Parasitism of Atta sexdens Forel, 1908 (Hymenoptera: Formicidae) by phorids (Diptera: Phoridae) in Londrina-PR
DOI:
https://doi.org/10.5433/1679-0359.2023v44n5p1603Keywords:
Apocephalus, Biological Control, Eibesfeldtphora, Leaf-cutting ants, Myrmosicarius.Abstract
Leaf-cutting ants belonging to the genus Atta are considered fundamental ecosystem engineers while also posing a threat to production systems due to their extensive defoliation behavior on several plant species. Several flies of the family Phoridae are parasitoids of social insects and engage in the biological control of leaf-cutting ants. This study aimed to assess the prevalence and diversity of parasitoids affecting Atta sexdens, a leaf-cutting ant species, in Londrina, state of Paraná, Brazil. Additionally, the study sought to record parasitism rates and the behavioral and biological traits of the species. Between June 2019 and May 2020, we conducted collections of worker ants and their associated phorid flies at previously selected nests located on the campus of the State University of Londrina and within the native forest of the Botanical Garden of Londrina. The collected phorid flies were preserved in 70% alcohol for subsequent species identification, while the leaf-cutting ants were brought to the laboratory to assess parasitism, following established protocols in the literature. Collected ants were frequently inspected and dead individuals were placed individually in plastic tubes for further analysis. A total of 216 adult phorid flies were captured in both environments, with the following parasitoid species identified: Apocephalus attophilus, Eibesfeldtphora declinata, Eibesfeldtphora elongata, Eibesfeldtphora tonhascai, and Myrmosicarius grandicornis. Among these, Myrmosicarius grandicornis predominated when employing the 'APC' adult parasitoid survey method. Only 1.28% of the collected leaf-cutting ants were parasitized, with A. attophilus emerging as the most abundant species with a relatively short developmental cycle. Parasitism rates remained below 2% throughout the year, with the highest rate observed in September (1.81%). The expansion of the geographic distribution of these flies to Paraná contributes relevant information about the biological and behavioral characteristics of some parasitoid species and their influence on nest activities. This underscores their potential as agents of biological control for managing A. sexdens in integrated management programs.
Downloads
References
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(6), 711-728. doi: 10.1127/0941-2948/2013/0507 DOI: https://doi.org/10.1127/0941-2948/2013/0507
Antwiki (2021). Atta sexdens rubropilosa. https://www.antwiki.org/wiki/Atta_sexdens_rubropilosa
Araújo Galvão, A. R. de, Bailez, O., Viana-Bailez, A. M., Abib, P. H., Pimentel, F. A., & Pereira, T. P. L. (2019). Parasitism by phorids on leaf cutter ants Atta sexdens (Linnaeus, 1758) (Hymenoptera: Formicidae) in natural and agricultural environments. Zoological Science, 36(5), 357-364. doi: 10.2108/zs180190 DOI: https://doi.org/10.2108/zs180190
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(1), 61-67. doi: 10.1093/ee/nvy166 DOI: https://doi.org/10.1093/ee/nvy166
Bedoya Cochet, R., Ortega León, Á., & Ortiz-Reyes, A. (2017). Patrones comportamentales de fóridos (Diptera: Phoridae) parasitóides de Atta colombica (Hymenoptera: Formicidae). Revista de Biología Tropical, 65(2), 461-473. doi: 10.15517/rbt.v65i2.24746 DOI: https://doi.org/10.15517/rbt.v65i2.24746
Bhering, S. B., Santos, H. G. dos, Manzatto, C. V., Bognola, I. A., Fasolo, P. J., Carvalho, A. P. de, Potter, R. O. & Curcio, G. R. (2007). Mapa de solos do estado do Paraná.
