Abstract
Bat flies are obligate ectoparasitic dipterans that are highly specialised to bats and have apomorphic characteristics, such as absent or reduced wings, and specialised legs and claws, which contribute to their survival. They are often associated with fungi and harbour a fungal diversity that is still poorly understood. Fungi were found in association with the bat flies in a cave of the Caatinga dry forest in Brazil. In total, 43% of the captured bat flies were associated with fungi. Seventy-six flies were collected. DNA sequence analyses of 39 isolates showed that the isolates belonged to 13 species within nine genera, with 38 isolates belonging to Ascomycota and one isolate to Basidiomycota, and Aspergillus was the most frequently isolated genus. Most of the genera found have also been isolated from bat bodies and other substrates/hosts in caves in different regions of the world. Based on morphological and multi-locus phylogenetic analyses, two new species of Ascomycota were described: Allophoma brasiliensis sp. nov. and Pyrenochaetopsis cecavii sp. nov.
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Data availability
DNA sequences are available in GenBank and alignments were deposited in TreeBASE.
References
Allen GM (1967) The parasites of bats. Museum of Comparative Zoology, Cambridge
Whitaker Jr JO (1988) Collecting and preserving ectoparasites for ecological study. In: Kunz T (ed) Ecological and behavioral methods for the study of bats. Smithsonian Inst Press, Washington, pp 459–474
Naegle MA, Mugleston JD, Bybee SM, Whiting MF (2016) Reassessing the phylogenetic position of the epizoic earwigs (Insecta: Dermaptera). Mol Phylogenet Evol 100:382–390. https://doi.org/10.1016/j.ympev.2016.03.012
Taylor S, Durden LA, Foley EH, Reeves WK (2016) The bat tick Carios azteci (Acari: Argasidae) from Belize with an endosymbiotic Coxiellaceae. Speleobiol Notes 8:16–21. https://doi.org/10.5563/spbn.v8i0.81
Haelewaters D, Hiller T, Dick CW (2018) Bats, bat flies, and fungi: a case of hyperparasitism. Trends Parasitol 34(9):784–799
Marshall AG (1982) Ecology of insects ectoparasitic on bats. In: Kunz TH (ed) Ecology of bats. Springer, Boston, pp 369–401. https://doi.org/10.1007/978-1-4613-3421-7_10
Frank R, Münster J, Schulze J, Liston A, Klimpel S (2014) Macroparasites of Microchiroptera: bat ectoparasites of Central and South America. In: Klimpel S, Mehlhorn H (eds) Bats (Chiroptera) as Vectors of Diseases and Parasites. Parasitology Research Monographs, vol 5. Springer, Berlin, pp 87–130
Szentiványi T, Christe P, Glaizot O (2019) Bat flies and their microparasites: current knowledge and distribution. Front Vet Sci 6:115. https://doi.org/10.3389/fvets.2019.00115
Graciolli G, Autino AG, Claps GL (2007) Catalogue of American Nycteribiidae (Diptera, Hippoboscoidea). Rev Bras Entomol 51:142–159. https://doi.org/10.1590/S0085-56262007000200004
Graciolli G, Azevedo AA, Árzua M, Barros-Battesti DM, Linardi PM (2008) Artrópodos ectoparasitos de morcegos no Brasil. In: Pacheco SM, Marques RV, Esbérard CEL (orgs) Morcegos do Brasil: biologia sistemática ecologia e conservação. Armazém Digital, Porto Alegre, 123 –138
Graciolli G, Zortéa M, Carvalho LFAC (2010) Bat flies (Diptera, Streblidae and Nycteribiidae) in a Cerrado area of Goiás state, Brazil. Rev Bras Entomol 54:511–514. https://doi.org/10.1590/S008556262010000300025
Hagan HR (1951) Embryology of the viviparus insects. Ronald Press, New York
Kunz TH, Lumsden LF, Fenton MB (2003) Ecology of cavity and foliage roosting bats. In: Kunz TH, Fenton MB (eds) Bat Ecology. The University of Chicago Press, Chicago, pp 3–89
Bequart J (1940) Moscas parasitas pupiparas de Colombia y Panamá. Rev Acad Colomb Cienc Exact Fis Nat 3:414–418
Patterson BD, Dick CW, Dittmar K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). J Trop Ecol 23:177–189. https://doi.org/10.1017/S0266467406003816
