Antonie van Leeuwenhoek

, Volume 107, Issue 3, pp 731–740 | Cite as

Escovopsis trichodermoides sp. nov., isolated from a nest of the lower attine ant Mycocepurus goeldii

  • Virginia E. Masiulionis
  • Marta N. Cabello
  • Keith A. Seifert
  • Andre Rodrigues
  • Fernando C. Pagnocca
Original Paper


Currently, five species are formally described in Escovopsis, a specialized mycoparasitic genus of fungus gardens of attine ants (Hymenoptera: Formicidae: tribe Attini). Four species were isolated from leaf-cutting ants in Brazil, including Escovopsis moelleri and Escovopsis microspora from nests of Acromyrmex subterraneusmolestans, Escovopsis weberi from a nest of Atta sp. and Escovopsis lentecrescens from a nest of Acromyrmex subterraneus subterraneus. The fifth species, Escovopsis aspergilloides was isolated from a nest of the higher attine ant Trachymyrmex ruthae from Trinidad. Here, we describe a new species, Escovopsis trichodermoides isolated from a fungus garden of the lower attine ant Mycocepurus goeldii, which differs from the five other species by highly branched, trichoderma-like conidiophores lacking swollen vesicles, with reduced conidiogenous cells and distinctive conidia morphology. Phylogenetic analyses based on partial tef1 gene sequences support the distinctiveness of this species. A portion of the internal transcribed spacers of the nuclear rDNA was sequenced to serve as a DNA barcode. Future molecular and morphological studies in this group of fungi will certainly unravel the taxonomic diversity of Escovopsis associated with fungus-growing ants.


