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Pseudogibellula formicarum parasitizing O. paltothyrei. A. Paltothyreus tarsatus biting onto a vertical stem. B. Dorsal view. C. Synnemata arising from ant sutures. D. Synnema with conidiophores. E. Close-up of a single conidiophore. F. Synnema tip and its multiple conidiophores. Bars: E = 20 µm; F = 100 µm.
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Ophiocordyceps species infecting ants are globally distributed, with diversity concentrated in the tropics and decreasing with increasing latitude. Among these myrmecophilous species, the ones exhibiting the ability to manipulate host behavior, the so-called “zombie-ant fungi” of the O. unilateralis clade, have been studied progressively over the l...
Citations
... In contrast to Beauveria, Ophiocordyceps species are highly specialized entomopathogens that generally infect only one insect species (4)(5)(6). The 'zombie-making' fungi of the species complex Ophiocordyceps unilateralis sensu lato infect ants from the Camponotini tribe. ...
... Following this summiting behavior, the fungus converts to a multicellular, mycelial growth, which eventually gives rise to a fruiting body that sprouts from the cadaver (11,12). This fruiting body carries the spores that are released to infect new ants (4)(5)(6). These manipulated behaviors are a crucial aspect of the Ophiocordyceps life cycle that aid in circumventing social immunity behaviors of healthy nest mates (13) and place the ant in a microclimate that promotes fungal growth and spore dispersal (10,14). ...
Microbiome composition impacts many host aspects including health, nutrition, reproduction, and behavior. This warrants the recent uptick in insect microbiota research across species and ecosystems. Commensurate with this, the bacterial microbiome of the ant Camponotus floridanus has been well characterized across body regions and maturation levels. However, potential effects of entomopathogens on the gut microbiome, and the fungal communities therein, are yet to be assessed. Investigation of the microbiome during infection could provide insight into entomopathogenic infection and manipulation strategies and inform effective biopesticide strategies. Additionally, the mycobiome remains often overlooked despite playing a vital role in gut ecology with potential implications for health and infection outcomes. To improve our limited understanding of fungal infections in insects, and ants in particular, we characterized the effects of two entomopathogens with different infection strategies on the gut micro- and mycobiota of C. floridanus over time; Ophiocordyceps camponoti-floridani and Beauveria bassiana. Specialist, zombie-making O. camponoti-floridani fungi hijack the behavior of C. floridanus ants over three weeks, causing them to find an elevated position, and fix themselves in place with their mandibles. This summiting behavior is adaptive to Ophiocordyceps as the ant transports the fungus to conditions that favor fruiting body development, spore production, dispersal, and transmission. In contrast, the generalist entomopathogen B. bassiana infects and kills the ant within a few days, without the induction of obvious fungus-adaptive behaviors. By comparing healthy ants with Beauveria- and Ophiocordyceps-infected ants we aimed to 1) describe the dynamics of the micro- and mycobiome of C. floridanus during infection, and 2) determine if the effects on gut microbiota are distinctive between fungi that have different infection strategies. While Beauveria did not measurably affect the ant host micro-and mycobiome, Ophiocordyceps did, especially for the mycobiome. Moreover, ants that were sampled during Ophiocordyceps-adaptive summiting behavior had a significantly different micro- and mycobiome composition compared to healthy controls and those sampled before and after manipulation took place. This suggests that the host microbiome might have a role to play in the manipulation strategy of Ophiocordyceps.
... clavate 130.0-250 × 5-6, filiform, septate Chen et al. (2011) Ophiocordyceps paludosa larvae of Lepidoptera 55-130 × 0.5-1.0, slender filiform, greyish-brown 800-855 × 375-410, superficial, greyish-brown to deep brown, flattened-ovoid 480-550 × 8-10, cylindrical 390-490 × 2.0-2.5, filiform, multi-septate, non-disarticulating Mains (1940) on more sufficient taxa sampling (Ban et al. 2009;Evans et al. 2011;Sanjuan et al. 2015;Simmons et al. 2015;Spatafora et al. 2015;Araújo et al. 2018;Khonsanit et al. 2019;Araújo et al. 2020;Mongkolsamrit et al. 2021;Yang et al. 2021;Araújo et al. 2022;Mongkolsamrit et al. 2022;Tang et al. 2022;Mongkolsamrit et al. 2023;Tang et al. 2023a, b). However, Cordyceps musicaudata has not been revised because there are no specimens available for study of its morphological and molecular data. ...
