Odonates from Bodoquena Plateau : checklist and information about endangered species

Here we provide an updated checklist of the odonates from Bodoquena Plateau, Mato Grosso do Sul state, Brazil. We registered 111 species from the region. The families with the highest number of species were Libellulidae (50 species), Coenagrionidae (43 species) and Gomphidae (12 species). 35 species are registered in the IUCN Red List species, four being Data Deficient, 29 of Least Concern and two species being in the threatened category. Phyllogomphoides suspectus Belle, 1994 (Odonata: Gomphidae) was registered for the first time in the state.


Introduction
Insects are arthropod group with largely unknown distribution patterns (Diniz-Filho et al. 2010), due to their high species richness, difficulties related to sampling and lack of taxonomic experts.Applying all of these conditions, odonates (Insecta: Odonata) constitutes an important group that play a major role as predators, with several insects making up a large portion of their diets.This group is also a good indicators of water quality, with their nymphs being an important link in food chains for fish and other aquatic vertebrates and serve as an inspired subject for artists, naturalists and collectors (Abbott 2015).
Even with important taxonomists in the recent Brazilian history, odonates are still poorly described and its distribution is deficiently known in the Neotropical region (Kalkman et al. 2008).Local inventories are recorded to several parts of Brazil like São Paulo (Costa et al. 2000), Espirito Santo (Costa & Oldrini 2005), Rio de Janeiro (Anjos-Santos & Costa 2006), Goiás and Distrito Federal (Nóbrega & De Marco 2011), Minas Gerais (Souza et al. 2013), and Rio Grande do Sul (Renner et al. 2016).In Mato Grosso do Sul, state originally covered by Cerrado, Pantanal, Atlantic Forest and Chaco vegetation, 198 odonatan species were registered (Rodrigues & Roque 2017).Despite this number, information gaps are recognized from many areas in this state (Vianna & De Marco 2012, Rodrigues & Roque 2017).
Bodoquena Plateau is a threatened area in the Mato Grosso do Sul state because of the broad conversion of natural areas to pastures and croplands (Roque et al. 2016).In the last five years, several research projects about biodiversity and the ecology of aquatic insects have been developed in Bodoquena Plateau, (e.g.LTER Planalto da Bodoquena, Dragonflies of Serra da Bodoquena Project and Observagua Project).These projects have promoted a great opportunity for extending sampling effort of aquatic insects, especially for odonates (e.g.Koroiva et al. 2016, Rodrigues et al. 2016a, Rodrigues et al. 2016b, Valente-Neto et al. 2016).Until 2011, about 68 Odonata species were registered to Bodoquena Plateau; a number that was considered underestimated because of the broad unsampled area (Dalzochio et al. 2011b).Therefore, even with the publications of checklists (Dalzochio et al. 2011a, Dalzochio et al. 2011b, Rodrigues & Roque 2017), the amount of information generated by these new sampling efforts and visits to museums demand an update.
Here, we provide an updated checklist of the odonates from Bodoquena Plateau, including species records from recent sampling efforts, from the literature, and from specimens deposited in the Reference Collection of the Federal University of Mato Grosso do Sul (CEUFMS).We also provide information about endangered species from the IUCN Red List (IUCN 2016), which is fundamental for updating the status of Brazilian species, as recently emphasized in the 1 st Meeting of the Latin American Odonatological Society -SOL.

Sources of data
We used different sources of information to produce the checklist, including samplings (from 2011 to 2016), previous available records on literature and information collected in zoological reference collections of the Mato Grosso do Sul state.For each source, we searched for names and geographic coordinates of the locations.For records that did not have latitude and longitude values, geographic coordinates of the centroid of the place where the site is located.

