Research Article |
Corresponding author: Manfredo Alejandro Turcios-Casco ( manturcios21@gmail.com ) Academic editor: Thomas von Rintelen
© 2020 Manfredo Alejandro Turcios-Casco, Hefer Daniel Ávila-Palma, Richard К. LaVal, Richard D. Stevens, Eduardo Javier Ordoñez-Trejo, José Alejandro Soler-Orellana, Diego Iván Ordoñez-Mazier.
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:
Turcios-Casco MA, Ávila-Palma HD, LaVal RК, Stevens RD, Ordoñez-Trejo EJ, Soler-Orellana JA, Ordoñez-Mazier DI (2020) A systematic revision of the bats (Chiroptera) of Honduras: an updated checklist with corroboration of historical specimens and new records. Zoosystematics and Evolution 96(2): 411-429. https://doi.org/10.3897/zse.96.51059
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During the last century, survey efforts for mammals in Honduras have been few and most distributional and conservation assessments of bats have been based on historical records. Taxonomy of many records has changed. Moreover, a number of supposed Honduran occurrences are based on records from bordering countries without confirmation by a Honduran voucher. Therefore, the list of bats of Honduras lacks precision. Here, we update the number of species in the country, including taxonomic changes not reflected in recent works and new records based on museum specimens. The known number of species for Honduras is 113 with seven expected (Cormura brevirostris, Lampronycteris brachyotis, Mesophylla macconnelli, Molossus coibensis, M. pretiosus, Thyroptera discifera and Trinycteris nicefori), based on records in adjoining countries. We provide a new record for Honduras of Natalus lanatus. We confirm the presence of Cynomops greenhalli and Diaemus youngii and clarify the taxonomic status of Artibeus intermedius, Chiroderma gorgasi, Eumops ferox, Gardnerycteris keenani, Lasiurus frantzii, Myotis pilosatibialis, Molossus and Pteronotus species, and Tonatia bakeri. We recommend a reassessment of the conservation status of the bats of Honduras considering recent changes and that a number of species (e.g. Choeronycteris mexicana) have not been observed since their reports in historical records. This requires an update of the taxonomic identification keys for Honduras. The updated checklist below demonstrates the high biodiversity of Honduran bats but is also an example of how poorly many groups have been studied since they were first recorded in the country.
Artibeus intermedius, Central America, Cynomops greenhalli, Diaemus youngii, Natalus lanatus, taxonomy
Frequent taxonomic changes, molecular vs. morphological methods of delineating species and historical vouchers whose identifications have not been updated, are amongst the factors that affect the number of species known for each country. For this reason, our study aims to update species distributions, species checklists and corroborate museum vouchers for the bats of Honduras.
During the last century, sampling effort in Honduras has been very low and most distributional and conservation assessments of bat species have been based on historical records (
