Skip to main content
SpringerLink
Log in

Fungal Community Associated with the Leaf-Cutting Ant Acromyrmex crassispinus (Hymenoptera: Formicidae) Colonies: a Search for Potential Biocontrol Agents

  • Invertebrate Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

A Correction to this article was published on 25 May 2023

This article has been updated

Abstract

The leaf-cutting ant Acromyrmex crassispinus is considered an important pest in forest plantations in southern Brazil. This work aimed to study the fungal community associated with A. crassispinus colonies, subjected to treatments with subdoses of granulated baits (sulfluramid), which might reduce the ability of the ants to care for their symbiotic fungus and other fungi (maybe biocontrol fungi) would take over, to prospect for potential biological control agents. Samplings of fungus gardens and dead ants allowed the identification of 195 fungal isolates, distributed in 29 families, 36 genera, and 53 species. The most frequent genera were Trichoderma (49.2%), Penicillium (13.8%), Chaetomium (6.2%), and Fusarium (3.6%). This is the first study that conducted a survey of antagonistic and entomopathogenic fungi to A. crassispinus and its symbiotic fungus, reporting for the first time the occurrence of potential biological control agents. Escovopsis weberi, Fusarium oxysporum, Rhizomucor variabilis, Trichoderma atroviride, Trichoderma harzianum, Trichoderma koningiopsis, and Trichoderma spirale are considered some of the potential biocontrol organisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The datasets generated and analyzed during the study are available from the corresponding author on reasonable request.

Change history

References

  1. Fisher PJ, Stradling DJ, Pegler DN (1994) Leucoagaricus basidiomata from a live nest of the leaf-cutting ant Atta cephalotes. Mycol Res 98:884–888

    Article  Google Scholar 

  2. Currie C, Scott J, Summerbell R, Malloch D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701–704. https://doi.org/10.1038/19519

    Article  CAS  Google Scholar 

  3. Rodrigues A, Pagnocca FC, Bacci M, Hebling MJA, Bueno OC, Pfenning LH (2005) Variability of non-mutualistic filamentous fungi associated with Atta sexdens rubropilosa nests. Folia Microbiol 50:421. https://doi.org/10.1007/BF02931424

    Article  CAS  Google Scholar 

  4. Rodrigues A, Cable RN, Mueller UG, Bacci M, Pagnocca FC (2009) Antagonistic interactions between garden yeasts and microfungal garden pathogens of leaf-cutting. Antonie Van Leeuwenhoek 96:331–342. https://doi.org/10.1007/s10482-009-9350-7

    Article  PubMed  Google Scholar 

  5. Goffré D, Folgarait PJ (2018) Insights into the biodiversity and causes of distribution of potential entomopathogens associated with leaf-cutting ants. Insectes Soc 65:103–115. https://doi.org/10.1007/s00040-017-0592-5

    Article  Google Scholar 

  6. Pagnocca FC, Rodrigues A, Bacci JRM (2011) Microrganismos associados às formigas cortadeiras. In: Della Lucia TMC (ed) Formigas-cortadeiras: da bioecologia ao manejo. 1st edn. Ed. UFV, Viçosa, pp 262–283

  7. Reynolds HT, Currie CR (2004) Pathogenicity of Escovopsis weberi: the parasite of the attine ant-microbe symbiosis directly consumes the ant-cultivated fungus. Mycologia 96:955–959. https://doi.org/10.1080/15572536.2005.11832895

    Article  PubMed  Google Scholar 

  8. Bacci M Jr, Ribeiro SB, Casarotto MEF, Pagnocca FC (1995) Biopolymer-degrading bacteria from nests of the leaf-cutting ant Atta sexdens rubropilosa. Braz J Med Biol Res 28:79–82

    Google Scholar 

  9. Carreiro SC, Pagnocca FC, Bacci MJ, Bueno OC, Hebling MJA, Middelhoven WJ (2002) Occurrence of killer yeasts in leaf-cutting ant nests. Folia Microbiol 47:259–262. https://doi.org/10.1007/BF02817648

