New occurrences of dragonflies in the Atlantic Forest fragments of Santa Teresa, Espírito Santo, Brazil

One of the greatest obstacles to biodiversity conservation is the lack of information to prioritize efforts on practical actions. This lack of information comes mainly from absence of inventories in many areas where few groups have reasonably complete databases. The distribution of the dragonfly fauna of Brazil is little known only 29% of the Brazilian territory presents data about the richness of Odonata. In this contribution, a database of Odonata species of Santa Teresa Municipality was built, Espírito Santo State, Brazil. The database has 627 specimens registered, 77 species distributed in eight families and thirty-eight genera, forty of these species are common, one endemic of the State of Espírito Santo, and nineteen endemic of Brazil. In relation to the measure of conservation, four species are present in the category Insufficient Data (DD), one present in the Nearly Endangered (NT) category, three species in the Vulnerable category (VU) and one in the category In Danger (EN). Twentyfive species are considered new occurrences for the city. These results suggest that the fauna of the studied region deserves attention and points to the interest in implanting future conservation units in the region of Santa Teresa municipality.


Introduction
The Atlantic Forest is one of the most important regions for world's biodiversity conservation, thanks to a combination of high species richness and endemism, combined with the advanced state of degradation. According to data from the Fundação SOS Mata Atlântica (SOS Atlantic Forest Foundation) and Instituto Nacional de Pesquisas Espaciais (INPE -National Institute of Spacial Research), in 2008, well preserved (over 100 ha) forest fragments totalled 7,91% of the original area of the Atlantic Forest -showing up a point of priority for conservation of the biodiversity (Myers et al., 2000;Mittermeier et al., 2004).
One of the biggest obstacles for conservation is the lack of information (knowledge of the distribution and abundance of species) that allow the implementation of efforts and priorities in management practices (Pimm et al., 2001). Many parameters are used as criteria for the selection of areas of priority for conservation, such as species richness, endemism, threatened state, taxonomic singularities and environmental representability (Prendergast et al., 1999). Nowadays, few biological groups have well represented data bases, causing priority areas for conservation to be selected based mostly -if not solelyon data of mammals, birds and, more scarcely, reptiles and amphibians (e.g. MMA, 2002). However, there are studies showing that areas with bigger richness and endemism fora group do not necessarily coincide with high richness and endemism for other groups that are intent on being preserved as well (Prendergast et al., 1993).
Despite the big representation as part of the biodiversity and the undeniable role in the functioning of the tropical ecosystems, insects are not frequently used in the determination of priority areas for conservation, specially in Brazil, because of the lack of systematized information (De Marco and Coelho, 2004). Most arthropods seem not to cause interest in conservation studies, making them general neglected by the management plan's creators. Such reality should be different, considering how easy it is to sample animals from this group (Merret and Snazel, 1983) and how efficient they are as ecological bioindicators (Wise, 1993), what makes them very useful for management politics. The conservation status of Brazilian invertebrates was summarized in lists of species threatened both in a national level (MMA, 2003;MMA, 2014) as well as a state/regional level (e.g. Passamani and Mendes, 2007). The biggest utility of these lists has been in the planning of the landscapes, in the monitoring and in the conservation of whole ecosystems (Casagrande et al., Rev. Bras. Gest. Amb. Sustent., 2019, vol. 6, n. 13, p. 481-497. 1998; Machado, 1998;Bergallo et al., 2000).
The Odonata Order (also known as dragonflies and damselflies) comprises 5.827 species (Garrison and Von Ellenrieder, 2016) and has three suborders: Anisoptera, Zygoptera and Anisozygoptera (Corbet, 1952 andDavies, 1981;May, 1991), though only the first two occur in Brazil, where there are 851 registered species, divided in 145 genera (Pinto, 2017). The adult members generally settle in the vicinity of fresh water, although some can be seen far from it. The immature state (larvae) are aquatic and can be found potentially in all fresh water environments (Corbet, 1999). Because of their dependence on water, the odonata are heavily affected by its physical and chemical condition, which enables them to be used as bioindicators of water quality for lakes and streams (Castella, 1987;Gorham and Vodopich, 1992;Peruquetti and De Marco, 2002). Additionally, both larvae and adults are dependent on the matrix of characteristics of the surrounding environment, making them good indicators of environmental changes in a variety of parameters (Peruquetti and De Marco, 2002).
The main goal of this study was to do a survey of the species of Odonata occurring in the Santa Teresa Municipality, in the Brazilian State of Espírito Santo, as well as to determine the occurrence of threatened and endemic species and determine, through their biological data, their potential for use as bioindicator. Therefore, expanding the knowledge of the order for Santa Teresa Municipality and the Atlantic Forest as a whole too. The knowledge of the regional faunas is important to provide numerical data that are more representative of the reality for the species and their composition.