Ophiocordyceps is the largest genus in Ophiocordycipitaceae and has a broad distribution with high diversity in subtropical and tropical regions. In this study, two new species, pathogenic on lepidopteran larvae are introduced, based on morphological observation and molecular phylogeny. Ophiocordyceps fenggangensis sp. nov. is characterised by having fibrous, stalked stroma with a sterile tip, immersed perithecia, cylindrical asci and filiform ascospores disarticulating into secondary spores. Ophiocordyceps liangii sp. nov. has the characteristics of fibrous, brown, stipitate, filiform stroma, superficial perithecia, cylindrical asci and cylindrical-filiform, non-disarticulating ascospores. A new combination Ophiocordyceps musicaudata (syn. Cordyceps musicaudata ) is established employing molecular analysis and morphological characteristics. Ophiocordyceps musicaudata is characterised by wiry, stipitate, solitary, paired to multiple stromata, yellowish, branched fertile part, brown stipe, immersed perithecia, cylindrical asci and cylindrical-filiform, non-disarticulating ascospores.
... Some fungi evolved to exploit other fungi which are themselves pathogenic or parasitic on other organisms, a lifestyle called "hyperparasitism" (Boosalis 1964, Parratt & Laine 2016. Hyperparasitism by fungi on fungal pathogens of other organisms is commonly called "mycoparasitism" (Bushley et al. 2013, Wang et al. 2015, Crous et al. 2017, Araújo et al. 2020 although the initial meaning of the latter term referred to fungi parasitising other fungi whether the hosts be parasites/ pathogens or not (Barnett 1963). Mycoparasitism has evolved multiple times in the Kingdom Fungi (Gleason et al. 2014). ...
... coffee rust fungus Hemileia vastatrix) and entomopathogens (Vandermeer et al. 2009, Baiswar et al. 2014, Wei et al. 2019. Pseudogibellula is found to grow directly on Ophiocordyceps, suggesting an apparent mycoparasitism (Araújo et al. 2020, Mongkolsamrit et al. 2021, and the genus Niveomyces has been recently proposed as a mycoparasite of Ophiocordyceps camponoti-floridani (Araújo et al. 2022). Within Hypocreaceae, Syspastospora parasitica is found to infect a wellknown insect pathogen/endophyte, Beauveria bassiana (Posada et al. 2004). ...
... De Hoog (1974) described the type specimen of Spor. insectorum as being found on "Paltothyreus tarsatus" (Hymenoptera, Formicidae) "associated with Gibellula [= Pseudogibellula] formicarum", which was further supported and discussed by Araújo et al. (2020) and considered to be a mycoparasite of Ophiocordyceps paltothyreum, a commonly found ant parasite in West Africa. ...
Four new species of the genus Niveomyces are described from Thailand. They were found as mycoparasites on: Ophiocordyceps infecting flies ( Diptera ) for Niveomyces albus ; ants ( Hymenoptera ) for N. formicidarum ; and leafhoppers ( Hemiptera ) for N. hirsutellae and N. multisynnematus . A new genus, Pseudoniveomyces with two species: Pseudoniveo. blattae (type species), parasitic on Ophiocordyceps infecting cockroaches, and Pseudoniveo. arachnovorum , found on a spider egg sac, are also described. These fungi share a common feature which is a sporothrix-like asexual morph. Based on our molecular data, Sporothrix insectorum is shown to be affiliated to the genus Niveomyces , and thus a new combination N. insectorum comb. nov. is proposed. Niveomyces coronatus , N. formicidarum and N . insectorum formed the N. coronatus species complex found on ant-pathogenic Ophiocordyceps from different continents. Pseudoniveomyces species are distinguished from Niveomyces spp. based on the presence of fusoid macroconidia in culture and a red pigment diffused in the medium, resembling to Gibellula and Hevansia . The molecular phylogenetic analyses also confirmed its generic status. The host/substrates associated with the genera within Cordycipitaceae were mapped onto the phylogeny to demonstrate that mycoparasitism also evolved independently multiple times in this family.
