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Systematics of big-eyed bats, genus Chiroderma Peters, 1860 (Chiroptera: Phyllostomidae)

September 2020
Zootaxa 4846(1):1-93

DOI:10.11646/zootaxa.4846.1.1

Authors:

Guilherme Siniciato Terra Garbino

Universidade Federal de Viçosa (UFV)

Burton K Lim

Royal Ontario Museum

Valeria Da Cunha Tavares

Instituto Tecnologico Vale

We present a revision of the Neotropical bat genus Chiroderma, commonly known as big-eyed bats. Although species of Chiroderma have a wide distribution from western México to southern Brazil, species limits within Chiroderma are not clearly defined, as attested by identification errors in the literature, and there is no comprehensive revision of the genus that includes morphological and molecular data. Our review is based on phylogenetic analyses of two mitochondrial (COI and CYTB) and two nuclear (RAG2 and DBY) genes, coalescence analyses of mitochondrial genes, and morphological analyses including type specimens of all named taxa. We recognize seven species in three clades: the first clade includes (1) C. scopaeum Handley, 1966, endemic to western México and previously considered a subspecies of C. salvini; and (2) C. salvini Dobson, 1878, a taxon associated with montane forests, distributed from México to Bolivia; the second clade includes (3) C. improvisum Baker and Genoways, 1976, endemic to the Lesser Antilles, and (4) C. villosum Peters, 1860, widely distributed on the continental mainland and polytypic, with subspecies C. v. villosum and C. v. jesupi; and the third clade includes (5) the polytypic C. doriae Thomas, 1891, with C. d. doriae distributed in eastern Brazil and Paraguay, and C. d. vizottoi, occurring in northeastern Brazil; (6) C. trinitatum Goodwin, 1958, distributed from Trinidad to Amazonia; and (7) C. gorgasi Handley, 1960, distributed from Honduras to trans-Andean South America, previously considered a subspecies of C. trinitatum.

Adult male Chiroderma trinitatum captured in Santana do Araguaia, Pará, Brazil, in February 2017 (MZUSP 36012). Note the conspicuous facial stripes and ears with whitish margins.

…

Adult female Chiroderma villosum captured in Puerto Maldonado, Madre de Dios, Perú, in August 2016 (ROM F63087). Note the faint facial stripes, the long guard hairs on the head, and the noseleaf with notched tip.

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Bayesian phylogeny obtained from the analysis of cytochrome c oxidase subunit 1 (COI) of Chiroderma. The diagram represents the MCC (Maximum Clade Credibility) tree summarizing 22,501 molecular phylogenies. The vertical dashed line indicates the threshold between the between-species Poisson tree processes (PTP) and the within-species PTP. The triangle base lengths are proportional to the sample size of each clade. The posterior probability values are shown above the corresponding branches.

…

Chiroderma phylogeny obtained from the Bayesian inference analysis of partial sequences of cytochrome c oxidase subunit 1, recombination-activating gene 2, and DEAD box RNA helicase Y. The MCC (Maximum Clade Credibility) tree summarizes 15,002 molecular phylogenies. The pie charts at the nodes show the posterior probability (PP), with the full circle indicating PP = 1.

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Collecting localities of the Chiroderma specimens analyzed in this study. The localities are compiled in the gazetteer (Appendix 1).

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https://doi.org/10.11646/zootaxa.4846.1.1

http://zoobank.org/urn:lsid:zoobank.org:pub:6F6EBF63-5598-416C-8694-14C4A8687693

ZOOTAXA

ISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)

Accepted by P. Velazco: 17 Jul. 2020; published: 7 Sept. 2020

4846

ZOOTAXA

Magnolia Press

Auckland, New Zealand

Zootaxa 4846 (1): 001–093

https://www.mapress.com/j/zt/

Systematics of big-eyed bats, genus Chiroderma Peters, 1860

(Chiroptera: Phyllostomidae)

GUILHERME S. T. GARBINO1*, BURTON K. LIM2 & VALÉRIA DA C. TAVARES1,3

1Pós-graduação, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Avenida

Antônio Carlos 6627, Pampulha, 31270-901, Belo Horizonte, Minas Gerais, Brazil

2Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario M5S 2C6, Canada

�

burtonl@rom.on.ca, https://orcid.org/0000-0002-0884-0421

3Laboratório de Mamíferos, Departamento de Sistemática e Ecologia, CCEN/DSE, Universidade Federal da Paraíba, Campus I,

58059-900 João Pessoa, Paraíba, Brazil.

�

val.c.tavares@gmail.com, http://orcid.org/0000-0003-0966-0139

*Corresponding author.

�

gstgarbino@hotmail.com; http://orcid.org/0000-0003-1701-5930

GARBINO ET AL.

GUILHERME S. T. GARBINO, BURTON K. LIM & VALÉRIA DA C. TAVARES

Systematics of big-eyed bats, genus Chiroderma Peters, 1860 (Chiroptera: Phyllostomidae)

(Zootaxa 4846)

93 pp.; 30 cm.

7 Sept. 2020

ISBN 978-1-77688-040-9 (paperback)

ISBN 978-1-77688-041-6 (Online edition)

FIRST PUBLISHED IN 2020 BY

Magnolia Press

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https://www.mapress.com/j/zt

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ISSN 1175-5326 (Print edition)

ISSN 1175-5334 (Online edition)

Table of Contents

Abstract ...................................................................................................3

Resumen ..................................................................................................3

Resumo ...................................................................................................4

Introduction ................................................................................................4

Materials and methods .......................................................................................6

Results ..................................................................................................10

Discussion ................................................................................................14

Taxonomy ................................................................................................16

Genus Chiroderma Peters, 1860. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

Chiroderma salvini Dobson, 1878 .............................................................................20

Chiroderma scopaeum Handley, 1966 ..........................................................................29

Chiroderma doriae Thomas, 1891 .............................................................................31

C. d. doriae Thomas, 1891 ...................................................................................37

C. d. vizottoi Taddei and Lim, 2010 ............................................................................37

Chiroderma trinitatum Goodwin, 1958 .........................................................................40

Chiroderma gorgasi Handley, 1960 ............................................................................44

Chiroderma improvisum Baker and Genoways, 1976 ..............................................................46

Chiroderma villosum Peters, 1860 .............................................................................48

C. v. villosum Peters, 1860 ...................................................................................54

C. v. jesupi Allen, 1900 ......................................................................................54

Key to the species and subspecies of genus Chiroderma ............................................................58

Acknowledgements .........................................................................................58

Literature cited ............................................................................................59

Appendix ...................................................................................................

Abstract

We present a revision of the Neotropical bat genus Chiroderma, commonly known as big-eyed bats. Although species of

Chiroderma have a wide distribution from western México to southern Brazil, species limits within Chiroderma are not

clearly defined, as attested by identification errors in the literature, and there is no comprehensive revision of the genus

that includes morphological and molecular data. Our review is based on phylogenetic analyses of two mitochondrial (COI

and CYTB) and two nuclear (RAG2 and DBY) genes, coalescence analyses of mitochondrial genes, and morphological

analyses including type specimens of all named taxa. We recognize seven species in three clades: the first clade includes

(1) C. scopaeum Handley, 1966, endemic to western México and previously considered a subspecies of C. salvini; and (2)

C. salvini Dobson, 1878, a taxon associated with montane forests, distributed from México to Bolivia; the second clade

includes (3) C. improvisum Baker and Genoways, 1976, endemic to the Lesser Antilles, and (4) C. villosum Peters, 1860,

widely distributed on the continental mainland and polytypic, with subspecies C. v. villosum and C. v. jesupi; and the third

clade includes (5) the polytypic C. doriae Thomas, 1891, with C. d. doriae distributed in eastern Brazil and Paraguay, and

C. d. vizottoi, occurring in northeastern Brazil; (6) C. trinitatum Goodwin, 1958, distributed from Trinidad to Amazonia;

and (7) C. gorgasi Handley, 1960, distributed from Honduras to trans-Andean South America, previously considered a

subspecies of C. trinitatum.

Key words: Chiroderma gorgasi, Chiroderma scopaeum, species delimitation, taxonomy, Vampyressina

Resumen

Presentamos una revisión del género de murciélagos neotropicales Chiroderma, comúnmente conocidos como murciélagos

de ojos grandes. No obstante la amplia distribución de las especies de Chiroderma, los límites específicos dentro del

género no están claramente definidos, como lo demuestran los errores de identificación que se encuentran en la literatura.

Tampoco existe hasta el presente, una revisión exhaustiva del género basada en datos morfológicos y moleculares.

Nuestra revisión se basa en análisis filogenéticos de dos genes mitocondriales (COI y CYTB) y dos nucleares (RAG2

y DBY), en análisis de coalescencia de genes mitocondriales y en análisis morfológicos que incluyen los holotipos de

todos los taxones nombrados históricamente en el género. Como resultado de nuestra revisión reconocemos siete especies

de Chiroderma agrupados en tres clados: el primer clado incluye (1) C. scopaeum Handley, 1966, especie endémica del

oeste de México, anteriormente fue considerada como una subespecie de C. salvini; (2) C. salvini Dobson, 1878, un taxón

asociado a bosques montanos, distribuida desde México hasta Bolivia; el segundo (3) C. improvisum Baker y Genoways,

GARBINO ET AL.

1976, especie endémica de las Antillas Menores; (4) C. villosum Peters, 1860, especie politípica distribuida en Centro y

Suramérica, con las subespecies C. v. villosum y C. v. jesupi; y el tercer clado incluye (5) la politípica C. doriae Thomas,

1891, con C. d. doriae distribuido en el este de Brasil y Paraguay, y C. d. vizottoi que ocurre en el noreste de Brasil;

(6) C. trinitatum Goodwin, 1958 distribuido en Trinidad y en la Amazonia; y (7) C. gorgasi Handley, 1960, especie

distribuida desde Honduras hacia la región transandina de Suramérica, considerada anteriormente como una subespecie

de C. trinitatum.

Palabras clave: Chiroderma gorgasi, Chiroderma scopaeum, delimitación de especies, taxonomía, Vampyressina

Resumo

Apresentamos uma revisão taxonômica do gênero de morcegos neotropicais Chiroderma, comumente denominados “big-

eyed bats” (morcegos de olhos grandes). Embora as espécies de Chiroderma tenham uma ampla distribuição, ocorrendo

desde o oeste do México ao sudeste do Brasil, a caracterização das mesmas e os limites interespecíficos entre elas não

estavam claramente definidos, como demonstram os erros de identificação que encontramos na literatura. Até o presente,

tampouco havia sido feita uma revisão robusta do gênero, levando em conta dados morfológicos e moleculares. Nossa

revisão baseia-se em análises filogenéticas de dois genes mitocondriais (COI e CYTB) e dois genes nucleares (RAG2 e

DBY), em análises de coalescência dos genes mitocondriais e em análises morfológicas, incluindo os espécimes-tipo de

todos os táxons já nomeados historicamente. Em conclusão, nós reconhecemos sete espécies distribuídas em três clados: o

primeiro clado inclui (1) C. scopaeum Handley, 1966, endêmico a região oeste do México e previamente considerado uma

subespécie de C. salvini; (2) C. salvini Dobson, 1878, um táxon associado a florestas de altitude, com distribuição desde o

México até a Bolivia; o segundo clado inclui (3) C. improvisum Baker e Genoways, 1976, endêmico às Antilhas Menores;

(4) C. villosum Peters, 1860, amplamente distribuído no continente centro e sul americano e politípico, representado pelas

subespécies C. v. villosum e C. v. jesupi; o terceiro clado inclui (5) o táxon politípico C. doriae Thomas, 1891, sendo

que C. d. doriae ocorre no leste brasileiro e no Paraguai e C. d. vizottoi ocorre no nordeste do Brasil; (6) C. trinitatum

Goodwin, 1958, distribuído em Trinidad e na Amazônia; e (7) C. gorgasi Handley, 1960, que ocorre desde Honduras até

a América do sul transandina, considerado anteriormente como uma subespécies de C. trinitatum.

