Research Article |
Corresponding author: Ricardo Moratelli ( rmoratelli@fiocruz.br ) Academic editor: Wieslaw Bogdanowicz
© 2015 Ricardo Moratelli, Daniela Dias.
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:
Moratelli R, Dias D (2015) A new species of nectar-feeding bat, genus Lonchophylla, from the Caatinga of Brazil (Chiroptera, Phyllostomidae). ZooKeys 514: 73-91. https://doi.org/10.3897/zookeys.514.10013
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We describe Lonchophylla inexpectata sp. n. from the Caatinga of Brazil. This new species can be distinguished from all known species of Lonchophylla that occur in Brazil by dental traits, cranial size, and fur colour. Specimens of L. inexpectata have been misidentified as L. mordax; but L. inexpectata is a pale-venter species, similar in external appearance to L. dekeyseri. We have found L. inexpectata in the Caatinga of North-eastern Brazil; L. mordax along the eastern border of the Caatinga and in the Atlantic Forest–Caatinga ecotone in North-eastern Brazil; and L. dekeyseri in the Cerrado of Mid-western Brazil, in the Brazilian Cerrado–Caatinga ecotone, and as far west as the Cerrado of Bolivia.
Atlantic Forest, Caatinga, Cerrado, Lonchophylla inexpectata, Lonchophylla dekeyseri, Lonchophylla mordax, North-eastern Brazil
Lonchophylla Thomas, 1903 (Phyllostomidae) comprises 12 species of nectar-feeding bats restricted to the Neotropics (
Lonchophylla mordax was described from Lamarão, Bahia (
To test this hypothesis and further understand the geographic distribution of Brazilian species, we examined series of Lonchophylla from localities in the Caatinga, Cerrado, and Atlantic Forest, as well as from transitional zones between these habitats. The material used in our comparisons represents all Lonchophylla species known to occur in Brazil. During this process we found additional features that support our hypothesis that the pale-venter Lonchophylla from the Caatinga represents a new species, which we describe below.
The material we used in the comparisons includes series of Lonchophylla from the Caatinga of NE Brazil (Bahia [municipalities of Andaraí, Barra, Buíque], Ceará, Pernambuco, Piauí, Sergipe [Grota do Angico]); Cerrado of Bolivia (Santa Cruz) and Mid-western Brazil (Distrito Federal, Goiás, Mato Grosso do Sul); Atlantic Forest of SE Brazil (Espírito Santo, Rio de Janeiro); and the Atlantic Forest–Caatinga ecotone in NE Brazil (Bahia [Lamarão], Sergipe [Itabaiana]). This material includes representatives of all currently recognized Brazilian species of Lonchophylla, and includes primary and secondary types of L. bokermanni (6 specimens from the type series), L. dekeyseri (holotype and one paratype), L. mordax (holotype and one paratype), and L. peracchii (holotype and two paratypes). Vouchers are preserved in the American Museum of Natural History (AMNH, New York, USA); Carnegie Museum of Natural History (CM, Pittsburgh, USA); Museu Nacional (MN, Rio de Janeiro, Brazil); Muséum d’histoire naturelle (MHNG, Geneva, Switzerland); Natural History Museum (BM, London, England); Smithsonian’s National Museum of Natural History (USNM, Washington DC, USA); Universidade Estadual Paulista Júlio de Mesquita Filho (DZSJRP, São José do Rio Preto, Brazil); Universidade Federal do Espírito Santo (UFES, Espírito Santo, Brazil); Universidade Federal Rural do Rio de Janeiro (ALP, LMD, Seropédica, Brazil). A complete list of specimens examined is in the Appendix. Most geographical coordinates follow
