Research Article |
Corresponding author: Burton K. Lim ( burtonl@rom.on.ca ) Academic editor: DeeAnn Reeder
© 2020 Burton K. Lim, Livia O. Loureiro, Guilherme S.T. Garbino.
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:
Lim BK, Loureiro LO, Garbino GST (2020) Cryptic diversity and range extension in the big-eyed bat genus Chiroderma (Chiroptera, Phyllostomidae). ZooKeys 918: 41-63. https://doi.org/10.3897/zookeys.918.48786
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Since the last systematic review of Chiroderma (big-eyed bats) more than two decades ago, we report on biodiversity surveys that expand the distribution and species diversity of this Neotropical genus. The Caribbean endemic species Chiroderma improvisum is documented for the first time from Nevis in the northern Lesser Antilles. A broader geographic sampling for a molecular analysis identifies a paraphyletic relationship in Chiroderma trinitatum with respect to Chiroderma doriae. Cis-Andean populations of C. trinitatum are most closely related to the morphologically distinctive and allopatrically distributed C. doriae in the Cerrado and Atlantic Forest of Brazil and Paraguay. The sister taxon to this grouping includes trans-Andean populations of C. trinitatum, which we recommend to elevate to species status as C. gorgasi. This is an example of a cryptic species because C. gorgasi was previously considered morphologically similar to C. trinitatum, but more detailed examination revealed that it lacks a posterolabial accessory cusp on the lower second premolar and has a narrower breadth of the braincase. We provide an amended description of Chiroderma gorgasi.
Chiroderma gorgasi, Chiroderma improvisum, cryptic species, cytochrome c oxidase subunit 1, Lesser Antilles
Cryptic species, phenotypically similar organisms that are classified as a single species but are genetically divergent lineages, are being discovered at a greater rate due to the increasing prevalence of molecular methods, such as DNA barcoding (e.g.,
The big-eyed bats in the genus Chiroderma Peters (Phyllostomidae) are characterized by greatly reduced nasal bones in the skull and a combination of external features including a white dorsal stripe that does not extend onto the head; legs and interfemoral membrane conspicuously hairy; and relatively large eyes (
The systematics of Chiroderma was last reviewed by
We conducted a survey of bats on the Caribbean island of Nevis from 24–29 April 2016. Live traps used included a harp trap and 6 m or 12 m mist nets set singly in the forest understory or on a triple-high telescoping pole system. Traps were regularly monitored for the first 2–3 hours after sunset when bat activity is the highest after they leave their roosts to feed. Individuals not kept as part of the representative collection documenting the species diversity were released at point of capture. A combined scientific research and export permit (F002) was issued through the authority of the Nevis Historical and Conservation Society. An Animal Use Protocol (2016-01) was obtained from the Royal Ontario Museum Animal Care Committee. An import permit (#2016-02101-4) was authorized by the Canadian Food Inspection Agency. Use of wild mammals followed the guidelines of the American Society of Mammalogists (
The cytochrome c oxidase subunit 1 (CO1) gene is the best represented molecular marker for Chiroderma on the genetic sequence database GenBank (www.ncbi.nih.gov/genbank). There are 117 samples from nine countries in Central and South America (Brazil, Ecuador, El Salvador, French Guiana, Guatemala, Guyana, Mexico, Panama, and Suriname). We add 26 new sequences to bring the sample size to 143 sequences representing 12 countries in the Neotropics, including Venezuela, Peru, and Nevis, and five species in the genus (Appendix
Molecular methods for new sequences of CO1 follow the protocol for DNA extraction, PCR amplification, and automated nucleotide sequencing outlined in
Morphological and morphometric comparisons included 138 specimens from five species of Chiroderma, including two C. improvisum, four C. doriae, seven C. salvini, 58 C. trinitatum, and 66 C. villosum (Appendix
Measurements defined below were taken with digital calipers accurate to 0.01 mm following the descriptions of
We report the first occurrence of Chiroderma improvisum (Fig.
For COI, the 657 basepairs (bp) at the 5’ end were available for most (82%) of the specimens analyzed. The complete 1140 bp of Cytb were available, including the newly generated sequence, for most (75%) of the specimens analyzed. The topology of the Chiroderma COI maximum likelihood tree identified six primary terminal clades with (1) C. salvini as sister species to all other taxa; (2) C. improvisum and (3) C. villosum as sister species; and (4) C. doriae sister to (5) C. trinitatum trinitatum with (6) C. trinitatum gorgasi sister to these taxa (Fig.
