Mycophagy of Attini Ants (Hymenoptera, Formicidae, Myrmicinae) with Agaricales Mushrooms (Basidiomycota, Agaricomycetes) at Riparian Zone in Southern Brazil

Micofagia de Formigas Attini (Hymenoptera, Formicidae, Myrmicinae) com Cogumelos Agaricales (Basidiomycota, Agaricomycetes) em Zonas Ripárias no Sul do Brasil

Autores

  • Alice Lemos Costa
  • Cassiane Furlan-Lopes
  • Fernando Augusto Bertazzo-Silva
  • Ana Luiza Klotz-Neves
  • Kamille Rodrigues Ferraz
  • Andreas Köhler
  • Jair Putzke

DOI:

https://doi.org/10.34188/bjaerv5n4-039

Palavras-chave:

Food resource, spore dispersing agents, ecological interactions

Resumo

Attini ants (Hymenoptera, Formicidae, Myrmicinae) have great diversity in exploiting food resources. However, little is known about the mycophagy involving Agaricales fungi (Basidiomycota, Agaricomycetes). Moreover, these associations are of paramount importance in riparian zones, as the interaction among soil, fauna and flora is fundamental to the maintenance of these environments. Thus, the aim of this study was to describe cases of mycophagy between ants and fungi in order to understand how these associations occur in riparian zones. To this, collections were made between 2021-2022 in the valleys of the Rio Vacacaí, Rio dos Sinos and Rio Pardo in the state of Rio Grande do Sul, Brazil. The samples were analyzed for characters macro and microscopic and identified taxonomically. Mycophagy activities of six species of ants worker were cataloged, among them Acromyrmex niger, Acromyrmex versicolor, Tranopelta gilva, Tranopelta subterranea, Pheidole flavens and Mycetosoritis hartmanni, which included in their diet the mushrooms Agaricus rufoaurantiacus, Macrocybe titans, Agrocybe underwoodii, Dactylosporina steffenii, Lepiota micropholis and Neopaxillus echinospermus, respectively. The observed interactions demonstrate the dispersal of fungal spores through ant body structures, such as legs, antennae, thorax and abdomen; basidiomata as aliment source, such as pileus, lamellae and stipe; and generalized and specialized levels of predation on various fungi structures. Our results demonstrate unprecedented mycophagous relationships and show that Agaricales fungi can be considered a food source for Attini in riparian zones in Brazil south.

Referências

Amaringo-Cortegano CA, Vargas-Isla R, Morais JW & Ishikawa NK. Artrópodos asociados a seis especies de hongos comestibles de ocurrencia natural en Manaus, Amazonas, Brasil. Biota Amazônia (Biote Amazonie, Biota Amazonia, Amazonian Biota), v. 3, n. 3, p. 54-63, 2013. DOI: http://dx.doi.org/10.18561/21795746/biotaamazonia.v3n3p54-63

Aylward FO, Burnum-Johnson KE, Tringe SG, Teiling C, Tremmel DM, Moeller JA & Currie CR. Leucoagaricus gongylophorus produces diverse enzymes for the degradation of recalcitrant plant polymers in leaf-cutter ant fungus gardens. Applied and Environmental Microbiology, v. 79, n. 12, p. 3770-3778, 2013. DOI: https://doi.org/10.1128/AEM.03833-12

Baccaro FB, Feitosa RM, Fernández F, Fernandes IO, Izzo TJ, Souza JD & Solar R. Guia para os gêneros de formigas do Brasil. Manaus: Editora INPA, v. 388, 2015.

Batra SWT & Batra LR. The fungus gardens of insects. Scientific American, v. 217, n. 5, p. 112-124, 1967.

Battistin E, Picciola P. Two particular taxa from Brazil: Macrocybe titans and Marasmius leoninus. Rivista Micologica Romana. Bollettino dell’Associazione Micologica ed Ecologica Romana, v. 96, n. 3, p. 31-38, 2015.

Biedermann PHW & Vega FE. Ecology and evolution of insect–fungus mutualisms. Annu. Rev. Entomol, v. 65, p. 431-455, 2020.

