Parasitism and behavioral responses of Acromyrmex coronatus (Fabricius, 1804) and Acromyrmex crassispinus (Forel, 1909) (Hymenoptera: Formicidae) to Myrmosicarius catharinensis
DOI:
https://doi.org/10.5433/1679-0359.2021v42n5p2669Keywords:
Behavioral change, Leaf-cutting ant, Natural enemy, Parasitoid.Abstract
Leaf-cutting ants of the genus Acromyrmex cause serious damage to cultivated forest areas. Some flies of the family Phoridae are known to parasitize them, and the result of this interaction can provide a promising basis for the management of these ants. This study was developed to record the parasitism and behavioral responses of Acromyrmex spp. leaf-cutting ants to parasitoid phorids in the municipality of Londrina-PR, Brazil. Visual examinations and collections of leaf-cutting ants and associated phorids were carried out between October/2019 and April/2020 in selected anthills and their trails, located on the campus of the State University of Londrina (UEL) and at the Botanical Garden of Londrina. The collected insects were preserved in 70% alcohol, for later identification of the species. The behavioral response of the ants to the parasitoids was recorded individually and collectively, following protocols cited in the literature. The frequencies of the different response behaviors exhibited by the attacked ants were compared using analysis of variance. The leaf-cutting ant species Acromyrmex coronatus and Acromyrmex crassispinus were found at the two evaluated sites. Myrmosicarius catharinensis was the only species of parasitoid phorid found, which attacked both ant species. Although the occurrence of M. catharinensis has been reported in other Brazilian states and its association with A. crassispinus recorded in Buenos Aires, Argentina, this is the first report of the occurrence of the phorid in the state of Paraná with a new association for the species A. coronatus. Under foraging action by the parasitoid, 63.5% of the ants exhibited only one behavioral response, while 36.5% showed two. Accelerated walking, attempting to "bite" the parasitoid, and adopting a 'C' posture were the most frequent behavioral responses to avoid parasitism. Ants crowding together around a worker and the presence of "hitchhiker" workers on the transported leaf fragments were the observed changes in collective behavior, the latter being the most frequent. These changes occurred in all observed ant nests and, in two of them, the constancy of alteration in collective behavior was 53%. These results demonstrate the interference caused in nests of Acromyrmex spp. by the occurrence of M. catharinensis, a potential control agent for this pest.Metrics
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References
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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
Baccaro, F. B., Feitosa, R. M., Fernández, F., Fernandes, I. O., Izzo, T. J., Souza, J. D., & Solar, R. (2015). Guia para os gêneros de formigas do Brasil. Manaus: Editora INPA.
Bailez, O. (2016) Strategies and tactics in phorid-ant interactions. Oecologia Australis, 20(3), 322-331. doi: 10.4257/oeco.2016.2003.01
Barrera, C. A., Becker, E. L., Elizalde, L., & Queiroz, J. M. (2017). Parasitoid phorid flies of leaf cutting ants are negatively affected by loss of forest cover. Entomologia Experimentalis et Applicata, 164(1), 66-77. doi: 10.1111/eea.12593
Belchior, D. C. V., Souza Saraiva, A. de, López, A. M. C., & Scheidt, G. N. (2017). Impactos de agrotóxicos sobre o meio ambiente e a saúde humana. Cadernos de Ciência & Tecnologia, 34(1), 135-151. doi: 10. 35977/0104-1096.cct2017.v34.26296
Bollazzi, M., Kronenbitter, J., & Roces, F. (2008). Soil temperature, digging behaviour, and the adaptive value of nest depth in South American species of Acromyrmex leaf-cutting ants. Oecologia, 158(1), 165-175. doi: 10.1007/s00442-008-1113-z
Bragança, M. A., Tonhasca, A., Jr., & Della Lucia, T. (2009). Características biológicas e comportamentais de Neodohrniphora elongata Brown (Diptera, Phoridae), um parasitóide da saúva Atta sexdens rubropilosa Forel (Hymenoptera, Formicidae). Revista Brasileira de Entomologia, 53(4), 600-606. doi: 10.1590/S0085-56262009000400009
