Diversity of Odonata (Insecta) in lotic systems from Serra da Bodoquena, Mato Grosso do Sul State, Brazil

BIOLOGY, ECOLOGY AND DIVERSITY

Diversity of Odonata (Insecta) in lotic systems from Serra da Bodoquena, Mato Grosso do Sul State, Brazil

Marina Schmidt Dalzochio^I; Janira Martins Costa^II; Manoel Araécio Uchôa^III

^ILaboratório de Ecologia e Conservação de Ecossistemas Aquáticos, Universidade do Vale do Vale do Rio dos Sinos, Av. Unisinos, 950, Cristo Rei, 93022–000 São Leopoldo-RS. [e-mail]

^IIDepartamento de Entomologia, Universidade Federal do Rio de Janeiro, Museu Nacional, Quinta da Boa Vista. São Cristovão, 20940–040 Rio de Janeiro-RJ, Brasil. [e-mail]

^IIIPrograma de Pós-Graduação em Entomologia e Conservação da Biodiversidade, Universidade Federal da Grande Dourados, Rodovia Dourados-Itaum km 12, Cidade Universitária, 79804–970 Dourados-MS, Brasil. [e-mail]

ABSTRACT

Diversity of Odonata (Insecta) in lotic systems from Serra da Bodoquena, Mato Grosso do Sul State, Brazil. A systematic survey was carried out in four lotic systems from Serra da Bodoquena, the largest natural forests of the State, from August 2007 to November 2008. 548 specimens belonging to 33 species, distributed in 5 families were sampled. Libellulidae was dominant, with 13 species, followed by Gomphidae, Coenagrionidae, Protoneuridae and Calopterygidae.

Keywords: Aquatic insects; Odonata community; Neotropical Region; species richness.

RESUMO

Diversidade de Odonata (Insecta) em sistemas lóticos da Serra da Bodoquena, Mato Grosso do Sul, Brasil. Um estudo sistemático foi realizado em quatro sistemas lóticos da Serra da Bodoquena, maior extensão de florestas naturais do estado, de Agosto de 2007 a Novembro de 2008. Foram coletados 548 espécimes pertencentes a 33 espécies, distribuídas em 5 famílias. Libellulidae foi dominante, com 13 espécies, seguida por Gomphidae, Coenagrionidae, Protoneuridae e Calopterygidae.

Palavras-chaves: Insetos aquáticos; comunidade de Odonata; Região Neotropical; riqueza de espécies.

One of the biggest problems for conservation in tropical forests is the lack of information allowing the establishment of priorities and concentration of efforts on practical actions. This is largely due to low availability of faunal inventories, which limits the knowledge of the distribution and abundance of species (De Marco & Vianna 2005). Faunal surveys are necessary for conservation, ecosystem management and environmental protection, not only as representations of biodiversity but also from organisms serving as indicators of environmental conditions. Such surveys have been particularly important in relation to estimate species richness in highly diverse groups such as insects (Kremen et al. 1993).

In this context, Odonata have been increasing, in recent years, as a tool to assess the health of aquatic ecosystems. Odonata are widely distributed in aquatic ecosystems and spend long periods in an aquatic immature stage, thereby allowing for an evaluation of the stability of the community and the environment (Von Ellenrieder 2000; Osborn 2005). The Odonata include insects known as dragonflies or damselflies and have about 6000 species worldwide (Kalkman et al. 2008). In Brazil, the Odonata fauna is estimated at around 800 species (Souza et al. 2007), approximately 48% of all species of the Neotropical Region. Unfortunately, only 29% of Brazilian territory presents data on Odonata species richness (De Marco & Vianna 2005). Some of our knowledge comes from the state of Mato Grosso do Sul, where the known fauna of Odonata is about 150 species, with the most information from the Pantanal region (Longfield 1929; Santos 1944; Souza et al. 2002; Heckman 2006, 2008; Souza & Costa 2006; Pessacq & Costa 2007). However, even this state lacks faunal information from many portions.

