Skip to main content
SpringerLink
Log in

Diversity and ecological adaptations in Palaeogene lichens

  • Article
  • Published:

From Nature Plants

View current issue Submit your manuscript

Abstract

Lichens are highly specialized symbioses between heterotrophic fungi and photoautotrophic green algae or cyanobacteria. The mycobionts of many lichens produce morphologically complex thalli to house their photobionts. Lichens play important roles in ecosystems and have been used as indicators of environmental change. Here we report the finding of 152 new fossil lichens from European Palaeogene amber, and hence increase the total number of known fossil lichens from 15 to 167. Most of the fossils represent extant lineages of the Lecanoromycetes, an almost exclusively lichen-symbiotic class of Ascomycota. The fossil lichens show a wide diversity of morphological adaptations that attached epiphytic thalli to their substrates, helped to combine external water storage with effective gas exchange and facilitated the simultaneous reproduction and dispersal of both partners in symbiosis. The fossil thallus morphologies suggest that the climate of European Palaeogene amber forests was relatively humid and most likely temperate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1: Growth forms of lichens preserved in Palaeogene amber.
Figure 2: Morphology and anatomy of Palaeogene lichen thalli.
Figure 3: SEM images of lichens from Palaeogene amber.
Figure 4: Reproductive structures of lichens from Palaeogene amber.
Figure 5: Taxonomic affiliation, thallus morphology and mode of reproduction of 161 lichen fossils preserved in Baltic and Bitterfeld amber (for details, see Supplementary Table 1).

Similar content being viewed by others

References

  1. Lawrey, J. D. et al. High concentration of basidiolichens in a single family of agaricoid mushrooms (Basidiomycota: Agaricales: Hygrophoraceae). Mycol. Res. 113, 1154–1171 (2009).

    Google Scholar 

  2. Schoch, K. et al. The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst. Biol. 58, 224–239 (2009).

    Google Scholar 

  3. Lücking, R., Dal-Forno, M. & Sikaroodi, M. A single macrolichen constitutes hundreds of unrecognized species. Proc. Natl Acad. Sci. USA 111, 11091–11096 (2014).

    Google Scholar 

  4. Feuerer, T. & Hawksworth, D. L. Biodiversity of lichens, including a world-wide analysis of checklist data based on Takhtajan's floristic regions. Biodivers. Conserv. 16, 85–98 (2007).

    Google Scholar 

  5. Rikkinen, J. Cyanolichens. Biodivers. Conserv. 24, 973–993 (2015).

    Google Scholar 

  6. Köhler, L., Hölscher, D., Bruijnzeel, L. A. & Leuschner, C. in Tropical Montane Cloud Forests (eds Bruijnzeel, L. A., Scatena, F. N. & Hamilton, L. S. ) 67–76 (Cambridge Univ. Press, 2010).

    Google Scholar 

  7. Elbert, W. et al. Contribution of cryptogamic covers to the global cycles of carbon and nitrogen. Nat. Geosci. 5, 459–462 (2012).

    Google Scholar 

  8. Ellis, C. J. Lichen epiphyte diversity: a species, community and trait-based review. Perspect. Plant Ecol. Evol. Syst. 14, 131–152 (2012).

    Google Scholar 

  9. Honegger, R. in The Mycota IX: Fungal Associations 2nd edn (ed. Hock, B. ) 287–339 (Springer, 2012).

    Google Scholar 

  10. Matsunaga, K. K. S., Stockey, R. A. & Tomescu, A. M. F. Honeggeriella complexa gen. et sp. nov., a heteromerous lichen from the Lower Cretaceous of Vancouver Island (British Columbia, Canada). Am. J. Bot. 100, 450–459 (2013).

    Google Scholar 

  11. Hartl, C. et al. Lichen preservation in amber: morphology, ultrastructure, chemofossils, and taphonomic alteration. Foss. Rec. 18, 127–135 (2015).

    Google Scholar 

  12. Kaasalainen, U. et al. The enigmatic fossil Alectoria succini Mägdefrau reconsidered, and new evidence of alectorioid morphologies in Palaeogene lichens. PLoS ONE 10, e0129526 (2015).

    Google Scholar 

  13. Kaasalainen, U. et al. A Caribbean epiphyte community preserved in Miocene Dominican amber. Earth Env. Sci. T. R. Soc. (in the press).

  14. Taylor, T. N., Hass, H. & Kerp, H. A cyanolichen from the Lower Devonian Rhynie chert. Am. J. Bot. 84, 992–1004 (1997).

