Research Article |
Corresponding author: Túlio Henrique Lemos ( tuliohlemos@gmail.com ) Corresponding author: Ligiane Martins Moras ( ligimoras@gmail.com ) Academic editor: Ricardo Moratelli
© 2020 Túlio Henrique Lemos, Valéria da Cunha Tavares, Ligiane Martins Moras.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Lemos TH, da Cunha Tavares V, Moras LM (2020) Character variation and taxonomy of short-tailed fruit bats from Carollia in Brazil. Zoologia 37: 1-7. https://doi.org/10.3897/zoologia.37.e34587
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Carollia has a complex taxonomic history and is widely distributed in the Neotropics. Species of Carollia appear to have differentiated recently in the late Cenozoic, and present overlapping morphological characters that may not be useful to distinguish among species. Carollia has recently been revised, but only a few specimens representing the Brazilian distribution of Carollia within Brazil were studied. We reviewed specimens of Carollia distributed in several localities of Brazil revisiting previously described morphological characters for species identification, and taxonomic problems within the genus. We found a large degree of overlap between characters previously used to distinguish among species of Carollia, and some of them constitute variation within a same species. We also report new records extending the known distribution of C. benkeithi to farther east of its previously known distribution (Parauapebas, southeastern Pará, and Vitória do Xingu, Pará, eastern Amazonian Brazil) and one record extending the distribution of C. brevicauda south to Corumbá, Mato Grosso do Sul, Brazil.
Carollia, morphology, Phyllostomidae
The short-tailed bats from Carollia Gray, 1838 are gleaning frugivores that forage in highly cluttered spaces, and may complement their diet with insects (
Carollia currently includes eight species distributed from central Mexico southward to southern Brazil and northern Argentina (
The sister species Carollia brevicauda and C. perspicillata, and the closely related small-sized species C. castanea, C. benkeithi and an undescribed taxa from Eastern Ecuador and Peru are overall difficult to identify based on morphological characters only along most of their distribution (
Herein we studied specimens of Carollia from several regions of Brazil previously identified as C. benkeithi, C. brevicauda or C. perspicillata checking the consistency of the characters available in the literature traditionally used for their differentiation (e.g.,
Specimens analyzed for this study are housed in the mammals collection of the Universidade Federal de Minas Gerais (UFMG) and Museu Paraense Emílio Goeldi (MPEG), Brazil (see Appendix 1). To identify them we used a set of characters described in the literature (
We analyzed morphometric variation of the skull using selected measurements and included additional characters to describe and analyze the skull/mandible articulation, which have been considered useful to distinguish among species of Carollia (
We performed the Student´s t-test (p < 0.01) to test for sexual dimorphism within individuals of the same species. We run a principal component analysis (PCA) to display the variation across the three species (C. perspicillata, C. brevicauda, and C. benkeithi) using 16 log10-transformed measurements. To test for the variation of measurements between C. perspicillata and C. brevicauda we applied Student´s t-test (p < 0.01) and the nonparametric Mann-Whitney U-test. The statistical analysis ware performed using PAST V 3.11 (
We also studied the distribution and the scoring of discrete morphological characters available in the literature for species of Carollia (e.g.,
We examined 123 specimens of Carollia, and identified northern, midwestern and southeastern populations of Carollia brevicauda (34) and C. perspicillata (86), and northern populations of C. benkeithi (3) within Brazil (Appendix 1, Fig.
Distribution map of C. perspicillata (black dots), C. brevicauda (blue diamonds), C. brevicauda and C. perspicillata in sympatry (gray dots and red cross). C. benkeithi and C. perspicillata in sympatry (red pentagon), and C. benkeithi, C. brevicauda and C. perspicillata in sympatry (red star). Both localities of C. benkeithi represent new records for the species, and the red cross is a new record for C. brevicauda.
The hair covering of the forearm, the forearm length, the dorsal fur length and the banding pattern of the individual hairs were the most useful external characters to separate the three species of Carollia present in our sampling. We identified individuals having naked forearms with lengths measuring less than 37.0 mm, short dorsal fur, and no evident banding of individual hairs as C. benkeithi (Tables
According to our sampling the three species of Carollia: C. benkeithi, C. brevicauda and C. perspicillata, occur sympatrically in Parauapebas, in the FLONA Carajás, southern Pará, and in Vitória do Xingu, Pará, eastern Amazonian Brazil. Sympatric populations of C. perspicillata and C. brevicauda also occur in the states of Espírito Santo (Guaçuí, Linhares and Mimoso do Sul), Minas Gerais (Jequitaí and Mariana), Bahia (Caetité), Mato Grosso do Sul (Corumbá) and in several localities in Pará, including the East, Center and Southeast in the Amazon basin and the Northwest, in the Guiana shield (Altamira, Xinguara, Canaã dos Carajás, Paragominas and Porto Trombetas) (Appendix 1, Fig.
