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Braz. J. Biol. vol.68 no.3 São Carlos Aug. 2008
Variação de tamanho e forma no crânio de Myotis nigricans (Schinz, 1821) (Chiroptera: Vespertilionidae) de duas áreas geográficas no Brasil
Bornholdt, R.I, *; Oliveira, LR.II, III, IV; Fabián, ME.I
IPrograma de Pós-graduação em Biologia Animal, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul UFRGS, Av. Bento Gonçalves, 9500, Bloco IV, Prédio 43435, Sala 123, CEP 91540-000, Porto Alegre, RS, Brazil
IIGrupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul GEMARS, Rua Felipe Néri, 382/202, CEP 90440-150, Porto Alegre, RS, Brazil
IIICentro de Estudos Costeiros, Limnológicos e Marinhos CECLIMAR, Universidade Federal do Rio Grande do Sul UFRGS, Av. Tramandaí, 976, CEP 95625-000, Imbé, RS, Brazil
IVLaboratório de Biologia Genômica e Molecular da Faculdade de Biociências, Pontifícia Universidade Católica do Rio Grande do Sul PUCRS, Av. Ipiranga, 6681, Prédio 12A, sala 172, CEP 90619-900, Porto Alegre, RS, Brazil
We present a quantitative analysis of sexual dimorphism and geographic variation in the skull of Myotis nigricans (Schinz, 1821) assessed by geometric morphometrics. Differences in size and shape of skulls were investigated using 30 landmarks plotted on two-dimensional images of lateral and ventral views. Results of geometric morphometrics revealed sexual dimorphism in the centroid size of the skull in both views. Females were larger than males. Nevertheless, there was no sexual dimorphism in skull shape of M. nigricans. Geographic variation was detected in size and shape of the skull. South Brazilian specimens were significantly larger than Ceará specimens only in the lateral view. Differences in skull shape were statistically significant in both views: specimens from South Brazil were brevirostri and presented a more expanded skull in the posterior region while Ceará specimens were longirostri and do not present any expansion in the brain case. Ecological factors for these phenomena are discussed in the text.
Keywords: Chiroptera, Myotis nigricans, skull morphology, geometric morphometrics.
Uma análise quantitativa do dimorfismo sexual e da variação geográfica do crânio de Myotis nigricans (Schinz, 1821) é apresentada através da morfometria geométrica. Diferenças no tamanho e na forma do crânio foram avaliadas através de imagens bidimensionais das vistas lateral e ventral do crânio, onde foram estabelecidos 30 marcos anatômicos. Os resultados indicaram a existência de dimorfismo sexual no tamanho do centróide do crânio para ambas as vistas estudadas. As fêmeas foram maiores que os machos. Contudo, não foi detectado dimorfismo sexual na forma do crânio de M. nigricans. A variação geográfica esteve presente no tamanho e na forma do crânio. Espécimes do Sul do Brasil tiveram tamanho do centróide maior que os espécimes do Ceará apenas na vista lateral. Diferenças na forma do crânio foram estatisticamente significativas em ambas as vistas: os espécimes do Sul do Brasil apresentaram-se brevirostri e com grande expansão na região posterior do crânio, enquanto os espécimes do Ceará apresentaram crânios longirostri e sem expansão posterior da caixa craniana. São discutidos fatores ecológicos para estes fenômenos.
Palavras-chave: Chiroptera, Myotis nigricans, morfologia craniana, morfometria geométrica.
