Publications

Forthcoming
Haelewaters, D., Blackwell, M. & Pfister, D.H., Forthcoming. Laboulbeniomycetes: Intimate Fungal Associates of Arthropods. Annual Review of Entomology , 66 (13) , pp. 1-20. Publisher's VersionAbstract
Arthropod–fungus interactions involving the Laboulbeniomycetes have been pondered for several hundred years. Early studies of Laboulbeniomycetes faced several uncertainties. Were they parasitic worms, red algal relatives, or fungi? If they were fungi, to which group did they belong? What was the nature of their interactions with their arthropod hosts? The historical misperceptions resulted from the extraordinary morphological features of these oddly constructed ectoparasitic fungi. More recently, molecular phylogenetic studies, in combination with a better understanding of life histories, have clearly placed these fungi among filamentous Ascomycota (subphylum Pezizomycotina). Species discovery and research on the classification of the group continue today as arthropods, and especially insects, are routinely collected and examined for the presence of Laboulbeniomycetes. Newly armed with molecular methods, mycologists are poised to use Laboulbeniomycetes–insect associations as models for the study of a variety of basic evolutionary and ecological questions involving host–parasite relationships, modes of nutrient intake, population biology, host specificity, biological control, and invasion biology. Collaboration between mycologists and entomologists is essential to successfully advance knowledge of Laboulbeniomycetes and their intimate association with their hosts.
2021
Mitchell, J.K., et al., 2021. Sareomycetes: more diverse than meets the eye. IMA Fungus , 12 (6). Publisher's VersionAbstract

Since its resurrection, the resinicolous discomycete genus Sarea has been accepted as containing two species, one with black apothecia and pycnidia, and one with orange. We investigate this hypothesis using three ribosomal (nuITS, nuLSU, mtSSU) regions from and morphological examination of 70 specimens collected primarily in Europe and North America. The results of our analyses support separation of the traditional Sarea difformis s.l. and Sarea resinae s.l. into two distinct genera, Sarea and ZythiaSarea as circumscribed is shown to comprise three phylospecies, with one corresponding to Sarea difformis s.s. and two, morphologically indistinguishable, corresponding to the newly combined Sarea coeloplataZythia is maintained as monotypic, containing only a genetically and morphologically variable Z. resinae. The new genus Atrozythia is erected for the new species A. klamathicaArthrographis lignicola is placed in this genus on molecular grounds, expanding the concept of Sareomycetes by inclusion of a previously unknown type of anamorph. Dating analyses using additional marker regions indicate the emergence of the Sareomycetes was roughly concurrent with the diversification of the genus Pinus, suggesting that this group of fungi emerged to exploit the newly-available resinous ecological niche supplied by Pinus or another, extinct group of conifers. Our phylogeographic studies also permitted us to study the introductions of these fungi to areas where they are not native, including Antarctica, Cape Verde, and New Zealand and are consistent with historical hypotheses of introduction.

Iturriaga, T., et al., 2021. First collection of the asexual state of Trichaleurina javanica from nature and the placement of Kumanasamuha. Asian Journal of Mycology , 4 (1) , pp. 19-28. Publisher's VersionAbstract
Ascomata of Trichaleurina javanica (Pezizomycetes) are encountered frequently in nature in tropical Asia. Its anamorphic state has been described previously as similar to Kumanasamuha. Our study describes the unusual anamorphic fungal specimen, MOZ170, collected from Gorongosa National Park, Mozambique. The fungal strain MOZ170 is identified using ribosomal DNA sequence data, its morphology is described, and morphological differences between the naturally growing anamorph and in vitro derived culture are compared. Phylogenetic placement of Kumanasamuha sundara was also determined using available data. The internal transcribed spacer (ITS) and partial large ribosomal subunit (LSU) were sequenced. Phylogenetic analyses of LSU supported MOZ170 as the anamorph of T. javanica, and revealed the proper placement of the type species of Kumanasamuha, i.e., K. sundara, within the Dothideomycetes. MOZ170 is characterized by its dark conidiophores growing in tufts, and conidia with curved, appressed crests and ridges. The comparison between naturally growing and in vitro grown cultures showed that the in vitro cultured anamorph had larger conidiogenous cells, larger conidia, and longer and more numerous lateral fertile branches compared to the fungus in nature. The present report represents the first anamorph collected from nature for this genus and one of the few natural collections of the anamorphic state within Chorioactidaceae with the exception of those of Desmazierella species.
Gómez-Zapata, P.A., et al., 2021. Notes on Trochila (Ascomycota, Leotiomycetes), with new species and combinations. MycoKeys , (78) , pp. 21-47.Abstract

