Parasitism of Automeris liberia (Lepidoptera: Saturniidae) by tachinids (Diptera: Tachinidae) in oil palm in the Brazilian Amazon

ABSTRACT

Automeris liberia (Lepidoptera: Saturniidae) caterpillars are important defoliators of the African oil palm, Elaeis guineensis (Arecaceae) in Central and South America. The family Tachinidae (Diptera) comprises flies that are parasitoids of many insect pests, mainly from the order Lepidoptera. However, host records for tachinids are still relatively scarce. In the present work, we report the occurrence of Belvosia sp. aff. williamsi (Diptera: Tachinidae: Exoristinae: Goniini) and Leptostylum oligothrix (Diptera: Tachinidae: Exoristinae: Blondeliini) parasitizing caterpillars of A. liberia in E. guineensis in the municipality of Tailândia, state of Pará, Brazil. This is the first record of the parasitism of A. liberia by Leptostylum in Brazil, as well as by Belvosia in the world.

KEYWORDS:
Belvosia; Leptostylum; Exoristinae; Blondeliini; Goniini

RESUMO

Lagartas de Automeris liberia (Lepidoptera: Saturniidae) são importantes desfolhadoras da palma de óleo, Elaeis guineensis (Arecaceae) nas Américas Central e do Sul. A família Tachinidae (Diptera) compreende moscas parasitoides de muitos insetos-praga, principalmente da ordem Lepidoptera. Contudo, o registro de hospedeiros de taquinídeos ainda é relativamente escasso. No presente trabalho, relatamos a ocorrência de Belvosia sp. aff. williamsi (Diptera: Tachinidae: Exoristinae: Goniini) e Leptostylum oligothrix (Diptera: Tachinidae: Exoristinae: Blondeliini) parasitando lagartas de A. liberia em E. guineensis no município de Tailândia, Pará, Brasil. Trata-se do primeiro registro do parasitismo de A. liberia por Leptostylum no Brasil, bem como o primeiro por Belvosia no mundo.

PALAVRAS-CHAVE:
Belvosia; Leptostylum; Exoristinae; Blondeliini; Goniini

Automeris liberia (Cramer, 1780) (Lepidoptera: Saturniidae) is a moth with caterpillars that infest oil palm, Elaeis guineensis Jacq. (Arecaceae), with records of infestation of palm plantations in Colombia, Peru, Venezuela and the Brazilian Amazon (Genty et al. 1978; Aldana de La Torre et al. 2010). The northern region of Brazil is the largest producer of oil palm in the country, and the state of Pará has approximately 88% of the area devoted to palm oil production in the country (Brandão et al. 2019). Considerable outbreaks of A. liberia caterpillars in the field cause defoliation that makes production unfeasible and, in addition, the caterpillars are dangerous to humans because their bodies are covered with urticating setae (Genty et al. 1978; Aldana de La Torre et al. 2010).

The Tachinidae (Diptera) family comprises more than 8,500 species distributed in all geographic regions of the planet, with the exception of Antarctica (O’Hara 2013; O’Hara et al. 2020; Stireman et al. 2019). The Neotropical region has 3,032 species (O’Hara et al. 2020), with about 785 recorded for Brazil (Nihei et al. 2021). All known species are endoparasitoids of insects and other arthropods and, although they attack hosts of 15 different orders of Arthropoda, the vast majority of tachinids parasitize holometabolic insect larvae (Stireman et al. 2019; 2021). The order Lepidoptera represents 70% of known host species (Dindo and Grenier 2014; Dindo and Nakamura 2018). As natural enemies of these primarily phytophagous groups, tachinids have been considered one of the most important groups of biological control agents (Gudin and Messas 2018; Weber et al. 2021), both in natural environments and in managed ecosystems (Stireman et al. 2019). However, when compared to the diversity of tachinid species, host records for them are still scarce (Scaramozzino et al. 2020).

As there is no product with permitted use for the control of A. liberia in Brazil, the search for management alternatives, including natural enemies, is of great importance. Identifying natural enemies is an essential step in establishing a pest management program. Thus, aiming to contribute to the knowledge about alternatives for the biological pest control, here we report the parasitism of A. liberia by two tachinid species in oil palm in the Brazilian Amazon.