    Article  CAS  Google Scholar 

  10. Santos AV, Dillon RJ, Dillon VM, Reynolds SE, Samuels RI (2004) Ocurrence of the antibiotic producing bacterium Burkholderia sp. in colonies of the leaf-cutting ant Atta sexdens rubropilosa. FEMS Microbiol Lett 239:319–323. https://doi.org/10.1016/j.femsle.2004.09.005

    Article  CAS  PubMed  Google Scholar 

  11. Mueller UG (2012) Symbiont recruitment versus ant-symbiont co-evolution in the attine ant–microbe symbiosis. Curr Opin Microbiol 15:269–277. https://doi.org/10.1016/j.mib.2012.03.001

    Article  PubMed  Google Scholar 

  12. Hughes WOH, Thomsen L, Eilenberg J, Boomsma JJ (2004) Diversity of entomopathogenic fungi near leaf-cutting ant nest in a neotropical forest, with particular reference to Metarhizium anisopliae var. anisopliae. J Invertebr Pathol 85:46–53. https://doi.org/10.1016/j.jip.2003.12.005

    Article  CAS  PubMed  Google Scholar 

  13. Carlos AA, Rodrigues A, Forti LC, Passador MM, Sierra JF (2011) Filamentous fungi found in Atta sexdens rubropilosa colonies after treatment with different toxic bait formulations. J Appl Entomol 135:326–331. https://doi.org/10.1111/j.1439-0418.2010.01551.x

    Article  Google Scholar 

  14. Marfetán JA, Folgarait PJ (2017) Diversity of mycobiota in colonies of different species of leaf-cutting ants and sampling sites across Argentina. Ecología Austral 27:312–495. https://doi.org/10.25260/EA.17.27.3.0.488

    Article  Google Scholar 

  15. Vinha GL, Alcántara de La Cruz R, Della Lucia TMC, Wilcken CF, Dias da Silva E, Lemes PG, Zanuncio JC (2020) Leaf-cutting ants in commercial forest plantations of Brazil: biological aspects and control methods. South For 82:95–103

    Article  Google Scholar 

  16. Rando JSS, Forti LC (2005) Ocorrência de formigas Acromyrmex Mayr, 1865, em alguns municípios do Brasil. Acta Sci Biol Sci 27:129–133. https://doi.org/10.4025/actascibiolsci.v27i2.1322

    Article  Google Scholar 

  17. MCT-PR (2021) Dados gerais. Município de Campo do Tenente - Estado do Paraná http://campodotenente.pr.gov.br/portal/dados-gerais. Acessed 01 Feb 2021

  18. Silveira VD (1981) Micologia, 4th edn. Interamericana, Rio de Janeiro

    Google Scholar 

  19. Barnett HL, Hunter BB (1998) Descriptions and illustrations of genera. Illustrated genera of imperfect fungi, 4th edn. American Phytopathological Society. St. Paul

  20. Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006

    Article  Google Scholar 

  21. Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349. https://doi.org/10.2307/1942268

    Article  Google Scholar 

  22. Hammer Ø, Harper DA, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9. https://paleo.carleton.ca/2001_1/past/past.pdf. Accessed 21 March 2021

  23. Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456. https://doi.org/10.1111/2041-210X.12613

    Article  Google Scholar 

  24. Weber NA (1972) Gardening Ants: the attines. American Philosophical Society, Philadelphia

    Google Scholar 

  25. Bass M, Cherrett JM (1994) The role of leaf-cutting ant workers (Hymenoptera: Formicidae) in fungus garden maintenance. Ecol Entomo 19:215–220. https://doi.org/10.1111/j.1365-2311.1994.tb00412.x

    Article  Google Scholar 

  26. Ortiz A, Madrigal A, Orduz S (1999) Evaluacion del comportamiento de las hormigas Atta cephalotes (Hymenoptera: Formicidae) frente a la contaminacion del jardin del hongo con Trichoderma lignorum. Rev Colomb Entomol 150:53–60. https://doi.org/10.25100/socolen.v25i2.9770

    Article  Google Scholar 

  27. Silva A, Bacci M Jr, Siqueira CG, Bueno OC, Pagnocca FC, Hebling MJA (2003) Survival of Atta sexdens workers on different food sources. J Insect Physiol 49:307–313. https://doi.org/10.1016/S0022-1910(03)00004-0