Measurements in this report are from adults, and are either in millimetres (mm) or grams ([g] body mass). The body mass was recorded from skin labels. Other dimensions include: the forearm length (FA), from the elbow to the distal end of the forearm including carpals, measured with the wing partially folded; greatest length of skull (GLS), from the posteriormost point of the occiput to the tips of the upper inner incisors; condylo-incisive length (CIL), from the line connecting the occipital condyles to the tips of the upper inner incisors; basal length (BAL), from the anterior margin of the foramen magnum to the tips of the upper inner incisors; maxillary toothrow length (MTL), from the anterior surface of the upper canine, including the cingulum, to the posterior surface of M3; molariform toothrow length (M1M3), from the crown of M1 to the crown of M3; breadth across canines (BAC), greatest breadth across outer surface of the crowns of upper canines, including cingulae; breadth across molars (BAM), greatest breadth across outer edges of the crowns of upper molars; postorbital breadth (POB), least breadth across frontals posterior to the postorbital bulges; braincase breadth (BCB), greatest breadth of the globular part of the braincase; mastoid breadth (MAB), greatest breadth across the mastoid region; mandibular length (MAL), from the mandibular symphysis to the condyloid process; and the mandibular toothrow length (MAN), from the anterior crown of the lower canine, including cingulum, to the posterior crown of m3. Craniodental measurements were taken under binocular dissection microscopes with low magnification (usually 6×). Dimensions were taken by only one of us, using digital callipers accurate to 0.02 mm. Measurements were recorded and analysed to the nearest 0.01 mm, but values were rounded off to 0.1 mm throughout the text because this is the smallest unit that allows accurate repeatability with callipers (
Discriminant Function Analysis (DFA) was used to compare taxa. For the analysis, we selected a subset of the cranial dimensions (GLS, CIL, MAB, BCB, POB, BAC, BAM, M1M3, MTL, MAL) to represent different axes of length and width of the skull. As multivariate procedures require complete datasets, missing values (< 3% of the total dataset) were substituted by means. Measurements were transformed to natural logarithms and the covariance matrices were computed considering all variables. DFA was performed in SPSS.
Nomenclature of tooth morphology follows
Lonchophylla mordax:
Lonchophylla mordax:
Lonchophylla mordax:
Lonchophylla dekeyseri:
Lonchophylla mordax:
Lonchophylla dekeyseri:
An adult male, USNM 238008, with skin and skull (Figures
Body mass (g) and external and skull measurements (mm) of the holotype (USNM 238008) of L. inexpectata, and descriptive statistics for L. inexpectata (from Caatinga [type series]), L. dekeyseri (from Cerrado), and L. mordax (from Caatinga and Caatinga–Atlantic Forest ecotone).
L. inexpectata | L. inexpectata | L. dekeyseri | L. mordax | |
---|---|---|---|---|
Holotype | Mean | Mean | Mean | |
USNM 238008 | (Min.–Max.) N | (Min.–Max.) N | (Min.–Max.) N | |
Body mass | – | 8.2 | – | – |
(7.0–9.5) 15 | ||||
FA | 33.7 | 34.6 | 36.9 | 35.8 |
(32.3–36.4) 62 | (35.5–38.0) 15 | (34.5–37.4) 32 | ||
GLS | 22.3 | 23.1 | 22.4*** | 23.6** |
(22.0–23.9) 38 | (22.0–22.7) 16 | (22.6–24.5) 24 | ||
CIL | 20.8 | 21.7 | 21.0*** | 22.2*** |
(20.5–22.6) 37 | (20.4–21.4) 16 | (21.3–23.2) 24 | ||
