A new fossil mushroom is described and illustrated from the Lower Cretaceous Crato Formation of northeast Brazil. Gondwanagaricites magnificus gen. et sp. nov. is remarkable for its exceptional preservation as a mineralized replacement in laminated limestone, as all other fossil mushrooms are known from amber inclusions. Gondwanagaricites represents the oldest fossil mushroom to date and the first fossil mushroom from Gondwana.
Citation: Heads SW, Miller AN, Crane JL, Thomas MJ, Ruffatto DM, Methven AS, et al. (2017) The oldest fossil mushroom. PLoS ONE12(6): e0178327. https://doi.org/10.1371/journal.pone.0178327
Editor: William Oki Wong, Institute of Botany, CHINA
Received: March 26, 2017; Accepted: May 10, 2017; Published: June 7, 2017
Copyright: © 2017 Heads et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper.
Funding: This work was partly supported by US National Science Foundation grant EF-1304622 (to SWH) and EF-1205935 and EF-1502735 (to ANM).
Competing interests: The authors have declared that no competing interests exist.
Exceptionally preserved fossils can shed important and unprecedented light on the history of life. Particularly remarkable deposits, known as Lagerstätten, yield fossils characterized by preservation of soft tissues that decay rapidly and which are not normally preserved. In many cases, large and important groups of soft-bodied organisms would be missing entirely from the fossil record if not for their exceptional preservation in Lagerstätten. Mushrooms, an ecologically important group of fungi in the order Agaricales, produce fleshy, gilled fruiting bodies (called basidiomes) that are rarely fossilized . While certainly ancient, they have an extremely depauperate fossil record with only ten fossil mushrooms reported to date, all unique amber inclusions ranging from mid-Cretaceous to Early Miocene in age [2–8]. Here we report the discovery of a new fossil mushroom that is unique in its preservation as a mineralized replacement, and the oldest yet encountered. The specimen comes from the laminated limestones of the Crato Formation, which outcrop on the northern flanks of the Chapada do Araripe in Ceará, Brazil; a Lagerstätte famous for the exceptional preservation of its diverse Lower Cretaceous paleobiota [9–11].
Material and methods
The specimen comprises a single, nearly complete mushroom preserved as a primarily goethitic replacement on a small slab (approximately 50 × 60 mm) of typical, buff-colored, millimetrically-laminated limestone from the Nova Olinda Member; the lowermost unit of the Crato Formation. It is housed in the URM Herbarium at the Universidade Federal de Pernambuco in Recife, Brazil, having been repatriated from the Illinois Natural History Survey Paleontological Collection. It was studied using a Zeiss SteREO Discovery.V20 zoom stereomicroscope with a Plan-Apochromat S 0.63x f/ Reo WD = 81 mm objective. Photographs were taken using a Canon 5D Mark III and MP-E 65 mm macro lens mounted to a Cognisys Stackshot motor rail on a copy stand. Multiple high-resolution images were then stacked using HeliconSoft’s Helicon Focus 6 and subsequently stitched together as a mosaic using Photoshop CC. Scanning electron micrographs were produced using a JEOL JSM-6060LV SEM.
The electronic version of this article in Portable Document Format (PDF) in a work with an ISSN or ISBN will represent a published work according to the International Code of Nomenclature for algae, fungi, and plants, and hence the new names contained in the electronic publication of a PLOS ONE article are effectively published under that Code from the electronic edition alone, so there is no longer any need to provide printed copies. In addition, new names contained in this work have been submitted to MycoBank from where they will be made available to the Global Names Index. The unique MycoBank number can be resolved and the associated information viewed through any standard web browser by appending the MycoBank number contained in this publication to the prefix http://mycobank.org/MB/. The online version of this work is archived and available from the following digital repositories: PubMed Central, LOCKSS.
Kingdom Fungi (L.) Moore, 1980; Phylum Basidiomycota Moore, 1980; Class Agaricomycetes Doweld, 2001; Order Agaricales Underwood, 1899; Family incertae sedis
Gondwanagaricites magnificus Heads, A.N. Mill. et J.L. Crane, gen. et sp. nov.
(A) Photomicrograph of holotype (URM 88000) showing general habitus. (B) Interpretive drawing of (A) with major morphological features indicated. The red box indicates the position of gills shown in Fig 2.
(A) Section of preserved gills (location indicated by red box on Fig 1B). (B) close-up view of (A) showing detailed structure.
Brazil: Ceará: Chapada do Araripe; Crato Formation: Nova Olinda Member (Lower Cretaceous: Upper Aptian, 113–120 Ma); URM-88000. While precise locality details are unknown, the lithology of the matrix is consistent with the specimen having been collected in one of the extensive quarry complexes near the town of Nova Olinda (7.0939°S, 39.6796°W).
