First record of egg sac predation of the fly Pseudogaurax cingulatus Sabrosky (Diptera, Chloropidae) upon spider Tetragnatha sp. (Araneae, Tetragnathidae) in northern Brazil

Pseudogaurax Malloch is a worldwide genus of Chloropidae with 33 species in the Neotropical region and 12 occurring in Brazil. The genus is well-known for the feeding habits of its larvae which attack egg masses and larvae of several arthropods, usually breeding in the egg sacs of spiders. In this study, we expanded the distribution of P. cingulatus to northern Brazil and recorded for the first time the species preying on Tetragnatha egg sacs. In addition, diagnosis, digital images and a distribution map are provided. Key-Words. Biodiversity; Oscinellinae; Geographic distribution; Taxonomy; Neotropic.


INTRODUCTION
Pseudogaurax Malloch is a worldwide genus of Chloropidae well-known for the feeding habits of their larvae. They usually attack egg masses and larvae of several arthropods, usually breeding in egg sacs of spiders (Sabrosky, 1966;Melo & Wheeler, 2009;González et al., 2016). Some species seem to be opportunists, utilizing a variety of hosts, however little is known about the life histories of several Pseudogaurax species (Barnes et al., 1992). There are 33 species of Pseudogaurax in the Neotropical region (Sabrosky & Paganelli, 1984;Sabrosky, 1989;Barnes et al., 1992;Melo & Wheeler, 2009). Of these, 12 species are recorded from Brazil (Riccardi, 2020), however, the knowledge of their distribution and biology are still scarce.
The species P. cingulatus Sabrosky occurs in the Brazilian territory with previous records to the states of São Paulo and Rio Grande do Sul (Sabrosky & Paganelli, 1984) and, so far, this species was reared only from the araneid spider Metazygia unguiformis (= Alpaida veniliae (Keyserling)) (Sabrosky, 1966).
Here we provide a new record of occurrence for P. cingulatus including another spider host. Also, a diagnosis of P. cingulatus is given along with digital images and a distribution map.

MATERIAL AND METHODS
The study was conducted at the "Agrolucas" farm localized in the municipality Boa Vista, Roraima state, Brazil (Fig. 1). Spider egg sacs were collected during an expedition on August 2019. These samples were collected manually and each adult spider and respective egg sac was placed into a plastic tube (1.5 and 2.0 ml), transported to the rearing laboratory at Instituto Nacional de  Pesquisas da Amazônia (INPA), where the egg sacs were kept until the emergence of the spiders or their predators/parasitoids. Among the material collected were egg sacs from Tetragnatha sp. (n = 3).
Voucher specimens of the spider (Figs. 2-4), its egg sacs (Fig. 5) and one Pseudogaurax cingulatus were deposited at the Invertebrate Collection of INPA and three P. cingulatus vouchers were deposited at the Museu de Zoologia da Universidade de São Paulo (MZUSP). Additional specimens of P. cingulatus deposited at the MZUSP were examined. The identification of the emerged flies was made based on the key to species and original description of P. cingulatus of Sabrosky (1966), then compared with all more recent descriptions of the Neotropical Pseudogaurax species (Sabrosky, 1989;Barnes et al., 1992;Melo & Wheeler, 2009).
Digital images of the chloropids and its puparium were taken using a stereomicroscope Leica M205C coupled to the software Las X and assembled in Helicon Focus 6 at the University of São Paulo and digital images of the spider and its egg sac were taken using a Leica DMC4500 digital camera attached to a Leica M205A stereomicroscope and combined by using the software Helicon Focus 5.3 Pro at INPA.
The protocol for preparing the female terminalia followed Riccardi et al. (2018). Pictures were treated with Adobe Photoshop CC and illustrations of the terminalia were vectorized with Adobe Illustrator CC. The morphological nomenclature followed Andersson (1977) and Cumming & Wood (2017). The digital map was produced in the online website SimpleMappr (www.simplemappr. net). Sabrosky, 1966 (Figs. 6-10)

Remarks:
The specimens from Fazenda Agrolucas differ from the type material only in the scutum longitudinal stripe. Sabrosky's (1966) illustration of P. cingulatus (Fig. 14, p. 123) shows a scutal longitudinal stripe thin anteriorly and slightly wider posteriorly. However, the specimen from Fazenda Agrolucas exhibits an anchor-like mark posteriorly (Fig. 7) which is considered here an intraspecific variation. On the other hand, the additional specimens examined from Ilha de Maracá have the scutal stripe as the type of P. cingulatus, but the dark marks on the legs are faded. Pseudogaurax nigrolineatus (Enderlein) is another Brazilian species which has a scutum similar to P. cingulatus, but the absence of dark spots on pleuron and legs completely yellow are features restricted to the former species (Sabrosky, 1966). Unfortunately, no information on the male terminalia of P. cingulatus is available. This organ could improve the species identification and help confirm the specimens identity. Biological note: Egg sac predator of the spider Metazygia unguiformis (= Alpaida veniliae (Keyserling)) (Araneidae) (Sabrosky, 1966) and Tetragnatha sp. (Tetragnathidae) (Figs. 1-4).

DISCUSSION
The Tetragnatha sp. egg sacs (n = 3) were collected on August 22, 2019 and 13 days after (September 4, 2019) four Pseudogaurax cingulatus specimens emerged. After emergency of the flies, four juvenile spiders emerged showing that P. cingulatus predation were not on 100% of the spider eggs. Barnes et al. (1992) observed that the predation of P. higginsi Sabrosky and P. mexoculatus Sabrosky in many Trichonephila clavipes (Linnaeus) egg sacs was also not total. The predatory behavior of Pseudogaurax larvae is unlike other insect groups, such as the wasp Tromatobia sp. (Ichneumonidae, Pimplinae) its larvae fully prey the egg sac of Araneus omnicolor (Keyserling) (Sobczak et al., 2012).
The geographic distribution of the Brazilian Pseudogaurax species is concentrated in the south-central region (states of Mato Grosso do Sul, Rio de Janeiro, São Paulo, Paraná, Santa Catarina and Rio Grande do Sul), except for two species -P. souzalopesi Sabrosky and P. trilineatus (Duda) -recorded in the northern region (states of Pará and Roraima respectively) (Rafael, 1991;Riccardi, 2020). However, the biased distribution of Pseudogaurax is due to the lack of studies of the chloropid diversity in northern and central Brazil. Our study, besides representing the third formal record of a Pseudogaurax species for the northern region, also reveal another host of P. cingulatus and some morphological variation within the species.