Full Citation:

Gómez-Zapata P.A., D. Haelewaters, L. Quijada, D.H. Pfister and M.C. Aime. 2021. Notes on Trochila (Ascomycota, Leotiomycetes), with new species and combinations. MycoKeys 78: 21-47.

 

Studies of Trochila (Leotiomycetes, Helotiales, Cenangiaceae) are scarce. Here, we describe two new species based on molecular phylogenetic data and morphology. Trochila bostonensis was collected at the Boston Harbor Islands National Recreation Area, Massachusetts. It was found on the stem of Asclepias syriaca, representing the first report of any Trochila species from a plant host in the family Apocynaceae. Trochila urediniophila is associated with the uredinia of the rust fungus Cerotelium fici. It was discovered during a survey for rust hyperparasites conducted at the Arthur Fungarium, in a single sample from 1912 collected in Trinidad. Macro- and micromorphological descriptions, illustrations, and molecular phylogenetic analyses are presented. The two new species are placed in Trochila with high support in both our six-locus (SSUITSLSUrpb1rpb2tef1) and two-locus (ITSLSU) phylogenetic reconstructions. In addition, two species are combined in TrochilaTrochila colensoi (formerly placed in Pseudopeziza) and T. xishuangbanna (originally described as the only species in Calycellinopsis). This study reveals new host plant families, a new ecological strategy, and a new country record for the genus Trochila. Finally, our work emphasizes the importance of specimens deposited in biological collections such as fungaria.

K.Abarenkov,, et al., 2021. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Diversity. Publisher's VersionAbstract
Põlme, S., K. Abarenkov, R.H. Nilsson, B.D .Lindahl, K.E. Clemmensen, H. Kauserud, N. Nguyen, R. Kjøller, S.T.  Bates, P. Baldrian, T.G. Frøslev, K. Adojaan, A. Vizzini, A.Suija, D.H. Pfister, et al. 2021. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Diversity.


The cryptic lifestyle of most fungi necessitates molecular identification of the guild in environmental studies. Over the past decades, rapid development and affordability of molecular tools have tremendously improved insights of the fungal diversity in all ecosystems and habitats. Yet, in spite of the progress of molecular methods, knowledge about functional properties of the fungal taxa is vague and interpretation of environmental studies in an ecologically meaningful manner remains challenging. In order to facilitate functional assignments and ecological interpretation of environmental studies we introduce a user friendly traits and character database FungalTraits operating at genus and species hypothesis levels. Combining the information from previous efforts such as FUNGuild and FunFun together with involvement of expert knowledge, we reannotated 10,210 and 151 fungal and Stramenopila genera, respectively. This resulted in a stand-alone spreadsheet dataset covering 17 lifestyle related traits of fungal and Stramenopila genera, designed for rapid functional assignments of environmental studies. In order to assign the trait states to fungal species hypotheses, the scientific community of experts manually categorised and assigned available trait information to 697,413 fungal ITS sequences. On the basis of those sequences we were able to summarise trait and host information into 92,623 fungal species hypotheses at 1% dissimilarity threshold.