We summarise the history of bat research in Honduras: the description of Ectophylla alba H. Allen, 1892 (see
In response to the uncertain number of bat species in Honduras, we provide an update, including taxonomic proposals not considered by
They also failed to consider
To update the number of bat species in Honduras, we first reviewed the database of GBIF.org (2019). Amongst the approximately 9000 Honduran records of bats deposited in museums over the world, we re-examined certain vouchers that were misidentified and that we could correctly identify, based on cranial and external measurements. These were measured to the nearest 0.01 mm with digital calipers. Measurements followed
We accept the changes of Gardnerycteris Hurtado & Pacheco, 2014 for G. keenani (Handley, 1960) (
Acronyms used for the museums are the following:
Annotated list of species of the species that occur in Honduras, authors and years follow
Emballonuridae Gervais, 1856
Emballonurinae Gervais, 1856
Balantiopteryx Peters, 1867
1. Balantiopteryx io Thomas, 1904
2. Balantiopteryx plicata Peters, 1867
Centronycteris Gray, 1838
3. Centronycteris centralis Thomas, 1912
Diclidurus Wied-Neuwied, 1819
4. Diclidurus albus Wied-Neuwied, 1819
Peropteryx Peters, 1867
5. Peropteryx kappleri Peters, 1867
6. Peropteryx macrotis (Wagner, 1843)
Rhynchonycteris Peters, 1867
7. Rhynchonycteris naso (Wied-Neuwied, 1820)
Saccopteryx Illiger, 1811
8. Saccopteryx bilineata (Temminck, 1838)
9. Saccopteryx leptura (Schreber, 1774)
Phyllostomidae Gray, 1825
Carolliinae Miller, 1924
Carollia Gray, 1838
10. Carollia castanea H. Allen, 1890
11. Carollia perspicillata (Linnaeus, 1758)
12. Carollia sowelli Baker, Solari, & Hoffmann, 2002
13. Carollia subrufa (Hahn, 1905)
Desmodontinae J.A. Wagner, 1840
Desmodus Wied-Neuwied, 1826
14. Desmodus rotundus (E. Geoffroy, 1810)
Diaemus Miller, 1906
15. Diaemus youngii (Jentink, 1893)
Diphylla Spix, 1823
16. Diphylla ecaudata Spix, 1823
Glossophaginae Bonaparte, 1845
Anoura Gray, 1838
17. Anoura geoffroyi Gray, 1838
Choeroniscus Thomas, 1928
18. Choeroniscus godmani (Thomas, 1903)
Choeronycteris Tschudi, 1844
19. Choeronycteris mexicana Tschudi, 1844
Glossophaga E. Geoffroy, 1818
20. Glossophaga commissarisi Gardner, 1962
21. Glossophaga leachii Gray, 1844
22. Glossophaga soricina (Pallas, 1766)
Hylonycteris Thomas, 1903
23. Hylonycteris underwoodi Thomas, 1903
Leptonycteris Lydekker, 1891
24. Leptonycteris yerbabuenae Martínez & Villa-R, 1940
Lichonycteris Thomas, 1895
25. Lichonycteris obscura Thomas, 1895
Glyphonycterinae Baker, Solari, Cirranello & Simmons, 2016
Glyphonycteris Thomas, 1896
26. Glyphonycteris daviesi (Hill, 1964)
27. Glyphonycteris sylvestris Thomas, 1896
Lonchorhininae Gray, 1 866
Lonchorhina Tomes, 1863
28. Lonchorhina aurita Tomes, 1863
Micronycterinae Van Den Bussche, 1992
Micronycteris Gray, 1866
29. Micronycteris hirsuta (Peters, 1869)
30. Micronycteris microtis Miller, 1898
