First Record of Parasitoidism by Phoridae Flies in Atta opaciceps Borgmeier (Hymenoptera: Formicidae), a Leafcutter Ant from the Northeast Region of Brazil

Authors

  • Luis Carlos Ferreira do Nascimento Department of Ecology, Federal University of Sergipe – UFS, Campus São Cristóvão, Sergipe, Brazil
  • Thalles Platiny L. Pereira Harvard University, Museum of Comparative Zoology, 26 Oxford Street, Cambridge, MA, USA https://orcid.org/0000-0003-2075-3643
  • Marcos Antonio Lima Bragança Biological Sciences Course, Federal University of Tocantins – UFT, Porto Nacional, Tocantins, Brazil https://orcid.org/0000-0001-5748-4737
  • Leandro Sousa-Souto Department of Ecology, Federal University of Sergipe – UFS, Campus São Cristóvão, Sergipe, Brazil https://orcid.org/0000-0001-6981-5628

DOI:

https://doi.org/10.13102/sociobiology.v72i3.11408

Keywords:

Natural enemies, biological control, parasitism rate, Neotropical Region

Abstract

Leafcutter ants of the genus Atta Fabricius, 1804 (Hymenoptera: Formicidae) are important actors in natural environments, as they are part of crucial ecological processes; however, they are also considered important pests in agroecosystems. Numerous species of flies from the Phoridae family have been recorded as parasitoids of several species of leafcutter ants, with details of their biology, life cycle, and forms of attack behavior. For the leafcutter Atta opaciceps Borgmeier, 1939, however, to date, there is no record of associated phorids or even records made in the state of Sergipe on the occurrence of parasitoid phorids. This study is the first to report the occurrence of phorids associated with A. opaciceps and the observed parasitoidism rates. Workers collected in the field were kept in the laboratory for parasitoid emergence. The parasitoidism rate was 8.4%, with the majority of workers being parasitized by Myrmosicarius grandicornis Borgmeier, 1928 (n = 267; 99%). There were two other records: one parasitized by Eibesfeldtphora declinata (Borgmeier, 1925) and another worker hosting Apocephalus setitarsus Brown, 1997. This study expands the knowledge about phorids associated with Atta in Brazil, including A. opaciceps on the list of natural hosts, the state of Sergipe in its distribution area, and information on parasitoidism rates.

Downloads

Download data is not yet available.

References

Almeida, J.C., Hoshino, A.T., Pereira, T.P.L. & Pasini, A. (2023) Parasitism of Atta sexdens Forel, 1908 (Hymenoptera:Formicidae) by phorids (Diptera: Phoridae) in Londrina-PR. Semina: Ciências Agrárias, 44: 1603-1620. DOI: https://doi.org/10.5433/1679-0359.2023v44n5p1603

Almeida, J.C.D., Hoshino, A.T., Menezes Junior, A.D.O., Fazam, J.C., Pereira, T.P.L. & Pasini, A. (2021) Parasitism and behavioral responses of Acromyrmex coronatus (Fabricius, 1804) and Acromyrmex crassispinus (Forel, 1909) (Hymenoptera: Formicidae) to Myrmosicarius catharinensis Borgmeier, 1928 (Diptera: Phoridae) in Londrina, PR. Semina: Ciências Agrárias, 42: 2669-2684. DOI: https://doi.org/10.5433/1679-0359.2021v42n5p2669

Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.D.M. & Sparovek, G. (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22: 711-728. DOI: https://doi.org/10.1127/0941-2948/2013/0507

Araujo, S., Seibert, J., Ruani, A., Cruz, R., Cruz, A., Pereira, A., Zandonai, D., Forim, M., Silva, M., Bueno, O., & Fernandes, J. (2022) The symbiotic fungus Leucoagaricus gongylophorus (Möller) Singer (Agaricales, Agaricaceae) as a target organism to control leaf-cutting ants. Insects, 13: 359. DOI: https://doi.org/10.3390/insects13040359