2020
Mitchell, J.K. & L., Q., 2020. Proposal to conserve the name Cytospora resinae (Zythia resinae) with a conserved type (Ascomycota). Taxon: The Journal of the International Association for Plant Taxonomy , 69 (5) , pp. 1102-1103. Publisher's Version
Mitchell, J.K. & L., Q., 2020. Proposal to conserve the name Dendrostilbella prasinula against Stilbum viridipes, Belonidium viridiatrum, and B. clarkei (Ascomycota). Taxon: The Journal of the International Association for Plant Taxonomy. , 69 (5) , pp. 1103-1104. Publisher's Version
Pfister, D.H. & Brown, J., 2020. Inspired by Plants: The Glass Flowers as a Window into Botanical Education. Journal of Antiques & Collectibles .Abstract
The Glass Flowers exhibit is one of the major attractions at the Harvard Museum of Natural History. This remarkable collection is the product of the father and son artists-naturalists, Leopold (1822-1895) and Rudolf Blaschka (1857-1939). These renowned artists and glassworkers created life-like models that allow museum visitors to experience both the familiar and the exotic. Their masterful work, informed by detailed studies of each plant from nature, employed inventive methods to shape and color glass; they developed methods to mimic the surface textures and colors of leaves, branches, and flowers. Why did the Blaschkas produce this collection and who inspired them in this endeavor? To answer this question, we look deeply into the initiation of the project and the era in which the models were made.
Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi.
Haelewaters, D., et al., 2020. Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi. Zoological Science. Publisher's VersionAbstract
Harmonia axyridis is an invasive alien ladybird in North America and Europe. Studies show that multiple natural enemies are using Ha. axyridis as a new host. However, thus far, no research has been undertaken to study the effects of simultaneous infection by multiple natural enemies on Ha. axyridis. We hypothesized that high thallus densities of the ectoparasitic fungus Hesperomyces virescens on a ladybird weaken the host’s defenses, thereby making it more susceptible to infection by other natural enemies. We examined mortality of the North American-native Olla v-nigrum and Ha. axyridis co-infected with He. virescens and an entomopathogenic fungus—either Beauveria bassiana or Metarhizium brunneum. Laboratory assays revealed that He. virescens-infected O. v-nigrum individuals are more susceptible to entomopathogenic fungi, but Ha. axyridis does not suffer the same effects. This is in line with the enemy release hypothesis, which predicts that invasive alien species in new geographic areas experience reduced regulatory effects from natural enemies compared to native species. Considering our results, we can ask how He. virescens affects survival when confronted by other pathogens that previously had little impact on Ha. axyridis. View Infographic here
Exploration of marine lichenized fungi as bioindicators of coastal ocean pollution in the Boston Harbor Islands National Park
Nokes, L. & Pfister, D.H., 2020. Exploration of marine lichenized fungi as bioindicators of coastal ocean pollution in the Boston Harbor Islands National Park.Abstract

View Poster Presentation online or as a PDF

Presented at the Mycological Society of America's "MSA 2020: Mycology from the Cloud" virtual conference.