Thaxter R (1901) Preliminary diagnoses of new species of Laboulbeniaceae. III Proc Am Acad Arts Sci 36:397–414
Graciolli G, Aguiar LS (2002) Ocorrência de moscas ectoparasitas (Diptera, Streblidae e Nycteribiidae) de morcegos (Mammalia, Chiroptera) no Cerrado de Brasília, Distrito Federal, Brasil. Rev Bras Zoo 19:177–181. https://doi.org/10.1590/S0101-81752002000500012
Walker MJ, Dorrestein A, Camacho JJ, Meckler LA, Silas KA, Hiller T, Haelewaters D (2018) A tripartite survey of hyperparasitic fungi associated with ectoparasitic flies on bats (Mammalia: Chiroptera) in a neotropical cloud forest in Panama. Parasite 25:19. https://doi.org/10.1051/parasite/2018017
Haelewaters D, Verhaeghen SJ, Rios Gonzalez TA, Bernal Vega JÁ, Villarreal Saucedo RV (2017) New and interesting Laboulbeniales from Panama and neighboring areas. Nova Hedwigia 105:267–299. https://doi.org/10.1127/nova_hedwigia/2017/0410
de Groot MD, Dumolein I, Hiller T, Sándor AD, Szentiványi T, Schilthuizen M, Catherine MA, Verbeken A, Haelewaters D (2020) On the fly: tritrophic associations of bats bat flies and fungi. J Fungus 6:361. https://doi.org/10.3390/jof6040361
Tan JS (1997) Human zoonotic infections transmitted by dogs and cats. Archives Intern Med 157:1933–1943
Parola P, Davoust B, Raoult D (2005) Tick- and flea-borne rickettsial emerging zoonoses. Vet Res 36:469–492. https://doi.org/10.1051/vetres:2005004
Förster M, Klimpel S, Mehlhorn H, Sievert K, Messler S, Pfeffer K (2007) Pilot study on synanthropic flies (e.g. Musca, Sarcophaga, Calliphora, Fannia, Lucilia, Stomoxys) as vectors of pathogenic microorganisms. Parasitol Res 101:243–246. https://doi.org/10.1007/s00436-007-0522-y
Beugnet F, Marie JL (2009) Emerging arthropod–borne diseases of companion animals in Europe. Vet Parasitol 163:298–305. https://doi.org/10.1016/j.vetpar.2009.03.028
Lučan RK, Bandouchova H, Bartonička T, Pikula J, Zahradníková A, Zukal J, Martínková N (2016) Ectoparasites may serve as vectors for the white-nose syndrome fungus. Parasites Vectors 9:16. https://doi.org/10.1186/s13071-016-1302-2
Foley J, Clifford D, Castle K, Cryan P, Ostfeld RS (2011) Investigating and managing the rapid emergence of white nose syndrome a novel fatal infectious disease of hibernating bats. Conserv Biol 25:223–231. https://doi.org/10.1111/j.1523-1739.2010.01638.x
Turner JM, Warnecke L, Wilcox A, Baloun D, Bollinger TK, Misra V, Willis CK (2015) Conspecific disturbance contributes to altered hibernation patterns in bats with white-nose syndrome. Physiol Behavior 140:71–78. https://doi.org/10.1016/j.physbeh.2014.12.013
Hoyt JR, Kilpatrick AM, Langwig KE (2021) Ecology and impacts of white-nose syndrome on bats. Nat Rev Microbiol 19:196–210. https://doi.org/10.1038/s41579-020-00493-5
Bandouchova H, Bartonicka T, Berkova H, Brichta J, Cerny J, Kovacova V, Kolarik M, Köllner B, Kulich P, Martínková N, Rehak Z, Turner GG, Zukal J, Pikula J (2015) Pseudogymnoascus destructans: evidence of virulent skin invasion for bats under natural conditions, Europe. Transbound Emerg Dis 62:1–5. https://doi.org/10.1111/tbed.12282
Barlow AM, Worledge L, Miller H, Drees KP, Wright P, Foster JT, Sobek C, Borman AM, Fraser M (2015) First confirmation of Pseudogymnoascus destructans in British bats and hibernacula. Vet Rec 177:73–73. https://doi.org/10.1136/vr.102923
Garzoli L, Riccucci M, Patriarca E, Debernardi P, Boggero A, Pecoraro L, Picco AM (2019) First isolation of Pseudogymnoascus destructans the fungal causative agent of white-nose disease in bats from Italy. Mycopathologia 184:637–644. https://doi.org/10.1007/s11046-019-00371-6
Urbina J, Chestnut T, Allen JM, Levi T (2021) Pseudogymnoascus destructans growth in wood soil and guano substrates. Sci Rep 11:763. https://doi.org/10.1038/s41598-020-80707-1