Arruda, F.V., Teresa, F.B., Martins, H.C., Pesquero, M.A. & Bragança, M.A.L.(2019) Seasonal and site differences in phorid parasitoidism rates of leaf-cutting ants. Environmental Entomology, 48: 61-67. DOI: https://doi.org/10.1093/ee/nvy166

Barber, S. & Jennison, C. (1999) Symmetric tests and confidence intervals for survival probabilities and quantiles of censored survival data. Biometrics, 55: 430-436. DOI: https://doi.org/10.1111/j.0006-341X.1999.00430.x

Barrera, C.A., Sosa‐Calvo, J., Schultz, T.R., Rabeling, C. & Bacci Jr, M. (2022) Phylogenomic reconstruction reveals new insights into the evolution and biogeography of Atta leaf‐cutting ants (Hymenoptera: Formicidae). Systematic Entomology, 47: 13-35. DOI: https://doi.org/10.1111/syen.12513

Bragança, M.A.L. (2011). Parasitoides de formigas-cortadeiras. In: T.M.C. Della Lucia (Ed.), Formigas cortadeiras: da biologia ao manejo (pp. 321-43). Viçosa: Editora UFV.

Bragança, M.A.L, Tonhasca, A.J. & Della Lucia, T.M.C. (1998) Reduction in the foraging activity of the leaf-cutting ant Atta sexdens caused by the phorid Neodohrniphora sp. Entomologia Experimentalis et Applicata, 89: 305–311. DOI: https://doi.org/10.1046/j.1570-7458.1998.00413.x

Bragança, M.A.L., Della Lucia, T. & Tonhasca, A.J. (2003) First record of phorid parasitoids (Diptera: Phoridae) of the leaf-cutting ant Atta bisphaerica Forel (Hymenoptera: Formicidae). Neotropical Entomology, 32: 169-171. DOI: https://doi.org/10.1590/S1519-566X2003000100028

Bragança, M.A.L. & Medeiros, Z. (2006) Ocorrência e características biológicas de forídeos parasitóides (Diptera: Phoridae) da saúva Atta laevigata (Smith) (Hymenoptera: Formicidae) em Porto Nacional, TO. Neotropical Entomology, 35: 408-411. DOI: https://doi.org/10.1590/S1519-566X2006000300018

Bragança, M.A.L, Arruda, F.V., Souza, L.R.R., Martins, H.C. & Della Lucia, T.M.C. (2016) Phorid flies parasitizing leaf-cutting ants: their occurrence, parasitism rates, biology and the first account of multiparasitism. Sociobiology, 63: 1015–1021. DOI: https://doi.org/10.13102/sociobiology.v63i4.1077

Bragança, M.A.L., Martins, H.C., Oliveira, R.J. & Della Lucia, T.M.C. (2021) Parasitism of the leaf-cutting ant Atta bisphaerica by phorid flies: biology and seasonal and inter-colonial parasitism rates. Entomologia Experimentalis et Applicata, 169: 338–349. DOI: https://doi.org/10.1111/eea.13020

Bragança, M.A.L., Souza, M.L.O., Oliveira, R.J. & Samuels, R.I. (2023) Phorid fly parasitism rates vary between individual colonies of the leaf-cutting ant Atta laevigata. Agricultural and Forest Entomology, 25: 558-570. DOI: https://doi.org/10.1111/afe.12575

Brown, B.V. (1997) Revision of the Apocephalus attophilus-group of ant-decapitating flies. (Diptera: Phoridae). Contributions in Science, 468: 1-60. DOI: https://doi.org/10.5962/p.208097

Brown, B.V. (2001) Taxonomic revision of Neodohrniphora, subgenus Eibesfeldtphora (Diptera: Phoridae). Insect Systematics and Evolution 32: 393–409. DOI: https://doi.org/10.1163/187631201X00272

Brown, B.V., Disney, R.H.L., Elizalde, L. & Folgarait, P.J. (2010) New species and new records of Apocephalus Coquillett (Diptera: Phoridae) that parasitize ants (Hymenoptera: Formicidae) in America. Sociobiology, 55: 165–190.