Brener, A. G. F., & Ruggiero, A. (1994). Leaf-cutting ants (Atta and Acromyrmex) inhabiting Argentina: patterns in species richness and geographical range sizes. Journal of Biogeography, 21(4), 391-399. doi: 10.2307/2845757
Britto, J. S. de, Forti, L. C., Oliveira, M. A. de, Zanetti, R., Wilcken, C. F., Zanuncio, J. C., & Silva Camargo, R. da. (2016). Use of alternatives to PFOS, its salts and PFOSF for the control of leaf-cutting ants Atta and Acromyrmex. International Journal of Research in Environmental Studies, 3, 11-92. doi: 10.33500/ijres.2016.3.002
Cantarelli, E. B., Costa, E. C., Pezzutti, R. V., Zanetti, R., & Fleck, M. D. (2019). Damage by Acromyrmex spp. to an Initial Pinus taeda L. Planting. Floresta e Ambiente, 26(4), 1-7. doi: 10.1590/2179-8087.00 6016
De Bekker, C., Will, I., Das, B., & Adams, R. M. (2018). The ants (Hymenoptera: Formicidae) and their parasites: effects of parasitic manipulations and host responses on ant behavioral ecology. Myrmecological News, 28, 1-24. doi: 10.25849/myrmecol.news_028:001
Della Lucia, T. M. C., & Amaral, K. D. (2020). Past and current strategies for the control of leaf-cutting ants in Brazil. In A. Sergio (Ed.), Estay, Forest pest and disease management in Latin America (pp. 31-43). Cham: Springer.
Della Lucia, T. M. C., Gandra, L. C., & Guedes, R. N. (2014). Managing leafcutting ants: peculiarities, trends and challenges. Pest Management Science, 70(1), 14-23. doi: 10.1002/ps.3660
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. Recovered from https://www.researchgate.net/publication/262800244
Duarte, J. L., Vaz, D. B., & Krüger, R. F. (2018). New records of phorid flies (Diptera, Phoridae) from Rio Grande do Sul, with five new records to Brazil. Check List, 14(1), 125-139. doi: 10.15560/14.1.125
e-Flora UEL (2017). Guia de plantas da UEL. Recuperado em https://play.google.com/store/ apps/details? id=com.goodbarber.eflora&hl=pt_BR
Elizalde, L., & de Queiroz, J. M. (2013). Parasitoids of Acromyrmex (Hymenoptera: Formicidae) leaf-cutting ants in continuous and fragmented Atlantic forest. Sociobiology, 60(4), 397-404. doi: 10.13102/ sociobiology.v60i4.397-404
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
Elizalde, L., Folgarait, P. J., & Muscedere, M. (2012). Behavioral strategies of phorid parasitoids and responses of their hosts, the leaf-cutting ants. Journal of Insect Science, 12(135), 1-26. doi: 10.1673/03 1.012.13501
Elizalde, L., Patrock, R. J., Disney, R. H. L., & Folgarait, P. J. (2018). Spatial and temporal variation in host–parasitoid interactions: leafcutter ant hosts and their phorid parasitoids. Ecological Entomology, 43(1), 114-125. doi: 10.1111/een.12477
Elizalde, L., Treanor, D., Pamminger, T., & Hughes, W. O. (2019). Immunity of leaf-cutting ants and its role in host-parasitoid relationships. Journal of Insect Physiology, 116, 49-56. doi: 10.1016/j.jinsphys.2019. 04.008
Feener, D. H., & Brown, B. V. (1993). Oviposition behavior of an ant-parasitizing fly, Neodohrniphora curvinervis (Diptera: Phoridae), and defense behavior by its leaf-cutting ant host Atta cephalotes (Hymenoptera: Formicidae). Journal of Insect Behavior, 6(6), 675-688. doi: 10.1007/BF01201669
Folgarait, P. J. (2013). Leaf-cutter ant parasitoids: current knowledge. Psyche: A Journal of Entomology, 2013(Article ID 539780), 1-10. doi: 10.1155/2013/539780
Fowler, H. G. (1983). Latitudinal gradients and diversity of the leaf-cutting ants (Atta and Acromyrmex) (Hymenoptera: Formicidae). Revista de Biología Tropical, 31(2), 213-216. Recovered from https:// revistas.ucr.ac.cr/index.php/rbt/article/view/24936/25141
Goffre, D., & Folgarait, P. J. (2019). Phorid species from Acromyrmex’s hosts and effect on their survival of two fungi proposed for the control of leafcutter ants. Entomologia Experimentalis et Applicata, 167(11), 939-949. doi: 10.1111/eea.12842
Gonçalves, C. R. (1961). O gênero Acromyrmex no Brasil (Hym. Formicidae). Studia Entomologica, 4(1-4), 113-180.