Serra da Bodoquena is one of the priority areas for conservation in the state of Mato Grosso do Sul, concentrating the largest natural forest of this state. The region's rivers have clear waters, which facilitates the observation and the study of underwater flora and fauna. However, there are few inventories of its aquatic insects. In the region, the known fauna of Odonata is only about 80 species, with inventories primarily from the northern portion of Serra da Bodoquena (according to records from Zoology Collection of Universidade Federal do Mato Grosso do Sul (ZUFMS) and Santos 1944).

The current work presents the Odonata species composition and richness in four rivers at Serra da Bodoquena. These data enhance additional information about Odonata in the region and can support future conservation and management strategies in the area.

MATERIAL AND METHODS

Characterization of the study area. Serra da Bodoquena (21º08'02" to 20º38'26"S and 56º48'31" to 56º44'28"W) is located in the mid-southern portion of Mato Grosso do Sul State, and extends from Miranda City to the north to Porto Murtinho City, to the south, including parts of Bodoquena, Bonito and Jardim (Ibama 2002) (Fig. 1). It is a plateau steeply sloping to the Pantanal, consisting by carbonatic rocks (Boggiani et al. 1998; Sallun-Filho et al. 2004). The region is characterized by a mountain-chain (Boggiani et al. 1998), with altitudes that vary between 450 and 800 m. 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 highest rainfall occurs during October to April, with periods of drought during May to September (PCBAP 1997). Native vegetation is formed by deciduous and semideciduous Atlantic forest, Cerrado and savanna (Furtado et al. 1982; Scremin-Dias et al. 1999). The hydrography of the region is characterized by limestone Rivers with high alkalinity and low turbidity. The region is part of the Paraguay River basin and is fed by streams such as the Salobra, Prata, Perdido, Formoso, Sucuri and Aquidaban.

The Serra da Bodoquena are located biogeographically in the central portion of a Neotropical Region called "Chaqueño" (sensu Morrone 2004), which includes continuous biomes (e.g. Caatinga, Cerrado, Chaco) to the Amazon and Atlantic forests. These biomes form a "Corridor of Savanna" between these forests and can therefore foster a heterogeneous biota comprised of both endemic taxa (of which there are relatively few in this area) as well as widespread species.

Collection sites. We sampled at four rivers in the Serra da Bodoquena: Perdido, Laudejá, Aquidaban and Salobra Rivers (Fig. 1). Two locations were sampled in each river, separated by 500 to 1000 m, with each sampling location covering about 50 m linear. Diversity in vegetation and structure among the sampling locations was designed to maximize potential Odonata species encounters.

Perdido River (21º26'59.04"S and 56º47'28.14"W – Fazenda Santa Maria do Rio Perdido – Municipality of Jardim) – This is a third-order river, a tributary of the Apa River. The points sampled consisted primarily of plant species characteristic of seasonal deciduous forest. The landscape around this forest is characterized by extensive areas of pasture. In this locality, the width of the river is about 20 m, with only marginal shading. The substrate is predominantly rocky, with coastal areas also containing sand and macrophytes (Myriophyllum sp.).

Laudejá River (21º07'12.62"S and 56º45'24.64"W – Fazenda Laudejá – Municipality of Bonito) – This is a fourth-order river, a tributary of the Perdido River. The sampling locations contained degraded riparian vegetation, and some area in regeneration, with late successional forest. It is surrounded by large area of pasture. One of the samples was located in an area with cattle and Cyperaceae. In this locality, the width of the river is about 15 m, with only marginal shading. The bottom substrate is predominantly sand, with little marginal vegetation. The depth varied according by season. In the rainy season (October to April), its average depth was 2.60 m. In the dry season (May-September), its depth reached the maximum of 0.80 m.

