Diversidad de adultos de Odonata en el Bioma Pampa brasileno.
Rio Grande do Sul (RS) State is located in the Southernmost territory of Brazil. It coverseveral regions and environments diversified climatic and geomorphologically. The Pampa Biome is located in the Southern of the state and is made up of a set of distinct ecosystems containing vast biodiversity. Although it remains mostly unexplored, this area consists of an extremely rich gene pool (Boldrini et al., 2010).
These ecosystems have been affected by several human activities, such as inadequate use of the soil, inadequate disposal of industrial and domestic effluents, as well as the increasing use of agrochemicals (Esteves, 2011). This has contributed to biodiversity loss, jeopardizing the balance of aquatic and terrestrial biomes and, consequently, impacting human welfare (Cardinale et al., 2012). According to Merritt and Cummins (1996) invertebrates are one of the most common groups in freshwater environments, and, among them, insects stand out because of their association with other freshwater communities.
The Odonata order comprise insects commonly known as dragonflies, damselflies, lavabunda, zig-zag, and, specifically in Rio Grande do Sul, Cicadas. This order is composed of paleopterous amphibiotic insects, under hemimetabolous development, and is divided into three suborders: Zygoptera, Anisoptera and Anisozygoptera (Rehn, 2003). Globally, this order contains 6 500 species (Trueman & Rowe, 2009), and about 800 of them from 15 different families were reported in Brazil alone (Neiss & Hamada, 2014).
These insects are relevant bioindicators for assessing and monitoring environmental conditions of specific locations. Thus, the greater the biodiversity, the better the health of that ecosystem (Ferreira-Peruquetti & De Marco, 2002; Foote & Rice, 2005; Silva, Marco, & Resende, 2010; Carvalho, Silva-Pinto, Oliveira-Junior, & Juen, 2013; Monteiro Junior, Couceiro, Hamada, & Juen, 2013). In this context, some researchers have recognized the need to list the diversity of these animals and develop models and criteria that can be applied in environmental change assessments (Reaka-Kudla, Wilson, & Wilson, 1997).
Species inventories are indispensable in management and conservation processes, in which the entomofauna diversity is an important tool for environmental sanity. Furthermore, the knowledge of insect diversity may provide valuable information on the integrity of the studied environments (Lutinski & Garcia, 2005).
According to the Red List of Threatened Species of the International Union for Conservation of Nature (IUCN), one in ten Odonata species is in critical danger of being extinct (Mace et al., 2008), and 35 % of them species lack incidence data (Clausnitzer et al., 2009). In Rio Grande do Sul (RS), there are very few studies that address the Odonata inventory and are limited almost exclusively to the reports made by Costa (1971) and Teixeira (1971) in Santa Maria and Porto Alegre cities, respectively. The last data concerning Odonato fauna in RS are present in the work of Kittel and Engels (2014), who studied the diversity of Zygotera in Sao Francisco de Paula. They included four new species in the list of registered species of the State. Furthermore, Renner, Perico, Sahlen, Dos Santos, and Consatt (2015) conducted an inventory study in 12 cities of the Rio Taquari valley region, where 50 Odonata species were found.
This study aims to widen the knowledge on the Odonata species and measure the species incidence in the aforementioned region. In addition, fauna indexes will be associated with the sampling areas.
MATERIALS AND METHODS
Field of study: Known as the "Southern fields", the Pampa Biome covers approximately 62 % of Rio Grande do Sul (177 767 [km.sup.2]) along with part of Argentina and the entire territory of Uruguay, which is rich in water resources. Most of the water bodies are ecologically classified as shallow lakes, which are easily influenced by natural and human activity because of their shallow depth (Trindade, Furlanetto, & Silva, 2009; Zambrano, Contreras, Hiriart, & Arista, 2009). The sampling areas are located in the Lagoa Mirim and Lagoa dos Patos, both lakes with well defined seasons with cold and rainy winters and hot and dry summers. According to the Koppen-Geiger climate classification, local climate is considered Cfa (humid subtropical). In this region, average annual temperature varies between 16 [grados]C and 18 [degrees]C and average annual rainfall is approximately 1 500 mm.
In the cities where the study was conducted, two collection sites were selected with three sampling points each. In Capao do Leao, sampling was conducted at Campus of the Federal University of Pelotas--UFPel (31[degrees]80'16" S-52[degrees]41'94" W) and at Irmao Teodoro Luis Botanical Garden (31[degrees]81'27" S-52[degrees]43'58" W). In Pelotas, the samples were collected in Vila Princesa (31[degrees]62'79" S-52[degrees]32'66" W) and Balneario dos Prazeres (31[degrees]72'07" S - 52[degrees]19'14" W). In Rio Grande city, the samples collected in Arroio Bolaxa (32[degrees]16'02" S - 52[degrees]18'80" W) and Taim Ecological Station (32[degrees] 44'33" S - 52[degrees] 34'28" W).
