Hymenoptera “ Parasitica ” in the state of Mato Grosso do Sul , Brazil

A checklist composed of 105 species of parasitic Hymenoptera, which includes the non-aculeate Apocrita, recorded in the state of Mato Grosso do Sul (MS), Brazil, is presented. A new list, containing 153 genera obtained in recent surveys is also presented; out of these 131 are new records. The major knowledge gaps for these organisms in the State and the prospects for future studies for these organisms are discussed.

It is widely recognized, among the researchers of the area of invertebrates, that there is a lack of studies for the area in the Center-West region of Brazil, mainly in the state of Mato Grosso do Sul (Lewinsohn & Prado, 2002).Lewinsohn et al. (2005) pointed out the wide scientifi c knowledge gap that exists about biological diversity of biomes in Brazil.According to them, the Amazonian and Atlantic Forests are the best studied ones, whereas the Pantanal and Caatinga are the least known, as seen on recent inventories of species.Brandão et al. (2000) reported that after the Northeast region, the Center-West region is classifi ed as the second least known for the invertebrates.In the same study, the authors considered as inexistent the knowledge and collection status for parasitoid wasps (Hymenoptera), represented by the Ichneumonoidea, in the Pantanal area, a biome whose largest portion is in the state of Mato Grosso do Sul (MS).
The diffi cult access to the region in the past, as well as the low demographic rate and confl icts for land in the area are among the reasons that explain the gaps of knowledge in the region, facts that limited the visit of naturalists, mainly during the period of large expeditions which were common until the middle of the 20 th century.The entomological knowledge in Brazil was built based on specimens collected by those expeditions and by naturalists from Europe and USA, who concentrated their eff orts in the exuberant wet forests of this country, such as the Atlantic and Amazon Rainforests.Henry W. Bates in the state of Amazonas and Fritz Plaumann in the state of Santa Catarina, are two well-known examples of this phase.The greatest eff orts in sampling the fauna of the Center-West region occurred during the last years of the 19 th century, and were carried out by Herbert H. Smith, a naturalist from the USA, who spent four years in the state of Mato Grosso (Smith, 1922;Kunzler et al., 2011).Apart from the geological work he performed, Herbert Smith collected vertebrates, insects and fossils.Although he concentrated his studies in the Chapada dos Guimarães, he also carried out collections in other regions, including Corumbá (MS).During the 20 th century, a relevant expedition in the region was the "Royal Geographical Society" in Nova Xavantina, state of Mato Grosso, which brought a large contribution for the knowledge of Hymenoptera, in particular eusocial wasps (Richards, 1978).
With the establishment of research centers in the country, the Brazilian Entomology initiated a new phase.However, the concentration of these research centers in the South, Southeast and North regions were determinant for the lack of studies about the Hymenoptera parasitoids fauna in the Center-West region.Within this new context, the situation of the state of Mato Grosso do Sul was aggravated by its relative recent creation.
The Hymenoptera contain approximately 115,000 described species, being the third Order in number of species after Coleoptera and Lepidoptera.When considering the nondescribed species, it is possible that the Hymenoptera be the richest order in number of species (Gaston, 1991;Stork, 1991;Grissell, 1999).Gaston et al. (1996) estimated that the number of species could reach as much as three million.More conservative estimates forecast a number of species ranging between 600,000 and 1,200,000 (Grimaldi & Engel, 2005).
The traditional division of the Hymenoptera order into two suborders, Symphyta and Apocrita, is recognized to be artificial, since the former group composes an ancestral grade to the Apocrita + Orussoidea (Sharkey et al., 2012).The latter compose a clade that theoretically has a common ancestral of ectoparasitoid habit, from which originated the large diversity of habits currently known to be present on the Apocrita, such as endoparasitism, cecidogenesis, predation and eusocial behavior (Whitfield, 1992(Whitfield, , 2003)).
The Apocrita form a monophyletic group, which is also traditionally divided into two groups, the Aculeata (monophyletic) and the parasitoid wasps, also known as "Parasitica".A large proportion of phylogenetic studies point "Parasitica" as a paraphyletic group, being Aculeata a sister group of Evanioidea (Sharkey et al., 2012).Despite of the predominance of the parasitoid habit found in the non-aculeate Apocrita, some of the evolutionary lineages developed different habits, mainly the associations as and galls formations (Whitfield, 2003;Zaldívar-Riverón et al., 2007).