Bizarria JRR, Pagnocca FC & Rodrigues A. Yeasts in the attine ant–fungus mutualism: Diversity, functional roles, and putative biotechnological applications. Yeast, v. 39, n. 1-2, p. 25-39, 2022. DOI: https://doi.org/10.1002/yea.3667

Branstetter MG, Ješovnik A, Sosa-Calvo J, Lloyd MW, Faircloth BC, Brady SG & Schultz TR. Dry habitats were crucibles of domestication in the evolution of agriculture in ants. Proceedings of the Royal Society B: Biological Sciences, v. 284, n. 1852, p. 20170095, 2017. DOI: https://doi.org/10.1098/rspb.2017.0095

Brasil. Lei no 12.651, de 15 de maio de 2012. Institui o Novo Código Florestal Brasileiro. Diário Oficial da União, 15 maio 2012. Disponível em: <https://www.planalto.gov.br/ccivil_03/_ato2011-2014/2012/lei/l12651.htm> Acesso em 17 de abril de 2022.

Casadei-Ferreira A, Economo EP & Feitosa RM. Additions to the taxonomy of Pheidole (Hymenoptera: Formicidae) from the southern grasslands of Brazil. Revista Brasileira de Entomologia, v. 64, 2020. DOI: https://doi.org/10.1590/1806-9665-RBENT-2020-0068

Claridge AW & Trappe JM. Sporocarp mycophagy: nutritional, behavioral, evolutionary, and physiological aspects. Mycology Series, v. 23, p. 599, 2005.

Clark RM & Fewell JH. Transitioning from unstable to stable colony growth in the desert leafcutter ant Acromyrmex versicolor. Behavioral ecology and sociobiology, v. 68, n. 1, p. 163-171, 2014. DOI: https://doi.org/10.1007/s00265-013-1632-4

Coimbra VRM. Checklist of Central and South American Agaricales (Basidiomycota) II: Strophariaceae. Mycosphere, v. 6, n. 4, p. 441-458, 2015.

Csata E & Dussutour A. Nutrient regulation in ants (Hymenoptera: Formicidae): a review. Myrmecological News, v. 29, p. 111-124, 2019. DOI: https://doi.org/10.25849/myrmecol.news_029:111

Dash CK, Bamisile BS, Keppanan R, Qasim M, Lin Y, Islam SU, & Wang L. Endophytic entomopathogenic fungi enhance the growth of Phaseolus vulgaris L.(Fabaceae) and negatively affect the development and reproduction of Tetranychus urticae Koch (Acari: Tetranychidae). Microbial pathogenesis, v. 125, p. 385-392, 2018. DOI: https://doi.org/10.1016/j.micpath.2018.09.044

de Fine LHH, Boomsma JJ & Tunlid A. Symbiotic adaptations in the fungal cultivar of leaf-cutting ants. Nature Communications, v. 5, n. 1, p. 1-10, 2014. DOI: https://doi.org/10.1038/ncomms6675

de Moura RG & Okura MH. Cogumelos comestíveis no Brasil: uma revisão bibliográfica. Research, Society and Development, v. 11, n. 8, p. e24711830830-e24711830830, 2022. DOI: DOI: https://doi.org/10.33448/rsd-v11i8.30830

Delabie JHC, Agosti D & Nascimento IC. Litter ant communities of the Brazilian Atlantic rain forest region. Sampling Ground-dwelling Ants: case studies from the world’s rain forests. Curtin University of Technology School of Environmental Biology Bulletin, v. 18, 2000.

Demétrio MF, Silvestre R., Souza PRD & Aoki C. Inventário da fauna de formigas (Hymenoptera, formicidae) no Mato Grosso do Sul, Brasil. Iheringia. Série Zoologia, v. 107, 2017. DOI: https://doi.org/10.1590/1678-4766e2017126

Epps MJ & Penick CA. Facultative mushroom feeding by common woodland ants (Formicidae, Aphaenogaster spp.). Food webs, v. 14, p. 9-13, 2018. DOI: https://doi.org/10.1016/j.fooweb.2017.12.001

Estat - Sistema de Análise Estatística (ESTAT 2.0). Jaboticabal: Pólo Computacional do Departamento de Ciências Exatas da UNESP. 1994.

Fernández CF & Sendoya SF. List of neotropical ants (Hymenoptera: Formicidae). Lista de las hormigas neotropicales (Hymenoptera: Formicidae). Biota Colombiana., v. 5, n. 1, p. 3-93, 2004.

Fernandez CF. Myrmicine ants of the genera Ochetomyrmex and Tranopelta (Hymenoptera: Formicidae). Sociobiology, v. 41, n. 3, p. 633-662, 2003.

Fisher BL & Cover SP. Ants of North America: a guide to the genera. Univ of California Press, 2007.

Fowler HG. Taxa of the neotropical grass-cutting ants, Acromyrmex (Moellerius) (Hymenoptera: Formicidae: Attini). Científica, v. 16, p. 281-295, 1988.