Vanderwolf KJ, McAlpine DF, Malloch D, Forbes GJ (2013) Ectomycota associated with hibernating bats in eastern Canadian caves prior to the emergence of white-nose syndrome. Northeastern Nat 20:115–130. https://doi.org/10.1656/045.020.0109
Cunha AOB, Bezerra JDP, Oliveira TGL, Barbier E, Bernard E, Machado AR, Souza-Motta CM (2020) Living in the dark: bat caves as hotspots of fungal diversity. PLoS ONE 15:e0243494. https://doi.org/10.1371/journal.pone.0243494
Bertola PB, Aires CC, Favorito SE, Graciolli G, Amaku M, Pinto-da-Rocha R (2005) Bat flies (Diptera: Streblidae Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira São Paulo Brazil: parasitism rates and host–parasite associations. Mem Inst Oswaldo Cruz 100:25–32. https://doi.org/10.1590/S0074-02762005000100005
Pereira MLS, Carvalho JLVR, Lima JMS, Barbier E, Bernard E, Bezerra JDP, Souza-Motta CM (2022) Richness of Cladosporium in a tropical bat cave with the description of two new species. In press, Mycol Prog. https://doi.org/10.1007/s11557-021-01760-2
Rito KF, Arroyo Rodríguez V, Queiroz RT, Leal IR, Tabarelli M (2017) Precipitation mediates the effect of human disturbance on the Brazilian Caatinga vegetation. J Ecol 105:828–838. https://doi.org/10.1111/13652745.12712
Silva JMC, Barbosa LCF, Leal IR, Tabarelli M (2017) The Caatinga: Understanding the challenges. In: Silva JMC, Leal IR, Tabarelli M (eds) Caatinga. Springer, Cham, pp 3–19
Leal ESB, Bernard E (2021) Mobility of bats between caves: ecological aspects and implications for conservation and environmental licensing activities in Brazil. Stud Neotrop Fauna Environ. https://doi.org/10.1080/01650521.2021.1964910
MMA Ministério do MeioAmbienteSecretaria de Biodiversidade e Florestas (2002) Biodiversidade brasileira: avaliação e identificação de áreas e ações prioritárias para conservação utilização sustentável e repartição dos benefícios da biodiversidade nos biomas brasileiros. MMA/SBF, Brasília
Gomes APDS, Rodal MJN, Melo ALD (2006) Florística e fitogeografia da vegetação arbustiva subcaducifólia da Chapada de São José, Buíque, PE, Brasil. Acta Bot Bras 20:37–48. https://doi.org/10.1590/S010233062006000100005
SNE – SociedadeNordestina de Ecologia (2002) Projeto Técnico para a Criação do Parque Nacional do Catimbau/PE – versão final em cumprimento ao Contrato no 086–00/02 Subprojeto “Proposta para Criação do Parque Nacional do Catimbau/PE.” Sociedade Nordestina de Ecologia, Recife
Specht MJ, Santos BA, Marshall N, Melo FPL, Leal IR, Tabarelli M, Baldauf C (2019) Socioeconomic differences among resident users and neighbour populations of a protected area in the Brazilian dry forest. J Environ Manage 232:607–614. https://doi.org/10.1016/j.jenvman.2018.11.101
Gardner AL (2007) Mammals of South America: marsupials xenarthrans shrews and bats, vol 1. The University of Chicago Press, Chicago
Díaz MM, Solari S, Aguirre LF, Aguiar LMS, Barquez RM (2016) Clave de identificación de los murciélagos de Sudamérica/Chave de identificação dos morcegos da América do Sul. Programa de Conservación de los Murciélagos de Argentina, Tucumán
Barbier E, Bernard E (2017) From the Atlantic Forest to the borders of Amazonia: species richness distribution and host association of ectoparasitic flies (Diptera: Nycteribiidae and Streblidae) in northeastern Brazil. Parasitol Res 116:3043–3055. https://doi.org/10.1007/s00436-017-5615-7
Samson AR, Houbraken J, Thrane U, Frisvald JC, Andersen B (2010) Food and indoor fungi. CBS-KNAW Fungal Biodiversity Centre, Utrecht
Seifert K, Morgan-Jones G, Gams W, Kendrick B (2011) The genera of Hyphomycetes. CBS-KNAW Fungal Biodiversity Centre, Utrecht
Tuite J (1969) Plant pathological methods. Fungi and bacteria. Plant pathological methods, Fungi and bacteria
Rayner RW (1970) A mycological colour chart. CMI and British Mycological Society, Kew