Palavras chave: Chiroderma gorgasi, Chiroderma scopaeum, delimitação de espécies, taxonomia, Vampyressina

Introduction

Species of Chiroderma, commonly known as “big-eyed bats”, are granivorous–frugivorous bats that occur from

western México to southern Brazil, and the Lesser Antilles (Nogueira & Peracchi 2003; Gardner 2008a). Chiro-

derma commonly have two pairs of facial stripes (Figs. 1, 2) and a dorsal stripe, markings shared by most of its

closely related genera (subtribe Vampyressina: Platyrrhinus, Mesophylla, Uroderma, Vampyressa, Vampyriscus and

Vampyrodes—Cirranello et al. 2016). Cranially, species of Chiroderma differ from other Phyllostomidae mainly by

the presence of a conspicuous notch in the region of the nasal bones, which are extremely shortened (Straney 1984).

Chiroderma is further diagnosed by the presence of two upper and two lower molars with the last lower molar large

and bearing five distinct cusps.

Peters (1860) described the genus Chiroderma and species C. villosum as distinct from every other bat known

at the time by having the last molars, lower (m2) and upper (M2), significantly larger than the preceding teeth (m1

and M1). He also mentioned the nasal notch as a nasal fissure extending towards the interorbital region. In a subse-

quent publication, Peters (1866) included Phyllostoma pusillum Wagner, 1843 in Chiroderma, suggesting that the

notch in the nasal region was fused in this adult specimen. Dobson (1878) described two other species for the genus,

Chiroderma salvini and Chiroderma bidens. Thomas (1889), however, considered the nasal notch to be a diagnostic

character of Chiroderma, not an ontogenetic feature as assumed by Peters (1866), and transferred C. bidens and C.

pusillum to the genus Vampyrops, now a junior synonym of Platyrrhinus.

Between 1890 and 1920, three new species of Chiroderma were described: Chiroderma doriae from Brazil

(Thomas 1891), Chiroderma jesupi from Colombia (Allen 1900), and Chiroderma isthmicum from Panamá (Miller

1912). During the second half of the 20th century, four additional forms were described: Chiroderma trinitatus [sic]

from the island of Trinidad (Goodwin 1958), Chiroderma gorgasi from Panamá (Handley 1960), Chiroderma sal-

vini scopaeum from western México (Handley 1966a), and Chiroderma improvisum from the Lesser Antilles (Baker

& Genoways 1976).

FIGURE 1. Adult male Chiroderma trinitatum captured in Santana do Araguaia, Pará, Brazil, in February 2017 (MZUSP

36012). Note the conspicuous facial stripes and ears with whitish margins.

FIGURE 2. Adult female Chiroderma villosum captured in Puerto Maldonado, Madre de Dios, Perú, in August 2016 (ROM

F63087). Note the faint facial stripes, the long guard hairs on the head, and the noseleaf with notched tip.

The following five species of Chiroderma are recognized in most of the recent literature: C. doriae, C. improvi-

sum, C. salvini, C. trinitatum, and C. villosum, including gorgasi, jesupi and scopaeum as subspecies, and isthmicum

as a junior synonym of jesupi (Jones & Carter 1976; Honacki et al. 1982; Koopman 1994; Simmons 2005; Gardner

2008b). Recently, a new species, Chiroderma vizottoi, was described from the Caatinga of Piauí, northeastern Bra-

GARBINO ET AL.

zil, based on morphological characters (Taddei & Lim 2010; Solari et al. 2019), and the subspecies Chiroderma

trinitatum gorgasi was recognized as a full species (Lim et al. 2020).

There are 10 available names in Chiroderma (Table 1), but there are no recent phylogenetic analyses or system-

atic revisions that test the validity of these nominal taxa, or that indicate the existence of unnamed lineages. Previ-

ous descriptions of new taxa of big-eyed bats that included comparisons among the other valid species used only

morphological characters (Handley 1966a; Baker & Genoways 1976; Taddei & Lim 2010). The only studies that

employed DNA nucleotide sequences to estimate the phylogenetic relationships within Chiroderma used sequences

of the mitochondrial gene cytochrome b (Baker et al. 1994), or of the mitochondrial gene cytochrome c oxidase

subunit 1 combined with cytochrome b (Lim et al. 2020).

TABLE 1. Species-group names associated with Chiroderma.

Nomen Type Type locality

doriae Thomas, 1891 BMNH 44.9.2.6aBrazil: Minas Gerais

gorgasi Handley, 1960 USNM 309903 Panamá: Darién, Tacarcuna Village

improvisum Baker and Genoways, 1976 TTU 19900 Guadeloupe: Basse-Terre, Baie-Mahault

isthmicum Miller, 1912 USNM 173834 Panamá: Panamá, Cabima

jesupi Allen, 1900 AMNH 14574 Colombia: Magdalena, Cagualito

salvini Dobson, 1878 BMNH 68.8.16.2 Costa Rica

scopaeum Handley, 1966 USNM 338711 México: Colima, Pueblo Juaréz

trinitatum Goodwin, 1958 AMNH 175325 Trinidad and Tobago: Trinidad, Cumaca

villosum Peters, 1860 ZMB 408bBrazil

vizottoi Taddei and Lim, 2010 DZSJRP 18054 Brazil: Piauí, Teresina

a The skull and mandible have the voucher number BMNH 49.8.16.29.

b Lectotype, selected by Thomas (1891).

In this report, we review the systematics of Chiroderma across its entire distributional range, including speci-

mens representing all of the named taxa. Based on phylogenetic and coalescent analyses of the largest mitochondrial

DNA dataset yet assembled for the genus, complemented by nuclear DNA sequences and morphological analyses,

we define the species limits within the genus and provide a revised taxonomy for Chiroderma.

Materials and methods

Material analyzed. The specimens examined morphologically in this study are deposited in the following collec-

tions: ALP (Adriano Lúcio Peracchi, Universidade Federal Rural do Rio de Janeiro), Seropédica; AMNH (American

Museum of Natural History), New York; BMNH (Natural History Museum), London; CMUFLA (Universidade Fed-

eral de Lavras), Lavras; CMUFS (Universidade Federal de Sergipe), Aracaju; DZSJRP (Departamento de Zoologia

da Universidade Estadual Paulista), São José do Rio Preto; IAvH-M (Instituto Alexander von Humboldt), Villa de

Leyva; LMUSP (Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo), Piracicaba; LSUMZ

(Museum of Natural Science, Louisiana State University), Baton Rouge; MCN-MQ (Museu de Ciências Naturais da

Pontifícia Universidade Católica), Belo Horizonte; MUSM (Museo de Historia Natural de la Universidad Nacional

Mayor de San Marcos), Lima; MZUSP (Museu de Zoologia da Universidade de São Paulo), São Paulo; ROM (Roy-

al Ontario Museum), Toronto; TTU (Museum of Texas Tech University), Lubbock; UFMT (Universidade Federal

de Mato Grosso), Cuiabá; UFPB (Universidade Federal da Paraíba), João Pessoa; UFMG (Universidade Federal de

Minas Gerais), Belo Horizonte; USNM (National Museum of Natural History, Smithsonian Institution), Washington

D.C.; ZMB (Museum für Naturkunde), Berlin; ZUEC (Museu de Zoologia da Universidade Estadual de Campinas),

Campinas; and ZUFMS (Universidade Federal de Mato Grosso do Sul), Campo Grande.

We obtained tissue samples from the following collections: AMNH; CMUFLA; FMNH (Field Museum of

Natural History), Chicago; IDSM (Instituto de Desenvolvimento Sustentável Mamirauá), Tefé; LSUMZ; MPEG

(Museu Paraense Emílio Goeldi), Belém; MSB (Museum of Southwestern Biology, University of New Mexico),

Albuquerque; MZUC (Museo de Zoologia, Universidad de Carabobo), Valencia; MZFC (Museo de Zoología Al-

fonso L. Herrera), México City; ROM; TTU; UFMG; UFPB; and UFES (Universidade Federal do Espírito Santo),

Vitória. The collecting localities of the specimens and their geographical coordinates are compiled in the gazetteer

(Appendix 1).

Tissue samples. We obtained DNA sequences from 252 specimens of Chiroderma representing every known

phenotype of Chiroderma and spanning the entire geographic distribution of the genus (Hall 1981; Gardner 2008a).

The associated tissue collection of the specimens, GenBank accession numbers, and base-pair length are listed in

Table S1 (Appendix 2) and Table 2.

TABLE 2. Specimens of Chiroderma and the outgroup sequenced for the concatenated molecular analyses. The GenBank

accession numbers are given under the columns of each loci. COI = cytochrome c oxidase subunit 1; CYTB = cytochrome

b; RAG2 = recombination activating gene 2; DBY = DEAD box RNA helicase Y.

Taxon Voucher Tissue COI CYTB RAG2 DBY

Chiroderma doriae TTU 99569 TK 64800 MN814079 MN823703 MN814190 MN814199

Chiroderma doriae ROM 111114 or

111149

TK 16379 ―AY169958 ―MN814198

Chiroderma gorgasi ROM 104342 F 38196 MN714901 MN714902 MN814210 ―

Chiroderma improvisum ROM 126002 F 59453 MN714893 ―MN814211 MN814200

Chiroderma improvisum TTU 31403 TK 15713 MN814080 L28938 MN814191 ―

Chiroderma salvini FMNH 174645 BDP 4069 MN814098 MN823704 KM362058 ―

Chiroderma salvini LSUMZ 25470 M 521 MN814104 ―MN814192 MN814202

Chiroderma salvini TTU 62462 TK 34858b MN814083 MN823712 MN814196 ―

Chiroderma salvini TTU 34309 TK 9031 MN814085 MN823708 MN814197 MN814201

Chiroderma scopaeum TTU 109703 TK 148769 MN814082 MN823707 MN814195 ―

Chiroderma scopaeum TTU 110649 TK 148371 MN814081 MN823706 MN814194 ―

Chiroderma trinitatum ROM 120168 F 52956 HQ545629 ―MN814214 MN814204

Chiroderma trinitatum ROM 125124 F 58815 MN714882 ―MN814212 MN814203

Chiroderma villosum ROM 101245 F 35423 JF446499 ―MN814217 MN814206

Chiroderma villosum ROM 105361 F 37690 JF448825 ―MN814216 MN814205

Chiroderma villosum ROM 104352 F 38209 JF447405 ―MN814221 MN814208

Chiroderma villosum ROM 108219 F 43260 JF454564 ―MN814218 MN814207

Chiroderma villosum ROM 120239 F 53027 HQ545445 ―MN814222 MN814209

Vampyressa thyone Not located TK 70533 ―AY157050 AF316493 ―

Vampyriscus bidens Not located TK 55322 ―AY157045 AF316492 ―

Vampyriscus brocki ROM 112094 TK 11496 JF448145 AY157043 ― ―

DNA amplification and sequencing. Genomic DNA was extracted from skeletal muscle or internal organs

stored in ethanol or frozen in liquid nitrogen, using the DNeasy Tissue Kit (QIAGEN, Inc.) following their sug-

gested protocol. Four loci were amplified using the Polymerase Chain Reaction (PCR) method: the mitochondrial

cytochrome c oxidase subunit 1 (COI) and cytochrome b (CYTB), the nuclear exon recombination-activating gene

2 (RAG2), and the chromosome Y-linked intron, DEAD box RNA helicase Y (DBY). Primers used and the PCR

protocols are described in Baker et al. (2000), Clare et al. (2007), Lim et al. (2008), and Lim (2017). For example,

the PCR mix for COI consisted of 8.92 μL of distilled deionized water, 1.25 μL of buffer EH, 0.5 μL of each primer

at a concentration of 10 μM, 0.28 μL of dNTP’s (Invitrogen) at a concentration of 10 mM, 0.05 μL of 1 U Platinum

Taq polimerase (Invitrogen), and 1 μL of standard DNA.

The PCR products were sequenced using 4 μL and a mix of 11 μL composed of 3.5 μL of distilled deionized

water, 1 μL of primers, 2 μL of 5x sequencing buffer 5´ (Applied Biosystems), 0.5 μL of BigDye® v. 3.1 (Applied

Biosystems). The amplification reactions were carried out in a 1-minute cycle at 96 °C followed by 30 cycles of 10

seconds at 96 °C, 5 seconds at 50 °C, 4 minutes at 60 °C, and 5 minutes at 60 °C. The reactions products were puri-

fied using a precipitation protocol of EDTA/NaOAc/Ethanol, and the nucleotides of both strands were sequenced in

an ABI PRISM 3730 Genetic Analyzer® sequencer, using the protocols of Applied Biosystems.

GARBINO ET AL.

Resulting chromatograms were edited and aligned in Sequencher™ v. 4.8 (Gene Codes Corporation, Ann Ar-

bor, Michigan). Genetic distances between pairs of species were calculated for the COI dataset using the Kimura

2-parameter substitution model (Kumar et al. 2016).