Bragança, M. A. L. (2011). Parasitóides de formigas-cortadeiras. In T. M. C. Della Lucia (Ed.), Formigas Cortadeiras: da Bioecologia ao Manejo, (pp. 321-343). Editora UFV, Viçosa,
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(3), 408-411. doi: 10.1590/S1519-566X2006000300018 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(4), 1015-1021. doi: 10.13102/sociobiology.v63i4.1077 DOI: https://doi.org/10.13102/sociobiology.v63i4.1077
Bragança, M. A. L., Della Lucia, T., & Tonhasca, A., Jr. (2003). First record of phorid parasitoids (Diptera: Phoridae) of the leaf-cutting ant Atta bisphaerica Forel (Hymenoptera: Formicidae). Neotropical Entomology, 32(1), 169-171. doi: 10.1590/S1519-566X2003000100028 DOI: https://doi.org/10.1590/S1519-566X2003000100028
Bragança, M. A. L., Souza, L. M. D., Nogueira, C. A., & Della Lucia, T. M. C. (2008). Parasitismo por Neodohrniphora spp. Malloch (Diptera, Phoridae) em operárias de Atta sexdens rubropilosa Forel (Hymenoptera, Formicidae). Revista brasileira de Entomologia, 52(2), 300-302. doi: 10.1590/S0085-56262008000200011 DOI: https://doi.org/10.1590/S0085-56262008000200011
Brown, B. V. (1992). Generic revision of Phoridae of the Nearctic Region and phylogenetic classification of Phoridae, Sciadoceridae, and Ironomyiidae (Diptera: Phoridea). The Memoirs of the Entomological Society of Canada, 124(S164), 3-144. doi: 10.4039/entm124164fv DOI: https://doi.org/10.4039/entm124164fv
Brown, B. V. (1997). Revision of the Apocephalus attophilus-group of ant-decapitating flies (Diptera: Phoridae). Revisión del grupo attophilus del género Apocephalus de moscas decapitadoras de hormigas (Diptera: Phoridae). Contributions in Science, 468, 1-60. doi: 10.5962/p.208097 DOI: https://doi.org/10.5962/p.208097
Brown, B. V. (2000). Revision of the Apocephalus miricauda-group of ant-parasitizing flies (Diptera: Phoridae). DOI: https://doi.org/10.5962/p.241289
Brown, B. V. (2001). Taxonomic revision of Neodohrniphora, subgenus Eibesfeldtphora (Diptera: Phoridae). Insect Systematics & Evolution, 32(4), 393-409. doi: 10.1163/187631201X00272 DOI: https://doi.org/10.1163/187631201X00272
Brown, B. V., Disney, R. H., Elizalde, L., & Folgarait, P. J. (2010). New species and new records of Apocephalus Coquillett (Diptera: Phoridae) that parasitize ants (Hymenoptera: Formicidae) in South America.
Bueno, O. C., Campos, A. E. D. C., & Morini, M. D. C. (2017). Formigas em ambientes urbanos no Brasil. Canal, 6.
Disney, R. H. L., Elizalde, L., & Folgarait, P. J. (2006). New species and revision of Myrmosicarius (Diptera: Phoridae) that parasitize leaf-cutter ants (Hymenoptera: Formicidae). Sociobiology, 47(3), 771-810.
Disney, R. H. L., Elizalde, L., & Folgarait, P. J. (2009). New species and new records of scuttle flies (Diptera: Phoridae) that parasitize leaf-cutter and army ants (Hymenoptera: Formicidae). Sociobiology, 54(2), 601.
Elizalde, L., & Folgarait, P. J. (2011). Biological attributes of Argentinian phorid parasitoids (Insecta: Diptera: Phoridae) of leaf-cutting ants, Acromyrmex and Atta. Journal of Natural History, 45(43-44), 2701-2723. doi: 10.1080/00222933.2011.602478 DOI: https://doi.org/10.1080/00222933.2011.602478
Erthal, M., Jr., & Tonhasca, A., Jr. (2000). Biology and oviposition behavior of the phorid Apocephalus attophilus and the response of its host, the leaf‐cutting ant Atta laevigata. Entomologia Experimentalis et Applicata, 95(1), 71-75. doi: 10.1046/j.1570-7458.2000.00643.x DOI: https://doi.org/10.1046/j.1570-7458.2000.00643.x
Farder-Gomes, C. F., Oliveira, M. A., Gonçalves, P. L., Gontijo, L. M., Zanuncio, J. C., Bragança, M. A. L., & Pires, E. M. (2017). Reproductive ecology of phorid parasitoids in relation to the head size of leaf-cutting ants Atta sexdens Forel. Bulletin of Entomological Research, 107(4), 487-492. doi: 10.1017/S0007485316001073 DOI: https://doi.org/10.1017/S0007485316001073
Farder-Gomes, C. F., Silva, V. P. da, 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(12), e0208253. doi: 10.1371/journal.pone.0208253 DOI: https://doi.org/10.1371/journal.pone.0208253
Gazal, V., Bailez, O., & Viana-Bailez, A. M. (2009). Mechanism of host recognition in Neodohrniphora elongata (Brown) (Diptera: Phoridae). Animal Behaviour, 78(5), 1177-1182. doi: 10.1016/j.anbehav.2009.07.036 DOI: https://doi.org/10.1016/j.anbehav.2009.07.036
Guillade, A. C., & Folgarait, P. J. (2011). Life-history traits and parasitism rates of four phorid species (Diptera: Phoridae), parasitoids of Atta vollenweideri (Hymenoptera: Formicidae) in Argentina. Journal of Economic Entomology, 104(1), 32-40. doi: 10.1603/EC10173 DOI: https://doi.org/10.1603/EC10173
Guillade, A. C., & Folgarait, P. J. (2014). Natural enemies of Atta vollenweideri (Hymenoptera: Formicidae) leaf-cutter ants negatively affected by synthetic pesticides, chlorpyrifos and fipronil. Journal of Economic Entomology, 107(1), 105-114. doi: 10.1603/EC12498 DOI: https://doi.org/10.1603/EC12498
Hölldobler, B., & Wilson, E. O. (2009). The superorganism: the beauty, elegance, and strangeness of insect societies. WW Norton & Company.
