Zootaxa 2985: 41 54 (2011) www.mapress.com/zootaxa/ Copyright 2011 Magnolia Press Article ISSN 1175-5326 (print edition) ZOOTAXA ISSN 1175-5334 (online edition) Morphometric and morphological variation in Myotis simus Thomas (Chiroptera, Vespertilionidae), with an appraisal of the identity of Myotis guaycuru Proença based on the analysis of the type material RICARDO MORATELLI 1, ADRIANO L. PERACCHI 2 & JOÃO A. DE OLIVEIRA 3 1 Campus Fiocruz da Mata Atlântica, Fundação Oswaldo Cruz, Rio de Janeiro, RJ, Brazil. E-mail: rmoratelli@fiocruz.br 2 Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro, Rio de Janeiro, RJ, Brazil. E-mail: alperacchi@yahoo.com.br 3 Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil. E-mail: jaoliv@mn.ufrj.br Abstract Twelve species are recognized in the South American bat genus Myotis Kaup (Vespertilionidae, Myotinae), with several nominal forms currently regarded as synonyms, among them Myotis guaycuru Proença, 1943. Its holotype, so far the only specimen assigned to the species, has not been examined in recent taxonomic reviews. To address the taxonomic status of M. guaycuru, we located and redescribed its holotype and compared it to representatives and/or descriptions of all South American species in the genus. Qualitative traits, namely the plagiopatagium attached at ankles, the short and wooly fur and the lingually displaced P3, unambiguously assign the holotype of M. guaycuru to Myotis simus Thomas (1901). The analysis of cranial variation and pelage color across a wide geographical range of M. simus reveals morphometric and morphological discontinuity between Bolivian and Amazonian/Peruvian samples, the latter including topotypes of M. simus. The holotype of M. guaycuru was found to be morphometrically and morphologically more similar to these Amazonian samples than to the geographically nearer Bolivian sample, preventing the use of this nominal form to refer to the Bolivian population if its distinction suggested by morphometric analyses is confirmed by the analyses of other character systems. Key words: Myotis, Myotinae, taxonomy, synonymy, multivariate analyses, South America Introduction Based primarily on LaVal s (1973) revisionary work on Neotropical Myotis Kaup, 1829 (Vespertilionidae, Myotinae), Wilson (2008) has recently recognized 12 valid names to South American species. Several other proposed names have been regarded as synonyms, among them, Myotis guaycuru, described by Proença (1943) on the basis of one specimen collected in 1940 in Salobra, Paraguay Basin, Mato Grosso do Sul, Brazil (Travassos 1940). The taxonomic status of M. guaycuru was f irst questioned by LaVal (1973), who t entatively regarded this taxon as a probably senior synonym of Myotis riparius Handley, 1960. Subsequently, López-González et al. (2001) considered Myotis guaycuru a junior synonym of Myotis simus Thomas, 1901, an assignment followed by Wilson (2008). However, neither LaVal (1973) nor López-González et al. (2001) examined the holotype. Myotis simus was described by Thomas (1901) based on one female specimen from Loreto, Peru. According to Thomas (1901) description, no recognized species resembles M. simus in external traits, the main diagnostic characters being the wings attached at the toes or at ankles by a narrow band of membrane and the very short fur (Baud and Menu 1993; López-González et al. 2001; López-González 2005). Myotis riparius was described by Handley (1960) for a series from Darien, Panama. It was originally proposed as a subspec ies of M. simus, but was subsequently raised to the species level by LaVal (1973). Myotis riparius can be di stinguished from M. simus by th e attachment of its plagiopatagium to the base of the toes by a broad band of membrane, by its longer and generally bicolored fur, and by th e P3 not crowded to the lingual side (LaVal 1973; López-González et al. 2001; López- González 2005). Accepted by P. Cordeiro-Estrela: 28 Jun. 2011; published: 4 Aug. 2011 41
Herein, as part of an ongoing systematic and biogeographic review of South American species of Myotis, and in order to determine the taxonomic status of M. guaycuru, we qualitatively compared its holotype with type specimens or original descriptions of other South American species. Subsequently, we analyzed the craniometric variation within and among geographic samples of M. simus and classified the cranial morphology of the type specimen of M. guaycuru within this morphometric context, in order to evaluate the possible application of this nominal form in the recognition of geographic units within M. simus. Material and methods The holotype of M. guaycuru: Among a series of specimens donated to the Instituto de Biologia (Universidade Federal Rural do Rio de Janeiro, UFRRJ), by the Instituto Oswaldo Cruz (Fundação Oswaldo Cruz), there was a specimen bearing an original label which reads: Myotis guaycuru, Salobra, M. Grosso, 237. This specimen was deposited in the Adriano Lúcio Peracchi Collection at Instituto de Biologia, UFRRJ, under the number ALP 9277, and was recognized as the holotype of M. guaycuru after comparisons with the original description and photographs given by Proença (1943). Comparisons: the holotype of M. guaycuru (ALP 9277) was compared with the currently recognized South American species of Myotis, represented by their type specimens, original descriptions and/or redescriptions provided by LaVal (1973). The type specimens used in comparisons were: M. albescens (É. Geoffroy, 1806) (AMNH 205195, neotype), M. levis levis (I. Geoffroy, 1824) (MNHN type no. 203, lectotype), M. keaysi keaysi J.A. Allen, 1914 (AMNH 15814, holotype), M. nesopolus larensis LaVal, 1973 (AMNH 130709, holotype), M. riparius Handley, 1960 (USNM 310255, holotype) and M. ruber (É. Geoffroy, 1806) (USNM 115097, neotype). The original descriptions used in comparisons wer e: M. aelleni B aud, 1 979, M. atacamensis ( Lataste, 1892 ), M. chiloensis (Waterhouse, 1840), M. levis dinellii (Thomas, 1902), M. keaysi pilosatibialis LaVal, 1973, M. nigricans nigricans (Schinz, 1821), M. oxyotus (Peters, 1867) and M. simus Thomas, 1901. Specimens selection: Specimens of M. simus in collections were identified by a set of qualitative characters regarded as diagnostic by Thomas (1901), LaVal (1973), López-González et al. (2001), López-González (2005), Moratelli (2008) and Wilson (2008), as follows: plagiopatagium attached at the level of the toes by a narrow band of membrane or at the level of the ankles (q.v., López-González et al. 2001: 141, fig. 1), extremely short and woolly fur, tips of dorsal hairs not contrasting with bases, and absence of fringe of hairs along the trailing edge of the uropatagium. To address the variation in qualitative and quantitative characters among South American population samples, 99 specimens referable to M. simus from Bolivia, Brazil, Ecuador and Peru were analyzed, 47 of which from Bolivia, Brazil and Peru having been included in the multivariate statistical analyses. A list of sp ecimens examined with their localities is in the Appendix. Samples analyzed: Considering that sex ratios in each geo graphic sample varied considerably, with males usually less r epresented than females, to avoid possible effects of secondary sexual dimorphism related to this unbalanced design, o nly f emales wer e i ncluded i n t he geog raphic an alyses. T he f ollowing g eographic sampl es were available for morphometric analyses (Figure 1): 1: Cercado, Beni, Bolivia (N = 20); 2: Borba, Amazon as, Brazil (N = 5); 3: Manaus, Amazonas, Brazil (N = 5); 4: Parintins, Amazonas, Brazil (N = 9); 5: El Refugio, Santa Cruz, Bolivia (N = 1); 6: Salobra, Mato Grosso do Sul, Brazil (type specimen of M. guaycuru, N = 1); 7: Rio Juruá, Amazonas, Brazil (N = 1); 8: Ucayali, Loreto, Peru (topotypes of M. simus, N = 3); and 9: San Juan, Pasco, Peru (N = 2). Quantitative data: All observations and measurements are from adult individuals with closed epiphyses. Fifteen cranial and five external dimensions were measured using a digital caliper accurate to 0.02 mm. The measurements, reported in millimeters (mm), and their abbreviations are defined as follows (lengths were measured from the anteriormost point of the first structure to the posteriormost point of the second structure mentioned below): greatest length of skull (GLS), from the premaxillae, including the incisors, to the occiput; condylo-canine length (CCL), from the occipital condyles to the upper canines; condylo-incisive length (CIL), from the occipital condyles to the upper incisors; basal length (BL), from the foramen magnum to the upper incisors; zygomatic breadth (ZB), greatest breadth across the outer edges of the zygomatic arches; mastoid breadth (MAB), greatest cranial breadth across the mastoid region; braincase breadth (BCB), greatest breadth of the globular part of the braincase; interorbital breadth (IOB), least breadth across orbital bulges; postorbital breadth (POB), least breadth across frontals posterior to the postorbital bulges; breadth across canines (BAC), greatest breadth across outer edges of the crowns 42 Zootaxa 2985 2011 Magnolia Press MORATELLI ET AL.
of upper canines; breadth across molars (BAM), greatest breadth across outer edges of the crowns of upper molars; maxillary toothrow length (MTL), from the upper canine crown to the crown of M3; molariform toothrow length (M13), from the crown of M1 to the crown of M3; mandibular length (MAL), from the dentary, without incisors, to the angular process; mandibular toothrow length (MAN), from the lower canine to m3; thumb length (THL), from the proximal end of the metacarpal to the tip of the claw; forearm length (FA), from the elbow to the distal end of the forearm including carpals; third metacarpal length (3MC), from the distal end of the forearm to the distal end of the third metacarpal; and length of the dorsal (LDH) and ventral hairs (LVH), from the base to the tip of the hair, measured between scapulae. The weight, reported in grams, was obtained from the skin tags. FIGURE 1. Geographic mapping of samples analyzed in the present study: (1) Cercado, Beni, Bolivia; (2) Borba, Amazonas, Brazil; (3) Manaus, Amazonas, Brazil; (4) Parintins, Amazonas, Brazil; (5) El Refugio, Santa Cruz, Bolivia; (6) Salobra, Mato Grosso do Sul, Brazil (type specimen of M. guaycuru) (7) Rio Juruá, Amazonas, Brazil; (8) Ucayali, Loreto, Peru; and (9) San Juan, Pasco, Peru. Analyses of geographic variation: All available specimens were included in a Principal Components Analysis (PCA) to summarize the general trends of size and shape variation within the total dataset treated as a unique sample. To assess patterns of craniometrical geographic variation, a C anonical Variate Analysis (CVA) was performed o n l ocality sampl es t o assess craniometric characters t hat b est discriminate amo ng g eographic sampl es (Neff & Marcus 1980; Manly 1994). Localities represented by on e to three specimens were not included in this analysis, but classified a posteriori to the larger samples on the basis of bootstrapped Mahalanobis distances. As multivariate procedures require complete data matrices, missing values (2.5% of total dataset) were estimated from the existing data using the expectation-maximization algorithm (Little & Rubin 1987; Strauss et al. 2003). For descriptive and comparative purposes, mean and range of each character were reported for the largest samples. The GEOGRAPHIC VARIATION IN MYOTIS SIMUS Zootaxa 2985 2011 Magnolia Press 43