In March 2021, a collection of A. liberia caterpillars was carried out in commercial oil palm plantations of Grupo Agropalma S/A, in the municipality of Tailândia, state of Pará, Brazil (2º31’16”S; 48º46’25”W). The cultivation area has 120 ha and density of 143 palms ha^-1, with ages ranging from three to five years. We found 68 caterpillars of different instars infesting palms in the field. The caterpillars were taken to the laboratory, placed individually in plastic pots (10 cm in diameter × 6 cm high) and kept in a rearing room at 25 ± 2 ºC, relative humidity of 68 ± 10% and 12L/12D photoperiod, with natural diet (host plant leaflets). The containers were monitored every 24 hours to check the possible presence of natural enemies.

Parasitism by tachinids was observed in two instances. In 10.3% of the A. liberia specimens, tachinid larvae left the body of the caterpillars and pupated inside the plastic containers (the pupae were collected and kept until the emergence of the adult flies). In 4.4% of the A. liberia specimens, adult tachinids emerged directly from the host’s pupae. In both cases, adult parasitoids were collected and preserved in 70% alcohol. The tachinids were identified based on Aldrich (1928) and Gudin and Messas (2018), and the specimens were deposited in the zoological reference Collection of the Universidade Federal de Mato Grosso do Sul (ZUFMS), in Campo Grande, Mato Grosso do Sul, Brazil.

The emerged tachinids were identified as Belvosia sp. aff. williamsiAldrich, 1928 (Exoristinae: Goniini) (Figure 1) (eight individuals, six males and two females) (vouchers ZUFMS-DIP01252 - ZUFMS-DIP01254) and Leptostylum oligothrixGudin & Messas, 2018 (Exoristinae: Blondeliini) (Figure 2) (30 individuals, 12 males and 18 females) (vouchers ZUFMS-DIP01248 - ZUFMS-DIP01251).

Figure 1
Male of Belvosia sp. aff. williamsi. A - dorsal view; B - detail of wing; C - lateral view. Scale bars = 1 mm. This figure is in color in the electronic version.

Figure 2
Male of Leptostylum oligothrix. A - dorsal view; B - lateral view. Scale bars = 1 mm. This figure is in color in the electronic version.

Male specimens of Belvosia run to B. williamsi in the key of Aldrich (1928) and, with the exception of the genal hairs without reddish reflections and the postpedicel a little less than twice the length of the pedicel, agree with the description of this species. However, Aldrich (1928) did not describe the male terminalia of B. williamsi, so that it is not currently possible to make a definitive identification.

The specimens identified as L. oligothrix can be easily distinguished from other species of the genus by the following combination of features: ocellar triangle and fronto-orbital plate with golden pruinosity, well-developed ocellar setae, eyes sparsely haired with short hairs, palpus yellow, tegula and basicosta black, calyptra white with yellowish margin, basal dorsal surface of tergites 3, 4 and 5 with faint yellowish pruinosity, and postgonite subtrapezoidal (Gudin and Messas 2018). However, our specimens differed slightly from the description by Gudin and Messas (2018) in having the golden pruinosity of the fronto-orbital plate extending bellow the second anterior frontal seta covering the upper half of the parafacial (instead of having fronto-orbital plate with golden pruinosity to the level of the second anterior seta), antenna brown with the apex of the pedicel and the basal portion of the postpedicel reddish brown (instead of antenna being black), labella yellow (instead of labella being reddish-brown), surstylus in posterior view slightly wider and less straight and in lateral view slightly broader at the base, cercus in posterior view narrowing more evenly from base to apex, postgonite narrowing towards apex but more digitiform, and pregonite with posterior margin straighter. Despite the above differences, our specimens were tentatively identified here as L. oligothrix until more material is available for further study.

The genus Belvosia Robineau-Desvoidy, 1830 has 71 valid species, some of them with Nearctic distribution, but most described from the Neotropical region, from Mexico to Argentina and Chile (O’Hara et al. 2020). The genus Leptostylum Macquart, 1851 is distributed from southern Mexico to southeastern Brazil. Despite being considered a diverse taxon, with many species yet to be described (Wood and Zumbado 2010), the genus currently has nine valid species (Gudin and Messas 2018; O’Hara et al. 2020).

