Abstract:

The first case of parasitoidism of a Myrmicinae ant by a sarcophagid fly has been observed in the Brazilian Cerrado. The larva of a Helicobia Coquillet (Sarcophagidae) specimen fed on head tissues of an Atta laevigata Smith, 1858 soldier and an adult male fly emerged from a puparium formed outside the host.

Keywords:
Brazilian savanna; Helicobia; natural enemies; parasitoid-host interaction

Resumo:

O registro do parasitoidismo de uma formiga Myrmecinae por uma mosca Sarcophaginae foi relatado no Cerrado brasileiro. A larva de um exemplar de Helicobia Coquillet (Sarcophagidae) se alimentou dos tecidos da cabeça de um soldado de Atta laevigata Smith, 1858 e um adulto macho emergiu de um pupário que se formou fora do hospedeiro.

Palavras-chave:
Savana Brasileira; Helicobia; inimigos naturais; interação parasitoide-hospedeiro

Introduction

Parasitoidism of ants by flies (Diptera) have been reported for single species of the families Tachinidae and Syrphidae and many species of the family Phoridae. The tachinid Strongygaster globula Meigen, 1824 (formerly called Tamiclea globula) has as its host young queens of the genus Lasius Fabricius, 1804 (Hymenoptera: Formicidae: Formicinae) (Schmid-Hempel 1998SCHMID-HEMPEL, P. 1998. Parasites in social insects. Ney Jersey: Princeton University Press, 392 p., Herting 2017HERTING, B. 2017. A critical revision of host records of Palearctic Tachinidae (Diptera) until 1937. Integrative Systematics: Stuttgart Contributions to Natural History, 10: 41-173.), while the syrphid Hypselosyrphus trigonus Hull, 1937 is known as a parasitoid of workers of the tree ant Neoponera villosa (Fabricius, 1804) (Hymenoptera: Formicidae: Ponerinae) (Pérez- Lachaud et al. 2014). On the other hand, phorid flies are important parasitoids of a wide range of social insects, with ants as the main hosts (Disney 1994DISNEY, R.H.L. 1994. Scuttle flies: the Phoridae. Londres: Chapmam & Hall, p. 467.). Accordingly, interactions between phorid parasitoids and many members of the family Formicidae have been described, including species of the genus Atta Fabricius, 1805 and Acromyrmex Mayr, 1865 (Myrmicinae) of the tribe Attini (Disney 1994DISNEY, R.H.L. 1994. Scuttle flies: the Phoridae. Londres: Chapmam & Hall, p. 467., Schmid-Hempel 1998SCHMID-HEMPEL, P. 1998. Parasites in social insects. Ney Jersey: Princeton University Press, 392 p., Bragança 2011BRAGANÇA, M.A.L. 2011. Parasitoides de formigas-cortadeiras. In T.M.C. DELLA LUCIA (Ed.), As formigas-cortadeiras: da bioecologia ao manejo, p. 321-343. Viçosa: Editora UFV., Uribe et al. 2014URIBE, 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.). Generally, phorids that attack ants are small flies that pursue workers along their trails or in foraging areas, ovipositing eggs on the heads or abdomens of the host (Erthal & Tonhasca 2000ERTHAL, 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. Entomol Exp Appl. 95: 71-75., Tonhasca et al. 2001TONHASCA, 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 Soc. 48: 154-158., Bragança et al. 2002BRAGANÇA, M.A.L., TONHASCA, A. JR. & MOREIRA, D.D.O. 2002. Parasitism characteristics of two phorid fly species in relation to their host, the leaf-cutting ant Atta laevigata (Smith) (Hymenoptera: Formicidae). Neotrop. Entomol. 31: 241-244.).

The large leaf-cutting ant Atta laevigata Smith, 1858, an eusocial insect widely distributed in Brazil, causes significant damage to agricultural and forest crops (Montoya-Lerma et al. 2012MONTOYA-LERMA, J., GIRALDO-ECHEVERRI, C., ARMBRECHT, I., FARJI-BRENER, A. & CALLE, Z. 2012. Leaf-cutting ants revisited: towards rational management and control. Int J Pest Manage. 58: 225-247.) and therefore, it is a target of biological control. We observed the interactions between phorid flies and leaf-cutting ants along their foraging trails to assess the levels of parasitoidism of A. laevigata in the Cerrado of the Central-West region of Brazil.