Collected data: Odonata samples were obtained between November 2014 to October 2015; no samples were taken during the winter season because of the lack of activity among adult insects due to low temperatures. Each location was visited nine times, totalizing 54 samplings. In order to capture the insects, the active collection method was conducted with entomological nets. The samplings were performed on sunny days, between 9 am to 4 pm, during a period of three hours at each collection site.
Species identification: The collected specimens were kept alive in entomological envelopes for at least four hours and were later treated with Acetone, as methodology proposed by Lencioni (2005). Samples were identified using the taxonomic keys proposed by Lencioni (2005; 2006) and Heckman (2006; 2008). Damaged especimens or those that had no similarity with the descriptions offered in literature were classified at generic level. The specimens were deposited at the Ceslau Biezanko Entomological Museum, UFPEL.
Data analysis: The data analyses were conducted considering specific abundance (n), generating the species-accumulation curve. Relative frequency (Rf) was measured by dividing the total number of collected species by the total of collected insects, multiplied by 100 (Silveira Neto, Nakana, Barbin, & Vila Nova, 1976; Bianconi, Mikich, & Pedro, 2004). For this measurement, a 5 % confidence interval was used, and species were classified as very frequent (C [greater than or equal to] 50 %), frequent (25 % [less than or equal to] C < 50 %) and infrequent (C < 25 %).
The abundance assessments and comparisons were conducted using the Chao-1 estimator. Based on abundance, this evaluation relates the number of species represented by only one individual (singletons), and the number of species with only two sample individuals (doubletons) (Colwell, 2012). Furthermore, it is calculated by the equation: Chao 1 = S + ([a.sup.2]/2b); in which S is the number of encountered species in the samples, a is the number of species represented by one specimen, and b is the number of species represented by two specimens (Chao, 1984; 1987; Ferraz, Gadelha, & Aguiar-Coelho, 2009).
The diversity measurement was performed using the Shannon-Wiener index: H'= -[SIGMA](fi) log (fi); in which fi is the proportion of individuals belonging to the nth specie and ln is the neperian logarithm (Pielou, 1975).
For the species-diversity estimates and their confidence intervals (95 %), the analytical estimator first-order Jackknife index was used (Jack 1 = S + L (n-1/n), in which S is the sum of the species found in the samples, L is the number of species present in a single sample, and n is the total number of samples (Palmer, 1991). For calculations and graph and table elaboration, Excel and EstimateS 8.0 programs were used.
Considering all our sample collections, 2 680 specimens were found, comprised by 45 species distributed into 22 genera and 6 families (Table 1). The species Progomphus complicatus, Lestes minutus, Homeoura ambigua and Tauriphila xiphea were recorded for the first time, in ascending order of frequency, in RS (Table 1).
The most speciose genera were Erythrodiplax and Micrathyria, with eight and five species, respectively. These genera, represented by two species (Rhionaeschna bonariensis and Telebasis willinki), along with Ischnura, were found at least once in all the visited sites. Gomphidae specimens were less frequent and exhibited low density in this study, since P complicatus specimens were found only in Pelotas, specifically on sandbanks of Arroio Pelotas, located in Vila Princesa. Female Phyllocycla were collected close to the pools of UFPel Campus in Capao do Leao (Table 1).
Ten species, from the Libellulidae (6) and Coenagrionidae (4), were considered very frequent (VF), reaching a total of 65 % of the captured individuals. The Gomphidae and Calopterygidae were represented by 32 total specimens, corresponding to 1.19 % of the collected insects and considered infrequent (IF) (Table 1).
The Libellulidae family was the most abundant since it comprising 57.78 % of the samples (Table 2), in which Miathyria marcella was the most common specie, amounting to 9.66 % of total dragonfly samples (Table 1). The next most common families were Coenagrionidae and Aeshnidae, with a total of 20 % and 8.89 % of the specimens, respectively. Lastly, the least abundant families were Lestidade with 6.67 %, Gomphidae with 4.44 %, and Calopterygidae with 2.22 % of the sampled species. Concerning the sample density, the Libellulidae family comprised 60.82 % of total collected specimens, followed by Coenagrionidae of the Zigoptera suborder at 30.35 % of total collected Odonata (Table 2).
Based on the different faunistc indexes (faunistic) (Table 3), the highest number of specimens were collected in Capao do Leao, followed by Pelotas, and Rio Grande, with 969, 860, and 851 specimens respectively. In addition, the highest specific wealth was also found at Capao do Leao, where 42 species were reported, while in Rio Grande and Pelotas 40 and 36 species were collected, respectively.
In the current study, the highest ShannonWiener diversity indexes were found in Capao do Leao (1.62) and Rio Grande (1.54), while Pelotas (1.49) exhibited the lowest result. On the other hand, regarding the species-diversity estimator, Chao 1 method, Pelotas reached the highest value, followed by Rio Grande (48.0) and Capao do Leao (46.3) (Table 3).