BAL | 19.1 | 19.8 | 19.1*** | 20.2** |
(18.7–20.7) 36 | (18.5–19.6) 16 | (19.6–20.8) 20 | ||
MTL | 7.6 | 7.8 | 7.6** | 8.0*** |
(7.4–8.2) 45 | (7.3–7.9) 16 | (7.6–8.4) 26 | ||
M1M3 | – | 3.3 | 3.4* | 3.5*** |
(3.1–3.6) 40 | (3.3–3.6) 14 | (3.3–3.7) 30 | ||
BAC | 3.4 | 3.6 | 3.7** | 3.7* |
(3.3–3.8) 44 | (3.4–3.9) 16 | (3.5–4.1) 27 | ||
BAM | 4.8 | 5.1 | 5.1 | 5.3* |
(4.8–5.5) 43 | (4.9–5.3) 16 | (4.7–5.7) 26 | ||
POB | 4.1 | 4.3 | 4.5*** | 4.3 |
(4.1–4.7) 46 | (4.2–4.6) 16 | (4.0–4.6) 27 | ||
BCB | 7.9 | 8.3 | 8.4* | 8.5 |
(7.9–8.6) 46 | (8.0–8.7) 16 | (8.1–8.9) 27 | ||
MAB | 8.5 | 9.0 | 9.1*** | 9.3* |
(8.5–9.6) 44 | (8.8–9.4) 16 | (8.9–9.7) 27 | ||
MAL | 14.9 | 15.6 | 15.1*** | 16.1*** |
(14.1–16.3) 44 | (14.8–15.4) 16 | (15.5–17.0) 25 | ||
MAN | 8.0 | 8.2 | 8.1* | 8.4*** |
(7.8–8.5) 43 | (7.7–8.4) 16 | (7.9–8.9) 25 |
The paratype series comprises 46 vouchers. Three paratypes are from the type locality in Barra, Bahia (AMNH 235608, FMNH 21077, 21078), and were collected by R. H. Becker in 1914. One is from Serra do Catimbau, Buíque, Pernambuco (FMNH 137414; 08°37'S, 37°09'W [coordinates for Catimbau National Park]), and was collected by D. Guerra in 1970. Thirty-eight vouchers are from 17 km south of Exu, Pernambuco (CM 99413–99450; 07°41'S, 39°32'W), elevation ca. 480 m, and were collected by M. R. Willig in 1976. Paratypes from Barra (AMNH 235608, FMNH 21077, 21078), and Buíque (FMNH 137414) are in spirits, others are prepared as dry skin.
One additional specimen (ALP 3686) from the Caatinga of Andaraí, Bahia may represent L. inexpectata. The specimen is preserved in spirit, and the dentition is partially worn, preventing its unambiguous identification.
Lonchophylla inexpectata occurs in the Caatinga of North-eastern (NE) Brazil, with confirmed records from Pernambuco (NE), and Bahia (NE) (Figure
Map of part of South America showing the geographic distribution of samples we confirmed as L. inexpectata (black star [type locality] and square), L. dekeyseri (circles), and L. mordax (white star [type locality] and triangles). Localities 1, 2, 5 are in the Caatinga; localities 3, 4 are in the Caatinga–Atlantic Forest ecotone; and localities 6–8 are in the Cerrado.
Lonchophylla inexpectata can be distinguished from all South American species that occur east of the Andes by the following set of traits: presence of a lingual cusp in the P4, absence of a lingual cusp in the P3, absence of a deep longitudinal groove in the posterior face of the upper canine, proximal portion of the dorsal surface of the forearm not furred, and ventral fur pale.
Like other Lonchophylla, the dental formula of L. inexpectata is 2/2, 1/1, 2/3, 3/3 = 34. Lonchophylla inexpectata, L. dekeyseri and L. bokermanni are the three pale-venter Brazilian species of the genus, whereas L. mordax and L. peracchii have pale-brown ventral pelage. We did not find evidence of L. bokermanni and L. peracchii in sympatry with L. inexpectata—L. bokermanni is restricted to a small area in the Serra do Espinhaço, Cerrado of Minas Gerais; and L. peracchii occurs in the Atlantic Forest, from Espírito Santo southward to São Paulo. Lonchophylla inexpectata can be distinguished from these two species by the presence of a well-developed lingual cusp in the P4, with lingual root in the median portion of the tooth; absence of a groove along the anterior surface of the upper canines; and proximal portion of the dorsal surface of the forearm not covered with fur.