White TJ, Bruns T, Lee S, Taylor L (1990) Amplification and direct sequencing of fungal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols. Academic Press, Cambridge, A guide to methods and applications, pp 315–322
Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556. https://doi.org/10.1080/00275514.1999.12061051
Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330. https://doi.org/10.1007/s11046-019-00371-6
Hong SB, Go SJ, Shin HD, Frisvad JC, Samson RA (2005) Polyphasic taxonomy of Aspergillus fumigatus and related species. Mycologia 97:1316–1329. https://doi.org/10.1080/15572536.2006.11832738
Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172(8):4238–4246
Vilgalys R, Sun BL (1994) Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA sequences. Proc Natl Acad Sci USA 91(10):4599–4603
Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol 16:1799–1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092
Sung GH, Sung JM, Hywel Jones NL, Spatafora JW (2007) A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): identification of localized incongruence using a combinational bootstrap approach. Mol Phylogenet Evol 44:1204–1223. https://doi.org/10.1016/j.ympev.2007.03.011
Bezerra JDP, Oliveira RJV, Paiva LM, Silva GA, Groenewald JZ, Crous PW, Souza-Motta CM (2017) Bezerromycetales and Wiesneriomycetales ord. nov. (class Dothideomycetes) with two novel genera to accommodate endophytic fungi from Brazilian cactus. Mycol Prog 16:297–309. https://doi.org/10.1007/s11557-016-1254-0
Bezerra JDP, Sandoval-Denis M, Paiva LM, Silva GA, Groenewald JZ, Souza-Motta CM, Crous PW (2017) New endophytic Toxicocladosporium species from cacti in Brazil and description of Neocladosporium gen. nov. IMA Fungus 8:77–97. https://doi.org/10.5598/imafungus.2017.08.01.06
Samson RA, Visagie CM, Houbraken J, Hong SB, Hubka V, Klaassen CH, Perrone G, Seifert KA, Susca A, Tanney JB, Varga J, Kocsubé S, Szigeti G, Yaguchi T, Frisvad JC (2014) Phylogeny identification and nomenclature of the genus Aspergillus. Stud Mycol 78:141–173. https://doi.org/10.1016/j.simyco.2014.07.004
de Gruyter J, Woudenberg JH, Aveskamp MM, Verkley GJ, Groenewald JZ, Crous PW (2010) Systematic reappraisal of species in Phoma section Paraphoma, Pyrenochaeta and Pleurophoma. Mycologia 102:1066–1081. https://doi.org/10.3852/09-240
Hou LW, Groenewald JZ, Pfenning LH, Yarden O, Crous PW, Cai L (2020) The phoma-like dilemma. Stud Mycol 96:309–396. https://doi.org/10.1016/j.simyco.2020.05.001
Chen Q, Jiang JR, Zhang GZ, Cai L, Crous PW (2015) Resolving the Phoma enigma. Stud Mycol 82:137–217
Houbraken J, Kocsubé S, Visagie CM, Yilmaz N, Wang XC, Meijer M, Kraak B, Hubka V, Bensch K, Samson RA, Frisvad JC (2020) Classification of Aspergillus, Penicillium, Talaromyces and related genera (Eurotiales): an overview of families genera subgenera sections series and species. Stud Mycol 95:5–169. https://doi.org/10.1016/j.simyco.2020.05.002
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Ronquist F, Teslenko M, van Der Mark P, Ayres DL, Darling A, Höhna S, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE), pp 1–8
Nylander JAA (2004) MrModeltest 2.2. Computer program and documentation distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala
Rambaut A (2010) FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 17 Feb 2022
Colwell RK, Elsensohn JE (2014) Estimates turns 20: statistical estimation of species richness and shared species from samples, with non‐parametric extrapolation. Ecography 37:609–613. https://doi.org/10.1111/ecog.00814
De León JG, Méndez RG, Cadilla CL, Rivera-Mariani FE, Bolaños-Rosero B (2018) Identification of immunoglobulin E-Binding proteins of the xerophilic fungus Aspergillus penicillioides crude mycelial mat extract and serological reactivity assessment in subjects with different allergen reactivity profiles. International Archives of Allergy and Immunology 175:147–159. https://doi.org/10.1159/000484898