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Saba, M., et al., 2020. New species of Pseudosperma (Agaricales, Inocybaceae) from Pakistan revealed by morphology and multi-locus phylogenetic reconstruction. MycoKeys , (69) , pp. 1-31. Publisher's VersionAbstract
During fungal surveys between 2012 and 2014 in pine-dominated forests of the western Himalayas in Pakistan, several collections of Pseudosperma (Agaricales, Inocybaceae) were made. These were documented, based on morphological and molecular data. During this work, three new species came to light, which are here formally described as Pseudosperma brunneoumbonatumP. pinophilum and P. triacicularis. These species belong in the genus Pseudosperma fide Matheny et al (2019) = Pseudosperma clade fide Matheny (2005) = Inocybe sect. Rimosae s.s. fide Larsson et al. (2009). Macro- and micro-morphological descriptions, illustrations and molecular phylogenetic reconstructions of the studied taxa are provided. The new species are differentiated from their close relatives by basidiospore size and colouration of basidiomata. Molecular phylogenetic relationships are inferred using ITS (ITS1–5.8S–ITS2), nrLSU and mtSSU sequence data. All three newly-described taxa likely share an ectomycorrhizal association with trees in the genus Pinus. In addition, five names are recombined in InospermaMallocybe and Pseudosperma. These are Inosperma vinaceobrunneumMallocybe erratumPseudosperma alboflavellumPseudosperma friabile and Pseudosperma neglectum.
Quijada, L., et al., 2020. Orbilia jesu-laurae (Ascomycota, Orbiliomycetes), a new species of neotropical nematode-trapping fungus from Puerto Rico, supported by morphology and molecular phylogenetics. Willdenowia: Annals of the Botanic Garden and Botanical Museum Berlin , 50 (2) , pp. 241-251. Publisher's VersionAbstract
Orbilia jesu-laurae is a new species of nematode-trapping fungus found on decorticated angiosperm wood in a tropical rainforest in Puerto Rico. The single specimen was studied from fresh apothecia and cultures. Morphology was studied and phylogenetic analysis (rDNA: ITS and LSU) was conducted using both sexual and asexual morphs. Nematodes were added to cultures to verify the formation and morphology of the trapping structures. Our results show that the species is in the Arthrobotrys clade, the phylogenetically closest relative being a possibly Mexican genotype with unknown morphology, erroneously referred to as Arthrobotrys musiformis in GenBank. Macro- and micromorphological, ecological and biogeographic data are provided along with a discussion of closely related species.
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Blackwell, M., Haelewaters, D. & Pfister, D.H., 2020. Laboulbeniomycetes: Evolution, natural history, and Thaxter’s final word. Mycologia , 112. Publisher's VersionAbstract
Historically, thallus-forming Laboulbeniomycetes, including the orders Laboulbeniales and Herpomycetales, were set apart because of their distinctive morphology and ecology. Although some biologists correctly interpreted these arthropod ectoparasites as fungi, even ascomycetes, others thought they were worms, red algae, or members of taxa described especially for them. Speculation on the evolution of the group involving red algae, the morphology-based Floridean Hypothesis, persisted deep into the 20th century, in part because valid alternatives were not presented. Although the distinctive features of Laboulbeniales clearly set them apart from other fungi, the difficulty was in the absence of characters grouping them among the fungi. Thaxter considered the Laboulbeniales to be ascomycetes, but he avoided phylogenetic discussions involved in the Floridean Hypothesis all of his life. Eventually, developmental studies of the life history of Pyxidiophora species, hyphal perithecial ascomycetes with 2-celled ascospores, revealed characters connecting Laboulbeniales to other ascomycetes. The distinctive morphological features of Laboulbeniales (absence of mycelium, a thallus developed from 2-celled ascospores by cell divisions in several planes, arthropod parasitism) can be best understood by comparison with Pyxidiophora. The development of a 3-dimensional thallus composed of true parenchyma occurs not only in Laboulbeniales, but also in Pyxidiophora species. The life history of arthropod ectoparasitism of Laboulbeniales as well as mycoparasitism and phoretic dispersal by arthropods of Pyxidiophora species can be explained by Tranzschel’s Law, originally applied to rust fungi. Molecular analyses including other arthropod-associated fungi have contributed to a better understanding of an enlarged class, Laboulbeniomycetes, which now includes a clade comprising Chantransiopsis, Tetrameronycha, and Subbaromyces. A two-locus phylogenetic tree highlights evolutionary and life history questions with regard to the placement of Herpomycetales as the first diverging lineage of the Laboulbeniomycetes. The sister group for all the Laboulbeniomycetes remains to be discovered.
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Beimforde, C., et al., 2020. Sareomycetes cl. nov.: A new proposal for placement of the resinicolous genus Sarea (Ascomycota, Pezizomycotina). Fungal Systematics and Evolution , 6. Publisher's VersionAbstract

Full citation: Beimforde, C., Schmidt, A.R., Rikkinen, J. and J.K. Mitchell. 2020. Sareomycetes cl. nov.: A new proposal for placement of the resinicolous genus Sarea (Ascomycota, Pezizomycotina). Fungal Systematics and Evolution.

Resinicolous fungi constitute a heterogeneous assemblage of fungi that live on fresh and solidified plant resins. The genus Sarea includes, according to current knowledge, two species, S. resinae and S. difformis. In contrast to other resinicolous discomycetes, which are placed in genera also including non-resinicolous species, Sarea species only ever fruit on resin. The taxonomic classification of Sarea has proven to be difficult and currently the genus, provisionally and based only on morphological features, has been assigned to the Trapeliales (Lecanoromycetes). In contrast, molecular studies have noted a possible affinity to the Leotiomycetes. Here we review the taxonomic placement of Sarea using sequence data from seven phylogenetically informative DNA regions including ribosomal (ITS, nucSSU, mtSSU, nucLSU) and protein-coding (rpb1rpb2mcm7) regions.