Based on the samples we have available, L. inexpectata resembles L. dekeyseri in the pale ventral fur, and L. mordax in the dental morphology. These three species overlap partially in external and cranial size, but in general, cranial measurements for L. inexpectata average significantly larger than those for L. dekeyseri and smaller than those for L. mordax (Table
Lonchophylla mordax has been reported in the literature as a pale-venter species (e.g.,
Lonchophylla inexpectata averages significantly smaller than L. mordax in all cranial dimensions except in POB and BCB (Table
Lonchophylla inexpectata resembles L. dekeyseri in the pelage colour, but these species can be distinguished by qualitative and quantitative cranial characteristics. Lonchophylla inexpectata is significantly larger than L. dekeyseri in all length measurements of skull and rostrum (GLS, CIL, BAL, MTL, M1M3, MAL, MAN), but L. dekeyseri averages slightly larger in those measurements of the width of skull and rostrum (BAC, POB, BCB, MAB), indicating a longer but narrower skull in L. inexpectata (Table
Upper dentition of L. dekeyseri A, C (LDM 3185) and L. mordax B, D (ALP 6149). A, B Moderate inner lobe in the first upper premolar (P3) of L. dekeyseri A contrasting with the lingual lobe of P3 absent or very reduced in L. mordax B (similar condition observed in L. inexpectata) C, D metastyles of M1 and M2 reduced or absent in dekeyseri C contrasting with the metastyles well developed and distinct in L. inexpectata and L. mordax D.
To test the results obtained from the morphological analyses, we performed a discriminant function analysis including samples we confidently assigned to L. dekeyseri (three groups from the Cerrado of Mid-western Brazil), L. inexpectata (two groups from the Caatinga of NE Brazil), and L. mordax (one group from the Caatinga of NE Brazil, and one group from the Atlantic Forest–Caatinga ecotone in NE Brazil). The first two discriminant functions (DF1, DF2) summarized 47% and 40% of the total variation, respectively (Table
Plots of multivariate individual scores in the first two discriminant functions (DF1, DF2). Samples: Lonchophylla dekeyseri (Goiás [black diamonds, N = 12]; Mato Grosso do Sul [black squares, N = 2]; Distrito Federal [black triangles, N = 2]), L. inexpectata (Barra, Bahia [crosses, N = 3]; Exu, Pernambuco [stars, N = 31]), and L. mordax (Itabaiana, Sergipe [white triangles, N = 8]; Grota do Angico, Sergipe [white inverted triangles, N = 12]). Centroid groups are marked with grey asterisks.
Vector correlation coefficients (loadings) between original variables and discriminant functions (DF1, DF2) for samples of L. dekeyseri, L. inexpectata and L. mordax.
DF1 | DF2 | |
---|---|---|
Characters | 46.5% | 40.4% |
GLS | 0.724 | 0.021 |
CIL | 0.706 | -0.130 |
MAB | 0.240 | 0.388 |
BCB | 0.268 | 0.413 |
POB | -0.149 | 0.261 |
BAC | 0.117 | 0.336 |
BAM | 0.413 | 0.193 |
M1M3 | 0.226 | 0.477 |
MTL | 0.523 | 0.151 |
MAL | 0.645 | 0.100 |
The name “inexpectata” is Latin for “unexpected”, in allusion to the unexpected (at least for the authors) new taxonomic status of pale-venter populations of Lonchophylla from the Caatinga of North-eastern Brazil.