Jayasiri SC, Hyde KD, Jones EBG et al (2019) Diversity, morphology and molecular phylogeny of Dothideomycetes on decaying wild seed pods and fruits. Mycosphere 10:1–186. https://doi.org/10.5943/mycosphere/10/1/1
Yuan J, Zeng XY, Geng K et al (2021) Allophoma species (Pleosporales: Didymellaceae) associated with Thunbergia grandiflora in Guangxi Province, China. Biodiversity Data Journal 9:e63643. https://doi.org/10.3897/BDJ.9.e63643
Viswanathan TS (1957) A new species of Pyrenochaeta from sugarcane in India. Curr Sci 26:117–118
De Gruyter J, Boerema GH (2002) Contributions towards a monograph of Phoma (Coelomycetes) VIII. Section Paraphoma: Taxa with setose pycnidia. Persoonia 17:541–561
Špetík M, Berraf-Tebbal AKILA, Pokluda R, Eichmeier A (2021) Pyrenochaetopsis kuksensis (Pyrenochaetopsidaceae), a new species associated with an ornamental boxwood in the Czech Republic. Phytotaxa 498:177–185. https://doi.org/10.11646/phytotaxa.498.3.3
Magaña-Dueñas V, Stchigel AM, Cano-Lira JF (2021) New Coelomycetous fungi from freshwater in Spain. J Fungi 7:368. https://doi.org/10.3390/jof7050368
Johnson LJ, Miller AN, McCleery RA, McClanahan R, Kath JA, Lueschow S, Porras-Alfaro A (2013) Psychrophilic and psychrotolerant fungi on bats and the presence of Geomyces spp. on bat wings prior to the arrival of white nose syndrome. Appl Environ Microbiol 79:5465–5471. https://doi.org/10.1128/AEM.0142913
Visagie CM, Yilmaz N, Vanderwolf K, Renaud JB, Sumarah MW, Houbraken J, Assebgui R, Seifert KA, Malloch D (2020) Penicillium diversity in Canadian bat caves including a new species P. speluncae. FUSE 5:1–16. https://doi.org/10.3114/fuse.2020.05.01
Dick CW, Patterson BD (2006) Bat flies: obligate ectoparasites of bats. In: Morand S, Krasnov BR, Poulin R (eds) Micromammals and macroparasites. Springer, Tokyo, pp 179–194
Vanderwolf KJ, Malloch D, McAlpine DF, Forbes GJ (2013) A world review of fungi yeasts and slime molds in caves. Int J Speleol 42:77–96. https://doi.org/10.5038/1827-806X.42.1.9
Ogórek R, Kurczaba K, Cal M, Apoznański G, Kokurewicz T (2020) A culture-based ID of Micromycetes on the wing membranes of greater Mouse-Eared bats (Myotis myotis) from the “Nietoperek” site (Poland). Animals 10:1337. https://doi.org/10.3390/ani10081337
Spegazzini C (1896) Hongos de la caña de azúcar. Revista Fac Agron Univ Nac La Plata 2:227–258
Sklenář F, Jurjević Ž, Zalar P, Frisvad JC, Visagie CM, Kolařík M, Hubka V (2017) Phylogeny of xerophilic aspergilli (subgenus Aspergillus) and taxonomic revision of section Restricti. Stud Mycol 88:161–236. https://doi.org/10.1016/j.simyco.2017.09.002
Amend AS, Seifert KA, Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19:5555–5565. https://doi.org/10.1111/j.1365-294X.2010.04898.x
Nazareth SW, Gonsalves V (2014) Halophilic Aspergillus penicillioides from at halassohaline thalassohaline and polyhaline environments. Front Microbiol 5:412. https://doi.org/10.3389/fmicb.2014.00412
Chi LP, Yang SQ, Li XM, Li XD, Wang BG, Li X (2020) A new steroid with 7β,8β–epoxidation from the deep sea–derived fungus Aspergillus penicillioides SD-311. J Asian Nat Prod Res 23:884–891. https://doi.org/10.1080/10286020.2020.1791096
Paria K, Chakraborty SK (2019) Eco-potential of Aspergillus penicillioides (F12): bioremediation and antibacterial activity. SN Appl Sci 1:1515. https://doi.org/10.1007/s42452-019-1545-6
Ali I, Akbar A, Anwar M, Prasongsuk S, Lotrakul P, Punnapayak H (2015) Purification and characterization of a polyextremophilic α–amylase from an obligate halophilic Aspergillus penicillioides isolate and its potential for souse with detergents. Biomed Res Int 2015:245649. https://doi.org/10.1155/2015/245649