    Google Scholar 

  15. Karatygin, I. V., Snigerevskaya, N. S. & Vikulin, S. V. The most ancient terrestrial lichen Winfrenatia reticulata: a new find and new interpretation. Paleontol. J. 43, 107–114 (2009).

    Google Scholar 

  16. Honegger, R., Edwards, D. & Axe, L. The earliest records of internally stratified cyanobacterial and algal lichens from the Lower Devonian of the Welsh Borderland. New Phytol. 197, 264–275 (2013).

    Google Scholar 

  17. Goeppert, H. R. & Berendt, G. C. Der Bernstein und die in ihm befindlichen Pflanzenreste der Vorwelt (Nicolaische Buchhandlung, 1845).

    Google Scholar 

  18. Caspary, R. & Klebs, R. Die Flora des Bernsteins und anderer fossiler Harze des ostpreußischen Tertiars (Königlich Preußische Geologische Landesanstalt, 1907).

    Google Scholar 

  19. Caspary, R. & Klebs, R. Atlas von dreissig Tafeln zu der Abhandlung: Die Flora des Bernsteins und anderer fossiler Harze des ostpreußischen Tertiärs (Königlich Preußische Geologische Landesanstalt, 1907).

    Google Scholar 

  20. Rikkinen, J. & Poinar, G. O. Jr. Fossilised Anzia (Lecanorales, lichen-forming Ascomycota) from European Tertiary amber. Mycol. Res. 106, 984–990 (2002).

    Google Scholar 

  21. Rikkinen, J. Calicioid lichens from European Tertiary amber. Mycologia 95, 1032–1036 (2003).

    Google Scholar 

  22. Beimforde, C. et al. Estimating the Phanerozoic history of the Ascomycota lineages: combining fossil and molecular data. Mol. Phylogenet. Evol. 78, 386–398 (2014).

    Google Scholar 

  23. Peterson, E. B. An overlooked fossil lichen (Lobariaceae). Lichenologist 32, 298–300 (2000).

    Google Scholar 

  24. Poinar, G. O. Jr, Peterson, E. B. & Platt, J. L. Fossil Parmelia in new world amber. Lichenologist 32, 263–269 (2000).

    Google Scholar 

  25. Rikkinen, J. & Poinar, G. O. Jr. A new species of Phyllopsora (Lecanorales, lichen-forming Ascomycota) from Dominican amber, with remarks on the fossil history of lichens. J. Exp. Bot. 59, 1007–1011 (2008).

    Google Scholar 

  26. Amo de Paz, G., Cubas, P., Divakar, P. K., Lumbsch, H. T. & Crespo, A. Origin and diversification of major clades in parmelioid lichens (Parmeliaceae, Ascomycota) during the Palaeogene inferred by Bayesian analysis. PLoS ONE 12, e28161 (2011).

    Google Scholar 

  27. Prieto, M. & Wedin, M. Dating the diversification of the major lineages of Ascomycota (fungi). PLoS ONE 8, e65576 (2013).

    Google Scholar 

  28. Divakar, P. K. et al. Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi. New Phytol. 208, 1217–1226 (2015).

    Google Scholar 

  29. Crespo, A. et al. Phylogenetic generic classification of parmelioid lichens (Parmeliaceae, Ascomycota) based on molecular, morphological and chemical evidence. Taxon 59, 1735–1753 (2010).

    Google Scholar 

  30. Miadlikowska, J. et al. A multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families. Mol. Phylogenet. Evol. 79, 132–168 (2014).

    Google Scholar 

  31. Yoshimura, I. Taxonomy and speciation of Anzia and Pannoparmelia. Bibl. Lichenol. 25, 185–195 (1987).

    Google Scholar 

  32. Jayalal, U. et al. Anzia mahaeliyensis and Anzia flavotenuis, two new lichen species from Sri Lanka. Lichenologist 44, 381–389 (2012).

    Google Scholar 

  33. Wang, X. Y. et al. Taxonomic study of the genus Anzia (Lecanorales, lichenized Ascomycota) from Hengduan Mountains, China. Lichenologist 47, 99–115 (2015).

    Google Scholar 

  34. Mosbrugger, V., Utescher, T. & Dilcher, D. L. Cenozoic continental climatic evolution of central Europe. Proc. Natl Acad. Sci. USA 102, 14964–14969 (2005).