statistical significance of differences among geographical samples was assessed by single classification analyses of variance (ANOVAs). To test if the isolation-by-distance model adequately describes the pattern of geographical variation revealed for M. simus, we assessed the correlation between the geographical and morphometric distance matrices by means of a non-parametric Mantel s test (Mantel 1967). All analyses were performed in Matlab for Windows, version 4.2c (Mathworks 1994), using functions written by R. E. S trauss a vailable a t ht tp://www.faculty.biol.ttu.edu/strauss/matlab/matlab.htm (accessed 14 February, 2011). FIGURE 2. Body (in fluid) of the holotype of M. guaycuru (ALP 9277). Scale b ar = 10 mm. Bellow on the left, the arrow shows the plagiopatagium attachment. Qualitative characters: A set of qualitative characters selected by previous authors (e.g., Thomas 1901; 1902; Miller & Allen 1928 ; Hand ley 1960; LaVal 1973; B aud & Menu 19 93; López-González et al. 2 001; López- González 2005; Moratelli 2008; Wilson 2008) was used to characterize the available samples of M. simus, as follows: point of insertion of the plagiopatagium (attached at toes by a narrow band of membrane or at ankles); position of P3 (aligned with other premolars or displaced to the lingual side, and visible or not visible when observed in lateral view); occurrence and height of sagittal crest (absent or present, and hei ght: very low, low, medium and high); occurrence and height of occipital crests (absent or present, and height: very low, low, medium and high); shape of the braincase roof (parietal inclined forward or straight); shape of the occipital region (occipital flattened when obser ved in l ateral vi ew, bei ng not pr ojected m uch beyo nd the limit of occi pital condyles, or occipital rounded, being project beyond the limit of occipital condyles). Capitalized colors nomenclature follows Ridgway (1912). 44 Zootaxa 2985 2011 Magnolia Press MORATELLI ET AL.
Results The holotype of M. guaycuru and qualitative comparisons. The holotype of Myotis guaycuru is an adult female specimen (ALP 9277), preserved in fluid, with the skull and mandible complete (Figures 2 and 3). The skin is torn on the abdominal region and hairs are lacking in a great part of the abdominal and lumbar regions. The holotype is a medium-sized specimen (FA 38.1 mm; GLS 13.6 mm), with extremely short and woolly fur (LVH and LDH, 3.6 and 3.8, respectively). Bases and tips of hairs in dorsal and ventral pelage are of similar color, the dorsum of uropatagium is almost naked, and the plagiopatagium is attached at the level of the ankles. The skull lacks a sagittal crest, the interorbital constriction is wide and the rostrum is short and wide. The P3 is smaller and displaced to the lingual side i n relation to other pr emolars. C onsidering these traits, mai nly the plagiopatagium attached at the ankles and the extremely short fur, the holotype of M. guaycuru differs from the type specimens of all South American forms, with the exception of M. simus. Apart from the lack of sagittal crest, none of the above characters can be used to distinguish the holotypes of M. guaycuru and M. simus. Although the sagittal and occipital crests have been used by Proença (1943) to distinguish those species, as discussed bellow, these structures have a great range of variation in M. simus, not allowing their use as diagnostic characters. Quantitative variation in M. simus. Due to small sample sizes, to avoid redundancy matrices, only 10 skull measurements sampling distinct regions of the skulls and mandibles (GLS, MAB, BCB, IOB, POB, BAC, BAM, MTL, M13 and MAN) were selected for the multivariate geographic analyses. Principal Component Analysis The 1st principal component (PC1), which accounted for 77% of the total craniometric variation, is regarded as a general size axis based on the positive and high magnitude loadings of all variables. Regarding measurements of the width (MAB, BCB, IOB, POB, BAC and BAM) an d length (GLS, MTL, M13 and MAN) of skull, PC1 scores show that the Bolivian sample (sample 1) is larger than the Peruvian samples (samples 8 and 9), with intermediate values, and Amazonian samples (samples 2, 3 and part of 4), with the lower values. The score of the holotype of M. guaycuru (sample 6) reveals that this specimen is similar in size to Amazonian specimens. PC2 scores are not informative on the distinction of samples (Figure 4; Table 1). TABLE 1. Vector correlation coefficients ( loadings ) between original variables and principal components (PC1 and PC2) and between original variables and canonical variates (CV1 and CV2) for South American samples of M. simus. Numbers in bold indicate vector correlations with magnitudes larger than 0.29. Loadings of PCA and CVA Characters PC1 PC2 CV1 CV2 Greatest length of skull (GLS) 0.85 0.24-0.44 0.44 Mastoid breadth (MAB) 0.95 0.14 0.42 0.07 Braincase breadth (BCB) 0.85 0.41 0.34-0.63 Interorbital breadth (IOB) 0.92 0.07-0.36 0.05 Postorbital breadth (POB) 0.74 0.43 0.13 0.09 Breadth across canines (BAC) 0.84-0.45-0.10-0.09 Breadth across molars (BAM) 0.87-0.38 0.02 0.30 Maxillary toothrow length (MTL) 0.91 0.15-0.05 0.09 Molariform toothrow length (M13) 0.93-0.11 0.11 0.25 Mandibular toothrow length (MAN) 0.94 0.10 0.59-0.48 Canonical Variate Analysis The 1st and 2nd canonical variate axes (CV1 and CV2) respectively accounted for 82% and 15% of the variation among largest geographic samples. In relation to the first axis, scores of the Bolivian sample (sample 1) are co mpletely distinct from t hose of Amazonian samples (samples 2, 3 and 4 ). CV2 scores mainly separate the three Amazonian samples. A contrast between GLS and MAN, as w ell as between IOB and MAB characterizes distinction along CV1, wh ereas a co ntrast between GLS and BC B characterizes distinction along CV2 (Figure 5; Table 1). GEOGRAPHIC VARIATION IN MYOTIS SIMUS Zootaxa 2985 2011 Magnolia Press 45
FIGURE 3. Dorsal, lateral and ventral views of the skull and mandible of the holotype of M. guaycuru (ALP 9277). Scale bar = 5 mm. The distance between the dentary bones is reduced due to the disarticulation of the mandibular symphysis. 46 Zootaxa 2985 2011 Magnolia Press MORATELLI ET AL.