The genus Myotis (Kaup, 1821) has more than 100 species globally widespread (Simmons, 2005). The species are morphologically similar and hardly ever reflect specialization, which may cause some problems in their correct identification (LaVal, 1973; Bogan, 1978; Reduker, 1983; Ruedi et al., 1990; Baud and Menu, 1993; Barquez et al., 1999; Gannon et al., 2001; Ruedi and Mayer, 2001; López-Gonzales et al., 2001; Stadelmann et al., 2004) and leads to a taxonomic complexity of the group. Myotis has had a meaningful evolutionary success, being found in all continents (except in Antarctic), from semi-deserted habitats to sub-Antarctic regions (Ruedi and Mayer, 2001). Most of them are insectivore, even though some fish eater species were registered (Rice, 1998). The species from this genus are able to live together in colonies, sharing space and food, without apparent competitive exclusion (Ruedi and Mayer, 2001; Stadelmann et al., 2004), because morphological similarity does not reflect necessarily ecological similarity (Sauders and Barclay, 1992). According to Benda and Horácek (1995) the morphological variation pattern for this genus provides complex information about taxonomy, adaptation and the history of the distribution of the species as well.
The genus Myotis has 14 species in the Neotropical region (LaVal, 1973), from which six are registered for Brazil: M. albescens (E. Geoffroy, 1806), M. levis (I. Geoffroy, 1824), M. nigricans (Schinz, 1821), M. riparius Handley, 1960, M. ruber (E. Geoffroy, 1806) and M. simus Thomas, 1901 (Simmons, 2005). Myotis nigricans is found from South Mexico (Nayarit and Tamaulipas) to Peru, Bolivia, North Argentina, Paraguay and South Brazil. It is also occurring in Trinidad and Tobago and Lesser Antilles (St. Martin, Montserrat and Grenada) (Simmons, 2005). González (2000) stated that M. nigricans is common in Rio Grande do Sul, including Porto Alegre urban areas. This species has sociable habits and lives in spaces like tree barks, foliages and ceiling of buildings and houses (González, 2000).
Studies about sexual dimorphism and geographic variation from M. nigricans are scarce. LaVal (1973), who is a pioneer in the research about morphological variation of this species, suggested that M. nigricans should present differences among populations from different geographic areas in South America. Nevertheless, he did not mention any data about sexual dimorphism. Myers and Wetzel (1983), throughout the analyses of body and skull linear measurements, found some evidence of geographic variation among species from Argentina, Bolivia and Paraguay; however no significant differences were found between male and female specimens. Up to now, the studies describing M. nigricans morphology in South America have been exploring just the tradicional morphometrics (linear measurements) and literally no information about the shape changes was presented (Ihering, 1895; Cabrera, 1957; LaVal, 1973; Myers and Wetzel, 1983; Lopez-Gonzales et al., 2001). Besides, very few information is known about sexual dimorphism and geographic variation from this species in Brazil and most of them are related to body size. In this sense, the current study presents the first information about sexual dimorphism and geographic variation on the size and shape of M. nigricans skulls, from two Brazilian geographic areas.
2. Material and Methods
2.1. Studied areas
South Brazil area comprises the states of Paraná, Santa Catarina and Rio Grande do Sul. The examined specimens from this area were collected between 23 and 31º S of latitude, mainly in localities covered by the Brazilian Atlantic Forest (see the appendix for a detailed list of the sampling localities). This biome is composed of two major vegetation types: the Atlantic Rain Forest (coastal forest) and the Atlantic Semi-deciduous forest (tropical seasonal forest). The Atlantic Rain Forest covers the mountain chain that runs along the coastline from northeastern to southern Brazil, which includes our sampling areas in Santa Catarina. The Atlantic Semi-deciduous Forest extends across the plateau in the center and southeastern interior of the country (Leitão-Filho and Morellato, 1997; Oliveira-Filho and Fontes, 2000) and covers most of sampling areas in Rio Grande do Sul and Paraná states. This area experiences warm and wet climate, with dry seasons eventually. The temperatures range from 6 ºC during winter months to more than 30 ºC in the summer season (Morellato et al., 2000; Morellato and Haddad, 2000; Oliveira-Filho and Fontes, 2000).