Grizio-Orita, E. V., Hirata, C. A., Tissiano, G. M., & Marques, P. M. (2020). Levantamento turístico do Jardim Botânico de Londrina (PR). Revista Brasileira de Educação Ambiental (RevBEA), 15(1), 150-159. doi: 10.34024/revbea.2020.v15.9920
Guillade, A. C. (2013). Control biológico de hormigas cortadoras de hoja (FORMICIDAE: ATTINI) mediante parasitoides (DIPTERA: PHORIDAE). Tesis doctoral, Universidad Nacional de Quilmes, Quilmes, Argentina. Obtenido de https://ridaa.unq.edu.ar/handle/20.500.11807/412
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
Guillade, A. C., Goffre, D., & Folgarait, P. J. (2017). New records and new host-parasitoid interactions of phorids (Diptera: Phoridae) parasitizing leafcutter ants (Hymenoptera: Formicidae) in Argentina. Revista de la Sociedad Entomológica Argentina, 76(3-4), 50-54. doi: 10.25085/rsea.763409
Hölldobler, B., & Wilson, E. O. (2009). The superorganism: the beauty, elegance, and strangeness of insect societies. New York: WW Norton & Company.
Indústria Brasileira de Árvores (2020). Desempenho das árvores plantadas. Recuperado de https://iba.org/ datafiles/publicacoes/pdf/iba-relatorioanual2017.pdf
Leal, I. R., Wirth, R., & Tabarelli, M. (2011). Dispersão de sementes por formigas-cortadeiras. Formigas-cortadeiras: da bioecologia ao manejo. Viçosa, MG: Della Lucia TMC, Universidade Federal de Viçosa.
Nascimento, R. A., Nunoo, D. B., Bizkarguenaga, E., Schultes, L., Zabaleta, I., Benskin, J. P.,... & Leonel, J. (2018). Sulfluramid use in Brazilian agriculture: A source of per-and polyfluoroalkyl substances (PFASs) to the environment. Environmental Pollution, 242, 1436-1443. doi: 10.1016/j.envpol.2018.07. 122
Nickele, M. A., Reis, W., Fº., Penteado, S. D. R., de Queiroz, E. C., Schaitza, E. G., & Pie, M. R. (2021). Potential damage by Acromyrmex ant species in pine plantations in southern Brazil. Agricultural and Forest Entomology, 23, 32-40, doi: 10.1111/afe.12400
Nickele, M. A., Reis, W., Fº., Penteado, S., & Queiroz, E. C. de. (2018). Manejo de Acromyrmex (Hymenoptera: Formicidae) em plantios florestais na Região Sul do Brasil. Anais do Encontro Brasileiro de Silvicultura, Ribeirão Preto, SP, Brasil, 4. Recuperado de http://www.alice.cnptia. embrapa .br/alice/handle/doc/1092382
Rando, J. S. S., & Forti, L. C. (2005). Ocorrência de formigas Acromyrmex Mayr, 1865, em alguns municípios do Brasil. Acta Scientiarum. Biological Sciences, 27(2), 129-133. doi: 10.4025/ actascibiolsci.v27i2.1322
Singer, R. (1986). The Agaricales in modern taxonomy. (4a ed.). Koegnistein: Koeltz Scientific Books.
