Skip to main content
Log in

Biodeterioration of Antarctic fossil penguin bones caused by lichens from the Eocene La Meseta Formation

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

A large part of the Antarctic surface is covered by lichens since they can withstand extreme environmental conditions. Lichens are primary colonizers and contribute to soil formation by deteriorating rocks through a combination of chemical and physical mechanisms. Therefore, fossil remains found exposed on the surface are usually colonized by epilithic and endolithic lichens. The objective of this work is to determine the biodeterioration generated by lichens on fossil remains and its taphonomic implications. We identified the presence of the euendolithic lichens Lecidea andersonii and Athallia holocarpa growing into fossil penguin bones from Antarctica. The bioerosive damage was evaluated using light and electron microscopic techniques. Pits corresponding to apothecium and sinuous thin fissures remodeled, or in some cases produced, by hyphae were distinguished from the cracks originating from physical weathering. The maximum depth that hyphae extend inside the bone, probably constrained by the light supply, was established to be 2.5 mm. We provided a tool for the reconstruction of the chronology of the taphonomic events, describing the type and magnitude of the damage into the bones.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

(modified from Montes et al. 2013)

Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Materials reviewed in this work are housed in the collection of the División Paleontología Vertebrados (DPV) of the Museo de La Plata (MLP), La Plata (Argentina): MLP 08-XI-30-3/12A, MLP 08-XI-302-3/12B, and MLP 12-I-20-34.

Code availability

Not applicable.

References

  • Acosta Hospitaleche C, Márquez G, Pérez LM, Rosato V, Cione AL (2011) Lichen bioerosion on fossil vertebrates from the Cenozoic of Patagonia and Antarctica. Ichnos 18:1–8

    Article  Google Scholar 

  • Acosta Hospitaleche CA, Pérez LM, Acosta W, Reguero M (2012) A traumatic fracture in a giant Eocene penguin from Antarctica. Antarct Sci 24:619–624

    Article  Google Scholar 

  • Adamo P, Violante P (1991) Weathering of volcanic rocks from Mt. Vesuvius associated with the lichen Stereocaulon vesuvianum. Pedobiologia 35:209–217

    CAS  Google Scholar 

  • Arup U (2009) The Caloplaca holocarpa group in the Nordic countries, except Iceland. Lichenologist 41:111–130

    Article  Google Scholar 

  • Ascaso C, Wierzchos J, de los Ríos A (1995) Cytological investigations of lithobiontic microorganisms in granitic rocks. Bot Acta 108:474–481

    Article  Google Scholar 

  • Ascaso C, Wierzchos J, Souza-Egipsy V, De los Rios A, Delgado-Rodriguez J (2002) In situ evaluation of the biodeteriorating action of microorganisms and the effects of biocides on carbonate rock of the Jeronimos Monastery (Lisbon). Int Biodeterior Biodegrad 49:1–12

    Article  Google Scholar 

  • Bachmann E (1890) Die Beziehungen der Kalkflechten zu ihrem Substrat. Ber Dtsch Bot Ges 8:141–145

    Google Scholar 

  • Bachmann E (1892) Der Thallus der Kalkflechten. Ber Dtsch Bot Ges 8:141–145

    Google Scholar 

  • Bachmann E (1913) Der Thallus der Kalkflechten II. Ber Dtsch Bot Ges 31:3–12

    Google Scholar 

  • Bachmann E (1919) Der Thallus der Kalkflechten III. Nova Acta Leopol 100:1–80

    Google Scholar 

  • Barker WW, Banfield JF (1996) Biologically versus inorganically mediated weathering reactions: relationship between minerals and extracellular microbial polymers in lithobiontic communities. Chem Geol 132:55–69

    Article  CAS  Google Scholar 

  • Behrensmeyer AK (1978) Taphonomic and ecologic information from bone weathering. Paleobiology 4:150–162

    Article  Google Scholar 

  • Bjelland T, Saebo L, Thorseth IH (2002) The occurrence of biomineralization products in four lichen species growing on sandstone in western Norway. Lichenologist 34:229–440

    Article  Google Scholar 

  • Bjelland T, Grube M, Hoem S, Jorgensen SL, Daae FL, Thorseth IH, Øvreås L (2011) Microbial metacommunities in the lichenerock habitat. Environ Microbiol Rep 3:434–442

    Article  PubMed  Google Scholar 

  • Canfield DE (1991) Pyrite formation and fossil preservation. Taphonomy: releasing the data locked in the fossil record. Geobiology 9:337–387

