Range extension of Myotis midastactus (Chiroptera, Vespertilionidae) to Paraguay

Abstract Background Myotis midastactus Moratelli and Wilson, 2014 (Vespertilionidae, Myotinae) was described from the Myotis simus Thomas, 1901 complex based on collections from the Bolivian Savannah. New information Four vouchers previously assigned to M. simus from the Alto Chaco in Paraguay (West of the Paraguay River) are reassigned here to M. midastactus. These specimens extend the geographic distribution of M. midastactus 1200 km southward, and constitute the first evidence of the species in the country. Based on other material from the Brazilian Pantanal and Cerrado, Central Paraguay and north-eastern Argentina, we also discuss the identity of simus-like populations south of the Amazon Basin. The status of these populations is still unclear, but the little evidence we have at hand indicates that these populations may represent another taxon—M. guaycuru Proença, 1943; whereas M. simus seems to be restricted to the Amazon basin. This hypothesis is still very speculative and requires further investigation. With the assignment of material from Alto Chaco to M. midastactus, seven species of Myotis are confirmed for Paraguay: M. albescens, M. lavali, M. levis, M. midastactus, M. nigricans, M. riparius, and M. ruber.


Introduction
Myotis simus was described by Thomas (1901) based on one specimen from Río Ucayali, Loreto, Peruvian Amazon. The species was known from tropical South American lowlands, with records east of the Andes in Colombia, Ecuador, Peru, Bolivia, Paraguay, northern and mid-western Brazil, and north-eastern Argentina (Wilson 2008, Moratelli et al. 2011b, Moratelli 2012. Previous records of M. simus from southern Brazil (Wallauer et al. 2000, Peracchi et al. 2006, Bianconi and Pedro 2007 and from west of the Ecuadorian Andes (Carrera et al. 2010) seem to be misidentifications of M. levis (I. Geoffroy, 1824) and M. riparius Handley, 1960, respectively (Cherem et al. 2004, Moratelli et al. 2011b).
Based on morphological and morphometric evidence (Moratelli et al. 2011a), Bolivian savannah populations were reassigned to a new species-Myotis midastactus Moratelli and Wilson, 2014; and populations from the Amazon lowlands in Colombia, Ecuador, Peru, Bolivia, and northern Brazil were retained as M. simus (see Moratelli and Wilson 2014). Populations from outside of the Amazon Basin, including those from the Brazilian Pantanal and Cerrado, Paraguay, and north-eastern Argentina, are represented by few specimens in collections. We examined four from west of the Paraguay River, Paraguay, and concluded they represent M. midastactus. A few others we examined from mid-western Brazil and north-eastern Argentina might represent neither M. midastactus nor M. simus. These specimens partially fit in the descriptions of M. simus provided by Thomas (1901) andLaVal (1973), but they differ slightly in the development of skull crests. In addition, a distribution modelling for M. simus (sensu LaVal 1973 and Wilson 2008) has supported the disjunctive distribution proposed by Wilson (2008), where Amazon Basin populations are isolated from southern South American populations by unsuitable habitats (Moratelli et al. 2011b). This disjunctive distribution was strengthened after the assignment of Bolivian savannah populations to M. midastactus. Based on this evidence, the taxonomic status of the southernmost populations of M. simus is pending further evaluation (Moratelli and Wilson 2014).
In this report we extend the geographic distribution of M. midastactus from the Bolivian savannah to west of the Paraguay River, Paraguay. We also discuss the status of populations of M. simus out of the Amazon Basin (herein referred as simus-like).

Material and methods
Four pregnant females deposited as vouchers at the Museum of Vertebrate Zoology (MVZ), Berkeley, USA, constitute the first records of M. midastactus from Paraguay (MVZ 144481-144484). These vouchers were collected by P. Myers on 22 October 1972, 230 km NW from Villa Hayes (by road), Presidente Hayes, Paraguay (23°23′ S, 58°46′ W). Geographical coordinates for these specimens were obtained from Gardner's gazetteer of marginal localities (Gardner 2008). Identifications were based on the diagnostic characters reported by Moratelli and Wilson (2014).
Qualitative and quantitative traits from the external and skull morphology were used to compare specimens representing M. midastactus from Paraguay with others representing M. midastactus (N = 33; type series) from Bolivia; M. simus (N = 79) from the Amazon Basin (northern Brazil, Colombia, Ecuador, and Peru); and simus-like (N = 8) from midwestern Brazil and northern Argentina ( Figure 1). Sub-adults and adults were used in the qualitative analyses, but quantitative data was retrieved from adults only. These specimens and the geographical coordinates of their localities are listed in the supplementary material. We also compared M. midastactus from Paraguay with representatives of other species confirmed for the country except M. levis, which include: M. albescens (N = 161), M. lavali (N = 4), M. nigricans (N = 103), M. riparius (N = 10), and M. ruber (N = 5). Myotis levis is represented in Paraguay by a single record (Stevens et al. 2010), and characters used in the comparison were retrieved from Stevens et al. (2010).