Landis, D. A., Wratten, S. D., & Gurr, G. M. (2000). Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology, 45(1), 175-201. doi: 10.1146/annurev.ento. 45.1.175 DOI: https://doi.org/10.1146/annurev.ento.45.1.175
Martins, H. C. (2015). Bioecologia de três espécies de forídeos parasitóides da saúva Atta bisphaerica. Dissertação de mestrado, Universidade Federal de Viçosa, UFV. Viçosa, MG, Brasil.
Medina, P., Morales, J. J., Budia, F., Adan, A., Del Estal, P., & Vinuela, E. (2007). Compatibility of endoparasitoid Hyposoter didymator (Hymenoptera: Ichneumonidae) protected stages with five selected insecticides. Journal of Economic Entomology, 100(6), 1789-1796. doi: 10.1093/jee/100.6.1789 DOI: https://doi.org/10.1093/jee/100.6.1789
Pesquero, M. A., Bessa, L. A., Silva, H. C. M., Carmo Silva, L. do, & Arruda, F. V. (2010). Influência ambiental na taxa de parasitismo (Diptera: Phoridae) de Atta laevigata e Atta sexdens (Hymenoptera: Formicidae). Revista de Biologia Neotropical/Journal of Neotropical Biology, 7(2), 45-48. doi: 10.5216/rbn.v7i2.15459
Pimentel, F. A. (2017). Forídeos parasitóides de Atta laevigata (Smith, 1958) (Hymenoptera: Formicidae), em Mata Atlântica: ocorrência, taxa de parasitismo e tamanho de hospedeiro. Dissertação de mestrado, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brasil.
Silva, V. S. G., Bailez, O. E., Viana-Bailez, A. M., & Tonhasca, A., Jr. (2007). Effect of the size of workers of Atta sexdens rubropilosa (Forel) on the attack behavior of Neodohrniphora spp. (Diptera: Phoridae). Sociobiology, 50(1), 1-10.
Silva, V. S. G., Bailez, O., Viana-Bailez, A. M., Tonhasca, A., & Della Lucia, T. 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(2), 203-206. doi: 10.1017/S0007485307005548 DOI: https://doi.org/10.1017/S0007485307005548
Souza, L. R. R. (2013). Influência do tamanho das operárias e da sazonalidade no parasitismo das saúvas Atta sexdens e Atta laevigata (Hymenoptera: Formicidae) por moscas da família Phoridae. Dissertação de mestrado, Universidade Federal do Tocontins, UFT, Porto Nacional, TO, Brasil.
Swanson, A. C., Schwendenmann, L., Allen, M. F., Aronson, E. L., Artavia‐León, A., Dierick, D., Fernandez-Bou, A. S., Harmon, T. C., Murillo-Cruz, C., Oberbauer,S. F., Pinto-Tomás, A. A., Rundel, P. W. & Zelikova, T. J. (2019). Welcome to the Atta world: A framework for understanding the effects of leaf‐cutter ants on ecosystem functions. Functional Ecology, 33(8), 1386-1399. doi: 10.1111/1365-2435.13319 DOI: https://doi.org/10.1111/1365-2435.13319
Tonhasca, A., Jr., 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(2), 154-158. doi: 10.1007/PL00001759 DOI: https://doi.org/10.1007/PL00001759
Uribe, S., Brown, B. V., Braganca, M. A., Queiroz, J. M., & Nogueira, C. A. (2014). New species of Eibesfeldtphora Disney (Diptera: Phoridae) and a new key to the genus. Zootaxa, 3814(3), 443-450. doi.org/10.11646/zootaxa.3814.3.11 DOI: https://doi.org/10.11646/zootaxa.3814.3.11
Viana-Bailez, A. M., & Endringer, F. B. (2016). Plasticidade do comportamento de forrageamento em formigas cortadeiras. Oecologia Australis, 20(3), 11-19. doi: 10.4257/oeco.2016.2003.02 DOI: https://doi.org/10.4257/oeco.2016.2003.02
Wartchow, F. (2018). Breve história da sistemática de Agaricaceae (Fungi) e distribuição no Brasil. Pesquisa e Ensino em Ciências Exatas e da Natureza, 2(2), 130-147. doi: 10.29215/pecen.v2i2.1067 DOI: https://doi.org/10.29215/pecen.v2i2.1067
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Semina: Ciências Agrárias
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Semina: Ciências Agrárias adopts the CC-BY-NC license for its publications, the copyright being held by the author, in cases of republication we recommend that authors indicate first publication in this journal.
This license allows you to copy and redistribute the material in any medium or format, remix, transform and develop the material, as long as it is not for commercial purposes. And due credit must be given to the creator.
The opinions expressed by the authors of the articles are their sole responsibility.
The magazine reserves the right to make normative, orthographic and grammatical changes to the originals in order to maintain the cultured standard of the language and the credibility of the vehicle. However, it will respect the writing style of the authors. Changes, corrections or suggestions of a conceptual nature will be sent to the authors when necessary.