Cherrett, J.M. (1986) The biology, pest status and control of leaf-cutting ants. Agricultural Zoology Reviews, 1: 1-37.

Corrêa, M.M., Bieber, A.G., Wirth, R. & Leal, I.R. (2005) Occurrence of Atta cephalotes (L.) (Hymenoptera: Formicidae) in Alagoas, Northeastern Brazil. Neotropical Entomology, 34: 695-698. DOI: https://doi.org/10.1590/S1519-566X2005000400023

Crawley, M.J. (2013) The R book. 2nd edition. England: Ed John Wiley & Sons Ltd., 1060 p.

Delabie, J.H.C., Nascimento, I.C., Fonseca, E., Sgrillo, R.B., Soares, P.A.O., Casimiro, A.B. & Furst, M. (1997) Biogeografia das formigas cortadeiras (Hymenoptera, Formicidae, Myrmicinae, Attini) de importância econômica no leste da Bahia e nas regiões periféricas dos estados vizinhos. Agrotrópica, 9: 49–58.

Della Lucia, T.M.C. (2011) Formigas cortadeiras: da bioecologia ao manejo. Viçosa: Ed. UFV, 419 p.

Disney, R.H.L, Elizalde, L., Folgarait, P.J. (2006) New species and revision of Myrmosicarius (Diptera: Phoridae) that parasitize leafcutter ants (Hymenoptera: Formicidae). Sociobiology, 47: 771–809.

Disney, R.H.L., Bragança, M.A.L., Silva, L.A., Oliveira, M.A., Fader-Gomes, C.F., Souza, D.J. & Silva, J.C.R. (2016) New records, including new species, of scuttle flies (Diptera: Phoridae) associated with leaf-cutting ants (Hymenoptera: Formicidae) in Brazil. Studia Dipterologica, 23: 183–216.

Elizalde, L. & Folgarait, P.J. (2010) Host diversity and environmental variables as determinants of the species richness of the parasitoids of leaf-cutting ants. Journal of Biogeography, 37: 2305–2316. DOI: https://doi.org/10.1111/j.1365-2699.2010.02361.x

Elizalde, L. & Folgarait, P.J. (2012) Behavioral strategies of phorid parasitoids and responses of their hosts, the leaf-cutting ants. Journal of Insect Science, 12: 135. DOI: https://doi.org/10.1673/031.012.13501

Elizalde, L. & Superina, M. (2019) Complementary effects of different predators of leaf-cutting ants: implications for biological control. Biological Control, 128: 111-117. DOI: https://doi.org/10.1016/j.biocontrol.2018.09.015

Erthal, M. Jr. & Tonhasca, A.J. (2000) Biology and oviposition behavior of the phorid Apocephalus attophilus and the response of its host, the leafcutting ant Atta laevigata. Entomologia Experimentalis et Applicata, 95: 71-75. DOI: https://doi.org/10.1046/j.1570-7458.2000.00643.x

Farder-Gomes, C.F., Silva, V.P., Pereira, T.P.L., Serrão, J.E., Pires, E.M. & Oliveira, M.A. (2018) Parasitism, sexual dimorphism and effect of host size on Apocephalus attophilus offspring, a parasitoid of the leaf-cutting ant Atta bisphaerica. PLoS ONE, 13: 208253. DOI: https://doi.org/10.1371/journal.pone.0208253

Farji-Brener, A.G. & Werenkraut, V. (2015) A meta-analysis of leaf-cutting ant nest effects on soil fertility and plant performance. Ecological Entomology, 40: 150-158. DOI: https://doi.org/10.1111/een.12169

Feener, D.H. & Brown, B.V. (1997) Diptera as parasitoids. Annual Review of Entomology, 42: 73-97. DOI: https://doi.org/10.1146/annurev.ento.42.1.73

Feener, D.H. & Moss, K.A.G. (1990) Defense against parasites by hitchhikers in leaf-cutting ants: a quantitative assessment. Behavioral Ecology and Sociobiology, 26: 17-29. DOI: https://doi.org/10.1007/BF00174021