Fung SY & Tan CS. Mushroom Market in Malaysia. In: Advances in Macrofungi. CRC Press, 2022. p. 41-50.

Garcia FRM, Ahlert CC, de Freitas BR, Trautmann MM, Tancredo SP & Lutinski JA. Ants (Hymenoptera: Formicidae) in five hospitals of Porto Alegre, Rio Grande do Sul State, Brazil. Acta Scientiarum. Health Sciences, v. 33, n. 2, p. 203-209, 2011. DOI: https://doi.org/10.4025/actascihealthsci.v33i2.10999

Gonçalves CR. O gênero Acromyrmex no Brasil (Hym. Formicidae). Studia entomológica, v. 4, n. 1-4, p. 113-180, 1961.

Hervey A, Rogerson CT & Leong I. Studies on fungi cultivated by ants. Brittonia, v. 29, n. 2, p. 226-236, 1977.

Houadria M & Menzel F. Temporal and dietary niche is context‐dependent in tropical ants. Ecological Entomology, v. 45, n. 4, p. 761-770, 2020. DOI: https://doi.org/10.1111/een.12857

Innocenti G & Sabatini MA. Collembola and plant pathogenic, antagonistic and arbuscular mycorrhizal fungi: A review. Bulletin of Insectology, v. 71, n. 1, p. 71-76, 2018.

Julian GE, Fewell JH. Genetic variation and task specialization in the desert leaf-cutter ant, Acromyrmex versicolor. Animal Behaviour, v. 68, n. 1, p. 1-8, 2004. DOI: https://doi.org/10.1016/j.anbehav.2003.06.023

Lanan M. Spatiotemporal resource distribution and foraging strategies of ants (Hymenoptera: Formicidae). Myrmecological news/Osterreichische Gesellschaft fur Entomofaunistik, v. 20, p. 53, 2014.

Lenth R, Lenth MR. Package ‘lsmeans’. The American Statistician, v. 34, n. 4, p. 216-221, 2018.

Loeck AE, Grutzmacher D & Coimbra S. Ocorrência de formigas cortadeiras do gênero Acromyrmex nas principais regiões agropecuárias do Rio Grande do Sul. Current Agricultural Science and Technology, v. 9, n. 2, 2003.

Meijer AAR. Macrofungos notáveis das Florestas de Pinheiro-do-Paraná. Colombo: Embrapa, 2008.

Mertl AL, Traniello JF, Ryder WK & Constantino R. Associations of two ecologically significant social insect taxa in the litter of an Amazonian rainforest: is there a relationship between ant and termite species richness?. Psyche, v. 2012, 2012. DOI: https://doi.org/10.1155/2012/312054

Moreira IDJS, Cruz CDF, Fernandes AKC, Delabie JHC, Castaño-Meneses G & Mariano CDSF. Estudo comparativo da fauna de comensais nos formigueiros de três espécies de grande tamanho da mirmecofauna brasileira (Hymenoptera: Formicidae). Boletim do Museu Paraense Emílio Goeldi-Ciências Naturais, v. 15, n. 2, p. 377-391, 2020. DOI: https://doi.org/10.46357/bcnaturais.v15i2.303

Mueller GM & Mata M. Newsletter of the Mycological Society of America. Mycologia, v. 52, p. 5, 2001.

Nelsen MP, Ree RH & Moreau CS. Ant–plant interactions evolved through increasing interdependence. Proceedings of the National Academy of Sciences, v. 115, n. 48, p. 12253-12258, 2018. DOI: https://doi.org/10.1073/pnas.1719794115

Pegler DN, Lodge DJ & Nakasone KK. The pantropical genus Macrocybe gen. nov. Mycologia, v. 90, n. 3, p. 494-504, 1998.

Pegler DN. The agarics of Sao Paulo: an account of the agaricoid fungi (Holobasidiomycetes) of Sao Paulo State, Brazil. Royal Botanic Gardens Kew, 1997.