The species accumulation curve (Fig. 1) was unable to reach the asymptote, indicating that the diversity in the region is relatively larger than the 45 species found in the current study. The first-order Jackknife index is 57.3 species, with standard deviation of [+ or -] 8.2.
The heterogeneity of the sampled environments enabled us to collect 45 Odonata species. Regarding their frequency, 26 of 45 species occurred infrequently (IF), totaling 57.78 %, ten species were found very frequently (VF), comprising 1 765 collected specimens, and nine species were considered frequent (F) (Table 1).
Regarding genus diversity, De Figueiredo et al. (2013) found 34 Odonata genera in the Rio Ibicui river basin in Central RS. Their results were higher than the results obtained in this study, which was conducted in the Southern region of the state. However, inferior diversity wealth in this region may be due to insufficient studies. In addition, the huge fields of the Pampa Biome, permeated with small forest areas and several types of water bodies, are ideal environments for Odonata (Maluf, 2000).
The UFPel Campus, located in Capao do Leao city, exhibited 42 species, the greatest diversity among all collection sites. Furthermore, Capao do Leao was also where the highest number of insects were captured (579) (Table 1). These data indicate that, despite flow of people in the university campus, the sampling area, that is far away, provide adequate conditions for the Odonata diversity found in the present study. In Rio Grande, the greatest diversity was observed in Arroio Bolaxa, with 34 collected species, while at the Taim Ecologic Station 31 species were observed. The difference in total species found in Arroio Bolaxa and in Taim, may have occurred because of the larger green area exhibited in the first (Juen & De Marco, 2012). Contraringly to diversity, 161 more specimens were collected at Taim Ecologic Station than in Arroio Bolaxa.
According to the Shannon-Wiener index (H'), the lowest diversity was found in Pelotas (Table 3). This may be attributed the fact that the collection sites in this city constantly suffer human disturbances, which, according to Clausnitzer & Jodicke (2004), occur when industrial and/or domestic effluents are inadequately disposed, i.e. in locations close to urban areas. This describes Vila Princesa, an area located near the BR116 road. Human disturbances are also found in the Balneario dos Prazeres collection site, which exhibits large flow of people, such as residents and bathers. The impacts caused on Odonata diversity by human actions in these areas are still unclear, especially because these types of studies are rare in Brazil (Ferreira-Peruquetti & De Marco, 2002; Clausnitzer et al., 2009). In Pelotas, although lower species diversity was found, its Chao 1 index was higher than Capao do Leao and Rio Grande, estimating 48.6 species. This difference may be because the latter index considers rare species, i.e. it analyzes the number of species represented by only one specimen and the number of species represented by only two sample specimens.
Dragonflies are outstanding insects that can be affected both by environmental (Juen & De Marco, 2011) and spacial factors (Juen, Cabette, & De Marco, 2007; Clausnitzer et al., 2009). This indicates that these insects are potential bioindicators for monitoring the quality of aquatic environments (Ferreira-Peruquetti & De Marco, 2002). Furthermore, dragonflies may be considered valuable tools of freshwater environments, since the diversity of immature Odonata in the environment elucidates the diversity of the entire macroinvertebrate community (Foote & Rice, 2005).
Twenty-six of the 45 collected species were from the Libellulidae family, which can be explained by the fact that most of these specimens are generalist and can be found in many different environments. Like the rest of the Anisoptera suborder, this family exhibits the largest insects of all Odonata, making them more capable of flying and distributing themselves geographically (Kalkman et al., 2008; Juen & De Marco, 2012).
M. marcella was the most common of this study with 259 captured specimens and is considered VF at 9.66 % frequency. This may be explained by the fact that it is an abundant and generalist specie. In fact, M. marcella is strongly associated with floating vegetation, such as Eichhornia and Pistia, commonly known as water hyacinth and water lettuce, respectively. Dragonflies deposit their eggs on these floating plants (Paulson, 2017) for reproduction, which is in agreement with the sampling environments studied here.
Concerning the species reported for the first time in Rio Grande do Sul state, P. complicatus was collected only six times, all of which occurred in the city of Pelotas. L. minutus specimens were collected only in Rio Grande and Taim, and all 15 specimens of the Homeoura ambigua were collected in Rio Grande. T. xiphea specimens were present in all the sampling locations, having been most frequent in Rio Grande, totaling 23 individuals. The aforementioned species expanded its geographic distribution since it was previously only found in Paraguay, Argentina and Rio de Janeiro (Heckman, 2006). Regarding frequency, all the specimens reported for the first time were classified as IF.
According to Juen et al., (2007), the distributions of some species are limited by physical and ecological factors. Having that in mind, Southern landscape of RS favors the species that are more agile and more capable of dispersion, since the vegetation is composed mainly by open fields. This may explain the low diversity of Zygoptera found during this study, considering that the small forest areas present in this region are mostly spread out and distant from one another. Due to their type of thermoregulation, these small specimens would have trouble taking long flights in open fields (De Marco & Resende, 2002). In addition, according to Carvalho, Oliveira-Junior, Faria, and Juen (2013), the Zygoptera would have trouble surviving in open spaces exposed to light and heat.