1 | Proximal portion of the dorsal surface of the forearm covered with fur; upper canines distinctly grooved along the anterior surface; P4 narrow in occlusal view, with inner lobe reduced and lingual root displaced posteriorly | 2 |
– | Proximal portion of the dorsal surface of the forearm not conspicuously furred; upper canines lacking a groove along the anterior surface; P4 robust, with inner lobe well developed and lingual root in the median portion of the tooth | 3 |
2 | Smaller size; forearm length 37 mm or less; pale-brownish ventral fur; tip of the tragus rounded; parastyles, mesostyles and metastyles of M1 and M2 absent or poorly developed | Lonchophylla peracchii |
– | Larger size; forearm length 39 mm or more; pale-greyish ventral fur; tip of the tragus pointed; parastyles, mesostyles and metastyles of M1 and M2 well developed | Lonchophylla bokermanni |
3 | P3 robust in occlusal view, with lingual lobe varying from small to moderately developed projection; presence of a conspicuous longitudinal groove along the posterior surface of the canine; metastyle of M1 and M2 absent or reduced | Lonchophylla dekeyseri |
– | P3 narrow in occlusal view, usually without inner lobe or with a reduced lobe; absence of a conspicuous longitudinal groove along the posterior surface of the canine; metastyle of M1 and M2 distinct and developed | 4 |
4 | Ventral fur pale-brownish; mandibular length 15.5–17.0 mm | Lonchophylla mordax |
– | Ventral fur whitish or pale-greyish on the throat and abdomen (particularly on the posterior region of the belly); mandibular length 14.1–16.3 mm | Lonchophylla inexpectata |
Historical remarks. Previous assignments of L. inexpectata to L. mordax seem to have originated with
General external appearance, so far as can be judged by skins, exactly as in Glossophaga soricina, except that the colour averages paler. The type is near “cinnamon-brown” above, the bases of the hairs whitish, and “wood-brown” below, but there is some variation in tone, and the darker specimens are quite as dark as the paler examples of Glossophaga obtained at the same place.
Taxonomic remarks. Molecular and morphological analyses have recovered Lonchophylla (sensu
The samples we have available show that L. dekeyseri and L. mordax are in parapatry with L. inexpectata: L. dekeyseri occurs in the Cerrado of Brazil and possibly in the Bolivian savannah (USNM 584472, 584473) and the Cerrado–Caatinga ecotone in NE Brazil (DZSJRP 11459); and L. mordax occurs in the Atlantic Forest–Caatinga ecotone (agreste), and along the eastern border of the Caatinga (sertão). We are not convinced that L. dekeyseri occurs in the Bolivian savannah and in the Cerrado–Caatinga ecotone in NE Brazil. One of the specimens supporting these records was examined a long time ago (DZSJRP 11459), and the other two (USNM 584472, 584473) are distinct from other samples of L. dekeyseri as determined in a previous discriminant function analysis. These specimens are not included in this analysis because we were not able to compare them with samples from other localities. Records previously assigned to L. mordax from N Brazil are based primarily on
After
We thank the following curators and collections staff for loans, information on specimens in their care, for making collections available, or for assistance during museum work: A. L. Peracchi (UFRRJ, Brazil), E. Morielle-Versute (UNESP, Brazil), J. A. de Oliveira (MN, Brazil), J. Wible, S. McLaren (CM, USA), K. Helgen, D. Lunde (NMNH, USA), M. Ruedi (MHNG, Switzerland), N. Simmons, E. Westwig (AMNH, USA), M. Nascimento, and Y. L. R. Leite (UFES, Brazil). R. Portela Miguez (BMNH, England) provided images of the holotype of L. mordax. M. R. Nogueira (UENF, Brazil) provided access to material he collected and assisted us in the morphological analyses. C. Aires (UMC), D. Seripierri, and F. Nascimento (MZUSP) helped us with literature about E. Garbe. A. L. Gardner (USGS Patuxent Wildlife Research Center, USA) revised a previous draft of the manuscript. This work was supported by the Brazilian National Council for Scientific and Technological Development / Science Without Borders Program (CNPq 202612/2012), and the Smithsonian Institution.
Specimens examined. Abbreviations for collections are in “Methods”.
Lonchophylla bokermanni (08): Brazil, Minas Gerais: Diamantina (18°23'S, 43°61'W: MN 79996, MN 79997); Serra do Cipó (19°16'S, 43°36'W: DZSJRP 10342 [paratype], 10347 [holotype], 10408 [paratype], 11410 [paratype], 11411 [paratype], 10412 [paratype; referred in the original description as ZUEC 585]).
Lonchophylla dekeyseri (16): Brazil, Distrito Federal: Parque Nacional de Brasília (15°41'S, 47°59'W: DZSJRP 10099 [holotype]); unknown locality (ALP 6706, 6707). Brazil, Goiás: Mambaí (14°29'S, 46°06'W: LDM 283, 3008, 3065, 3066, 3104, 3169, 3170, 3184, 3185, 3201, 3215, 3270). Brazil, Mato Grosso do Sul: Corumbá (19°61'S, 57°45'W: LDM 2642).
