Distribution patterns of riodinid butterflies (Lepidoptera: Riodinidae) from southern Brazil
© Siewert et al.; licensee Springer. 2014
Received: 14 October 2013
Accepted: 27 February 2014
Published: 12 March 2014
The aim of this study was to synthesize the knowledge of Riodinidae butterflies (Lepidoptera: Papilionoidea) in Rio Grande do Sul state (RS), southern Brazil, evaluating the role of climatic, topographic, and vegetational variables on the observed patterns of occurrence and distribution of these butterflies in the Pampa and Atlantic Forest biomes. The records of riodinid butterflies in RS were collected from published studies and the examination of museum collections in Brazil.
A total of 97 taxa of Riodinidae were recorded, distributed in 92 municipalities. The NMDS analysis and the Constrained Analysis of Principal Coordinates grouped the municipalities according to the phytogeographic regions and biomes - Pampa and Atlantic Forest domains - in which the species records were made. Distance from the ocean, precipitation and temperature were the environmental variables which most contributed to explain the distribution patterns of these butterflies. The multivariate Mantel correlogram suggests that over short distances, the composition of species shows significant levels of spatial autocorrelation, and as geographic distance increases, these levels tend to present negative values.
The results suggest that the observed distribution pattern of Riodinidae in the different biomes and phytogeographic regions in the extreme southern Brazil could be explained by climatic, environmental variables and geographic distance.
KeywordsAtlantic forest Occurrence Pampa Spatial autocorrelation
The distribution of insects is highly influenced by a combination of factors, such as climate, vegetation and topography (Wolda 1988; Goldsmith 2007; Bonebrake and Deutsch 2012). Environmental heterogeneity can derive from the variation of the abovementioned factors across time and space, shaping the patterns of occurrence and diversity of these organisms. Butterflies are closely associated with a variety of biotic and abiotic variables, being a useful group for environmental diagnosis and identification of priority areas for conservation (Brown and Freitas 2000a). Moreover, butterflies are reasonably easy to sample, some taxa have relatively well-known taxonomy and may be considered a charismatic group. For all these features, some butterfly groups can be used as flagships in biodiversity conservation (New 1997; Brown and Freitas 1999; Freitas 2010). However, there is a paucity of knowledge and a lack of studies concerning general patterns of distribution in tropical butterflies on large scales, especially in Brazil (see Bonebrake et al. 2010 for more details).
Riodinid richness is highly concentrated in the neotropics, with 95% of the species (c.a. 1,300) occurring in this region (DeVries 1997; Hall 2002). These butterflies are generally associated in restricted to specific microhabitats and may be spatially rare with low population densities, even if showing, in some cases, wide distributions (Callaghan 1978; Brown 1992; DeVries 1997). For example, the genus Seco Hall and Harvey 2002 is restricted to xeric habitats (Hall and Harvey 2002a), while some species from Euselasia only occur in wet environments (e.g. Nishida 2010) and most Aricoris species are linked to grasslands habitats in vast areas of South America. Despite being the second most diverse family (after the Nymphalidae), Riodinidae is a poorly studied group among the butterflies (Hall and Harvey 2002b). Natural history and basic aspects of its biology, such as life history and morphology, are unknown for most species (85% to 87%, Hall et al. 2004; Kaminski 2008). The little knowledge available, however, points to a high habitat specificity of the riodinid butterflies and the sheer number of species present in a given site may be a good indicator of environmental health.
Brazil is one of the three countries with the largest richness of Neotropical butterflies, with more than 3,200 estimated species (Brown and Freitas 1999). However, there is a lack of inventories, especially taking into account its great diversity of biomes. Most of the surveys are concentrated in the Atlantic Forest domain, and many regions of the Brazilian territory still require much sampling effort (Marini-Filho and Freitas 2011). When compared to other Brazilian states, the butterfly fauna of Rio Grande do Sul, the southernmost state of Brazil, is relatively well known and studied (Santos et al. 2008). In particular, few other parts of the country were ever surveyed since as early as the end of the 19th and beginning of the 20th centuries. Most recently published inventories are related to Atlantic Forest habitats (Teston and Corseuil 1999,2000,2002; Corseuil et al. 2004; Iserhard and Romanowski 2004; Giovenardi et al. 2008; Grazia et al. 2008; Bonfantti et al. 2009; Romanowski et al. 2009; Iserhard et al. 2010; Pedrotti et al. 2011; Ritter et al. 2011; Santos et al. 2011; Bellaver et al. 2012; Morais et al. 2012), and the major gaps of information concern the Pampa (native grasslands), a biome restricted in Brazil to its extreme south and which covers about 2% of its surface, extending through Uruguay and northwest Argentina (Bencke 2009; Pillar et al. 2009), exclusive to austral South America.
This study aimed (1) to compile and upgrade a species list of riodinid of this extreme southern Brazilian state, (2) to identify environmental variables that shape the patterns of occurrence and distribution of Riodinidae in this region, and (3) to compare the species composition of these butterflies among the different phytogeographic regions in Atlantic Forest and Pampa from southern Brazil.