The sampling efficiency reached in this study was around 78 % (Jack 1) of the expected diversity and was far from reaching the asymptote. This shows that the number of existing species in the studied region is larger than the 45 species found in the present study and that more sampling efforts are required in all regions of the state to find the expected diversity.
Although this study presents the Odonata diversity found in a small sample portion of the Pampa Biome in the south of Rio Grande do Sul, the data are still limited. The species herein reported for the first time in the state show that more studies must be conducted so more precise data about the species of the region can be observed. Furthermore, aquatic sampling should be include the collection of immature stages.
In conclusion, Progomphus complicatus, Lestes minutus, Homeoura ambigua, and Tauriphila xiphea were reported for the first time in the State of Rio Grande do Sul. In regard to the Odonata diversity in the Brazilian pampa biome, 45 species were encompassed in 22 genera and the most commonly found genera were Erythrodiplax and Micrathyria. Concerning the occurrence frequency, 26 species were considered infrequent, 9 were frequent, and 10 were very frequent. The city of Capao do Leao exhibited the largest species diversity (wealth), the largest number of collected specimens, and greatest diversity, in comparison to Pelotas and Rio Grande. The Miathyria marcella species represented 9.6 % of all collected libellulidae and was the most abundant species.
Ethical statement: authors declare that they all agree with this publication and made significant contributions; that there is no conflict of interest of any kind; and that we followed all pertinent ethical and legal procedures and requirements. A signed document has been filed in the journal archives.
Received 14-V-2017. Corrected 25-XI-2018. Accepted 21-I-2019.
This research was supported by the Coordination for the Improvement of Higher Education Personnel (CAPES), National Council for Scientific and Technological Development (CNPq), Foundation for Research Support of the State of Rio Grande do Sul (FAPERGS) and the members of the Ecological Station of TAIM (ESEC of TAIM) for the indispensable colaboration.
Bianconi, G. V., Mikich, S. B., & Pedro, W. A. (2004). Diversidade de morcegos (Mammalia, Chiroptera) em remanescentes florestais do municipio de Fenix, noroeste do Parana, Brasil. Revista Brasileira de Zoologia, 21(4), 943-954. Retrieved from http://www. scielo.br/pdf/rbzool/v21n4/22961.pdf
Boldrini, I. I., Ferreira, P. M. A., Andrade, B. O., Schneider, A. A., Setubal, R. B., Trevisan, R., & Freitas, E. M. (2010) Bioma Pampa: diversidade floristica e fisionomica. Porto Alegre, Brasil: Pallotti.
Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings, C., Venail, P., ... Naeem, S. (2012). Biodiversity loss and its impact on humanity. Nature, 486, 59-67. Retrieved from https://www.nature.com/articles/nature11148 DOI: http://10.1038/nature11148
Carvalho, F. G., Oliveira-Junior, J. M. B., Faria, A. P. J., & Juen, L. (2013). Uso da curva abc como metodo para detectar o efeito de modificacao antropogenica sobre assembleia de Odonata (insecta). Interciencia, 38, 516-522. Retrieved from https://www.interciencia. net/wp-content/uploads/2017/12/516-c-JUEN-7.pdf
Carvalho, F. G., Silva-Pinto, N., Oliveira-Junior, J. M. B., & Juen, L. (2013). Effects of marginal vegetation removal on Odonata communities. Acta Limnologica Brasiliensia, 25(1), 10-18. Retrieved from http://www.scielo.br/scielo.php?script=sci_ arttext&pid=S2179-975X2013000100003 DOI: 10.1590/S2179-975X2013005000013
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11, 265-270. Retrieved from http:// dns2.asia.edu.tw/~ysho/YSHO-English/1000%20 Taiwan%20(Independent)/PDF/Sca%20J%20 Sta11,%20265.pdf
Chao, A. (1987). Estimating the Population Size for Capture-Recapture Data with Unequal Catchability. Biometrics, 43, 783-791. Retrieved from https://www.jstor. org/stable/2531532?seq=1#page_scan_tab_contents
Clausnitzer, V., & Jodicke, R. (2004). Guardians of the watershed global status of dragonflies: critical species, threat and conservation. International Journal of Odonatology, 7, 111-430. Retrieved from https:// www.tandfonline.com/DOI/abs/10.1080/13887890.2004.9748201
Clausnitzer, V., Kalkman, V. J., Ramc, M., Collen, B., Baillie, J. E. M., Bedjanic, M., & Wilson, K. (2009). Odonata enter the biodiversity crisis debate: the first global assessment of an insect group. Biological Conservation, 142(8), 1864-1869. Retrieved from https://www.sciencedirect.com/science/ article/pii/S0006320709001621 DOI: 10.1016/j. biocon.2009.03.028
Colwell, R. K. (2012). User's guide to EstimateS. Statistical Estimation of species richness and shared species from samples. Version 9.1.0. Copyright 19942012. Retrieved from http://viceroy.eeb.uconn.edu/ estimates
Costa, J. M. (1971). Contribuicao ao conhecimento da fauna odonatologica do municipio de Santa Maria, Rio Grande do Sul. Atas da Sociedade Biologica Rio de Janeiro, 14, 193-194.