Swanson, A. C., Schwendenmann, L., Allen, M. F., Aronson, E. L., Artavia León, A., Dierick, D.,... Pinto Tomás, A. A. (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: 10.1111/1365-2435.13 319
Toffoli, A. L. de, Mata, K. da, Bisinoti, M. C., & Moreira, A. B. (2015). Development, validation, and application of a method for the GC-MS analysis of fipronil and three of its degradation products in samples of water, soil, and sediment. Journal of Environmental Science and Health, Part B, 50(11), 753-759. doi: 10.1080/03601234.2015.1058091
Vieira, E. H. M., Neto, Mundim, F. M., & Vasconcelos, H. L. (2006). Hitchhiking behaviour in leaf-cutter ants: an experimental evaluation of three hypotheses. Insectes Sociaux, 53(3), 326-332. doi: 10.1007/s0 0040-006-0876-7
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
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
Baccaro, F. B., Feitosa, R. M., Fernández, F., Fernandes, I. O., Izzo, T. J., Souza, J. D., & Solar, R. (2015). Guia para os gêneros de formigas do Brasil. Manaus: Editora INPA.
Bailez, O. (2016) Strategies and tactics in phorid-ant interactions. Oecologia Australis, 20(3), 322-331. doi: 10.4257/oeco.2016.2003.01
Barrera, C. A., Becker, E. L., Elizalde, L., & Queiroz, J. M. (2017). Parasitoid phorid flies of leaf cutting ants are negatively affected by loss of forest cover. Entomologia Experimentalis et Applicata, 164(1), 66-77. doi: 10.1111/eea.12593
Belchior, D. C. V., Souza Saraiva, A. de, López, A. M. C., & Scheidt, G. N. (2017). Impactos de agrotóxicos sobre o meio ambiente e a saúde humana. Cadernos de Ciência & Tecnologia, 34(1), 135-151. doi: 10. 35977/0104-1096.cct2017.v34.26296
Bollazzi, M., Kronenbitter, J., & Roces, F. (2008). Soil temperature, digging behaviour, and the adaptive value of nest depth in South American species of Acromyrmex leaf-cutting ants. Oecologia, 158(1), 165-175. doi: 10.1007/s00442-008-1113-z
Bragança, M. A., Tonhasca, A., Jr., & Della Lucia, T. (2009). Características biológicas e comportamentais de Neodohrniphora elongata Brown (Diptera, Phoridae), um parasitóide da saúva Atta sexdens rubropilosa Forel (Hymenoptera, Formicidae). Revista Brasileira de Entomologia, 53(4), 600-606. doi: 10.1590/S0085-56262009000400009
Brener, A. G. F., & Ruggiero, A. (1994). Leaf-cutting ants (Atta and Acromyrmex) inhabiting Argentina: patterns in species richness and geographical range sizes. Journal of Biogeography, 21(4), 391-399. doi: 10.2307/2845757
Britto, J. S. de, Forti, L. C., Oliveira, M. A. de, Zanetti, R., Wilcken, C. F., Zanuncio, J. C., & Silva Camargo, R. da. (2016). Use of alternatives to PFOS, its salts and PFOSF for the control of leaf-cutting ants Atta and Acromyrmex. International Journal of Research in Environmental Studies, 3, 11-92. doi: 10.33500/ijres.2016.3.002
Cantarelli, E. B., Costa, E. C., Pezzutti, R. V., Zanetti, R., & Fleck, M. D. (2019). Damage by Acromyrmex spp. to an Initial Pinus taeda L. Planting. Floresta e Ambiente, 26(4), 1-7. doi: 10.1590/2179-8087.00 6016
De Bekker, C., Will, I., Das, B., & Adams, R. M. (2018). The ants (Hymenoptera: Formicidae) and their parasites: effects of parasitic manipulations and host responses on ant behavioral ecology. Myrmecological News, 28, 1-24. doi: 10.25849/myrmecol.news_028:001
Della Lucia, T. M. C., & Amaral, K. D. (2020). Past and current strategies for the control of leaf-cutting ants in Brazil. In A. Sergio (Ed.), Estay, Forest pest and disease management in Latin America (pp. 31-43). Cham: Springer.