Attini Fungus-growing ant Hypocreales Mycoparasitism 


  1. Allegrucci N, Eliades L, Cabello M, Arambarri A (2011) New species Koorchaloma and Ciliochlorella from xeric forests in Argentina. Mycotaxon 115:175–181CrossRefGoogle Scholar
  2. Almeida J (2005) Yeast community survey in the Tagus estuary. FEMS Microbiol Ecol 53:295–303CrossRefPubMedGoogle Scholar
  3. Augustin JO, Groenewald JZ, Nascimento RJ, Mizubuti ESG, Barreto RW, Elliot SL, Elliot SL, Evans HC (2013) Yet more “weeds” in the garden: fungal novelties from nests of leaf-cutting ants. PLoS One 8:e82265CrossRefPubMedCentralPubMedGoogle Scholar
  4. Bass M, Cherret JM (1995) Fungal hyphae as source of nutrients for the leaf-cutting ant Atta sexdens. Physiol Entomol 20:1–6CrossRefGoogle Scholar
  5. Chapela IH, Rehner SA, Schultz TR, Mueller UG (1994) Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:1691–1694CrossRefPubMedGoogle Scholar
  6. Currie CR (2001) Prevalence and impact of a virulent parasite on a tripartite mutualism. Oecologia 128:99–106CrossRefGoogle Scholar
  7. Currie CR, Mueller UG, Malloch D (1999) The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci USA 96:7989–8002CrossRefGoogle Scholar
  8. Currie CR, Wong B, Stuart AE, Schultz TR, Rehner SA, Mueller UG, Sung G, Spatofora JW, Straus NA (2003) Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299:386–388CrossRefPubMedGoogle Scholar
  9. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  10. Gams W (1973) Phialides with solitary conidia? Persoonia 7:161–169Google Scholar
  11. Gerardo NM, Mueller UG, Price SL, Currie CR (2004) Exploiting a mutualism: parasite specialization on cultivars within the fungus-growing ants symbiosis. Proc R Soc Lond B 271:1791–1798CrossRefGoogle Scholar
  12. Gerardo NM, Mueller UG, Currie CR (2006) Complex host-pathogen coevolution in the Apterostigma fungus-growing ant-microbe symbiosis. BMC Evol Biol 6:88CrossRefPubMedCentralPubMedGoogle Scholar
  13. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  14. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780CrossRefPubMedCentralPubMedGoogle Scholar
  15. Kendrick B (1971) Taxonomy of the fungi Imperfecti. University of Toronto Press, TorontoGoogle Scholar
  16. Kreisel H (1972) Pilzen aus Pilzgarten von Atta insularis in Kuba. A Allg Microbiol 12:643–654CrossRefGoogle Scholar
  17. Littledyke M, Cherrett JM (1976) Direct ingestion of plant sap from cut leaves by the leaf-cutting ants Atta cephalotes (L.) and Acromyrmex octospinosus (Reich) (Formicidae, Attini). Bull Entomol Res 66:205–217CrossRefGoogle Scholar
  18. Möller A (1893) Die Pilzgärten einiger Südamerikanischer Ameisen. Bot Mitt Trop 6:1–127Google Scholar
  19. Muchovej JJ, Della Lucia TMC (1990) Escovopsis, a new genus from leaf cutting ant nests to replace Phialocladus nomen invalidum. Mycotaxon 37:191–195Google Scholar
  20. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Accessed 29 July 2014
  21. Pagnocca FC, Masiulionis VE, Rodrigues A (2012) Specialized fungal parasites and opportunistic fungi in gardens of attine ants. Psyche. doi:10.1155/2012/905109 Google Scholar
  22. Quinlan RJ, Cherret JM (1979) The role of fungus in the diet of the leaf-cutting ants Atta cephalotes. Ecol Entomol 4:151–160CrossRefGoogle Scholar
  23. Reynolds HT, Currie CR (2004) Pathogenicity of Escovopsis: the parasite of the attine ant-microbe symbiosis directly consumes the ant cultivated fungus. Mycologia 96:955–959CrossRefPubMedGoogle Scholar
  24. Rodrigues A, Pagnocca FC, Bacci M Jr, Hebling MJA, Bueno OC, Penning LH (2005) Variability of non-mutualistic fungi associated with Atta sexdens rubropilosa nests. Folia Microbiol 50:421–425CrossRefGoogle Scholar
  25. Rodrigues A, Bacci M Jr, Mueller UG, Ortiz A, Pagnocca FC, Pagnocca FC (2008) Microfungal “weeds” in the leafcutter ant symbiosis. Microb Ecol 56:604–614CrossRefPubMedGoogle Scholar
  26. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542CrossRefPubMedCentralPubMedGoogle Scholar
  27. Schultz TR, Brady SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci USA 105:5435–5440CrossRefPubMedCentralPubMedGoogle Scholar
  28. Seifert KA, Samson RA, Chapela IH (1995) Escovopsis aspergilloides, a rediscovered hyphomycete from leaf-cutting ant nests. Mycologia 87:407–413CrossRefGoogle Scholar
  29. Seifert K, Morgan-Jones G, Gams W, Kendrick W (2011) The genera of hyphomycetes. CBS Biodivers Ser 12:1–997CrossRefGoogle Scholar
  30. Solomon SE, Lopes CT, Mueller UG, Rodrigues A, Sosa-Calvo J, Schultz TR, Vasconcelos HL (2011) Nesting biology and fungiculture of the fungus-growing ant, Mycetagroicus cerradensis: new light on the origin of higher attine agriculture. J Insect Sci 11:12CrossRefPubMedCentralPubMedGoogle Scholar
  31. Taerum SJ, Cafaro MJ, Little AEF, Schultz TR, Currie CR (2007) Low host-pathogen specificity in the leaf-cutting ant-microbe symbiosis. Proc R Soc Lond B 274:1971–1978CrossRefGoogle Scholar
  32. Taerum SJ, Cafaro MJ, Currie CR (2010) Presence of multiparasite infections within individual colonies of leaf-cutter ants. Environ Entomol 39:105–113CrossRefPubMedGoogle Scholar
  33. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedCentralPubMedGoogle Scholar
  34. Villesen P, Mueller UG, Schultz TR, Adams RM, Bouck AC (2004) Evolution of ant-cultivar specialization and cultivar switching in Apterostigma fungus-growing ants. Evolution 58:2252–2265CrossRefPubMedGoogle Scholar
  35. Weber NA (1972) Gardening ants: the attines. American Philosophical Society, PhiladelphiaGoogle Scholar
  36. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Virginia E. Masiulionis
    • 1
  • Marta N. Cabello
    • 2
  • Keith A. Seifert
    • 3
  • Andre Rodrigues
    • 4
    • 1
  • Fernando C. Pagnocca
    • 4
    • 1
  1. 1.Centro de Estudos de Insetos Sociais, Instituto de BiociênciasUNESP – Univ Estadual PaulistaRio ClaroBrazil
  2. 2.Comisión de Investigaciones Científicas, Facultad de Ciencias Naturales y Museo, Instituto de Botánica Carlos SpegazziniUniversidad Nacional de La PlataLa PlataArgentina
  3. 3.Biodiversity (Mycology)Eastern Cereal and Oilseed Research Centre, Agriculture & Agri-Food CanadaOttawaCanada
  4. 4.Departamento de Bioquímica e Microbiologia, Instituto de BiociênciasUNESP – Univ Estadual PaulistaRio ClaroBrazil

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