Myotis midastactus
The four Paraguayan vouchers (MVZ 144481-144484) from Presidente Hayes (Fig. 1, loc.  19), have the set of diagnostic character of M. midastactus provided by Moratelli and Wilson (2014) and fit their description of the especies. They have the woolly, extremely short (LDH 4-5 mm, LVH 3-5 mm), golden-yellow fur typical of the species (Fig. 2; Table  1); plagiopatagium attached to the foot by a narrow band of membrane (≤ 1.5 mm); and mastoid breadth equal or larger than 7.8 mm (7.8-8.1 mm). The zygomatic breadth, which is part of the set of diagnostic characters, is not reported here because the arches are broken in these vouchers.      present and low (usually absent in albescens, levis and nigricans). In addition, they differ from M. albescens and M. levis by the absence of a fringe of hairs along the trailing edge of uropatagium. On the other hand, M. lavali has a yellowish general appearance but the dorsal fur is silky, longer, paler and strongly bicolored with blackish or dark-brownish basis in M. lavali (unicolor in midastactus). See pictures of the pelage colour of M. lavali in Moratelli et al. (2011c) and . Myotis midastactus from Paraguay (MVZ 144481-144484) differ from M. riparius and M. ruber by the paler colour (reddishbrown or brownish in riparius, and reddish in ruber), shorter fur (ca. 7 mm in riparius and ruber), and plagiopatagium attached to the foot by a narrow band of membrane (plagiopatagium broadly attached to the foot in riparius and ruber).

Myotis simus-like
Four specimens from three different localities in Argentina were tentatively assigned to M. simus-like. These specimens match M. simus from the Amazon Basin in fur texture and length, and zygomatic breadth (Table 1). However, they lack sagittal and lambdoidal crests, and the dorsal fur colour is close to Buffy Brown or Dresden Brown, while those from the Amazon Basin generally have medium to high crests (Moratelli et al. 2011a:50, table 4), with a dorsal fur colour ranging from Tawny, Russet and Cinnamon-brown. These Argentinian specimens are very close to the holotype of M. guaycuru in the skull morphology; and close to specimens from mid-western Brazil (MZUSP 13815, MN 71451, 71458) in fur colour, texture, and length.

Other Paraguayan specimens
A few specimens in the simus-group from Paraguay are pending identification. They are from localities east of the Paraguay River (Fig. 1, locs 22,

Myotis midastactus
The Paraguayan vouchers we identified here as M. midastactus (MVZ 144481-144484) were previously identified as M. simus by Myers and Wetzel (1979) and Myers and Wetzel (1983), and part of them (MVZ 144483, 144484) were reidentified as M. ruber by Baud and Menu (1993). These vouchers extend the geographic distribution of M. midastactus in ca. 1200 km southward, and constitute the first records of the species for Paraguay. They enlarge the species distribution from the Beni Savannah (Fig. 1, locs 1-3) and Cerrado ecoregion (Fig. 1, loc. 4) to the north of the Humid Chaco ecoregion (Fig. 1, loc. 19; ecoregion nomenclature following Olson et al. 2001). All records for this species are associated with flooded habitats (see Kingsbury 2010, Rumiz and Sainz 2002, López-González 2004. Myotis midastactus was described from a Bolivian habitat that harbours a few endemic birds and small mammals (Olson et al. 2001, Emmons andPatton 2005) -e.g., Hylaemys acritus (Emmons and Patton, 2005)   .

Myotis simus-like from southern South America
All Argentinian specimens of this taxon have been collected in flooded areas and wetland biomes of the Humid Chaco ecoregion (following Olson et al. 2001). Specimens from Corrientes are from "Los Esteros del Iberá", one of the largest South America's freshwater wetlands (Cózar et al. 2005). This region is similar to the Brazilian Pantanal, the region where we found other simus-like specimens. The holotype of M. guaycuru was collected in the Cerrado ecoregion (Olson et al. 2001), in an area geographically close to a Cerrado-Pantanal ecotone, near to the border of Paraguay (Fig. 1, loc. 5).
We envision two more realistic scenarios for this puzzle. Assuming that those specimens from mid-western Brazil (Pantanal and Cerrado) are conspecific with M. simus from the Amazon Basin, and those from Central Paraguay and north-eastern Argentina are M.
simus as well; Amazon basin populations of M. simus can be connected with southernmost populations throughout the Brazilian savannah (Cerrado [ Fig. 1, loc. 5]) and wetlands (Pantanal [Fig. 1, loc. 6, 7). However, a previous distribution modelling did not retrieve good support for this corridor (see Moratelli et al. 2011b). In another scenario, M. simus might be restricted to the Amazon basin, and those from mid-western Brazil and northeastern Argentina may represent a third species morphologically closer to M. simus than to M. midastactus. Populations of this third species can be connected by central Paraguayan populations throughout the Humid Chaco. If future research confirms this second hypothesis, Myotis guaycuru Proença, 1943 is the name available for this taxon.