Aquidaban River (21º03'10.1"S and 56º55'36.5"W – Indian Village São João – Municipality of Porto Murtinho) – This is a third-order river, a tributary of the Paraguay River. This area was mainly composed of plant species of great size and characteristic of seasonal semi-deciduous forest and Cerrado. The surrounding landscape is characterized by forest in an advanced stage of regeneration. In this transect, the width of the river is approximately 8 m, with a great deal of shading, thereby restricting vegetational growth in the understory. The bottom substrate is composed of sand, gravel and leaf litter.

Salobra River (20º40'22.67"S and 56º44'49.46"W – settlement Canaan – Municipality of Bodoquena) – This is a third-order river, a tributary of the Miranda River. This sampling locality was quite degraded, with some areas completely without vegetation and others in early stages of regeneration. The landscape around this river is characterized by extensive areas of pasture, with some areas flooding during the rainy season, and pools and dams for cattle. The width of the river is about 15 m, with little shading, especially from trees of greater size. The bottom substrate is composed of pebbles and aquatic macrophytes attached to a sandy bottom.

Data collection. The inventory was carried out bimonthly, conducted between 30 August 2007 and 25 November 2008. For a comprehensive inventory, adult and immature species were collected. Adults were collected with entomological nets and packed live into rectangular envelopes (12 x 8 cm) of thin paper, following Lencioni's (2005) methodology. The sampling effort consisted of an active search, usually lasting between 9 and 15 hours of the day, always by the same person. The immatures were collected with a metal sieve with 30 cm diameter mesh and 5 mm openings. Immature samplings were standardized by set of 20 sieved samples. We particularly focused on collecting adults and larvae in the last instar in order to be able to determine sex. The immatures were brought alive to the laboratory to be reared to adulthood for accurate identification to species. The specimens were nominally recognized to the level of genus and species when possible. Identification of adults followed the works of Carvalho & Calil (2000), Costa et al. (2002), Lencioni (2005, 2006), Garrisson et al. (2006) and Heckman (2006, 2008), and identification of immatures followed the works of Carvalho et al. (2002) and Costa et al. (2004). The collected material is deposited in the Entomological Collection of the Museum of Biodiversity in the Universidade Federal da Grande Dourados (UFGD) and in the National Museum in the Universidade Federal do Rio de Janeiro (UFRJ), Brazil.

Analysis of data. The species richness (S) observed in each stream was calculated by aggregating the collected data from adults and immatures that were identified through comparison with emerged immatures or by association. To determine the species richness sampled in the Serra da Bodoquena, all data from the four rivers' transects were combined. The estimated number of species in each stream was calculated using the estimator Jacknife of 2^nd order, because it is considered the best estimation method for aquatic environments (Melo & Froelich 2001). Species accumulation curves were plotted for each site and for all sites pooled. All analyses were performed with the aid of the statistical program EstimateS 8.0 (Colwell 2006).

RESULTS

Faunal composition. In Serra da Bodoquena, we collected 548 specimens of 33 species (see Table I), distributed in 5 families. Libellulidae was the most dominant, with 13 species, followed by Gomphidae (8 species), Coenagrionidae (7 species), Protoneuridae (4 species) and Calopterygidae (1 species). The most dominant genera were Acanthagrion Selys, 1876, Erythrodiplax Brauer, 1868, Macrothemis Hagen, 1868and Progomphus, with 3 species each (A. aeopilum, A. gracile, A. chararum, E. fusca, E. paraguayensis, E. umbrata, M. hemichlora, M. heteronyncha, M. imitans, P. intricatus, Progomphus sp1 and sp2), following by Neoneura Selys, 1860 with 2 species (N. ethela and N. sylvatica).

The most abundant species was Hetaerina rosea (Calopterygidae) (Δ = 138), following by Phyllocycla sp. (Gomphidae) (Δ = 98) and Argia indocilis (Coenagrionidae) (Δ = 88).