In the Ceará state, the specimens of M. nigricans examined were collected between 06 and 04º S of latitude (see the appendix for a detailed list of the sampling localities). The dominant biome is Caatinga, which is a vast xeric biome that covers most of north-eastern Brazil (Mares et al., 1985). This biome is covered by several xeric, deciduous plants associations from dry, open woodland to thorn scrub with cacti ant terrestrial bromelias. In general, the climate conditions are semi-arid, which a variable annual precipitation between 250 and 1270 mm which falls unpredictably between September and March. There is no permanent water course, only some springs, water-holes and man-made reservoirs (Olmos, 1993). The dryness station remains five to eight months annually and the temperature varies from 27 to 33 ºC (Mares et al., 1985).
2.2. Material examined
For this study, the specimens from the following institutions were examined: Zoology Departament from the Instituto de Biociências from the Universidade Federal do Rio Grande do Sul (ZMAM), Museu de Ciências Naturais from the Fundação Zoobotânica do Rio Grande do Sul (MCN), Museu de Ciências Naturais from the Centro Universitário UNIVATES (ZMUMCN) and Universidade de Blumenau (FURB-SLA).
The age group was determined observing the presence of bone or cartilage epiphysis on the metacarpal-phalangeal joint from the left forth digit (Burnett and Kunz, 1982; Kunz and Anthony, 1982; Anthony, 1988).
The sexual dimorphism was analyzed just using adult specimens from South Brazil, due to the absence of male specimens from Ceará area. Geographic variation was also analyzed just for adult female specimens for the same reason mentioned above.
2.3. Geometric morphometrics
The geometric morphometrics (see Bookstein, 1991; Rohlf and Marcus, 1993; Monteiro and Reis, 1999) were used to analyze sexual dimorphism and geographic variation in skulls of Myotis nigricans. This technique has showed to be objective and efficient when compared to tradicional methods (Zelditch et al., 1995; Rohlf et al., 1996; Rohlf, 1998).
A total of 120 (lateral view) and 119 (ventral view) images of M. nigricans skull were analysed (see Table 1). The images were taken using a Nikon Coolpix 4500 digital camera joined to a Nikon SMZ 800 stereo microscope and saved in JPEG format. All the images had an 800 x 600 pixels resolution. The skulls were positioned at 90º from the stereo microscope lenses. A scale was used in this process. Thirty homologous and topologically equivalent landmarks were plotted on the skull in order to describe the size and shape variation. They were digitized using TpsDig1.40 (Rohlf, 2004a). All the landmarks were positioned on the left side of the skull image (Figure 2).
2.4. Landmarks definition
Lateral view (Figure 2a): (1) supra occipital basis; (2) skull anterior extremity, leveled to the first incisor alveolus; (3) post extremity of the occipital condyle; (4) dorsal external auditory meatus; (5) third molar post extremity; (6) alveolar limit between first and second molar; (7) alveolar limit between third pre-molar and first molar; (8) alveolar limit between first and second pre-molar; (9) canine alveolus anterior extremity; (10) ocular orbit; (11) nasal fossa dorsal extremity; (12) rostrum/skull congruent point; (13) skull anterior lateral extremity; (14) intersection between interparietal and supraoccipital bone.
Ventral view (Figure 2b): (15) skull anterior extremity, in the level of second incisor; (16) occipital condyle post extremity; (17) premaxillary incisura; (18) palatal incisura; (19) foramen magnum incisura; (20) skull lateral extremity, in the level of auditory region; (21) articular fossa left lateral extremity; (22) articular fossa right lateral extremity; (23) lacerated foramen right lateral extremity; (24) zygomatic incisura; (25) third molar post extremity; (26) mandibular arcade incisura; (27) alveolar limit between first and second molar; (28) alveolar limit between third pre-molar and first molar; (29) alveolar limit between first and second molar; (30) canine alveolus left extremity.
To avoid inflation of degrees of freedom related to the bilaterally symmetrical of the ventral view, landmarks were digitized in half of the skull and all the analysis was performed using this configuration.