... In tropical forests, they contributed as much as 50% of animal biomass (Hölldobler et al. 2009). Among the hosts of many entomopathogenic fungi, ants were also the most common host of species within Ophiocordyceps (Evans and Samson 1982;Evans et al. 2011b;Kepler et al. 2011;Luangsa-ard et al. 2011;Kobmoo et al. 2012Kobmoo et al. , 2015Araújo et al. 2015Araújo et al. , 2018Araújo et al. , 2020Sanjuan et al. 2015;Spatafora et al. 2015;Crous et al. 2016;Tasanathai et al. 2019;Wei et al. 2020;Tang et al. 2022;Xu et al. 2022). ...
Some Ophiocordyceps species infecting ants are able to manipulate the host behavior. The hosts are manipulated in order to move to location that are advantageous for fungal spore transmission. Ophiocordyceps species that are able to manipulate the ant's behavior are called "zombie-ant fungi". They are widespread within tropical forests worldwide, with relatively few reports from subtropical monsoon evergreen broad-leaf forest. Zombie-ant fungi have been described and reported in different countries worldwide. However, there were a few reports from China. This study proposed six new species of zombie-ant fungi from China based on multi-gene (SSU, LSU, TEF , RPB1 and RPB2 ) phylogenetic analyses and morphological characteristics. Six novel species of Ophiocordyceps from China were identified as the Ophiocordyceps unilateralis core clade, forming a separate lineage with other species. Six novel species of Ophiocordyceps with hirsutella-like asexual morphs exclusively infecting ants were presented herein, namely, Ophiocordyceps acroasca , Ophiocordyceps bifertilis , Ophiocordyceps subtiliphialida , Ophiocordyceps basiasca , Ophiocordyceps nuozhaduensis and Ophiocordyceps contiispora . Descriptions and illustrations for six taxon were provided. Five of these species were collected from the subtropical monsoon evergreen broad-leaf forest, and one was collected from the rainforest and subtropical monsoon evergreen broad-leaf forest. This work proposes that the same host of Camponotus can be infected by multiple ant pathogenic fungi, while multiple ants of Polyrhachis can be infected by the same pathogenic fungi at the same time. This study contributes towards a better understanding of the evolutionary relationship between hosts and fungi, and provides novel insights into the morphology, distribution, parasitism, and ecology of Ophiocordyceps unilateralis sensu lato. We have provided a method for obtaining living cultures of Ophiocordyceps unilateralis complex species and their asexual morphs based on the living cultures, which is of significant value for further studies of Ophiocordyceps unilateralis complex species in the future.
... (Araújo and Hughes 2019). In the last decade, there has been increasing interest in the Ophiocordyceps on ants, including their morphological characters, ecology, evolution, and behavioral manipulation of hosts (Andersen et al. 2009;Evans et al. 2011aEvans et al. , 2011bEvans et al. , 2018Araújo et al. 2018Araújo et al. , 2020. Araújo and Hughes (2017) proposed that Ophiocordyceps-infecting ants could be divided into five species complexes: O. myrmecophila/irangiensis, O. lloydii, Section Editor: Roland Kirschner O. australis, O. kniphofioides, and O. unilateralis. ...
... & C.P. Robin) Spatafora, Kepler & C.A. Quandt (Samson et al. 1981;Spatafora et al. 2015), S. burmensis (Mains) Samson & H.C. Evans, and S. dolichoderinarum Samson & H.C. Evans. Based on the multi-locus phylogeny presented by Araújo et al. (2020), O. buquetii belongs to the O. australis complex. Robin (1853) first described O. buquetii (formerly Stilbella buquetii) on weevil hosts (Pycnopus bufo Bohem. ...