The genus name is a combination of Gondwana, the ancient supercontinent, the Greek word agarikon, “a mushroom,” and the Greek suffix -ites, denoting a fossil. The specific epithet is the Latin adjective magnificus, meaning “magnificent” or “splendid” in reference to the remarkable preservation of the holotype.
Basidiome color unknown (preserved as orange-brown goethitic replacement). Pileus 10.0 mm diameter, 7.5 mm high at widest point; apparently circular, convex; probably glabrous and striate; margin slightly incurved; veil absent; context 3.0 mm thick. Lamellae (gills) 4.5 mm broad at widest point, broadly attached to stipe apex; edge entire, up to 50μm wide. Stipe 34.0 mm long, 6.5 mm wide, straight, cylindrical, with longitudinal striations, annulus absent, base slightly bulbous. Basidiospores not observed.
While Gondwanagaricites is without doubt a gilled mushroom in the Agaricales, familial placement is presently impossible since no evidence of basidiospores was found during SEM examination of the specimen. The general habitus of Gondwanagaricites is reminiscent of mushrooms in the family Strophariaceae and placement in this family would be supported by the small size and robust shape of the overall basidiome, the thick context of the pileus, the putative complete attachment of the gills to the central stipe, and the apparent absence of a universal and partial veil. However, a number of other mushroom families present similar basidiome morphology (e.g., Agaricaceae, Tricholomataceae, Bolbitiaceae, etc.) and can only be separated by detailed studies of basidiospore shape, ornamentation, and coloration. Thus, since the spores of Gondwanagaricites were not observed, we refrain from assigning the new genus to a family.
Fungi are ecologically diverse, geographically widespread, speciose organisms that account for the second largest group of eukaryotes . Despite their global distribution and evolutionary history extending some 1,430 Ma , the fossil record for fungal structures other than spores is exceedingly scant with reports of mostly sexual [14–18] and asexual stages [19–23] of ascomycetes from mid-Cretaceous to Miocene ambers. The Basidiomycota contains over 30,000 extant species , but their fossil record—especially in the case of gilled mushrooms—is nearly non-existent due to their ephemeral nature and a strong preservational bias against their fleshy basidiomes [1–8]. The earliest report of a member of the Basidiomycota is from hyphae with diagnostic clamp connections dating c. 330 Ma from the Upper Visean (Mississippian) of France . Only ten fossils resembling modern-day gilled mushrooms have been recorded to date, all from amber. The hitherto oldest fossil mushroom, Palaeoagaricites antiquus, was reported from mid-Cretaceous Burmese amber (c. 99 Ma) . More recently, four unnamed mushrooms placed in the Agaricales have also been reported from Burmese amber . Archaeomarasmius leggetti was recorded from Cretaceous amber (c. 90–94 Ma) from New Jersey, USA [3,4]. Most recently, Gerontomyces lepidotus was reported from Eocene Baltic amber (c. 45–55 Ma) from the Samland Peninsula of Russia . Three other mushrooms, Aureofungus yaniguaensis , Coprinites dominicana , and Protomycena electra [3,4] have all been recorded from Early Miocene amber (Burdigalian, c. 16–18 Ma) from the Dominican Republic.
Gondwanagaricites magnificus represents the oldest fossil record of a gilled mushroom and is the only fossil mushroom known from a mineralized replacement. The unique specimen extends the geological range of gilled mushrooms back by approximately 14–21 million years and confirms their presence in Gondwana during the Early Cretaceous. Molecular clock estimates suggest the divergence of the Basidiomycota around 500 Ma to 1.2 billion years  and G. magnificus establishes the earliest calibration point so far for the Agaricales, with a new minimum age of 113–120 Ma.
We thank Dra. Leonor Costa Maia of the URM Herbarium for providing a URM accession number and for assistance repatriating the specimen to Brazil. SEM work was carried out in the Frederick Seitz Materials Research Laboratory Central Research Facilities at the University of Illinois. This work was partly supported by NSF grant EF-1304622 (to SWH) and EF-1205935 and EF-1502735 (to ANM).
- Conceptualization: SWH.
- Investigation: SWH ANM JLC MJT DMR ASM DBR.
- Resources: YW.
- Visualization: MJT DMR.
- Writing – original draft: SWH ANM JLC MJT DMR ASM.
- 1. Taylor TM, Krings M, Taylor EL. Fossil Fungi. London: Elsevier/Academic Press; 2015.