The coordinates produced by TpsDig 1.40 program (Rohlf, 2004a) from the images (originally recorded as pixels) were converted in millimeters by the multiplication of the established conversion factor pixel/mm of each image using the included scale in the image, and then saved in nts format.
Centroid size was calculated using the software TPS Regr 1.28 (Rohlf, 2003), and used as a size variable independent of shape (Bookstein, 1991). Mean centroid size was calculated for both sexes and for both studied regions and compared through Student's t-test.
In order to compare shape, the coordinates for each specimen in this study were scaled, aligned and transformed by General Procrustes Alignment (GPA) using the software TpsRel 1.39 (Rohlf, 2004b) with the options α = 0, projection orthogonal and include uniform component. The GPA method computes a consensus configuration (least-squares Procrustes average configuration) based on the landmark coordinates of all specimens (see Bookstein, 1991, for methodological details). Shape differences between the consensus landmark configuration of each individual specimen were obtained and used to compute a matrix of partial warp scores. Relative warp scores were computed over the covariance matrix of the partial warp scores, therefore being analogous to PCA in the sense that they describe the axes of greater variation in shape for all of the analyzed specimens. The α parameter was set to zero to give the same weight to partial warps in smaller and greater scales (Rohlf, 1993). The partial warps matrix, including the uniform component, was used in a Canonical Variates Analysis (CVA), to describe differences between the populations and in order to confirm patterns previously suggested by the relative warp scores. In this case, if CVA confirms any a priori group, the scores from canonical variant 1 (CV1) and centroid size (CS) of M. nigricans skull were plotted for both views, in order to visualize and evaluate how size and shape contributed for the arrangement of these groups. In addition, thin-plate spline diagrams were generated in order to represent the deformation of skull shape in each population using the software Morpheus et al. (Slice, 1999).
All the statistical analyses of geometric morphometrics were performed using SPSS 11.5 (SPSS for Windows, Lead Technologies Inc, Chicago).
3.1. Sexual dimorphism
Size: The mean of the centroid size was statistically different between male and female specimens from South Brazil (see Table 2) for both studied views. Female skulls were larger than male skulls (P < 0.05).
Shape: For the lateral view, 24 relative warps were generated. The first one explained 25.59% of the total variation, the second 15%, and the third 11.06%. Together they represent more than 50% of the skull total shape variation. Scatter plots among the three first relative warps did not show any a priori group formation for the genders.
For the ventral view, 28 relative warps were generated. The first one explained 24.37% of the total variation, the second 16.18%, and the third 11.5%. Together they represented more than 50% of total skull shape variation. Scatter plots among the three first relative warps from this view also did not show any a priori group formation for the genders, indicating that there is no differences in the skull shape between males and females of M. nigricans.
3.2. Geographic variation
Size: The mean differences in the centroid size were statistically significant in the lateral view (see Table 3), in which specimens from South Brazil were larger than those from Ceará (P < 0.05). Nevertheless, in the ventral view, the mean centroid size was not statistically significant between the studied areas (see Table 3), which indicates a lack of geographic variation in size for this view (P > 0.05).
Shape: 24 relative warps were generated for the lateral view. The first one explained 21.95% of the total variation, the second 17.71% and the third 11.93%. Together they represented more than 50% of the total variation of the skull. The two first relative warps (RW1 and RW2) in the lateral view (Figure 3a) suggested a formation of a priori groups and a partial separation between South Brazil and Ceará specimens along the axis of the second relative warp due to skull shape differences. The CVA of partial warps confirmed the existence of geographic variation in the lateral view, fundamentally related to the change in the skull shape and not related to size (centroid size) (Figure 4). These differences were statistically significant (Wilk's Lambda = 0.470; g1 = 4; F = 22.62; P < 0.0001).
The region between the rostrum and the skull congruent point generated the strongest deformation in the lateral view of the skull. The specimens from South Brazil are brevirostri, and those from Ceará are longirostri. As a consequence, the brevirostri have a shorter rostrum but a broad and less inclined skull. The longirostri ones have a longer rostrum but a less extensive and abrupt inclined skull.