31. Micronycteris minuta (Gervais, 1856)
32. Micronycteris schmidtorum Sanborn, 1935
Phyllostominae Gray, 1825
Chrotopterus Peters, 1865
33. Chrotopterus auritus (Peters, 1856)
Gardnerycteris Hurtado & Pacheco, 2014
34. Gardnerycteris keenani (Handley, 1960)
Lophostoma d’Orbigny, 1836
35. Lophostoma brasiliense Peters, 1866
36. Lophostoma evotis (Davis & Carter, 1978)
37. Lophostoma silvicolum d’Orbigny, 1836
Macrophyllum Gray, 1838
38. Macrophyllum macrophyllum (Schinz, 1821)
Mimon Gray, 1847
39. Mimon cozumelae Goldman, 1914
Phylloderma Peters, 1865
40. Phylloderma stenops Peters, 1865
Phyllostomus Lacépède, 1799
41. Phyllostomus discolor Wagner, 1843
42. Phyllostomus hastatus (Pallas, 1767)
Tonatia Gray, 1827
43. Tonatia bakeri Williams, Willig & Reid, 1995
Trachops Gray, 1847
44. Trachops cirrhosus (Spix, 1823)
Vampyrum Rafinesque, 1815
45. Vampyrum spectrum (Linnaeus, 1758)
Stenodermatinae Gervais, 1856
Artibeus Leach, 1821
46. Artibeus inopinatus Davis & Carter, 1964
47. Artibeus intermedius J.A. Allen, 1897
48. Artibeus jamaicensis Leach, 1821
49. Artibeus lituratus (Olfers, 1818)
Centurio Gray, 1842
50. Centurio senex Gray, 1842
Chiroderma Peters, 1860
51. Chiroderma gorgasi Handley, 1960
52. Chiroderma salvini Dobson, 1878
53. Chiroderma villosum Peters, 1860
Dermanura Gervais, 1856
54. Dermanura azteca K. Andersen, 1906
55. Dermanura phaeotis (Miller, 1902)
56. Dermanura tolteca (Saussure, 1860)
57. Dermanura watsoni Thomas, 1901
Ectophylla H. Allen, 1892
58. Ectophylla alba H. Allen, 1892
Enchisthenes K. Andersen, 1906
59. Enchisthenes hartii (Thomas, 1892)
Platyrrhinus Saussure, 1860
60. Platyrrhinus helleri (Peters, 1866)
Sturnira Gray, 1842
61. Sturnira hondurensis Goodwin, 1940
62. Sturnira parvidens Goldman, 1917
Uroderma Peters, 1865
63. Uroderma convexum Lyon, 1902
64. Uroderma davisi Baker & McDaniel, 1972
65. Uroderma magnirostrum Davis, 1968
Vampyressa Thomas, 1900
66. Vampyressa thyone Thomas, 1909
Vampyriscus Thomas, 1900
67. Vampyriscus nymphaea (Thomas, 1909)
Vampyrodes Thomas, 1900
68. Vampyrodes major Allen, 1908
Mormoopidae Saussure, 1860
Mormoops Leach, 1821
69. Mormoops megalophylla (Peters, 1864)
Pteronotus Gray, 1838
70. Pteronotus fulvus (Thomas, 1892)
71. Pteronotus gymnonotus (J.A. Wagner, 1843)
72. Pteronotus mesoamericanus Smith, 1972
73. Pteronotus psilotis (Dobson, 1878)
Noctilionidae G ray, 1821
Noctilio Linnaeus, 1766
74. Noctilio albiventris Desmarest, 1818
75. Noctilio leporinus (Linnaeus, 1758)
Thyropteridae Miller, 1907
Thyroptera Spix, 1823
76. Thyroptera tricolor Spix, 1823
Natalidae Gray, 1866
Natalus Gray, 1838
77. Natalus lanatus Tejedor, 2005
78. Natalus mexicanus Miller, 1902
Molossidae Gervais, 1856
Molossinae Gervais, 1856
Cynomops Thomas, 1920
79. Cynomops greenhalli Goodwin, 1958
80. Cynomops mexicanus (Jones & Genoways, 1967)
Eumops Miller, 1906
81. Eumops auripendulus (Shaw, 1800)
82. Eumops ferox (Gundlach, 1861)
83. Eumops hansae Sanborn, 1932
84. Eumops nanus (Miller, 1900)
85. Eumops underwoodi Goodwin, 1940
Molossus É. Geoffroy, 1805
