First record of the parasitoid wasp Lymeon sp. (Ichneumonidae: Cryptinae) associated with spider eggs-sac of Araneus vincibilis (Araneae: Araneidae) in Northeastern Brazil

31, 2020 (With 1 figure) Abstract Lymeon Förster, 1869 is a very large genus of the Cryptinae (Ichneumonidae) with predominantly Neotropical distribution where females attack small cocoons of various groups of insects and spider eggs-sac. In the present study, we report the first record the interaction between the parasitoid wasp Lymeon sp. (Ichneumonidae), with eggs-sac of spider Araneus vincibilis (Araneidae) in Northeastern Brazil. We observed that although the female of A. vincibilis cares for the eggs that were attacked by Lymeon sp, the wasp larva consumed about 80% of spider eggs, indicating that both maternal care and the physical barrier offered by the eggs-sac may not


Introduction
Ichneumonidae is one of the most species-rich families of Hymenoptera, with approximately 23,000 valid described species worldwide (Yu et al., 2012;Quicke, 2015). All members are endo or ectoparasitoids of other arthropods including larvae and pupae of Coleoptera, Hymenoptera and Lepidoptera (Camargo et al., 2015;Pereira et al., 2015;Morales-Silva et al., 2018). Some ichneumonid wasps like the Polysphincta genus-group (sensu Gauld and Dubois, 2006), are well known to act exclusively as koinobiont ectoparasitoid on various groups of spiders (e.g. Sobczak et al., 2017). On the other hand, some groups are predators of spider eggs where can consume up to 100% of the eggs (Villanueva-Bonilla et al., 2016).
Cryptinae is one of the largest subfamilies within Ichneumonidae with 397 recognized genera and some 4,500 described species (Yu et al., 2012;Quicke, 2015). They include taxa with a large range of biologies, some attack naked hosts (e.g. the wasp Gambrus incubator Linnaeus, 1758 is a parasitoid of pupae of moths of the family Zygaenidae); some are idiobiont ectoparasitoids of weakly to strongly concealed hosts; some Cyptinae has evolved as a pseudohyperparasitoid like the genera Gelis and Lysibia; a few attack pseudoscorpion egg masses (Phygadeuontini, Obisiphaga); and some are strictly predators within spider egg cocoons (e.g. Hydrata sordida Tschek 1870 reared from egg cocoons of the Lycosidae spider Pardosa pullata Clerck, 1757) (Schwarz and Shaw, 1999). In the Neotropical region there are few studies involving Cryptinae wasps acting as spider egg predators.
Lymeon Förster, 1869 is a very large genus of the tribe Cryptini within the subfamily Cryptinae with predominantly Neotropical distribution (Yu et al., 2012;Kasparyan, 2017). Currently, Cryptinae is represented by about 86 species of which four are found only in the Nearctic region (Townes and Townes, 1962). Species of this genus generally inhabit dense vegetation of forests where females attack small cocoons of various groups of insects and spider eggs-sac (Townes, 1970). The vast majority of studies with this genus describe new species where nothing is mentioned about the biology of the individuals (e.g. Kasparyan, 2004;Kasparyan and Ruíz-Cancino, 2008;Kasparyan, 2017).
Recently, in the forest reserve of the Hotel Remanso de Serra, Ceará State, Northeast of Brazil, we collected eggs-sacs of the spider Araneus vincibilis Keyserling, 1893 (Araneae: Araneidae) which contained cocoons of the wasp Lymeon sp. In this study we present the first record of predation of A. vincibilis spider eggs by the wasp Lymeon sp. We also present biological information about the spider host.