Study area
The survey was done for the municipality of Santa Teresa, located at 650 m above sea level in meso-central area of the State of Espírito Santo. Santa Teresa has a total area of 71.110 ha and is located in the Atlantic Forest Region, considered to have the biggest biodiversity of plants on Earth (Mendes and Padovan, 2000); 40% of its area is covered by preserved areas of Atlantic Forest (Thomaz and Monteiro, 1997). The hidrography of the Santa Teresa Municipality is composed of many streams, most important of all being the Timbuí River, composed by the junction of the São Pedro and São Lourenço Streams. The Timbuí River is in a critic state in regards to the quality of the water, and has an old history of pollution (Louzada and Fonseca 2002). between 1960 and 2016 that included Odonata registered for Santa Teresa. Finally, a visit to the local faculty of Santa Teresa (Escola Superior São Francisco de Assis -ESFA), where was found a nonpublished monograph (Buss et al., unpublished data) and many related specimens deposited in the collection of the Museu de Biologia Professor Mello Leitão (Mello Leitão Museum). All obtained data was revised by Dr. Karina Furieri, group specialist and researcher participant during the mentioned monograph's work.

Database construction
The data base includes the following information: species name; family; locality (municipality and state); sampling point (e.g. name of the farm or lake, if possible); latitude and longitude; additional observation (such as type of vegetation). The species were identified utilizing identification Keys for the group (Garrizon et al., 2006 and2010;Lencioni, 2005 and2006) and comparisons with specimens previously identified by specialists. Dubious specimens and females were not included and can be posteriorly added to the Data Base. The species registered for Santa Teresa were classified as commons, endemic for the Espírito Santo, endemic for Brazil, rare and/or threatened by extinction, at a state (Simonelli, 2007) and national level (MMA, 2014).

Record of biological aspects of the catalogued species
After the construction of the updated Data Base, a research was done about each recorded species. In addition to bibliography, description sheets developed by the group for evaluation of conservation state of Odonata from Brazil (ICMBio and specialists on Odonata) were used -this data being provided by Dr. Karina Furieri. Some species were not described due to lack of information.
Elaboration of the map By using the program QGIS version 2.14.3 (GRASS version 7.0.4), a map was generated with the distribution of all the species recorded in the Data Base, in which is present all the forest remains in the Santa Teresa Municipality, as well as other areas of occurrence of species (as long as they present coordinates).

Biological aspects of the species Aceratobasis cornicauda (Calvert, 1909)
Adults of this genus fly slowly in areas shadowed by secondary forests, by short distances, until roosting (Lencioni, 2005).
Behaviour, habitat of reproduction and larvae are unknown (Von Ellenrieder, 2008), though with indications that this species uses Bromeliads for larval development (Lencioni, 2006). This is a forest species and has low populational density (Garrison et al., 2010).

Forcepsioneura lucia Machado, 2000
Forcepsioneura lucia is a forest species. Usually roosts on small branches close to the humid floor of the forest. This species is not found close to the river and it is possible its larvae lives in the humid litter of the forest instead of in the bodies of water. Normally are found near lentic parts of the stream (Machado, 2000). Heteragrion is a forest genus found exclusively in wood streams where its larvae lives. It is very susceptible to environmental changes (Monteiro-Junior et al., 2014). Some genera are indicators of environmental quality, like Heteragrion, which is not found in deforested or polluted places (Monteiro-Junior et al., 2014). Heteragrion aurantiacum occurs in areas with small changes (Peruquetti and De Marco, 2002). Oliveira (2013) found the species to be well represented and highly abundant at well preserved streams and Peruquetti and De Marco (2002) found Heteragrion aurantiacum only in areas with well-preserved riparian vegetation. Heteragrion petiense was always found roosting on marginal vegetation of small streams with nearly still water, where its larvae probably live, in the depths of preserved woods (Machado, 1998;Machado, 2008).

Leptagrion capixabae Santos, 1965; Leptagrion dispar Selys, 1876; Leptagrion macrurum (Burmeister, 1839) and Leptagrion perlongum Calvert, 1909
The larvae of the genus Leptagrion develops in the water accumulated on bromeliads (Furieri, 2004). Santos (1966) estimated the development time for four species of the genus as being between six and twelve months. The dependence on preserved habitats with bromeliads makes Leptagrion a bioindicator species, even more those threatened of extinction. The distribution of Leptagrion capixabae includes areas with rocky outbursts that are usually colonized by bromeliads of the genus Alcantarea, which could be the preferred habitat for L. capixabae. Adult males were observed roosting on big bromeliads of the species Alcantarea extensa in the Municipality of Ibiraçu and data suggests that this species has a resident behaviour and prefers bromeliads of rocky areas as their reproductive site (Furieri, 2004). The biggest threats to this species are the changes to its habitat by means of deforestation, rock extractions and forest fires (ICMBio research sheets). Leptagrion dispar has been observed, most of the time, in sunny areas and roosting on bromeliads of bigger size, like Aechmea blanchetiana (Furieri, 2004).  Santos, 1953 The genus Micrathyria habits lakes and streams, including temporary and saline (Garrison et al., 2006). Consatti (2014) found Micrathyria ocellata only in poorly preserved areas, though this is the only record for this preference. Peruquetti (2002) found Micrathyria pirassunungae happening only in areas of monoculture, though for this case as well, no other report has been found to confirm the preference.