Twenty eight relative warps were generated for the ventral view. The first one explained 24.61% of the total variation, the second 16.86% and the third 10.47%. Together they represented more than 50% of the total variation of the skull. The two first relative warps (RW1 and RW2) in the ventral view (Figure 3b) suggested a formation of a priori groups and a partial separation between South Brazil and Ceará specimens along the axis of the first relative warp due to skull shape differences. The CVA from partial warps also confirmed the existence of two groups for this view, suggesting that the geographic variation in M. nigricans is also related to shape changes, but not to size (Figure 5). These differences were statistically significant (Wilk's Lambda = 0.495; g1 = 4; F = 20.297, P < 0.0001).
The extremities of the occipital condyle and the articular fossa regions generated the most evident shape deformation in ventral view. Specimens from South Brazil presented a more expanded skull in the posterior region (in which there is the articular fossa, the tympanic bulla and the occipital condyle) when compared to the same skull region from Ceará specimens.
The lateral view was the most informative for the analysis of geographic variation in M. nigricans skulls, because both, centroid size and shape of skull, presented significant differences between specimens from the two studied geographic areas (see Figure 4).
The results for sexual dimorphism suggested that differences between M. nigricans male and female skulls were fundamentally related to size and not to shape, with female skulls being larger than male. Myers (1978) stated that bat females of Vespertilionidae are usually larger than males in order to perform appropriately parental care. Females, when pregnant, fly carrying their fetuses. After that they need to take care of the offspring in the colonies. Because of this, a larger size of the body may be favorable to provide a successful reproductive process (Myers, 1978).
Carvalho (1973) commented on the absence of information related to M. nigricans' life history. Nevertheless, when analyzing other species from the same genus, Barclay (1991) and Rodrigues et al. (2003) found that, when entering the reproductive period, the females go to reproductive colonies, and there they remain looking after their offspring. For this reason, parental care is, in fact, energetically demanding for females (Kurta et al., 1989) and in this sense a larger size could be favorable.
Our results corroborated the results obtained by Sauders and Barclay (1992). They observed a larger forearm length in females of M. lucifugus and M. volans. In addition, Bogdanowicz and Owen (1996) also found sexual dimorphism in Otonycteris hemprichi skull (Vespertilionidae) using geometric morphometrics. Females presented larger centroid size than males. Overall, the observed differences between male and female skulls of M. nigricans presented in the current study confirm the literature data about the existence of sexual dimorphism in vespertilionids related to size.
Size variation in specimens from different latitudes has already been detected in the genus Myotis. Bogdanowicz (1990) foud that, in Europe, specimens of M. daubentoni from higher latitudes are larger than those from lower latitudes. Benda and Horácek (1995) obtained the same result for other species of Myotis (M. myotis, M. blythi and M. nattereri) in Paleartic region. Some longitudinal geographic variation patterns were also found in several species of the genus Myotis (Topál, 1971; Myers and Wetzel, 1983; Ruedi et al., 1990; Albayrak and Asan, 2002).
LaVal (1973), based on body size, suggested the existence of a different geographic variation in M. nigricans from Brazil. According to him, specimens from Amazonian Basin were larger than those from Minas Gerais, Rio de Janeiro and São Paulo, regions considered by the author as South Brazil. The data from the current study did not confirm the author's observation. However, it is important to mention that LaVal (1973) only presented the suggestion of geographic variation based on descriptive and qualitative results, which were not statistically tested.
