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Acaulium caviariforme. a-black ascocarps on dead dormouse body; b-detail of dead dormouse body with black ascocarps of A. caviariforme and white Mortierella sp. growth; c-f-a mass of black ascocarps on bat skeletons from Slovak caves: Guličková Passage in Demänovská Peace Cave (c, d), Ruins Passage in Demänovská Peace Cave (e), Stray Dome in Harmanecká Cave (f). Photo A. Nováková.
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V průběhu dlouhodobého studia mikroskopických hub v osmdesáti evropských podzemních prostorách (jeskyně, opuštěné doly) byly nalezeny také mrtvá těla a kostry živocičhu žijících v tomto prostředí či nahodilých návštěvníků, některé s viditelnými nárosty mikroskopických hub. Přímá izolace, zředovací metoda a různá média byly použity pro izolaci konkr...
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... frog Chaetocladium mainly belong to facultative, gall-forming parasites on other Mucorales (Benny 2005) and strains of this genus were earlier isolated from mar- ten dung in Ardovská Cave as well as from cave sediment of the Domica Cave (Nováková, unpublished). On the contrary, older bat cadavers found in Demänovská Peace Cave and Harmanecká Cave (Fig. 3) as well as dormouse cadavers found in Gombasecká Cave (Slovak Karst, Slovakia) were found to be covered by a mass of black asco- carps of Acaulium caviariforme. The isolation of this species was unsuccessful but its typical morphology enabled reliable identification. In the case of two dor- mouse (Dryomys nitedula) cadavers found in ...
Citations
... Cephalotrichum stemonitis has previously been isolated from bats by Nováková et al. (2018b) in Demanovska Peace Cave, and also Nováková et al. (2018a) in Movile Cave from air, sediments and microbial mat. Under the synonym Doratomyces stemonitis, this species was also isolated from koala feces (Peterson et al., 2011). ...
Our study unveils the complex interplay between fungal diversity and geochemical environments within the Demänovská Slobody Cave, marking the first comprehensive speleomycological and chemical investigation of its kind. Through meticulous analysis using both microscopic techniques and ITS region gene barcoding, we recorded 17 fungal species, including four previously unrecorded in subterranean settings (Cladosporium ramo-tenellum, Porostereum spadiceum, Rhexocercosporidium carotae, and Trichocladium nigrospermum), with Porostereum spadiceum as the most prevalent. These findings illuminate the crucial role of fungi in subterranean biogeo-chemical cycles, demonstrating how nutrient levels and pH significantly influence fungal populations. Namely, the levels of mineral nutrients (N, P, K, Mg, Ca) and organic matter in sediments within the cave were lower than in soil those outside it. Conversely, the pH values of the tested samples inside the cave were higher compared to those outside. Positive correlations were observed between the average number of fungi and the content of N, P, K, CO, and organic matter (p < 0.05). Conversely, the concentration of fungi decreased with increasing levels of Mg, Ca, and pH (p < 0.05). This research not only expands our understanding of cave ecosystems but also sets a new precedent for exploring the ecological impact of fungi in extreme environments.
... However, other authors found fungi in cave biofilms from different countries [7,14,15]. It should be noted that fungi are common in cave air, as well as in excrements, guano, and animal cadavers frequently found in caves and sediments [16,17]. ...
... Among all Mortierella species, the most commonly recovered in caves were M. alpina and M. elongata (=Linnemannia elongata) [24,25,59]. Many species of the genus Mortierella have been isolated from bats, dung samples collected in caves and mines, wings and bat carcasses, in addition to soils where they are abundant [16,[58][59][60]. Podila species are frequent in soils, compost and dung [45]. ...
The Gypsum Karst of Sorbas, Almeria, southeast Spain, includes a few caves whose entrances are open and allow the entry and roosting of numerous bats. Caves are characterized by their diversity of gypsum speleothems, such as stalactites, coralloids, gypsum crusts, etc. Colored biofilms can be observed on the walls of most caves, among which the Covadura and C3 caves were studied. The objective was to determine the influence that bat mycobiomes may have on the fungal communities of biofilms. The results indicate that the fungi retrieved from white and yellow biofilms in Covadura Cave (Ascomycota, Mortierellomycota, Basidiomycota) showed a wide diversity, depending on their location, and were highly influenced by the bat population, the guano and the arthropods that thrive in the guano, while C3 Cave was more strongly influenced by soil- and arthropod-related fungi (Ascomycota, Mortierellomycota), due to the absence of roosting bats.