De Figueiredo, N. S. B, Pires, M. M., Davanso, R. C. S., & Kotzian, C. B. (2013). Diversity of larvae Odonata (Insecta) River Basin Ibicui, Rio Grande do Sul, Brasil. Ciencia e Natura, 35(2), 084-094. Retrieved from https://periodicos.ufsm.br/index.php/ cienciaenatura/article/viewFile/12563/7974 DOI:10.5902/2179-460X833
De Marco, P., & Resende, D. C. (2002). Activity patterns and thermoregulation in a tropical dragonfly assemblage. Odonatologica, 31, 129-138. Retrieved from http://natuurtijdschriften.nl/search?identifier=592390
Esteves, F. A. (2011). Fundamentos de Limnologia. Rio de Janeiro, Brasil: Interciencia.
Ferraz, A. C. P., Gadelha, B. Q., & Aguiar-Coelho, V. M. (2009). Analise faunistica de Calliphoridae (Diptera) da Reserva Biologica do
Tingua, Nova Iguacu, Rio de Janeiro. Revista Brasileira de Entomologia, 53(4), 620-628. Retrieved from http://www.scielo.br/scielo.php?script=sci_artt ext&pid=S0085-56262009000400012 DOI: 10.1590/S0085-56262009000400012
Ferreira-Peruquetti, P. S., & De Marco, Jr. P. (2002). Efeito da alteracao ambiental sobre a comunidades de Odonata em riachos de Mata Atlantica de Minas Gerais, Brasil. Revista Brasileira de Zoologia, 19(2), 317327. Retrieved from http://www.scielo.br/pdf/rbzool/v19n2/v19n2a02
Foote, A. L., & Rice, C. L. (2005). Odonates as biological indicators of grazing effects on Canadian prairie wetlands. Ecological Entomology, 30, 1-11. Retrieved from https://onlinelibrary.wiley.com/ DOI/abs/10.1111/j.0307-6946.2005.00701.x DOI:10.1111/j.0307-6946.2005.00701.x
Heckman, C. W. (2006). Encyclopedia of South American aquatic insects: Odonata--Anisoptera. Dordrecht, Netherlands: Springer.
Heckman, C. W. (2008). Encyclopedia of South American aquatic insects: Odonata--Zygoptera. Washington, DC, USA: Springer.
Juen, L., Cabette, H. S. R., & De Marco, P. J. (2007). Odonate assemblage structure in relation to basin and aquatic habitat structure in Pantanal wetlands. Hydrobiologia, 579, 125-134. Retrieved from https:// link.springer.com/article/10.1007/s10750-006-03956 DOI: 10.1007/s10750-006-0395-6
Juen, L., & De Marco, P. J. (2011). Odonate biodiversity in terra-firme forest streamlets in Central Amazonia: on the relative effects of neutral and niche drivers at small geographical extents. Insect Conservation and Diversity, 4, 1-10. Retrieved from https://onlinelibrary.wiley.com/DOI/ abs/10.1111/j.1752-4598.2010.00130.x DOI:10.1111/j.1752-4598.2010.00130.x
Juen, L., & De Marco, P. J. (2012). Dragonfly endemism in the Brasilian Amazon: competing hypotheses for biogeographical patterns. Biodiversity and Conservation, 21(13), 3507-3521. Retrieved from https:// link.springer.com/article/10.1007/s10531-012-03770 DOI: 10.1007/s10531-012-0377-0
Kalkman, V. J., Clausnitzer, V., Dijkstra, K. D. B., Orr, A. G., Paulson, D. R., & Tol, J. V. (2008). Global diversity of dragonflies (Odonata) in freshwater. Hydrobiologia, 595, 351-363. Retrieved from https://link. springer.com/article/10.1007/s10750-007-9029-x DOI: 10.1007/s10750-007-9029-x
Kittel, R. N., & Engels, W. (2014). Diversity of damselflies (Odonata: Zygoptera) of the state of Rio Grande do Sul, Brasil, with four new records for the state. Notulae Odonatologicae, 8(3), 49-55. Retrieved from https://www.researchgate.net/ publication/262766709_Diversity_of_damselflies_ Odonata_Zygoptera_of_the_state_Rio_Grande_do_ Sul_Brasil_with_four_new_records_for_the_state
Lencioni, F. A. A. (2005). Damselflies of Brasil: an illustrated identification guide 1--non-Coenagrionidae families. Sao Paulo, Brasil: All Print Editora.
Lencioni, F. A. A. (2006). Damselflies of Brasil: an illustrated identification guide, Volume 2 -Coenagrionidae. Sao Paulo, Brasil: All Print Editora.
