Christina Beimforde

Estimating the Phanerozoic history of the Ascomycota lineages: Combining fossil and molecular data

The phylum Ascomycota is by far the largest group in the fungal kingdom. Ecologically important mutualistic associations such as mycorrhizae and lichens have evolved in this group, which are regarded as key innovations that supported the evolution of land plants. Only a few attempts have been made to date the origin of Ascomycota lineages by using molecular clock methods, which is primarily due to the lack of satisfactory fossil calibration data. For this reason we have evaluated all of the oldest available ascomycete fossils from amber (Albian to Miocene) and chert (Devonian and Maastrichtian). The fossils represent five major ascomycete classes (Coniocybomycetes, Dothideomycetes, Eurotiomycetes, Laboulbeniomycetes, and Lecanoromycetes). We have assembled a multi-gene data set (18SrDNA, 28SrDNA, RPB1 and RPB2) from a total of 145 taxa representing most groups of the Ascomycota and utilized fossil calibration points solely from within the ascomycetes to estimate divergence times of Ascomycota lineages with a Bayesian approach. Our results suggest an initial diversification of the Pezizomycotina in the Ordovician, followed by repeated splits of lineages throughout the Phanerozoic, and indicate that this continuous diversification was unaffected by mass extinctions. We suggest that the ecological diversity within each lineage ensured that at least some taxa of each group were able to survive global crises and rapidly recovered.

Ectomycorrhizas from a Lower Eocene angiosperm forest.

The development of mycorrhizal associations is considered a key innovation that enabled vascular plants to extensively colonize terrestrial habitats. Here, we present the first known fossil ectomycorrhizas from an angiosperm forest. Our fossils are preserved in a 52 million-yr-old piece of amber from the Tadkeshwar Lignite Mine of Gujarat State, western India. The amber was produced by representatives of Dipterocarpaceae in an early tropical broadleaf forest. The ectomycorrhizas were investigated using light microscopy and field emission scanning electron microscopy. Dissolving the amber surrounding one of the fossils allowed ultrastructural analyses and Raman spectroscopy. Approx. 20 unramified, cruciform and monopodial-pinnate ectomycorrhizas are fossilized adjacent to rootlets, and different developmental stages of the fossil mycorrhizas are delicately preserved in the ancient resin. Compounds of melanins were detectable in the dark hyphae. The mycobiont, Eomelanomyces cenococcoides gen. et spec. nov., is considered to be an ascomycete; the host is most likely a dipterocarp representative. An early ectomycorrhizal association may have conferred an evolutionary advantage on dipterocarps. Our find indicates that ectomycorrhizas occurred contemporaneously within both gymnosperms (Pinaceae) and angiosperms (Dipterocarpaceae) by the Lower Eocene.

Stuck in time – a new Chaenothecopsis species with proliferating ascomata from Cunninghamia resin and its fossil ancestors in European amber

Resin protects wounded trees from microbial infection, but also provides a suitable substrate for the growth of highly specialized fungi. Chaenothecopsis proliferatus is described growing on resin of Cunninghamia lanceolata from Hunan Province, China. The new fungus is compared with extant species and two new fossil specimens from Eocene Baltic and Oligocene Bitterfeld ambers. The Oligocene fossil had produced proliferating ascomata identical to those of the newly described species and to other extant species of the same lineage. This morphology may represent an adaptation to growing near active resin flows: the proliferating ascomata can effectively rejuvenate if partially overrun by fresh, sticky exudate. Inward growth of fungal hyphae into resin has only been documented from Cenozoic amber fossils suggesting comparatively late occupation of resin as substrate by fungi. Still, resinicolous Chaenothecopsis species were already well adapted to their special ecological niche by the Eocene, and the morphology of these fungi has since remained remarkably constant.

Microbes in Resinous Habitats: A Compilation from Modern and Fossil Resins

Amber can be considered as a window into the past allowing insights into the palaeoecology of Mesozoic and Cenozoic woodlands. Insects, spiders, fragments of higher plants and even small vertebrates were trapped by resins of conifers and angiosperms of the ancient “amber forests”.

The anamorphic genus Monotosporella (Ascomycota) from Eocene amber and from modern Agathis resin.

The anamorphic fungal genus Monotosporella (Ascomycota, Sordariomycetes) has been reco-vered from a piece of Early Eocene Indian amber, as well as from the surface of extant resin flows in New Caledonia. The fossil fungus was obtained from the Tarkeshwar Lignite Mine of Gujarat State, western India, and was part of the biota of an early tropical angiosperm rainforest. The amber inclusion represents the second fossil record of Sordariomycetes, as well as the first fossil of its particular order (either Savoryellales or Chaetosphaeriales). The fossil fungus is distinguished from extant representatives by possessing both short conidiophores and small two-septate pyriform conidia, and is described as Monotosporella doerfeltii sp. nov. Inside the amber, the anamorph is attached to its substrate, which is likely the degraded thallus of a cladoniform lichen. The extant New Caledonian species is assigned to Monotosporella setosa. It was found growing on semi-solidified resin flows of Agathis ovata (Araucariaceae), and is the first record of Monotosporella from modern resin substrates.

Resinogalea humboldtensis gen. et sp. nov., a New Resinicolous Fungus from New Caledonia, Placed in Bruceomycetaceae fam. nova (Ascomycota)

A novel species of ascomycetes is described from resin of Araucaria humboldtensis on Mont Humboldt in New Caledonia. The fungus is placed in the new genus Resinogalea Rikkinen & A.R. Schmidt, with the species name R. humboldtensis Rikkinen & A.R. Schmidt. It has only been found growing on semi-hardened resin flows on branches of its endemic and endangered conifer host. The morphology and anatomy of the new fungus are compared with those of ecologically similar taxa, including Bruceomyces castoris. The new family Bruceomycetaceae Rikkinen & A.R. Schmidt is described to accommodate Resinogalea and Bruceomyces.