... Generally, carcasses decompose quickly, which may preclude the formation of fungal reproductive structures directly on the waste (Sagara 1995). However, various species of mold grow on carcasses (Hawksworth and Wiltshire 2011;Ishii et al. 2006;Nováková et al. 2018). Ammonia and postputrefaction fungi undergo a succession of fruiting where one set of fungi is later replaced by another (Sagara 1992(Sagara , 1995. ...
... Animal carcasses are sometimes found in caves where decomposition is slow and carcasses are colonized by molds (Nováková et al. 2018). During routine surveys of hibernating bats , we found small mushrooms growing on the flesh of a muskrat carcass (Ondatra zibethicus) on the ground in an abandoned mine. ...
... Although we did not attempt to identify the variety of molds present on the carcasses, masses of black ascocarps of Acaulium caviariforme were readily identifiable and occurred extensively on the flesh of the muskrat and beaver carcasses. This species is commonly found on carcasses in caves and mines (Nováková et al. 2018). The slow decomposition and fruiting process may also be due to constant low temperatures (6.6 C) in the mine. ...
Fungi are important decomposers of organic material, including animal waste. Ammonia and postputrefaction fungi grow in soil enriched in ammonium and nitrogen from carcasses. In 2014, we observed mushrooms fruiting on the flesh of a dead muskrat (Ondatra zibethicus) in an abandoned underground copper mine in southeastern New Brunswick, Canada. We placed an adult beaver (Castor canadensis) carcass near the muskrat to facilitate fungal colonization and fruiting. The beaver carcass was colonized by a variety of molds, especially Acaulium caviariforme. We observed mushrooms of an unidentified copriniid on the flesh 6 years and 9 months after carcass placement. Using morphological and molecular (nuclear internal transcribed spacer [nrITS]) data, we identified the mushrooms as Coprinopsis laanii, a rarely encountered species generally considered lignicolous. We discuss the role of C. laanii, and other postputrefaction fungi, in cave environments.
... This knowledge is crucial in evaluating the impact of human activities such as tourism on these ecosystems and in designing effective management plans. Furthermore, it will aid in identifying appropriate methods for restoring cave microbiomes in areas of the Satun UNESCO Global Geopark that have been disturbed by tourism 38,52 . ...
Karst caves are distinctive ecosystems that have limited nutrients, darkness, low to moderate temperatures, and high moisture levels, which allow for a diverse range of fungal communities to thrive. Despite their significance, little is understood about the fungi found in karst caves in Thailand. In 2019, we studied the cultured mycobiota from five substrate types (air, water, rock, soil/sediment, and organic debris) in two karst caves (Le Stegodon and Phu Pha Phet Caves) of the Satun UNESCO Global Geopark, southern Thailand. A cumulative count of 829 distinct fungal morphological types was identified, encompassing 319 fungal culturable were observed. Based on preliminary analyses of the internal transcribed spacer (ITS) sequence using BLAST searches, the most common phylum among the fungal morphotypes was Ascomycota, harboring 282 species in 91 genera, 93.4% of which were distributed in the classes Eurotiomycetes, Sordariomycetes, and Dothideomycetes. The most common fungal genera identified in the two karst caves were Aspergillus, Penicillium, Cladosporium, Talaromyces, Xylaria, and Trichoderma, with 45, 41, 24, 14, 14, and 6 species identified, respectively. Discovering fungi in Thai karst caves highlights the extensive fungal diversity in the Satun UNESCO Global Geopark, implying undiscovered species, and emphasizing the need for comprehensive investigations in other unexplored Thai karst caves.
... Fungi are abundant in cave environments (Cunha et al. 2020;Zhang et al. 2021). They can play important roles in the subsurface ecosystem, contributing to the weathering of rocks and minerals, organic matter decaying, nitrogenous and phosphorus cycling, and degradation of recalcitrant compounds, besides serving as food to the cave fauna (Nováková et al. 2018;Joshi and Chettri 2019;Wiseschart and Pootanakit 2020;Zhang et al. 2021). Approximately 2000 fungal species have been reported in the underground environment worldwide, mainly from the genera Aspergillus and Penicillium (Vanderwolf et al. 2013;Zhang et al. 2021). ...