We combined available and new sequence data with sequences from major Pezizomycotina classes, especially Lecanoromycetes and Leotiomycetes, and assembled three different taxon samplings in order to place the genus Sarea within the Pezizomycotina. Based on our data, none of the applied phylogenetic approaches (Bayesian Inference, Maximum Likelihood and Maximum Parsimony) supported the placement of Sarea in the Trapeliales or any other order in the Lecanoromycetes. A placement of Sarea within the Leotiomycetes is similarly unsupported. Based on our data, Sarea forms an isolated and highly supported phylogenetic lineage within the "Leotiomyceta". From the results of our multilocus phylogenetic analyses we propose here a new class, order, and family, SareomycetesSareales and Sareaceae in the Ascomycota to accommodate the genus Sarea. The genetic variability within the newly proposed class suggests that it is a larger group that requires further infrageneric classification.

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Haelewaters, D., et al., 2020. Draft Genome Sequence of the Globally Distributed Cockroach-Infecting Fungus Herpomyces periplanetae Strain D. Haelew. 1187d. Microbiology Resource Announcements , 9 (6). Publisher's VersionAbstract
Herpomyces periplanetae is an obligate biotroph of Periplaneta americana, the American cockroach. Its nearly cosmopolitan distribution is shaped by its globally invasive host and the international pet trade. Here, we report the draft genome sequence of H. periplanetae, based on a thallus from P. americana collected in Cambridge, Massachusetts
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Pfister, D.H., Quijada, L. & LoBuglio, K.F., 2020. Geodina (Pezizomycetes: Wynneaceae) has a single widespread species in tropical America. Fungal Systematics and Evolution , 5 (June 2020) , pp. 131-138. Publisher's VersionAbstract

Geodina salmonicolor is shown to be a synonym of G. guanacastensis, the type and only species of the genus. Comparisons of ITS rDNA sequences of a paratype and two recent collections of G. guanacastensis with published ITS sequences of G. salmonicolor, from the Dominican Republic, show that these are nearly identical. When G. salmonicolor was erected no sequences of the type species were available. Morphological comparisons supports the conspecificity. Details regarding the description of G. salmonicolor are pointed out. A four-gene phylogeny places Geodina and Wynnea as a supported sister group to the rest of the Sarcoscyphaceae. Species in these genera share morphological traits of cyanophobic spore markings, dark angular outer excipular cells that give rise to hairs and the origin of several apothecia from a common basal stalk. Their occurrence on soil rather than on wood or plant material distinguish them from other Sarcoscyphaceae. Based on morphology, phylogenic relationships and trophic interactions we erect a new family, Wynneaceae, for Geodina and Wynnea.

L, Q., et al., 2020. Cones, needles and wood: Micraspis (Micraspidaceae, Micraspidales fam. et ord. nov.) speciation segregates by host plant tissues. Fungal Systematics and Evolution , 5 , pp. 99-111. Publisher's VersionAbstract
Micraspis acicola was described more than 50 years ago to accommodate a phacidium-like fungus that caused a foliar disease of Picea mariana. After its publication, two more species were added, M. strobilina and M. tetraspora, all of them growing on Pinaceae in the Northern Hemisphere, but each species occupying a unique type of host tissue (needles, cones or wood). Micraspis is considered to be a member of class Leotiomycetes, but was originally placed in Phacidiaceae (Phacidiales), later transferred to Helotiaceae (Helotiales) and recently returned to Phacidiales but in a different family (Tympanidaceae). The genus remains poorly sampled, and hence poorly understood both taxonomically and ecologically. Here, we use morphology, cultures and sequences to provide insights into its systematic position in Leotiomycetes and its ecology. Our results show that the genus should not be included in Tympanidaceae or Phacidiaceae, and support the erection of a new family and order with a unique combination of morphological features supported by molecular data
2019
A new nematode trapping Orbilia from Puerto Rico Presented at the 2019 Mycological Society of America Annual Meeting
L., Q., et al., 2019. A new nematode trapping Orbilia from Puerto Rico Presented at the 2019 Mycological Society of America Annual Meeting .Abstract