    Article  CAS  PubMed  Google Scholar 

  28. Fisher PJ, Stradling DJ, Sutton BC, Petrini LE (1996) Microfungi in the fungus gardens of the leaf-cutting ant Atta cephalotes: a preliminary study. Mycol Res 100:541–546. https://doi.org/10.1016/S0953-7562(96)80006-2

    Article  Google Scholar 

  29. Currie CR, Mueller UG, Malloch D (1999) The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci 96:7998–8002. https://doi.org/10.1073/pnas.96.14.7998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Rodrigues A, Bacci M Jr, Mueller UG, Ortiz A, Pagnocca FC (2008) Microfungal “weeds” in the leafcutter ant symbiosis. Microb Ecol 56:604–614. https://doi.org/10.1007/s00248-008-9380-0

    Article  CAS  PubMed  Google Scholar 

  31. Kredics L, Hatvani L, Naeimi S, Körmöczi P (2014) Biodiversity of the genus Hypocrea/Trichoderma in different habitats. In: Gupta S, Herrera-Estrella A, Upadhyay RS (eds) Biotechnology and biology of Trichoderma. Elsevier, Amsterdam, pp 3–24

    Chapter  Google Scholar 

  32. Silva A, Rodrigues A, Bacci M, Pagnocca FC, Bueno ODC (2006) Susceptibility of the ant-cultivated fungus Leucoagaricus gongylophorus (Agaricales: Basidiomycota) towards microfungi. Mycopathologia 162:115–119. https://doi.org/10.1007/s11046-006-0037-6

    Article  CAS  PubMed  Google Scholar 

  33. Castrillo ML, Bich GA, Zapata PD, Villalba L (2016) Biocontrol of Leucoagaricus gongylophorus of leaf-cutting ants with the mycoparasitic agent Trichoderma koningiopsis. Mycosphere 7:810–819. https://doi.org/10.5943/mycosphere/7/6/12

    Article  Google Scholar 

  34. Nascimento MO, Sarmento RA, Santos GR, Oliveira CA, Souza DJ (2017) Antagonism of Trichoderma isolates against Leucoagaricus gongylophorus (Singer) Möller. J Basic Microbiol 57:699–704. https://doi.org/10.1002/jobm.201600755

    Article  CAS  PubMed  Google Scholar 

  35. Rodrigues A, Passarini MRZ, Ferro M, Nagamoto NS, Forti LC, Bacci M, Sette LD, Pagnocca FC (2013) Fungal communities in the garden chamber soils of leaf-cutting ants. J Basic Microbiol 54:1186–1196. https://doi.org/10.1002/jobm.201200458

    Article  CAS  PubMed  Google Scholar 

  36. Rocha SL, Evans HC, Jorge VL, Cardoso LAO, Pereira FST, Rocha FB, Barreto RW, Hart AG, Elliot SL (2017) Recognition of endophytic Trichoderma species by leaf-cutting ants and their potential in a Trojan-horse management strategy. R Soc Open Sci 4:160628. https://doi.org/10.1098/rsos.160628

  37. Farrow WM (1954) Tropical soil fungi. Mycol 46:632–646. https://doi.org/10.1080/00275514.1954.12024399

    Article  Google Scholar 

  38. Marfetán JA, Romero AI, Folgarait PJ (2015) Pathogenic interaction between Escovopsis weberi and Leucoagaricus sp.: mechanisms involved and virulence levels. Fungal Ecol 17:52–61. https://doi.org/10.1016/j.funeco.2015.04.002

    Article  Google Scholar 

  39. De Lucca AJ (2007) Harmful fungi in both agriculture and medicine. Rev Iberoam Micol 24:3–13

    PubMed  Google Scholar 

  40. Marti HE, Carlson AL, Brown BV, Mueller UG (2015) Foundress queen mortality and early colony growth of the leafcutter ant, Atta texana (Formicidae, Hymenoptera). Insectes Soc 62:357–363. https://doi.org/10.1007/s00040-015-0413-7

