Skip to main content

Morphological diversity of fungal reproductive units in the Lower Devonian Rhynie and Windyfield cherts, Scotland: a new species of the genus Windipila

Abstract

The Lower Devonian Rhynie and Windyfield cherts from Scotland contain a remarkable diversity of microscopic fungal propagules and reproductive units; however, only relatively few of these fossils are described. One of them is Windipila spinifera, an unusual reproductive unit from the Windyfield chert that consists of a walled spheroid (~ 100 µm in diam.) surrounded by a mantle of interlaced hyphae; prominent spines and otherwise shaped projections, produced by these hyphae, extend out from the mantle. Here, we present W. wimmervoecksii sp. nov., also from Windyfield, which differs from W. spinifera in that the mantle hyphae produce vesicle-like inflations instead of spines. Narrow processes arising from the inflations connect the persistent inner mantle tier with a probably ephemeral outer tier of irregularly inflated hyphae. There is some evidence to suggest that W. wimmervoecksii was a member of the Glomeromycota; however, the precise systematic affinities remain unresolved. This discovery broadens our understanding of the patterns of mantle formation that were present in fungi by the Early Devonian.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Agnolucci, M., F. Battini, C. Cristani, and M. Giovannetti. 2015. Diverse bacterial communities are recruited on spores of different arbuscular mycorrhizal fungal isolates. Biology and Fertility of Soils 51: 379–389.

    Google Scholar 

  • Agnolucci, M., L. Avio, A. Pepe, A. Turrini, C. Cristani, P. Bonini, V. Cirino, F. Colosimo, M. Ruzzi, and M. Giovannetti. 2019. Bacteria associated with a commercial mycorrhizal inoculum: community composition and multifunctional activity as assessed by illumina sequencing and culture-dependent tools. Frontiers in Plant Science 9: 1956.

    Google Scholar 

  • Benjamin, R.K. 1979. Zygomycetes and their spores. In The Whole Fungus. II. The Sexual-Asexual Synthesis [Proceedings of the 2nd International Mycological Conference held at the Environmental Sciences Centre of the University of Calgary Kananaskis, Alberta, Canada], ed., B. Kendrick, 573–621. Ottawa: National Museum of Natural Sciences, National Museums of Canada, and the Kananaskis Foundation.

  • Benny, G.L. 2012. Current systematics of Zygomycota with a brief review of their biology. In Systematics and evolution of fungi, eds. J.K. Misra, J.P. Tewari, and S.K. Deshmukh, 55–105. Boca Raton: CRC Press.

    Google Scholar 

  • Benny, G.L., R.A. Hamber, and J.B. Morton. 2001. Zygomycota: zygomycetes. In The Mycota VIIA Systematics and evolution, eds. D.J. McLoughlin, E.G. McLoughlin, and P.E. Lemke, 113–146. Berlin: Springer.

    Google Scholar 

  • Błaszkowski, J. 2012. Glomeromycota, 1–303. Kraków: W. Szafer Institute of Botany, Polish Academy of Sciences.

    Google Scholar 

  • Bonfante, P., and A. Desirò. 2017. Who lives in a fungus? The diversity, origins and functions of fungal endobacteria living in Mucoromycota. ISME Journal 11: 1727–1735.

    Google Scholar 

  • Bucholtz, F. 1912. Beiträge zur Kenntnis der Gattung Endogone Link. Beihefte zum Botanischen Centralblatt (Abteilung II) 29: 147–224.

    Google Scholar 

  • Calhim, S., P. Halme, J.H. Petersen, T. Læssøe, C. Bässler, and J. Heilmann-Clausen. 2018. Fungal spore diversity reflects substrate-specific deposition challenges. Scientific Reports 8: 5356.

    Google Scholar 

  • Chagnon, P.L. 2014. Ecological and evolutionary implications of hyphal anastomosis in arbuscular mycorrhizal fungi. FEMS Microbial Ecology 88: 437–444.

    Google Scholar 

  • Channing, A. 2017. A review of active hot-spring analogues of Rhynie: environments, habitats and ecosystems. Philosophical Transactions of the Royal Society London (B: Biological Sciences) 373: 20160489.

    Google Scholar 

  • Dotzler, N., C. Walker, M. Krings, H. Hass, H. Kerp, T.N. Taylor, and R. Agerer. 2009. Acaulosporoid glomeromycotan spores with a germination shield from the 400-million-year-old Rhynie chert. Mycological Progress 8: 9–18.