Resin exudation and resinicolous communities on Araucaria humboldtensis in New Caledonia

Conifers of the endemic species Araucaria humboldtensis on Mont Humboldt in New Caledonia exhibit extensive resin exudation. The resin flows of these threatened trees are here shown to be induced by two beetle species, which bore into branches and branchlets, leading to abundant outpouring of resin, which gradually solidifies into often drop-shaped resin bodies. The exudate is colonized by a resinicolous and likely insect-vectored ascomycete, Resinogalea humboldtensis, which is only known from Mont Humboldt. The fungus grows into fresh resin and eventually develops ascomata on the surface of solidifying resin. The solidified resin is also colonized by another fungus, a dematiaceous hyphomycete. Based on protein coding (CO1, CAD, ArgK) and ribosomal (LSU) genes, the larger branch-boring beetle is a weevil of the tribe Araucariini, which represents the sister group of all other cossonine weevils. The smaller beetle species belongs to the longhorn beetles (Cerambycidae). The strong host specificity of the Araucariini, along with the occurrence of two unique fungi, suggests that the resin-associated community is native and has evolved on the endemic conifer host. The formation of large amber deposits indicates massive resin production in the past, but the environmental triggers of exudation in Mesozoic and Cenozoic ecosystems remain unclear. Our observations from Mont Humboldt support the notion that the occurrences of small drop-shaped amber pieces in Triassic to Miocene amber deposits were linked to ancient insect infestations.

Production and preservation of resins - past and present.

Amber is fossilised plant resin. It can be used to provide insights into the terrestrial conditions at the time the original resin was exuded. Amber research thus can inform many aspects of palaeontology, from the recovery and description of enclosed fossil organisms (biological inclusions) to attempts at reconstruction of past climates and environments. Here we focus on the resin itself, the conditions under which it may have been exuded, and its potential path to fossilisation, rather than on enclosed fossils. It is noteworthy that not all plants produce resin, and that not all resins can (nor do) become amber. Given the recent upsurge in the number of amber deposits described, it is time to re‐examine ambers from a botanical perspective. Here we summarise the state of knowledge about resin production in modern ecosystems, and review the biological and ecological aspects of resin production in plants. We also present new observations on conifer‐derived resin exudation, with a particular focus on araucarian conifer trees. We suggest that besides disease, insect attacks and traumatic wounding from fires and storms, other factors such as tree architecture and local soil conditions are significant in creating and preserving resin outpourings. We also examine the transformation of resin into amber (maturation), focusing on geological aspects of amber deposit formation and preservation. We present new evidence that expands previous understanding of amber deposit formation. Specific geological conditions such as anoxic burial are essential in the creation of amber from resin deposits. We show that in the past, the production of large amounts of resin could have been linked to global climate changes and environmental disruption. We then highlight where the gaps in our knowledge still remain and potential future research directions.

Chaenothecopsis schefflerae (Ascomycota: Mycocaliciales): a widespread fungus on semi-hardened exudates of endemic New Zealand Araliaceae

ABSTRACT Ascomycetes specialised to live on hardened plant exudates occur worldwide, but the number of species so far described is relatively small (c.30). Particularly within the genus Chaenothecopsis (Ascomycota: Mycocaliciales), many species produce their ascomata on hardened but still relatively fresh outpourings of conifer resin or angiosperm exudate. Temperate rainforests of New Zealand provide habitat for several endemic Chaenothecopsis species, including Chaenothecopsis schefflerae, which was previously known from a single sample collected from the exudate of Schefflera digitata (Araliaceae) in the early 1980s. Here we show that C. schefflerae is neither lost nor very rare, but occurs sporadically throughout New Zealand. The fungus does not primarily grow on Schefflera but on exudate of several species of Pseudopanax (Araliaceae), also endemic to the region. We compare the morphology of the new specimens to the type specimen of C. schefflerae and provide a detailed description of the new material. Phylogenetic analyses based on nuclear ITS and LSU rDNA place C. schefflerae together with other morphologically similar Chaenothecopsis species growing on angiosperm exudates.

Parasitaxus parasitized: novel infestation of Parasitaxus usta (Podocarpaceae)

The world’s sole ‘parasitic’ gymnosperm Parasitaxus usta (Podocarpaceae) is endemic to the island of Grande Terre, New Caledonia. It is a threatened species because of its limited geographic range and progressing habitat fragmentation. Here, we report a novel scale insect outbreak on a Parasitaxus sub-population from Monts Dzumac in the southern part of Grande Terre. The identity of the scale insect was determined through combining morphological and molecular methods. The field collection of scale insects and their secretions from infested Parasitaxus specimens allowed morphological identification of the superfamily Coccoidea. Subsequent genetic sequencing using CO1 markers allowed phylogenetic placement of the wax scale insects to the genus Ceroplastes (Coccoidea, Coccidae), a widespread pest genus. The identified species, C. pseudoceriferus, has not been previously recorded from New Caledonia. As Parasitaxus is already vulnerable to extinction, this new threat to its long-term survival needs to be monitored. Other New Caledonian endemic plant species are potentially at risk of this new species, although it was not observed on Falcatifolium taxoides, the host of Parasitaxus.