Interspecific genetic distances of the larger COI dataset ranged from 11.3% between C. doriae and C. salvini to 2.5% between C. doriae and C. t. trinitatum (Table
Genetic divergence of cytochrome c oxidase subunit 1 for the big-eyed bat Chiroderma and outgroup taxa Uroderma and Platyrrhinus. Interspecific distances shown in the lower left matrix; intraspecific distances shown in bold in the diagonal.
(1) | (2) | (3) | (4) | (5) | (6) | (7) | (8) | |
---|---|---|---|---|---|---|---|---|
U. bilobatum (1) | – | |||||||
P. incarum (2) | 0.203 | – | ||||||
C. villosum (3) | 0.223 | 0.178 | 0.010 | |||||
C. improvisum (4) | 0.231 | 0.194 | 0.047 | – | ||||
C. t. trinitatum (5) | 0.222 | 0.184 | 0.067 | 0.075 | 0.009 | |||
C. salvini (6) | 0.205 | 0.185 | 0.093 | 0.101 | 0.110 | – | ||
C. t. gorgasi (7) | 0.195 | 0.149 | 0.059 | 0.070 | 0.039 | 0.101 | – | |
C. doriae (8) | 0.213 | 0.173 | 0.066 | 0.077 | 0.025 | 0.113 | 0.039 | 0.002 |
Cranial and body measurements for the six taxa of Chiroderma identified in the molecular analyses are shown in Table
Cranial and body measurements of six taxa of the big-eyed bat Chiroderma. See Material and methods for variable abbreviations.
C. trinitatum gorgasi (N = 11) | C. trinitatum trinitatum (N = 47) | C. villosum (N = 66) | C. salvini (N = 6) | C. doriae (N = 4) | C. improvisum (N = 2) | |
---|---|---|---|---|---|---|
FA | 37.7 (37.0–40.5) | 38.9 (37.1–42.6) | 47.9 (44.6–51.0) | 49.6 (49.3–50.0) | 54 (53.0–55.0) | 58.2 (56.2–60) |
GLS | 21.2 (20.6–21.7) | 21.1 (20.0–22.7) | 24.5 (23.2–25.7) | 26.1 (24.2–26.5) | 28.2 (27.6–28.9) | 29.3 (28.7–29.9) |
CLI | 17.3 (16.3–18.1) | 17.4 (16.1–18.8) | 20.3 (18.7–21.58) | 21.6 (21.5–22.3) | 23.9 (23.1–24.5) | 26.3 (25.3–27.8) |
ZB | 13.0 (12.5–13.5) | 12.9 (11.7–14.2) | 15.5 (14.4–16.7) | 16.2 (15.8–16.7) | 17.84 (17.7–18.1) | 18.75 (18.5–19) |
POW | 5.3 (4.9–5.6) | 5.3 (5.8–5.8) | 5.9 (5.3–6.3) | 6.2 (5.9–6.3) | 6.4 (6.1–6.6) | 6.6 (6.5–6.6) |
IOW | 5.6 (5.2–5.9) | 5.5 (5.0–6.2) | 6.0 (5.5–6.8) | 6.8 (6.1–7.3) | 7.6 (7.1–7.8) | 7.4 (7.4–7.4) |
BCW | 9.4 (8.9–9.8) | 9.6 (9.2–10.4) | 10.7 (10.1–11.5) | 11.21 (11.0–11.5) | 11.9 (11.3–12.1) | 12.0 (11.5–12.5) |
C-M | 7.0 (6.5–7.3) | 7.1 (6.7–7.8) | 8.7 (8.1–9.4) | 9.4 (9.1–9.4) | 10.3 (10.0–11.1) | 11.0 (10.9–11.1) |
M-M | 9.6 (9.2–10.0) | 9.5 (8.7–10.3) | 11.3 (10.3–12.4) | 12.0 (11.5–12.3) | 13.3 (13.0–13.7) | 13.8 (13.6–13.9) |
C-C | 4.7 (4.4–5.0) | 4.6 (4.1–5.0) | 5.8 (5.3–6.3) | 6.1 (6.0–6.2) | 6.5 (6.3–6.8) | 7.4 (7.4–7.4) |
Eigenvalue and loadings for the first and second components in the Principal Component Analysis (PCA) of big-eyed bats Chiroderma. See Material and methods for variable abbreviations.
