Occurrence of the Parasitic Fly Philornis torquans on Fledglings of the Rufous-Fronted Thornbird (Phacellodomus rufifrons) in Southeast Brazil Open Access

Philornis is a genus of Muscidae (Diptera) with 49 species distributed in the neotropical region (De Carvalho 2005). These insects parasitize birds, and the larvae have three main levels of association with their hosts: living in the birds' nests with coprophagous habits, living in the nest with semihematophagous habits, or becoming intradermal parasites on the nestlings (Löwenberg-Neto 2008). Obligatory parasitism is attributed to about 20 species (Dudaniec and Kleindorfer 2006), and prevalence can reach up to 100% of nests in certain regions (McNew and Clayton 2018). The parasite plays a prominent role in the population dynamics of various bird species because the flies can severely affect the fitness and survival rate of the offspring (Kleindorfer and Dudaniec 2016; Fessl et al. 2018; McNew and Clayton 2018). In the Galapagos Islands, for example, parasitism by Philornis downsi, an invading fly with high prevalence of infection (64–100%), may account for about 55% of losses of finch nestlings (Kleindorfer and Dudaniec 2016).

To date, Philornis larvae have been described in association with more than 130 species of birds, with the more generalist flies in the genus able to invade the nests of different bird species (Teixeira 1999; Löwenberg-Neto 2008; McNew and Clayton 2018). Although Philornis is a relatively common parasite, the habits and ecology of its larvae are known only for about half the described species, and there is relatively little information on their relationship with the host.

Birds of the Phacellodomus genus are common in southeast Brazil (Ridgely and Tudor 1994). Although Phacellodomus is one of the main hosts of Philornis parasites (Antoniazzi et al. 2011), there is no information on the association Philornis–Phacellodomus in the state of Minas Gerais, Brazil. Therefore, the objectives of the present work were to report the presence of Philornis at the study area, provide data on the biology of this parasitic fly, which is scarce in the literature, and warn for the possible impact it may cause in the bird population. At the end of April 2015, two nests of the Rufous-fronted Thornbird Phacellodomus rufifrons, containing three and five chambers, were collected in the rural area of the municipality of Pedro Leopoldo, Minas Gerais, Brazil (19°37′S, 44°2′W). The first nest (Fig. 1A) contained four young feathered birds near to the time of fledging, probably around 20 d old, as Phacellodomus rufifrons leave their nests around 22 d after hatching (Skutch 1969). While the nests were being disassembled to search for insects, an adult fly was collected from between the sticks, with its wings in the distension and stiffening period, indicating recent emergence from the puparium. The fly was transferred to a container, taken to the laboratory, and identified as a female Philornis torquans according to Couri (1989).

The second nest contained an adult bird and three 4–6-cm-long nestlings, suggesting that these birds were less than 7 d old (Skutch 1969). The nestlings were taken to the laboratory, kept in an artificial nest mounted with medical bandage tissue in a temperaturecontrolled environment (28 ± 2 C), and fed with moistened chick food. The three siblings had multiple subcutaneous larvae in several regions of the body such as head, throat, wings (mainly near the joints), chest, abdomen and uropygial area. One of the siblings (nestling 3) was heavily parasitized, especially on the head and left dorsal side, which had two clusters of larvae with at least 15 larvae in each wound (Fig. 1B, C). Nestling 3 died the day after nest collection, and 53 larvae (Fig. 2A) of various sizes (Table 1) left the wounds and were collected.

On day 2 after nest collection, the larvae that were parasitizing the other two siblings (nestlings 1 and 2) were removed by mechanical compression of the infested sites with the aid of forceps. Nestling 1 had seven larvae removed from the dorsal region of the head near the beak (one larva), uropygial region (one larva), left wing (one larva), and right wing (four larvae from the same wound). Nestling 2 had 11 larvae removed (Table 1). One wound on the left wing contained five larvae, and there were five wounds on different regions of the head, one with two larvae and four with one larva each. In total, 71 larvae were collected from the nest, with nestling parasitism varying from 7 to 53 larvae (mean=23.7±25.5 larvae/nestling). Larvae size varied from 3 to 15 mm (Table 1), and only 1 (3 mm long) was a second instar; the remaining 69 were third instars (2 of them, 4 and 5 mm in length, were still encapsulated with the second-instar cuticle).