Map with the points of occurrence for the species
The localities sampled in Santa Teresa are: São Pedro Stream, Santa Lucia Biological Station, Santa Lucia Spring, Santo Antônio Spring, São Pedro Spring, Paradiso Inn, Biological Reserve Augusto Ruschi, Timbuí River, São Lourenço and Vargem Alta (Figura 2).
The São Pedro Stream is an affluent to the Timbuí River and is surrounded by woods, pasture and agricultural areas. The São Pedro Stream point 1 is a lotic environment of dirty water, the point 2 is a lotic environment of clean water, the point 3 is a lotic environment surrounded by woods and the point 4 is lotic environment of dirty water. The spring of the São Pedro Stream is disturbed and altered, and is a lentic environment with riparian vegetation on one side and pasture on the other (Buss et al., unpublished data).
The Santa Lucia Biological Station (Estação Biológica Santa Lúcia, EBSL), that includes other points, is managed by the Museu Biologia Professor Mello Leitão (MBML) and, besides being a preservation area, is not included in the National System of Preservation Areas, nor is under any particular category of protection. The vegetation of the EBSL is in advanced stages of succession, with indications of anthropic disturbances localized in areas of old agricultural use (Mendes and Padovan, 2000). The Santa Lucia Spring is located inside the EBSL, is characterized as a lentic environment of woods (Buss et al., unpublished data). The Santo Antônio Spring is a lentic environment in the woods (Buss et al., unpublished data).
The Timbuí River, that includes most of the coordinates of occurrences of Odonata for the Santa Teresa Municipality, runs through the urban perimeter and receives the domestic wastes and other effluents, being one of the main hydric resources of Santa Teresa (Mauri et al., 2007). The physical and chemical parameters show that the Timbuí River is very polluted, presenting low concentration of solved oxygen and high turbidity (Mauri et al., 2007). The point 13 consists of a lentic environment in the woods; the point 14 is a lotic environment with riparian vegetation on one side and pasture on the other; the point 15 is a lotic environment in the woods; the point 16 is a lotic environment with riparian vegetation on one side and pasture on the other; the point 17 is a lotic environment surrounded by pasture and the point 18 is a well preserved environment of clean stream (Buss et al., unpublished data).