... Its main morphological characters are the multiple brown to black synnemata arising from adult ants' heads, thorax, and abdomen, and the swollen apex is seen as a dense hymenium-like layer of conidiogenous cells (Samson et al. 1981). Recently, Araújo et al. (2020) studied the taxonomic placement of O. buquetii specimens from Ghana attacking various ant host species. Interestingly, a phylogenetic analysis revealed that O. buquetii from Ghana comprises a single species occurring on a broad range of ant host species. ...
Fungal specimens parasitic on ants producing Stilbella-like anamorph were collected from Thailand. Based on morphological characters and phylogenetic analyses, a new record for Ophiocordyceps buquetii and a new species, Ophiocordyceps laotii, were identified. Ophiocordyceps laotii is a pathogen specific to the ant species Dolichoderus laotius, while O. buquetii is a species distributed globally with a broad range of ant host species, occurring on Camponotus sp., Crematogaster sp., Dilobocondyla sp., Oecophylla smaragdina, Platythyrea sp., Polyrhachis illaudata, Polyrhachis sp. 1, and Polyrhachis sp. 2. Ophiocordyceps buquetii and O. laotii share the morphological character of producing multiple synnemata from ant hosts but differ in the shape of fertile head and conidia, as well as its phylogenetic placement, which clearly distinguishes these species.
... Ophiocordyceps then utilizes the ant's body as a platform to grow the spore-producing structures needed for transmission to the next host (Evans et al. 2011a, Hughes et al. 2011 Masters of the manipulator: two new hypocrealean genera, Niveomyces (Cordycipitaceae) and Torrubiellomyces (Ophiocordycipitaceae), parasitic on the zombie ant fungus Ophiocordyceps camponoti-floridani De Bekker et al. 2015, Araújo et al. 2018. However, despite being sophisticated parasites themselves, but not unlike most (if not all) life on earth, Ophiocordyceps species are also parasitized by other hypocrealean fungi (Evans et al. 2011a, b, Andersen & Hughes 2012, Araújo et al. 2020. ...
... However, none of these species are associated with a behaviour-manipulating Ophiocordyceps. In addition, mycoparasites growing on other Ophiocordyceps-manipulated ants, such as Ophiocordyceps camponoti-rufipedis in Brazil (Evans et al. 2011a, b, Andersen & Hughes 2012 and Ophiocordyceps paltothyrei in Ghana (Araújo et al. 2020), have been reported. These records, along with our unpublished observations of mycoparasites on Ophiocordyceps across North and South America, as well as in Africa and Australia (JPM Araújo & HC Evans pers. ...
... Few mycoparasitic species of entomopathogenic fungi have been formally described, thus far, including recent records of Polycephalomyces on Ophiocordyceps species from Asia (Wang et al. 2015b, Zhong et al. 2016, Xiao et al. 2018). However, mycoparasites associated with behaviour-manipulating Ophiocordyceps have only been noted in the field as an ecological aspect of those interactions (Andersen & Hughes 2012, Araújo et al. 2020, Mongkolsamrit et al. 2021. In this study, we present two new genera Niveomyces and Torrubiellomyces, which were recorded consistently infecting the zombie-ant fungus O. camponoti-floridani. ...
During surveys in central Florida of the zombie-ant fungus Ophiocordyceps camponoti-floridani, which manipulates the behavior of the carpenter ant Camponotus floridanus, two distinct fungal morphotypes were discovered associated with and purportedly parasitic on O. camponoti-floridani. Based on a combination of unique morphology, ecology and phylogenetic placement, we discovered that these morphotypes comprise two novel lineages of fungi. Here, we propose two new genera, Niveomyces and Torrubiellomyces, each including a single species within the families Cordycipitaceae and Ophiocordycipitaceae, respectively. We generated de novo draft genomes for both new species and performed morphological and multi-loci phylogenetic analyses. The macromorphology and incidence of both new species, Niveomyces coronatus and Torrubiellomyces zombiae, suggest that these fungi are mycoparasites since their growth is observed exclusively on O. camponoti-floridani mycelium, stalks and ascomata, causing evident degradation of their fungal hosts. This work provides a starting point for more studies into fungal interactions between mycopathogens and entomopathogens, which have the potential to contribute towards efforts to battle the global rise of plant and animal mycoses.