Phylogenetic analyses. The best-fit nucleotide substitution models, as well as the best partitioning scheme

were selected using the Bayesian information criterion (BIC) and a greedy search algorithm, as implemented in

PartitionFinder2 (Lanfear et al. 2016).

Phylogenetic analyses were carried out using maximum likelihood and Bayesian inference on three datasets: (1)

a matrix containing the partial sequences of COI for 252 specimens of Chiroderma and 6 specimens of the outgroup

(see Table S1 in Appendix 2), (2) a matrix with concatenated data of four sequenced mitochondrial and nuclear loci

(COI, CYTB, RAG2, and DBY), and (3) a third matrix with concatenated data from three loci (COI, RAG2, and

DBY). We excluded CYTB sequences from the third dataset because several specimens sequenced for the nuclear

loci lacked sequences for this mitochondrial gene, and because CYTB has a similar and linked inheritance mode as

COI. We trimmed out part of the RAG2 and DBY sequences, for the analyses including the three genes, by exclud-

ing regions in which several individuals had missing data after the alignment. After trimming, the length of RAG2

sequences was 840 bp (from the original 876 bp), and DBY was 460 bp (reduced from 484 bp). Length of the COI

fragment was 657 bp.

Bayesian inference analyses were conducted in MrBayes v.3.2.6 (Ronquist et al. 2012). For the three analy-

ses, i.e. the analysis including only COI sequences, the analysis with the three genes, and the analysis with four

genes, we used the partitioning schemes suggested by PartitionFinder2. For the three phylogenetic inferences, two

independent Markov Chain Monte Carlo (MCMC) analyses were run for 30,000,000 generations each, sampling at

every 2,000 generations. We used four independent chains and a burn-in of 25%.

Two phylogenetic analyses using maximum likelihood were conducted in IQ-TREE, as implemented in the

online platform W-IQ-TREE (Nguyen et al. 2014; Trifinopoulos et al. 2016). One analysis included only the COI

dataset, and the other one included the three-gene dataset used in the Bayesian inference (COI, RAG, and DBY).

The partitioning schemes were used in both maximum likelihood analyses (Chernomor et al. 2016). Branch support

estimation was inferred using the ultrafast bootstrap (UFBoot), as implemented in IQ-TREE, using 1,000 replicates

(Hoang et al. 2017).

Delimitation of putative species was based on the COI phylogeny, using the Multi-rate Poisson Tree Process

(mPTP) algorithm, as implemented in Kapli et al. (2017). This coalescence-based species delimitation method uses

rooted, non-ultrametric, gene trees and heuristic algorithms to infer speciation events based on the nucleotide substi-

tution rates (Zhang et al. 2013; Kapli et al. 2017). The tree used in the delimitation test was estimated in MrBayes,

and included only unique haplotypes (155 terminals). To estimate support in the delimitations, we carried out a

MCMC analysis with 1,000,000 generations.

The MrBayes and PartitionFinder2 analyses were carried out in the CIPRES Science Gateway online platform

(Miller et al. 2010). We used the R packages Ape (Paradis et al. 2004) and Phytools (Revell 2012) to plot the con-

catenated cladograms.

Morphological analyses. We have examined 1063 specimens of Chiroderma. External and osteological char-

acters were based on Handley (1966a), Velazco (2005), Tavares (2008), and Tavares et al. (2014). Dental nomen-

clature followed Miller (1907) and Garbino & Tavares (2018a). We took measurements of the skull, dentition, and

external characters with digital calipers (to the nearest 0.01 mm) and calculated descriptive statistics (mean, range,

and standard deviation) for each sample. We also collected information from specimen labels or collection cata-

logues of body mass (in grams), head and body length (TL), foot length (HF), ear length (E), and tibia length, but

these values were used for only descriptive assessments, not for statistical analyses. Statistical analyses were carried

out in SPSS 19 for Windows and in Past3 (Hammer et al. 2001).

The following measurements were taken (Fig. 3):

Forearm length (FA): distance from the distal extremity of the olecranon to the wrist (including carpals), mea-

sured with the wing folded.

Greatest length of skull (GLS): distance from the most caudal point of the occipital region to the most anterior

point of the premaxilla, excluding the upper incisors.

FIGURE 3. Schematic drawing of the cranium of an adult Chiroderma villosum, based on specimen AMNH 235314, showing

the limits of the cranial and dental measurements.

GARBINO ET AL.

Condylo-incisive length (CIL): distance from the most caudal point of the occipital condyle to the labial surface

of upper incisors.

Condyle-canine length (CCL): distance from the most caudal point of the occipital condyle to the labial surface

of upper canines.

Post orbital breadth (PB): least breadth across the frontals, measured posterior to the post-orbital processes.

Braincase breadth (BB): greatest width of braincase, measured above and behind the zygomatic arches, on the

more globular portion of braincase, and excluding the paraoccipital and mastoid processes.

Mastoid breadth (MB): greatest width, measured between the most lateral points of the mastoid processes of

the temporal bone.

Zygomatic breadth (ZB): greatest transverse dimension across zygomatic arches, measured between the most

lateral points of each arch.

Maxillary toothrow length (MTRL): distance from the mesial surface of the upper canine to the distal surface

of the second upper molar.

Distance across upper canines (C-C): distance between the labial surfaces of the upper canines.

Distance across upper first molars (M1-M1): distance between the labial surfaces of the first upper molars.

Distance across upper second molars (M2-M2): distance between the labial surfaces of the second upper mo-

lars.

Dentary length (DENL): distance from the most caudal point of the mandibular condyle to the most anterior

point of the dentary.

Mandibular toothrow length (MANDL): distance from the distal surface of the second lower molar to the mesial

surface of the lower canine.

Distance between coronoid and angular processes (CAL): distance from the most dorsal point of the coronoid

process to the most ventral point of the angular process.

Only adult specimens were used in the morphological analyses. Specimens were classified as “adults” based on

complete fusion of epiphyses on the metacarpals and phalanxes (Pine 1972).

Occurrence of sexual dimorphism in Chiroderma was tested in series of more than five specimens of each sex,

collected at the same locality or nearby localities. We performed principal component analyses (PCA) for each

sample and extracted the PC1. We used t-tests to compare the PC1 values of males and females.

To verify grouping in the morphospace among the specimens of the distinct species of Chiroderma, the lin-

ear measurements were log-transformed and the principal components were extracted from a variance-covariance

matrix. Due to the low number of specimens measured for the C-C variable, that measurement was used only in

descriptive statistics, not in the principal component analyses.

Geographic variation in C. doriae. To investigate a possible correlation between the phenotype of C. doriae

and the abiotic features across the distribution of the species, we extracted 19 climatic variables, related to tempera-

ture and rainfall, from the WorldClim database (Hijmans et al. 2005; https://www.worldclim.org/bioclim). Latitude

was also extracted from the collecting localities of C. doriae and used in the analysis.

The climatic and morphometric variables were log-transformed and two principal component analyses were

done. The first PCA included the 19 climatic variables and the latitude, and the second PCA included the 13 mor-

phometric variables. The first component (PC1) was extracted from both analyses and compared using Pearson’s

correlation.

Results

Analyses of cytochrome c oxidase subunit 1 sequences. We obtained COI sequences of 252 specimens of Chi-

roderma, of which 141 were downloaded from GenBank and 111 were sequenced in this study. Sequence length

varied from 539 to 657 base pairs (bp). The best partitioning scheme for the COI dataset implements a nucleotide

substitution model for each codon position. For the first position the selected model was the K80 + I; for the second

position, the F81 model; and for the third, the GTR + Gamma model. The phylogenetic analyses recovered high

support values for the monophyly of Chiroderma and for the two species of Vampyriscus used as outgroup. Seven

species were suggested by the mPTP species delimitation tests, which coincide with highly-supported nodes of the

phylogenetic analyses (Figs. 4, 5). Phenotypic data overlaid with the results of the molecular analysis also supported

the recognition of seven species in Chiroderma, two of them polytypic. All taxa we recognize here have available

names.

FIGURE 4. Bayesian phylogeny obtained from the analysis of cytochrome c oxidase subunit 1 (COI) of Chiroderma. The dia-

gram represents the MCC (Maximum Clade Credibility) tree summarizing 22,501 molecular phylogenies. The vertical dashed

line indicates the threshold between the between-species Poisson tree processes (PTP) and the within-species PTP. The triangle

base lengths are proportional to the sample size of each clade. The posterior probability values are shown above the correspond-

ing branches.

GARBINO ET AL.

FIGURE 5. Chiroderma phylogeny obtained from the Bayesian inference analysis of partial sequences of cytochrome c oxi-

dase subunit 1, recombination-activating gene 2, and DEAD box RNA helicase Y. The MCC (Maximum Clade Credibility) tree

summarizes 15,002 molecular phylogenies. The pie charts at the nodes show the posterior probability (PP), with the full circle

indicating PP = 1.

The Bayesian Inference (BI) and maximum likelihood (ML) phylogenetic analyses consistently recovered three

clades: salvini and scopaeum; improvisum and villosum; and doriae, gorgasi, and trinitatum. However, in the ML

analysis, branch supports were generally lower, and there was a polytomy at the base of Chiroderma. In addition,

the clade containing salvini and scopaeum was recovered as the sister group to the clade containing improvisum

and villosum, albeit with low support (UFBoot=79%) (Fig. 4, Fig. S2 in Appendix 3). In the BI analysis, the clade

containing salvini and scopaeum was the sister group to the remaining Chiroderma species. Another difference

between the two analyses was that the nodes supporting the salvini and scopaeum lineages were not recovered in

the ML phylogeny, although the node supporting the two putative species was recovered with a high support value

(UFBoot=97%). In the ML analysis improvisum is nested in the villosum clade, but the nodes leading to this topol-

ogy had low support (UFBoot < 75%).

Both BI and ML analyses recovered a highly supported clade (posterior probability or PP=1, UFBoot=97%)

containing individuals of scopaeum and salvini. Within this clade, the BI analyses recovered two haplogroups, one

distributed from western México to Central America, that corresponds to scopaeum and another distributed from

eastern México to South America, that we identify as salvini (Fig. 4). This (salvini + scopaeum) clade is sister to the

group of remaining Chiroderma species, which consists of two clades. One clade (PP=1, UFBoot=96%) contains

two haplogroups, one widely distributed and the other restricted to the Lesser Antilles that correspond to villosum

and improvisum, respectively. The other clade (PP=1, UFBoot=79%) has a trans-Andean haplogroup (sensu Haffer

1967) identified as gorgasi, the sister group of a clade containing two cis-Andean haplogroups, an Amazonian one

identified as trinitatum and one from eastern Brazil and Paraguay identified as doriae. A single individual, identified

based on phenotypic characteristics as Chiroderma vizottoi Taddei and Lim, 2010, was nested in the clade identified

as doriae. The mean genetic distance between pairs of putative species, as defined by the analysis of COI sequences,

varied between 2.5% (between doriae and trinitatum) and 11.6% (between doriae and scopaeum) (Table 3). Within

the putative species, the mean genetic distance varied between 0.2% (improvisum) to 1.2% (villosum) (Table 3).

TABLE 3. Pairwise COI sequence divergence (percentage) among the putative species of Chiroderma. The intraspecific

percentages of genetic distance are presented in bold on the diagonal.

salvini scopaeum doriae trinitatum gorgasi improvisum villosum

salvini 0.39

scopaeum 4.25 0.68

doriae 11.05 11.59 0.49

trinitatum 11.28 11.43 2.52 0.67

gorgasi 10.2 10.54 3.88 3.96 1.04

improvisum 10.06 9.97 6.96 6.73 6.00 0.22

villosum 9.67 9.57 7.38 7.16 6.36 4.19 1.17

Concatenated genetic analyses. The concatenated alignment of three loci had a length of 1957 bp, including

657 bp of COI, 840 bp of RAG2, and 460 bp of DBY. The complete concatenated analysis including four loci had

a length of 3157 bp: 657 bp of COI, 1140 bp of CYTB, 876 bp of RAG2, and 484 bp of DBY. The partitioning

schemes used in each analysis are shown in Table 4.

TABLE 4. Partitioning schemes and substitution models for the two concatenated molecular datasets of Chiroderma. COI

= cytochrome c oxidase subunit 1, CYTB = cytochrome b, RAG2 = recombination-activating gene 2, and DBY = DEAD

box RNA helicase Y.