The records of riodinid butterflies were collected from published studies (Mabilde 1896; Azzará 1978; Biezanko et al. 1978; Ruszczyk 1986; Hall and Harvey 2001,2002a; Krüger and Silva 2003; Iserhard and Romanowski 2004; Marchiori and Romanowski 2006a, b; Dessuy and Morais 2007; Sackis and Morais 2008; Giovenardi et al. 2008; Bonfantti et al. 2009; Iserhard et al. 2010; Siewert et al. 2010,2014; Fronza et al. 2011; Ritter et al. 2011; Rosa et al. 2011; Morais et al. 2012; Bellaver et al. 2012; Dolibaina et al. 2013; Dias et al. 2013) and the examination of museum collections in Brazil, as follows: Centro de Pesquisa Agropecuária Clima Temperado da Embrapa (CAMB), Museu de História Natural da Universidade Católica de Pelotas (MUCP), Museu de Ciências Naturais Carlos Ritter (MNCR), and Museu Entomológico Ceslau Biezanko (MECB), in Pelotas, Museu Anchieta de Porto Alegre (MAPA), Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul (MCTP), Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul (MCNZ), Museu Ramiro Gomes Costa da Fundação Estadual de Pesquisa Agropecuária (MRGC) and Coleção de Lepidoptera do Departamento de Zoologia da Universidade Federal do Rio Grande do Sul (CLDZ), in Porto Alegre, Coleção de Lepidoptera Alfred Moser (CLAM), in São Leopoldo, Museu e Arquivo Histórico Professor Hermann Wegermann (MAHP) in Panambi, and Departamento de Zoologia da Universidade Federal do Paraná (DZUP), in Curitiba. The collections of Museu de Zoologia da Universidade Federal de São Paulo, in São Paulo (MZSP), Museu Nacional da Universidade Federal do Rio de Janeiro, in Rio de Janeiro (MNRJ), and Coleção de Lepidoptera do Museu de Zoologia da Universidade Estadual de Campinas, in Campinas (ZUEC), were also consulted but there were no Riodinidae from RS in any of them.
All identifications and nomenclature of museum specimens were checked and revised, and for each specimen, the municipality, geographical coordinates, and reference collection were recorded. As reported by Ferro and Melo (2011), geographical coordinates were not available for most museum specimens, and thus, we used geographical coordinates from the municipality nearest to the point in which the specimen was collected, obtained by the GeoLoc tool for the information system ‘splink’, available from the Reference Center on Environmental Information (http://splink.cria.org.br/geoloc). The specimens were identified from D’Abrera (1994), comparison with types from the Butterflies of America project (http://www.butterfliesofamerica.com/L/Neotropical.htm) and by specialists. The nomenclature follows Callaghan and Lamas (2004).
The dataset used was plotted in cells of 27 × 27 km using the Diva-GIS 7.5 software (Hijmans et al. 2001), so that the spatial patterns of species richness through RS could be determined. To verify if the species richness per cell was correlated with the number of sites sampled on a cell, a Spearman correlation was performed.
To reduce the noise in the statistical analysis, we selected the 25 best-sampled municipalities for assessing all the eight phytogeographic regions (according to Cordeiro and Hasenack 2009) and its climatic and geographical combined factors. The similarities in riodinid species composition among the phytogeographic regions were performed through a non-metric multidimensional scaling (NMDS, Clarke 1993), in which the sampling units were the municipalities. The data matrix generated was calculated using the Simpson beta-diversity index (βsim), which takes into account only the difference in species composition among samples, reducing any variation in sampling effort in different sites (Koleff et al. 2003). To test for differences in riodinid species composition, an analysis of similarities (ANOSIM) based in 10,000 permutations was used (Clarke and Warwick 1994).
To evaluate the effect of climatic and geographical factors on riodinid species composition, five environmental variables were included: (1) average monthly temperature, (2) daily range of temperature, (3) annual precipitation, (4) altitude, and (5) distance from the ocean (a measure of continentality). We choose these variables based on their importance to the description of the structure of lepidopteran assemblages in the Neotropical region (e.g., Brown and Freitas 2000a, b; Ferro and Melo 2011). The climatic variables were selected from the WorldClim database (Hijmans et al. 2005) in a resolution of 2.5 arc min (approximately 5 km). The distance to the ocean was obtained through the minimum distance between the coast and the municipalities. A Constrained Analysis of Principal Coordinates (CAPC, Anderson and Willis 2003) was used based on a dissimilarity matrix employing the Simpson beta-diversity index. The significance of the axes generated by CAPC was tested by an ANOVA based in 10,000 permutations (Legendre and Legendre 1998).
The spatial autocorrelation between sampling sites was assessed using a multivariate Mantel correlogram (Legendre and Legendre 1998; Borcard and Legendre 2012). A matrix based on species composition of each municipality using the Sørensen index as a measure of distance was built. This matrix was evaluated in relation to a geographic distance matrix in which for each municipality, eight distance classes were quantified, and a respective value of Pearson’s R statistic was assigned. This analysis was performed to determine whether closest locations were more similar in species composition of Riodinidae, showing a positive autocorrelation, or less similar, showing a negative autocorrelation (Legendre and Legendre 1998). The significance of the correlogram was tested with 10,000 permutations.
The Mantel correlogram was computed with the software Spatial Analysis in Macroecology (SAM) version 4.0 (Rangel et al. 2010), other analyses were performed using the ‘vegan’ package (Oksanen et al. 2008) on the software R version 2.15 (R Development Core Team 2012).
A total of 97 taxa (Additional file 1) of Riodinidae recorded from 92 municipalities on RS were gathered (Additional file 2), belonging to Euselasiini (6 spp), Eurybiini (3 spp), Helicopini (1 spp), Mesosemiini (5 spp), Nymphidiini (31 spp), Riodinini (29 spp), Symmachiini (11 spp), and Incertae Sedis (11 spp). Fourteen species are unpublished records, and for each municipality, the richness ranged from 1 to 37 species.