Discussion
The protected areas in Santa Teresa are of big biological importance because of their high diversity of plants and their role as ecological corridors (IPEMA, 2005). The Municipality of Santa Teresa is considered an Atlantic Forest sanctuary in the Espírito Santo State, possessing some of the most species rich environment on the planet: the Estação Biológica de Santa Lúcia and the Reserva Biológica Augusto Ruschi (Mauri et al., 2007). Santa Teresa still conserver 35% of its territory covered by Atlantic Forest vegetation, making it an important area of remnant for this biome (IPES, 2016).
Compared with the Odonata diversity of the Espírito Santo State (224 species, 73 genera and 11 families -Cruz, unpublished data), Santa Teresa show a big representation, with 35% of the species, 52% of the genera and 73% of the families recorded for the state. The data from CZNC added 25 new occurrences, highlighting the importance of identifying the specimens kept in zoological collections. It is important to give priority to the information of specimens already deposited in collections and to spread that data in the form of papers or data bases.
Zygoptera is a group of insects that normally is associated to more preserved places with riparian vegetation, because of its more restricted biological needs (Corbet, 1999). The bigger richness of Zygoptera in Santa Teresa Municipality can reflect the large (35%) portion of the territory still covered by Atlantic Forest vegetation (relatively preserved places), showing that the local systems might be in an equilibrium.
The vegetation in the Estação Biológica Santa Lúcia is in advanced stages of succession (Mendes and Padovan, 2000). Despite its relatively big forest cover, Santa Teresa suffers the impact of domestic wastes, garbage accumulation and other types of residue that are deposited in the Timbuí River. The Timbuí River and the other streams that run through the city are known as Rev. Bras. Gest. Amb. Sustent., 2019, vol. 6, n. 13, p. 481-497. 'sewers', mainly because 90% of the residences uses them as recipient of their wastes, which brings consequences like turning these streams into producers of vectors (Mendes and Padovan, 2000).
The bigger representation of Zygoptera in Santa Teresa might be explained as well by bigger sampling effort in relation to this group, justified for example by the bigger number of specialists on this group and its genera, like the specimens found in the CZNC, mostly having been collected by Dr. Karina Furieri, researcher who works mainly with the Zygoptera Suborder.
The endemic species, as well as those with bigger area requirements, answer more quickly to the habitat fragmentation dynamics, therefore making up a significative number of the threatened taxa that need to be protected (Grelle et al., 1999;Paglia, 2005). The presence of endemic species is, then, considered an important factor to point the environmental representation of a place. Leptagrion capixabae must be highlighted for its status as a rare species, endemic to the Espírito Santo State, and its recent rediscovery with few known populations (Furieri et al., 2004). The species is also in the Critically Endangered (CR) category according to the state Red List and Vulnerable (VU) according to the national Red List. The specialization on phytotelma microhabitat can leave the species exposed to habitat destruction, be it by deforestation or illegal extraction of bromeliads for use as ornaments (Simonelli and Fraga 2007). Other than L. capixabae, L. dispar, L. macrurum and L. perlongum occur in Santa Teresa as well. It's important to observe that other species of Leptagrion were not included in the list of threatened species, despite their rarity in collections, due to the lack of information even about their points of occurrence. This set of species is probably under threat of extinction, mainly because of habitat loss.
Other species in the region must also be highlighted, like Heteragrion petiense, inserted in the category Endangered -EN (MMA, 2014), which is a species with restricted distribution (Machado, 1998); it's population has been considered severely fragmented due to the intensity of habitat loss (converted to agriculture) added to its need of streams with well-preserved woods, causing a decline in its areas of occurrence (ICMBio research sheets).
Another Vulnerable (VU) species -Acerotobasis cornicauda, is also in this category because of the limited area of occurrence and its growing occupation and alteration by human activities (agriculture and urbanization), resulting in a continuous fragmentation and severe loss of habitat quality and extension, representing a direct threat to the populations (ICMBio research sheets).
A species in the Nearly Threatened (NT) category, Leptagrion díspar, deserves attention for its preference for areas of restinga (sandbank vegetation), specially points with higher rates of Sunshine on the bromeliads; its habitat is severely altered (deforested, fragmented, under urban influence, receiving wastes and under illegal exploitation of sand and bromeliads), with continued decline of vegetation (ICMBio research sheets). Considering that Brazil has recognized 18 dragonfly species threatened by extinction, the presence of three of them in a single municipality makes it very relevant to preserve the diversity of the group.
Other than the threatened species, it is also important to consider the three species in the Data Deficient (DD) category (Forcepsioneura lucia, Minagrion canaanense and Micrathyria ocellata), showing the need to expand the knowledge of these taxa. The preference of the Odonata species for habitats in Brazil is still poorly known, and determining the reason behind the preferences for impacted habitats by certain genera is important to their utilization in works monitoring the quality of aquatic systems (Fore et al., 1996). However, Hetaerina brightwelli is an indicator of a well-preserved habitat, on the opposite of the other species in the genus, further demonstrating the need to study each species individually and the difficulty of expanding the patterns of a species to a whole genus for use as bioindicators.
It is possible that rare species occur in Santa Teresa and have yet to be registered. Observing the map with the registered species for the municipality and the published studies, it is perceptible that a big area has not yet been sampled, and most of the registered species came from the Timbuí River and the Estação Biológica Santa Lúcia. The municipality includes three basins: Três Magos River Basin (with two river arms: the Fundão River and the Timbuí Riverthe latter being most important source of water the Santa Teresa municipality), the Piraquê-açu river and the Santa Maria do Rio Doce River (Mendes and Padovan, 2000). The sampling in not yet studied points is needed to complete the knowledge about the fauna of Odonata in Santa Teresa. Species distribution modelling can be used to predict new areas of occurrence for rare and threatened species (e.g. Engler et al., 2004;Guisan et al., 2006;Gibson et al., 2007).

Conclusion
The species richness found, the presence of populations of threatened species and the inclusion of newly registered species for Santa Teresa suggests that the fauna of the region deserves more attention and points to the benefits of creating new conservation units. New samples in the region are needed, especially in the northern and western sides of the municipality, where the register of occurrences is virtually inexistent. The affluents of the Piraquê-Açu and the Santa Maria do Rio Doce Basin are highlighted as important points for future samples, in order to better represent the Odonata diversity of Santa Teresa. It is also needed the study of the Data Deficient (DD) species.
The future of the conservation of invertebrates depends on the preservation of habitats as a whole and on a more complete comprehension of the roles on maintaining ecosystem's processes. The potential of the conservation units in Santa Teresa is dependent not only on their integrity but also on a program of conservation of the Atlantic Forest in a regional scale. Since most of the forest remnants of the region are under private ownership, a system that encourages their maintenance is needed, such as the recommendation to create private conservation units.