Measurements (mm) of adults of Carollia benkeithi, C. brevicauda, and C. perspicillata. See Material and Methods for explanation of measurements and abbreviations. Statistics include the mean, range (in parentheses) and sample size, respectively. Useful measurements to distinguish between C. perspicillata and C. brevicauda are indicated in boldfaced (Mann-Whitney U-test, p < 0.01).
Characters | C. benkeithi | C. brevicauda | C. perspicillata | |||||
Males | Females | Males | Females | Males | Females | |||
ML | 12.87 | 12.26 | 14.55 (13.41-15.44) 23 | 14.16 (13.08-14.64) 10 | 14.67 (13.80-15.61) 50 | 14.50 (13.79-15.25) 34 | ||
COH | 4.04 | 3.74 | 5.37 (4.69-5.90) 23 | 5.17 (4.39-5.79) 11 | 5.36 (4.48-6.34) 48 | 5.26 (4.78-5.66) 32 | ||
MANDL | 7.25 | 6.88 (6.82-6.94) 2 | 8.38 (7.45-9.23) 23 | 8.02 (7.17-8.38) 10 | 8.41 (7.68-8.86) 50 | 8.32 (7.52-8.89) 34 | ||
GLS | 19.78 | 19.07 (18.70-19.43) 2 | 21.83 (20.51-22.97) 23 | 21.58 (20.30-22.73) 11 | 22.05 (20.81-23.37) 51 | 21.82 (20.93-22.74) 35 | ||
CIL | 15.35 | 15.26 (14.99-15.52) 2 | 17.83 (16.36-19.01) 23 | 17.53 (15.86-18.50) 11 | 18.07 (17.03-19.12) 51 | 17.81 (16.97-18.89) 35 | ||
PL | 8.64 | 8.42 (8.03-8.81) 2 | 9.13 (8.00-9.90) 23 | 9.00 (7.45-9.88) 11 | 9.24 (8.44-10.14) 51 | 9.19 (8.32-10.19) 35 | ||
BH | 7.68 | 7.31 (7.11-7.51) 2 | 8.41 (7.61-8.89) 23 | 8.23 (7.93-8.55) 11 | 8.45 (7.79-8.93) 51 | 8.20 (7.43-8.58) 35 | ||
BB | 8.41 | 8.12 (7.85-8.38) 2 | 9.32 (8.87-10.01) 23 | 9.11 (8.82-9.55) 11 | 9.39 (8.77-9.80) 51 | 9.12 (8.65-9.65) 35 | ||
POB | 5.24 | 5.06 (4.93-5.19) 2 | 5.41 (4.91-5.79) 23 | 5.32 (5.09-5.55) 11 | 5.45 (5.03-5.85) 51 | 5.27 (4.90-5.63) 35 | ||
MFB | 4.98 | 5.18 (4.93-5.42) 2 | 5.82 (5.52-6.34) 23 | 5.72 (5.32-6.13) 10 | 5.83 (5.07-6.35) 50 | 5.74 (5.21-6.38) 35 | ||
C-C | 4.25 | 3.96 (3.94-3.98) 2 | 4.64 (4.20-4.88) 23 | 4.43 (4.08-4.61) 11 | 4.62 (4.07-5.05) 51 | 4.40 (4.09-4.76) 35 | ||
MTRL | 6.30 | 6.14 (5.99-6.28) 2 | 7.20 (6.42-7.82) 23 | 7.12 (7.10-7.34) 10 | 7.22 (6.65-7.79) 48 | 7.19 (6.47-7.87) 35 | ||
BPM | 3.78 | 3.59 (3.54-3.63) 2 | 4.34 (3.77-4.70) 22 | 4.25 (3.88-4.78) 11 | 4.41 (3.87-4.93) 51 | 4.31 (3.71-4.90) 35 | ||
BM | 6.89 | 6.79 (6.58-7.00) 2 | 7.82 (7.30-8.39) 23 | 7.85 (7.13-8.42) 10 | 7.82 (7.04-8.47) 48 | 7.69 (7.00-8.27) 35 | ||
FA | 35.98 | 34.83 (34.33-35.32) 2 | 39.44 (35.34-42.55) 23 | 39.86 (36.13-42.02) 11 | 40.87 (37.82-44.47) 51 | 41.41 (38.42-44.64) 35 | ||
E | 13.98 | 17.06 (17.04-17.08) 2 | 19.24 (16.50-20.76) 21 | 19.25 (17.38-21.55) 7 | 19.79 (17.32-21.99) 47 | 19.75 (17.72-22.94) 29 | ||
Ti | 16.91 | 14.70 (14.38-15.02) 2 | 17.59 (14.31-19.74) 23 | 17.37 (15.97-20.06) 10 | 18.46 (16.06-20.39) 51 | 18.29 (15.40-20.59) 31 |
Morphological characters useful for identification of Brazilian populations of C. benkeithi, C. brevicauda, and C. perspicillata.