Citation: Araújo JPM, Lebert BM, Vermeulen S, et al. 2022. Masters of the manipulator: two new hypocrealean general, Niveomyces (Cordycipitaceae) and Torrubiellomyces (Ophiocordycipitaceae), parasitic on the zombie ant fungus Ophiocordyceps camponoti-floridani. Persoonia 49: 171–194. https://doi.org/10.3767/persoonia.2022.49.05.
... Ophiocordyceps is a terminal summiting behaviour whereby the fungus induces the ant to bite and affix itself to vegetation at an elevated position that promotes fungal growth and transmission (Andersen et al., 2009;Evans & Samson, 1984;Hughes et al., 2011). However, specific Ophiocordyceps-ant species interactions do vary across climates and habitats, producing the fatal change in host behaviour and subsequent fungal development in slightly different ways (Araújo et al., , 2020Evans et al., 2011;Loreto et al., 2018). ...
... In addition to abiotic effects, adverse biotic interactions such as hyperparasitism, during which one organism is parasitized by another parasite (Kirk et al., 2008), could hamper Ophiocordyceps development and transmission capacity Araújo et al., 2022;Evans, 1982). Fungal hyperparasitisms of Ophiocordyceps have regularly been observed by field scientists who study and document the biodiversity of these fungus-ant interactions in the wild Araújo et al., 2020Araújo et al., , 2022Kobmoo et al., 2012). Nevertheless, official species descriptions and reports of these fungi are hard to come by and their potential ecological impact (e.g. ...
Ophiocordyceps fungi manipulate the behaviour of their ant hosts to produce a summit disease phenotype, thereby establishing infected ant cadavers onto vegetation at elevated positions suitable for fungal growth and transmission. Multiple environmental and ecological factors have been proposed to shape the timing, positioning and outcome of these manipulations.
We conducted a long‐term field study of Ophiocordyceps camponoti‐floridani infections of Camponotus floridanus ants—the Florida zombie ants. We propose and refine hypotheses on the factors that shape infection outcomes by tracking the occurrence of and fungal growth from hundreds of ant cadavers. We modelled and report these data in relation to weather, light, vegetation and attack by hyperparasites.
We investigated environmental factors that could affect the occurrence and location of newly manipulated ant cadavers. New cadaver occurrence was preferentially biased towards epiphytic Tillandsia bromeliads, canopy openness and summer weather conditions (an interactive effect of temperature, humidity and precipitation). Furthermore, we suggest that incident light at the individual cadaver level reflects microhabitat choice by manipulated ants or selective pressure on cadaver maintenance for conditions that improve fungal survival.
We also asked which environmental conditions affect fungal fitness. Continued fungal development of reproductive structures and putative transmission increased with moist weather conditions (interaction of humidity and precipitation) and canopy openness, while being reduced by hyperparasitic mycoparasite infections. Moreover, under the most open canopy conditions, we found an atypical Ophiocordyceps growth morphology that could represent a plastic response to conditions influenced by high light levels.
Taken together, we explore general trends and the effects of various ecological conditions on host and parasite disease outcomes in the Florida zombie ant system. These insights from the field can be used to inform experimental laboratory setups that directly test the effects of biotic and abiotic factors on fungus–ant interactions or aim to uncover underlying molecular mechanisms.
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... The heterogeneous genus Ophiocordyceps is cosmopolitan, with the highest species diversity observed in the tropics and subtropics (e.g., Sanjuán et al., 2015;Araújo et al., 2018Araújo et al., , 2020Araújo et al., , 2021Luangsa-ard et al., 2018). As for other cordycipitoid fungi, the species taxonomy, distribution and host diversity of the genus Ophiocordyceps is relatively well explored. ...
