Ceromasia auricaudata Townsend (Diptera: Tachinidae) is recorded for the first time in Mexico. This also is the first time that C. auricaudata is associated with Neodiprion omosus Smith (Hymenoptera: Diprionidae), increasing the number of genera of Tachinidae associated with sawflies.
The family Diprionidae (Insecta: Hymenoptera), commonly known as sawflies, includes at least 90 described species and is a group of conifer-defoliating insects in the Northern Hemisphere (Smith 1988; Taeger et al. 2010; Smith et al. 2012). Many reports have indicated the presence of sawflies of the genus Neodiprion Rohwer, Zadiprion Rohwer, and Monoctenus Dahlbom (Hymenoptera: Diprionidae) in Mexican conifer forests (Smith 1988; Smith et al. 2010, 2012). Defoliation attributed to sawflies leads to reduced growth in terms of diam, height, and root size in affected trees; if attack is severe and prolonged, it can result in tree death, especially among young trees in the sprouting phase (González-Gaona & Sánchez-Martínez 2018; Aguilera-Molina et al. 2019).
The genus Neodiprion currently contains 51 described species (Taeger et al. 2010) of which Neodiprion autumnalis Smith, Neodiprion bi-color Smith, Neodiprion equalis Smith, and Neodiprion omosus Smith (all Hymenoptera: Diprionidae) are reported to occur in Mexico (Smith 1988). Neodiprion omosus is a univoltine species that is well known in central Mexico and is associated with 9 species of Pinus L. (Pinaceae) (Cibrián-Tovar et al. 1995; Coria-Avalos et al. 2014). The larvae of N. omosus are gregarious, feeding on young needles and the bark of young twigs. As they near pupation, N. omosus larvae leave the trees to overwinter underground as pupae. Adults emerge in summer (Cibrián-Tovar et al. 1995).
Parasitism is a natural cause of mortality of sawfly larvae (González-Gaona & Sánchez-Martínez 2018). The main groups of parasitoids associated with sawflies include members of the families Ichneumonidae (Hymenoptera) and Tachinidae (Diptera); however, many reports indicate that ichneumonids account for the majority of cases of parasitism in sawfly populations (Ruiz-Cancino & Khalaim 2015; Tao et al. 2016; Khalaim et al. 2019). Despite the abundance of ichneumonids, the literature cites 31 genera of Tachinidae associated with sawflies (Richter & Kasparyan 2013). In this study, we report for the first time the presence of Ceromasia auricaudata Townsend (Diptera: Tachinidae) in Mexico in association with larvae of the sawfly N. omosus, which constitutes a new host record.
In Aug 2018, we observed an outbreak of N. omosus larvae in the experimental station of the Facultad de Ciencias Agrícolas de la Universidad Autónoma del Estado de México, located in the community of the Cerrillo, Piedras Blancas (19.2432°N, 99.4120°W; 2,614 masl), Toluca, Estado de Mexico, Mexico. The outbreak affected 2 populations of 9-yr-old pine trees: 17 Pinus gregii Engelm. ex Parl. trees and 14 Pinus patula Schiede ex Schltdl. & Cham. (Pinaceae). In Oct of the same yr, 1,500 late stage N. omosus larvae were collected and transported to the laboratory for conditioning.
The larvae were placed in 32.5 × 18.0 × 11.5 cm plastic containers (Rubbermaid®, Atlanta, Georgia, USA) and fed with pine needles from P. gregii that were replaced every 5 d. A total of 1,294 puparia were obtained and transferred to a new container with previously disinfected soil with hot water (70 °C for 15 min) as a pupation substrate. The soil was moistened with distilled water once per wk to avoid desiccation and premature death of the pupae. The pupation containers were covered with cheesecloth so that parasitoids and sawfly adults could not escape, and were kept in uncontrolled laboratory conditions. Of the 1,294 puparia, 1,047 adult sawflies and 11 Tachinidae specimens emerged, with a single fly emerging from each puparia. It was identified as C. auricaudata by D. H. Zetina. The specimens were deposited in the Colección de Insectos del Colegio de Postgraduados, Montecillo, Texcoco, Estado de Mexico, Mexico.
The genus Ceromasia Rondani (Diptera: Tachinidae: Goniini) is composed of 3 species: C. auricaudata, Ceromasia hybreas (Walker), and Ceromasia rubrifrons (Macquart) (Diptera: Tachinidae), which are recorded from North America, Europe, and Asia (O'Hara et al. 2019). The current distribution of C. auricaudata includes Canada and the US (O'Hara et al. 2019). Our findings contribute to knowledge of range expansion of this species toward central Mexico. Ceromasia auricaudata is a solitary koinobiont endoparasitoid associated with larvae of the genus Choristoneura Lederer (Lepidoptera: Tortricidae) (O'Hara 2005). The literature does not report parasitism of sawflies by members of the genus Ceromasia; as such, our findings are also a new host-parasitoid interaction for Mexico, increasing the number of genera of Tachinidae associated with sawflies previously cited by Richter & Kasparyan (2013). Other cases of parasitism of sawfly larvae attributed to Tachinidae in Mexico include Spathimeigenia (vibrissina) mexicana (Aldrich) (Diptera: Tachinidae) parasitizing larvae of Zadiprion falsus Smith (Hymenoptera: Diprionidae) in Michoacán (Méndez 1983); Lespesia postica (Walker) and v. mexicana (Diptera: Tachinidae) parasitizing larvae of Monoctenus sanchezi Smith (Hymenoptera: Diprionidae) in San Luis Potosí (Ordaz-Silva et al. 2014); and Chetogena (Diplostichus) nr. lophyri (Townsend) (Diptera: Tachinidae) reported as a parasitoid of Zadiprion rohweri Middleton (Hymenoptera: Diprionidae) in Coahuila (Smith et al. 2016).
Other parasitoids that emerged from N. omosus in this study included the ichneumonids Lamachus cushmani Khaleim & Ruiz-Cancino and Lamachus toluca Khaleim & Ruiz-Cancino (Hymenoptera: Ichneumonidae), previously described by Khaleim et al. (2019).
According to O'Hara (2005), C. auricaudata eggs are deposited onto foliage and do not hatch until they are ingested by a potential host. This reproductive strategy leads to a low probability of parasitism, but is much more efficient than other tachinids with more conventional strategies. Ceromacia auricaudata overwintered as a larvae within an overwintering N. omosus prepupae. In this study, average time from the collection of parasitized larvae to the emergence of adult parasitoids was 297.72 d (n = 11, 170–340 days). Coppel & Maw (1954) pointed out that adult C. auricaudata required 9 to 11 d to emerge from their primary host, Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae). Despite the ecological and behavioral similarity between diprionid and lepidopteran larvae, the use of sawfly larvae as potential hosts by tachinids has not been successful particularly from an evolutionary perspective, such that parasitism of diprionids by tachinids is apparently secondary (Richter & Kasparyan 2013). This behavior may explain why only 0.85% of N. omosus larvae were naturally parasitized by C. auricaudata in the study site.
We thank the Universidad Autónoma del Estado de México and the Secretaria de Investigación y Estudios Avanzados for financing this project as part of grant 4795/2019CIB. Thanks to Lynna M. Kiere for assistance in revision of our manuscript.