Della Lucia, T. M. C., Gandra, L. C., & Guedes, R. N. (2014). Managing leafcutting ants: peculiarities, trends and challenges. Pest Management Science, 70(1), 14-23. doi: 10.1002/ps.3660
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. Recovered from https://www.researchgate.net/publication/262800244
Duarte, J. L., Vaz, D. B., & Krüger, R. F. (2018). New records of phorid flies (Diptera, Phoridae) from Rio Grande do Sul, with five new records to Brazil. Check List, 14(1), 125-139. doi: 10.15560/14.1.125
e-Flora UEL (2017). Guia de plantas da UEL. Recuperado em https://play.google.com/store/ apps/details? id=com.goodbarber.eflora&hl=pt_BR
Elizalde, L., & de Queiroz, J. M. (2013). Parasitoids of Acromyrmex (Hymenoptera: Formicidae) leaf-cutting ants in continuous and fragmented Atlantic forest. Sociobiology, 60(4), 397-404. doi: 10.13102/ sociobiology.v60i4.397-404
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
Elizalde, L., Folgarait, P. J., & Muscedere, M. (2012). Behavioral strategies of phorid parasitoids and responses of their hosts, the leaf-cutting ants. Journal of Insect Science, 12(135), 1-26. doi: 10.1673/03 1.012.13501
Elizalde, L., Patrock, R. J., Disney, R. H. L., & Folgarait, P. J. (2018). Spatial and temporal variation in host–parasitoid interactions: leafcutter ant hosts and their phorid parasitoids. Ecological Entomology, 43(1), 114-125. doi: 10.1111/een.12477
Elizalde, L., Treanor, D., Pamminger, T., & Hughes, W. O. (2019). Immunity of leaf-cutting ants and its role in host-parasitoid relationships. Journal of Insect Physiology, 116, 49-56. doi: 10.1016/j.jinsphys.2019. 04.008
Feener, D. H., & Brown, B. V. (1993). Oviposition behavior of an ant-parasitizing fly, Neodohrniphora curvinervis (Diptera: Phoridae), and defense behavior by its leaf-cutting ant host Atta cephalotes (Hymenoptera: Formicidae). Journal of Insect Behavior, 6(6), 675-688. doi: 10.1007/BF01201669
Folgarait, P. J. (2013). Leaf-cutter ant parasitoids: current knowledge. Psyche: A Journal of Entomology, 2013(Article ID 539780), 1-10. doi: 10.1155/2013/539780
Fowler, H. G. (1983). Latitudinal gradients and diversity of the leaf-cutting ants (Atta and Acromyrmex) (Hymenoptera: Formicidae). Revista de Biología Tropical, 31(2), 213-216. Recovered from https:// revistas.ucr.ac.cr/index.php/rbt/article/view/24936/25141
Goffre, D., & Folgarait, P. J. (2019). Phorid species from Acromyrmex’s hosts and effect on their survival of two fungi proposed for the control of leafcutter ants. Entomologia Experimentalis et Applicata, 167(11), 939-949. doi: 10.1111/eea.12842
Gonçalves, C. R. (1961). O gênero Acromyrmex no Brasil (Hym. Formicidae). Studia Entomologica, 4(1-4), 113-180.