During fieldwork, we observed a single sarcophagid fly interacting with an A. laevigata soldier. The observation was noteworthy because sarcophagid species commonly establish predatory, kleptoparasitic, or parasitic interactions with butterflies, grasshoppers, moths, termites, wasps, and bees, but not with ants (Pape 1987PAPE, T. 1987. The Sarcophagidae (Diptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica, v 19, Copenhagen: Scandinavian Science Press Ltd., p. 203., Schmid-Hempel 1998SCHMID-HEMPEL, P. 1998. Parasites in social insects. Ney Jersey: Princeton University Press, 392 p.).

Material and Methods

Fieldwork was carried out in a Cerrado area (10°10′56.3″S, 48°18′23.8″W) close to the city of Palmas, Tocantins, Brazil. During the search for phorids attacking A. laevigata workers, an unidentified sarcophagid or tachinid was observed flying over, and sometimes walking on, the head and back of an individual soldier, who was moving unusually slowly manner. The soldier was collected carefully using forceps, transferred to a small glass jar, and taken to the laboratory. However, the ant-attacking fly escaped during the capture attempt. Later that same day, the soldier was examined under a magnifying lens, and a larva was detected moving within the cephalic capsule. The ant was placed in a Petri dish, fed with 10% honey solution soaked into a cotton wool pad, and maintained at 26^oC in a rearing chamber. The larva developing inside the cephalic capsule was observed every 24 hours. The puparium was subsequently detached from the pad, transferred to a glass vial (100 mm high x 13 mm diameter), and maintained in the rearing chamber. An adult male fly emerged from the puparium (Figure 1A), and the specimen was identified by Dr. Cátia Mello Patiu (National Museum, Rio de Janeiro, RJ, Brazil), using a Sarcophagidae identification key for the genus (Pape & Dahlem 2010PAPE, T. & DAHLEM, G.A. 2010. Sarcophagidae. In: Brown, B.V., Borkent, A., Cumming, J.M., Wood, D.M., Woodley, N.E. & Zumbado, M. (Eds.), A Manual of Central American Diptera. Vol. 2. NRC Research Press, Ottawa, p. 1313-1335.). Although the male holotype was fully described, the specimen, along with its description and undigitized drawings, was unfortunately lost in a fire that destroyed the Rio de Janeiro’s National Museum on 2 September 2018 (personal communication, C. Mello-Patiu).

Figure 1
(A) Puparium of the Helicobia sp. Coquillet (Diptera: Sarcophagidae: Sarcophaginae) after emergence of the adult fly, showing the operculum detached from the rest of the puparium. Puparium length: 3.5 mm. (B) Adult male of the sarcophagid parasitoid.

Results and Discussion

Approximately 72 hours after being placed in the rearing chamber, the soldier was confirmed dead, with the mandibles open. Further inspection revealed that the cephalic capsule was empty and the head devoid of tissues. Except for the mandibles, all other mouthparts were released from the cephalic capsule (Figure 2). The larva exited the capsule through the gap between the mandibles and formed a puparium between the cotton fibers inside the Petri dish. The fly emerged 12 days later and the fly was identified as a member of the genus Helicobia Coquillet, 1985 (Diptera: Sarcophagidae: Sarcophaginae) (Figure 1B).

Figure 2
Ventral face of the cephalic capsule of an Atta laevigata Smith, 1858 (Hymenoptera: Formicidae: Myrmicinae) soldier. Capsule width: 6.4 mm.