PC1 | PC2 | |
---|---|---|
Eigenvalue | 1.57 | 0.53 |
% Variance | 91.4 | 3.11 |
IOW | 0.25 | 0.44 |
POW | 0.21 | 0.40 |
C-M | 0.34 | -0.23 |
GSL | 0.31 | -0.05 |
BCW | 0.34 | 0.35 |
CIL | 0.34 | 0.07 |
C-C | 0.36 | -0.23 |
M-M | 0.36 | -0.14 |
ZB | 0.37 | -0.12 |
FA | 0.42 | 0.32 |
All variables had p > 0.05 for Bartlett’s test of homoscedasticity, indicating constant variances (p values: FA = 0.06, GSL = 0.25, IOW = 0.59, POW = 0.3l, BCW = 0.06, CIL = 0.45, ZB = 0.08, M-M = 0.32, C-C = 0.08, and C-M = 0.06). The MANOVA and the ANOVA demonstrated that C. t. trinitatum and C. t. gorgasi are significantly different from the other taxa of Chiroderma (P < 0.001) for all measured variables (Appendix
Although similar in size, C. t. trinitatum has a more robust breadth of the braincase than C. t. gorgasi. Chiroderma t. trinitatum also has an accessory cusp on the second lower premolar, which is absent in C. t. gorgasi (Fig.
Chiroderma gorgasi Handley, 1960:464
Chiroderma trinitatum gorgasi Barriga-Bonilla, 1965:246
Holotype. – USNM 309903 (Field number COH 5436), adult male with skin, skull and partial skeleton. Collected on March 6, 1959, by C. O. Handley, Jr, and B. R. Feinstein in Tacarcuna Village (8°05'N, 77°17'W), 3200 feet [975 meters], Río Pucro, Darién, Panama.
Chiroderma gorgasi is distributed west of the Andes in northwestern Ecuador (
Geographic distribution of Chiroderma gorgasi (▲) and C. trinitatum (●) localities analyzed in our study (See Appendix
Chiroderma gorgasi is a small species of Chiroderma (FA 37.0–40.5; GLS 20.2–22.5) that is similar in size to C. trinitatum (sensu stricto) (Table
Chiroderma gorgasi is morphologically very similar to C. trinitatum. Both species have a small cranial and body size for the genus (Table
ANOVA comparing Chiroderma trinitatum trinitatum to C. doriae, C. improvisum, C. villosum, C. salvini, and C. trinitatum gorgasi. * indicates significantly distinct variables (p ≤ 5%).
Variables | C. doriae | C. improvisum | C. villosum | C. salvini | C. t. gorgasi |
---|---|---|---|---|---|
GSL | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | 0.1541 |
CI | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | 0.4423 |
ZB | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | 0.3094 |
POW | < 2.2e-16* | 1.373e-06* | < 2.2e-16* | 1.061e-12* | 0.6747 |
IOW | < 2.2e-16* | 1.347e-09* | 2.366e-14* | 1.355e-14* | 0.6272 |
BWC | < 2.2e-16* | 2.602e-08* | < 2.2e-16* | < 2.2e-16* | 0.0339* |
M-C | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | 0.5257 |
B-M | < 2.2e-16* | 1.527e-15* | < 2.2e-16* | < 2.2e-16* | 0.1444 |
B-C | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | 0.1251 |
FA | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | < 2.2e-16* | 0.1753 |
Chiroderma gorgasi is easily distinguished from other species of the genus by its smaller cranial and body size (Table
Chiroderma doriae and C. improvisum are the largest species of the genus, and unlike C. gorgasi have a triangular occipital complex in dorsal view, a pointed and developed supraorbital region, a relatively more developed sagittal and lambdoidal crest, and a long nasal aperture. In addition, C. doriae also tends to have a relatively broader braincase than C. gorgasi and the presence of an undeveloped third cusp in the second lower premolar. We were not able to examine specimens of the more recently described C. vizottoi, but it is larger than C. gorgasi and most similar to C. doriae in qualitative craniodental traits.