de Hoog G, Guarro J, Figueiras MJ, Gené J (2009) Atlas of clinical fungi. CBS–KNAW Fungal Biodiversity Centre, Utrecht
Gupta K, Gupta P, Mathew JL, Bansal A, Singh G, Singh M, Chakrabarti A (2016) Fatal disseminated Aspergillus penicillioides infection in a 3-month-old infant with suspected cystic fibrosis: Autopsy case report with review of literature. Pediatr Dev Pathol 19:506–511. https://doi.org/10.2350/15-10-1729-CR.1
Machowicz-Matejko E, Furmańczyk A, Zalewska ED (2018) Aspergillus penicillioides Speg. implicated in keratomycosis. Pol J Microbiol 67:407–416. https://doi.org/10.21307/pjm-2018-049
Zhang ZF, Liu F, Zhou X, Liu XZ, Liu SJ, Cai L (2017) Culturable mycobiota from Karst caves in China with descriptions of 20 new species. Persoonia 39:1–31. https://doi.org/10.3767/persoonia.2017.39.01
Zhang ZF, Zhou SY, Eurwilaichitr L, Ingsriswang S, Raza M, Chen Q, Zhao P, Liu F, Cai L (2021) Culturable mycobiota from Karst caves in China II with descriptions of 33 new species. Fungal Divers 106:29–136. https://doi.org/10.1007/s13225-020-00453-7
Crous PW, Luangsa-Ard JJ, Wingfield MJ et al (2018) Fungal Planet description sheets: 785–867. Persoonia 41:238–417. https://doi.org/10.3767/persoonia.2018.41.12
Lorch JM, Palmer JM, Vanderwolf KJ, Schmidt KZ, Verant ML, Weller TJ, Blehert DS (2018) Malassezia vespertilionis sp. nov.: a new cold-tolerant species of yeast isolated from bats. Persoonia 41:56–70. https://doi.org/10.3767/persoonia.2018.41.04
Valenzuela-Lopez N, Cano-Lira JF, Guarro J, Sutton DA, Wiederhold N, Crous PW, Stchigel AM (2018) Coelomycetous Dothideomycetes with emphasis on the families Cucurbitariaceae and Didymellaceae. Stud Mycol 90:1–69. https://doi.org/10.1016/j.simyco.2017.11.003
Marin-Felix Y, Hernández-Restrepo M, Iturrieta-González I, García D, Gené J, Groenewald JZ, Crous PW (2019) Genera of phytopathogenic fungi: GOPHY 3. Stud Mycol 94:1–124. https://doi.org/10.1016/j.simyco.2019.05.001
Acknowledgements
We thank Narjara Pimentel (UFPE) for her invaluable support during the fieldwork. We also thank Fundação Nacional do Índio (FUNAI), and Jailton Fernandes (ICMBio/PARNA do Catimbau) for their logistical support.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES, Finance Code 001; CAPES-PRInt process number 88887.311891/2018–00), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, processes 310298/2018–0 and 408788/2021-6), and the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE, process number APQ-0350-2.12/19). Funding for fieldwork was also partially provided by the Anglo American. E. Barbier is supported by a postdoctoral grant from CAPES and FACEPE (process #88887.353052/2019–00). C.M. Souza-Motta and E. Bernard have a fellowship from CNPq.
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João L. V. R. Carvalho, formal analysis, investigation, data curation, writing (original draft, review, and editing); Joenny M. S. Lima, formal analysis, investigation, data curation, writing (review and editing); Eder Barbier, Enrico Bernard, Jadson D. P. Bezerra, and Cristina M. Souza-Motta: conceptualization, supervision, project administration, funding acquisition, writing (original draft, review, and editing).
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The collection was authorised by the Ministério do Meio Ambiente (MMA)/Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) (SISBIO number 68992–3) and by the Ethics Committee on Animal Care–UFPE (number 114/2019).
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Carvalho, J.L.V.R., Lima, J.M.S., Barbier, E. et al. Ticket to ride: fungi from bat ectoparasites in a tropical cave and the description of two new species. Braz J Microbiol 53, 2077–2091 (2022). https://doi.org/10.1007/s42770-022-00841-y
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DOI: https://doi.org/10.1007/s42770-022-00841-y