FIGURE 4. L eft ( a): M ultivariate individual scores of data in the two f irst principal components for samples of M. simus labeled by locality (1) Cercado, Beni, Bolivia; (2) Borba, Amazonas, Brazil; (3) Manaus, Amazonas, Brazil; (4) Parintins, Amazonas, Brazil; (5) El Refugio, Santa Cruz, Bolivia; (6) Salobra, Mato Grosso do Sul, Brazil (type specimen of M. guaycuru) (7) Rio Juruá, Amazonas, Brazil; (8) Ucayali, Loreto, Peru; and (9) San Juan, Pasco, Peru. Right (b): Corresponding vector correlations (greater than 0.29 ) of craniometric characters with the first two eigenvectors. FIGURE 5. Left (a): Multivariate individual scores in the first two discriminant axes on the discriminant function for the four largest samples of M. simus labeled by locality (1) Cercado, Beni, Bolivia; (2) Borba, Amazonas, Brazil; (3) Manaus, Amazonas, Brazil; (4) Parintins, Amazonas, Brazil. Right (b): Corresponding vector correlations (greater than 0.29 ) of craniometric characters with the first two eigenvectors. A Mantel test did not detect a significant correlation between geographic and morphologic distance matrices (r = 0.63; p = 0.125). This result suggests that the morphometric divergence between Bolivian and Amazonian samples cannot be explained by the geographic distance between them. Allocation of small samples: A pattern more congruent with the isolation-by-distance model was revealed by the probabilistic allocations of smaller to larger samples, with most small samples allocated to nearby larger ones. The specimen from Rio Juruá (Amazonas, Brazil) was mainly allocated to the Amazonian samples (97%). Speci- GEOGRAPHIC VARIATION IN MYOTIS SIMUS Zootaxa 2985 2011 Magnolia Press 47
mens from San Juan (Pasco, Peru) and Ucayali (Loreto, Peru) were mostly allocated to Amazonian samples (100 and 90%, respectively), whereas the specimen from El Refugio (Santa Cruz, Bolivia) was allocated to the Bolivian sample (91%) (Table 2). An exception to this allocation pattern was found for the holotype of M. guaycuru, from Mato Grosso do Sul, Brazil, which was not allocated to the Bolivian sample, as would be expected on geographical grounds, but to Amazonian samples in 100% of 1,000 bootstrap iterations (Table 2). The classification of Proença s type specimen to Amazonian samples may be explained by its narrower skull base, which resembles the condition of the majority of Amazonian and Peruvian specimens, the latter including topotypes of M. simus. In contrast, Bolivian specimens generally have mastoids more laterally projected. TABLE 2. Frequency distribution of classification of single specimens using the minimum Mahalanobs distances to the centroids of remaining samples based on 1,000 bootstrap iterations. Bold values correspond to higher classification values. Large samples Small samples Cercado Borba Manaus Parintins El Refugio 0.91 0.05 0.03 0.01 Salobra 0 0.65 0.17 0.17 Rio Juruá 0.03 0.02 0.95 0 Ucayali 0.10 0.03 0.10 0.77 San Juan 0 0.06 0.04 0.90 TABLE 3. Measurements of the holotype of M. guaycuru and summary of measurements (mm) and weight (g) for two samples of f emales of M. simus. F-statistics an d ass ociated p robability fro m o ne-way analyses o f v ariance (ANOVAs) for th e n ull hypothesis of equality of means for skull measurements of two samples of M. simus. Significant values are in bolt. Myotis guaycuru Pooled Amazonian samples: Borba, Manaus and Parintins (Amazonas, Brazil) Bolivian sample: Cercado (Beni, Bolivia) ANOVAs Characters Holotype Mean (Range) N Mean (Range) N F p FA 38.1 38.1 (35.5 39.7) 16 39.4 (38.5 40.7) 13 3MC 35.6 34.9 (33.1 36.5) 16 36.3 (35.3 37.9) 13 THL 6.2 5.9 (4.7 6.6) 16 5.9 (5.5 6.5) 13 LDH 3.8 3.9 (3.1 4.7) 15 4.5 (3.4 5.4) 13 LVH 3.6 3.4 (3.0 4.0) 15 3.7 (2.9 4.4) 12 Weight 10.3 (9.0 10.8) 12 GLS 13.66 14.05 (13.57 14.59) 19 14.62 (13.93 14.99) 27 52.438 <0.001 CCL 12.17 12.36 (11.87 12.85) 18 12.94 (12.42 13.31) 27 67.904 <0.001 CIL 13.01 13.23 (12.75 13.73) 19 13.93 (13.31 14.28) 27 86.736 <0.001 BL 11.55 11.82 (11.18 12.23) 19 12.4 (12.10 12.69) 20 63.408 <0.001 ZB 8.83 9.05 (8.93 9.18) 3 9.93 (9.61 10.23) 11 53.604 <0.001 MAB 7.43 7.47 (7.26 7.64) 17 8.21 (7.97 8.46) 27 324.753 <0.001 BCB 7.03 6.94 (6.67 7.27) 18 7.38 (7.06 7.71) 27 90.266 <0.001 IOB 4.86 4.74 (4.57 4.97) 19 4.8 (3.91 5.28) 27 0.33 0.569 POB 3.9 3.82 (3.63 3.96) 19 4.03 (3.79 4.34) 21 33.006 <0.001 BAC 3.86 4.01 (3.67 4.27) 17 4.22 (3.98 4.41) 27 23.992 <0.001 BAM 5.53 5.69 (5.28 5.98) 19 6.08 (5.82 6.35) 27 58.367 <0.001 MTL 5.03 5.03 (4.86 5.19) 18 5.37 (5.14 5.58) 27 110.41 <0.001 M13 2.95 2.94 (2.72 3.11) 19 3.2 (3.08 3.32) 21 103.612 <0.001 MAL 9.98 10.16 1 10.77 (10.21 11.83) 18 3.35 0.085 MAN 5.16 5.4 (5.19 5.54) 18 5.77 (5.48 5.97) 25 111.795 <0.001 Summary statistics: N = sample size. See text for a description of measurement methods. 48 Zootaxa 2985 2011 Magnolia Press MORATELLI ET AL.