Among the Apocrita, Aculeata and parasitoids have approximately the same number of described species.A large proportion of the non-described species, however, is of Hymenoptera parasitoids (Sharkey, 2007).In the Neotropical region 24,000 species of Hymenoptera are known, out of which little less than half are of non-aculeate species (Fernández & Sharkey, 2006).According to Fernández (2006), there is at least 80,000 species in the Neotropical region, although there is not an estimate account for the region.
From the 89 families of Hymenoptera recognized by Sharkey (2007), 76 occur in the Neotropical region, out of which 41 are within the "Parasitica" series (i.e.Apocrita, except Aculeata) (Fernández, 2006;Sharkey, 2007).Among the groups with the poorest degree of knowledge for the Neotropical region are the Ceraphronoidea, Cynipoidea, Evanioidea, Platygastroidea and Chalcidoidea.Considering the number of species, the Ichneumonoidea can also be included within those groups (Fernández & Sharkey, 2006).
This work analyzed all families belonging to the "Parasitica" series, which includes all Apocrita but Aculeata ones (Chrysidoidea, Vespoidea and Apoidea).A checklist is presented for the species recorded for the state, since most consulted catalogues do not consider, or were elaborated, before the creation of the state of Mato Grosso do Sul (MS).Also, an unprecedented list, containing genera obtained through recent surveys is presented.
The locality of the occurrences of all species recorded for the state of Mato Grosso were designated, through the consultation to original descriptions and recent publications, in order to adequate its occurrence to the Brazilian current political division.The toponymies referring to localities within the current state of Mato Grosso do Sul are listed and the occurrences of species in those localities transferred.
A newly elaborated list of genera identified for the state was produced.The material examined was mainly collected in Pantanal area within the municipality of Corumbá, MS.The collection of this material was carried out under the Biota-MS Program (FAPESP 2010/52314-0) using Malaise traps.Material collected in Cerrado area within the municipality of Campo Grande (MS) was also identified.Also, material collected using Malaise traps by students from the Biological Sciences course at Universidade Católica Dom Bosco, under the supervision of Dr. Antonia Railda Roel, was identified.Additional material, deposited in the Coleção de Hymenoptera do Museu de Biodiversidade da Faculdade de Ciências Biológicas e Ambientais/Universidade Federal da Grande Dourados (MuBio-Hym), is also included in the list, only for the Braconidae.This material was collected with Möericke traps in the Parque Nacional da Serra da Bodoquena and in the Municipality of Porto Murtinho, both in the state of Mato Grosso do Sul (MS).In addition to the MuBio-Hym's collection, the collected material is also deposited at the Coleção Entomológica do Museu de Zoologia da USP (MZUSP), at the Coleção Entomológica do Depto.de Ecologia e Biologia Evolutiva da UFSCar (DCBU) and at the Coleção de Invertebrados da Universidade Católica Dom Bosco (UCDB).
The identification was carried out based on current literature and keys for each family in addition to consultations with specialists.The identification in genus level is justified by the high diversity of the group and the lack of revisions that enable a reliable identification at the species level.

RESULTS AND DISCUSSION
List of species.The list of species presented here includes only species with existing records in the literature which, given the precise information about the locality of their collection could be confirmed as belonging to the state of Mato Grosso do Sul.As much as 139 records for 105 species, belonging to 63 genera in 18 of the 41 known families of "Parasitica" Hymenoptera (Tab.I), were accounted for.This information was obtained from 51 references published between 1904 and 2013.In addition to information taken from the literature, six species of Ichneumonidae are being recorded for the first time in this work.
Taxonomic works are 22 and the remaining 29 were concerned with insects' natural enemies, mostly of economic relevance.The papers on natural enemies were published after the state of Mato Grosso do Sul was established; from all the taxonomic works available, only four were published before this date (Fig. 1).Ashmead (1904), for instance, contributed with 39 records of species of Chalcidoidea from a total of 59 records of this superfamily for the state of Mato Grosso do Sul.This valuable contribution was carried out based on specimens collected by Herbert Smith, most of them in Corumbá (MS) (see Fig. 2).Taxonomic works present more species number as expected, but works on natural enemies contain valuable information about the host-parasitoid association, useful not only for biological control programs, also for a better understanding of their interaction patterns at the ecological and evolutionary scale.
The checklist comprises a majority of species with previous record for the state of Mato Grosso, transferred here for the state of Mato Grosso do Sul.Hence, the number of species presented in this list exceeds the sum of the numbers in previous catalogs for this state.However, this number can be at least as three times as bigger considering the number of genera identified in the present study.