The only big-eyed bat species occurring in the Caribbean is Chiroderma improvisum, which until recently was known from Guadeloupe (
Chiroderma gorgasi was originally described by
Our morphological review identified the presence of three cusps on the second lower premolar in cis-Andean populations referable to C. trinitatum and two cusps in trans-Andean populations referable to C. gorgasi that also match the taxonomic boundaries of
The overall topology of the Cytb tree proposed by
Although not an overly species-rich genus, biodiversity surveys and molecular analyses are finding new distributional and taxonomic discoveries in Chiroderma. However, there are still large geographic gaps in sampling throughout the Neotropics, such as the Amazon basin in Brazil and northern South America in Colombia and Venezuela. In addition, this has hindered detailed study of the biogeography of the genus and more broadly the evolution of bats in the Neotropics.
GSTG is grateful to Valéria da Cunha Tavares for the valuable assistance during his PhD research. GSTG was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil (CAPES; Code 001). Funding for fieldwork in Nevis was obtained by BKL through a generous contribution from the Collections and Research Fieldwork Fund of the Royal Ontario Museum. DNA sequencing was done by Kristen Choffe in the Laboratory of Molecular Systematics at the ROM.
Tissue samples of Chiroderma used in the cytochrome c oxidase subunit 1 analysis.
Sample ID | Species | GenBank | Country | State/Department |
---|---|---|---|---|
ROM 111114 | Chiroderma doriae | JF448016 | Brazil | Sao Paulo |
ROM 111141 | Chiroderma doriae | JF446371 | Brazil | Sao Paulo |
ROM 111149 | Chiroderma doriae | JF446373 | Brazil | Sao Paulo |
ROM 111163 | Chiroderma doriae | JF446372 | Brazil | Sao Paulo |
Chiroderma villosum | KT236232 | Brazil | Espirito Santo | |
Chiroderma villosum | KT236233 | Brazil | Espirito Santo | |
ROM 105191 | Chiroderma trinitatum | JF448017 | Ecuador | Napo |
ROM 105230 | Chiroderma trinitatum | JF448810 | Ecuador | Napo |
ROM 105243 | Chiroderma trinitatum | JF448806 | Ecuador | Napo |
ROM 105253 | Chiroderma trinitatum | JF448805 | Ecuador | Napo |
ROM 105581 | Chiroderma trinitatum | JF448811 | Ecuador | Napo |
ROM 105685 | Chiroderma trinitatum | JF448807 | Ecuador | Napo |
ROM 105718 | Chiroderma trinitatum | JF448809 | Ecuador | Napo |
ROM 105766 | Chiroderma trinitatum | JF448808 | Ecuador | Napo |
ROM 106342 | Chiroderma trinitatum | JF448812 | Ecuador | Napo |
ROM F40504 | Chiroderma trinitatum | JF448813 | Ecuador | Napo |
ROM 104448 | Chiroderma villosum | JF448818 | Ecuador | Napo |
ROM 104540 | Chiroderma villosum | JF448829 | Ecuador | Napo |
ROM 104541 | Chiroderma villosum | JF448814 | Ecuador | Napo |
ROM 104549 | Chiroderma villosum | JF448828 | Ecuador | Napo |
ROM 105244 | Chiroderma villosum | JF448815 | Ecuador | Napo |
ROM 105254 | Chiroderma villosum | JF448816 | Ecuador | Napo |
ROM 105267 | Chiroderma villosum | JF448826 | Ecuador | Napo |
ROM 105361 | Chiroderma villosum | JF448825 | Ecuador | Napo |
ROM 105540 | Chiroderma villosum | JF448824 | Ecuador | Napo |
ROM 105587 | Chiroderma villosum | JF448830 | Ecuador | Napo |