In South America, species of Belvosia have been previously reported from hosts from the families Arctiidae, Limacodidae, Megalopygidae, Mimallonidae, Notodontidae, Nymphalidae, Saturniidae and Sphingidae (Lepidoptera) (Guimarães 1977). With respect to the genus Leptostylum, most known hosts are lepidopterans from the family Saturniidae (Jacobson 1991; Stireman et al. 2009; Gudin and Messas 2018). However, the record of hosts of Tachinidae, especially in the Neotropical region, is still considered scarce (Gudin and Messas 2018). Additional families of lepidopteran hosts for Belvosia and Leptostylum were identified in Costa Rica, such as Erebidae, Eupterotidae, Hesperiidae and Noctuidae (Janzen and Hallwachs 2009).

Tachinidae larvae develop inside the host, consuming its tissues and typically killing it, and then pupate inside the host’s corpse or in the litter or soil (Stireman et al. 2006). The tachinids identified as L. oligothrix in our study abandoned the host’s body when the host was still in the larval stage, leaving the caterpillar corpse flaccid and pupating out of it. In contrast, the larvae of Belvosia sp. aff. williamsi allowed the host to reach the stage of pupa, from which they emerged, leaving the host’s pupa still rigid.

A species of Leptostylum has been reported to parasitize A. liberia in Peru (Jacobson 1991). However, the present work is the first formal record of A. liberia being parasitized by a Leptostylum species in Brazil, as well as the first worldwide record of an association between A. liberia and Belvosia. It should be noted that these genera are well-known to be associated with other species of Automeris (Guimarães 1977; Jacobson 1991; Ramírez et al. 2004; Janzen and Hallwachs 2009; Stireman et al. 2009; Gudin and Messas 2018).

Our results open a perspective of potential use of the parasitoids Belvosia sp. aff. williamsi and L. oligothrix in the biological control of A. liberia in oil palm and other crops attacked in South America, and potentially bring gains in production without impacting humans and the environment.

ACKNOWLEDGMENTS

The authors are grateful to Grupo Agropalma S/A (Tailândia, PA, Brazil), for providing the insects that made this work possible; and to Fagner Pimentel Cardoso de Oliveira, from Universidade Federal de Alagoas - UFAL (Rio Largo, AL, Brazil), for helping with insect imaging.