    Google Scholar 

  • Edelmann, R.E., and K.L. Klomparens. 1995. Zygosporogenesis in Zygorhynchus heterogamus, with proposal for standardization of structural nomenclature. Mycologia 87: 304–318.

    Google Scholar 

  • Edwards, D., L. Dolan, and P. Kenrick (eds.). 2018. The Rhynie cherts: our earliest terrestrial ecosystem revisited. Philosophical Transactions of the Royal Society of London (B: Biological Sciences) 373: 1–201.

  • Fayers, S.R. 2003. The biota and palaeoenvironements of the Windyfield Chert, Early Devonian, Rhynie, Scotland, 1–549. PhD thesis, University of Aberdeen, Aberdeen, Scotland.

  • Fayers, S.R., and N.H. Trewin. 2004. A review of the palaeoenvironments and biota of the Windyfield chert. Transactions of the Royal Society of Edinburgh, Earth Sciences 94: 325–339.

    Google Scholar 

  • Frey-Klett, P., J. Garbaye, and M. Tarkka. 2007. The mycorrhiza helper bacteria revisited. New Phytologist 176: 22–36.

    Google Scholar 

  • Garwood, R.J., H. Oliver, and A.R.T. Spencer. 2019. An introduction to the Rhynie chert. Geological Magazine. https://doi.org/10.1017/s0016756819000670.

    Article  Google Scholar 

  • Giovannetti, M., D. Azzolini, and A.S. Citernesi. 1999. Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Applied and Environmental Microbiology 65: 5571–5575.

    Google Scholar 

  • Giovannetti, M., L. Avio, and C. Sbrana. 2015. Functional significance of anastomosis in arbuscular mycorrhizal fungi. In Mycorrhizal networks, ed. T.R. Horton, 41–67. Dordrecht: Springer.

    Google Scholar 

  • Glass, N.L., and A. Fleissner. 2006. Re-wiring the network: understanding the mechanism and function of anastomosis in filamentous ascomycete fungi. In The Mycota, I. Growth, differentiation and sexuality, eds. U. Kües and R. Fischer, 123–139. Berlin, Heidelberg: Springer.

    Google Scholar 

  • Gregory, P.H. 1984. The fungal mycelium—an historical perspective. In The ecology and physiology of the fungal mycelium, eds. D.H. Jennings and A.D.M. Rayner, 1–22. Cambridge: Cambridge University Press.

    Google Scholar 

  • Hass, H., T.N. Taylor, and W. Remy. 1994. Fungi from the Lower Devonian Rhynie chert: mycoparasitism. American Journal of Botany 81: 29–37.

    Google Scholar 

  • Hemkemeyer, M., B.T. Christensen, C.C. Tebbe, and M. Hartmann. 2019. Taxon-specific fungal preference for distinct soil particle size fractions. European Journal of Soil Biology 94: 103103.

    Google Scholar 

  • Ivarsson, M., J. Peckmann, A. Tehler, C. Broman, W. Bach, K. Behrens, J. Reitner, M.E. Böttcher, and L. Norbäck Ivarsson. 2015. Zygomycetes in vesicular basanites from Vesteris Seamount, Greenland Basin—a new type of cryptoendolithic fungi. PLoS One 10(7): e0133368.

    Google Scholar 

  • Kidston, R., and W.H. Lang. 1921. On Old Red Sandstone plants showing structure, from the Rhynie Chert bed, Aberdeenshire. Part V. The Thallophyta occurring in the peat-bed; the succession of the plants throughout a vertical section of the bed, and the conditions of accumulation and preservation of the deposit. Transactions of the Royal Society of Edinburgh 52: 855–902.

    Google Scholar 

  • Krings, M., and C.J. Harper. 2017. A mantled fungal reproductive unit from the Lower Devonian Windyfield chert, Scotland, with prominent spines and otherwise shaped projections extending out from the mantle. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 285: 201–211.

    Google Scholar 

  • Krings, M., and C.J. Harper. 2018a. Additional observations on the fungal reproductive unit Windipila spinifera from the Windyfield chert, and description of a similar form, Windipila pumila nov. sp., from the nearby Rhynie chert (Lower Devonian, Scotland). Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 288: 235–242.