Species Richness. The Aquidaban River showed the largest number of species (S = 25), followed by Salobra River (S = 20) and Laudejá River (S = 17). The Perdido River presented the lowest species richness (S = 11) (Table I).

The collector's curves (Fig. 2), when plotted for each river, show that in the first three expeditions, significant in number of species were added, generating a pronounced upward line. The collector's curve started its trend of stability from the 5th sample. The same is observed when the collector's curve for all sites is plotted (Fig. 3), where about 50% of species (17 of 33 species collected) in the Serra da Bodoquena were already collected by the 2nd or 3rd survey. The collector's curve started its trend of stability (asymptote) from the 5th sample, when about 75% of species were obtained (Fig. 3).

Estimated Species Richness. The analysis of Jackknife 2nd estimated that the all species collected had reached a total of 51 species on the Serra da Bodoquena. As noted, Aquidaban River have shown the largest number of species (Sej = 41), followed by Salobra River (Sej = 33) and Laudejá River (Sej = 29) and Perdido River (Sej = 20) (Table II).

The species accumulation curve (e.g. species estimated) when plotted for each river showed a tendency to stabilize in the same way that as noted in collector's curves (Fig. 4). The accumulation curve started its trend of stability (asymptote) from the 5th sample, when about 95% of species were obtained (Fig. 3). The ratio analysis indicated that 12 samples would be needed to reach the possible number of species.

Rare species. From the total of 33 species collected in all the sampled rivers, six species were represented by a single individual (singletons) (Telebasis sp., Epipleoneura venezuelensis, Cyanogomphus sp., Gomphoides infumata, Macrothemis heteronyncha and Perithemis mooma)and two by two individuals (doubletons) (Archaeogomphus sp. and Erythemis vesiculosa). Fourteen species were found only in one of the sampled rivers (uniques) (Acanthagrion aeopilum, Acanthagrion gracile, Acanthagrion chararum, Telebasis sp., Epipleoneura venezuelensis, Cyanogomphus sp., Gomphoides infumata, Progomphus intricatus, Progomphus sp. 1 and sp. 2, Erythemis vesiculosa, Macrothemis heteronyncha, Micrathyria longisfasciata and Perithemis mooma and six were found in two sampled rivers (duplicates) (Archaeogomphus sp., Brechmorhoga sp., Macrothemis hemichlora, Macrothemis imitans and Orthemis sp.). The river that contained the most singletons species was the Aquidaban River (11 spp.) (Enallagma novaehispanie, Telebasis sp., Neoneura ethela, Peristicta muzoni, Archaeogomphus sp., Cyanogomphus sp., Gomphoides infumata, Erythrodiplax paraguayensis, Erythrodiplax umbrata, Macrothemis heteronyncha, Perithemis mooma) (Table II). Nine species were unique to the Aquidaban River: Acanthagrion aeopilum, Cyanogomphus sp., Erythemis vesiculosa, Gomphoides infumata, Macrothemis heteronyncha, Progomphus intricatus, Perithemis mooma and Progomphus sp. 1 and sp. 2. Four species were unique to the Rio Salobra: Acanthagrion gracile, Acanthagrion chararum, Epipleoneura venezuelensis and Micrathyria longifasciata. The Laudejá River had only 1 unique species: Telebasis sp., and the Perdido River had no unique species (Table I).

DISCUSSION

Faunal Composition. Libellulidae (S = 13) was most diverse family, containing about 40% of all collected specimens. A comparison with other studies on the diversity of Odonata shows that this pattern is common in the Neotropical Region. In São Paulo State (Costa et al. 2000) and Espírito Santo State, for example, about 50% of the known species belong to this family (Costa & Oldrini 2005). Recent papers such as Anjos-Santos & Costa (2006), Souza & Costa (2006) and Muzón et al. (2008) have also found a high number of species from this family. This pattern is attributed to the generally large body size of the species in this family, which increases vagility and consequently dispersion and distribution. Furthermore, in larger species, thermoregulation is made possible by solar radiation (May 1979, 1991), and thus they are more frequently found in open areas. In species of smaller body size, as in the diverse and abundant Zygoptera suborder, thermoregulation seems to be by convection (due to smaller body size) (May 1979, 1991), thereby permitting occupation of shaded places such as forest. Given that most of our sampling areas were mainly surrounded by open areas (pasture) and degraded riparian forest, it is to be expected that species of the suborder Anisoptera (the larger-bodied species) are predominant in Serra da Bodoquena.