... Samples of dead, Ophiocordyceps-infected ants have been collected from tropical and temperate forests all over the globe. [50][51][52][53][54][55] These biodiversity studies so far suggest that every ant species that is parasitized by a unique Ophiocordyceps species has specialized to infect that host. When a given species interaction results in an elevated death position (i.e., the summiting position), or when its fungus-sprouting cadavers are found in areas outside of the ants' general ecological niche, 53,55 20 Nevertheless, when this species pair was moved into the laboratory for more detailed behavioural studies, the summiting behaviour remained synchronized but shifted to take place in the early morning before the onset of light. ...
... [50][51][52][53][54][55] These biodiversity studies so far suggest that every ant species that is parasitized by a unique Ophiocordyceps species has specialized to infect that host. When a given species interaction results in an elevated death position (i.e., the summiting position), or when its fungus-sprouting cadavers are found in areas outside of the ants' general ecological niche, 53,55 20 Nevertheless, when this species pair was moved into the laboratory for more detailed behavioural studies, the summiting behaviour remained synchronized but shifted to take place in the early morning before the onset of light. 20 A similar synchronized shift was observed in lab studies with another species pair (i.e., Camponotus castaneus and Ophiocordyceps kimflemingiae from South Carolina, USA). ...
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Ophiocordyceps fungi manipulate ant behaviour as a transmission strategy. Conspicuous changes in the daily timing of disease phenotypes suggest that Ophiocordyceps and other manipulators could be hijacking the host clock. We discuss the available data that support the notion that Ophiocordyceps fungi could be hijacking ant host clocks and consider how altering daily behavioural rhythms could benefit the fungal infection cycle. By reviewing time‐course transcriptomics data for the parasite and the host, we argue that Ophiocordyceps has a light‐entrainable clock that might drive daily expression of candidate manipulation genes. Moreover, ant rhythms are seemingly highly plastic and involved in behavioural division of labour, which could make them susceptible to parasite hijacking. To provisionally test whether the expression of ant behavioural plasticity and rhythmicity genes could be affected by fungal manipulation, we performed a gene co‐expression network analysis on ant time‐course data and linked it to available behavioural manipulation data. We found that behavioural plasticity genes reside in the same modules as those affected during fungal manipulation. These modules showed significant connectivity with rhythmic gene modules, suggesting that Ophiocordyceps could be indirectly affecting the expression of those genes as well.
... Recently published researchs are mostly restricted to the Sordariomycetes macrofungi in the Brazilian Amazon: Yuyama et al. (2013) studied the taxonomic and in vitro cultivation aspects of Daldinia eschscholtzii (Ehrenb.) Rehm collected in the municipality of Manaus whereas Araújo et al. (2015Araújo et al. ( , 2018Araújo et al. ( , 2020 investigated the diversity of the entomopathogenous genus Ophiocordyceps Petch. As far as we know, for members of the class Eurotiomycetes, where Pseudotulostoma O.K.Mill. ...
Pseudotulostoma is a genus described for fungi with stipitate sporocarps that have an exposed gleba and a woody, volvate base. The two species that belong to this genus (P. volvatum and P. japonicum) form unusual epigeous ascomata that are atypical among the hypogeous members of the Elaphomycetaceae. The genus was first described from the Guiana Shield and was suggested to be restricted to rainforests dominated by the ectomycorrhizal tree Dicymbe corymbosa (Leguminosae-Detarioideae). Pseudotulostoma volvatum was also later described from Colombia in association with Pseudomonotes tropenbosii (Dipterocarpaceae- Monotoidea). Here we report a new occurrence of P. volvatum that is also the first occurrence of an ectomycorrhizal Ascomycota fungus in a native host plant in Brazil. The description includes images of the macroscopic and microscopic characteristics, a discussion of the distinctive features, and phylogenetic placement using the nLSU of this fungus among Elaphomyces species. This new collection (third known location) demonstrates that P. volvatum also occurs in a white-sand forest composed of the canopy tree Aldina heterophylla (Leguminosae-Papilionoideae). Thus, we provide additional information regarding P. volvatum that expands its known distribution.