Environmental variables and its correlations in the Constrained Analysis of Principal Coordinates
Distance from ocean
Daily range of temperature
Average monthly temperature
The distribution pattern of Riodinidae in the different biomes and phytogeographic regions in the extreme southern Brazil observed could be explained by climatic, environmental variables and geographic distance. The richness of Riodinidae recorded in this study represents 12.8% from the estimated total of this butterfly family in Brazil (Brown and Freitas 1999), 7.9% in the Neotropical region, and 7.5% in the global fauna (Hall 2002). The high number of unpublished records (approximately 18%) for the extreme southern region in Brazil corroborates the study developed by Morais et al. (2007) with butterflies in austral South America, in which Riodinidae, Lycaenidae, and Hesperiidae are the families which take longer to reach sampling sufficiency. Thus, these are likely to have the larger number of new occurrences to be registered in southern Brazil, and in the Neotropical region as a whole.
The grids which contained the higher number of species richness were located on the Atlantic Forest domain and in the ecotone between this biome and Pampa. On the other hand, the records of Riodinidae in Pampa are quite sparse, leaving significant gaps to be investigated. In general, this scenario is common for all butterfly families present in Pampa (Rosa et al. 2011). An important aspect should be considered: the well-sampled sites are reported in areas with an amount of researchers and established research institutions (mainly represented by universities) near the state capital (Porto Alegre) or their main research project sites (Iserhard and Romanowski 2004; Marchiori and Romanowski 2006a, b; Iserhard et al. 2010; Bellaver et al. 2012). In Brazil, this pattern is similar for all butterfly fauna, in which the counties that contain more inventories and higher values of species richness are located in areas surrounding important research centers, greatly limiting the access and exploitation to few and limited areas (Santos et al. 2008).
The NMDS result showed similar patterns to those found by Ferro and Teston (2009) for the Arctiidae assemblages in the same region in southern Brazil, but in a more restricted scale: grassland environments had a distinct fauna than that occurring in forested areas. In fact, the composition and occurrence of Lepidoptera are strongly associated with gradients of vegetation (e.g., Brown and Gifford 2002; Summerville et al. 2001); although, in this study, most records were concentrated in regions of Atlantic Forest, it was possible to observe differences on the composition of riodinid between Pampa and Atlantic Forest sites. This result is not surprising given that, when compared, these two biomes have very distinct habitats and formations, floristic composition, and structure and architecture of vegetation and suffer influences of different subsets of abiotic factors segregating, in this way, the riodinid fauna.
The riodinid species composition grouped by phytogeographic regions in areas of the Atlantic Forest domain were not well defined, except for sites located on the ecological tension area. The lack of sampling effort in sites on the Seasonal Semideciduous Forests and the occurrence of the most frequent Riodinidae species in all phytogeographic forested regions (not helping to recognize differences in vegetation in this scale of evaluation) are possible explanations for these patterns. In this study, two common riodinid species whose presence indicates an especially rich environment were recorded for the first time in the Atlantic Forest of this Brazilian region: Euselasia zara and Symmachia arion (Brown and Freitas 2000b). The Atlantic Forest domain is a highly threatened biome due to changes and depletion of their native habitats over time, and actually less than 7.5% of their original extension remains, broken into small and sparse fragments (Myers et al. 2000; Ribeiro et al. 2009). Brown and Freitas (2000a) recorded 368 species of Riodinidae for the Brazilian Atlantic Forest, and about 40% are endemic to this biome, emphasizing the importance of conserving these remaining fragments to the maintenance of biological diversity. On the other hand, the grouping of butterflies according to the phytogeographic regions present in the Pampa indicate a peculiar composition related to each open grassland habitat and to the endemism of some species found in the present study. These results reinforce the fact that different Pampa habitat types are unique and diverse with large levels of endemism and biodiversity (Pillar et al. 2009).
Emphasizing the abovementioned results, an important record related to an endemic species in the Rio Grande do Sul was found: Stichelia pelotensis was collected only twice, through a historical record in the extreme southern region of this state, near the boundaries with Uruguay in the 1950s and one recent collection (in 2001) from the vicinities of the state capital in a protected area in the Rio Grande do Sul east region, located in the Coastal Plain. Probably, this species is distributed only in this region in Brazil, since records were made in a narrow range concerning the extreme southern Brazilian Coastal Plain in ‘Restinga’ forest and ‘Butiazal’ formation, the latter being a peculiar and exclusive physiognomy in this region. These environments have been suffering intense modification due to irregular settlements and building, so their depletion and fragmentation can bring irreversible consequences to riodinid butterflies.
Several species of Riodinidae present a restricted spatial distribution given their population rates being lower than other butterflies and tending to high fluctuations, which make them easily threatened by the loss of native areas (New 1993). In addition, they are difficult to sample in short periods of time. In southern Brazil, the natural grasslands are being increasingly converted into areas for agriculture, silviculture, and livestock grazing. The Pampa biome has less than 0.5% of its area included in protected areas (Overbeck et al. 2007). Thus, not only Riodinidae but also all butterflies in close association with this vegetation may be threatened, and the first step to their conservation ought to be the creation of new legal protected areas (Overbeck et al. 2007; Dolibaina et al. 2011).