According to Thorpe (1987), there are two suggestions for the existence of geographic variation: (1) current ecology and (2) historical process. The current ecology conditions can be biotic (mimicry, interspecific competition, etc) or physical (substrate adaptation, adaptation for climatic conditions such as Bergmann's rule, etc). The two geographic areas studied are highly differentiated in terms of vegetation, temperatures and also latitude. The Ceará region is located in the arid Caatinga biome in the northeast of Brazil with sampling areas positioned between 06 and 04 ºS (see material and methods for details) and high temperatures varying from 27 to 33 ºC (Mares et al., 1985). While South Brazil sampling areas were in the Brazilian Atlantic forest region, which presents both: a warm and wet climate without a dry season and also a seasonal climate with a relatively severe dry season. The temperatures in this area range from 6 ºC during winter months to more than 30 ºC in the summer season (Morellato and Haddad, 2000).
In this sense we can speculate Bergmann's rule (Bergammn, 1847), which states that "...races from cooler climates tend to be larger than species of warmblooded vertebrates than races of the same species in living in warmer climates..." (quoted in Mayr, 1963: 319). The usual explanation for this rule is that large animals expend less energy for thermoregulation because of their small surface-to-volume ratio; it is therefore argued that it is more economical for large than for small individuals to live in cold climates (McNab, 1971). Nevertheless, an evocation of this theory to explain our findings could only be reassure if we had examined all the species distribution and found a clinal variation along the different latitudes occupied by M. nigricans. In spite of the limitations derived from our restricted sampling areas, we believe that any historical process, could result in population isolation (segregation in the species distribution, for instance) which may lead to a geographic variation pattern associated to specialization.
Based on size and shape geographical variation of the analyzed structures, the occurrence of subspecies or distinct species could be suggested. Nevertheless, the small number of male samples coming from Ceará area did not allow an analysis of the geographic variation for this gender. Moreover, there is a lack of knowledge about M. nigricans from other regions from Brazil, which would be fundamental for a taxonomic definition. In this sense, we strongly recommend the continuity of this study throughout the analysis of skull and external morphology by traditional morphometrics as well as molecular markers, and mainly to examine specimens along all M. nigricans species distribution.
Acknowlegements We thank to the collection managers: Professor Hamilton Grillo and the biologist Elisangela Mander from Centro Universitário UNIVATES, Professor Sergio Althoff from Fundação Universitária da Região de Blumenau and Dr. Márcia Jardim from Fundação Zoobotânica do Rio Grande do Sul, for the admirable contribution in providing scientific material. We also thank to the anonymous referee for the comments and suggestions. And finally we thank to CNPq (Conselho Nacional do Desenvolvimento Científico e Tecnológico), which provided the MsC grant to Renata Bornholdt. This study is part of the dissertation presented by R. B., submitted in partial fulfillment for a MsC degree in Animal Biology at Universidade Federal do Rio Grande do Sul, Brazil.