The association between Formicidae (A. laevigata) and Sarcophagidae (Helicobia sp.) is reported here for the first time. The biological characteristics of this interaction are comparable with those described for A. laevigata and the phorid Apocephalus attophilus Borgmeier, 1928, which is one of the several parasitoids of the family that oviposit on at least four other species of leaf-cutting ants (Erthal & Tonhasca 2000ERTHAL, 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. Entomol Exp Appl. 95: 71-75., Bragança & Medeiros 2006BRAGANÇA, M.A.L. & MEDEIROS, Z.C.S. 2006. Ocorrência e características biológicas de forídeos parasitóides (Diptera: Phoridae) da saúva Atta laevigata (Smith) (Hymenoptera: Formicidae) em Porto Nacional, TO. Neotrop. Entomol. 35: 408-411., Bragança 2011BRAGANÇA, M.A.L. 2011. Parasitoides de formigas-cortadeiras. In T.M.C. DELLA LUCIA (Ed.), As formigas-cortadeiras: da bioecologia ao manejo, p. 321-343. Viçosa: Editora UFV.). In both interactions, the parasitoid larva develops inside the head of an A. laevigata worker, consumes the capsule contents, exits through the gap between the mandibles, and forms a puparium outside the host. When A. laevigata is parasitized by A. attophilus, the number of larvae per host ranges between 1 and 14, depending on the size of the cephalic capsule of the workers and soldiers, with the number of puparia also varying (Erthal & Tonhasca 2000ERTHAL, 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. Entomol Exp Appl. 95: 71-75., Bragança et al. 2016BRAGANÇA, 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.). However, in the novel interaction reported here, a single Helicobia sp. larva developed inside the head of an A. laevigata soldier, in which the cephalic capsule was 6.4 mm wide and the puparium was 3.5 mm in length, i.e., substantially larger than those of A. attophilus larvae (0.97 ± 0.11 mm [range from 0.86 to 1.23], n = 26; unpublished results). Interestingly, associations between A. laevigata and other phorid parasitoids, such as those of the genera EibesfeldtphoraDisney, 2009DISNEY, R.H.L. 1994. Scuttle flies: the Phoridae. Londres: Chapmam & Hall, p. 467., and Myrmosicarius Borgmeier, 1928, almost invariably result in the development of a single larva per host. However, the puparium is generally formed between the mandibles of the ant, or inside its cephalic capsule or thorax (Bragança et al. 2002BRAGANÇA, M.A.L., TONHASCA, A. JR. & MOREIRA, D.D.O. 2002. Parasitism characteristics of two phorid fly species in relation to their host, the leaf-cutting ant Atta laevigata (Smith) (Hymenoptera: Formicidae). Neotrop. Entomol. 31: 241-244., Bragança et al. 2003BRAGANÇA, M.A.L., DELLA LUCIA, T.M.C. & TONHASCA, A. JR. 2003. First record of phorid parasitoids (Diptera: Phoridae) of the leaf-cutting ant Atta bisphaerica Forel (Hymenoptera: Formicidae). Neotrop. Entomol. 32: 169-171., Bragança & Medeiros 2006BRAGANÇA, M.A.L. & MEDEIROS, Z.C.S. 2006. Ocorrência e características biológicas de forídeos parasitóides (Diptera: Phoridae) da saúva Atta laevigata (Smith) (Hymenoptera: Formicidae) em Porto Nacional, TO. Neotrop. Entomol. 35: 408-411.).

The common biological characteristics of A. attophilus and Helicobia sp. differ from those of Tachinidae and Syrphidae flies that reportedly parasitize ants other than A. laevigata. For example, tachinid S. globula is an endoparasite that develops in the gaster of young queens (i.e., colony-founding queens) of the black garden ant Lasius niger Linnaeus, 1758 or Lasius alienus Foerster, 1850. During the final instar, the larva exits the abdomen of the host through the anus and forms a puparium among the offspring of other ants, where it is raised by workers as if it were part of the colony itself (Gösswald 1950GÖSSWALD, K. 1950. Pflege des Ameisenparasiten Tamiclea globula Meig. (Dipt.) durch den Wirt mit Bemerkungen über den Stoffwechsel in der parasitierten Ameise. Verhandlungen der Deutschen Zoologen, Mainz, p. 256-264., Hölldobler & Wilson 1990HÖLLDOBLER, B. & WILSON, E.O. 1990. The ants. Cambridge: Harvard University Press, p. 732.). On the other hand, the larva of the syrphid H. trigonus consumes almost all contents of the N. villosa prepupa and forms its puparium inside the cocoon of the host (Pérez-Lachaud et al. 2014PÉREZ-LACHAUD, G., JERVIS, M.A., REEMER, M. & LACHAUD, J.P. 2014. An unusual, but not unexpected, evolutionary step taken by syrphid flies: the first record of true primary parasitoidism of ants by Microdontinae. Biol. J. Linn. Soc. 111: 462-472.).