86. Molossus alvarezi Gonzalez-Ruiz, Ramirez-Pulido & Arroyo-Cabrales, 2011
87. Molossus aztecus Saussure, 1860
88. Molossus bondae J.A. Allen, 1904
89. Molossus molossus (Pallas, 1766)
90. Molossus nigricans Miller, 1902
Nyctinomops Miller, 1902
91. Nyctinomops aurispinosus (Peale, 1848)
92. Nyctinomops laticaudatus (E. Geoffroy, 1805)
93. Nyctinomops macrotis (Gray, 1840)
Promops Gervais, 1855
94. Promops centralis Thomas, 1915
Tadarida Rafinesque, 1814
95. Tadarida brasiliensis (I. Geoffroy, 1824)
Vespertilionidae Gray, 1821
Myotinae Tate, 1942
Myotis Kaup, 1829
96. Myotis albescens (E. Geoffroy, 1806)
97. Myotis elegans Hall, 1962
98. Myotis nigricans (Schinz, 1821)
99. Myotis pilosatibialis LaVal, 1973
100. Myotis riparius Handley, 1960
101. Myotis velifer (J. A. Allen, 1890)
Vespertilioninae Gray, 1821
Bauerus Van Gelder, 1959
102. Bauerus dubiaquercus (Van Gelder, 1959)
Eptesicus Rafinesque, 1820
103. Eptesicus brasiliensis (Desmarest, 1819)
104. Eptesicus furinalis (d’Orbigny, 1847)
105. Eptesicus fuscus (Beauvois, 1796)
Lasiurus Gray, 1831
106. Lasiurus cinereus (Palisot de Beauvois, 1796)
107. Lasiurus ega (Gervais, 1856)
108. Lasiurus egregius (Peters, 1870)
109. Lasiurus frantzii Peters, 1870
110. Lasiurus intermedius H. Allen, 1862
Perimyotis Menu, 1984
111. Perimyotis subflavus (F. Cuvier, 1832)
Rhogeessa H. Allen, 1866
112. Rhogeessa bickhami Baird, Marchan-Rivadeneira, Perez & Baker, 2012
113. Rhogeessa menchuae Baird, Marchan-Rivadeneira, Perez & Baker, 2012
Artibeus Leach, 1821. Recently,
Before
The case of Artibeus (sensu lato) has been controversial and
Balantiopteryx io Thomas, 1904. This species is known from Honduras only by the records of
Centronycteris centralis Thomas, 1912. This species is included by
Chiroderma gorgasi Handley, 1960. The first record of C. gorgasi (
Cynomops Thomas, 1920.
Erroneously, the species that had been previously recognised in Honduras was C. mexicanus [e.g.
Table
Comparison of the new record of C. mexicanus with the record of
Cynomops mexicanus ( |
Cynomops mexicanus by |
Cynomops greenhalli ( |
Cynomops greenhalli by |
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Sex | 1 female | 1 male | 5 females | 1 female | 11 males | 22 females |
FA | 36.71 | 37.05 | 35.08 (33.02–36.3) | 35.7 | 37.41 (35–39.7) | 35.36 (33.40–38.28) |
GLS | 18.90 | 18.78 | 17.02 (15.87–17.57) | 19.3 | 18.41 (17.37–19.23) | 17.12 (15.91–17.82) |
CIL | 17.02 | 19.39 | 16.87 (16.05–17.19) | – | 18.68 (17.92–19.5) | 16.93 (16.06–17.68) |
PB | 4.07 | 4.73 | 4.55 (4.23–4.80) | 4.8 | 4.78 (4.53–5.02) | 4.63 (4.29–4.97) |
ZB | 10.75 | 13.20 | 11.76 (11.32–12.00) | 12.6 | 12.77 (12.06–13.65) | 11.85 (11.23–12.51) |
BB | 7.51 | 9.18 | 8.75 (8.65–8.92) | – | 9.24 (8.68–9.65) | 8.86 (8.20–9.25) |
MB | 8.47 | 13.16 | 11.21 (10.71–11.41) | 12.1 | 12.26 (11.9–13.01) | 11.24 (10.49–11.86) |
MTL | 5.80 | 7.62 | 6.79 (6.38–6.92) | 7.2 | 7.18 (6.79–7.67) | 6.61 (6.22–7.05) |
Diaemus youngii (Jentink, 1893). Amongst the three haematophagous species, D. youngii (Fig.
