Hymenoptera fauna, with emphasis on Ichneumonidae from an area of Caatinga in Northeast Brazil

The objectives of this study were to carry out a survey of families of Hymenoptera, with emphasis on Ichneumonidae, in an area of Caatinga, and register the occurrence of new species, if any, for the biome. Samples were taken with Malaise traps between September and November 2008 in a native area of vegetation of Serra do Lima, municipality of Patu, Rio Grande do Norte, Brazil. 7,562 hymenopterans, from 11 superfamilies and 31 families, were collected. The most abundant superfamilies were: Chalcidoidea (2,887 specimens / 38.33% of the total), Platygastroidea (1,572 / 20.87%) and Vespoidea (1,131 / 15.02%) which constituted more than 70% of the captured hymenopterans. A total of 160 specimens of Ichneumonidae from 17 subfamilies were sampled, of which four are new records for Rio Grande do Norte: (Lycorininae, Nesomesochorinae, Phygadeuontinae and Tryphoninae). Altogether, 26 genera were recognized, with 16 new records for the state. Cryptophion espinozai Gauld & Janzen (Campopleginae) and Labena marginata Szépligeti (Labeninae) were registered for the first time in Caatinga. The obtained data demonstrate a considerable diversity of the studied groups in this area and also affirms the necessity of additional studies to establish the richness of this fauna in a more extensive and conclusive way.


EntomoBrasilis 13: e0874 (2020)
n the order Hymenoptera, there are about 115 thousand described species, but it is estimated that this number can be greater than 250 thousand (Hanson & Gauld 2006). In the Neotropical region, 21 superfamilies and 76 families of Hymenoptera have been found (Fernández 2006), and 70 families have been cataloged for the Brazilian territory (Penteado-dias & BraGa 2002;oliveira et al. 2020). Although the fauna of this order is estimated to have about 70 thousand species for Brazil (Melo et al. 2012), only 10,456 species, distributed in 1,610 genera have been registered until now (oliveira et al. 2020).
Among the families of Hymenoptera, Ichneumonidae is one of the most prominent, as it is one of the largest families in the animal kingdom, with about 25 thousand described species, and an estimate of more than 100 thousand species (Gauld et al. 2002;Yu et al. 2016). In general, Ichneumonidae consists of species of solitary parasitoids; most species with known biology attack larvae and pupae of Lepidoptera, Coleoptera and Hymenoptera (Gauld 1991). Due to their parasitoid habit, ichneumonids have potential importance for the biological control of holometabolic phytophagous insects, which can act as agricultural pests.
The only inventory of Hymenoptera families in Caatinga areas of Rio Grande do Norte (RN) was carried out by Fernandes et al. (2014a), who verified the presence of 36 families. Regarding Ichneumonidae, the little information available for the state is from the lists and descriptions of the species santos & aGuiar 2013;Fernandes et al. 2014b;sHiMBori et al. 2014). In Brazil, this family is represented by 1,019 species and 233 genera, however, for RN only eight species have been registered so far .
In many areas of Caatinga biome, including mountainous regions and its slopes, which form microclimates within the semiarid environment, there is no information on the diversity of Hymenoptera. The studies carried out in these regions may present taxa, which are still undiscovered, in addition to the ecological importance of the information. Thus, the objectives of this work were to carry out a survey of families of Hymenoptera with emphasis on Ichneumonidae, present in an area in Caatinga, located in Serra do Lima, Patu, RN, and record any occurrence of new species in the studied area.

MATERIAL AND METHODS
The studied specimens were collected using two Malaise traps about 100 m apart, installed at Sítio Miranda (6º6'18" S / 37º37'41" W, 248 m above sea level [asl]), in Serra do Lima, municipality of Patu, RN, Brazil. The traps remained active throughout the collection period.
A monthly sampling was carried out for the months of September, October and November 2008 (dry season). Despite being located in the semiarid region, the average annual temperature in this region is 26.6 ºC, with a relative humidity of 66% and rainfall of 873 mm (EMPARN 2016). During the installation of traps, despite the drought period, some plants had abundant green leaves, especially those situated near water bodies ( Figure 1).
Hymenoptera families were identified according to Fernández & sHarkeY (2006). Subsequently, the status of superfamily and family nomenclature was updated according to aGuiar et al. (2013). For bees, the classification used by Melo & Gonçalves (2005) was maintained, considering all bees as Apidae sensu lato. Subsequently, Ichneumonidae were identified in a subfamily according to Palacio & WaHl (2006), and Gauld (2006). The Cryptinae specimens had their nomenclature updated based on the recent proposal by santos (2017). Each subfamily was subsequently identified in genera based on specialized literature for each group.
For a preliminary comparison of the sampled material, the richness of families obtained from the two areas of the Caatinga biome was analyzed: Mossoró -RN (5º01'25" S / 37º22'57" W, 59 m asl) (material previously collected by Fernandes et al. 2014a) vs. Patu (present study). For this, a family rarefaction curve was elaborated based on the number of individuals sampled in each study. The rarefaction curves were obtained by the bootstrap process with resampling, to obtain a confidence interval for family richness, similar to that proposed for species by Moreno et al. (2008). Bootstrap analyses were calculated with EstimateS Win9.1 software (colWell 2013), using 2,000 randomizations and 95% of confidence interval.
The analyzed material was deposited in the Entomological Collection of the Laboratorio de Sistemática e Bioecologia de Parasitoides e Predadores (LRRP) of the Instituto Biológico, Ribeirão Preto, São Paulo, Brazil (NW Perioto, curator).
The distribution map was created using SimpleMappr online software (sHortHouse 2010).