Climatic and geographical factors are important to describe patterns of structure of butterfly communities (Brown and Freitas 2000a). In our study, distance from the ocean, precipitation, and temperature were the most important variables which explain the variation of the riodinid assemblages in the Atlantic Forest. Altitude was another important factor, grouping sites characterized by the presence of the Mixed Ombrophilous Forest (Araucaria angustifolia Forest), a type of vegetation exclusive of the south Brazilian region. In Atlantic Forest, the montane forests, such as Araucaria Forest sites, seem to present a higher similarity on its floristic composition (e.g., Oliveira-Filho and Fontes 2000; Garcia et al. 2009; Urbanetz et al. 2010), which may be influencing the patterns of occurrence of some lepidopteran species (e.g., Brown and Freitas 2000a; Ferro and Melo 2011).
All municipalities in the Pampa biome, in the southern portion of the south region, were associated with the range of temperature. In fact, areas further from the equator present wide ranges of temperature, reflecting a decrease in species along a latitudinal gradient (see Hillebrand 2004). The study area lies in a transition zone between tropical and temperate climate (Overbeck et al. 2007), showing marked seasonality with four defined seasons. The richness of Riodinidae seemed to be correlated with warmer temperatures, presenting high values in Amazonia and in areas of Atlantic Forest in southeast Brazil (Brown 2005). Thus, the lower richness of Riodinidae in Pampa when compared with other sites near the equator, may be associated, beyond the lack of specific inventories, to the influence of a latitudinal gradient.
As geographical distance increases, the similarity in environmental factors decays across landscapes and the species composition of Riodinidae as well (e.g., Nekola and White 1999). The overall shape of the correlogram could be attributed either to a species gradient or to environmental factors (Legendre and Fortin 1989), corroborating the previous multivariate analysis.
It is important to note that our database was constructed mainly with museum data, and in many cases, its use should be carefully interpreted because of the bias regarding the different sampling efforts (Ponder et al. 2001; Graham et al. 2004; Moerman and Estabrook 2006). Similarly, Ferro and Melo (2011) also used museum data to describe the diversity of tiger moths in the Brazilian Atlantic Forest and discussed this aspect. Even so, both their results and ours seem quite robust. The information yielded indicates a structure for the riodinid assemblages of southern Brazil similar to that described for the tropical lepidopteran fauna (e.g., Brown and Freitas 2000b).
Despite the fact that the extreme southern Brazil has been considered one of the better sampled regions for butterfly surveys (Santos et al. 2008), it is important to emphasize the need to intensify specific and well-sampled inventories. Thus, it is possible to more accurately evaluate patterns of structure, distribution, and composition of butterflies, to generate data for larger scales of evaluation in the Neotropical region, reaching the level of macroecology. This study may be seen as reflecting the current knowledge on the Riodinidae fauna in an austral South American region, and we suggest these same variables may also affect the distribution of the taxon in other parts of the neotropics as well. The data on Riodinidae species distribution show variable degrees of endemism in unprotected areas, providing subsidies to a better assessment directed towards conservation schemes and public policies to justify the maintenance of protected areas and, mainly, the proposal and creation of others.
We are grateful to Olaf HH Mielke (DZUP), Eduardo JE Silva (MECB), Gervásio S Carvalho (MCTP), Maria Helena S Vaz (MUCP), Mirtes Melo (CAMB), César J Drehmer (MNCR), Vera Regina S Wolff (MRCG), Têmia Wehrmann (MAHP), Fernando Meyer (MAPA), and Maria Helena M Galileo (MCNZ) for providing access to the collections and to Milton S Mendonça Jr, Viviane G Ferro, Márcio B Martins and the two anonymous reviewers for the critical reading of the manuscript. We are also in debt to Jason Hall, Lucas A Kaminski, Diego R Dolibaina, and Fernando MS Dias for their essential help in the identification and information on some specimens. RRS received a master fellowship from the CAPES. HPR received a research fellowship from CNPq (Proc No. 307635/2010-4). CAI received a post-doctoral fellowship from Fundação de Amparo a Pesquisa do Estado de São Paulo (Fapesp – 2011/08433-8). This paper is part of the Pampa e Mata Atlântica Sul subproject of the RedeLep “Rede Nacional de Pesquisa e Conservação de Lepidópteros” SISBIOTA-Brasil/CNPq (563332/2010-7).