    Google Scholar 

  • Krings, M., and C.J. Harper. 2018b. Deciphering interfungal relationships in the 410 million-year-old Rhynie chert: glomoid spores under attack. Geobios 51: 151–160.

    Google Scholar 

  • Krings, M., and T.N. Taylor. 2012. Fungal reproductive units enveloped in a hyphal mantle from the Lower Pennsylvanian of Great Britain, and their relevance to our understanding of Carboniferous fungal “sporocarps”. Review of Palaeobotany and Palynology 175: 1–9.

    Google Scholar 

  • Krings, M., and T.N. Taylor. 2013. Zwergimyces vestitus (Kidston et W.H. Lang) nov. comb., a fungal reproductive unit enveloped in a hyphal mantle from the Lower Devonian Rhynie chert. Review of Palaeobotany and Palynology 190: 15–19.

    Google Scholar 

  • Krings, M., and T.N. Taylor. 2014. A mantled fungal reproductive unit from the Lower Devonian Rhynie chert that demonstrates Carboniferous “sporocarp” morphology and development. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 273: 197–205.

    Google Scholar 

  • Krings, M., and T.N. Taylor. 2015a. A fungal reproductive unit from the Lower Devonian Rhynie chert (Aberdeenshire, Scotland) that demonstrates an unusual hyphal investment pattern. Scottish Journal of Geology 51: 131–139.

    Google Scholar 

  • Krings, M., and T.N. Taylor. 2015b. Mantled fungal reproductive units in land plant tissue from the Lower Devonian Rhynie chert. Bulletin of Geosciences 90: 1–6.

    Google Scholar 

  • Krings, M., T.N. Taylor, J. Galtier, and N. Dotzler. 2010. Microproblematic endophytes and epiphytes of fern pinnules from the Upper Pennsylvanian of France. Geobios 43: 503–510.

    Google Scholar 

  • Krings, M., T.N. Taylor, N. Dotzler, and G. Persichini. 2012. Fossil fungi with suggested affinities to the Endogonaceae from the Middle Triassic of Antarctica. Mycologia 104: 835–844.

    Google Scholar 

  • Krings, M., T.N. Taylor, and N. Dotzler. 2013a. Fossil evidence of the zygomycetous fungi. Persoonia 30: 1–10.

    Google Scholar 

  • Krings, M., J.F. White, N. Dotzler, and C.J. Harper. 2013b. A putative zygomycetous fungus with mantled zygosporangia and apposed gametangia from the Lower Coal Measures (Carboniferous) of Great Britain. International Journal of Plant Sciences 174: 269–277.

    Google Scholar 

  • Krings, M., T.N. Taylor, E.L. Taylor, H. Kerp, and N. Dotzler. 2014. First record of a fungal “sporocarp” from the Lower Devonian Rhynie chert. Palaeobiodiversity and Palaeoenvironments 94: 221–227.

    Google Scholar 

  • Krings, M., T.N. Taylor, N. Dotzler, and C.J. Harper. 2016. Morphology and ontogenetic development of Zwergimyces vestitus, a fungal reproductive unit enveloped in a hyphal mantle from the Lower Devonian Rhynie chert. Review of Palaeobotany and Palynology 228: 47–56.

    Google Scholar 

  • Krings, M., C.J. Harper, and E.L. Taylor. 2017a. Fungi and fungal interactions in the Rhynie chert: A review of the evidence, with the description of Perexiflasca tayloriana gen. et sp. nov. Philosophical Transactions of the Royal Society of London (B: Biological Sciences) 373: 20160500.

    Google Scholar 

  • Krings, M., C. Walker, C.J. Harper, H. Martin, S. Sónyi, E. Kustatscher, and T.N. Taylor. 2017b. Unusual fungal reproductive units from the Lower Devonian Rhynie chert. Zitteliana 89: 29–37.

    Google Scholar 

  • Mark, D.F., C.M. Rice, A.E. Fallick, N.H. Trewin, M.R. Lee, A. Boyce, and J.K.W. Lee. 2011. 40Ar/39Ar dating of hydrothermal activity, biota and gold mineralization in the Rhynie hot-spring system, Aberdeenshire, Scotland. Geochimica et Cosmochimica Acta 75: 555–569.