Measurements summarized on Table 3 revea l that the Bolivian sample is larger than Amazon samples in all characters, the majority being statistically significant (except IOB and MAL). Among cranial measurements, two better distinguish Amazon and Bolivian samples, the zygomatic breadth (ZB) and the mastoid breadth (MAB). Qualitative variation in M. simus. The majority of Bolivian specimens have more laterally projected mastoid processes, a condition present in few specimens from Amazoni an and Peruvian samples (Figure 6), resulting in larger averages for the mastoid breadth (see Table 3). In few specimens of these samples considerable variation in the color of f ur was recorded, t he dorsal and vent ral pelage of one B olivian specimen ( USNM 584502) being Ochraceous-orange, while the dorsal pelage of central and western Amazonian specimens being Tawny, Russet or Cinnamon-brown, and the ventral pelage Ochraceous-tawny or Buckthorn-brown (USNM 364482, AMNH 76252, AMNH 91414). The frequency of distribution of other qualitative characters analyzed did not reveal consistent differences among samples (Table 4). FIGURE 6. Dorsal view of the skulls of two specimens of M. simus: A from Santa Cruz, Bolivia (USNM 584502), B from Pasco, Peru (USNM 364482). Scale bar = 5 mm. Description of M. simus. The holotype of M. simus is an adult female (BMNH 8.5.12.2), preserved in fluid, with skull and mandible cleaned, collected by W. Davis in 1876 in Río Ucayali, Loreto, Peru, altitude of 100 m (06 44 S, 75 06 W) (Thomas 1901; LaVal 1973; Carter & Dolan 1978). The following description is base d on photographs generously provided by L. Tomsett (BMNH): the skull and mandible are complete, with the exception of the zygomatic arches, in which both jugal and squamosal processes are broken (Fig. 7). The rostrum is short and wide, the P3 is lingually displaced, being smaller than the P2, the sagittal and occipital crests are present, the pari- GEOGRAPHIC VARIATION IN MYOTIS SIMUS Zootaxa 2985 2011 Magnolia Press 49
etal is inclined forward and the supraoccipital region is flattened in lateral view, not projected much beyond the posterior limit of occipital condyles (Fig. 7). According to Thomas (1901) description, the pelage is short and the plagiopatagium is attached at ankles. TABLE 4. Occurrence and distribution of sel ected qualitative characters in M. simus for Bolivian (group 1) and pooled Amazonian (groups 2, 3 and 4) samples. Sample 1 (Bolivia) Samples 2, 3 and 4 (Amazon) Characters N (%) N (%) P3 (position regarding other premolars) N total = 23 N total = 33 Displaced and not visible in lateral view 1 (4.3) 3 (9.1) Displaced and visible in lateral view 0 (0.0) 0 (0.0) Aligned and not visible in lateral view 21 (91.3) 24 (72.7) Aligned and visible in lateral view 1 (4.3) 6 (18.2) Sagittal crest (occurrence) N total = 23 N total = 37 Absent 1 (4.3) 1 (2.7) Present 22 (95.7) 36 (97.3) Sagittal crest (height) N total = 22 N total = 35 Very low 8 (36.4) 10 (28.6) Low 6 (27.3) 1 (2.9) Medium 8 (36.4) 5 (14.3) High 0 (0.0) 19 (54.3) Occipital crests (occurrence) N total = 23 N total = 37 Absent 0 (0.0) 1 (2.7) Present 23 (100) 36 (97.3) Occipital crests (height) N total = 23 N total = 34 Very low 4 (17.4) 2 (5.9) Low 7 (30.4) 8 (23.5) Medium 11 (47.8) 14 (41.2) High 1 (4.3) 10 (29.4) Braincase roof (shape) N total = 23 N total = 34 Parietal straight 3 (13.0) 5 (14.7) Parietal inclined forward 20 (87.0) 29 (85.3) Occipital region (shape) N total = 23 N total = 34 Occipital rounded 0 (0.0) 5 (14.7) Occipital flattened 23 (100) 29 (85.3) Plagiopatagium (point of insertion) N total = 17 N total = 29 At ankles 0 (0.0) 5 (17.2) At toes by a narrow band of membrane 17 (100) 24 (82.8) Based on the series available for the present study, M. simus can be described as follows: a medium-sized species (FA 35.5 39.7 mm; weight 5 10 g) compared with other South American Myotis; ears small (11 13 mm); plagiopatagium attached at toes by a narrow band of membrane (78%) or at ankles (22%); short and woolly pelage; length of dorsal hairs ranging from 3 to 5 mm; color of dorsal pelage varying between Ochaceous-orange and Sudan-brown, without contrast between bases and tips; length of ventral hairs varying from 3 to 5 mm and slightly 50 Zootaxa 2985 2011 Magnolia Press MORATELLI ET AL.
FIGURE 7. Dorsal, lateral and ventral views of the skull and mandible of the holotype of M. simus (BMNH 85.5.12.2). Scale bar = 5 mm. Photographs provided by Roberto Portela Miguez (The Natural History Museum, England). GEOGRAPHIC VARIATION IN MYOTIS SIMUS Zootaxa 2985 2011 Magnolia Press 51