    Article  Google Scholar 

  • Cione AL, Acosta Hospitaleche C, Pérez LM, Laza JH, César I (2010) Trace fossils on penguin bones from the Miocene of Chubut, Southern Argentina. Alcheringa 34:433–454

    Article  Google Scholar 

  • De los Ríos A, Ascaso C (2005) Contributions of in situ microscopy to the current understanding of stone biodeterioration. Int Microbiol 8:181–188

    Google Scholar 

  • De los Ríos A, Wierzchos J, Sancho LG, Sancho TG, Ascaso C (2005) Ecology of endolithic lichens colonizing granite in continental Antarctica. Lichenologist 37:383–395

    Article  Google Scholar 

  • de Los Ríos A, Cámara B, Del Cura MAG, Rico VJ, Galván V, Ascaso C (2009) Deteriorating effects of lichen and microbial colonization of carbonate building rocks in the Romanesque churches of Segovia (Spain). Sci Total Environ 407:1123–1134

  • De los Ríos A, Perez-Ortega S, Wierzchos J, Ascaso C (2012) Differential effects of biocide treat-ments on saxicolous communities: case study of the Segovia cathedral cloister (Spain). Int Biodeterior Biodegrad 67:64–72

    Article  Google Scholar 

  • Doppelbaur HW (1959) Studien zur Anatomie und Entwicklungsgeschichte einiger endolithischen pyrenocarpen Flechten. Planta 53:246–292

    Article  Google Scholar 

  • Edwards HGM, Farwell DW, Seaward MRD (1991) Raman spectra of oxalates in lichen encrustations on Renaissance frescoes. Spectrochim Acta 47:1531–1539

    Article  Google Scholar 

  • Edwards HGM, Farwell DW, Jenkins R, Seaward MRD (1992) Vibrational Raman spectroscopic studies of calcium oxalate monohydrate and dihydrate in lichen encrustations and Renaissance frescoes. J Raman Spectrosc 23:185–189

    Article  CAS  Google Scholar 

  • Edwards HGM, Farwell DW, Seaward MRD (1994a) FT-Raman spectroscopic studies of lichen encrustations on Renaissance frescoes. Deutsche Gesellschaft Für Zerstörungsfreie Prüfung E 45:743–752

    Google Scholar 

  • Edwards HGM, Edwards KAE, Farwell DW, Lewis IR, Seaward MRD (1994b) An approach to stone and fresco lichen biodeterioration through Fourier transform Raman microscopic investigation of thallus-substratum encrustations. J Raman Spectrosc 25:99–103

    Article  CAS  Google Scholar 

  • Francischini H, Lucas SG, Dentzien-Dias P, Schultz CL (2020) Recent root damages of fossilized vertebrate remains from New Mexico, USA. In: Martínez S, Rojas A, Cabrera F (eds) Actualistic taphonomy in South America. Springer, Cham, pp 139–150

    Chapter  Google Scholar 

  • Frank-Kamenetskaya OV, Ivanyuk GY, Zelenskaya MS, Izatulina AR, Kalashnikov AO, Vlasov DY, Polyanskaya EI (2019) Calcium oxalates in lichens on surface of apatite-nepheline ore (Kola Peninsula, Russia). Minerals 9:656

    Article  CAS  Google Scholar 

  • Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215:1045–1053

    Article  CAS  PubMed  Google Scholar 

  • Friedmann EI, Ocampo-Friedmann R (1984) Endolithic microorganisms in extreme dry environments: analysis of a lithobiontic microbial habitat. In: Klug MJ, Reddy CA (eds) Current perspectives in microbial ecology. proceedings of the Third International Symposium on Microbial Ecology. American Society for Microbiology, Washington D.C., pp 177–185

  • Fry EJ (1922) Some types of endolithic limestone lichens. Ann Bot 36:541–562

    Article  Google Scholar 

  • Fry EJ (1927) The mechanical action of crustaceous lichens on substrata of shale, schist, gneiss, limestone, and obsidian. Ann Bot 41:437–460

    Article  CAS  Google Scholar 

  • Galván Josa V, Fracchia D, Castellano G, Crespo E, Kang A, Bonetto R (2013) Backscattered electron images, X-ray maps and Monte Carlo simulations applied to the study of plagioclase composition in volcanic rocks. Spectrochim Acta Part B At Spectrosc 8:50–58