    Google Scholar 

  • Mark, D.F., C.M. Rice, and N.H. Trewin. 2013. Discussion on ‘A high-precision U–Pb age constraint on the Rhynie Chert Konservat-Lagerstätte: time scale and other implications’ (Journal, Vol. 168, 863–872). Journal of the Geological Society of London 170: 701–703.

    Google Scholar 

  • McLean, R.C. 1922. On the fossil genus Sporocarpon. Annals of Botany 36: 71–90.

    Google Scholar 

  • Naito, M., and T.E. Pawlowska. 2016. Defying Muller’s Ratchet: Ancient heritable endobacteria escape extinction through retention of recombination and genome plasticity. mBio 7(3): e02057-15.

    Google Scholar 

  • Naumann, M., A. Schüssler, and P. Bonfante. 2015. The obligate endobacteria of arbuscular mycorrhizal fungi are ancient heritable components related to the Mollicutes. ISME Journal 4: 862–871.

    Google Scholar 

  • Norros, V., E. Karhu, J. Nordén, A.V. Vähätalo, and O. Ovaskainen. 2015. Spore sensitivity to sunlight and freezing can restrict dispersal in wood-decay fungi. Ecology and Evolution 5: 3312–3326.

    Google Scholar 

  • Novais, C.B. de, C. Sbrana, O.J. Saggin Júnior, J.O. Siqueira, and M. Giovannetti. 2013. Vegetative compatibility and anastomosis formation within and among individual germlings of tropical isolates of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23: 325–331.

    Google Scholar 

  • Novais, C.B. de, A. Pepe, J. Oswaldo Siqueira, M. Giovannetti, and C. Sbrana. 2017. Compatibility and incompatibility in hyphal anastomosis of arbuscular mycorrhizal fungi. Scientia Agricola 74: 411–416.

    Google Scholar 

  • Parry, S.F., S.R. Noble, Q.G. Crowley, and C.H. Wellman. 2011. A high precision U–Pb age constraint on the Rhynie chert Konservat-Lagerstätte: time scale and other implications. Journal of the Geological Society of London 168: 863–872.

    Google Scholar 

  • Powell, C.L., N.H. Trewin, and D. Edwards. 2000. Palaeoecology and plant succession in a borehole through the Rhynie cherts, Lower Old Red Sandstone, Scotland. Geological Society of London Special Publication 180: 439–457.

    Google Scholar 

  • Rice, C.M., N.H. Trewin, and L.I. Anderson. 2002. Geological setting of the Early Devonian Rhynie cherts, Aberdeenshire, Scotland: an early terrestrial hot spring system. Journal of the Geological Society of London 159: 203–214.

    Google Scholar 

  • Roesti, D., K. Ineichen, O. Braissant, D. Redecker, A. Wiemken, and M. Aragno. 2005. Bacteria associated with spores of the arbuscular mycorrhizal fungi Glomus geosporum and Glomus constrictum. Applied and Environmental Microbiology 71: 6673–6679.

    Google Scholar 

  • Shahzad, R., A.L. Khan, S. Bilal, S. Asaf, and I.-J. Lee. 2018. What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Frontiers in Plant Science 9: 24.

    Google Scholar 

  • Stubblefield, S.P., T.N. Taylor, C.E. Miller, and G.T. Cole. 1983. Studies in Carboniferous fungi. II. The structure and organization of Mycocarpon, Sporocarpon, Dubiocarpon, and Coleocarpon (Ascomycotina). American Journal of Botany 70: 1482–1498.

    Google Scholar 

  • Taylor, T.N., and J.F. White Jr. 1989. Fossil fungi (Endogonaceae) from the Triassic of Antarctica. American Journal of Botany 76: 389–396.

    Google Scholar 

  • Taylor, T.N., J. Galtier, and B.J. Axsmith. 1994. Fungi from the Lower Carboniferous of central France. Review of Palaeobotany and Palynology 83: 253–260.

    Google Scholar 

  • Taylor, T.N., M. Krings, N. Dotzler, and J. Galtier. 2011. The advantage of thin sections over acetate peels in the study of late Paleozoic fungi and other microorganisms. Palaios 26: 239–244.

    Google Scholar 

  • Taylor, T.N., M. Krings, and E.L. Taylor. 2015. Fossil fungi, 1st ed. Amsterdam, Boston, Heidelberg, London: Elsevier/Academic Press Inc.