Out of 71 larvae recovered, 37 were stored in 70% alcohol, and 34 third instars were transferred to flasks containing wood shavings and kept in an incubator at 28±2 C temperature and 60±5% humidity. All 34 larvae placed in the incubator developed into pupae (Fig. 2B) and later into adult flies (Fig. 2C), 21 males and 13 females, which were all identified as Philornis torquans. The pupation time lasted from 9 to 13 d (median=11 d, quartile 1=11 d, quartile 3=12 d), and pupae were aggregated in groups of up to 10 held together by a spongy white substance and small pieces of material, which together formed a frothy cocoon (Fig. 2B). This probably provided the pupae with protection against parasites, especially microhymenopterans (Teixeira 1999).

Phacellodomus rufifrons is a common bird species in the region (Ridgely and Tudor 1994). Their nests are built using several sticks measuring 10 to 30 cm to create several stacked modules (from one to more than five independent chambers) that resemble a tower (Fig. 1A; Skutch 1969). Each nest is a small ecosystem, as it can accommodate several groups of arthropods, such as Coleoptera, Orthoptera, Hemiptera, Lepidoptera, Diptera, and Arachnida, as well as other bird species.

Parasitism by subcutaneous larvae of Philornis spp. can lead to retarded nestling development or mortality (Kleindorfer and Dudaniec 2016). The level of parasitism by Philornis torquans previously reported ranged from 3.6 to 13.4 larvae per nestling (Manzoli et al. 2013). This is in line with the level of parasitism seen for nestlings 1 and 2; however, it is considerably lower than the parasite burden seen in nestling 3. Antoniazzi et al. (2011) estimated that the chances of death double with 10 parasitizing larvae. However, the number of parasites does not equal impact, and several other factors are also involved, such as host mass, host species, Philornis species, the area of the body infested by larvae, and even climatic conditions (Dudaniec and Kleindorfer 2006; Kleindorfer and Dudaniec 2009; Antoniazzi et al. 2011). In the present study, the impact of the parasitism was not assessed, but it is of note that no dead nestlings were found in any of the nests at the time of collection.

Based on the characteristics described by Skutch (1969), we estimated the age of nestlings from nest 2 as less than 7 d old. This is in accordance with previous findings showing that the nestlings of several bird species between 2 and 11 d old are more susceptible to Philornis infestations (Dudaniec and Kleindorfer 2006; Quiroga and Reboreda 2012). In addition, ecological data collected in the present study corroborated Saravia-Pietropaolo et al. (2018), who confirmed the production of the cocoon by Philornis torquans and described pupal periods of 8–15 d. However, our results diverged from other descriptions that did not attribute the presence of a frothy cocoon to Philornis torquans (Ferrar 1980; Teixeira 1999), and described pupation periods of 5–6 d (Teixeira 1999).

Under laboratory conditions, Philornis torquans females lay clutches of 1–148 eggs (Saravia-Pietropaolo et al. 2018). We deduced that the 71 larvae found in our study came from at least two clutches of eggs laid at different times. The earlier clutch was represented by third instars at 9–18 mm and the later clutch by second and third instars varying from 3 to 7 mm.

Philornis torquans has been previously described as a subcutaneous tissue feeder of several bird species (Teixeira 1999). In Argentina, Philornis torquans was recorded as an ectoparasite of more than 30 bird species with a preference for species of the genera Phacellodomus and Pitangus (Antoniazzi et al. 2011; Manzoli et al. 2013). Phacellodomus rufifrons is not considered to be an endangered species in Brazil, and the presence of four nestlings in an advanced stage of development from nest 1 suggests the association between Philornis and the Rufousfronted Thornbird in the study site is not as deleterious as the one observed for Philornis downsi and many Galapagos bird species (Kleindorfer and Dudaniec 2016; McNew and Clayton 2018). However, a more detailed study should be conducted to determine the prevalence of this parasitism and the potential impact it might have on the avian populations in Southeast Brazil.

The work was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais, Conselho Nacional de Desenvolvimento Científico e Tecnológico and Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular. Experimental procedures were approved by the Ethics Committee in Animal Experimentation at Universidade Federal de Minas Gerais (115/2011) as part of a larger research project that investigates the presence and behavior of triatomine vectors in nests of Rufous-fronted Thornbirds.