Dataset (partition number) Partition Model

3 genes (1) COI (position 1), RAG2 (position 2) K80+I

3 genes (2) COI (position 2) F81+I

3 genes (3) COI (position 3) GTR+G

3 genes (4) RAG2 (position 1), RAG2 (position 3) HKY+I

3 genes (5) DBY JC+I

4 genes (1) COI (position 1), CYTB (position 1), RAG2 (position 2) K80+I

4 genes (2) COI (position 2), CYT (position 2) F81

4 genes (3) COI (position 3) GTR+G

4 genes (4) CYTB (position 3) HKY

4 genes (5) RAG2 (position 1), RAG2 (position 3) F81+I

Resulting topologies estimated using the three loci dataset analyzed with BI and ML were similar and generally

agreed with the COI topology, however, the support values for each node were different (Fig. 5, Fig. S3 in Appendix

3). Both analyses recovered the clade containing salvini and scopaeum as the sister group of a clade containing the

other putative species of Chiroderma; however, neither taxon was reciprocally monophyletic. In the BI analysis, the

two sequences of improvisum were nested in the villosum clade, but the node was not strongly supported (PP=0.79)

and formed a trichotomy, whereas the two putative species were reciprocally monophyletic in the ML analysis, with

the villosum node having low support (UFBoot=70%). Contrasting with the COI analysis, the doriae + trinitatum

clade had low support (PP=0.87, UFBoot=76%) in the ML analysis.

GARBINO ET AL.

The BI analysis including the four loci also recovered the three main clades of Chiroderma identified in the

other analyses, i.e., (salvini + scopaeum), (improvisum + villosum) and (doriae + gorgasi + trinitatum) (Fig. S4 in

Appendix 3). However, the relationship among them differed. In the BI analysis, the improvisum + villosum clade

was recovered as the sister group to a low-supported clade (PP=0.64) containing all of the other species. The vil-

losum + improvisum clade also was recovered with low support (PP=0.79) and, as in the three-loci analysis, the two

sequences of improvisum were nested within the villosum clade. The doriae + trinitatum clade had high support

(PP=0.99), however, trinitatum was paraphyletic, with the single specimen of doriae forming a weakly-supported

clade (PP=0.59) with one of the two individuals of trinitatum.

Morphological analyses. Specimen series large enough to verify the presence of sexual dimorphism were ob-

tained for each putative species, except for improvisum. For villosum, we analyzed representative series from Pan-

amá, the Venezuelan Amazon, and southeastern Brazil. In most of the sample, females averaged slightly larger than

males, but the difference was not statistically significant (Appendix 4). The exception was the villosum series from

Venezuela in which the females were significantly larger than males, with no overlap at the 95% level (Appendix

4). However, we found no significant sexual dimorphism in other species or populations of Chiroderma; therefore,

males and females were analyzed together.

FIGURE 6. Dispersion of the first and second principal components (PC1 and PC2) extracted from the variance-covariance ma-

trix of a principal component analysis of 13 cranio-dental measurements of 839 specimens of Chiroderma. The convex polygons

represent the recognized species and subspecies, except for C. improvisum where only two specimens were measured.

We compared measurements of 839 specimens belonging to the seven putative species suggested by the coales-

cent analysis using a PCA based on the 13 morphometric variables described in the Materials and Methods section.

The first component (PC1) accounted for 94.1% of the observed variation, and the second component (PC2) was

responsible for 2%, suggesting that most of the variation is concentrated along the size axis (Table 5). The two

smallest putative species, gorgasi and trinitatum, grouped with wide overlap at the lower extreme of the PC1 axis

(Fig. 6). The two largest putative species, doriae and improvisum, were placed at the higher extremity of the PC1

axis. The results of the principal component analyses carried out between selected pairs of species are discussed in

the “Taxonomy” section together with results of the analyses of discrete phenotypic traits relevant to diagnose each

species discussed in this study.

Discussion

Speciation is a continuous process and depending on the stage of the divergence and the theoretical concept adopted,

distinct numbers of species may be recognized (de Queiroz 2007). Whatever the species concept adopted, most

taxonomists agree that species correspond to distinct evolutionary lineages (Simpson 1961; Wiley 1978; Mayden

1999; de Queiroz 2005). Such lineages can be identified based on, but not restricted to, reciprocal monophyly and

diagnostic morphological and ecological characters (Gutiérrez & Garbino 2018).

TABLE 5. Loadings of the first two principal components (PC1 and PC2) extracted from the analysis of Chiroderma

specimens.

Measurements PC 1 PC 2

GLS 0.249 0.073

CIL 0.279 0.066

CCL 0.283 0.042

PB 0.169 0.173

BB 0.198 0.080

MB 0.222 -0.066

ZB 0.270 0.008

MTRL 0.328 0.159

M1-M1 0.288 0.126

M2-M2 0.282 0.098

MANDL 0.342 0.249

DENL 0.306 0.064

CAL 0.331 -0.912

Therefore, we understand that the coalescence-based “species delimitation” tests useful to identify population

structure, may or may not correspond to speciation processes (Sukumaran & Knowles 2017). In this study, together

with the evidence from molecular phylogenetics data and coalescent methods, species recognition was corroborated

by morphology, ecology, and geographic distribution. As a prelude to the formal taxonomic treatment of the species,

we summarize our logic behind the species we recognize in this study.

Chiroderma doriae is a haplogroup with strong molecular support, corroborated by morphological characters

that clearly distinguishes it from the other species of Chiroderma. C. doriae occurs in sympatry only with the

distantly-related C. villosum (Table 6). Our concept of C. doriae includes vizottoi Taddei & Lim, 2010, a taxon

considered to be endemic to the Caatinga (Carmignotto & Astúa 2017), that we classify here as a subspecies of C.

doriae. We justify subspecific recognition because vizottoi represents a geographically and phenotypically (smaller

and paler-colored) distinct population that is genetically indistinguishable from other C. doriae populations.

TABLE 6. Geographic relationships among the species of Chiroderma.

doriae gorgasi improvisum salvini scopaeum trinitatum villosum

doriae —

gorgasi allopatric —

improvisum allopatric allopatric —

salvini allopatric sympatric allopatric —

scopaeum allopatric allopatric allopatric sympatric —

trinitatum allopatric allopatric allopatric sympatric allopatric —

villosum sympatric sympatric allopatric sympatric sympatric sympatric —

Chiroderma improvisum is the largest species in the genus, easily diagnosed by size, and skull and pelage char-

acters. It is the only Chiroderma occurring in the Lesser Antilles, and consequently it is genetically isolated and does

not occur in sympatry with other congeners (Table 6).

Chiroderma villosum is a strongly supported haplogroup and clearly diagnosable morphologically although it

is the most variable taxon, both individually and geographically. We consider the subspecies C. villosum jesupi as

valid, and representing the haplogroup exclusive to the trans-Andean region. The name isthmicum of Miller (1912)

is a junior synonym of jesupi.

GARBINO ET AL.

The salvini complex

The morphological analyses suggest a species of Chiroderma exclusive to the Pacific versant of western–north-

western México, north of the isthmus of Tehuantepec. The oldest available name for this lineage is scopaeum of

Handley (1966a). The mitochondrial DNA analyses also recovered a haplogroup from western México distinct in

most sequences from individuals from Central and South America we diagnosed morphologically as salvini, partly

corroborating our morphology-based conclusion. However, three specimens, from Guatemala, El Salvador, and

Panamá, had a salvini phenotype but were nested in the western México clade. In the taxonomy section dealing

specifically with scopaeum we discuss the implications of these results, which suggest a paraphyletic salvini if sco-

paeum is recognized as a full species.

Chiroderma salvini comprises a clade containing specimens from Costa Rica, Panamá, Bolivia, Perú, and Ven-

ezuela supported by morphology, geographic distribution, and mitochondrial DNA sequences, that also included

haplotypes of C. scopaeum. The species most similar morphologically to C. salvini is C. villosum, from which it can

be distinguished by larger size and by several qualitative features. It occurs in sympatry with C. gorgasi, C. trinita-

tum, C. v. jesupi, and C. v. villosum, and there is a probable contact zone with C. scopaeum in the state of Veracruz,

eastern México (Table 6).

Chiroderma scopaeum comprises a haplogroup, with specimens from México, Guatemala, El Salvador, and

Panamá having high support values in the phylogenetic analyses. However, the specimens from western México are

morphologically distinct from Central American and eastern Mexican specimens, which we identify as C. salvini.

We consider scopaeum to be a valid species, restricted to western/northwestern México.

The trinitatum complex

The following two species are the smallest in Chiroderma, distinguishable from larger Chiroderma spp. by their

size and qualitative characteristics of the skull and dentition. However, the two species are phenotypically similar

to each other. The molecular phylogenies recovered a cis-Andean haplogroup of small Chiroderma, for which the

applicable name would be trinitatum Goodwin, 1958, as the sister group of C. doriae. However, the sister group of

this clade is a trans-Andean haplogroup of small Chiroderma, for which the oldest name is gorgasi Handley, 1960.

Under the scenario of a paraphyletic C. trinitatum, one option is to synonymize the two small species into the oldest

name, which is C. doriae Thomas, 1891, and recognize three subspecies. C. d. doriae, C. d. trinitatum, and C. d.

gorgasi. However, given the significant phenotypic differences among C. doriae and the other species, we recog-

nize gorgasi and trinitatum as distinct species, bearing in mind that both are not easily diagnosed morphologically,

although there are subtle dental and cranial shape differences (Lim et al. 2020).

Chiroderma gorgasi Handley, 1960 is the name we use for the trans-Andean populations of small Chiroderma.

The name gorgasi has been used as a subspecies of C. trinitatum by some authors (Barriga-Bonilla 1965; Jones &

Carter 1976; Gardner 2008a). The species occurs in sympatry with C. salvini and C. v. jesupi (Table 6).

Chiroderma trinitatum consists of a highly supported haplogroup of small Chiroderma from the cis-Andean

Guiana Shield and Amazon basin. It occurs in sympatry with C. salvini and C. v. villosum (Table 6).

Taxonomy

Family Phyllostomidae Gray, 1825

Subfamily Stenodermatinae Gervais, 1856

Tribe Stenodermatini Gervais, 1856

Subtribe Vampyressina Baker et al. 2016

Genus Chiroderma Peters, 1860

Synonyms:

Chiroderma Peters, 1860: 747. Type-species Chiroderma villosum Peters, 1860, by monotypy.

Mimetops Gray, 1866: 117. Listed in the synonymy of Chiroderma; being a nomen nudum.

Chirodesma Thenius, 1989: 113 (not verified). Incorrect spelling of Chiroderma W. Peters, 1860.

Distribution. Chiroderma is in western, eastern, and southern México, Central America (Guatemala, Belize, Hon-

duras, El Salvador, Nicaragua, Costa Rica, and Panamá), Lesser Antilles (Guadeloupe, Marie-Galante, Monserrat,

Saint Kitts and Nevis), Trinidad and Tobago, and South America (Venezuela, Guyana, Suriname, French Guiana,

Colombia, Ecuador, Perú, Bolivia, Paraguay, and Brazil south to the state of Santa Catarina) (Fig. 7).

FIGURE 7. Collecting localities of the Chiroderma specimens analyzed in this study. The localities are compiled in the gazet-

teer (Appendix 1).

Diagnosis. Chiroderma is a genus of small to large-sized fruit and seed-eating bats (total length of head and

body 50–93 mm, length of forearm 34–58 mm, body mass 11–42 g; Tables 7 and 8). Dorsal fur dense, with long

guard hairs, standing out above the underfur covering the body, and especially conspicuous on the cephalic region.

Dorsal fur varies from buff to dark brown or dark gray; individual hairs with three well-defined bands, with the

middle band always wider and paler than basal and terminal bands. Ventral pelage varies from pale gray to plum-

bous gray. The median dorsal stripe conspicuous or faint; may be absent in some C. villosum. Dorsal stripe begins

at interscapular region and extends to the base of uropatagium. Four facial stripes present in most individuals, and

may be bright and wide or faint and narrow. Tip of the spear of noseleaf may be notched. Horseshoe of noseleaf with

free margins along its entire extension. Ears relatively small and round. Forearm densely furred along the proximal

⅔ of its length. Wing membranes, i.e., propatagium, chiropatagium, plagiopatagium, and uropatagium, are dark and

opaque, except for the pale, translucent membrane between digits II and III of the dactylopatagium. Uropatagium

relatively well-developed, extending posteriorly to the level of the knees; densely furred dorsally along ⅔ of its

length. Plagiopataium inserts at the metatarsus. Tail absent. Calcar shorter than foot.