ROM 105719 | Chiroderma villosum | JF448822 | Ecuador | Napo |
ROM 105720 | Chiroderma villosum | JF448821 | Ecuador | Napo |
ROM 105721 | Chiroderma villosum | JF448820 | Ecuador | Napo |
ROM 105928 | Chiroderma villosum | JF448817 | Ecuador | Napo |
ROM 105968 | Chiroderma villosum | JF448819 | Ecuador | Napo |
ROM F37400 | Chiroderma villosum | JF448827 | Ecuador | Napo |
ROM F37774 | Chiroderma villosum | JF448823 | Ecuador | Napo |
ROM 101245 | Chiroderma villosum | JF446499 | El Salvador | Ahuachapan |
Chiroderma villosum | KU295490 | French Guiana | ||
ROM 99703 | Chiroderma salvini | JF446777 | Guatemala | El Progreso |
ROM 103486 | Chiroderma trinitatum | JF454560 | Guyana | Upper Demerara-Berbice |
ROM 103503 | Chiroderma trinitatum | JF454561 | Guyana | Upper Demerara-Berbice |
ROM 103504 | Chiroderma trinitatum | MN714876 | Guyana | Upper Demerara-Berbice |
ROM 103505 | Chiroderma trinitatum | JF454562 | Guyana | Upper Demerara-Berbice |
ROM 107205 | Chiroderma trinitatum | EF080285 | Guyana | Potaro-Siparuni |
ROM 107419 | Chiroderma trinitatum | EF080286 | Guyana | Potaro-Siparuni |
ROM 107476 | Chiroderma trinitatum | MN714877 | Guyana | Potaro-Siparuni |
ROM 108144 | Chiroderma trinitatum | JF454552 | Guyana | Cuyuni-Mazaruni |
ROM 108244 | Chiroderma trinitatum | JF454559 | Guyana | Cuyuni-Mazaruni |
ROM 108463 | Chiroderma trinitatum | JF454544 | Guyana | Potaro-Siparuni |
ROM 108554 | Chiroderma trinitatum | JF454545 | Guyana | Potaro-Siparuni |
ROM 108587 | Chiroderma trinitatum | JF454555 | Guyana | Potaro-Siparuni |
ROM 108588 | Chiroderma trinitatum | JF454554 | Guyana | Potaro-Siparuni |
ROM 108714 | Chiroderma trinitatum | EF080287 | Guyana | Potaro-Siparuni |
ROM 108763 | Chiroderma trinitatum | MN714878 | Guyana | Potaro-Siparuni |
ROM 108889 | Chiroderma trinitatum | EF080288 | Guyana | Potaro-Siparuni |
ROM 108950 | Chiroderma trinitatum | JF454557 | Guyana | Potaro-Siparuni |
ROM 108993 | Chiroderma trinitatum | JF454556 | Guyana | Potaro-Siparuni |
ROM 109026 | Chiroderma trinitatum | MN714879 | Guyana | Potaro-Siparuni |
ROM 109195 | Chiroderma trinitatum | JF454558 | Guyana | Potaro-Siparuni |
ROM 109271 | Chiroderma trinitatum | JF454553 | Guyana | Potaro-Siparuni |
ROM 109333 | Chiroderma trinitatum | JF454542 | Guyana | Potaro-Siparuni |
ROM 111627 | Chiroderma trinitatum | JF454543 | Guyana | Potaro-Siparuni |
ROM 111809 | Chiroderma trinitatum | JF454547 | Guyana | Potaro-Siparuni |
ROM 111844 | Chiroderma trinitatum | MN714880 | Guyana | Potaro-Siparuni |
ROM 111884 | Chiroderma trinitatum | JF454546 | Guyana | Potaro-Siparuni |
ROM 111946 | Chiroderma trinitatum | JF454548 | Guyana | Potaro-Siparuni |
ROM 115807 | Chiroderma trinitatum | JF454550 | Guyana | Potaro-Siparuni |
ROM 116630 | Chiroderma trinitatum | JF454549 | Guyana | Potaro-Siparuni |
ROM 118996 | Chiroderma trinitatum | JF454551 | Guyana | Upper Takutu-Upper Essequibo |
ROM 121975 | Chiroderma trinitatum | MN714881 | Guyana | Potario-Siparuni |
ROM 125124 | Chiroderma trinitatum | MN714882 | Guyana | Potaro-Siparuni |
ROM 103214 | Chiroderma villosum | JF454584 | Guyana | Upper Takutu-Upper Essequibo |