Interest in cave fungal diversity is flourishing because it may represent a reservoir of new species and metabolites. However, the mycobiota remains poorly studied in the underground environment, especially in neotropical regions. During surveys that aimed to investigate the fungal diversity in quartzite and limestone caves in the Southern Espinhaço Mountain in Brazil, six Chaetomiaceae isolates were obtained from different cave substrates. Five taxonomical novelties of Chaetomiaceae in Brazilian caves were discovered based on phylogenetic analyses using DNA sequences from the ITS, LSU, TUB, and RPB2 genes. Chaetomium meridionalense, Pseudohumicola alba, and Pseudohumicola lutea are new species found in Gruta da Extração and Gruta Velha Nova caves. Parahumicola is introduced as a new genus representing a novel phylogenetic lineage with unique morphological characteristics in the family Chaetomiaceae. This new monotypic genus is typified by P. guana, which was found in a bat guano sample in the Gruta Monte Cristo cave. Furthermore, this is the first report of Collariella bostrychodes in a neotropical cave. Overall, these findings emphasise that Brazilian caves constitute an untapped source of fungal resources.
... The SEM images also revealed that many, if not most, of these calcite "spikes" represent, in fact, the exposed tips of spear head-shaped, flat hexagonal crystallites of ribbon calcite (see below), a sub-microscopic structure that was exhumed inside the calcite crystals by intense etching ( Figure 6D, Figure 7A,E and Figure 12). The presence of small calcite ball-like bodies, about 10 µm in diameter ( Figure 9E), possibly microbial carbonate spheroids [74], sparmicrite monticule [69], or calcified fruiting bodies of fungi [75], which are commonly associated with spiky calcite, suggest that processes induced by microorganisms had possibly been involved in its formation [33]. The exact affinity of these spherical bodies is, however, unknown due to their heavy calcification. ...
... The SEM images also revealed that many, if not most, of these calcite "spikes" represent, in fact, the exposed tips of spear head-shaped, flat hexagonal crystallites of ribbon calcite (see below), a submicroscopic structure that was exhumed inside the calcite crystals by intense etching (Figures 6D, 7A,E and 12). The presence of small calcite ball-like bodies, about 10 μm in diameter ( Figure 9E), possibly microbial carbonate spheroids [74], sparmicrite monticule [69], or calcified fruiting bodies of fungi [75], which are commonly associated with spiky calcite, suggest that processes induced by microorganisms had possibly been involved in its formation [33]. The exact affinity of these spherical bodies is, however, unknown due to their heavy calcification. ...
... Although the origin of ribbon calcite remains ambiguous, the analysis of SEM images of the Koněprusy speleothems allows for two conclusions to be made: (1) The regular arrangement of the individual calcite ribbons, the long axes of which ran parallel to the direction of the c-axis of the calcite crystals, suggest that calcite ribbons represent, in fact, sub-microscopic building units that have been exposed by deep etching and are fully intrinsic to the calcite crystals ( Figure 12). (2) The presence of fine hair-like blankets, possibly mucus of fungal or microbial origin, which cover the tips of some actively growing ribbonlike calcite sub-crystals and ball-like carbonate bodies, about 5-10 µm in diameter, possibly bacterial calcite spheroids [74,94,95], or calcified sporangia of microscopic fungi [75] that commonly occur in between calcite ribbons, indicate a possible influence of microbiological processes on the precipitation of ribbon calcite ( Figure 9E,F). ...