Skull with a conspicuous notch at the region of the nasal bones, which are extremely reduced (Fig. 8). Orbital

region relatively large; distinct postorbital processes. Frontonasal region relatively straight, in lateral view (neither

concave nor convex; Fig. 8). Hard palate long, extending posteriorly close to glenoid fossa. Basioccipital pits shal-

low or absent. Dental formula: I 2/2, C 1/1, P 2/2, M 2/2. First upper incisors (I1) conic in cross-section, elongated

with simple tips (not bilobed), and more than twice the crown size of the second upper incisors (I2). First upper

premolar (P3) and canine (C) in contact; diastema between P3 and second upper premolar (P4). First and second

GARBINO ET AL.

upper molars (M1 and M2) with approximately the same occlusal area, or M2 with slightly larger area than M1;

M2 triangular in occlusal view, with protocone distally placed and level with centrocrista. Hypocone absent in both

M1 and M2; small hypoconal basin present in M1. With cranium and mandible in occlusion, there is a lateral gap

bordered by the upper canine (C), first upper premolar (P3), and the two lower premolars (p2 and p4; Fig. 9).

FIGURE 8. Dorsal, ventral, and lateral views of skull and lateral view of the mandible of Chiroderma villosum (USNM

408644) from San Juan, Amazonas, Venezuela.

FIGURE 9. Lateral view of skull and mandible in occlusion for A) Chiroderma salvini (ROM 99703), B) Chiroderma sco-

paeum (TTU 110649), C) Chiroderma d. doriae (TTU 99569), D) Chiroderma villosum (USNM 560607), and E) Chiroderma

improvisum (ROM 126002).

Coronoid process of mandible tall, its height approximately level with the tip of lower canine (c). Angular pro-

cess conspicuous, projecting ventro-posteriorly in relation to the horizontal ramus of the mandible. Mandibular con-

dyle relatively high, level with or slightly above tooth row. First lower premolar (p2) close to canine, the two teeth

usually in contact; p2 shorter in height and length than second lower premolar (p4), ranging from approximately ¼

to ⅔ the height of p4. Diastema between p2 and p4. Second lower molar (m2) is the largest mandibular tooth and

approximately twice the mesiodistal length of the first lower molar (m1). Well-developed metaconid, entoconid,

protoconid, and hypoconid in m2. There is a fifth cusp between the hypoconid and entoconid, that we identify as

the hypoconulid, following Garbino & Tavares (2018a). Discrete morphological comparisons among the species of

Chiroderma recognized in this study are summarized in Table 9, and the descriptive statistics of the species is sum-

marized in Tables 7 and 8.

GARBINO ET AL.

TABLE 7. Descriptive statistics (mean, standard deviation, range in parentheses, and sample size) of adult specimens of

Chiroderma salvini, C. scopaeum, C. doriae (including subspecies), C. gorgasi and C. trinitatum. See Materials and Methods

for measure abbreviations and descriptions.

C. salvini C. scopaeum C. d. doriae C. d. vizottoi C. gorgasi C. trinitatum

Body

mass

28.3±2.49

(24–34) 31

23.5±2.98

(19–28) 17

31.3±4.47

(20–42) 51

– 13.3±1.68

(12–19) 11

14.8±2.35

(11–22) 54

TL 75.7±4.31

(66–89) 165

69.8±4.36

(61–80) 30

76.5±7.5

(67–93) 13

– 58.9±3.99

(53–65) 17

58.5±3.84

(50–70) 100

FA 49.53±1.5

(45.5–53) 177

45.2±1

(43.5–46.9) 33

51.8±1.4

(48.5–54.6) 91

47.9±1.37

(45.4–50.2) 14

37.7±0.72

(36.8–39.4) 17

39.1±1.44

(34.4–43) 113

GLS 26.4±0.56

(25.2–28.3) 205

24.4±0.46

(23.6–25.4) 32

27.9±0.53

(26–29.1) 93

25.8±0.42

(25.3–26.8) 13

20.9±0.42

(20.2–21.8) 16

21.4±0.55

(20.1–22.8) 118

CIL 24.7±0.56

(23.2–26.3) 201

22.5±0.46

(21.6–23.3) 31

26.3±0.51

(25–27.5) 92

24.1±0.43

(23.7–25.2) 12

19.2±0.44

(18.4–20.1) 15

19.6±0.56

(18–21.1) 115

CCL 23.7±0.53

(22.4–25.2) 201

21.7±0.45

(20.7–22.4) 32

25.4±0.5

(24.2–26.5) 93

23.2±0.39

(22.7–24.1) 12

18.4±0.45

(17.5–19.4) 15

18.8±0.55

(17.5–20.2) 115

PB 6.2±0.22

(5.6–7) 211

5.9±0.19

(5.5–6.5) 33

6.3±0.17

(5.9–6.7) 94

6±0.18

(5.7–6.3) 12

5.3±0.18

(4.9–5.6) 17

5.3±0.17

(4.8–5.8) 119

BB 11.3±0.29

(10.6–12.2) 205

10.8±0.25

(10.3–11.2) 32

11.9±0.34

(10.7–12.6) 93

11.2±0.22

(10.8–11.4) 12

9.5±0.18

(9.3–10) 16

9.6±0.25

(8.9–10.3) 118

MB 12.7±0.32

(11.7–13.6) 201

11.8±0.27

(11.2–12.5) 32

13.7±0.32

(12.6–14.5) 93

12.7±0.2

(12.4–13.1) 12

10.5±0.18

(10.3–11) 15

10.7±0.28

(10.2–11.6) 118

ZB 16.5±0.44

(15.5–17.6) 194

15.1±0.43

(14–15.8) 32

17.7±0.41

(16.9–18.7) 93

16.3±0.4

(15.7–16.8) 12

13±0.33

(12.4–13.9) 15

13.15±0.44

(11.6–14.3) 115

MTRL 9.6±0.25

(9–10.8) 209

8.6±0.23

(8–9.1) 33

10.3±0.25

(9.8–11.2) 95

9.4±0.24

(9–9.9) 12

7.1±0.23

(6.8–7.6) 16

7.3±0.24

(6.6–7.9) 119

C-C 6.2±0.2

(5.7–6.9) 210

5.5±0.17

(5.2–5.9) 29

6.3±0.19

(5.9–6.7) 35

5.8±0.1

(5.6–6) 9

4.7±0.15

(4.5–5) 16

4.8±0.17

(4.3–5.2) 112

M1-

11.6±0.35

(10.7–12.8) 209

10.4±0.31

(9.8–11) 32

12.5±0.3

(11.9–13.3) 95

11.5±0.35

(10.9–12) 12

9±0.27

(8.6–9.6) 16

9.2±0.33

(8.4–9.9) 119

M2-

12±0.34

(11–13) 209

10.8±0.3

(10.2–11.3) 32

13±0.33

(12.1–13.7) 95

11.9±0.39

(11.3–12.6) 12

9.4±0.28

(8.9–10.1) 16

9.55±0.33

(8.9–10.3) 117

DENL 18.2±0.48

(17–19.5) 210

16.5±0.41

(15.8–17.2) 33

19.4±0.49

(17–20.5) 95

17.9±0.22

(17.5–18.3) 11

13.8±0.35

(13.2–14.5) 17

14±0.43

(13.2–15.2) 120

MAN-

10.5±0.27

(10–11.6) 209

9.38±0.29

(8.6–10) 33

11.2±0.27

(10.1–11.7) 95

10.3±0.23

(9.7–10.8) 12

7.6±0.25

(7.3–8.2) 16

7.8±0.24

(7.3–8.5) 119

CAL 7±0.32

(6–8.2) 207

6.5±0.27

(6–7) 33

8.4±0.32

(7.6–9.2) 95

7.6±0.27

(7.2–8) 12

5.5±0.29

(5–6.1) 16

5.7±0.28

(5.1–6.5) 119

The species of Chiroderma for which the karyotype is known, i.e., C. doriae, C. improvisum, C. salvini, C. trini-

tatum, and C. villosum, have a chromosomal complement of 2n = 26 and FN = 48, a subtelocentric X-chromosome,

and a submetacentric or subtelocentric Y-chromosome (Baker 1967, 1973; Baker & Hsu 1970; Baker & Genoways

1976; Varella-Garcia & Taddei 1985).

Chiroderma salvini Dobson, 1878

Synonyms:

Chiroderma salvini Dobson, 1878: 532; type locality “Costa Rica.”

Chiroderma salvini salvini: Handley, 1966: 297; name combination.

Chiroderma salvini scopaeum Reid and Langtimm, 1993: 300; not Chiroderma salvini scopaeum Handley, 1966.

Type Material. The type of C. salvini (BMNH 68.8.16.2), fixed by original designation, is a fluid-preserved adult

male with skull removed and tongue still attached to the body. The anterior half of the pelage is more faded than

the posterior half. Nevertheless, it is possible to note whitish hairs above the lips and below the eyes. A thin median

dorsal stripe extends from the middle dorsum to the posterior extremity of the lower back (contra Dobson 1878:

532, who considered the stripe to be absent). The cranium and mandible are in good condition with all teeth present.

Some parts of the basicranium, as well as a large part of the palate have attached soft tissue. The I1s have convergent

tips that do not touch each other. The angular processes of the mandible are broken.

The species was named after Osbert Salvin, a British zoologist who edited and organized, with Frederick God-

man, the 40-volume “Biologia Centrali-Americana”. On the type specimen’s skull label, the locality is given as

“Costa Rica”, and to the right it is handwritten “O. Salvin [c]”, suggesting that the collector would indeed be Salvin.

However, this naturalist collected specimens exhaustively in Guatemala and bordering countries, such as Belize

(Godman 1915; Papavero 1973). Enrique Arcé, a Guatemalan field worker trained by Salvin, collected most of the

bird specimens from Costa Rica described by the British zoologist (Salvin 1864; Warren & Harrison 1971; Beolens

et al. 2014). Therefore, we suggest that the type of C. salvini probably was collected by E. Arcé during his work in

Costa Rica.

FIGURE 10. Plate of Chiroderma salvini, from the volume about mammals of the “Biologia Centrali-Americana” (plate iv,

dated 1879—Lyal 2011).

GARBINO ET AL.

In the volume on mammals of the “Biologia Centrali-Americana”, authored by E. Alston (except for a few

pages in the Supplement, authored by O. Thomas) and published between 1879 and 1882 (Lyal 2011), there is a

color plate of C. salvini depicting the species as lacking the medial dorsal stripe (Fig. 10), an error that probably

originated from Dobson (1878) description. Dobson (1880), however, recorded the presence of the stripe in an ad-

ditional specimen of C. salvini from Popayán, Colombia.

Distribution and Habitat. Chiroderma salvini is in eastern and southern México from Veracruz southeastward

through Central America (Guatemala, El Salvador, Honduras, Costa Rica, and Panamá), into South America (north-

ern and western Venezuela, western and northern Colombia, western Ecuador, eastern Perú in the Andean foothills,

and western Bolivia; Fig. 11). The absence of records from Nicaragua may be a sampling artifact, possibly related

to the fact that this country has lower mean elevations than the neighboring countries, and C. salvini is associated

with montane forests.

FIGURE 11. Collecting localities of the analyzed specimens of Chiroderma salvini and C. scopaeum. The locality numbers are

referenced in the gazetteer (Appendix 1).

Records of C. salvini are from humid tropical forests, mainly sub-montane and montane. In Guatemala, El

Salvador, and Honduras, the species also occurs in seasonally dry tropical forests. The distribution of C. salvini is

associated with moderate to high elevations, with records in or close to the Sierra Madre Oriental in México, the

cordilleras of Central America (e.g. Sierra Madre de Chiapas in Guatemala, Cordillera de Talamanca in Panamá

and Costa Rica), and on both slopes of the Andean cordillera in South America (Fig. 11). Among the 39 specimen

localities with precise coordinates, the mean elevation was 1,010 m above sea level (ranging from 73 m to 2,045

m), with 32 localities (82%) above 600 m and 20 (51%) above 1,000 m. In Panamá, C. salvini was more frequently

captured between 600 and 1,500 m (Handley 1966b). In Parque Nacional Braulio Carrillo, Costa Rica, the species

was recorded at 680 m (Timm et al. 1989). In Venezuela C. salvini was captured between 611 and 2,240 m, with

93% of the captures above 1,000 m (Handley 1976). In Parque Nacional de Manú, Peruvian Amazon, the species

was documented between 450 and 1,920 m (Solari et al. 2006). In the Department of Tolima, Colombia, records

of C. salvini are between 1,380 and 2,150 m (Bejarano-Bonilla et al. 2007; Galindo-Espinosa et al. 2010), and in

the Department of Valle del Cauca, C. salvini was captured at elevations from 1,200 to 1,700 m (Mora-Beltrán &

López-Arévalo 2018).