RESULTS
Were obtained 7,562 specimens of Hymenoptera belonging to 11 superfamilies and 31 families (Table 1).
Although the quantity of specimens captured decreased over the sampling time, 2,867 specimens (September), 2,745 (October) and 1,950 (November), the richness remained constant with 27 families. Platygastridae was the most abundant family in all sampled months, with 667 specimens collected in September, 675 in October and 230 in November.
The richness of the families captured in Mossoró -RN (by Fernandes et al. 2014a) was higher than the present study, which can be seen in Figure 2.
In all, 37 families were captured at the studied areas, 30 of them in both localities. Eucharitidae, Leucospidae, Sclerogibbidae, Proctotrupidae, Rhopalosomatidae and Pergidae were collected only in Mossoró and Sphecidae only in Patu.

e-ISSN 1983-0572
Hymenoptera fauna, with emphasis on Ichneumonidae from…  The 160 collected specimens of Ichneumonidae belong to 17 subfamilies and 26 genera, of which 16 are new records for RN (Table 2). Of the most abundant superfamilies, aGuiar et al. (2013) reported the existence of approximately 23 thousand species of Chalcidoidea in the world however, this group is still relatively less studied. Approximately 12 thousand species of insects are registered as their hosts which demonstrates the huge potential for parasitism and its importance as a factor of biotic mortality in different environments. Grissell & scHauFF (1997) pointed out that groups of insects belonging to Chalcidoidea have great diverse biological habits, with at least 14 different life strategies, including mainly solitary, gregarious, hyperparasitoid and polyembryonic habits.
As for Platygastroidea, the superfamily is composed only of Platygastridae [in the classification adopted in the present study, aGuiar et al. (2013)] however, in most inventories, it is still common to be divided into Platygastridae and Scelionidae (traditional classification).
Despite their abundance, and being frequently sampled, it is important to point out that the majority of Hymenoptera surveys carried out in Brazil have not taken into account the specimens of Vespoidea, Apoidea and Symphyta. The data obtained indicate that the diversity of Caatinga biome has not yet been studied for these groups, therefore further studies regarding the fauna of Hymenoptera are necessary in this region, and a deeper study of the already collected material, identification of genera and species are necessary as well.
Regarding the habits, 26 families of parasitoid hymenopterans sampled in this study is similar to that reported by   (Perioto et al. 2008;Pádua & zaMPieron 2012, respectively).
Some long-term sampling in the same collection area proved to be effective for capturing uncommon Hymenoptera families in the surveys with Malaise traps, such as Chrysididae, Dryinidae, Monomachidae, Pelecinidae and Sclerogibbidae (lucena et al. 2012;versuti et al. 2014;Perioto et al. 2016;Fernandes et al. 2017).
For the Ichneumonidae fauna, 14 subfamilies and 13 genera were previously registered for the Caatinga biome in RN (sHiMBori et al. 2014). Thus, four subfamilies are registered for the first time in this biome for the state of RN (Lycorininae, Nesomesochorinae, Phygadeuontinae and Tryphoninae).
As for the genera, Cryptophion, Xanthocampoplex  Fernandes et al. 2019); the other genera mentioned above are also associated with this biome for the first time.
Thus, from these results, 18 subfamilies and 30 genera were registered in the Caatinga biome, specifically in the state of RN. After adding these results with those of sHiMBori et al. recorded the occurrence of 100 genera for Espírito Santo (in areas of Atlantic Forest). In the present study, although the sampling is done only for three months, the material collected demonstrates a considerable diversity of Ichneumonidae in this biome, as well as in other biomes mentioned earlier. It is possible that, with greater sampling effort and with deeper taxonomic studies, this diversity may increase considerably in coming years.
We must also take into account that so far only eight species of Ichneumonidae have been registered for RN ). In the present study, the species Cryptophion espinozai Gauld & Janzen (Campopleginae) and Labena marginata Szépligeti (Labeninae) were recognized and are recorded for the first time in the Caatinga biome.
In Brazil, C. espinozai (Figure 3) has been registered only in Minas Gerais and São Paulo (Gauld & Janzen 1994;onodY et al. 2013;). The distribution of species L. marginata in the Brazilian territory was unknown. In its original description by széPliGeti (1914), it was only mentioned that the species L. marginata had been collected in Brazil, without pointing out the place of collection. Thus, the present study also mentions the place of occurrence of this species in Brazil for the first time.
The results presented in this study demonstrate that the areas of Caatinga biome are home to a substantial diversity of Hymenoptera families that is similar to other Brazilian biomes, and that this diversity still needs to be better sampled and studied, which may reveal the presence of unknown species. Thus, it is essential to develop more studies in this biome to know the diversity of this group of insects in this environment that is still little explored.