    Google Scholar 

  35. Collinson, M. E. in Eocene-Oligocene Climatic and Biotic Evolution (eds Prothero, D. R. & Berggren, W. A. ) 437–450 (Princeton Univ. Press, 1992).

    Google Scholar 

  36. Kohlman-Adamska, A. in The Amber Treasure Trove, Part 1 (ed. Kosmowska-Ceranowicz, B. ) 15–18 (Oficyna Wydawnicza Sadyba, 2001).

    Google Scholar 

  37. Sadowski, E.-M., Schmidt, A. R., Seyfullah, L. J. & Kunzmann, L. Conifers of the ‘Baltic amber forest’ and their palaeoecological significance. Stapfia (in the press).

  38. Kershaw, K. A. Physiological Ecology of Lichens (Cambridge Univ. Press, 1985).

    Google Scholar 

  39. Rikkinen, J. Habitat shifts and morphological variation of Pseudevernia furfuracea along a topographic gradient. Symb. Bot. Ups. 32, 223–245 (1997).

    Google Scholar 

  40. Gauslaa, Y. & Coxson, D. Interspecific and intraspecific variations in water storage in epiphytic old forest foliose lichens. Botany 89, 787–798 (2011).

    Google Scholar 

  41. Green, T. G. A. & Lange, O. L. Ecophysiological adaptations of the lichen genera Pseudocyphellaria and Sticta to south temperate rainforests. Lichenologist 23, 267–282 (1991).

    Google Scholar 

  42. Valladares, F., Sancho, L. G. & Ascaso, C. Water storage in the lichen family Umbilicariaceae. Bot. Acta. 111, 99–107 (1997).

    Google Scholar 

  43. Lange, O. L., Büdel, B., Meyer, A., Zellner, H. & Zotz, G. Lichen carbon gain under tropical conditions: water relations and CO2 exchange of Lobariaceae species of a lower montane rainforest in Panama. Lichenologist 36, 329–342 (2004).

    Google Scholar 

  44. Rikkinen, J. Molecular studies on cyanobacterial diversity in lichen symbioses. MycoKeys 6, 3–32 (2013).

    Google Scholar 

  45. Rikkinen, J. Ecological and evolutionary role of photobiont-mediated guilds in lichens. Symbiosis 34, 99–110 (2003).

    Google Scholar 

  46. Kaasalainen, U. et al. Cyanobacteria produce a high variety of hepatotoxic peptides in lichen symbiosis. Proc. Natl Acad. Sci. USA 109, 5886–5891 (2012).

    Google Scholar 

  47. Belinchón, R., Yahr, R. & Ellis, C. J. Interactions among species with contrasting dispersal modes explain distributions for epiphytic lichens. Ecography 37, 1–7 (2014).

    Google Scholar 

  48. Dal Grande, F. et al. Molecular phylogeny and symbiotic selectivity of the green algal genus Dictyochloropsis s.l. (Trebouxiophyceae): a polyphyletic and widespread group forming photobiont-mediated guilds in the lichen family Lobariaceae. New Phytol. 202, 455–447 (2014).

    Google Scholar 

  49. Cornejo, C. & Scheidegger, C. Cyanobacterial gardens: the liverwort Frullania asagrayana acts as a reservoir of lichen photobionts. Environ. Microbiol. Rep. 8, 352–357 (2016).

    Google Scholar 

  50. Standke, G. Bitterfelder Bernstein gleich Baltischer Bernstein?–Eine geologische Raum-Zeit-Betrachtung und genetische Schlußfolgerungen. Exkurs.f. und Veröfftl. DGG 236, 11–33 (2008).

    Google Scholar 

  51. Weitschat, W. & Wichard, W. Atlas of Plants and Animals in Baltic Amber (Verlag Dr. Friedrich Pfeil, 2010).

    Google Scholar 

  52. Kosmowska-Ceranowicz, B., Kohlman-Adamska, A. & Grabowska, I. Erste Ergebnisse zur Lithologie und Palynologie der bernsteinführenden Sedimente im Tagebau Primorskoje. Metalla 66, 5–17 (1997).

    Google Scholar 

  53. Standke, G. Die Tertiärprofile der samländischen Bernsteinküste bei Rauschen. Schriftenreihe für Geowissenschaften 7, 93–133 (1998).

    Google Scholar 

  54. Kasiński, J. R. & Kramarska, R. Sedimentary environment of amber-bearing association along the Polish-Russian Baltic coastline. Exkurs.f. und Veröfftl. DGG 236, 46–57 (2008).