In order to avoid possible misunderstandings between the two states, the species with records of occurrence in both states are indicated in Table I.Therefore, all species without indication do not have records for the state of Mato Grosso.Records in other states and countries were not considered.
List of genera obtained from recent surveys.A total of 153 genera of "Parasitica" Hymenoptera were identified, out of which 131 (85%) are new records (Tab.II).These genera belong to 20 families, out of which seven are recorded for the first time in the state of Mato Grosso do Sul.The Ceraphronoidea is recorded here for the first time.Most of the identified material was collected in Pantanal area at the municipality of Corumbá.
The families Aulacidae, Diapriidae, Stephanidae and Trichogrammatidae were not found in the examined material.Platygastroidea was relatively commonly collected, although the family was not identified because the lack of keys to genera and specialists in Brazil.Therefore it is not present in the genera list.
Main research groups.The main research groups in Hymenoptera parasitoids are concentrated in the Southeast region.A list of these groups, together with their researcher leaders follows: ( 1 Carbonari carried out collections during two years in the Serra da Bodoquena (MS) collecting 1,243 specimens of the Hymenoptera parasitoids; however, the deposited material in the MuBio-UFGD's collection is identified only at the family level (Carbonari, 2009).Under-graduate and Graduate students at the Universidade Católica Dom Bosco (UCDB) have been carrying out a survey of the entomofauna in the region of Campo Grande (MS), under the supervision of Dr. Antonia Railda Roel with the collaboration of the research group headed by Dr. Angélica Maria Penteado-Dias.Those students are being trained in the collection, preservation and identification of Hymenoptera, mainly the parasitoid ones.
Publications, locally produced, containing records of parasitoid Hymenoptera species were carried out by Dr. Manoel Araécio Uchôa-Fernandes research group at UFGD, in Dourados (MS), whose main group of interest are the fruit flies (Diptera: Tephritoidea) and their interaction with eventual parasitoids.More recently, the research groups leaded by Dr. Fabrício Fagundes Pereira from UFGD and by Dr. Harley Nonato de Oliveira from Embrapa Agropecuária Oeste, both in Dourados (MS), are researching biological aspects of parasitoid species with a focus on their use as biological controllers.
Main holdings.As happens with the research groups, the main holdings in Brazil are mostly concentrated in the Southeast region of the country, such as: DCBU, São Carlos (SP); MZUSP, São Paulo (SP); UFES, Vitória (ES); FIOC, Rio de Janeiro (RJ); MNRJ, Rio de Janeiro (RJ).In the South region, the DZUP and DCMP are both in Curitiba (PR); and Tab.I. Checklist of Hymenoptera "Parasitica" species recorded in Mato Grosso do Sul State (MS), Brazil (1, species recorded in Mato Grosso and Mato Grosso do Sul States; 2, new record locality; 3, record in distribution map, municipality/locality not provided).
Efforts like the Biota-MS Program are primary to fulfilling this gap through surveys over this region.Considering the regions and vegetal formations, the need for surveys seems more evident in areas of Pantanal, Chaco and on the state's remaining forest fragments.Our results point that the best sampled is the Pantanal area that belongs to the Municipality of Corumbá (MS), containing even endemic groups.We believe that there is a need for the integration of local researchers with specialists from the different taxonomic groups in order to establish research lines in that knowledge area.
Research perspectives for the next ten years.By analyzing the publications, it can be observed that since the state's creation a significant increase occurred on the number of works involving this fauna.This increase could be even more significant if the country's main research groups on "Parasitica" and local researchers could reach integration.If the gaps being pointed out here could be filled up during the following years, it is possible that a large number of species could be known and described and the distribution of species already known could be extended throughout the state of Mato Grosso do Sul.With a better knowledge about the species and their distribution, it is possible that this group could become useful as a means for the evaluation of priority areas for environmental conservation, since they include a significant percentage of the biota and show quick response to environmental changes.

Fig. 1 .
Fig. 1.Number of publications with Hymenoptera "Parasitica" species recorded, grouped by decade.Works are classified according to its subject: taxonomy or natural enemies (see text).
Tab. II.List of Hymenoptera "Parasitica" genera identified from recent surveys in the state of Mato Grosso do Sul (MS), Brazil (*, new record for taxon in Mato Grosso do Sul State).