Regarding the behavioral attraction mechanisms, phorids seem to use long-distance olfactory cues to guide them to ant nests and foraging trails (Feener & Brown 1997FEENER, D.H. JR. & BROWN, B.V. 1997. Diptera as parasitoids. Annu. Rev. Entomol. 42: 73-97.). In the interaction between A. attophilus and A. laevigata, the female fly approaches its prey in the foraging area and walks among the workers aiming to insert its ovipositor into their mouths while they are cutting the leaves (Erthal & Tonhasca 2000ERTHAL, 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. Entomol Exp Appl. 95: 71-75.). Other phorid parasitoids of A. laevigata, such as Eibesfeldtphora tonhascai Brown, 2001, and Eibesfeldtphora erthali Brown, 2001, have been observed to fly over workers and insert their ovipositors into the back of the head or gaster, respectively (Bragança et al. 2002BRAGANÇA, M.A.L., TONHASCA, A. JR. & MOREIRA, D.D.O. 2002. Parasitism characteristics of two phorid fly species in relation to their host, the leaf-cutting ant Atta laevigata (Smith) (Hymenoptera: Formicidae). Neotrop. Entomol. 31: 241-244.).

No information is currently available regarding the mechanisms of attraction of sarcophagids to their hosts. During the field research reported herein, we observed that the putative sarcophagid fly performed short flights and touched the head of the soldier. The fly also walked incessantly over the back of the ant, sometimes touching the last portion of the abdomen. Since sarcophagids typically lay ready-to-hatch or newly hatched larvae (Pape 1987PAPE, T. 1987. The Sarcophagidae (Diptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica, v 19, Copenhagen: Scandinavian Science Press Ltd., p. 203.), the touching and walking activities of the fly could be described as larviposition behavior. However, later examination of the soldier revealed that there was a larva already developing inside its cephalic capsule. Hence, it is possible that the touching and walking activities of the fly represented a host-searching behavior and that the soldier was rejected because it was already parasitized. It is worth noting that discriminatory activities towards parasitized and non-parasitized ant hosts have been observed previously among phorid flies, albeit with low frequency (Bragança et al. 2009BRAGANÇA, M.A.L., NOGUEIRA, C.A., SOUZA, L.M. & DELA LUCIA, T.M.C. 2009. Superparasitism and host discrimination by Neodohrniphora elongata (Diptera: Phoridae), a parasitoid of the leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae). Sociobiology. 54: 907-918.). Despite having no reports of Helicobia parasitoidism on Formicidae, there are parasitoidism records of this parasitic genus with other groups of the order Hymenoptera (e.g., bees) (Nowogrodzki & Morse 1990NOWOGRODZKI, R., & MORSE, R. A. 1990. Honey bee pests, predators, and diseases. Comstock Publishing Associates a division of Cornell University Press, Itahca and London., Schmid-Hempel 1998SCHMID-HEMPEL, P. 1998. Parasites in social insects. Ney Jersey: Princeton University Press, 392 p.).

Although the interaction between the leaf-cutting ant A. laevigata and the sarcophagid fly Helicobia sp. is atypical and rare, the form of parasitoidism resembles that observed between the same host and other flies, especially among phorids. Therefore, this sarcophagid species can be considered another natural enemy of leaf-cutting ants, which are destructive herbivores throughout South America.

Acknowledgments

The authors thank Dr. Cátia Mello-Patiu for kind assistance in the identification of the fly specimen. The study was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico/Rede de Biodiversidade e Biotecnologia da Amazônia Legal (CNPQ/BIONORTE) and the Secretaria Estadual de Desenvolvimento, Ciência, Tecnologia e Inovação do Tocantins (SEDECTI/TO), through an agreement with the Federal University of Tocantins. FVA thanks CNPQ by PCI-MCTIC/MPEG (302198/2020-2). To the reviewers for the valuable considerations.

References

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