Characters | C. benkeithi | C. brevicauda | C. perspicillata |
Banding of individual hair in the dorsal fur | Little marked or absent | Evident, with a large well marked black base | Less conspicuous, proximal dark colored band not as evidently marked as the other two bands |
Length of dorsal fur | Short | Long | Short |
Fur on dorsal forearm | Absent | Present | Present |
Forearm lenght (mm) | 34-36 | 36-42 | 37-44 |
We recorded two new locality records for C. benkeithi; Parauapebas, PA, and Vitória do Xingu, PA, eastern Amazon (Appendix 1, Fig.
We did not detect sexual dimorphism in size for the species analyzed (p < 0.01). Morphometric variation for C. benkeithi, C. brevicauda, and C. perspicillata are overall within the expected range according to the data available in literature (Table
Most of the morphometric variation can be explained by the first three components in the PCA (PC1 = 52,2%, PC2 = 10,2% and PC3 = 6.9%) (Table
Vector correlation coefficients (loadings) between original variables and principal components (PC1, PC2 and PC3) for analysis including Carollia benkeithi, C. brevicauda, and C. perspicillata. Values in boldface indicate vector correlations with magnitudes > 0.50. Descriptionn of the measurements are in the text.
Characters | PCA loadings | ||
PC 1 | PC 2 | PC 3 | |
ML | 0.212 | -0.086 | -0.118 |
COH | 0.315 | 0.294 | -0.681 |
MANDL | 0.287 | -0.116 | 0.004 |
GLS | 0.210 | -0.030 | -0.017 |
CIL | 0.255 | -0.037 | -0.036 |
PL | 0.240 | -0.105 | -0.133 |
BH | 0.193 | 0.060 | 0.071 |
BB | 0.153 | 0.143 | 0.117 |
POB | 0.145 | -0.041 | 0.189 |
MFB | 0.206 | 0.121 | 0.016 |
C-C | 0.190 | 0.277 | 0.280 |
MTRL | 0.260 | -0.115 | -0.029 |
BPM | 0.257 | 0.575 | 0.453 |
BM | 0.181 | 0.234 | -0.005 |
FA | 0.252 | -0.246 | 0.009 |
E | 0.275 | -0.001 | -0.232 |
Ti | 0.370 | -0.548 | 0.326 |
Similar patterns were observed in linear measurements (Table
Based on our revisionary work of Brazilian specimens of Carollia, we expanded the distribution of C. benkeithi to approximately 420 km to the east and 663 km to the southeast, and the distribution of C. brevicauda 580 Km to the east. Other than that, the distribution for the three species of Carollia (C. perspicillata, C. brevicauda, and C. benkeithi) is in agreement with the literature (e.g.,
A few measurements may be used for species determination of Carollia species together with other characters, but linear morphometry alone was not efficient to separate among them. Some external characters previously discussed for the variation of C. benkeithi, C. brevicauda and C. perspicillata (
Dental characters used by
Reports on the occurrence of sexual dimorphism in size for Carollia have been controversial in the literature. Sexual dimorphism in size for species of Carollia has been reported for
The difficulties to identifying useful discrete characters to differentiate among species of Carollia are related to the variation of characters along their geographic distribution resulting in problems for the taxonomy and species delimitation within the genus. Accordingly, several authors described characters to separate among species of Carollia, which were useful but generally limited to a certain part of the species distribution (
Data from some studies suggest that the articulation of skull and mandible, particularly the bone surface where the masticatory muscles are inserted is highly variable for Carollia species encompassing 80% of the cranial variation for the genus (
Several other species of Carollia have been described over the last decades based on molecular data with relatively little morphological delimitation often making it difficult the identification of the species based on morphology only (
We are thankful to Fernando Araújo Perini for providing access to the specimens and laboratory of the mammal’s collection of the Universidade Federal de Minas Gerais. We also thank Rodolfo G.A.V. Stumpp for helping with the preparation of the skull of some specimens.