Material and Methods
This study was conducted in a Montane semi-deciduous tropical forest ( Figure 1A) located in the municipally of Pacoti, Ceará State, Brazil (4°13'30''S 38°55'22''W, altitude of 736 m). This area presents mean annual temperature of 21.5 °C and average precipitation of 1,524 mm.
We collected eggs-sacs of Araneus vincibillis on April 21, 2018 on a trail in the forest reserve of the Hotel Remanso de Serra during all the day. In field, the eggs-sacs were photographed and kept the in plastic recipients (8 × 10 × 10 cm) sealed with tulle fabric to obtain the adult wasps, along with the adult spider. In the Laboratory of Ecology and Evolution of UNILAB, adult spiders were preserved in alcohol for later identification. Under stereomicroscope, eggs-sac were carefully opened to verify the predation and accounting the eggs. The pupa of the Ichneumonidae were removed and kept in separate pots, sealed with tulle, until the adult wasps emerged from the cocoons. The voucher specimens of wasps were sent to the Coleção de Hymenoptera Parasitoides da Universidade

Results
Araneus vincibillis ( Figure 1D) wraps the eggs with silk inside a sheet used as a shelter. The sheet is then sealed with another layer of silk ( Figure 1B, C). The orbicular web is constructed from the shelter leaf with the eggs ( Figure 1B). We collected five eggs-sacs, of which one had Lymeon sp. larva feeding on the eggs (Table 1). In this open eggs-sac, we found five cocoons, where three of them had already emerged in the field, and two cocoons contained wasps still in pupae to emerge ( Figure 1C). In laboratory, after five days, the adult wasps emerged. To leave the eggs-sac, the adult wasp cuts a hole in the outer web layer that seals the leaf. The eggs-sacs can contain from 230 -331 eggs when not attacked. However, with the presence of the predatory wasps, 80% of offspring can be lost ( Table 1).
Only 15 spiderlings remained in the eggs-sac attacked by the wasp larvae.

Discussion
Spider eggs-sacs are subject to a wide variety of attacks of predators and parasitoids wasp of different families of Hymenoptera. In the present study, we report for the first time a Lymeon sp. wasp preying on spider eggs of A. vincibilis. To our knowledge, there is a unique record of Lymeon attacking spider eggs by the author Townes (1970); however, the manuscript has no details about the type of host spider. The larvae of Lymeon sp. observed in this study consumed about 80% of spider eggs. This is not unusual, as recorded for Cobb and Cobb (2004) about the attack of the wasps Gelis sp. (Ichneumonidae) and Baeus sp. (Platygastridae) on the spider eggs of Pardosa moesta Banks, 1892 (Lycosidae) and P. sternalis Thorell, 1877 (Lycosidae). In that study, some spiderlings might emerge because the number of larvae was low (Fitton et al., 1988;Schwarz and Shaw, 1999). On the other hand, other records show that the egg consumption could be complete, for example, Camera lunavenatrix Santos & Onody, 2016 (Ichneumonidae: Cryptinae) consumed 100% of the eggs of the spider Selenops cocheleti Simon, 1880 (Selenopidae) (Villanueva-Bonilla et al., 2016). The genera Tromatobia (Ichneumonidae: Pimplinae) and Aprostocetus (Chalcidoidea: Eulophidae) also consume 100% of the eggs when they attack the eggs-sac of the spider Araneus omnicolor Keyserling, 1893 (Araneidae) (Sobczak et al., 2012(Sobczak et al., , 2015. However, the observed percentage of eggs consumed in the present study should be taken with caution, since the amount of eggs inside registered eggs-sacs not predated showed high variation, indicating that other mortality factors occurred in the eggs-sac preyed by Lymeon. Morse (1988) mentions that spiders can experience strong pressure by predatory wasps that cause spiders to exhibit behaviors that diminish the attack on eggs. Females of Misumena vatia Clerck, 1757 (Thomisidae), for example, take care of the egg masses over much or all of the period between egg-laying and emergence of the young from the eggs-sac (Morse, 1985). In our study, we observed the female of A. vincibilis taking care of the eggs that were attacked by Lymeon sp. indicating that both maternal care and the physical barrier offered by the eggs-sac may not provide absolute defense against predators. Similar results were observed in the spider M. vatia eggs-sacs attacked by Trychosis cyperia Townes, 1962 (Ichneumonidae: Cryptinae) which can consume from 60-100% of the eggs even with the care of the spider female (Morse and Fritz, 1987).