Pereira H, Jossart M & Detrain C. 2020. Waste management by ants: the enhancing role of larvae. Animal Behaviour, v. 168, p. 187-198, 2020. DOI: https://doi.org/10.1016/j.anbehav.2020.08.017

Pollierer MM, Scheu S & Tiunov AV. Isotope analyses of amino acids in fungi and fungal feeding Diptera larvae allow differentiating ectomycorrhizal and saprotrophic fungi‐based food chains. Functional Ecology, v. 34, n. 11, p. 2375-2388, 2020. DOI: https://doi.org/10.1111/1365-2435.13654

Prado LPD, Feitosa RM, Triana SP, Gutiérrez JAM, Rousseau GX, Silva RA & Andrade-Silva J. An overview of the ant fauna (Hymenoptera: Formicidae) of the state of Maranhão, Brazil. Papéis Avulsos de Zoologia, v. 59, 2019. DOI: https://doi.org/10.11606/1807-0205/2019.59.38

Putzke J & Putzke MTL. Cogumelos-Fungos agaricales no Brasil, familias agaricaceae, amanitaceae, bolbitaceae, entolomataceae, coprinaceae/psathyrellaceae, crepidotaceae e hygrophoraceae. vol. 1. São Gabriel: Editora JP, 2017.

Putzke J, Pereira AB. O gênero Oudemansiella Speg. no Rio Grande do Sul, Brasil. Caderno de Pesquisa: Série Botânica, v. 1, n. 1, p. 47-69, 1988.

Rayner ADM, Watling R & Frankland JC. Resource relations–an overview. Developmental biology of higher fungi, v. 10, p. 1-40, 1985.

Ryder WKT, Mertl AL & Traniello JFA. Biodiversity below ground: probing the subterranean ant fauna of Amazonia. Naturwissenschaften, v. 94, n. 9, p. 725-731, 2007.

Sabin TE & Stafford SG. Assessing the need for transformation of response variables. 1990.

Sanchez-Peña SR. Some fungus-growing ants (Hymenoptera: Formicidae) from northeastern Mexico. Florida Entomologist, v. 93, n. 4, p. 501-504, 2010. DOI: https://doi.org/10.1653/024.093.0404

Sarnat EM, Rabeling C, Economo EP & Wilson EO. First record of a species from the New World Pheidole flavens-complex (Hymenoptera: Formicidae) introduced to the southwestern Pacific. BioInvasions Record, v. 3, n. 4, 2014. DOI: http://dx.doi.org/10.3391/bir.2014.3.4.13

Schigel DS. Fungivory and host associations of Coleoptera: a bibliography and review of research approaches. Mycology, v. 3, n. 4, p. 258-272, 2012. DOI: https://doi.org/10.1080/21501203.2012.741078

Silva LT. Inventário rápido da mirmecofauna dos Parques Nacionais da Chapada dos Guimarães-MT e do Iguaçú-PR. 2018.

Silva-Filho AG, Seger C & Cortez VG. The neurotropic genus Copelandia (Basidiomycota) in western Paraná State, Brazil. Revista mexicana de biodiversidad, v. 89, n. 1, p. 15-21, 2018. DOI: https://doi.org/10.22201/ib.20078706e.2018.1.1994

Singer R. & Digilio APL. Pódromo de La Flora Agaricina Argentina. Lilloa, v. 25, n.2, p. 5-461, 1951.

Singer R. Agaricales new for Mexico or Central America. Anales del Instituto de Biología. Serie Botánica, v. 60, n. 1, p. 27-36, 1990.

Singer R. Boletes and related groups in South America. Nova Hedwigia, v.7, n.1, p. 93-132, 1964.

Solomon SE, Lopes CT, Mueller UG, Rodrigues A, Sosa-Calvo J, Schultz TR & Vasconcelos HL. Nesting biology and fungiculture of the fungus-growing ant, Mycetagroicus cerradensis: new light on the origin of higher attine agriculture. Journal of Insect Science, v. 11, n. 1, 2011. DOI: https://doi.org/10.1673/031.011.0112

Sosa-Calvo J, Brady SG & Schultz TR. The gyne of the enigmatic fungus-farming ant species Mycetosoritis explicata. Journal of Hymenoptera Research, v. 18, n. 1, p. 113-20, 2009.

Sosa-Calvo J, Ješovnik A, Vasconcelos HL, Bacci JrM & Schultz TR. Rediscovery of the enigmatic fungus-farming ant" Mycetosoritis" asper Mayr (Hymenoptera: Formicidae): implications for taxonomy, phylogeny, and the evolution of agriculture in ants. PLoS One, v. 12, n. 5, p. e0176498, 2017.