Carollia benkeithi: Pará – Parauapebas: VCT 4698, male, VCT 4710, female; Vitória do Xingu: MPEG 41122, female.
Carollia brevicauda: Bahia – Caetité: VCT 2912, male, VCT 2916, male, uncatalogued. Espírito Santo – Domingos Martins: PCH 183, male, uncatalogued; Guaçuí: UFMG 5052, male; Linhares: UFMG 5065, female, UFMG 5068, male; Mimoso do Sul: UFMG 5071, female; São José do Calçado: UFMG 5091, male. Mato Grosso do Sul – Corumbá: VCT 6071, male, uncatalogued. Minas Gerais – Brumadinho: VVM 02, male, VVM 67, male, uncatalogued; Jequitaí: UFMG 5025, male; Mariana: VCT 5296, female, VCT 5315, female, VCT 5381, male, VCT 6003, male, uncatalogued; Marliéria: UFMG 1060, female, UFMG 3341, female; Pará – Altamira: MPEG 41056, male; Canaã dos Carajás: VCT 1381, male, VCT 1383, male, VCT 1840, male, VCT 1847, male, uncatalogued; Paragominas: VCT 1013, female, uncatalogued; Parauapebas: VCT 1092, male, VCT 1150, male, VCT 4490, male, VCT 6202, male, uncatalogued; Porto Trombetas: UFMG 3219, female, UFMG 3237, female, VCT 0482, female, VCT 2887, male, uncatalogued; Xinguara: VCT 3834, male, uncatalogued. Rio de Janeiro – Silva Jardim: UFMG 1604, female.
Carollia perspicillata: Amazonas – Manaus: UFMG 3751, female, UFMG 5281, male, UFMG 5282, female. Bahia – Caetité: VCT 2908, female, VCT 2914, male, uncatalogued; Macarani: UFMG 4820, male. Espírito Santo – Guaçuí: UFMG 5053, male; Linhares: UFMG 5066, female, UFMG 5067, female; Mimoso do Sul: UFMG 5073, female; Sooretama: UFMG 4744, male, UFMG 4745, male, UFMG 4746, female, UFMG 4747, female. Maranhão – Cândido Mendes: UFMG 3719, male, UFMG 3720, male, UFMG 3723, male, UFMG 3726, male, UFMG 3728, male, UFMG 3733, male, UFMG 5325, male; São Luiz: VCT 0314, female, VCT 0319, male, VCT 0340, male, uncatalogued; Mato Grosso – Aripuanã: UFMG 5321, male. Mato Grosso do Sul – Corumbá: VCT 6066, uncatalogued, male. Minas Gerais – Belo Horizonte: UFMG 3495, male, UFMG 3743, male; Conceição do Mato Dentro: UFMG 4837, female, UFMG 4838, male, UFMG 4839, male, UFMG 4841, female; Cordisburgo: UFMG 0514, male; Jequitaí: UFMG 5022, female, UFMG 5023, male; Mariana: VCT 5293, male; Matutina: UFMG 4676, female, UFMG 4677, male; Patrocínio: UFMG 4731, female, UFMG 4733, male, UFMG 4734, female; Várzea da Palma: UFMG 2357, female, UFMG 2358, female. Pará – Altamira: VCT 1600, female; Anapu: VCT 1532, female; Canaã dos Carajás: BOC 05, male, BOC 09, female, BOC 21, male, BOC 26, male, BOC 382, female, BOC 387, male, BOC 435, female, BOC 452, male, VCT 1377, male, VCT 1857, female, uncatalogued; Curionópolis: UFMG 4622, male, UFMG 4623, male, UFMG 4624, male, UFMG 4628, female, UFMG 4629, female, UFMG 4663, female; Paragominas: VCT 0963, male/, VCT 0972, male, VCT 0982, male, VCT 1006, female; Parauapebas: VCT 4383, female, VCT 4700, male, VCT 6183, female, VCT 6184, female, VCT 6205, male, VCT 6207, female, VCT 6211, male, VCT 6245, male, uncatalogued; Porto Trombetas: UFMG 3193, female, UFMG 3223, male, UFMG 3229, male, UFMG 3230, male, UFMG 3253, female, UFMG 3266, female, UFMG 3223, male, VCT 2826, male, VCT 2875, female, uncatalogued; Vitória do Xingu: VCT 1498, male, VCT 1550, male, VCT 2487, male; Xinguara: VCT 3870, male, uncatalogued.