Grizio-Orita, E. V., Hirata, C. A., Tissiano, G. M., & Marques, P. M. (2020). Levantamento turístico do Jardim Botânico de Londrina (PR). Revista Brasileira de Educação Ambiental (RevBEA), 15(1), 150-159. doi: 10.34024/revbea.2020.v15.9920
Guillade, A. C. (2013). Control biológico de hormigas cortadoras de hoja (FORMICIDAE: ATTINI) mediante parasitoides (DIPTERA: PHORIDAE). Tesis doctoral, Universidad Nacional de Quilmes, Quilmes, Argentina. Obtenido de https://ridaa.unq.edu.ar/handle/20.500.11807/412
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
Guillade, A. C., Goffre, D., & Folgarait, P. J. (2017). New records and new host-parasitoid interactions of phorids (Diptera: Phoridae) parasitizing leafcutter ants (Hymenoptera: Formicidae) in Argentina. Revista de la Sociedad Entomológica Argentina, 76(3-4), 50-54. doi: 10.25085/rsea.763409
Hölldobler, B., & Wilson, E. O. (2009). The superorganism: the beauty, elegance, and strangeness of insect societies. New York: WW Norton & Company.
Indústria Brasileira de Árvores (2020). Desempenho das árvores plantadas. Recuperado de https://iba.org/ datafiles/publicacoes/pdf/iba-relatorioanual2017.pdf
Leal, I. R., Wirth, R., & Tabarelli, M. (2011). Dispersão de sementes por formigas-cortadeiras. Formigas-cortadeiras: da bioecologia ao manejo. Viçosa, MG: Della Lucia TMC, Universidade Federal de Viçosa.
Nascimento, R. A., Nunoo, D. B., Bizkarguenaga, E., Schultes, L., Zabaleta, I., Benskin, J. P.,... & Leonel, J. (2018). Sulfluramid use in Brazilian agriculture: A source of per-and polyfluoroalkyl substances (PFASs) to the environment. Environmental Pollution, 242, 1436-1443. doi: 10.1016/j.envpol.2018.07. 122
Nickele, M. A., Reis, W., Fº., Penteado, S. D. R., de Queiroz, E. C., Schaitza, E. G., & Pie, M. R. (2021). Potential damage by Acromyrmex ant species in pine plantations in southern Brazil. Agricultural and Forest Entomology, 23, 32-40, doi: 10.1111/afe.12400
Nickele, M. A., Reis, W., Fº., Penteado, S., & Queiroz, E. C. de. (2018). Manejo de Acromyrmex (Hymenoptera: Formicidae) em plantios florestais na Região Sul do Brasil. Anais do Encontro Brasileiro de Silvicultura, Ribeirão Preto, SP, Brasil, 4. Recuperado de http://www.alice.cnptia. embrapa .br/alice/handle/doc/1092382
Rando, J. S. S., & Forti, L. C. (2005). Ocorrência de formigas Acromyrmex Mayr, 1865, em alguns municípios do Brasil. Acta Scientiarum. Biological Sciences, 27(2), 129-133. doi: 10.4025/ actascibiolsci.v27i2.1322
Singer, R. (1986). The Agaricales in modern taxonomy. (4a ed.). Koegnistein: Koeltz Scientific Books.
Swanson, A. C., Schwendenmann, L., Allen, M. F., Aronson, E. L., Artavia León, A., Dierick, D.,... Pinto Tomás, A. A. (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: 10.1111/1365-2435.13 319
Toffoli, A. L. de, Mata, K. da, Bisinoti, M. C., & Moreira, A. B. (2015). Development, validation, and application of a method for the GC-MS analysis of fipronil and three of its degradation products in samples of water, soil, and sediment. Journal of Environmental Science and Health, Part B, 50(11), 753-759. doi: 10.1080/03601234.2015.1058091
Vieira, E. H. M., Neto, Mundim, F. M., & Vasconcelos, H. L. (2006). Hitchhiking behaviour in leaf-cutter ants: an experimental evaluation of three hypotheses. Insectes Sociaux, 53(3), 326-332. doi: 10.1007/s0 0040-006-0876-7
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
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2021-07-02
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Almeida, J. C. de, Hoshino, A. T., Menezes Junior, A. de 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. Semina: Ciências Agrárias, 42(5), 2669–2684. https://doi.org/10.5433/1679-0359.2021v42n5p2669
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