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Received October 13, 2006
Accepted March 14, 2007
Distributed August 31, 2008
BRASIL, Ceará: Canindé (4º 21' S and 39º 18' W), MCN 1144 (♀), MCN 1163 (♀), MCN 1359 (♀); Jaguaruana (4º 50' S and 37º 46' W), MCN 1146-1148 (♀); Palhano (4º 44' S and 37º 57' W), MNC 1113 (♀), MCN 1151-1153 (♀), MCN 1155 (♀), MCN 1157 (♀); Pereiro (6º 02' S 38º and 27' W), MCN 1149 (♀); Paraná: Castro (24º 79' S and 50º 01' W), ZMAM 0776 (♂), ZMAM 0780 (♂); Londrina (23º 31' S and 51º 16' W), ZMAM 0775 (♀), ZMAM 0777-0778 (♂); Santa Catarina: Água Doce (26º 99' S and 51º 16' W), FURB-SLA 1726 (♀), FURB-SLA 1730 (♀); Blumenau (26º 93' S and 49º 05' W), FURB-SLA 1634 (♂), FURB-SLA 1644 (♂); Florianópolis (27º 59' S and 48º 54' W), FURB-SLA 0057 (♀), FURB-SLA 0111 (♀), FURB-SLA 0238-0240 (♂), FURB-SLA 0241 (♀), FURB-SLA 0242 (♂), FURB-SLA 0254-0255 (♀), FURB-SLA 0256 (♂), FURB-SLA 0257-0258 (♀), FURB-SLA 0282 (♂), FURB-SLA 0283-0284 (♀), FURB-SLA 0286 (♀), FURB-SLA 0288 (♂), FURB-SLA 0289-0290 (♀), FURB-SLA 0305 (♂), FURB-SLA 0306-0308 (♀), FURB-SLA 0313 (♂), FURB-SLA 0314 (♀), FURB-SLA 0318 (♂), FURB-SLA 0320 (♂), FURB-SLA 321-0323 (♀), FURB-SLA 0352-0353 (♂), FURB-SLA 0360-0361 (♂), FURB-SLA 0552-0553 (♂), FURB-SLA 0560 (♀), FURB-SLA 0707 (♀), FURB-SLA 1022 (♂); Gaspar (26º 55' S and 48º 57' W), FURB-SLA 0075 (♀); Indaial (26º 89' S and 49º 23' W), FURB-SLA 1740 (♂), FURB-SLA 1781 (♀), FURB-SLA 1783 (♀), FURB-SLA 1802 (♂), FURB-SLA 1811 (♂), FURB-SLA 1823 (♀); Jaraguá do Sul (26º 29' S and 49º 04' W), FURB-SLA 1875 (♂); Joinville (26º 30' S and 48º 84' W), FURB-SLA 0063 (♀); Nova Veneza (28º 63' S and 49º 49' W), FURB-SLA 0897 (♂), FURB-SLA 0902 (♀), FURB-SLA 0908 (♀); Pomerode (26º 74' S and 49º 17' W), FURB-SLA 1220-1222 (♀); Santa Rosa do Sul (29º 08' S and 49º 42' W), FURB-SLA 0914 (♀), FURB-SLA 0918 (♂), FURB-SLA 0920 (♀); Rio Grande do Sul: Anta Gorda (28º 58' S and 52º 00' W), MCN 0556-0557 (♀); Arroio do Meio (29º 24' S and 51º 56' W), ZMUMCN 0391 (♂); Caxias do Sul (29º 10' S and 51º 10' W), ZMAM 0078 (♀), ZMAM 0079 (♂), ZMAM 0080 (♀); Dom Pedro de Alcântara (29º 22' S and 49º 50' W), ZMAM 0195 (♀), ZMAM 0196 (♂), ZMAM 0197 (♀), ZMAM 0200-0201 (♂), ZMAM 0257 (♂), ZMAM 0502 (♂); Forquetinha (29º 22' S and 52º 05' W), ZMUMCN 0648 (♀); General Câmara (29º 54' S and 51º 45' W), ZMAM 0165 (♀); Guaíba (30º 06' S and 51º 19' W), MCN 2351 (♂); Lajeado (29º 28' S and 51º 57' W), ZMUMCN 0225- 0226 (♂), ZMUMCN 0652 (♀); Maquiné (29º 40' S and 50º12' W), ZMAM ZMAM 0755-0756 (♀), ZMAM 0757 (♂); Marquês de Souza (29º 19' S and 52º 05' W), ZMUMCN 617 (♂); Pelotas (31º 46' S and 52º 20' W), ZMAM 0732 (♂), ZMAM 0735 (♀), ZMAM 0740 (♂); Putinga (29º 00' S and 52º 09' W), ZMUMCN 0265 (♀), ZMUMCN 0509 (♂); Santa Maria (29º 41' S and 53º 49' W), MCN 0299 (♀), MCN 0301 (♂); São José do Herval (29º 02' S and 52º 17' W), ZMUMCN 0383 (♀); São Lourenço do Sul (31º 21' S and 51º 58' W), MCN 0399 (♀); Teutônia (29º 26' S and 51º 48' W), ZMUMCN 0402 (♀); Viamão (30º 04' S and 51º 01' W), ZMAM 0782 (♀), ZMAM 0783 (♂), ZMAM 0785 (♂).