In addition, Kalkman et al. (2008) assumes that some genera of Neotropical Odonata are more diverse in high altitudes, due to the particular climate that creates a wide variety of habitats. The author explains that genera like Argia, Heteragrion, Palaemnema, Acanthagrion, Telebasis, Phyllogomphoides, Progomphus, Erythrodiplax and Micrathyria are easier to be found in hilly areas. This probably contributes to the high diversity observed in some genera found in this study, as Acanthagrion, Erythrodiplax and Progomphus.

Species richness. The diversity of tropical Odonata species is, in part, explained by the high diversity of aquatic environments in tropical forests (Orr 2006). The pattern of species richness found in our study is probably due to the physical characteristics of the studied rivers and the degree of surrounding landscape heterogeneity. Within some of the factors cited as influencing Odonata species richness (see Vannote et al. 1980; Minshall 1984; Townsend 1989; Ward 1992; Clenaghan et al. 1998; Jonsen & Taylor 2000; Puth & Wilson 2001; Cortes et al. 2002; Wiens 2002), certainly the amount and diversity of microhabitat within a given stretch of the river seem to be important. The immature stages of many species of Odonata inhabit various types of aquatic environments, but in most cases, exhibit preferences for specific types of habitats and substrates (Carvalho 1999), moreover, most adults exhibit territorial behavior, while remaining near the streams from which they emerged. Thus, the characteristics of rivers reflect as much on the species richness as does the quality of the surrounding terrestrial environment. The Aquidaban River had the highest species richness and highest estimated number of species (S = 25 respectively), possibly because this site possessed the greatest number of microhabitats (sand, rocks and leaf litter), thereby allowing the establishment of a greater number of species and consequently resulting in greater diversity. Along these lines, the Perdido River is relatively homogeneous in terms of substrate (mainly stones and isolated macrophytes), restricting the established number of species; the same was observed for the other rivers.

Rare species. The number of singletons and doubletons observed in this work (6 and 2 species, respectively) may have been directly influenced by our sampling method because the active method of adult capture can result in a high probability of recording "vagrant" species of low abundance (i.e., rare species). Indeed, most of the rare species we encountered were not collected as immatures. Moreover, the catch by this method can be highly dependent on the ability of the collector (Uieda & Castro 1999) as well as the flight capacity and agility of the species. The high number of species observed in only one river (Aquidaban River) was likely directly influenced by substrate. Gomphidae, for example, sampled in this river, tend to occur in waters with vegetation along the margins or protected springs with sandy substrates and moderately stable hydrological cycles.

Overall, these numbers of Odonata species demonstrate the need for more intensive surveys to document the complete fauna of Odonata in the Serra da Bodoquena; the information in this paper will hopefully help in the development of strategies on conservation and preservation of this unique biome.

ACKNOWLEGMENTS

We thank the staff of the Programa de Pós-Graduação em Entomologia e Conservação da Biodiversidade, Universidade Federal da Grande Dourados (UFGD), to IBAMA for the facilities given to our project, to Dr. Nancy E. McIntyre for the corrections and to the National Counsel of Technological and Scientific Development (CNPq) for the grant to MSD.

Received 16/6/2009;

accepted 4/11/2011

Editor: Mauricio Osvaldo Moura

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Publication Dates

• Publication in this collection
  02 May 2011
• Date of issue
  Mar 2011

History

• Received
  16 June 2009
• Accepted
  04 Nov 2011