchange of three Leptogium species of a lower montane rainforest in Panama. Flora 195:172-190

    Google Scholar 

  • Larcher W (2003) Physiological plant ecology, 4th edn. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Larigauderie A, Körner C (1995) Acclimation of leaf dark respiration to temperature in alpine and lowland plant species. Ann Bot 76:245–252

    Article  Google Scholar 

  • Larson DW (1980) Seasonal change in the pattern of net CO2 exchange in Umbilicaria lichens. New Phytol 84:349–369

    CAS  Google Scholar 

  • Larson DW, Kershaw KA (1975) Acclimation in arctic lichens. Nature 254:421–423

    PubMed  Google Scholar 

  • Luo Y, Wen S, Hui D, Wallace LL (2001) Acclimation of soil respiration to warming in a tall grass prairie. Nature 413:622-625

    Article  CAS  PubMed  Google Scholar 

  • Nash TH III (ed) (1996) Lichen biology. Cambridge University Press, Cambridge

    Google Scholar 

  • Oechel WC, Vourlltis GL, Hastings SJ, Zulueta RC, Hinzman L, Kane D (2000) Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406:978–981

    Article  CAS  PubMed  Google Scholar 

  • Palmqvist K (2000) Carbon economy in lichens. New Phytol 148:11–36

    Article  CAS  Google Scholar 

  • Palmqvist K, Dahlman L, Valladares F, Tehler A, Sancho LG, Mattsson J-E (2002) CO2 exchange and thallus nitrogen across 75 contrasting lichen associations from different climate zones. Oecologia 133:295–306

    Article  Google Scholar 

  • Quispel A (1960) Respiration of lichens. In: Wolf J (ed) Pflanzenatmung einschliesslich Gärung und Säurestoffwechsel (Handbuch der Pflanzenphysiologie, vol XII/2). Springer, Berlin Heidelberg New York, pp 455–460

  • Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353

    Article  CAS  Google Scholar 

  • Robinson PM, Morris GM (1984) Tolerance of hyphae of Fusarium oxyspermun f.sp. lycopersici to low temperature. Trans Br Mycol Soc 46:609–613

    Google Scholar 

  • Smith DC (1960) Studies in the physiology of lichens. 3. Experiments with dissected discs of Peltigera polydactyla. Ann Bot 24:186–199

    Google Scholar 

  • Stålfelt MG (1938) Der Gasaustausch der Flechten. Planta 29:11–31

    Google Scholar 

  • Sundberg B, Ekblad A, Näsholm T, Palmqvist K (1999) Lichen respiration in relation to active time, temperature, nitrogen and ergosterol concentrations. Funct Ecol 13:119–125

    Article  Google Scholar 

  • Valentini R et al. (2000) Respiration as the main determinant of carbon balance in European forests. Nature 404:861–865

    Article  CAS  PubMed  Google Scholar 

  • Zotz G (1999) Altitudinal changes in diversity and abundance of non-vascular epiphytes in the tropics—an ecophysiological explanation. Selbyana 20:256–260

    Google Scholar 

  • Zotz G, Winter K (1994) Photosynthesis and carbon gain of the lichen, Leptogium azurem, in a lowland tropical forest. Flora 189:179–186

    Google Scholar 

Download references

Acknowledgements

This research was funded by the Deutsche Forschungsgemeinschaft and by the Alexander-von-Humboldt-Stiftung, Bonn. Assistance and help of Wilma Samfaß, Gerhard Radermacher, and Hans Reichenberger with generating, handling, and evaluating the data are gratefully acknowledged. Prof. B. Büdel kindly provided lichen material.

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Authors and Affiliations

  1. Julius-von-Sachs-Institut für Biowissenschaften der Universität Würzburg, Lehrstuhl für Botanik II, Julius-von-Sachs-Platz 3, 97084, Würzburg, Germany

    Otto L. Lange

  2. Biological Sciences, University of Waikato, Hamilton, New Zealand

    T. G. Allan Green

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  1. Otto L. Lange
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  2. T. G. Allan Green
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Correspondence to Otto L. Lange.

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This work is dedicated to Professor Hubert Ziegler on the occasion of his 80th birthday. We would like to acknowledge his impressive contribution to physiological plant ecology, and to wish him continuing joie de vivre with his scientific interests during a happy retirement.

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Lange, O.L., Green, T.G.A. Lichens show that fungi can acclimate their respiration to seasonal changes in temperature. Oecologia 142, 11–19 (2005). https://doi.org/10.1007/s00442-004-1697-x

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