bicolor; plagiopatagium and uropatagium Cinnamon-brown; fringe of hairs along the trailing edge of the uropatagium absent; skull moderate in total length (GLS 13.5 15.0 mm), with a well-marked interorbital constriction in dorsal view. In lateral view, the parietal is generally inclined forward (88%) and the supraoccipital region is flattened (89%); sagittal crest generally present (86%) and very low (25%), low (17%), medium (24%) or high (34%); occipital crests always present (100%) and very low (8%), low (32%), medium (36%) or high (24%); P3 generally in toothrow (91%), not visible (73%) in lateral view. For field identification the most relevant characters are t he plagiopatagium attached at toes by a narrow band of membrane or at ankles, the extremely short and woolly fur and the absence of a fringe of hairs along the trailing edge of the uropatagium. Discussion Nomenclatural implications. Thomas (1901) and Miller and Allen (1928) used the attachment of plagiopatagium as a diagnostic character to distinguish M. simus from all other South American forms of Myotis. However, Handley (1960) considered this character an artifact of preparation, and regarded it as usel ess, a decision followed by LaVal (1973). More recently, Baud and Menu (1993) analyzed the insertion of plagiopatagium in live specimens and ratified its validity in distinguishing M. simus from other species, a f inding reiterated by subsequent authors (e.g., López-González et al. 2001; López-González 2005; Moratelli 2008; Wilson 2008). Based on the attached to the ankles condition of the plagiopatagium, the short pelage and the similar cranial morphology revealed by morphometric analyses with respect to the topotypical series of M. simus, Myotis guaycuru Proença, 1943 must be regarded as junior-synonym of Myotis simus Thomas, 1901, as formerly proposed by López-González et al. (2001). Variation in M. simus. The multivariate analyses revealed that (1) the Bolivian sample is larger than available northern samples, which was confirmed by the univariate comparisons; (2) Peruvian and Amazonian samples are craniometrically similar, whereas the Bolivian sample is the most distinct; finally, (3) the skull of the holotype of M. guaycuru is more similar to those of Amazonian/Peruvian specimens than to the geographically closer Bolivian samples. López-González et al. (2001) had found significant differences between northern (northern Brazil, Ecuador and Peru) and southern (Bolivia and Paraguay) samples of M. simus, the first being smaller for seven cranial measurements (condylo-canine l ength, mast oid l ength, braincase breadth, length of t he r ostrum, maxi llary t oothrow length, molariform toothrow length and mandibular toothrow length). Those authors also verified that Bolivian sample was s ignificantly l arger t han a Paraguayan sampl e in f our cranial measuremen ts (mast oid breadth, braincase breadth, length of the rostrum and maxillary toothrow length). Based on the morphometric structure revealed by López-González et al. (2001) and the present study, with Bolivian samples presenting larger averages than northern and southern samples, in addition to different pelage color and cranial morphology, we hypothesize that Bolivian population may con stitute a di stinct species. Under this interpretation, the holotype of M. guaycuru could fill in a ga p connecting the more similar Amazonian and Peruvian samples with the Paraguayan sample, at the exclusion of the population from Bolivia. However, considering the absence of specimens from Paraguay in the present analysis, and t he overall rarefaction of intermediate samples in relation to those from Bolivian and from Amazonian/Peruvian localities, a more definite conclusion in this r egard m ust be postponed. Together wit h mor e compr ehensive morphological sampl es, molecular st udies addressing the genetic variation of samples should help in evaluating this hypothesis. Finally, if future analyses confirm distinction of the Bolivian population, in order to formally recognize it a new name should be proposed, as the holotype of M. guaycuru was found to be morphometrically more similar to the Amazonian/Peruvian samples, this last including a topotypical series of M. simus. Acknowledgments Celia López González (Instituto Politécnico Nacional, Durango, Mexico) kindly made available data about the Paraguayan specimens of M. simus; we op ted not to include them in the morphometric analyses, as measurements could not be conf idently associated with ours, as they have been t aken under a distinct protocol by a dif ferent researcher. T he following curators and col lection staff provided access t o specimens under t heir care: Leandro Salles, Luiz Flamarion Oliveira and Stella Maris Franco (Museu Nacional, Brazil), Fernando de Camargo Passos (Universidade F ederal do P araná, Brazil), Teresa C ristina C. Margarido (Museu d e H istória N atural C apão da 52 Zootaxa 2985 2011 Magnolia Press MORATELLI ET AL.