- Anderson MJ, Willis TJ: Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 2003, 84: 511–525. 10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2View ArticleGoogle Scholar
- Azzará ML: Revisão do gênero Barbicornis Godart, 1824 (Lepidoptera, Lycaenidae, Riodininae). Acta Biol Parana 1978, 7: 23–69.Google Scholar
- Bellaver JM, Iserhard CA, Santos JP, Silva AK, Torres M, Siewert RR, Moser A, Romanowski HP: Borboletas (Lepidoptera: Papilionoidea e Hesperioidea) de Matas Paludosas e Matas de Restinga da Planície Costeira da região Sul do Brasil. Biota Neotrop 2012,12(4):181–190. 10.1590/S1676-06032012000400019View ArticleGoogle Scholar
- Bencke GA: Diversidade e conservação da fauna dos campos do sul do Brasil. In Campos Sulinos: Conservação e Uso Sustentável da Biodiversidade. Edited by: Pillar VP, Müller SC, Castilhos ZMS, Jacques AVA. Ministério do Meio Ambiente, Brasília; 2009:101–121.Google Scholar
- Biezanko CM, Mielke OHH, Wedderhoff A: Contribuição ao estudo faunístico dos Riodinidae do Rio Grande do Sul, Brasil (Lepidoptera). Acta Biol Parana 1978,7(1/4):7–22.Google Scholar
- Bonebrake TC, Deutsch CA: Climate heterogeneity modulates impact of warming on tropical insects. Ecology 2012,93(3):449–455. 10.1890/11-1187.1View ArticleGoogle Scholar
- Bonebrake TC, Ponisio LC, Boggs CL, Ehrlich PR: More than just indicators: a review of tropical butterfly ecology and conservation. Biol Conserv 2010, 143: 1831–1841. 10.1016/j.biocon.2010.04.044View ArticleGoogle Scholar
- Bonfantti D, Di Mare RA, Giovenardi R: Butterflies (Lepidoptera: Papilionoidea e Hesperioidea) from two forest fragments in northern Rio Grande do Sul, Brazil. Checklist 2009,5(4):819–829.Google Scholar
- Borcard D, Legendre P: Is the Mantel correlogram powerful enough to be useful in ecological analysis? A simulation study. Ecology 2012, 93: 1473–1481. 10.1890/11-1737.1View ArticleGoogle Scholar
- Brown KS Jr: Borboletas da Serra do Japi: diversidade, hábitats, recursos alimentares e variação temporal. In História Natural da Serra do Japi: Ecologia e preservação de uma área florestal no sudeste do Brasil. Edited by: Morellato LPC. Editora da UNICAMP, Campinas; 1992:142–187.Google Scholar
- Brown KS Jr: Geological, evolutionary and ecological bases of the diversification of Neotropical butterflies: implications for conservation. In Tropical rainforests: past, present and future. Edited by: Bermingham E, Dick CW, Moritz C. University of Chicago Press, Chicago; 2005:166–201.Google Scholar
- Brown KS Jr, Freitas AVL: Lepidoptera. In Biodiversidade do Estado de São Paulo. Edited by: Brandão CRF, Cancello ED. Brasil. Invertebrados Terrestres. FAPESP, São Paulo; 1999:225–245.Google Scholar
- Brown KS Jr, Freitas AVL: Atlantic Forest butterflies: indicators for landscape conservation. Biotropica 2000a, 32: 934–956.View ArticleGoogle Scholar
- Brown KS Jr, Freitas AVL: Diversidade de Lepidoptera em Santa Teresa, Espírito Santo. Bol Mus Mello Leitão 2000b,11(12):71–118.Google Scholar
- Brown KS Jr, Gifford DR: Lepidoptera in the cerrado landscape and the conservation of vegetation, soil and topographical mosaics. In The Cerrados of Brazil: ecology and natural history of a Neotropical savanna. Edited by: Oliveira PS, Marquis RS. Columbia University Press, New York; 2002:201–217.Google Scholar
- Callaghan CJ: Studies on restinga butterflies. II. Notes on the population structure of Menander felsina (Riodinidae). J Lepid Soc 1978, 32: 37–48.Google Scholar
- Callaghan CJ, Lamas G: Riodinidae. In Atlas of Neotropical Lepidoptera: Checklist: Part 4a Hesperioidea – Papilionoidea. Edited by: Lamas G. Scientific Publishers, Gainesville; 2004:141–170.Google Scholar
- Clarke KR: Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 1993, 18: 117–143. 10.1111/j.1442-9993.1993.tb00438.xView ArticleGoogle Scholar
- Clarke KR, Warwick RM: Similarity-based testing for community pattern: the two-way layout with no replication. Mar Biol 1994, 118: 167–176. 10.1007/BF00699231View ArticleGoogle Scholar
- Cordeiro JLP, Hasenack H: Cobertura vegetal atual do Rio Grande do Sul. In Campos Sulinos: Conservação e Uso Sustentável da Biodiversidade. Edited by: Pillar VP, Müller SC, Castilhos ZMS, Jacques AVA. Ministério do Meio Ambiente, Brasília; 2009:285–299.Google Scholar
- Corseuil E, Quadros FC, Teston JA, Moser A: Borboletas (Lepidoptera: Papilionoidea e Hesperioidea) coletadas no Centro de Pesquisa e Conservação da Natureza Pró-Mata. 4: Lycaenidae. Div Mus Ciênc Tecnol PUCRS 2004, 9: 65–70.Google Scholar
- D’Abrera B: Butterflies of the Neotropical region. Part VI, Riodinidae, Hill House, Victoria; 1994.Google Scholar