Sampling in study region
All the sampling sites were located within Bodoquena Plateau region (21º08'02" to 20º38'26"S and 56º48'31" to 56º44'28"W).The Bodoquena Plateau is located in the mid-southern portion of Mato Grosso do Sul State, including the cities of Bodoquena, Bonito and Jardim.The region is characterized by a mountain chain, with altitudes varying between 450 and 800 m.The climate is temperate humid with hot summers and two well-defined seasons.The average annual temperature varies between 20 and 22ºC and annual rainfall varies between 1300 and 1700 mm.The hydrography of the region is characterized by limestone, rivers with high alkalinity and low turbidity.Its tributaries are part of the Paraguay River watershed (PCBAP 1997).
Bodoquena Plateau has both areas of the Cerrado (Brazilian savanna) and Atlantic Forest biomes.This region is an important ecological corridor for biodiversity and one of the most important areas of Ecotourism in Brazil (Klein et al. 2011).Considered a priority area for conservation by the Brazilian Ministry of Environment (MMA) (Brasil 2016), the region is currently threatened by inadequate exploitation of its resources and the progressive agricultural expansion.
The dataset used in this checklist included 85 lotic environments (Figure 1) sampled during the period between 2011 and 2016.These samples were concentrated on adults from Odonata and were performed during Ph.D studies (Valente-Neto 2015, Rodrigues 2016), Long term ecological research in the Bodoquena Plateau (LTER-Serra da Bodoquena), Dragonflies of Serra da Bodoquena Project and Observagua Project.The sampling method used handhold insect nets, in sunny days, during the peak time of Odonata activities (between 09:00 h to 16:00 h).The collection authorization process was issued by IBAMA, through SISBio system under the number 41313-3 and 54386-1.All specimens collected were deposited in the Reference Collection of the Universidade Federal de Mato Grosso do Sul (CEUFMS), afterwards determined in laboratory according to Garrison et al. (2006Garrison et al. ( , 2010)), Heckman (2006Heckman ( , 2008) ) and Lencioni (2005Lencioni ( , 2006)).For the systematics classification, we followed Dijkstra et al. ( 2014) and for scientific names and followed the synonymic list of Garrisson & von Ellenrieder (2016).In the laboratory, dragonflies were analyzed under Zeiss Discovery V20 stereoscope and recorded with an AxioCam Icc 5 Microscope Camera.For capturing and editing images, we used the software Zen 2-2011.

Data analysis
We estimated the sampling accuracy of sampling sites with incidence-based non-parametric estimators: Chao 2, Jacknife 1 and Jacknife 2. Non-parametric methods have better performance compared to others estimators for aquatic insects (Melo & Froelich 2001).These analyses were performed with EstimateS version 9.1.0software (Colwell 2013).We set 1000 repetitions to calculated mean values with confidence intervals of 95%.

Literature and reference collections information
Aiming to improve our list of species, we used online available databases to find registers of Odonata species from Bodoquena Plateau, specifically Web of Knowledge (which includes the main journals of world), Scielo (which include the main journals of South America) and Google Scholar.We did the search on general keywords like "Odonata", "dragonfly" or "libélula" ("Dragonfly" in Portuguese) in combination with "Mato Grosso do Sul", "Bodoquena Plateau" or "Serra da Bodoquena" ("Bodoquena Plateau" in Portuguese).Souza (2003), Dalzochio et al. (2011a) and Dalzochio et al. (2011b) provided additional information about registers of Odonata species ("Reference" in Table 1).
In addition, we analyzed the deposited specimens from two important Zoological collections of Mato Grosso do Sul state: Reference Collection Universidade Federal de Mato Grosso do Sul (CEUFMS) and Biodiversity Museum of Universidade Federal da Grande Dourados (UFGD).CEUFMS provided additional register besides that found in the project samples or in literature ("CEUFMS" in Table 1).
The Odonata list records from the Bodoquena Plateau are presented in Table 1.We added another fourty-four species that were registered in the literature (34 species) or deposited in the Reference Collection of the Federal University of Mato Grosso do Sul (10 species).Thus, we have considered the presence of 111 Odonata species.We recorded for the first time the presence of 42 species from Bodoquena Plateau (24 anisopterans and 18 zygopterans).In this inventory list, 35 species are registered in IUCN red List (IUCN 2016), with four being in Data Deficient (DD), 29 in Least Concern (LC) and two species are in threatened categories, Elga newtonsantosi Machado, 1992 like Critically Endangered (CR)  The families with the higher number of species were Libellulidae (45.05%),Coenagrionidae (38.74%) and Gomphidae (10.81%) (Table 2).The most speciose genus were Argia, Micrathyria and Erythrodiplax, represented by twelve, ten and nine species, respectively.The endangered species classified in the IUCN Red List, Elga newtonsantosi and Micrathyria pseudhypodidyma, were registered only in two and one sampled sites, respectively.