Imbuia, Brazil), Mario de Vivo, Juliana Barros (Museu de Zoologia da Universidade de São Paulo, Brazil), Eliana Morielle-Versute (Uni versidade Estadual P aulista Ju lio d e Mesqu ita F ilho, B razil), Nanc y Si mmons, E ileen Westwig (American Museum of Natural History, USA), Don Wilson, Linda Gordon (National Museum of Natural History, USA), Alfred Gardner (USGS Patuxent Wildlife Researche Center, USA) and Patrick Boussès (Muséum national d Histoire nat urelle, Fr ance). R oberto Por tela-miguez ( The Natural Hi story Museum, England) generously provided pictures of the skull of the holotype of Myotis simus. We are grateful to Jane Steele for helpfully reviewing previous drafts of the manuscript. This work fulfils part of the requirements for PhD degree in Zoology of RM at Universidade Federal do Rio de Janeiro. RM was partially supported by a scholarship from Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior (CAPES, Ministério da Educação, Brazil), and by Short-Term Visitor and C ollection Study grants respectively from the N ational Museum of Natural History (USA) and the American Museum of Nat ural History ( USA). This work was al so supp orted by r esearch f ellowships to JAO (CNPq 306801/2007-8) and to ALP (CNPq 303622/2009-1). References Baud, F.J. & Menu, H. (1993) Paraguayan bats of the genus Myotis, with a redefinition of Myotis simus (Thomas, 1901). Revue Suisse de Zoologie, 100, 595 607. Bianconi, G.V. & Pedro, W.A. (2007) Família Vespertilionidae. In: Reis, N.R., Peracchi, A.L., Pedro, W.A. & Lima, I.P. (Eds.), Morcegos do Brasil. Editora da Universidade Estadual de Londrina, Londrina, pp. 167 195. Carter, D.C. & Dolan, P.G. (1978) Catalog of type specimens of Neotropical bats in selected European museums. Special Publications, The Museum, Texas Tech University Press, 15, 1 136. Cherem, J.J., Simões-Lopes, P.C., Althoff, S. & Graipel, M.E. (2004) Lista dos mamíferos do Estado de Santa Catarina, sul do Brasil. Mastozoologia Neotropical, 11, 151 184. Findley, J.S. (1993) Bats, a community perspective. Cambridge University Press, Cambridge, United Kingdom. Gardner, A.L. (2008) Mammals of South America. Volume 1, Marsupials, Xenarthrans, Shrews, and Bats. The University of Chicago Press, Chicago, xx + 669 pp. Handley, C.O., Jr. (1960) Descriptions of new bats from Panama. Proceedings of the United States National Museum, 112, 459 479. Krazanowski, W.J. & Lai, Y.T. (1988) A criterion for determining the number of % groups in a data set using sum-of-squares clustering. Biometrics, 44, 23 34. LaVal, R.K. (1973) A revision of the neotropical bats of the genus Myotis. Natural History Museum, Los Angeles County, Science Bulletin, 15, 1 54. Little, R.J.A. & Rubin, D.B. (1987) Statistical analysis with missing data. John Wiley & Sons, New York, xviii + 392 pp. López-González, C. (2005) Murciélagos de Paraguay. Publicaciones MAB, 9, 1 316. López-González, C., Presley, S.J., Owen, R.D. & Willig, M.R. (2001) Taxonomic status of Myotis (Chiroptera: Vespertilionidae) in Paraguay. Journal of Mammalogy, 82, 138 160. Manly, B.F. (1994) Multivariate statistical methods, a primer. 2 nd ed. Chapman & Hall, London, 215 pp. Mantel, R.M. (1967) The detection of disease clustering and a general regression approach. Cancer Research, 27, 209 220. Miller, G.S., Jr. & Alle n, G.M. ( 1928) The am erican b ats o f the genera Myotis and Pizonyx. Bulletin of the United States National Museum, 144, 1 128. Moratelli, R. (2008) Revisão taxonômica das espécies de Myotis Kaup, 1829 do Brasil (Mammalia, Chiroptera, Vespertilionidae): uma abordagem morfológica e morfométrica. PhD Thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, ix + 265 pp. Neff, N.A. & Marcus, L.F. (1980) A survey of multivariate methods for systematics. Private published, New York, x + 230 pp. Peracchi, A.L., Lima, I.P., Reis, N.R., Nogueira, M.R. & Ortencio-Filho, H. (2006) Ordem Chiroptera. In: Reis, N.R., Peracchi, A.L., Pedro, W.A. & Lima, I.P. (Eds.), Mamíferos do Brasil. Editora da Universidade Estadual de Londrina, Londrina, pp. 153 230. Proença, A.M.C. (1943) Myotis guaycurú n.sp., morcego proveniente de Salobra, Estado de Mato Grosso (Microchiroptera, Vespertilionidae). Revista Brasileira de Biologia, 3, 313 315. Ridgway, R. (1912) Color standards and color nomenclature. Privately published, Washington, D.C., 48 pp. + 53 pl. Simmons, N.B. (2005) Order Chiroptera. In: Wilson, D.E. & Reeder, D.M. (Eds.), Mammal Species of the World: a taxonomic and geographic reference. 