Gothic arch calcite, a specific crystallographic variety of calcite known from some hot springs and tufa streams, has been newly recognized in the Koněprusy Caves. The gothic-arch calcite occurs on the exteriors of exotic coralloid speleothems where it coexists with scalenohedral (dogtooth) spar crystals. The crystals exhibit microscopic ultrastructural features including deeply eroded topography, etch pits, and spiky and ribbon calcite crystallites, pointing to its extensive natural etching. Many gothic-arch calcites originated as late-stage, secondary overgrowths on older, etched dogtooth calcite crystals. Its characteristic outward curvature resulted from the recrystallization of etching-liberated fine carbonate grains and newly formed needle-fiber calcite laths, which were accumulated and bound on the faces and at the bases of corroded crystals. These intimately coexisting destructive and constructive processes of carbonate crystal corrosion and growth were probably mediated by bacteria, fungi, or other microorganisms. Fluid inclusions embedded in calcite crystals point to a vadose setting and temperatures below ~50 °C. This, combined with the wider geological context, indicates that the gothic arch calcite crystals originated only during the late Pleistocene to Holocene epochs, when the cave, initially eroded by hypogene fluids in the deeper subsurface, was uplifted to the subaerial setting and exposed to the meteoric waters seeping from the topographic surface. The radiocarbon analysis shows that gothic-arch calcite crystals are generally older than ~55,000 years, but the surface layers of some crystals still reveal a weak 14C activity, suggesting that microbiologically mediated alterations of the speleothems may have been occurring locally until now.
... Other interesting fungi detected inside the cave in the stagnation period were Trichophyton terrestre and Pseudogymnoascus pannorum. This last species, C. cladosporioides and P. chrysogenum, among other fungi, have been found on bat cadavers in a Slovakian cave (Nováková et al. 2018). ...
... The species found in La Garma Cave, P. pannorum, was found only in November 2015 in the Middle Gallery (33%) and Sector IV (50%) (Fig. 5, Supplementary Table 3). This species is relatively common in caves (Bastian et al. 2009;Nováková 2009; and was isolated from bats (Vanderwolf et al. 2013;Nováková et al. 2018). Their presence could be related to the hibernation of bats in the cave during the sampling period. ...
Airborne microorganisms can cause important conservation problems in caves with Paleolithic art and therefore the knowledge of cave aerodynamic is essential. La Garma Cave (Cantabria, Spain), an exceptional archaeological site with several levels of galleries interconnected and two entrances, presents a complex atmospheric dynamics. An approach including aerobiological sampling together with microclimate monitoring was applied to assess the factors controlling the origin of airborne fungi. Here we show that winter ventilation is critical for the increasing of Basidiomycota spores in the cave air and the highest concentrations were found in the most ventilated areas. On the contrary, Ascomycota spores prevailed in absence of ventilation. Besides, most Ascomycota were linked to insects and bats that visit or inhabit the cave. The combination of aerobiological and microclimate data constitutes a good approach to evaluate the influence of external climatic conditions and design the most suitable strategies for the conservation of cultural heritage in the cave environment.
... This was described in 2012 [58], and the type strain was isolated from sediments from Gruta de las Maravillas (Aracena, Huelva) along with other strains from Tesoro Cave. In addition, this fungus was isolated from air, cave sediments, and a dead spider (Agraecina cristiani) in Movile Cave, as well as from a bat cadaver in Demänovska Peace Cave [59], and from cave sediments in Nerja Cave [32]. ...
Nerja Cave, Southern Spain, was revealed as an important biodiversity reservoir from which several novel species of Aspergillus were described. We carried out an aerobiological study in Nerja Cave to assess the origin of airborne fungi. This study quantified the fungi present in the air of ten representative halls covering the three sectors comprising the cave: Touristic Galleries, High Galleries, and New Galleries. Microclimatological monitoring allowed us to understand the dynamic of airborne fungi in two seasons of the year (winter and summer), corresponding to the strongest and the lowest cave ventilation, and to validate the influence that the transport of airborne fungi from outside may have on the cave itself. The data show that cold air enters in winter, as confirmed by the abundant presence of Aspergillus and Penicillium spores inside and outside the cave. In summer, the abundance of some fungi in the air of Nerja Cave, which are not detected outside, indicates a stagnation or low ventilation, and therefore, the concentration of fungal spores is maxima. The high occurrence of Cladosporium outside the cave and the scarce abundance inside support the cave stagnation in this season.
... In the last decade, aerobiology has proved to be a suitable approach for studying the dispersion of airborne fungi in caves [6][7][8][9]. Fungal spores represent a potential risk to the conservation of cultural heritage since, in favorable cave environmental conditions (high relative humidity, stable temperature, nutrient inputs, etc.), fungi colonize speleothems and other mineral substrata in addition to the cadavers of animals and arthropods populating the cavity [2,10]. ...