Eptesicus Rafinesque, 1820. When
E. brasiliensis was not included by
In conclusion, there are only three species of Eptesicus (E. brasiliensis, E. furinalis and E. fuscus Beauvois, 1796) reported for Honduras and, even though
Glyphonycteris Thomas, 1896. We did not find any specimens in GBIF.org (2019) of the genus but both species are included by
Hylonycteris underwoodi Thomas, 1903. The occurrence of H. underwoodi has been debated, because there are no vouchers that can confirm presence in Honduras.
Lasiurus Gray, 1831.
Leptonycteris yerbabuenae Martínez and Villa-R, 1940. We followed
Cranial measurements (in mm) of the two individuals of L. yerbabuenae recorded in 1991 by R. D. Bradley et al. in the department of Valle, southern Honduras (
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Sex | Male | Male | 10 males | 10 females |
GLS | 26.68 | 27.65 | 26.8 (26.0–27.3) | 26.8 (26.4–27.3) |
CIL | 26.14 | 27.04 | – | – |
PB | 5.35 | 5.25 | – | – |
ZB | 10.75 | 11.16 | 11.1 (10.7–11.5) | 10.8 (10.6–10.9) |
BB | 9.66 | 10.39 | – | – |
MB | 10.85 | 11.06 | 10.3 (10.1–10.6) | 10.3 (10.1–10.5) |
MBL | 8.86 | 8.72 | 9.6 (9.2–9.8) | 9.5 (9.0–9.9) |
CCL | 25.09 | 25.69 | – | – |
MDTL | 9.46 | 9.86 | – | – |
Lonchorhina Tomes, 1863, Mimon Gray, 1847, Phylloderma Peters, 1865 and Tonatia Gray, 1827. A seventh locality of L. aurita Tomes, 1863 (
Molossus.
Myotis pilosatibialis LaVal, 1973.
Natalus lanatus Tejedor, 2005 and N. mexicanus Miller, 1902.
We identified the two individuals (
Comparison of N. lanatus specimens that comprise new records for Honduras with individuals captured by
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Individuals mentioned by |
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Sex | M | F | females | males | male | undetermined |
FA | 38 | 40 | 36.8 (35.4–38.6) | 37.0 (35.4–38.3) | 39.0 | 36.5–37 |
Ti | 19 | 17 | 16.5 (15.9–17.3) | 16.8 (15.5–18.4) | – | – |
3mt | 34 | 35 | 32.6 (31.2–33.9) | 33.0 (32.0–33.8) | – | – |
5mt | 36 | 37 | 34.2 (33.2–35.5) | 34.2 (33.2–34.9) | – | – |
E | 15 | 14 | 13.9 (13.0–15.3) | 14.1 (12.0–15.6) | 16.0 | 14.5–14.5 |
GSL | 16.5 | 16.2 | 15.8 (15.3–16.2) | 16.0 (15.4–16.4) | – | – |
ZB | 8.4 | 8.3 | 8.1 (7.9–8.3) | 8.2 (7.8–8.7) | – | – |
BB | 7.9 | 8.0 | 7.7 (7.6–7.9) | 7.9 (7.5–8.2) | – | – |
BAM | 5.7 | 5.5 | 5.4 (5.2–5.5) | 5.4 (5.2–5.6) | – | – |
BAC | 3.9 | 4.2 | 3.5 (3.4–3.6) | 3.6 (3.5–3.8) | – | – |
MTL | 6.9 | 6.7 | 6.5 (6.3–6.8) | 6.7 (6.4–6.9) | – | – |
MBL | 7.0 | 6.8 | 6.9 (6.7–7.2) | 7.1 (6.9–7.4) | – | – |
PB | 3.4 | 3.4 | 3.2 (3.1–3.3) | 3.2 (3.1–3.3) | – | – |
Nyctinomops Miller 1902.
Sturnira Gray, 1842. We re-examined the specimens
Thyroptera Spix, 1823.
Vampyriscus nymphaea (Thomas, 1909).