    Article  Google Scholar 

  41. Sun BD, Yu HY, Chen AJ, Liu XZ (2008) Insect-associated fungi in soils of field crops and orchards. Crop Prot 27:1421–1426. https://doi.org/10.1016/j.cropro.2008.07.010

    Article  Google Scholar 

  42. Castilho AMC, Fraga ME, Aguiar-Menezes EL, Rosa CAR (2010) Selection of Metarhizium anisopliae and Beauveria bassiana isolates pathogenic to Atta bisphaerica and Atta sexdens rubropilosa soldiers under laboratory conditions. Cien Rural 40:1243–1249

    Article  Google Scholar 

  43. Hughes WOH, Boomsma JJ (2004) Let your enemy do the work: within-host interactions between two fungal parasites of leaf-cutting ants. Proc R Soc B 271(Suppl_3):S104–S106. https://doi.org/10.1098/rsbl.2003.0115

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ribeiro MMR, Amaral KD, Seide VE, Souza BMR, Della Lucia TMC, Kasuya MCM, de Souza DJ (2012) Diversity of fungi associated with Atta bisphaerica (Hymenoptera: Formicidae): the activity of Aspergillus ochraceus and Beauveria bassiana. Psyche 2012:389806. https://doi.org/10.1155/2012/389806

    Article  Google Scholar 

  45. Angelone S, Bidochka MJ (2018) Diversity and abundance of entomopathogenic fungi at ant colonies. J Invertebr Pathol 156:73–76. https://doi.org/10.1016/j.jip.2018.07.009

    Article  PubMed  Google Scholar 

  46. Maciel CG, Walker C, dos Santos RF, Muniz MFB, Brum DL (2017) Fusarium oxysporum and F. verticillioides associated with damping-off in Pinus spp. Revista Ciência Agronômica 48:134–141. https://doi.org/10.5935/1806-6690.20170015

    Article  Google Scholar 

  47. Auer CG, Grigoletti A Jr, dos Santos AF (2001) Doenças em pinus: identificação e controle. Embrapa Florestas-Circular Técnica (INFOTECA-E), Colombo

  48. Dos Santos AF, Kleina HT, Fuzitani EJ, Duarte HSS (2019) Uso do Trichoderma em culturas florestais. In: Meyer MC, Mazaro SM, Silva JC (ed) Trichoderma uso na agricultura. Embrapa, Brasília, pp 521–536

Download references

Acknowledgements

We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for fellowship for the first author and Fundo Nacional de Controle de Pragas Florestais (FUNCEMA) for financial support. We also thank Arauco Forest Brasil company for granting the study area.

Author information

Authors and Affiliations

  1. Departamento de Ciências Florestais, Universidade Federal Do Paraná, Av. Pref. Lothário Meissner, 900, Jardim Botânico, Curitiba, Curitiba, Paraná, 80210-170, Brazil

    Thiele Sides Camargo

  2. Departamento de Zoologia, Universidade Federal Do Paraná, Curitiba, Paraná, Brazil

    Mariane Aparecida Nickele

  3. Epagri, Itajaí, Santa Catarina, Brazil

    Wilson Reis Filho

  4. Embrapa Florestas, Colombo, Paraná, Brazil

    Susete do Rocio Chiarello Penteado & Celso Garcia Auer

  5. Funcema, Curitiba, Paraná, Brazil

    Elisiane Castro de Queiroz

Authors
  1. Thiele Sides Camargo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mariane Aparecida Nickele
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wilson Reis Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Susete do Rocio Chiarello Penteado
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elisiane Castro de Queiroz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Celso Garcia Auer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thiele Sides Camargo.

Ethics declarations

Consent to Participate

The authors have given informed consent regarding the submission of the manuscript.

Conflict of Interest

The authors declare no competing interests.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Camargo, T.S., Nickele, M.A., Filho, W.R. et al. Fungal Community Associated with the Leaf-Cutting Ant Acromyrmex crassispinus (Hymenoptera: Formicidae) Colonies: a Search for Potential Biocontrol Agents. Microb Ecol 86, 1281–1291 (2023). https://doi.org/10.1007/s00248-023-02217-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-023-02217-7

Keywords

Search

Navigation