Lutinski, J. A., & Garcia, F. R. M. (2005). Analise faunistica de Formicidae (Hymenoptera: Apocrita) em ecossistema degradado no municipio de Chapeco, SC. Biotemas, 18(2), 73-86. Retrieved from https://periodicos.ufsc.br/index.php/biotemas/article/view/21413. DOI: 10.5007/%25x
Mace, G. M., Collar, N. J., Gaston, K. J., Hilton-Taylor, C., Akcakaya, H. R., Leader-Williams, N., ... Stuart, S. N. (2008). Quantification of extinction risk: IUCN's system for classifying threatened species. Conservation Biology, 22, 1424-1442. Retrieved from https:// www.ncbi.nlm.nih.gov/pubmed/18847444 DOI:10.1111/j.1523-1739.2008.01044.x
Maluf, J. R. T. (2000). Nova classificacao climatica do estado do Rio Grande do Sul. Revista Brasileira de Agrometeorologia, 8, 141-150.
Merritt, R., & Cummins, K. (1996). An introduction to aquatic insects of North America. Dubuque, USA: Hunt Publishing Company.
Monteiro-Junior, C. S., Couceiro, S. R. M., Hamada, N., & Juen, L. (2013). Effect of vegetation removal for road building on richness and composition of Odonata communities in Amazonia, Brasil. International Journal of Odonatology, 16, 135-144. Retrieved from https:// www.tandfonline.com/DOI/abs/10.1080/13887890.2 013.764798 DOI: 10.1080/13887890.2013.764798
Neiss, U. G., & Hamada, N. (2014). Insetos aquaticos na Amazonia Brasileira: taxonomia, biologia e ecologia. Manaus. Brasil: Editora INPA.
Palmer, M. W. (1991). Estimating species richness: The second-order jackknife reconsidered. Ecology, 72, 1512-1513. Retrieved from https://esajournals.onlinelibrary.wiley.com/DOI/abs/10.2307/1941127. DOI: 10.2307/1941127
Paulson, D. R. (2017). Miathyria marcella. Lista Vermelha da IUCN de Especies Ameacadas. e.T165066A80685834. Retrieved from 10.2305/ IUCN.UK.2017-3.RLTS.T165066A80685834.en
Pielou, E. C. (1975). Ecological diversity. New York, USA: John Wiley & Sons, Inc.
Reaka-Kudla, M. L., Wilson, D. E., & Wilson, O. (1997). Biodiversity II. Washington, DC, USA: Joseph Henry Press.
Rehn, A. C. (2003). Phylogenetic analysis of higher-level relationshipps of Odonata. Systematic Entomology, 28, 181-239. Retrieved from https://onlinelibrary.wiley. com/DOI/abs/10.1046/j.1365-3113.2003.00210.x DOI: 10.1046/j.1365-3113.2003.00210.x
Renner, S., Perico, E., Sahlen, G., Dos Santos, D. M., & Consatti, G. (2015). Dragonflies. (Odonata) from the Taquari River valley region, Rio Grande do Sul, Brasil. Check List, 11(5), 1740. Retrieved from https:// www. biotaxa.org/cl/article/view/11.5.1740 DOI:10.15560/11.5.1740
Silva, D. P., Marco, P., & Resende, D. C. (2010). Adult odonate abundance and community assemblage measures as indicators of stream ecological integrity: a case study. Ecological Indicators, 10(3), 744-752. Retrieved from https://www.sciencedirect.com/science/article/pii/S1470160X09002039 DOI: 10.1016/j.ecolind.2009.12.004
Silveira Neto, S., Nakana, O., Barbin D., & Vila Nova, N. A. (1976). Manual de ecologia dos insetos. Ouro Fino, Brasil: Editora Agronomica Ceres.
Teixeira, M. C. (1971). Contribuicao para o conhecimento da fauna odonatologica do Rio Grande do Sul. Arquivos do Museu Nacional (Rio de Janeiro), 54, 17-24.