Fowler, H.G., Pagani, M.I., Silva, O.A., Forti, L.C., Pereira da Silva, V. & Vasconcelos, H.L. (1989) A pest is a pest is a pest? The dilemma of Neotropical leaf‐cutting ants: keystone taxa of natural ecosystems. Environmental Management, 13: 671-675. DOI: https://doi.org/10.1007/BF01868306

Galvão, A.R.A., Bailez, O., Viana-Bailez, A.M., Abib, P.N., Pimentel, F.A. & Pereira, T.P. (2019) Parasitism by phorids on leaf cutter ants Atta sexdens (Linnaeus, 1758) (Hymenoptera: Formicidae) in natural and agricultural environments. Zoological Science, 36: 357–364. DOI: https://doi.org/10.2108/zs180190

INMET - Instituto Nacional de Meteorologia. (2024). Brasília, DF, Brasil. http://www.inmet.gov.br/portal/index.php?r=tempo2/mapasPrecipitacao (accessed date: 5 June 2024).

Leal, I.R., Wirth, R. & Tabarelli, M. (2014) The multiple impacts of leaf‐cutting ants and their novel ecological role in human‐modified neotropical forests. Biotropica, 46: 516-528. DOI: https://doi.org/10.1111/btp.12126

Mota Filho, T.M., Camargo, R.S., Zanuncio, J.C., Stefanelli, L.E., de Matos, C.A. & Forti, L.C. (2021a) Contamination routes and mortality of the leaf‐cutting ant Atta sexdens (Hymenoptera: Formicidae) by the insecticides fipronil and sulfluramid through social interactions. Pest Management Science, 77: 4411-4417. DOI: https://doi.org/10.1002/ps.6475

Mota Filho, T.M.M., Stefanelli, L.E.P., Camargo, R.D.S., Matos, C.A.O.D. & Forti, L.C. (2021b) Biological control in leaf-cutting ants, Atta sexdens (Hymenoptera: Formicidae), using pathogenic fungi. Revista Árvore, 45: e4516. DOI: https://doi.org/10.1590/1806-908820210000016

Nascimento, D.L., Chiapini, M., Vidal-Torrado, P., Phillips, J.D., Ladeira, F.S.B., Machado, D.F.T., Camargo, R.S & Valezio, E.V. (2024) The underestimated role of leaf-cutting ants in soil and geomorphological development in neotropical America. Earth-Science Reviews, 248: 104650. DOI: https://doi.org/10.1016/j.earscirev.2023.104650

Pereira, R.C., Bailez, O., Vieira‐Júnior, J.O.L., Silva, G.A. & Viana‐Bailez, A.M., (2022a) Seasonality of parasitism of phorid flies (Diptera: Phoridae) in the leafcutter ant Atta sexdens Linnaeus (Hymenoptera: Formicidae) in an Atlantic Forest area. Agricultural and Forest Entomology, 24: 564-574. DOI: https://doi.org/10.1111/afe.12521

Pereira, R.C., Bailez, O., Vieira-Júnior, J.O., Silva, G.A., Arêdes, A. & Viana-Bailez, A.M. (2022b) Host Size Preference of the Leafcutter Ant Parasitoid Eibesfeldtphora tonhascai (Diptera: Phoridae). Neotropical Entomology, 51: 593-599. DOI: https://doi.org/10.1007/s13744-022-00962-x

Pimentel, F.A., Bailez, O., Pereira, R.C. & Viana-Bailez, A.M. (2022) Phorid parasitoids of the leaf-cutting ant Atta laevigata in the Atlantic Forest: occurrence, parasitism rate, and host size. Entomologia Experimentalis et Applicata, 170: 495-504. DOI: https://doi.org/10.1111/eea.13170

Poderoso, J.C.M., Ribeiro, G.T., Gonçalves, G.B., Mendonça, P.D., Polanczyk, R.A., Zanetti, R., Serrão, J.E. & Zanuncio, J.C. (2009) Nest and foraging characteristics of Acromyrmex landolti balzani (Hymenoptera: Formicidae) in Northeast Brazil. Sociobiology, 54: 361-372.