- Dessuy MB, Morais ABB: Diversidade de Borboletas (Lepidoptera, Papilionoidea e Hesperioidea) em fragmentos de Floresta Estacional Decidual em Santa Maria, Rio Grande do Sul, Brasil. Rev Bras Zool 2007,24(1):108–120. 10.1590/S0101-81752007000100014View ArticleGoogle Scholar
- DeVries PJ: The butterflies of Costa Rica and their natural history II: Riodinidae. Princeton University, New Jersey; 1997.Google Scholar
- Dias FMS, Dolibaina DR, Mielke OHH, Casagrande MM: Revision of the genus Stichelia Zikán (Riodinidae: Riodininae: Symmachiini), with the description of a new species from southern Brazil. Zootaxa 2013,3693(4):579–593. 10.11646/zootaxa.3693.4.10View ArticleGoogle Scholar
- Dolibaina DR, Mielke OHH, Casagrande MM: Borboletas (Papilionoidea e Hesperioidea) de Guarapuava e arredores, Paraná, Brasil: um inventário com base em 63 anos de registros. Biota Neotrop 2011,11(1):341–354. 10.1590/S1676-06032011000100031View ArticleGoogle Scholar
- Dolibaina DR, Dias FMS, Mielke OHH, Casagrande MM: Taxonomy of the ‘ Synargis axenus complex’ belonging to the ‘ Synargis regulus ’ species group, with a phylogenetic reassessment of the genus Synargis Hübner, 1819 (Lepidoptera: Riodinidae: Nymphidiini). Zool J Linn Soc Lond 2013, 168: 427–451. 10.1111/zoj.12030View ArticleGoogle Scholar
- Ferro VG, Teston JA: Composição de espécies de Arctiidae (Lepidoptera) no sul do Brasil: relação entre tipos de vegetação e entre a configuração espacial do hábitat. Rev Bras Entomol 2009,53(2):278–286. 10.1590/S0085-56262009000200010View ArticleGoogle Scholar
- Ferro VG, Melo AS: Diversity of tiger moths in a Neotropical hotspot: determinants of species composition and identification of biogeographic units. J Insect Conserv 2011, 15: 643–651. 10.1007/s10841-010-9363-6View ArticleGoogle Scholar
- Freitas AVL: Impactos potenciais das mudanças propostas no Código Florestal Brasileiro sobre as borboletas. Biota Neotrop 2010,10(4):53–58.View ArticleGoogle Scholar
- Fronza E, Specht A, Corseuil E: Butterflies and moths (Insecta: Lepidoptera) associated with erva-mate , the South American Holly ( Ilex paraguariensis St. Hil.), in Rio Grande do Sul, Brazil. Checklist 2011,7(4):496–504.Google Scholar
- Garcia RJF, Longhi-Wagner HM, Pirani JR, Meirelles ST: A contribution to the phytogeography of Brazilian campos : an analysis based on Poaceae. Rev Bras Bot 2009,32(4):703–713.View ArticleGoogle Scholar
- Giovenardi R, Di Mare RA, Sponchado J, Roani S, Jacomassa FAF, Jung AB, Porn MA: Diversidade de Lepidoptera (Papilionoidea e Hesperioidea) em dois fragmentos de floresta no município de Frederico Westphalen, Rio grande do Sul, Brasil. Rev Bras Entomol 2008, 52: 599–605. 10.1590/S0085-56262008000400010View ArticleGoogle Scholar
- Goldsmith S: Density of longhorned beetles (Coleoptera: Cerambycidae) differs at different elevations in Hawaiian Montane Forest. Southwest Nat 2007,52(3):364–370. 10.1894/0038-4909(2007)52[364:DOLBCC]2.0.CO;2View ArticleGoogle Scholar
- Graham CH, Ferrier S, Huettman F, Moritz C, Peterson AT: New developments in museum-based informatics and applications in biodiversity analysis. Trends Ecol Evol 2004, 19: 497–503. 10.1016/j.tree.2004.07.006View ArticleGoogle Scholar
- Grazia J, Romanowski HP, Araújo PB, Schwertner CF, Iserhard CA, Moura LA, Ferro VG: Artrópodos terrestres. In Biodiversidade dos Campos de Cima da Serra. Edited by: Bond-Buckup G. Libretos, Porto Alegre; 2008:76–97.Google Scholar
- Hall JPW: Phylogeny of the riodinid butterfly subtribe Theopeina (Lepidoptera: Riodinidae: Nymphidiini). Syst Entomol 2002, 27: 139–167. 10.1046/j.1365-3113.2002.00171.xView ArticleGoogle Scholar
- Hall JPW, Harvey DJ: A phylogenetic analysis of the Neotropical riodinid butterfly genera Juditha , Lemonias , Thisbe and Uraneis , with a revision of Juditha (Lepidoptera: Riodinidae: Nymphidiini). Syst Entomol 2001, 26: 453–490. 10.1046/j.0307-6970.2001.00161.xView ArticleGoogle Scholar
- Hall JPW, Harvey DJ: A revision of the Neotropical butterfly genus Seco Hall and Harvey (Lepidoptera: Riodinidae). P Entomol Soc Wash 2002,104(4):941–947.Google Scholar
- Hall JPW, Harvey DJ: The phylogeography of Amazonia revisited: new evidence from riodinid butterflies. Evolution 2002,56(7):1489–1497.View ArticleGoogle Scholar
- Hall JPW, Harvey DJ, Janzen DH: Life history of Calydna sturnula with review of larval and pupal balloon setae in the Riodinidae (Lepidoptera). Ann Entomol Soc Am 2004, 97: 310–321. 10.1603/0013-8746(2004)097[0310:LHOCSW]2.0.CO;2View ArticleGoogle Scholar
- Hijmans RJ, Cruz M, Rojas E, Guarino L: DIVAGIS, version 7.5. A geographic information system for the management and analysis of genetic resources data. 2001.Google Scholar
- Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A: Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 2005, 25: 1965–1978. 10.1002/joc.1276View ArticleGoogle Scholar