Trindade, C. R. T., Furlanetto, L. M., & Silva, C. P. (2009). Nycthemeral cycles and seasonal variation of limnological factores of a subtropical shallow lake (Rio Grande, RS, Brasil). Acta Limnologica Brasiliensia, 21 , 34-44. Retrieved from http://repositorio.furg.br/bitstream/handle/1/117/ Nycthemeral%20cycles%20and%20seasonal%20 variation%20of%20limnological%20factors%20 of%20a%20subtropical%20shallow%20lake%20 %28Rio%20Grande%2C%20RS%2C%20Brasil%29.pdf?sequence=1
Trueman, J. W. H., & Rowe, R. J. (2009). Odonata. Dragonflies and damselflies. The Tree of Life Web Project. Electronic Database. Retrieved from http:// tolweb.org/Odonata/8266/2009.10.16
Zambrano, L., Contreras, V., Hiriart, M. M., & Arista, A. E. Z. (2009). Spatial heterogeneity of water quality in a highly degraded tropical freshwater ecosystem. Environmental Management, 43(2), 249-263. Retrieved from https://www.ncbi.nlm.nih.gov/pubmed/18941831 DOI: 10.1007/s00267-008-9216-1
Manoel D. N. Garcia Junior (1), Matheus Rakes (2) *, Juliano de B. Pazini (2), Rafael A. Pasini (3), Flavio R. M. Garcia (1) & Anderson D. Grutzmacher (2)
(1.) Department of Ecology, Zoology, and Genetics, Institute of Biology (IB), Federal University of Pelotas, Postcode 96010-900, Pelotas, Rio Grande do Sul, Brazil; firstname.lastname@example.org, email@example.com
(2.) Department of Plant Protection, Faculty of Agronomy "Eliseu Maciel" (FAEM), Federal University of Pelotas, postcode 96010-900, Pelotas, Rio Grande do Sul, Brazil; firstname.lastname@example.org, email@example.com, firstname.lastname@example.org
(3.) Center for Higher Education Riograndense, postcode 99560000, Sarandi, Rio Grande do Sul, Brazil; email@example.com
Caption: Fig. 1. The species accumulation curve of Odonata using the Jackknife index (Jack 1) in the Brazilian Pampa Biome The dashed lines represent the confidence interval (CI 95).
TABLE 1 List of the species collected in the Brazilian Pampa Biome (Southern region of Rio Grande do Sul) divided by suborder and families Family/Species Collection Sites (1) Suborder Zygoptera PBP PVP CHB CCL RAB RET Calopterygidae Hetaerina rosea Selys, 1853 5 9 0 3 2 0 Coenagrionidae Acanthagrion gracile 2 1 0 1 2 0 Rambur, 1842 Acanthagrion lancea Selys, 0 0 0 3 1 0 1876 Homeoura chelifera Selys, 0 26 48 23 10 26 1876 Homeoura ambigua Ris, 7 2 2 4 0 0 1904 * Ischnura capreolus Hagen, 36 26 41 47 29 40 1861 Ischnura fluviatilis Selys, 41 29 29 56 30 39 1876 Oxyagrion terminale Selys, 10 0 0 9 0 5 1876 Oxyagrion simile Costa, 0 0 0 5 0 0 1978 Telebasis willinki Fraser, 44 19 24 36 15 45 1948 Lestidae Lestes undulatus Say, 1839 8 10 0 9 8 0 Lestes tricolor Erichson, 7 11 0 0 9 0 1848 Lestes minutus Selys, 0 0 0 0 0 8 1862 * Suborder Anisoptera Aeshnidae Coryphaeschna amazonica 4 0 5 1 0 1 DeMarmels, 1989 Remartinia luteipennis 0 6 3 4 5 0 Burmeister, 1839 Rhionaeschna bonariensis 11 18 10 22 9 19 Rambur, 1842 Rhionaeschna cornigera 0 0 6 11 0 0 Brauer, 1865 Gomphidae Progomphus complicatus 0 6 0 0 0 0 Selys, 1854 * Phyllocycla sp. Calvert, 0 0 0 7 0 0 1948 Libellulidae Diastatops Intensa 0 3 0 4 2 0 Montgomery, 1940 Erythemis attala Selys in 0 23 18 22 15 41 Sagra, 1857 Erythemis plebeja 0 7 4 16 8 10 Burmeister, 1839 Erythemis peruviana Rambur 0 35 20 30 13 7 1842 Erythemis vesiculosa 0 0 1 5 0 4 (Fabricius, 1775) Erythrodiplax fusca Rambur, 21 16 9 31 10 30 1842 Erythrodiplax nigricans 0 18 0 24 0 2 Rambur, 1842 Erythrodiplax paraguayensis 5 0 3 7 4 2 Forster, 1904 Erythrodiplax atroterminata 30 20 27 28 12 33 Ris, 1911 Erythrodiplax chromoptera 0 0 0 7 4 0 Borror, 1942 Erythrodiplax media Borror, 14 38 32 20 29 23 1942 Erythrodiplax hyalina 10 6 8 19 1 5 Forster, 1907 Erythrodiplax sp. Brauer, 1 2 4 3 1 1 1868 Miathyria marcella Selys in 28 58 40 31 27 75 Sagra, 1857 Micrathyria tibialis Kirby, 0 0 2 1 0 1 1897 Micrathyria hypodidyma 33 51 39 30 30 22 Calvert, 1906 