Tozlu E, Tozlu G & Kotan R. Biocontrol of Cymbalophora rivularis (Menetries) (Lepidoptera: Erebidae) larvae by entomopathogenic bacteria and fungi. Egyptian Journal of Biological Pest Control, v. 32, n. 1, p. 1-7, 2022. DOI: https://doi.org/10.1186/s41938-022-00565-z

Tuma J, Eggleton P, Fayle TM. Ant‐termite interactions: an important but under‐explored ecological linkage. Biological Reviews, v. 95, n. 3, p. 555-572, 2020. DOI: https://doi.org/10.1111/brv.12577

Valões-Araújo JC, Wartchow F. Checklist da micota agaricoide e de morfologia similar do Estado da Paraíba, Brasil. Hoehnea, v. 48, 2021. DOI: https://doi.org/10.1590/2236-8906-132/2020

Vaz-de-Mello FZ, Louzada JN & Schoereder JH. New data and comments on scarabaeidae (Coleoptera: Scarabaeoidea) associated with attini (Hymenoptera: Formicidae). The Coleopterists' Bulletin, p. 209-216, 1998.

Vidon PG, Welsh MK & Hassanzadeh YT. Twenty years of riparian zone research (1997–2017): Where to next?. Journal of Environmental Quality, v. 48, n. 2, p. 248-260, 2019. DOI: https://doi.org/10.2134/jeq2018.01.0009

Von-Beeren C, Mair MM & Witte V. Discovery of a second mushroom harvesting ant (Hymenoptera: Formicidae) in Malayan tropical rainforests. Myrmecological News, v. 20, p. 37-42, 2014.

Wakil W, Ghazanfar MU, Usman M, Hunter D, & Shi W. Fungal-Based Biopesticide Formulations to Control Nymphs and Adults of the Desert Locust, Schistocerca gregaria Forskål (Orthoptera: Acrididae): A Laboratory and Field Cage Study. Agronomy, v. 12, n. 5, p. 1160, 2022. DOI: https://doi.org/10.3390/agronomy12051160

Walter BMT & Guarino ESG. Comparação do método de parcelas com o" levantamento rápido" para amostragem da vegetação arbórea do Cerrado sentido restrito. Acta Botanica Brasilica, v. 20, p. 285-297, 2006. DOI: https://doi.org/10.1590/S0102-33062006000200005

Wartchow F, Putzke J & Cavalcanti MAQ. Agaricaceae Fr.(Agaricales, Basidiomycota) from areas of Atlantic Forest in Pernambuco, Brazil. Acta Botanica Brasilica, v. 22, p. 287-299, 2008. https://doi.org/10.1590/S0102-33062008000100026

Wartchow F, Pereira J, Drechsler-Santos ER, Gomes-Silva AC, Tiago PV, Putzke J & Cavalcanti MAQ. Two Oudemansiella species with echinulate basidiospores from South America with O. macracantha lectotypified. Mycotaxon, v. 113, n. 1, p. 119-127, 2010. DOI: https://doi.org/10.5248/113.119

Watling R & Meijer AR. Macromycetes from the state of Paraná, Brazil: 5. Poroid and lamellate boletes. Edinburgh Journal of Botany, v. 54, n. 2, p. 231-251, 1997. DOI: https://doi.org/10.1017/S0960428600004042

Watling R. Observations on the Bolbitiaceae-30: some Brazilian taxa. Boletín de la Sociedad Argentina de Botánica, 1992.

White JF, Kingsley KL, Verma SK & Kowalski KP. Rhizophagy cycle: an oxidative process in plants for nutrient extraction from symbiotic microbes. Microorganisms, v. 6, n. 3, p. 95, 2018. DOI: https://doi.org/10.3390/microorganisms6030095

Wilson EO. Pheidole in the New World: a dominant, hyperdiverse ant genus. Harvard University Press, 2003.

Witte V & Maschwitz U. Mushroom harvesting ants in the tropical rain forest. Naturwissenschaften, v. 95, n. 11, p. 1049-1054, 2008. DOI: https://doi.org/10.1007/s00114-008-0421-9

Downloads

Publicado

2022-11-22

Como Citar

Costa, A. L., Furlan-Lopes, C., Bertazzo-Silva, F. A., Klotz-Neves, A. L., Ferraz, K. R., Köhler, A., & Putzke, J. (2022). Mycophagy of Attini Ants (Hymenoptera, Formicidae, Myrmicinae) with Agaricales Mushrooms (Basidiomycota, Agaricomycetes) at Riparian Zone in Southern Brazil: Micofagia de Formigas Attini (Hymenoptera, Formicidae, Myrmicinae) com Cogumelos Agaricales (Basidiomycota, Agaricomycetes) em Zonas Ripárias no Sul do Brasil. Brazilian Journal of Animal and Environmental Research, 5(4), 3935–3960. https://doi.org/10.34188/bjaerv5n4-039

Edição

Seção

Artigos originais