R Core Team (2023) A: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Santos, R.S. & Sousa-Souto, L. (2023) Nest refuse of Acromyrmex balzani (Hymenoptera:Formicidae) increases the plant vigor in Turnera subulata (Turneraceae). Brazilian Journal of Biology, 83: e244732. DOI: https://doi.org/10.1590/1519-6984.244732

Shorthouse, D.P. (2010) SimpleMappr, an online tool to produce publication-quality point maps. https://www.simplemappr.net. (accessed date: 24 April 2024).

Silva, V.S.G., Bailez, O., Viana-Bailez, A.M., Tonhasca, A.J. & Della Lucia, T.M.C. (2008). Survey of Neodohrniphora spp. (Diptera: Phoridae) at colonies of Atta sexdens rubropilosa (Forel) and specificity of attack behaviour in relation to their hosts. Bulletin of Entomological Research, 98: 203-206. DOI: https://doi.org/10.1017/S0007485307005548

Siqueira, F.F.S., Ribeiro-Neto, J.D., Tabarelli, M., Andersen, A.N., Wirth, R., Leal, I.R. (2017) Leaf-cutting ant populations profit from human disturbances in tropical dry forest in Brazil. Journal of Tropical Ecology, 33: 337-344. DOI: https://doi.org/10.1017/S0266467417000311

Sousa-Souto, L., Santos, D.C.J., Ambrogi, B.G., Santos, M.J.C., Guerra, M.B.B. & Pereira-Filho, E.R. (2012) Increased CO2 emission and organic matter decomposition by leaf-cutting ant nests in a coastal environment. Soil Biology and Biochemistry, 44: 21–25. DOI: https://doi.org/10.1016/j.soilbio.2011.09.008

Souza, M.L.O., Oliveira, R.J., Souza, D.J., Samuels, R.I. & Bragança, M.A. (2021) Differential parasitism by four species of phorid flies when attacking three worker castes of the leaf-cutting ant Atta laevigata (Smith, 1858). Plos One, 16: e0250973. DOI: https://doi.org/10.1371/journal.pone.0250973

Tonhasca, A.J. (1996) Interactions between a parasitic fly, Neodohrniphora declinata (Diptera: Phoridae), and its host, the leafcutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae). Ecotropica, 2: 157-164.

Tonhasca, A.J. & Bragança, M.A.L. (2000) Effect of leaf toughness on the susceptibility of the leaf-cutting ant Atta sexdens to attacks of a phorid parasitoid. Insectes Sociaux, 47: 220-222. DOI: https://doi.org/10.1007/PL00001706

Tonhasca, A.J., Bragança, M.A.L. & Erthal, M.Jr. (2001) Parasitism and biology of Myrmosicarius grandicornis (Diptera, Phoridae) in relationship to its host, the leaf-cutting ant Atta sexdens (Hymenoptera, Formicidae). Insectes Sociaux, 48: 154-158. DOI: https://doi.org/10.1007/PL00001759

Uribe, S., Brown, B.V., Bragança, M.A.L., Queiroz, J.M. & Nogueira, C.A. (2014). New species of Eibesfeldtphora Disney (Diptera: Phoridae) and a new key to the genus. Zootaxa, 3814: 443–450. DOI: https://doi.org/10.11646/zootaxa.3814.3.11

Downloads

Published

2025-07-14

How to Cite

Nascimento, L. C. F. do, Pereira, T. P. L., Bragança, M. A. L., & Sousa-Souto, L. (2025). First Record of Parasitoidism by Phoridae Flies in Atta opaciceps Borgmeier (Hymenoptera: Formicidae), a Leafcutter Ant from the Northeast Region of Brazil. Sociobiology, 72(3), e11408. https://doi.org/10.13102/sociobiology.v72i3.11408

Issue

Section

Research Article - Ants

Most read articles by the same author(s)