ROM 103331 | Chiroderma villosum | JF454585 | Guyana | Upper Takutu-Upper Essequibo |
ROM 106644 | Chiroderma villosum | JF454566 | Guyana | Upper Takutu-Upper Essequibo |
ROM 107111 | Chiroderma villosum | EF080290 | Guyana | Potaro-Siparuni |
ROM 107112 | Chiroderma villosum | EF080291 | Guyana | Potaro-Siparuni |
ROM 107394 | Chiroderma villosum | EF080292 | Guyana | Potaro-Siparuni |
ROM 108203 | Chiroderma villosum | JF454565 | Guyana | Cuyuni-Mazaruni |
ROM 108219 | Chiroderma villosum | JF454564 | Guyana | Cuyuni-Mazaruni |
ROM 108764 | Chiroderma villosum | JF454571 | Guyana | Potaro-Siparuni |
ROM 108765 | Chiroderma villosum | JF454570 | Guyana | Potaro-Siparuni |
ROM 108843 | Chiroderma villosum | EF080289 | Guyana | Potaro-Siparuni |
ROM 108998 | Chiroderma villosum | JF454573 | Guyana | Potaro-Siparuni |
ROM 109138 | Chiroderma villosum | JF454572 | Guyana | Potaro-Siparuni |
ROM 109175 | Chiroderma villosum | JF454569 | Guyana | Potaro-Siparuni |
ROM 109221 | Chiroderma villosum | JF454568 | Guyana | Potaro-Siparuni |
ROM 109270 | Chiroderma villosum | JF454567 | Guyana | Potaro-Siparuni |
ROM 109307 | Chiroderma villosum | JF454583 | Guyana | Potaro-Siparuni |
ROM 109308 | Chiroderma villosum | JF454582 | Guyana | Potaro-Siparuni |
ROM 109337 | Chiroderma villosum | JF454581 | Guyana | Potaro-Siparuni |
ROM 111628 | Chiroderma villosum | EF080293 | Guyana | Potaro-Siparuni |
ROM 111629 | Chiroderma villosum | JF459119 | Guyana | Potaro-Siparuni |
ROM 111754 | Chiroderma villosum | JF454580 | Guyana | Potaro-Siparuni |
ROM 111768 | Chiroderma villosum | JF454579 | Guyana | Potaro-Siparuni |
ROM 111769 | Chiroderma villosum | JF454578 | Guyana | Potaro-Siparuni |
ROM 111770 | Chiroderma villosum | JF454577 | Guyana | Potaro-Siparuni |
ROM 111788 | Chiroderma villosum | JF454576 | Guyana | Potaro-Siparuni |
ROM 111836 | Chiroderma villosum | JF454575 | Guyana | Potaro-Siparuni |
ROM 111845 | Chiroderma villosum | JF454574 | Guyana | Potaro-Siparuni |
ROM 119167 | Chiroderma villosum | MN714883 | Guyana | Upper Takutu-Upper Essequibo |
ROM 119230 | Chiroderma villosum | JF454586 | Guyana | Upper Takutu-Upper Essequibo |
ROM 122481 | Chiroderma villosum | MN714884 | Guyana | Potaro-Siparuni |
ROM 98850 | Chiroderma villosum | JF454563 | Guyana | Barima-Waini |
ROM 125179 | Chiroderma villosum | MN714885 | Guyana | East Berbice-Corentyne |
ROM F38952 | Chiroderma villosum | MN714886 | Guyana | Potaro-Siparuni |
ROM 98702 | Uroderma bilobatum | JF435925 | Guyana | Barima-Waini |
ROM 96536 | Chiroderma villosum | JF448018 | Mexico | Campeche |
ROM FN30654 | Chiroderma villosum | JF447242 | Mexico | Campeche |
ROM 104342 | Chiroderma gorgasi | MN714901 | Panama | Darien |
ROM 104352 | Chiroderma villosum | JF447405 | Panama | Darien |
ROM F38210 | Chiroderma villosum | JF447406 | Panama | Darien |
ROM 122084 | Chiroderma trinitatum | MN714887 | Peru | Loreto |
ROM 122137 | Chiroderma trinitatum | MN714888 | Peru | Loreto |
ROM 122149 | Chiroderma trinitatum | MN714889 | Peru | Loreto |
ROM 122165 | Chiroderma villosum | MN714890 | Peru | Loreto |
ROM 122260 | Chiroderma villosum | MN714891 | Peru | Loreto |
ROM 125567 | Chiroderma villosum | MN714892 | Peru | Tumbes |