Micrathyria pseudeximia 8 23 10 9 17 14 Westfall, 1992 Micrathyria stawiarskii 0 0 4 1 1 2 Santos, 1953 Micrathyria catenata 0 2 0 5 1 0 Calvert, 1909 Orthemis nodiplaga Karsch, 1 8 0 16 9 12 1891 Orthemis ambinigra Calvert, 3 5 0 2 3 6 1909 Pantala flavescens 0 13 0 8 17 9 Fabricius, 1798 Perithemis mooma Kirby, 2 9 1 5 7 3 1889 Tauriphila risi Martin, 12 4 0 8 11 6 1896 Tauriphila xiphea Ris, 0 6 0 3 2 12 1913 * Tramea cophysa Hagen, 1867 2 5 0 3 1 3 Total 345 515 390 579 345 506 Total by County 860 969 851 Family/Species Total % Fr (2) Suborder Zygoptera Calopterygidae Hetaerina rosea Selys, 1853 19 0.671 IF Coenagrionidae Acanthagrion gracile 6 0.223 IF Rambur, 1842 Acanthagrion lancea Selys, 4 0.149 IF 1876 Homeoura chelifera Selys, 133 4.964 VF 1876 Homeoura ambigua Ris, 15 0.559 IF 1904 * Ischnura capreolus Hagen, 219 8.137 VF 1861 Ischnura fluviatilis Selys, 224 8.361 VF 1876 Oxyagrion terminale Selys, 24 0.895 IF 1876 Oxyagrion simile Costa, 5 0.186 IF 1978 Telebasis willinki Fraser, 183 6.830 VF 1948 Lestidae Lestes undulatus Say, 1839 35 1.306 IF Lestes tricolor Erichson, 27 1.007 IF 1848 Lestes minutus Selys, 8 0.298 IF 1862 * Suborder Anisoptera Aeshnidae Coryphaeschna amazonica 11 0.410 IF DeMarmels, 1989 Remartinia luteipennis 18 0.671 IF Burmeister, 1839 Rhionaeschna bonariensis 89 3.322 F Rambur, 1842 Rhionaeschna cornigera 17 0.634 IF Brauer, 1865 Gomphidae Progomphus complicatus 6 0.223 IF Selys, 1854 * Phyllocycla sp. Calvert, 7 0.261 IF 1948 Libellulidae Diastatops Intensa 9 0.335 IF Montgomery, 1940 Erythemis attala Selys in 119 4.441 VF Sagra, 1857 Erythemis plebeja 45 1.679 F Burmeister, 1839 Erythemis peruviana Rambur 105 3.919 F 1842 Erythemis vesiculosa 10 0.373 IF (Fabricius, 1775) Erythrodiplax fusca Rambur, 117 4.367 VF 1842 Erythrodiplax nigricans 44 1.642 F Rambur, 1842 Erythrodiplax paraguayensis 21 0.783 IF Forster, 1904 Erythrodiplax atroterminata 150 5.559 VF Ris, 1911 Erythrodiplax chromoptera 11 0.410 IF Borror, 1942 Erythrodiplax media Borror, 156 5.823 VF 1942 Erythrodiplax hyalina 49 1.829 F Forster, 1907 Erythrodiplax sp. Brauer, 12 0.485 IF 1868 Miathyria marcella Selys in 259 9.667 VF Sagra, 1857 Micrathyria tibialis Kirby, 4 0.149 IF 1897 Micrathyria hypodidyma 205 7.652 VF Calvert, 1906 Micrathyria pseudeximia 81 3.023 F Westfall, 1992 Micrathyria stawiarskii 8 0.289 IF Santos, 1953 Micrathyria catenata 8 0.289 IF Calvert, 1909 Orthemis nodiplaga Karsch, 46 1.717 F 1891 Orthemis ambinigra Calvert, 19 0.709 IF 1909 Pantala flavescens 47 1.754 F Fabricius, 1798 Perithemis mooma Kirby, 27 1.007 IF 1889 Tauriphila risi Martin, 41 1.530 F 1896 Tauriphila xiphea Ris, 23 0.858 IF 1913 * Tramea cophysa Hagen, 1867 14 0.522 IF Total 2 680 100 Total by County (1) Pelotas, Balneario dos Prazeres (PBP) and Vila Princesa (PVP). Capao do Leao, Irmao Teodoro Luis Botanical Garden (CHB) and Capao do Leao Campus of the Federal University of Pelotas--UFPel (CCL). Rio Grande Arroio Bolaxa (RAB) and TAIM Ecological Station (RET). (2) Frequency was indicated as follows: infrequent (IF), frequent (F) and very frequent (VF). * Newly-reported species in RS. TABLE 2 Number of Odonata species collected in the the Brazilian Pampa Biome (Southern region of Rio Grande do Sul) from each family, their percentage (%) in relation to the total of collected species and to the total of collected specimens Suborder Family Number of Percentage Density species (%) (%) Zigoptera Coenagrionidae 9 20.00 30.35 Lestidae 3 6.67 2.61 Calopterygidae 1 2.22 0.70 Anisoptera Libellulidae 26 57. 78 60.82 Aeshnidae 4 8.89 5.03 Gomphidae 2 4.44 0.49 Total 45 100 100 TABLE 3 Fauna data analyses of the species collected in all three cities in the Brazilian Pampa Biome Faunistic indexes Capao do Leao Pelotas Rio Grande Individuals (n) 969 860 851 Species diversity 42 36 40 Shannon-Wiener (H') 1.62 1.49 1.54 Chao-1 46.3 48.6 48.0