The aerobiology of caves in Southern Spain possesses special characteristics, different from caves located in Northern Spain. Previous studies demonstrated the influence of outdoor air on caves in the north and the existence of two different patterns, depending on the season. In summer there is an abundance of Ascomycota, whereas in winter Basidiomycota predominates, which are related to the periods of stagnation and ventilation, respectively. In caves in Southern Spain the presence of airborne Basidiomycota is scarce and Ascomycota represents the main group of fungi widely distributed across the caves in all seasons. The most characteristic features were the abundant presence of entomopathogenic fungi (Beauveria bassiana, Parengyodontium album, Pochonia chlamydosporia, Leptobacillium symbioticum, Leptobacillium leptobactrum) and Cladosporium cladosporioides in Cueva del Tesoro, Cueva de Ardales and Gruta de las Maravillas. However, the presence of yeasts of the genera Cutaneotrichosporon, Trichosporon, Cryptococcus, Naganishia, Cystobasidium, Microstroma and Phragmotaenium was exclusive to Gruta de las Maravillas. Fungal hazard in the three show caves were determined using an ecological indicator based on the concentration of spores in cave air.
... Over 1150 species of fungi have been recorded from caves throughout the world, with the most species-rich division being Ascomycota, followed by Basidiomycota and Zygomycota with fewer species (Vanderwolf et al. 2013). Many of the fungi found in cave systems are not native to caves but are likely introduced and dispersed by humans, fauna, water sources, and air currents (Jablonsky et al. 1993;Ikner et al. 2007;Shapiro and Pringle 2010;Vanderwolf et al. 2016;Nováková et al. 2018). Some suspected obligate troglobitic fungi have been reported, such as Acaulium caviariforme (Vanderwolf et al. 2013), A. baecitus (Nováková et al. 2012), and A. thesauricus (Nováková et al. 2012). ...
... A variety of bats roost in the cave, with some colonies having populations over 100,000 individuals (Kobayasi et al. 1980). These bats bring in nutrient sources from outside the cave daily, and their guano and cadavers are known to harbour fungi (Nieves-Rivera et al. 2009;Nováková et al. 2018). Madai cave is also subject to major anthropogenic influence due to land use for palm-oil plantations surrounding the forest reserve, seasonal swiftlet farming harvesting by the local community for generations, and visits by tourists from all over the world as a major eco-tourism attraction. ...
... Our results reflect those from previous fungal studies from cave ecosystems as Ascomycota fungi usually dominate the fungal composition of cave ecosystems, followed by Basidiomycota, Zygomycota, and then others (Vanderwolf et al. 2013). Four species of fungi were discovered from cave samples for the first time in this study, namely A. nitens, Ganoderma australe, Pyrrhoderma noxium, and Xylaria feejeensis (Vanderwolf et al. 2013;Nováková et al. 2018;Karunarathna et al. 2020;Zhang et al. 2020;Cunha et al. 2020). ...
The island of Borneo is a global biodiversity hotspot. However, its limestone caves are one of its least-studied ecosystems. We report for the first time the fungal species richness, diversity and abundance from Madai cave, situated in north-eastern Borneo. Environmental samples from inside the cave environment were collected (guano, speleothem, and cavern water) via opportunistic sampling. The dilution method was performed for isolation of fungi. Morphological characterisation and molecular analysis of the ITS region were utilised for the identification of isolates. Fifty-five pure cultures of fungi were attained, comprising 32 species from 15 genera, eight orders, and two divisions, Ascomycota and Basidiomycota. Ascomycetes dominated the fungal composition, accounting for 53 (96%) out of 55 total isolates. Penicillium spp. accounted for more than 47.1% of fungal abundance in all sample types. However, Aspergillus spp. had the highest occurrence rate, being isolated from all environmental samples except one. Purpureocillium lilacinum was isolated most frequently, appearing in five separate samples across all three substrates. Annulohypoxylon nitens, Ganoderma australe, Pyrrhoderma noxium, and Xylaria feejeensis were discovered and reported for the first time from the cave environment. This study provides additional data for further research on the mycoflora of Sabah’s various ecosystems, especially limestone caves.