ROM 126002 | Chiroderma improvisum | MN714893 | Nevis | Saint Thomas Lowland Parish |
ROM 114170 | Chiroderma trinitatum | JF447622 | Suriname | Brokopondo |
ROM 114213 | Chiroderma trinitatum | JF447625 | Suriname | Brokopondo |
ROM 114233 | Chiroderma trinitatum | JF447623 | Suriname | Brokopondo |
ROM 114234 | Chiroderma trinitatum | JF447624 | Suriname | Brokopondo |
ROM 117003 | Chiroderma trinitatum | JF447627 | Suriname | Sipaliwini |
ROM 117003 | Chiroderma trinitatum | MN714894 | Suriname | Sipaliwini |
ROM 117027 | Chiroderma trinitatum | JF447626 | Suriname | Sipaliwini |
ROM 117083 | Chiroderma trinitatum | JF447628 | Suriname | Sipaliwini |
ROM 117376 | Chiroderma trinitatum | EU096695 | Suriname | Sipaliwini |
ROM 117555 | Chiroderma trinitatum | EU096696 | Suriname | Sipaliwini |
ROM 120098 | Chiroderma trinitatum | MN714895 | Suriname | Sipaliwini |
ROM 120168 | Chiroderma trinitatum | HQ545629 | Suriname | Sipaliwini |
ROM 120225 | Chiroderma trinitatum | HQ545678 | Suriname | Sipaliwini |
ROM 120384 | Chiroderma trinitatum | HQ919736 | Suriname | Sipaliwini |
ROM 114212 | Chiroderma villosum | JF447630 | Suriname | Brokopondo |
ROM 114228 | Chiroderma villosum | JF447631 | Suriname | Brokopondo |
ROM 117119 | Chiroderma villosum | JF447629 | Suriname | Sipaliwini |
ROM 117375 | Chiroderma villosum | EU096697 | Suriname | Sipaliwini |
ROM 120226 | Chiroderma villosum | HQ545679 | Suriname | Sipaliwini |
ROM 120239 | Chiroderma villosum | HQ545445 | Suriname | Sipaliwini |
ROM 120240 | Chiroderma villosum | HQ545446 | Suriname | Sipaliwini |
ROM 120354 | Chiroderma villosum | MN714896 | Suriname | Sipaliwini |
ROM 120364 | Chiroderma villosum | HQ919717 | Suriname | Sipaliwini |
ROM 121027 | Chiroderma villosum | MN714897 | Suriname | Sipaliwini |
ROM 121117 | Chiroderma villosum | MN714898 | Suriname | Sipaliwini |
ROM 126174 | Chiroderma villosum | MN714899 | Suriname | Para |
ROM 113919 | Platyrrhinus incarum | JF435616 | Suriname | Brokopondo |
ACUNHC 393 | Chiroderma villosum | MN714900 | Venezuela | Amazonas |
Sample ID | Species | GenBank | Country | State/Province |
---|---|---|---|---|
UNESP 16506 | Chiroderma doriae | L28937 | Brazil | Sao Paulo |
TK 16379 | Chiroderma doriae | AY169958 | Brazil | |
TK 15713 | Chiroderma improvisum | L28938 | Montserrat | St. Anthony |
TK 25052 | Chiroderma villosum | DQ312414 | Trinidad | St. George |
FMNH 174652 | Chiroderma villosum | FJ154121 | Peru | Madre de Dios |
TK 17627 | Platyrrhinus helleri | L28940 | Suriname | Marowijne |
TK 25256 | Uroderma bilobatum | L28941 | Trinidad | St. George |
TK 22581 | Chiroderma salvini | L28939 | Panama | Darien |
TK 25211 | Chiroderma trinitatum | DQ312413 | Trinidad | St. George |
ASK 7799 | Chiroderma villosum | JF442196 | Ecuador | Orellana |
ASK 7667 | Chiroderma villosum | JF442139 | Ecuador | Napo |
MN 36375 | Chiroderma villosum | DQ903823 | Brazil | |
SK-Bat-61 | Chiroderma improvisum | JQ915203 | Saint Kitts | |
ROM 104342 | Chiroderma gorgasi | MN714902 | Panama | Darien |
Specimens of Chiroderma examined morphologically. Vouchers examined are arranged alphabetically by species and country. See “Material and Methods” for collection acronyms.