Description and Comparisons. The dorsal pelage of C. salvini varies from pale brown to dark brown. Dorsal

hairs are tricolored, with a narrow (approximately ¼ of hair length) dark brown base, a wide (approximately ½ of

hair length) buff medial band, and a narrow terminal band approximating ¼ of hair length. Basal and terminal bands

are usually the same color. Genal and interocular pairs of facial stripes are always present; conspicuous, wide, and

brilliant-white. Interocular stripes are large, their widths varying between 1 and 4 mm, and entirely white. The me-

dian dorsal stripe is visible in most specimens, not detected in 2 of 174 specimens (1.1% of the sample): one from

Venezuela (USNM 415233) had a faint suggestion of the stripe on the middle dorsum, and another from Honduras

(TTU 12806) had no trace of a stripe. The spear of the noseleaf has a simple tip. The lateral margins of the horseshoe

and the spear are whitish. The base and margins of the ear are yellowish.

The dimensions of the cranium of C. salvini are similar to small C. doriae, large C. scopaeum, and large C.

villosum (Tables 7 and 8). The braincase is globose, conspicuously standing out from the adjacent frontal and nasal

regions. In dorsal view, the nasal notch extends posteriorly to the anterior margin of the orbits (Fig. 12). In lateral

view, the anterior margin of the orbits is even with the distal margin of P4 and mesial margin of M1 (Fig. 13). A

sagittal crest was present in 87.7% (186 of 212) of the specimens we examined. The sagittal crest was weakly de-

veloped in 22 (10.4%) specimens and not detected in four (1.8%). The posterior palatine process was absent in 77%

of the sample (159 of 206 specimens), and was poorly developed when present. With cranium and mandible in oc-

clusion, there is no frontal gap (as in C. improvisum and C. villosum; Fig. 14) but there is a small lateral gap, as in

C. doriae, C. scopaeum, C. gorgasi and C. trinitatum (Fig. 9).

FIGURE 12. Dorsal (A) and ventral (C) views of the skull of Chiroderma salvini (USNM 565812—Costa Rica, Guanacaste),

and dorsal (B) and ventral (D) views of C. scopaeum (USNM 511379—México, Nayarit).

GARBINO ET AL.

FIGURE 13. Skull and mandible, in lateral view, of A) Chiroderma salvini (USNM 565812—Costa Rica, Guanacaste); B) C.

scopaeum (USNM 511379—México, Nayarit).

The I1s converge medially in 97% of the specimens (200 of 206) and the tips may or may not be in contact. Six

specimens (3%) have parallel I1 crowns that lack any contact. The P3 is oval in occlusal outline, differing from the

antero-posteriorly compressed outline of P3 in C. doriae. The P3 contacts C. but not P4.

TABLE 8. Descriptive statistics (mean, standard deviation, range in parentheses, and sample size) of adult specimens of

Chiroderma improvisum and C. villosum (including subspecies). See Materials and Methods for measure abbreviations and

descriptions.

C. improvisum C. v. villosum C. v. jesupi

Body mass 34 23.5±3.26 (13–31) 130 22.7±2.7 (17–30) 36

TL 80, 85 69.16±4.3 (55–80) 165 68.8±3.8 (59–78) 92

FA 56.3, 57.3 46.6±1.87 (41–52.8) 283 44.2±1.41 (40.9–47.7) 103

GLS 28.7, 29.4 24.7±0.61 (23.2–26.6) 278 24±0.5 (22.9–25.3) 110

CIL 27.8, 28.4 22.7±0.63 (21.3–24.5) 271 22.2±0.5 (20.9–23.5) 106

CCL 27, 27.43 21.8±0.63 (20.5–23.6) 274 21.3±0.49 (20.2–22.5) 107

PB 6.5, 6.5 5.9±0.22 (5.3–6.7) 283 5.7±0.18 (5.2–6.2) 112

BB 12.2, 12.5 10.7±0.3 (10–12.3) 277 10.6±0.26 (9.9–11.1) 111

MB 14, 14.1 12±0.33 (11.1–13.4) 277 11.9±0.32 (10.4–12.9) 108

ZB 18.5, 19 15.7±0.49 (14.3–17.4) 271 15.5±0.4 (14.6–16.6) 110

MTRL 10.9, 11.1 8.9±0.29 (8.1–9.8) 283 8.6±0.29 (7.9–9.2) 108

C-C 7.4, 7.4 5.8±0.23 (5.2–6.6) 209 5.8±0.22 (5.3–6.3) 96

M1-M1 13.3, 13.3 10.9±0.43 (9.7–12.5) 281 10.8±0.41 (9.8–12) 108

M2-M2 13.6, 13.9 11.2±0.43 (9.5–12.9) 281 11±0.39 (10–12.2) 107

DENL 21.1, 21.1 16.7±0.52 (15.3–18.4) 282 16.4±0.42 (15.3–17.3) 112

MANDL 11.8, 12.2 9.64±0.32 (8.8–10.8) 280 9.4±0.29 (8.7–10) 110

CAL 9.2, 9.4 6.8±0.32 (5.9–7.9) 280 6.7±0.32 (5.9–7.8) 112

TABLE 9. Morphological comparisons of discrete characters among the species of Chiroderma.

salvini scopaeum doriae trinitatum

Facial stripes bright, conspi-

cuous

bright, conspi-

cuous

bright, conspi-

cuous

bright, conspi-

cuous

Noseleaf simple tip simple tip simple tip simple tip

Nasal notchalong short long short

Hard palatebstraight straight U-shaped straight

I1, tips convergent convergent convergent convergent

c, crown height relative to coronoid process same height shorter shorter shorter

p2, crown height relative to p4 crown between 1⁄4 and

1⁄3

between 1⁄4 and

1⁄3

between 1⁄2 and

2⁄3

between 1⁄2 and

2⁄3

Frontal gapcabsent absent absent absent

Continued

gorgasi improvisum villosum

Facial stripes bright, conspi-

cuous

dark, inconspi-

cuous

dark, inconspicuous

Noseleaf simple tip notched tip notched tip

Nasal notchashort long long

Hard palatebstraight straight palatine process

present

I1, tips convergent convergent usually parallel

c, crown height relative to coronoid process same height shorter same height

p2, crown height relative to p4 crown between 1⁄2 and

2⁄3

between 1⁄4 and

1⁄3

between 1⁄4 and 1⁄3

Frontal gapcabsent present present

along = extends posterior to interorbital region; short = does not reach interorbital region or reaches only its anterior

margin.

bcaudal portion of hard palate.

cgap delimited by I1, c, and i1,2, when skull and mandible are occluded.

The lower canine is pointed and relatively tall, and the tip is approximately the same height as the coronoid

process (as in C. villosum, but differing from C. doriae and C. scopaeum, in which the canines are clearly below the

level of the coronoid; Fig. 13). The crown of p2 is low, approximately ¼ of the crown height of p4, longer mesiodis-

tally than tall, and does not contact p4 (similar to the morphology of C. scopaeum and C. villosum).

Compared with the allopatric C. doriae, C. salvini can be distinguished by its smaller size, globose braincase

(less rounded in doriae), taller lower canines (lower canines in doriae are relatively shorter and below the level of

the coronoid process), and smaller p2 (in doriae the p2 is approximately ⅔ of the height of p4).

Where sympatric, C. salvini can be confused with C. scopaeum and C. villosum. Externally, C. salvini can be

separated from C. villosum by, on average, a longer forearm (Tables 7 and 8); basal and apical bands of dorsal fur

the same color (in villosum the base is usually darker than the tip); presence of wide and conspicuous facial stripes

(narrow, faint, or absent in villosum), and a simple tip on the noseleaf spear with pale lateral margins (notched tip

and noseleaf uniformly brown in villosum). Cranially, C. salvini differs from C. villosum by its relatively longer ros-

trum and shorter nasal notch (in villosum the notch is longer, ending near the level of the post-orbital constriction);

smaller orbits (in villosum the anterior margin of the orbit is even with the P4); post-orbital processes less pointed

than in villosum; posterior palatine process small or absent (in villosum process usually present and conspicuous),

and absence of a frontal gap when cranium and lower jaw are in occlusion (Fig. 14).

Compared with C. scopaeum, C. salvini is larger (Fig. 15, Tables 8 and 10) and externally it differs in pelage

color, usually being darker than scopaeum. The skull of C. salvini is more robust, and the lambdoid-suture region of

C. scopaeum is rounder, as can be seen in dorsal view (Fig. 12). The nasal notch of salvini is longer, usually reach-

GARBINO ET AL.

ing the interorbital region (Fig. 12). Lower canines are relatively taller and more pointed than in scopaeum, and the

medial cingulum of the lower canines is not as well developed as in scopaeum (Fig. 13).

TABLE 10. Loadings of the first and second principal components extracted from the variance-covariance matrix of a

principal component analysis of 13 cranio-dental measurements comparing Chiroderma salvini and C. scopaeum.

Measurements PC 1 PC 2

GLS 0.95 0.02

CIL 0.96 -0.03

CCL 0.96 -0.03

PB 0.58 0.08

BB 0.76 0.06

MB 0.91 0.06

ZB 0.93 0.05

MTRL 0.86 -0.24

M1–M1 0.93 -0.16

M2–M2 0.94 -0.14

MANDL 0.94 -0.18

DENL 0.95 -0.02

CAL 0.70 0.69

Eigenvalues 10.15 0.62

Proportion of variation 78.10% 4.80%

FIGURE 14. Frontal view of skull and mandible in occlusion for A) Chiroderma salvini (ROM 99703), B) Chiroderma sco-

paeum (TTU 110649), C) Chiroderma d. doriae (TTU 99569), D) Chiroderma villosum (USNM 560607), E) Chiroderma

improvisum (ROM 126002).

FIGURE 15. Dispersion of the first and second components, extracted from a principal component analysis of 13 cranio-dental

measurements, representing Chiroderma salvini (circles) and C. scopaeum (squares).

Geographic Variation and Phylogeography. Phylogenetic analyses of 18 sequences did not recover any geo-

graphical structuring from Costa Rica to Bolivia (Fig. 16). Phenotypically, C. salvini is a relatively homogeneous

species across its distribution.

Subspecies. C. salvini is monotypic.

Remarks. We found four published reports in which C. villosum from localities in Perú and Brazil were mis-

identified as C. salvini. The record of C. salvini for the Serra do Divisor, in the Peruvian Amazon (Medina et al.

2015), is here reidentified as C. villosum based on the reported forearm length (45.6 mm) and on a photograph of

the specimen clearly showing a notched tip on the noseleaf and ears lacking pale margins (C. Medina in litt.). We

also reanalyzed the specimens from Porto Velho, Rondônia, (MZUSP 35408) and Aricá, Mato Grosso, (MZUSP

6494) reported by Rocha et al. (2016), and confirmed that they have the diagnostic characters of C. villosum. Also,

the record for the Cerrado of Tocantins (Maas et al. 2018) is recognized here as a C. villosum based on the measure-

ments presented in the article and a photo of the skull (L.A.C. Gomes in litt.).

Natural History. Four genera and five species of plants are documented in the diet of C. salvini in Colombia:

Cecropia telealba (Urticaceae), Ficus insipida, F. cuatrecasana, Poulsenia armata (Moraceae), and Piper phytolac-

cifolium (Piperaceae) (Castaño et al. 2018). In Bolivia, one C. salvini was captured in a mist net set under a Ficus

guaranitica (Aguirre 1994 apud Anderson 1997). In Veracruz, México, individuals were covered in pollen of Pachi-

ra aquatica (Malvaceae) (Hernández-Montero & Sosa 2016). In the Peruvian Amazon, Bravo et al. (2008, 2010)

recorded C. salvini visting “collpas”, which are mineral licks containing clay-rich water that is ingested by the bats.

GARBINO ET AL.