    Google Scholar 

  • Trewin, N.H., and S.R. Fayers. 2016. Macro to micro aspects of the plant preservation in the Early Devonian Rhynie cherts, Aberdeenshire, Scotland. Earth and Environmental Sciences Transactions of the Royal Society of Edinburgh 106: 67–80.

    Google Scholar 

  • Trewin, N.H., and H. Kerp. 2017. The Rhynie and Windyfield cherts, Early Devonian, Rhynie, Scotland. In Terrestrial Conservation Lagerstätten. Windows into the evolution of life on land, eds. N.C. Fraser and H.D. Sues, 1–38. Edinburgh: Dunedin Academic Press.

    Google Scholar 

  • Trewin, N.H., and C.M. Rice. 1992. Stratigraphy and sedimentology of the Devonian Rhynie chert locality. Scottish Journal of Geology 28: 37–47.

    Google Scholar 

  • Verma, S.K., and J.F. White. 2018. Indigenous endophytic seed bacteria promote seedling development and defend against fungal disease in browntop millet (Urochloa ramosa L.). Journal of Applied Microbiology 124: 764–778.

    Google Scholar 

  • Verma, S.K., K. Kingsley, I. Irizarry, M. Bergen, R.N. Kharwar, and J.F. White. 2017. Seed-vectored endophytic bacteria modulate development of rice seedlings. Journal of Applied Microbiology 122: 1680–1691.

    Google Scholar 

  • Walker, C., C.J. Harper, M.C. Brundrett, and M. Krings. 2018. Looking for arbuscular mycorrhizal fungi (AMF) in the fossil record: An illustrated guide. In Transformative Paleobotany: Papers to Commemorate the Life and Legacy of Thomas N. Taylor, eds. M. Krings, C.J. Harper, N.R. Cúneo, and G.W. Rothwell, 481–517. London, San Diego, CA, Cambridge, MA, Oxford: Elsevier/Academic Press Inc.

    Google Scholar 

  • Wellman, C.H. 2006. Spore assemblages from the Lower Devonian ‘Lower Old Red Sandstone’ deposits of the Rhynie outlier, Scotland. Transactions of the Royal Society of Edinburgh, Earth Sciences 97: 167–211.

    Google Scholar 

  • Wellman, C.H. 2017. Palaeoecology and palaeophytogeography of the Rhynie chert plants: further evidence from integrated analysis of in situ and dispersed spores. Philosophical Transactions of the Royal Society of London (B: Biological Sciendes) 373: 20160491.

    Google Scholar 

  • Wellman, C.H., H. Kerp, and H. Hass. 2006. Spores of the Rhynie chert plant Aglaophyton (Rhynia) major (Kidston and Lang) D.S. Edwards, 1986. Review of Palaeobotany and Palynology 142: 229–250.

    Google Scholar 

  • White Jr., J.F., and T.N. Taylor. 1989. Triassic fungi with suggested affinities to the Endogonales (Zygomycotina). Review of Palaeobotany and Palynology 61: 53–61.

    Google Scholar 

  • White Jr., J.F., K.L. Kingsley, S. Butterworth, L. Brindisi, J.W. Gatei, M.T. Elmore, S.K. Verma, X. Yao, and K.P. Kowalski. 2019. Seed-vectored microbes: their roles in improving seedling fitness and competitor plant suppression. In Seed endophytes, eds. S.K. Verma and J.F. White Jr., 3–20. Cham: Springer.

    Google Scholar 

  • Yao, Y.J., D.N. Pegler, and T.W.K. Young. 1996. Genera of endogonales, 1–299. Surrey: Royal Botanic Gardens.

    Google Scholar 

Download references

Acknowledgements

We thank E. Lange and H. Martin (both Munich, Germany) for technical assistance, and James F. White Jr. (New Brunswick, NJ, USA) and an anonymous referee for insightful comments that improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Krings.

Additional information

Handling Editor: Mike Reich.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Krings, M., Harper, C.J. Morphological diversity of fungal reproductive units in the Lower Devonian Rhynie and Windyfield cherts, Scotland: a new species of the genus Windipila. PalZ 94, 619–632 (2020). https://doi.org/10.1007/s12542-019-00507-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12542-019-00507-5

Keywords

  • Fossil fungi
  • Fungal paleodiversity
  • Hyphal mantle
  • Glomeromycota
  • Reproduction
  • Subtending hypha