3 th Ed. Smithsonian Institution Press, Washington, D.C., pp. 312 529. Strauss, R.E., Atanassov, M.N. & Oliveira, J.A. (2003) Evaluation of the principal-component and expectation-maximization methods for estimating missing data in morphometric studies. Journal of Vertebrate Paleontology, 23, 284 296. Thomas, O. (1901) On a collection of bats from Pará. Annals and Magazine of Natural History, series 7, 8, 189 193. Thomas, O. (1902) On Azara s Chauve-souris onzieme (Myotis ruber, Geoff.) and a new species allied to it. The Annals and Magazine of Natural History Series, 7, 10, 494 495. GEOGRAPHIC VARIATION IN MYOTIS SIMUS Zootaxa 2985 2011 Magnolia Press 53
Travassos, L. (1 940) Relatório da Terceira excursão a zona da Estrada de Ferro Noroeste do Brasil re alizada em Fevereiro e Março de 1940. I Introdução. Memórias do Instituto Oswaldo Cruz, 35, 607 609. Wallauer J.P., Becker, M., Marins-Sá, L.G., Liermann, L.M., Perretto, S.H. & Schermack, V. (2000) Levantamento dos mamíferos da Floresta Nacional de Três Barras - Santa Catarina. Biotemas, 13, 103 127. Wilson, D.E. (2008) Genus Myotis Kaup 1829. In: Gardner, A.L. (Ed.). Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews, and Bats. Chicago and London: University of Chicago Press, pp. 468 481. Appendix: Specimens examined. The voucher-specimens examined are deposited in the following institutions: American Museum of Natural History, New York, USA (AMNH), National Museum of Natural History, Washington DC, USA (USNM), Museu de Zoologia da Universidade de São Paulo, São Paulo, Brazil (MZUSP) and Universidade Federal Rural do Rio de Janeiro, Seropédica, Brazil (ALP). Individuals marked with an asterisk were used in the morphometric analyses. The coordinates were obtained from the skin tags, from the Gazetteer of Marginal Localities of Gardner (2008) and from the Google Earth Program. BO LIVIA: Ce rcado, Be ni ( 14 39 S, 64 39 W): A MNH 2 11155, 21 1156, 2 11167*, 2 11168*, 2 11169*, 2 11170, 21 1171*, 211172*, 211173*, 211174*, 211178*, 211179*, 211180*, 211181*, 211182*, 211183*, 211190, 211192*, 211193*, 211194*, 211195*, 211196*, 211197*, 211198*. El Refugio, Santa Cruz (14 45 S, 61 02 W): USNM 584502*. BRAZIL: Borba, Amazonas (06 53 S, 52 02 W): A MNH 91 886, 91 887, 9 1888*, 91 889*, 91890*, 91891, 91892, 94224, 94225, 94227, 94230, 94231, 9 4232, 942 33*, 9 4234*. I tacoatiara, Amazonas (03 08 S, 5 8 26 W): MZ USP 34 72. M anaus, A mazonas (0 1 4 S, 63 36 W): AMNH 79534, 91472, 91473, 91474, 91475*, 91476*, 91477*, 91478*, 91500*. Parintins, Amazonas (02 38 S, 56 44 W): 92983*, 93489, 93490*, 93491, 93492*, 93493*, 93494*, 93495*, 93496*, 93497, 93922*, 93923*, 93924, 93925. Rio Juruá, Amazonas (04 48 S, 68 67 W): MZUSP 638, 1074*. Taiamã, Mato Grosso (16º48 S, 57º28 W): MZUSP 13815. Salobra, Mato Grosso do Sul (21 58 S, 56 31 W): ALP 9277*. Localidade desconhecida: MZUSP 1062. ECUADOR: Pastaza, Quito (1º27 S, 76º40 W): AMNH 71483, 71485, 71486, 71487, 71488, 71490, 71491, 71492, 71493, 71494 PERU: Maynas, Loreto (03 19 S, 72 07 W): AMNH 74105, 74109, 74110, 74378, 74379, 74380, 74381. Ucayali, Loreto (06 44 S, 75 06 W): AMNH 76 240, 76 241, 76 242, 76 243, 762 44*, 76245, 76246, 76 247, 76 248, 76 249, 76 252*, 76253*. S an Jua n, Pasco (10 30 S, 74 53 W): USNM 364481*, 364482*. 54 Zootaxa 2985 2011 Magnolia Press MORATELLI ET AL.