Map with new records of D. youngii and N. lanatus for Honduras. None of the previous records (except D. youngii) have exact coordinates, however, we shaded the municipality on each department in which they were recorded. The blue shaded area indicates the localities of N. lanatus captured in the municipality of Zamorano (municipality of San Antonio de Oriente) in the department of Francisco Morazán in central Honduras, and in La Cueva del Viejo in the department of La Paz in western Honduras. The big yellow-shaded area refers to two localities in which L. yerbabuenae was recorded in the municipality of Nacaome in the department of Valle in southern Honduras by
Although Honduras is a region in Mesoamerica of high biodiversity (McCranie et al. 2018;
We augmented the most recent bat list of Honduras (
Although there is no voucher of D. youngii from Honduras, we presented external measurements, ecological data and photos of a Honduran specimen, so now all three haematophagous species in America are confirmed for Honduras. This is the only record of D. youngii in Honduras, indicating that more sampling effort is needed to determine the distribution of the species in the country, but based on its frequency of occurrence elsewhere, D. youngii is the rarest of the desmodontinae species.
The following species are based on historical records only; in spite of our substantial effort since the 2000s, we do not know of any recent records (even unofficial) of the following species: C. mexicana, G. keenani, G. daviesi, G. sylvestris, L. yerbabuenae, L. obscura, M. macrophyllum and V. major. We strongly recommend a revision of the threatened species list proposed by
Our acceptance of not dividing Lasiurus into three genera: Lasiurus, Aeorestes and Dasypterus (
The keys for Honduras must be updated using the latest taxonomic arrangements and new records for the country. Furthermore, there are more than 9000 vouchers in different museums all over the world whose identification needs to be verified. More sampling is needed in certain areas of the country, especially in western Honduras (e.g. La Paz, Intibucá) or the most eastern region of the department of Gracias a Dios that borders Nicaragua. A reassessment of the conservation status for many species must be done considering these changes and this is especially true for many species that have not been recorded recently (e.g. M. macrophyllum has not been known since 1969). This updated checklist documents the high biodiversity of Honduran bats and is also an example of how poorly many groups have been studied since first being recorded in the country. We hope to encourage the existing and future generations of researchers to not only report new records and update checklists, but to engage in ecological bat research urgently needed in Honduras.
We are grateful to Gary Shugart for reviewing the Sturnira of the
The following list includes all the specimens examined in this study with their respective localities as were written in the labels:
Artibeus inopinatus (2)
Honduras: Comayagua: La Carbonera (CZB–2019–10); Francisco Morazán: Carboneras (
Chiroderma gorgasi (1)
Honduras: Gracias a Dios: Ciudad Blanca (
Cynomops greenhalli (1)
Honduras: Comayagua: 580 m (
Cynomops mexicanus (1)
Honduras: Atlántida: La Ceiba, S.A.G. Laboratorio (
Eptesicus furinalis (as Eptesicus andinus) (1)
Honduras: Atlántida: La Ceiba, S.A.G. Laboratorio (
Hylonycteris underwoodi (1)
Honduras: Gracias a Dios: Ciudad Blanca (
Leptonycteris yerbabuenae (2)
Honduras: Valle: 1.7 MI S, 8 MI W Nacaome (
Lonchorhina aurita (2)
Honduras: Francisco Morazán: Carboneras (
Mimon cozumelae (1)
Honduras: Colón: Wuarska (
Myotis pilosatibialis (1)
Honduras: Francisco Morazán: 1 km W Talanga (
Natalus lanatus (as Natalus mexicanus) (2)
Honduras: Francisco Morazán: 6 mi N Zamorano (
Natalus mexicanus (1)
Honduras: Copán: 6 km ESE Copan, 900 m (
Sturnira hondurensis (as Sturnira bogotensis) (2)
Honduras: Intibucá: La Esperanza (
Thyroptera tricolor (3)
Honduras: Gracias a Dios: Ciudad Blanca (