Chiroderma doriae – Brazil: São Paulo - ROM 111163, ROM 111141, ROM 111114, ROM 111149.
Chiroderma improvisum – Montserrat: St. Anthony Parsish – TTU 31403; St. Kitts and Nevis: Barnes Ghaut - ROM 126002.
Chiroderma salvini – El Salvador: Morazan - ROM 83365, ROM 85948, Santa Ana - ROM 101526; Guatemala: El Progreso - ROM 99703; Panama: Darien - ROM 78472, ROM 91194.
Chiroderma trinitatum gorgasi – Colombia: Valle del Cauca - USNM 483763, USNM 483765, Antioquia - USNM 499478, USNM 499476; Panama: Bocas Del Toro – USNM 319498, USNM 335295, Darien - FMNH 128132, ROM 104342, USNM 309901, USNM 309903-holotype, San Blas - USNM 309905.
Chiroderma trinitatum trinitatum – Colombia: Vaupes - ROM 45276, ROM 45278, ROM 45280, ROM 45281, ROM 45284, Putumayo – ROM 63236, ROM 63237, ROM 63238; Ecuador: Napo - ROM 105191, ROM 105243, ROM 105253, ROM 105685, ROM 105766, ROM 106342; Guyana: Cuyuni-Mazaruni - ROM 108144, Demerara-Berbice - ROM 57392, ROM 103486, ROM 103503, Upper, Potaro-Siparuni - ROM 107205, ROM 107419, ROM 107476, ROM 108463, ROM 108554, ROM 108587, ROM 108714, ROM 108763, ROM ROM 108889, ROM 108950, ROM 108993, ROM 109195, ROM 109333, ROM 111627, ROM 111809, ROM 111884, ROM 111946, ROM 115807, ROM 116630; Suriname: Brokopondo - ROM 114170, ROM 114213, ROM 114233, ROM 114234, Sipaliwini - ROM 117027, ROM 117376, ROM 120168, ROM 120225, ROM 120384; Trinidad: Saint Andrew County – AMNH 175325-holotype.
Chiroderma villosum – Bolivia: Carrasco - ROM 78471; Colombia: Choco - ROM 85849, Vaupes - ROM 44952, ROM 44953, ROM 44954, ROM 45243, ROM 45245, ROM 45246, ROM 45247, ROM 45249, ROM 45250, ROM 45251, ROM 45252, ROM 45253, ROM 45254, ROM 45255, ROM 45257; Ecuador: Napo - ROM 104448, ROM 104541, ROM 104549, ROM 105244, ROM 105254, ROM 105361, ROM 105720, ROM 105721); Guyana: Barima-Waini - ROM 98850, Potaro-Siparuni - ROM 107111, ROM 107112, ROM 107394, ROM 108219, ROM 108764, ROM 108843, ROM 108998, ROM 109138, ROM 109175, ROM 109221, ROM 109307, ROM 109308, ROM 109337, ROM 111628, ROM 111629, ROM 111754, ROM 111768, ROM 111769, ROM 111770, ROM 111788, ROM 111836, ROM 111845, ROM 122481, Upper Demerara-Berbice - ROM 60402, ROM 60423, Upper Takutu-Upper Essequibo - ROM 35614, ROM 103214, ROM 106644, ROM 119167, ROM 119230; Panama: Darien - ROM 104352; Suriname: Brokopondo - ROM 114212, Sipaliwini - ROM 117119, ROM 117375, ROM 120226, ROM 120239, ROM 120364, ROM 121027; Trinidad and Tobago: Nariva - ROM 124684, ROM 124691.
Maximum likelihood tree of cytochrome c oxidase subunit 1 gene for big-eyed bats Chiroderma as presented in Fig.
Data type: phylogenetic dendrogram
Maximum parsimony tree of cytochrome c oxidase subunit 1 gene for Chiroderma. Bootstrap percentages show support at each node
Data type: phylogenetic dendrogram
Maximum likelihood tree of cytochrome b gene for Chiroderma. Bootstrap percentages show support at each node
Data type: phylogenetic dendrogram
Maximum parsimony tree of cytochrome b gene for Chiroderma. Bootstrap percentages show support at each node
Data type: phylogenetic dendrogram