Lonchophylla cf. dekeyseri (3): Bolivia, Santa Cruz: Velasco (13°54'27"S, 60°48'52.92"W: USNM 584472, 584473). Brazil, Piauí: Sete Cidades, Piracuruca (03°56'S, 41°44'W: DZSJRP 11459 [paratype of dekeyseri]).
Lonchophylla inexpectata: Brazil, Bahia (43): Barra (12°42'S, 41°33'W: USNM 238008 [holotype], AMNH 235608, FMNH 21077, 21078 [paratypes]). Brazil, Pernambuco: Buíque, Serra do Catimbau (08°37'S, 37°09'W: FMNH 137414 [paratype]); 17 km south of Exu (07°41'S, 39°32'W: CM 99413–99450).
Lonchophylla cf. inexpectata (1): Brazil, Bahia: Andaraí, unknown locality (ALP 3686).
Lonchophylla mordax (35): Brazil, Bahia: Lamarão (11°45'S, 38°55'W: BM 1903.9.5.34 [holotype], USNM 123392 [paratype]). Brazil, Sergipe: Itabaiana (10°68'S, 37°42'W: ALP 6149, 8769, 8770, 8812–8819); Parque Nacional Grota do Angico (09°65'S, 37°67'W: ALP 9747, 9752, 9755, 9757, 9759, 9761, 9762, 9768, 9769, 10075–10082, 10084–10088).
Lonchophylla peracchii (75): Brazil, Espírito Santo: Sooretama, BR-101, Km 105, Reserva Biológica de Sooretama (19°1'48.97"S, 40°1'8.976” W: UFES 2046, 2047, 2117) Brazil, Rio de Janeiro: Angra dos Reis, Ilha da Gipóia (23°02'S, 44°21'W: LDM 4200, 4423); Angra dos Reis, Ilha Grande (23°10'S, 44°12'W: DZSJRP 15159 [paratype], 15160, 15161, 15162 [holotype], 15163 [paratype], LDM 246, 2090, 3450, 3896, 3897, 4052, 4233, 4533); Cambuci (21°34'S, 41°54'W: LDM 4250, 4253, 4477); Casimiro de Abreu, Morro de São João (22°29'S, 41°58'W: LDM 2219, 2245, 4113, 4222, 4226, 4227); Itaguaí, Ilha de Itacuruçá (23°56'S, 43°53'W: LDM 5085); Mangaratiba, Vale do Rio Sahy (23°55'S, 43°59'W: LDM 5128); Nova Iguaçú, Reserva Biológica do Tinguá (22°39'S, 43°34'W: ALP 6265, 6560, 6561, 6283, 6284, 6556, 6656–6559); Parati (23°19'S, 44°38'W: LDM 996, 997); Rio de Janeiro, Estrada Rio-Santos (23°55'S, 43°16'W: LDM 5008, 5010); Rio de Janeiro, Floresta da Tijuca (22°57'S, 43°24'W: LDM 1064, 1460); Rio de Janeiro, Jardim Botânico (22°58'S, 43°13'W: LDM 875); Rio de Janeiro, Parque Estadual da Pedra Branca (22°52'S, 43°23'W: ALP 5664, 5820, 5860); Rio de Janeiro, Reserva do Grajaú (22°55'S, 43°16'W: ALP 1783–1785, LDM 237, 238, 246–248, 250, 270, 280, 281, 345, 395, 531–533, 1359, 1495–1497, 1499); Rio de Janeiro, Reserva Rio das Pedras (22°59'S, 44°06'W: LDM 1781, 3700); Teresópolis, Parque Nacional da Serra dos Órgãos (22°26'S, 42°59'W: ALP 6482). Brazil, São Paulo: Ubatuba, Picinguaba (23°18'S, 44°53'W: ALP 10242).
Occurrence localities for Bolivian and Brazilian species of Lonchophylla
Data type: Occurrence localities