- 2. Poinar GO, Singer R. Upper Eocene gilled mushroom from the Dominican Republic. Science 1990;248: 1099–1101. pmid:17733372
- 3. Hibbett DS, Grimaldi G, Donoghue MJ. Cretaceous mushrooms in amber. Nature 1995;377: 487.
- 4. Hibbett DS, Grimaldi D, Donoghue MJ. Fossil mushrooms from Miocene and Cretaceous ambers and the evolution of Homobasidiomycetes. American Journal of Botany 1997;84: 981–991. pmid:21708653
- 5. Hibbett DS, Binder M, Wang Z, Goldman Y. Another fossil agaric from Dominican amber. Mycologia 2003;95: 685–687. pmid:21148976
- 6. Poinar GO, Buckley R. Evidence of mycoparasitism and hypermycoparasitism in Early Cretaceous amber. Mycological Research 2007;111: 503–506. pmid:17512712
- 7. Poinar GO. A gilled mushroom, Gerontomyces lepidotus gen. et sp. nov. (Basidiomycota: Agaricales), in Baltic amber. Fungal Biology 2016;120: 1090–1093. pmid:27567715
- 8. Cai C, Leschen RAB, Hibbett DS, Xia F, Huang D. Mycophagous rove beetles highlight diverse mushrooms in the Cretaceous. Nature Communications 2017; 8:14894: 1–7.
- 9. Martill DM. Fossils of the Santana and Crato Formation, Brazil. London: The Palaeontological Association; 1993.
- 10. Martill DM, Bechly G, Loveridge RF. The Crato Fossil Beds of Brazil: Window into an Ancient World. Cambridge: Cambridge University Press; 2007.
- 11. Barling N, Martill DM, Heads SW, Gallien F. High fidelity preservation of fossil insects from the Crato Formation (Lower Cretaceous) of Brazil. Cretaceous Research 2015;52: 605–622.
- 12. Purvis A, Hector A. Getting the measure of biodiversity. Nature 2000;405: 212–219. pmid:10821281
- 13. Butterfield NJ. Probably Proterozoic fungi. Paleobiology 2005;31: 165–182.
- 14. Caspary R, Klebs R. Die Flora des Bernsteins und anderer fossiler Harze des ostpeussischen Tertiars. Berlin: Koniglisch Preußische Geologische Landesanstalt; 1906.
- 15. Mägdefrau K. Flechten und Moose im baltischen Bernstein. Berichte der Deutschen Botanischen Gesellschaft 1957;71: 433–435.
- 16. Rikkinen J, Poinar GO. A new species of resinicolous Chaenothecopsis (Mycocaliciaceae, Ascomycota) from 20 million year old Bitterfeld amber, with remarks on the biology of resinicolous fungi. Mycological Research 2000;104: 7–15.
- 17. Rossi W, Kotrba M, Tribbell D. A new species of Stigmatomyces from Baltic amber, the first fossil record of Laboulbeniomycetes. Mycological Research 2005;109: 271–274. pmid:15912943
- 18. Taylor TN, Hass H, Kerp H, Krings M, Hanlin RT. Perithecial ascomycetes from the 400 million year old Rhynie chert: an example of ancestral polymorphism. Mycologia 2005;97: 269–285. pmid:16389979
- 19. Thomas GM, Poinar GO. A fossil Aspergillus from Eocene Dominican amber. Journal of Paleontology 1988;62: 141–143.
- 20. Rikkinen J, Dorfelt H, Schmidt AR, Wunderlich J. Sooty moulds from European Tertiary amber, with notes on the systematic position of Rosaria (‘Cyanobacteria’). Mycological Research 2003;107: 251–256. pmid:12747338
- 21. Dorfelt H, Schmidt AR. A fossil Aspergillus from Baltic amber. Mycological Research 2005;109: 956–960. pmid:16175799
- 22. Dorfelt H, Schmidt AR. A conifer seedling with two herbicolous fungi from Baltic amber forest. Botanical Journal of the Linnean Society 2007;155: 449–456.
- 23. Sadowski E-M, Beimforde C, Gube M, Rikkinen J, Singh H, Seyfullah LJ, et al. The anamorphic genus Monotosporella (Ascomycota) from Eocene amber and from modern Agathis resin. Fungal Biology 2012;116: 1099–1110. pmid:23063189
- 24. Taylor TN, Taylor EL, Krings M. Paleobotany: the Biology and Evolution of Fossil Plants. 2nd ed. London: Academic Press; 2008.
- 25. Krings M, Dotzler N, Galtier J, Taylor TN. Oldest fossil basidiomycete clamp connections. Mycoscience 2011;52: 18–23.
- 26. Berbee ML, Taylor JW. Dating the molecular clock in fungi–how close are we? Fungal Biology Reviews 2010;24: 1–16.