  • García R, Márquez G, Hospitaleche CA (2020) Richness of lichens growing on Eocene fossil penguin remains from Antarctica. Polar Biol 43:2011–2019

    Article  Google Scholar 

  • Gazzano C, Favero-Longo SE, Matteucci E, Roccardi A, Piervittori R (2009) Index of lichen potential biodeteriogenic activity (LPBA): a tentative tool to evaluate the lichen impact on stonework. Int Biodeterior Biodegrad 63:836–843

    Article  Google Scholar 

  • Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sediment Petrol 51:475–478

    Google Scholar 

  • Gouiric-Cavalli S, Rasia LL, Márquez GJ, Rosato V, Scasso RA, Reguero M (2018) First pachycormiform (Actinopterygii, Pachycormiformes) remains from the late jurassic of the Antarctic Peninsula and remarks on bone alteration by recent bioeroders. J Vertebr Paleontol 38:e1524384

    Article  Google Scholar 

  • Jones D, Wilson MJ, Tait JM (1980) Weathering of a basalt by Pertusaria corellina. Lichenologist 12:277–289

  • Kappen L, Friedmann EI, Garty J (1981) Ecophysiology of lichens in the dry valleys of Southern Victoria Land, Antarctica. I. Microclimate and the cryptoendolithic lichen habitat. Flora 171:216–235

    Article  Google Scholar 

  • Khomutovska N, de Los RA, Jasser I (2021) Diversity and colonization strategies of endolithic cyanobacteria in the cold mountain desert of Pamir. Microorganisms 9:6

    Article  CAS  Google Scholar 

  • Krumbein WE (1969) Über den Einfluss der Microflora auf die exogene Dynamik (Verwitterung und Krustenbildung). Geol Rundsch 58:333–363

    Article  CAS  Google Scholar 

  • Lange OL, Schulze ED, Koch W (1970) Experimentell-ökologische Untersuchungen an Flechten der Negev-Wüste. III. CO2-Gaswechsel und Wasserhaushalt von Krusten- und Blattflechten am natürlichen Standort während der sommerlichen Trockenperiode. Flora 159:525–538

    Article  Google Scholar 

  • Magnin L, Lynch V, García R (2017) Avances en el estudio de biodeterioro asociado a presencia de líquenes en materiales arqueológicos líticos. La Primavera (Santa Cruz, Argentina). Bol Soc Argent 52:409–422

    Article  Google Scholar 

  • Matthes U, Turner SJ, Larson DW (2001) Light attenuation by limestone rock and its constraint on the depth distribution of endolithic algae and cyanobacteria. Int J Plant Sci 162:263–270

    Article  Google Scholar 

  • Mikuláš R (1999a) Notes to the concept of plant trace fossils related to plant-generated sedimentary structures. Bull Czech Geol Surv 74:39–42

    Google Scholar 

  • Mikuláš R (1999b) Fossil corrosive root traces on rock surfaces and bioclasts (Bohemian Cretaceous Basin, Czech Republic). Bull Czech Geol Surv 74:289–292

    Google Scholar 

  • Mikuláš R (2001) Modern and fossil traces in terrestrial lithic substrates. Ichnos 8:177–184

    Article  Google Scholar 

  • Montes M, Nozal F, Santillana SN, Marenssi S, Olivero E (2013) Mapa Geológico de Isla Marambio (Seymour), Antártida; escala 1: 20.000. Serie Cartográfica Geocientífica Antártica Geológico y Minero de España, 1a edición. Buenos Aires, Argentina: Instituto Antártico Argentino

  • Nimis PL, Pinna D, Salvadori O (1992) Licheni e Conservazione dei Monumenti. Editrice Bologna, Bologna

    Google Scholar 

  • Olech M (2004) Lichens of King George Island, Antarctica. Institute of Botany of the Jagiellonian University, Kraków

    Google Scholar 

  • Øvstedal DO, Smith RI (2001) Lichens of Antarctica and South Georgia: a guide to their identification and ecology. Studies in Polar Research, Cambridge University Press, Cambridge

    Google Scholar 

  • Pfretzschner HU (2001) Pyrite in fossil bone. N Jb Geol Palaont Abh 220:1–23

    Article  Google Scholar 

  • Piervittori R, Salvadori O, Laccisaglia A (1994) Literature on lichens and biodeterioration of stonework I. Lichenologist 26:171–192

    Article  Google Scholar 

  • Piervittori R, Salvadori O, Laccisaglia A (1996) Literature on lichens and biodeterioration of stonework II. Lichenologist 28:471–483