- Hillebrand H: On the generality of the latitudinal diversity gradient. Am Nat 2004,163(2):192–211. 10.1086/381004View ArticleGoogle Scholar
- IBGE: Mapa de Vegetação do Brasil. 2004.Google Scholar
- Iserhard CA, Romanowski HP: Lista de espécies de borboletas (Lepidoptera, Papilionoidea e Hesperioidea) da região do vale do rio Maquiné, Rio Grande do Sul, Brasil. Rev Bras Zool 2004,21(3):649–662. 10.1590/S0101-81752004000300027View ArticleGoogle Scholar
- Iserhard CA, Quadros MT, Romanowski HP, Mendonça-Jr MS: Occurrence of butterflies (Lepidoptera: Papilionoidea and Hesperioidea) in different habitats at the Araucaria Moist Forest and the Grasslands in the Basaltic Highlands in Southern Brazil. Biota Neotrop 2010, 10: 309–320. 10.1590/S1676-06032010000100026View ArticleGoogle Scholar
- Kaminski LA: Immature stages of Caria plutargus (Lepidoptera: Riodinidae), with discussion on the behavioral and morphological defensive traits in nonmyrmecophilous riodinid butterflies. Ann Entomol Soc Am 2008,101(5):906–914. 10.1603/0013-8746(2008)101[906:ISOCPL]2.0.CO;2View ArticleGoogle Scholar
- Koleff P, Gaston KJ, Lennon JJ: Measuring beta diversity for presence-absence data. J Anim Ecol 2003, 72: 367–382. 10.1046/j.1365-2656.2003.00710.xView ArticleGoogle Scholar
- Krüger CP, Silva EJE: Papilionoidea (Lepidoptera) de Pelotas e seus arredores, Rio Grande do Sul, Brasil. Entomol Vectores 2003,10(1):31–45.Google Scholar
- Kuinchtner A, Buriol GA: Clima do Estado do Rio Grande do Sul segundo a classificação climática de Köppen e Thornthwaite. Discip Sci 2001, 2: 171–182.Google Scholar
- Legendre P, Fortin MJ: Spatial pattern and ecological analysis. Vegetatio 1989, 80: 107–138. 10.1007/BF00048036View ArticleGoogle Scholar
- Legendre P, Legendre L: Numerical ecology. Elsevier, Amsterdan; 1998.Google Scholar
- Mabilde AP: Guia practica para os principiantes colecionadores de insectos, contendo a descripção fiel de perto de mil borboletas com 280 figuras lythographadas em tamanho, formas e desenhos conforme o natural. Estudo sobre a vida de insectos do Rio Grande do Sul e sobre a caça, classificação e a conservação de uma collecção, mais ou menos regular. Gundlach Schuldt, Porto Alegre; 1896.Google Scholar
- Marchiori MO, Romanowski HP: Species composition and diel variation of a butterfly taxocene (Lepidoptera: Papilionoidea and Hesperioidea) in a restinga wood at Itapuã State Park, Southern Brazil. Rev Bras Zool 2006a,23(2):443–454. 10.1590/S0101-81752006000200019View ArticleGoogle Scholar
- Marchiori MO, Romanowski HP: Borboletas (Lepidoptera, Papilionoidea e Hesperioidea) do Parque Estadual do Espinilho e entorno, Rio Grande do Sul, Brasil. Rev Bras Zool 2006b,23(4):1029–1037. 10.1590/S0101-81752006000400007View ArticleGoogle Scholar
- Marini-Filho OJ, Freitas AVL: Plano de Ação Nacional para a Conservação dos Lepidópteros Ameaçados de Extinção. Instituto Chico Mendes de Conservação da. Biodiversidade, Brasília; 2011.Google Scholar
- Moerman DE, Estabrook GF: The botanist effect: counties with maximal species richness tend to be home to universities and botanists. J Biogeogr 2006, 33: 1969–1974. 10.1111/j.1365-2699.2006.01549.xView ArticleGoogle Scholar
- Morais ABB, Romanowski HP, Iserhard CA, Marchiori MO, Segui R: Mariposas del Sur de Sudamérica (Lepidoptera: Hesperioidea y Papilionoidea). Cienc Ambient 2007, 35: 29–46.Google Scholar
- Morais ABB, Lemes R, Ritter CD: Borboletas (Lepidoptera: Hesperioidea e Papilionoidea) de Val de Serra, região central do Rio Grande do Sul, Brasil. Biota Neotrop 2012,12(2):175–183. 10.1590/S1676-06032012000200017View ArticleGoogle Scholar
- Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J: Biodiversity hotspots for conservation priorities. Nature 2000, 403: 853–858. 10.1038/35002501View ArticleGoogle Scholar
- Nekola JC, White PS: The distance decay of similarity in biogeography and ecology. J Biogeogr 1999,26(4):867–878. 10.1046/j.1365-2699.1999.00305.xView ArticleGoogle Scholar
- New TR: Conservation biology of the Lycaenidae (Butterflies). IUCN, Gland; 1993.Google Scholar
- New TR: Butterfly conservation. Oxford University Press, New York; 1997.Google Scholar
- Nishida K: Description of the immature stages and life history of Euselasia (Lepidoptera: Riodinidae) on Miconia (Melastomataceae) in Costa Rica. Zootaxa 2010, 2466: 1–74.Google Scholar
- Oksanen J, Kindt R, Legendre P, O’Hara R, Simpson GL, Stevens MHH: vegan: community ecology package. R package version 1.13–0. 2008.Google Scholar
- Oliveira-Filho AT, Fontes MAL: Patterns of floristic differentiation among Atlantic Forests in Southeastern Brazil and the influence of climate. Biotropica 2000,32(4b):793–810. 10.1111/j.1744-7429.2000.tb00619.xView ArticleGoogle Scholar