    Google Scholar 

  55. Ritzkowski, S. K-Ar Altersbestimmungen der bernsteinführenden Sedimente des Samlandes (Paläogen, Bezirk Kaliningrad). Metalla 66, 19–24 (1997).

    Google Scholar 

  56. Clauer, N., Huggett, J. & Hillier, S. How reliable is the K-Ar glauconite chronometer? A case study of Eocene sediments from the Isle of Wight. Clay Minerals 40, 167–176 (2005).

    Google Scholar 

  57. Grimaldi, D. & Ross, A. in Terrestrial Conservation Lagerstätten: Windows into the Evolution of Life on Land (eds Fraser, N. C. & Sues, H.-D. ) (Dunedin Acad. Press, in the press).

  58. Blumenstengel, H. Zur Palynologie und Stratigraphie der Bitterfelder Bernsteinvorkommen (Tertiär). Exkurs.f. und Veröfftl. DGG 224, 17 (2004).

    Google Scholar 

  59. Knuth, G., Koch, T., Rappsilber, I. & Volland, L. Concerning amber in the Bitterfeld region—geologic and genetic aspects. Hallesches Jahrbuch für Geowissenschaften 24, 35–46 (2002).

    Google Scholar 

  60. Weitschat, W. Bitterfelder Bernstein – ein eozäner Bernstein auf miozäner Lagerstätte. Metalla 66, 71–84 (1997).

    Google Scholar 

  61. Dunlop, J. A. in Biodiversity of Fossils in Amber (ed. Penney, D. ) 57–68 (Siri Scientific Press, 2010).

    Google Scholar 

  62. Wolfe, A. P., McKellar, R. C., Tappert, R., Sodhi, R. N. S. & Muehlenbachs, K. Bitterfeld amber is not Baltic amber: three geochemical tests and further constraints on the botanical affinities of succinate. Rev. Palaeobot. Palynol. 225, 21–32 (2016).

    Google Scholar 

  63. Liehmann, G. Die maschinelle Gewinnung und Aufbereitung des Bernsteins im Tagebau Goitsche bei Bitterfeld – ein Erlebnisbericht. Exkurs.f. und Veröfftl. DGG 249, 24–30 (2013).

    Google Scholar 

  64. Schmidt, A. R. et al. Arthropods in amber from the Triassic Period. Proc. Natl Acad. Sci. USA 109, 14796–14801 (2012).

    Google Scholar 

  65. Nascimbene, P. & Silverstein, H. in Studies on Fossils in Amber, with Particular Reference to the Cretaceous of New Jersey (ed. Grimaldi, D. A. ) 93–102 (Backhuys Publishers, 2000).

    Google Scholar 

Download references

Acknowledgements

We thank V. Arnold (Heide), H. Grabenhorst (Wienhausen), C. Gröhn (Glinde), C. and H. W. Hoffeins (Hamburg), M. Kobbert (Münster), K. Nordman Ernst (Skagen), F. Witsch (Köln) and J. Wunderlich (Hirschberg) for providing specimens for this study, and G. Bechly (Stuttgart), A. Gehler (Göttingen) and C. Neumann (Berlin) for access to museum collections. D. Hause-Reitner (Göttingen) assisted with SEM imaging. This study was supported by the Alexander von Humboldt Foundation (grant to U.K.).

Author information

Authors and Affiliations

  1. Department of Geobiology, University of Göttingen, Goldschmidtstraβe 3, 37077 Göttingen, Germany

    Ulla Kaasalainen & Alexander R. Schmidt

  2. Finnish Museum of Natural History, University of Helsinki, PO Box 7, FIN-00014, Finland

    Jouko Rikkinen

  3. Department of Biosciences, University of Helsinki, PO Box 65, FIN-00014, Finland

    Jouko Rikkinen

Authors
  1. Ulla Kaasalainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexander R. Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jouko Rikkinen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

U.K., A.R.S. and J.R. designed and performed research, analysed data and wrote the paper.

Corresponding author

Correspondence to Jouko Rikkinen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Table 1. (PDF 286 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaasalainen, U., Schmidt, A. & Rikkinen, J. Diversity and ecological adaptations in Palaeogene lichens. Nature Plants 3, 17049 (2017). https://doi.org/10.1038/nplants.2017.49

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/nplants.2017.49

  • Springer Nature Limited

This article is cited by

Search

Navigation