Little is known about the diversity of Orbiliomycetes from Puerto Rico. Cantrell & Lodge (2008) compiled a list of the fungi from Puerto Rico, and only mentioned four species of Orbilia: O. andina, O. chysocoma, O. delicata and O. cf. gaillardii. During IMC11 in Puerto Rico, 2018, several collections of Orbiliomycetes were found in Juan Enrique Monagas Park during the Ascomycete workshop field trip. Some of these were sent to the Cornell and Farlow Herbaria. One collection caught the attention of Luis Quijada due to its interesting morphological features. This species is not related to any of the species reported by Cantrell & Lodge (2008). The morphology of the asci and ascospores of the sexual morph clearly indicates a relationship with Orbilia auricolor and related species (section Arthrobotrys). The morphology of the strongly mammiform paraphyses and the excipulum with large cortical cells with knob-like glassy caps had never before seen in this section. Our cultures produced an Arthrobotrys-like anamorph most similar to the anamorph of O. blumenaviensis (= A. vermicola), but the conidia are distinctly smaller and never more than 1-septate. Molecular data supports the placement of this Orbilia in series Arthrobotrys. Species in this series produce adhesive networks as trapping organs in the presence of nematodes, and this behavior was confirmed in cultures of this Orbilia. Our phylogenetic analysis shows this species as very distinct from O. blumenaviensis and supports it being new to science.

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Haelewaters, D., et al., 2019. Laboulbeniales (Ascomycota) of the Boston Harbor Islands II (and Other Localities): Species Parasitizing Carabidae, and the Laboulbenia flagellata Species Complex. Northeastern Naturalist , 25 (9).Abstract
This paper presents 13 new records of Laboulbenialean parasites on ground beetles (Coleoptera, Carabidae) from the Boston Harbor Islands National Recreation Area in Massachusetts: Laboulbenia anoplogenii, L. casnoniae, L. clivinalis, L. egens, L. filifera, L. flagellata, L. inflata, L. macrotheca, L. pedicellata, L. terminalis, L. varia-bilis, L. vulgaris, and Peyritschiella geminata. Laboulbenia clivinalis and L. egens are new country records for the US. Moreover, we present additional localities for L. casnoniae, L. clivinalis, L. filifera, L. flagellata, L. inflata, L. pedicellata, L. variabilis, and L. vulgaris. The following new country records are presented: Laboulbenia clivinalis, L. filifera, and L. variabilis from Canada; L. flagellata from the Democratic Republic of the Congo; L. pedicellata from Ukraine; L. vulgaris from Croatia and Slovenia (and the first undoubtful record from Slovakia). Laboulbenia flagellata was found on 11 host species in the genera Agonum, Oxypselaphus, Patrobus, Platynus, and Pterostichus. Using this abundant material, we performed morphometrics to test the hypothesis that L. flagel-lata is a species complex. Specimens cannot be separated based on host genus (Agonum, Pterostichus). One parameter is significant between Pterostichus mutus and each of the 4 Agonum species after applying a strong Bonferroni P-value correction: H1T, the ratio of height of cell I (HC1) to total thallus length (TTL). In addition, we collected fresh material to be able to add a molecular phylogenetic component to test said hypothesis. We generated ITS and nrLSU ribosomal sequences of several species of Laboulbenia, including isolates of L. flagellata from multiple hosts. Phylogenetic inference of the concatenated dataset shows that L. flagellata isolates from 3 host species form 2 distinct clades, providing support for our hypothesis. We also show that L. coneglianensis is sepa-rate from L. flagellata, unequivocally ending a long-standing taxonomic debate. Finally, examination of Roland Thaxter’s 1891–1932 slides led to the designation of lectotypes for L. macrothecia, L. terminalis, and P. geminata.
haelewaters_northeastern_naturalist.pdf
Saba, M., et al., 2019. Geopora ahmadii sp. nov. from Pakistan. Mycotaxon , 134 (2) , pp. 377-389. Publisher's VersionAbstract
A new species, Geopora ahmadii, is described and illustrated based on material from Punjab, Pakistan. This species is characterized by sessile, cup- to saucer-shaped, partly immersed apothecia with whitish to grayish hymenial surfaces; broad ellipsoid, mostly uniguttulate ascospores; and brown excipular hairs. Phylogenetic analyses of the nrDNA ITS region with maximum parsimony, maximum likelihood, and Bayesian inference methods reveal that G. ahmadii is distinct from other described Geopora species. A collection previously identified as Geopora arenosa from Rawalakot, Pakistan, likely represents a second locality of G. ahmadii.

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