Diurnal roosts used by C. salvini are unknown, but one animal was recorded flying through a lighted tunnel in a gold

mine in Panamá and, in Venezuela specimens, have been captured inside houses (Goldman 1920; Handley 1976).

The following ectoparasites have been recorded in C. salvini in Panamá: Amblyomma sp. n. (Ixodidae), Chir-

nyssoides caparti (Sarcoptidae), Periglischrus iheringi (Spinturnicidae), and Paratrichobius salvini (Streblidae)

(Fairchild et al. 1966; Furman 1966; Wenzel et al. 1966; Lourenço et al. 2013). In Venezuela, Periglischrus iheringi

and Trichobius persimilis (Streblidae) were collected in C. salvini (Herrin & Tipton 1975; Wenzel 1976), and in

México the mites Parichoronyssus lopezi (Macronyssidae), Periglischrus iheringi, and Eudusbabekia vampyrops

(Myiobiidae) were recorded on the species (Colín-Martínez et al. 2017).

FIGURE 16. Phylogenetic relationships of Chiroderma salvini and C. scopaeum based on 24 sequences of the cytochrome c

oxidase subunit 1 gene. Localities in parentheses are detailed in the gazetteer (Appendix 1). This subtree is a detailed version of

the clades named “salvini” and “scopaeum” in figure 4.

The reproductive pattern of C. salvini in Central America is best described as seasonal polyestry, with birth

peaks occurring between March and April, and in August. Based on label information, pregnant females were

recorded in Panamá in January (n=1), February (n=41), March (n=1), and June (n=1), while lactating individuals

were recorded in March (n=5). In Guatemala, a pregnant C. salvini was recorded in January (Carter et al. 1966). In

Honduras, pregnant or lactating C. salvini have been found in July and August (LaVal 1969).

In South American populations, the scarcity of data does not permit generalizations. Based on the information

we obtained from specimen labels, pregnant females have been recorded in Venezuela in July (n=2), August (n=1),

and November (n=1), and in the Colombian Pacific there is a record for June (n=1). Based on literature records,

pregnancies in Colombia are known for January, March, April, May, June, October, and December, and there are

records of females that were both pregnant and lactating in March and April (Wilson 1979). In cis-Andean South

America, two pregnant females were recorded from Perú, in August and September, and a lactating C. salvini was

noted in October.

Specimens Examined (N = 216): Bolivia: La Paz, Serrania Bellavista (AMNH 246625); Pando, Santa Rosa

(AMNH 262537, 262538); Santa Cruz, 4.5 km N and 1.5 km E of Cerro Amboro (AMNH 261666); Santa Cruz,

Estancia San Rafael de Amboro (AMNH 261667–261670). Colombia: Quindío, Vereda El Dorado (IAvH-M 7034),

Vereda San Juan d’Carolina (IAvH-M 7036, 7039), Valle del Cauca, Pance (USNM 483743–483746), Río Zabaletas

(USNM 483747–483762). Costa Rica: without precise locality (BMNH 68.8.16.2 [holotype of salvini]); Cartago,

Angostura (USNM 12913/22849), Guanacaste, Rincón de La Vieja (USNM 565812); Heredia, Parque Nacional

Braulio Carrillo (USNM 562856); Puntarenas, Cañas Gordas (AMNH 142484). El Salvador: Santa Ana, Los

Planes (TTU 62461, 62462). Guatemala: El Progreso, Rio Uyús (ROM 99703). Honduras: Francisco Morazán,

16 km by road N Tegucigalpa (TTU 12800–12808), La Flor (AMNH 126210, 126211, 126244–126251, 126253,

126255–126264, 126446, 126448–126455), San Marcos (AMNH 123331), Olancho, 50.4 km by road NNE Juti-

calpa (TTU 12809). México: Veracruz, Las Minas (USNM 329445). Panamá: Bocas del Toro, Río Changena Camp

(USNM 319415–319425, 319499, 319500), Rancho Mojica, Río Changena (USNM 319286), Chiriquí, Cuesta de

Piedra (USNM 331684–331686), Darién, Cana (USNM 179718), Cerro Malí (USNM 338042, 338043), Cerro

Pirre (LSUMZ 25468–25474), Cerro Tacarcuna (USNM 338044), Jaqué (USNM 362919), Tacarcuna Village Camp

(USNM 209969, 305387, 309443–309445, 309906, 309908–309910, 309912–309942, 309946–309968, 309972–

309977), Panamá, Cerro Azul (USNM 305388, 323445–323447). Perú: Cajamarca, San Ignacio (MUSM 12637),

Cusco, Consuelo (MUSM 19663–19665, 19667), Comunidad Nativa Tangoshiari (MUSM 13377), Ridge Camp

(USNM 588032), Madre de Dios, Hacienda Amazonia (MUSM 9742, 9751), Quebrada Aguas Calientes (MUSM

16650), Pasco, Palmira (MUSM 10878–10880), Puno, Yanacocha (MUSM 34980), Tumbes, Quebrada Naran-

jos (MUSM 19177). Venezuela: Carabobo, La Copa (USNM 440740–440744), La Vega del Río Santo Domin-

go (USNM 440746), Distrito Federal, Los Venados (USNM 370526, 370527), Hotel Humboldt (USNM 370528,

370530–370532), Miranda, Guatopo Natural Park (USNM 387191), Monagas, Hacienda San Fernando (USNM

415233–415235), San Agustín (USNM 415236, 415237).

Chiroderma scopaeum Handley, 1966

Synonyms:

Chiroderma [sp.]: Anderson, 1960: 7.

Chiroderma salvini scopaeum Handley, 1966a:297; type locality “Pueblo Juárez, Colima, México.”

Type Material. The type of C. salvini scopaeum, by original designation, is specimen USNM 338711, an adult

female collected by Alfred L. Gardner (field number ALG 1565) in Pueblo Juaréz, Mexican state of Colima, on

August 19, 1960. The specimen was previously stored in the University of Arizona collection, under the number

7952. The material consists of a stuffed skin with skull and mandible separated. The skin is in good condition, and

both pairs of facial stripes are visible. The median dorsal stripe is also visible and located immediately posterior to

the nape and extending to the posterior extremity of the animal. The auditory bullae have separated from the skull

and upper inner incisors are missing. The posterior palatine process is absent.

Distribution and Habitat. We consider C. scopaeum to be restricted to México, west of the isthmus of Te-

huantepec (Fig. 11). The species has been recorded in the states of Chihuahua, Sinaloa, Durango, Nayarit, Jalisco,

Colima, México, Morelos, Guerrero, Puebla, Veracruz, and Oaxaca (Anderson 1960; Handley 1966a; Crossin et

al. 1973; Alvarez & Alvarez-Castañeda 1996; Valiente-Banuet et al. 1997). Hall (1981) suggests that C. scopaeum

would occur from western México to northwestern Costa Rica, and based on this distribution Reid & Langtimm

(1993) identified specimen USNM 565812 as C. salvini scopaeum. The morphological characters of the specimen,

however, have allowed us to identify it as C. salvini.

Records of C. scopaeum are from areas dominated by tropical and subtropical coniferous forests, dry decidu-

ous forests at higher elevations, and shrubby vegetation at lower elevations. Studies suggest that in the arid areas

of western México, the species would be restricted to the more humid areas close to the Pacific coast and adjacent

montane forests, and along the riparian forests in the canyons that cut through the Sierra Madre Occidental (An-

derson 1960, 1972; Crossin et al. 1973; García-Mendoza & López-González 2013). All analyzed specimens were

collected within the altitudinal range of the species as reported by Handley (1966a), from sea level to 1,722 m.

Description and Comparisons. Dorsal pelage varies from pale brown to dark brown. Most of the 38 specimens

examined had pale brown pelage (84.2%, n=32), whereas dark brown pelage was found in 15.8% (n=6). Individu-

ally, dorsal hairs are tricolored, with a dark brown base, buff middle band, and light to dark brown tips. The medial

dorsal stripe was present in all specimens (n=34), but was weakly developed in 5.8% of the sample (n=2). Usually,

GARBINO ET AL.

the dorsal stripe extends from the interscapular region to the posterior extremity of the body, but in 10 specimens

the stripe originated in the region immediately posterior to the nape. Both pairs of facial stripes are bright and wide

(interocular stripe > 1.7 mm). The tragus and base of the ears are yellowish, as are the anterior and posterior margins

of the ears close to the base. The remainder of the ear is brown. The spear of the noseleaf has a simple tip and is

brown, except for the lateral margins of the horseshoe, which are whitish.

The dimensions of the skull of C. scopaeum are similar to those of C. villosum, and there is also some overlap

between the large C. scopaeum and the small C. doriae vizottoi and C. salvini (Tables 7 and 8). In dorsal view, the

brain case is round and less massive than in C. salvini. Approximately ⅓ of the length of the nasal notch extends

behind the anterior margin of the orbits. The post-orbital constriction is relatively wide (Table 7); post-orbital pro-

cesses are small and pointed. A sagittal crest was unambiguously present in 32 of the 38 specimens (84.2%), but not

detected in 2 (5.2%), or ambiguous in 4 (10.5%). The posterior palatine process was absent in 32 of the 38 analyzed

specimens (83.8%), but small or vestigial in the remaining 6 (16.2%).

Out of 35 specimens, 30 (85.7%) had convergent I1s, with the tips touching each other; whereas, 5 had both in-

cisors separated along their entire length. The P3 is approximately oval in occlusal outline and is not in contact with

P4. The M2 has well defined main cusps, but lacks a posterolingual cingulum. The lower canine has a relatively low

crown, below the level of the coronoid process in lateral view. The anterior cingulum of the lower canine projects

rostro-medially and is visible in lateral view (Fig. 17). The p2 is small, approximately ¼ of the height of p4; and is

longer than tall and does not touch p4.

Compared with C. salvini, C. scopaeum can be distinguished by its smaller size, usually paler dorsal pelage

(varying from pale brown to dark brown). C. scopaeum has a relatively broader post-orbital constriction (Fig. 12),

and rostro-medially projected cingula of lower canines (Fig. 17).

FIGURE 17. Lateral view of part of the right dentary of A) Chiroderma salvini (LSUMZ 25649—Panamá, Darién) and B) C.

scopaeum (USNM 511378—México, Nayarit). The lower left canine was removed from the image.

From C. villosum, C. scopaeum can be differentiated by its bicolored noseleaf and spear having a simple tip;

paler ear margins; shorter nasal notch (in villosum the notch reaches the post-orbital processes); shorter orbits (in

villosum the anterior margin is in line with the middle of P4); I1s with convergent tips (usually parallel in villo-

sum); relatively short lower canine (in villosum the tip of the lower canine is at approximately the same level as the

coronoid process); and absence of a frontal gap when cranium and mandible are in occlusion (in villosum there is a

frontal gap delimited by C, I1–2, and i1–2).

The subspecies C. d. vizottoi differs from C. scopaeum by having pale buff pelage, and larger size (Table 7).

The p2 of C. d. vizottoi is larger, about ½ to ⅔ of the height of p4, while in C. scopaeum, p2 is approximately ¼ the

height of p4.

Geographic Variation and Phylogeography. A clade, here identified as scopaeum, contains six specimens

of Chiroderma, of which five were analyzed morphologically (Fig. 16). The two specimens from México (TTU

109703 and TTU 110649) are phenotypically similar to the taxon we defined here as Chiroderma scopaeum, where-

as specimens from Panamá (LSUMZ 25470), El Salvador (TTU 62462), and Guatemala (ROM 99703) have the

diagnostic characters of Chiroderma salvini. The specimens morphologically diagnosed as salvini that nested in

the scopaeum clade may represent a case of incomplete lineage sorting (ILS), a relatively common phenomenon in

recently-diverged taxa (Maddison & Knowles 2006). To test the ILS hypothesis between C. salvini and C. scopae-

um, we recommend increasing the genetic sample of Chiroderma from western México, and obtaining additional

genomic information such as single nucleotide polymorphisms. Also, it is important to note that no specimens,

morphologically diagnosed as scopaeum, are nested in the salvini clade, which contains sequences from Central and

South American specimens.

Subspecies. C. scopaeum is monotypic.

Remarks. Anderson (1960) mentioned a record of Chiroderma from Chihuahua, western México, that at the

time would considerably increase the known distribution of the genus, suggesting an undescribed species for the

region. Based on a larger sample size, Handley (1966a) described the subspecies Chiroderma salvini scopaeum,

then considered a smaller variant of C. salvini salvini. In this study, we consider the morphological, genetic, and

biogeographic evidence as sufficiently strong to treat scopaeum as a species distinct from salvini, instead of as a

geographic variant, or subspecies.