- Overbeck GE, Muller SC, Fidelis A, Pfadenhauer J, Pillar VD, Blanco CC, Boldrini II, Both R, Forneck ED: Brazil’s neglected biome: the South Brazilian Campos. Perspect Plant Ecol Evol Syst 2007, 9: 101–116. 10.1016/j.ppees.2007.07.005View ArticleGoogle Scholar
- Pedrotti VS, Barros MP, Romanowski HP, Iserhard CA: Occurrence of fruit-feeding butterflies (Lepidoptera: Nymphalidae) in a fragment of Araucaria Moist Forest in Rio Grande do Sul State, Brazil. Biota Neotrop 2011,11(1):385–390. 10.1590/S1676-06032011000100036View ArticleGoogle Scholar
- Pillar VP, Müller SC, Castilhos ZSM, Jacques AVA: Campos Sulinos - conservação e uso sustentável da biodiversidade. Ministério do Meio Ambiente, Brasília; 2009.Google Scholar
- Ponder WF, Carter GA, Flemons P, Chapman RR: Evaluation of museum collection data for use in biodiversity assessment. Conserv Biol 2001,15(3):648–657. 10.1046/j.1523-1739.2001.015003648.xView ArticleGoogle Scholar
- R Development Core Team: R: a language and environment for statistical computing. 2012.Google Scholar
- Rangel TF, Diniz-Filho JAF, Bini LM: SAM: a comprehensive application for Spatial Analysis in Macroecology. Ecography 2010, 33: 46–50. 10.1111/j.1600-0587.2009.06299.xView ArticleGoogle Scholar
- Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM: The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 2009, 142: 1141–1153. 10.1016/j.biocon.2009.02.021View ArticleGoogle Scholar
- Ritter CD, Lemes R, Morais ABB, Dambros CS: Butterflies (Lepidoptera: Hesperioidea and Papilionoidea) from Mixed Ombrophilous Forest fragments, Rio Grande do Sul, Brazil. Biota Neotrop 2011,11(1):361–368. 10.1590/S1676-06032011000100033View ArticleGoogle Scholar
- Romanowski HP, Iserhard CA, Hartz SM: Borboletas da floresta com araucária. In Floresta com araucária: ecologia, conservação e desenvolvimento sustentável. Edited by: Fonseca CR, Souza AF, Dutra TL, Leal-Zanchet AM, Backes A, Ganade G. Holos Editora, Ribeirão Preto; 2009.Google Scholar
- Rosa PLP, Chiva EQ, Iserhard CA: Borboletas (Lepidoptera: Papilionoidea e Hesperioidea) do Sudoeste do Pampa Brasileiro, Uruguaiana, Rio Grande do Sul, Brasil. Biota Neotrop 2011, 11: 1–6.View ArticleGoogle Scholar
- Ruszczyk A: Ecologia urbana de borboletas, I. O gradiente de urbanização e a fauna de Porto Alegre, RS. Rev Bras Biol 1986,46(4):675–688.Google Scholar
- Sackis JD, Morais ABB: Borboletas (Lepidoptera: Hesperioidea e Papilionoidea) do Campus da Universidade Federal de Santa Maria, Santa Maria, Rio Grande do Sul. Biota Neotrop 2008,8(1):151–158. 10.1590/S1676-06032008000100018View ArticleGoogle Scholar
- Santos EC, Mielke OHH, Casagrande MM: Butterfly inventories in Brazil: the state of art and the priority-areas model research aiming at conservation. Nat Conserv 2008, 6: 176–198.Google Scholar
- Santos JP, Iserhard CA, Teixeira MO, Romanowski HP: Fruit-feeding butterflies guide of subtropical Atlantic Forest and Araucaria Moist Forest in State of Rio Grande do Sul, Brazil. Biota Neotrop 2011,11(3):253–274. 10.1590/S1676-06032011000300022View ArticleGoogle Scholar
- Siewert RR, Silva EJE, Marques LL: Catálogo do acervo de borboletas (Lepidoptera: Papilionoidea) depositadas no Museu de História Natural da Universidade Católica de Pelotas, Rio Grande do Sul, Brasil. Entomobrasilis 2010,3(3):77–84.View ArticleGoogle Scholar
- Siewert RR, Dolibaina DR, Mielke OHH, Casagrande MM, Moser A: A new species of Aricoris Westwood,  belonging to “ chilensis ” group (Lepidoptera: Riodinidae). Zootaxa 2014,3764(4):495–500. 10.11646/zootaxa.3764.4.10View ArticleGoogle Scholar
- Summerville KS, Metzler EH, Crist TO: Diversity of Lepidoptera in Ohio forests at local and regional scales: how heterogeneous is the fauna? Ann Entomol Soc Am 2001,94(4):583–591. 10.1603/0013-8746(2001)094[0583:DOLIOF]2.0.CO;2View ArticleGoogle Scholar
- Teston JA, Corseuil E: Borboletas (Lepidoptera, Rhopalocera) Ocorrentes no Centro de Pesquisas e Conservação da Natureza Pró-Mata. 1. Papilionidae. Div Mus Ciênc Tecnol PUCRS 1999, 4: 217–228.Google Scholar
- Teston JA, Corseuil E: Borboletas (Lepidoptera, Rhopalocera) ocorrentes no Centro de Pesquisas e Conservação da Natureza Pró-Mata. 2. Pieridae. Div Mus Ciênc Tecnol PUCRS 2000, 5: 143–155.Google Scholar
- Teston JA, Corseuil E: Borboletas (Lepidoptera, Rhopalocera) ocorrentes no Centro de Pesquisas e Conservação da Natureza Pró-Mata. 3: Nymphalidae. Div Mus Ciênc Tecnol PUCRS 2002, 7: 1–20.Google Scholar
- Urbanetz C, Tamashiro JY, Kinoshita LS: Floristic composition and similarity analysis of an Atlantic rain forest fragment in Cananéia, São Paulo State, Brazil. Rev Bras Bot 2010,33(4):639–651. 10.1590/S0100-84042010000400012View ArticleGoogle Scholar
- Wolda H: Insect seasonality: why? Ann Rev Ecol Syst 1988, 19: 1–18.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.