    Google Scholar 

  • Piervittori R, Salvadori O, Isocrono D (1998) Literature on lichens and biodeterioration of stonework III. Lichenologist 30:263–277

    Article  Google Scholar 

  • Purvis OW, Halls C (1996) A review of lichens in metal-enriched environments. Lichenologist 28:571–601

    Article  Google Scholar 

  • Ruprecht U, Lumbsch HT, Brunauer G, Green TG, Türk R (2010) Diversity of Lecidea (Lecideaceae, Ascomycota) species revealed by molecular data and morphological characters. Antarct Sci 22:727–741

    Article  Google Scholar 

  • Seaward MRD (1997) Major impacts made by lichens in biodeterioration processes. Int Biodeterior Biodegrad 40:269–273

    Article  Google Scholar 

  • Seaward MRD (2015) Lichens as agents of biodeterioration. In: Upreti D, Divakar P, Shukla V, Bajpai R (eds) Recent advances in lichenology. Springer, New Delhi, pp 189–211

    Chapter  Google Scholar 

  • Seaward MRD, Giacobini C (1988) Oxalate encrustation by the lichen Dirina massiliensis forma sorediata and its role in the deterioration of works of art. In: St.Clair LL, Seaward MRD (eds) Le Pellicole ad Ossalati: Origini e Significato nelle Conversazione della Opere d’Arte. Centro CNR, Milano, pp 115–219

    Google Scholar 

  • Singh S, Nayaka S, Upreti D (2013) Contribution to the lichen flora of Schirmacher Oasis and Larsemann Hills, Antarctica. In: Tripathy SC, Mishra RK, Mohan R, Khare N (eds) Studies in biological sciences and human physiology. Three decades of Indian scientific activities in Antarctica. National Centre for Antarctic and Ocean Research, Vasco-da-Gama, Goa, pp 135–155

    Google Scholar 

  • Sterflinger K, Krumbein WE (1997) Dematiaceous fungi as a major agent for biopitting on Mediterranean marbles and limestones. Geomicrobiol J 14:219–230

    Article  Google Scholar 

  • Syers JK, Iskandar IK (1973) Pedogenic significance of lichens. In: Ahmadjian V, Hale ME (eds) The lichens. Academic Press, New York, pp 225–248

    Chapter  Google Scholar 

  • Talevi M, Brezina S (2019) Bioerosion structures in a late Cretaceous mosasaur from Antarctica. Facies 65:5

    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  CAS  PubMed  Google Scholar 

  • Wessels D, Kappen L (1994) Photosynthetic performance of rock-colonising lichens in the Mountain Zebra National Park, South Africa. Koedoe 36:27–48

    Google Scholar 

Download references

Acknowledgements

This contribution honors Vilma Rosato for helping us in our first steps through the study of endolithic lichens into paleontological contexts. We thank Marcelo Reguero for the access to the materials, and Juan José Moly for the transversal sections. C.A.H. was invited to the field by the National Antarctic Directorate and the Argentine Antarctic Institute. The Argentine Air Force provided logistical support. C.A.H. is particularly grateful to Oceanwide Expeditions, Vlissingen (NL) for financial support. We thank the reviewers Dr. Radek Mikulas and Dr. Leandro Pérez for their useful comments.

Funding

This work was partially supported by grants from ANPCyT, PICT 2017-0043 (GJM) and UNLP N955 (CAH).

Author information

Authors and Affiliations

Authors

Contributions

R.G., C.A.H., and G.M. conceived and designed research. R.G. prepared the samples. R.G., C.A.H., and G.M. analyzed data and interpreted the results. All authors prepared the images, wrote the manuscript, and approved the manuscript.

Corresponding author

Correspondence to Renato García.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

The senior curator of the División Paleontología Vertebrados (Museo de La Plata), La Plata (Argentina) allowed access to the fossil penguin bones analyzed in the present contribution, and the permission for publication of the results, all according to Argentinian laws and requirements, in accordance with the Antarctic Treaty.

Consent to participate

All authors declare having consented to participation in this study.

Consent for publication

All authors declare their consent to the publication of this manuscript.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García, R., Acosta Hospitaleche, C. & Márquez, G. Biodeterioration of Antarctic fossil penguin bones caused by lichens from the Eocene La Meseta Formation. Polar Biol 44, 2243–2254 (2021). https://doi.org/10.1007/s00300-021-02957-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-021-02957-7

Keywords

Navigation