REFERENCES

• Aldana de La Torre, R.C.; Aldana de La Torre, J.A.; Calvache Guerrero, H.; Franco Bautista, P.N. 2010. Manual de plagas de la palma de aceite en Colombia 4 ed. Cenipalma, Bogotá, 198p.
• Aldrich, J.M. 1928. A revision of the American parasitic flies belonging to the genus Belvosia Proceedings of the United States National Museum, 73: 1-45.
• Brandão, F.; Castro, F.; Futemma, C. 2019. Between structural change and local agency in the palm oil sector: Interactions, heterogeneities and landscape transformations in the Brazilian Amazon. Journal of Rural Studies, 71: 156-168.
• Dindo, M.L.; Grenier, S. 2014. Production of dipteran parasitoids. In: Morales-Ramos, J.; Guadalupe Rojas, M.; Shapiro-Ilan, D. (Ed.). Mass production of beneficial organisms - invertebrates and entomopathogens, Academic Press, San Diego, p.101-143.
• Dindo, M.L.; Nakamura, S. 2018. Oviposition strategies of tachinid parasitoids: two Exorista species as case studies. International Journal of Insect Science, 10: 1-6.
• Genty, P.; Desmier de Chenon, R.; Morin, J.P. 1978. Les ravageurs du palmier à huile en Amérique Latine. Oléagineux, 33: 325-419.
• Gudin, F.M.; Messas, Y.F. 2018. On taxonomy and hosts of Leptostylum Macquart, 1851 (Diptera: Tachinidae: Blondeliini), with description of a new species and a new host record. Journal of Natural History, 52: 1395-1415.
• Guimarães, J.H. 1977. Host-parasite and parasite-host catalogue of South American Tachinidae (Diptera). Arquivos de Zoologia, 28: 1-131.
• Jacobson, N.L. 1991. Parasitoid and larval food plant records for three Peruvian moths (Arctiidae, Saturniidae). Journal of the Lepidopterists’ Society, 45: 173-175.
• Janzen, D.H.; Hallwachs, W. 2009. Dynamic database for an inventory of the macrocaterpillar fauna, and its food plants and parasitoids, of Area de Conservacion Guanacaste (ACG), northwestern Costa Rica (nn-SRNP-nnnnn voucher codes). ( (http://janzen.sas.upenn.edu ). Accessed on 18 Oct 2022.
  » http://janzen.sas.upenn.edu
• Nihei, S.S.; Alvarez-Garcia, D.M.; Gudin, F.M.; Santis, M.D.; Dios, R.V.P. 2021. Tachinidae in Catálogo Taxonômico da Fauna do Brasil. PNUD. ( (http://fauna.jbrj.gov.br/fauna/faunadobrasil/1115 ). Accessed on 18 Oct 2022.
  » http://fauna.jbrj.gov.br/fauna/faunadobrasil/1115
• O’Hara, J.E. 2013. History of tachinid classification (Diptera, Tachinidae). ZooKeys, 316: 1-34.
• O’Hara, J.E.; Henderson, S.J.; Wood, D.M. 2020. Preliminary checklist of the Tachinidae of the World. Version 2.1. (http://www.nadsdiptera.org/Tach/WorldTachs/Checklist/Tachchlist_ver2.1.pdf) Accessed on 18 Oct 2022.
• Ramírez, R.; Domínguez, O.; Inciarte, E.; Burgos, M.E. 2004. Himenópteros y dípteros parasíticos de Automeris incarnata Walker 1865 (Lepidóptera: Saturniidae) defoliador del cultivo plátano (Musa AAB, sub-grupo plátano cv. Hartón) en la zona Sur y Este del lago de Maracaibo, Venezuela. Revista de la Facultad de Agronomía (LUZ), 21(supl. 1): 148-154.
• Scaramozzino, P.L.; Di Giovanni, F.; Loni, A.; Gisondi, S.; Lucchi, A.; Cerretti, P. 2020. Tachinid (Diptera, Tachinidae) parasitoids of Lobesia botrana (Denis & Schiffermüller, 1775) (Lepidoptera, Tortricidae) and other moths. ZooKeys , 934: 111-140.
• Stireman, J.O.; Cerretti, P.; O’Hara, J.E.; Blaschke, J.D.; Moulton, J.K. 2019. Molecular phylogeny and evolution of world Tachinidae (Diptera). Molecular Phylogenetics and Evolution, 139: 106358.
• Stireman, J.O.; Cerretti, P.; O’Hara, J.E.; Moulton, J.K. 2021. Extraordinary diversification of the “bristle flies” (Diptera: Tachinidae) and its underlying causes. Biological Journal of the Linnean Society, 133: 216-236.
• Stireman, J.O.; Greeney, H.F.; Dyer, L.A. 2009. Species richness and host associations of Lepidoptera-attacking Tachinidae in the Northeast Ecuadorian Andes. Journal of Insect Science, 9: 39.
• Stireman, J.O.; O’Hara, J.E., Wood, D.M. 2006. Tachinidae: Evolution, behavior, and ecology. Annual Review of Entomology, 51: 525-555.
• Weber, I.D.; Lopes, W.R.; de Paula, L.C.B.; Albernaz-Godinho, K.C.; Czepak, C. 2021. Tachinids associated with lepidopteran pests in agricultural crops in south-central region of Goiás, Brazil. BioControl, 66: 625-637.
• Wood, D.M.; Zumbado, M.A. 2010. Tachinidae (tachinid flies, parasitic flies). In: Brown, B.V.; Borkent, A.; Cumming, J.M.; Wood, D.M.; Woodley, N.E.; Zumbado, M.A.; (Ed.) Manual of Central American Diptera, v. 2. NRC Research Press, Ottawa, p.1343-1417.

• CITE AS:

  Silva, K.B.; Silva, C.B.; Gourlat, H.F.; Tinôco, R.S.; Souza, J.M.; Chia, G.S.; Garcia, C.H.; Toma, R.; Guzzo, E.C. 2022. Parasitism of Automeris liberia (Lepidoptera: Saturniidae) by tachinids (Diptera: Tachinidae) in oil palm in the Brazilian Amazon. Acta Amazonica 53: 20-23.

Edited by

ASSOCIATE EDITOR:

Juliana Hipólito

Publication Dates

• Publication in this collection
  23 Jan 2023
• Date of issue
  Jan-Mar 2023

History

• Received
  29 Apr 2022
• Accepted
  11 Nov 2022