New record
We found that Phyllogomphoides suspectus Belle, 1994 represents a new records of odonate species for Mato Grosso do Sul state, compared with the list published by Rodrigues & Roque (2017).The genus Phyllogomphoides Belle, 1970, is composed of 45 species in the Neotropical Region, 29 of these in South America (Belle 1994).Phyllogomphoides suspectus Belle, 1994 has a distribution recorded by Belle (1994) andvon Ellenrieder (2009a) and is considered exclusive to Brazil.The species distribution ranges from Rondonia to the Mato Grosso with specimens found in Rio Ouro Preto and Sinop, respectively (Belle 1994), around 800 km northwards of our sampling site.
We collected one male adult of Phyllogomphoides in the rural area of Bonito, Mato Grosso do Sul state, Brazil.This specimen was identified as P. suspectus (Figure 3a), according to the characteristics indicated by Belle (1994) and Heckman (2008), like spines along ventral tergal margins of abdominal segment 7 small and largely black (Figure 3b), the cerci, in dorsal view, with forcipate shape (Figure 3c) and with a hatchet-shaped inferior protuberance near the base (Figure 3d) and anterior genital hamules without a posterior black hook (Figure 3e).

Discussion
Inventories promote skeletal support in many fields, including biogeography, population and community ecology.Such data establish a baseline of biodiversity and ecological information, which allow their application in conservation strategies.The list of species shown here represents 55.77% of all species recorded for Mato Grosso do Sul (199 species) (Rodrigues & Roque 2017, Rodrigues et al. 2016a), and is a significant advance in comparison with previous accounts (Souza 2013, Dalzochio et al. 2011a, Dalzochio et al. 2011b), increasing by 42 odonate species list of Bodoquena Plateau region.
Considering that insect inventories, especially those of very speciesrich taxa in tropical region, are often incomplete (Gotelli & Colwell 2001), our results show that accumulation curves have not tended to stabilize.The reference source emphasize this result, because there are 44 species registered by Souza (2003) and Dalzochio et al. (2011aDalzochio et al. ( , 2011b) ) and not sampled by the projects.Other reasons for the high number of non-sampled species are the large territory of the Bodoquena Plateau and many of these species had been collected in the southern part, region not sampled by the projects.Furthermore, the projects sample sites, like the other previous studies (Souza 2003, Dalzochio et al. 2011a, Dalzochio et al. 2011b), focused on lotic system rather lentic ones, such as lakes and reservoirs.Thus, future inventories in lentic environments and with other sampling methods (e.g.visual record, Malaise trap, light trap) may still increase the species records for Bodoquena Plateau, highlighting the importance of this region, which lies into two highly threatened biomes.
Our new records extend the register of distribution to many species, information considered critical for the definition of their threatened status (IUCN 2016).When considering the IUCN red list, the Odonata species of the Neotropical region have a high number of species listed as Data Deficient (Clausnitzer et al. 2009) or without status definition.In this study, 2/3 of the species do not have classification, which reinforces this information gap related to conservation for the group.Regarding the species classified as threatened, Elga newtonsantosi and Micrathyria pseudhypodidyma have limited information available about their distribution (number of locations), population size, and ability to survive in reduced habitat (von Ellenrieder  ).From a conservation perspective, the knowledge about threatened species distributions is crucial for biodiversity management, especially for the development and implementation of conservancy plans.Thus, both of them shall be targets of governmental protection plan, as required in the Brazilian legislation on endangered species.In summary, this study highlighted the Bodoquena Plateau as an important habitat for odonates, including species classified as threatened.

Figure 1 .
Figure1.Sampling locations in the Bodoquena Plateau region.On the north is the municipality of Bodoquena; on the middle is the municipality of Bonito and on the south is the municipality of Jardim.

Figure 2 .
Figure 2. Accumulation curves for observed and estimated number of species collected at 85 sample points.The estimates were calculated with the estimator Chao 2, Jackknife 1 and Jackknife 2. Black diamonds = number of species observed (est); Black squares = Chao 2 richness estimator; Grey circles = Jackknife 1 richness estimator; Grey stars = Jackknife 2 richness estimator .All curves are plotted form the means of 1000 randomizations of sample accumulation order.

Table 1 .
Inventory list of Odonata species from Bodoquena Plateau with information about endangered species (IUCN).CR = Critically Endangered, VU = Vulnerable, LC = Least Concern, DD = Data Deficient; *, first record to Bodoquena Plateau.

Table 2 .
Number of Odonata species collected per family in the Bodoquena Plateau.