Natural History. Information on the diet of C. scopaeum is scarce. In Tahuacán, Puebla, one individual was

observed visiting the flowers of the columnar cactus Pachycereus weberi (Pachyceraceae), but the bat was not cov-

ered in pollen (Valiente-Banuet et al. 1997). In Sinaloa, C. scopaeum was captured in mist nets set under fruiting

fig trees. In Jalisco, mist nets over a stream and under a canopy formed by wild figs and other trees also caught C.

scopaeum (Jones et al. 1972; Watkins et al. 1972). Specimens have been captured in altered landscapes, such as

cornfields (Almazán-Catalán et al. 2009).

Summarizing data from the literature, along with the specimens we examined, C. scopaeum appears to be sea-

sonally polyestrous. Pregnancies occurred in January (Sinaloa), February (Jalisco), and June (Jalisco and Nayarit)

(Jones et al. 1972; Watkins et al. 1972). Lactating females have been found in May (Morelos) and June (Nayarit

and Jalisco) (Watkins et al. 1972). Females noted as non-reproductive were recorded in July (Chihuahua; Anderson

1972) and August (Colima; Wilson 1979).

Specimens Examined (N = 35): México: Colima, La Sidra (TTU 61623), Pueblo Juárez (USNM 338711 [ho-

lotype of scopaeum]); Jalisco, 20 km SW Talpa de Allende (AMNH 254647), 9.3 km W Chapala (TTU 38049), 6.4

km NW Autlán de Navarro (TTU 109703), La Cumbre (TTU 40987); Morelos, Oaxtepec (USNM 559607); Nayarit,

12.9 km NE San Miguel del Zapote, 51.5 km W Mesa del Nayar (USNM 559608–559613), 13 km NE San Blas

(TTU 110649), 5 km E El Venado (USNM 559614, 559615), 12.9 km E San Blas (TTU 6122), Arroyo La Taberna,

, 3.2 km W Mesa del Nayar (USNM 511374–511377), 2.9 km NE (by road), Coapan (USNM 511380–511382), 2.3

km N (by road), El Tacote (USNM 508636), 3.2 km E Jalcotoán (USNM 523258, 523259), Mesa del Nayar (USNM

511378, 511379), Playa Novillero (USNM 553885); Oaxaca, 30 km NW Sala de Veja (AMNH 190006); Veracruz,

Ojo de Agua del Rio Atoyac (TTU 9996–9999).

Chiroderma doriae Thomas, 1891

Synonyms: See under subspecies.

Type Material. The type of Chiroderma doriae, by original designation, is specimen BMNH 44.9.2.6 (skin) and

BMNH 49.8.16.29 (skull and mandible). The holotype is an adult of undetermined sex, but possibly female, as there

is no vestige of scrotal sac on the skin. The skin was stitched longitudinally along the dorsum and probably for

this reason the descriptions described the dorsal stripe as absent (Dobson 1878, misdentified as C. villosum; Vieira

1942). The left ear, as well as the right tarsus and metatarsus, have been lost, but the right calcar and the tibia are

still attached to the skin. Interocular stripes are evident, but the color of the skin appears to be slightly faded. The

genal pair of facial stripes is less conspicuous, and the stripe on the right side is more evident than on the left. Part

of the medial uropatagium is torn.

The skull is damaged, and the region posterior to the mesopterygoid fossa, i.e. the basioccipital, occipital, and

the posterior part of the braincase are missing. The upper dental arcade is complete. The right zygomatic arch is

GARBINO ET AL.

broken, and the root of the right upper canine is exposed. Part of the palate is also broken. The inner upper incisors

have convergent tips, almost touching each other. The mandible and lower dentition are in good condition, except

for the left angular process, which is missing.

Information on the label indicates “Minas Geraes” as the locality and that the type was obtained from Parzu-

daki, referring to Charles Parzudaki and his adopted son Emile, two active dealers in natural history specimens in

Paris. As Charles and Emile probably never collected in South America (Gouraud et al. 2016), it is not possible to

determine the collector or to estimate a more precise locality for the specimen.

Distribution and Habitat. See under Subspecies.

Description and Comparisons. Dorsal pelage is pale brown in most specimens of C. d. doriae, but some have

dark brown pelage. In C. d. vizottoi the dorsal pelage is pale buff (Fig.18). Dorsal hairs are tricolored; the base is

dark brown, the middle is buff, and the tip is pale brown (C. d. doriae) or pale buff (C. d. vizottoi). Two pairs of

interocular and genal stripes are present, wide, and formed by entirely white hairs. A median dorsal stripe is present.

The stripe is conspicuous in 25 of the 29 (86%) C. d. doriae examined, and usually extends from the interscapular

region to the posterior extremity of the rump. One C. d. doriae (ZUFMS 395) has the dorsal stripe beginning on

the nape. The ear and tragus are yellowish at the bases, as well as is the margin of the ear. The remainder of the ear

is brownish. The spear of the noseleaf is simple-tipped and the lateral borders of the horseshoe are paler than the

medial portion and spear.

Chiroderma doriae has the second largest cranium among Chiroderma species, smaller only than C. improvi-

sum (Tables 7 and 8). There is some overlap among the measurements of small C. d. doriae and large C. salvini.

Measurements of C. d. vizottoi broadly overlap with those of C. villosum, C. salvini, and large C. scopaeum (Tables

7 and 8). The braincase is low in C. d. doriae, relative to the length of the skull, and less globose than in the other

species (except for C. improvisum; Figs. 19, 20). In C. d. vizottoi, the braincase is relatively higher and more globose

than in the nominal subspecies. A sagittal crest was present in every specimen of C. d. doriae we examined (n=71),

being conspicuous in 41 (57%), moderate in 25 (35%), and low or vestigial in 5 (7%). In C. d. vizottoi, the sagittal

crest was present in all specimens (n=11), conspicuous in ten (90.9%) and moderate or low in one (9.1%). The nasal

notch is long, extending well behind the anterior rim of the orbits. The post-orbital processes are moderately devel-

oped, more so than in gorgasi and trinitatum, but less than in salvini, scopaeum and villosum (Fig. 19).

FIGURE 18. Dorsal view of the skin of A) Chiroderma doriae doriae (ALP 6121—Brazil, Rio de Janeiro) and B) C. d. vizottoi

(ALP 10421—Brazil, Ceará).

FIGURE 19. Dorsal (A) and ventral (C) views of the skull of Chiroderma doriae doriae (TTU 99569—Paraguay, La Cordil-

lera), and dorsal (B) and ventral (D) views of the skull of C. doriae vizottoi (ALP 10421—Brazil, Ceará).

FIGURE 20. Skull and mandible, in lateral view, of A) Chiroderma doriae doriae (TTU 99569—Paraguay, La Cordillera); B)

C. doriae vizottoi (ALP 10421—Brazil, Ceará).

GARBINO ET AL.

FIGURE 21. Phylogenetic relationships of Chiroderma doriae, C. gorgasi and C. trinitatum, based on 87 sequences of the cyto-

chrome c oxidase subunit 1 gene. Localities in parentheses are detailed in the gazetteer (Appendix 1). This subtree is a detailed

version of the clades named “doriae”, “gorgasi”, “trinitatum A”, and “trinitatum B” in figure 4.

The posterior palatine process is absent in 51 (78%) of the 65 specimens of C. d. doriae we examined. When

present, the palatine process is small and inconspicuous, except for three specimens (4.6%), in which this structure

was conspicuous. In C. d. vizottoi, the palatine process was absent in five of nine specimens in our sample. The

posterior border of the palate is U-shaped, differing from other species of Chiroderma, which have an even posterior

border. Paraoccipital processes are present in C. d. doriae. When skull and mandible are in occlusion, a lateral gap

is formed, as in C. salvini, C. scopaeum, C. gorgasi, and C. trinitatum (Fig. 9).

The I1s have converging tips that contact each other in most specimens. One (ZUFMS 395) had parallel I1s,

with no contact. The P3, in occlusal view, is wider (buccolingually) than long (mesiodistally). P3 touches C, but

does not touch P4 (in the similar-sized C. improvisum, P3 and P4 are in contact; see Fig. 19). The P4 has a well-

developed disto-lingual cingulum (relatively less-developed in the other species). The mandible is robust, with the

condylar processes clearly above the toothrow plane, or at approximately the same level. The coronoid process

clearly is higher than the tip of the lower canine, when the mandible is viewed laterally (in C. salvini and C. vil-

losum, the coronoid process is at the same level as the canines). The p2 crown is ½ to ⅔ the height of p4, and is ap-

proximately as high as long (longer than tall in C. salvini, C. scopaeum, C. improvisum, and C. villosum) (Fig. 20).

The p2 does not touch p4. The mandible with a small p2 identified by Oprea & Wilson (2008) as C. doriae (their

Figure 2) is a C. villosum (USNM 309905).

The only other species of Chiroderma sympatric with C. doriae is C. villosum, from which doriae can be dif-

ferentiated by its larger size, the both pairs of facial stripes wide and conspicuous (narrow and inconspicuous in

villosum), bicolor noseleaf, and ears with pale margins. C. doriae also lacks posterior palatine processes, has con-

verging I1s (usually parallel in villosum), p2 taller than longer (p2 longer than tall in villosum), relatively short c (tall

in villosum), and lacks a frontal gap when cranium and mandible are in occlusion (Fig. 14).

Geographic Variation and Phylogeography. The phylogenetic analyses of 16 sequences of C. doriae did not

show geographic structuring, with haplotypes from geographically distant regions, e.g. from Paraguay north to Rio

Grande do Norte, Brazil grouped together (Fig. 21). Although intraspecific genetic variation (0.49%) is considered

low (Table 3), the phenotype of C. doriae varies geographically. Specimens from the Caatinga of Piauí and Ceará,

and from the Amazonia—Cerrado ecotone in Maranhão, are significantly smaller and have much paler pelage than

specimens from the Mata Atlântica and Cerrado, which are larger and have the pelage color varying from pale

brown to dark brown (Figs. 18, 20).

FIGURE 22. Dispersion of the two first principal components (PC1) of 20 climatic variables, and 13 morphometric variables

of Chiroderma doriae. Pearson correlation coefficient = -0.744.

GARBINO ET AL.

TABLE 11. Loadings of the first and second principal components, extracted from the variance-covariance matrix of a

principal component analysis of 19 climatic variables, plus latitude, from collecting localities of Chiroderma doriae doriae

and C. d. vizottoi.

Variables PC 1 PC 2

Latitude -0.86 -0.49

BIO1 0.48 0.49

BIO2 0.14 -0.87

BIO3 0.88 -0.07

BIO4 -0.84 -0.46

BIO5 0.39 0.12

BIO6 0.39 0.77

BIO7 -0.32 -0.83

BIO8 -0.02 0.33

BIO9 0.63 0.56

BIO10 0.20 0.54

BIO11 0.60 0.53

BIO12 -0.34 0.38

BIO13 0.45 -0.04

BIO14 -0.86 0.49

BIO15 0.79 -0.43

BIO16 0.37 -0.02

BIO17 -0.88 0.46

BIO18 -0.83 -0.50

BIO19 0.20 0.96

Eigenvalues 6.98 5.70

Proportion of variation 34.91% 28.52%

TABLE 12. Loadings of the first principal component (PC1) extracted from the variance-covariance matrix of a principal

component analysis of 13 cranio-dental measurements comparing Chiroderma doriae doriae and C. d. vizottoi.

Measurements PC 1

GLS 0.93

CIL 0.96

CCL 0.96

PB 0.71

BB 0.75

MB 0.89

ZB 0.91

MTRL 0.92

M1–M1 0.88

M2–M2 0.90

MANDL 0.89

DENL 0.84

CAL 0.81

Eigenvalues 9.98

Proportion of variation 76.80%

Given that population samples of C. doriae from the Caatinga (Ceará and Piauí) and Maranhão are phenotypi-

cally distinct from those from Mata Atlântica and Cerrado, but do not compose a distinct haplogroup, we treat this

population as a subspecies for which the available name is vizottoi, described by Taddei & Lim (2010). Subspecific

recognition followed Patten (2015) for phenotypically distinct and geographically restricted groups that do not form

clades.

Furthermore, geographic variation in C. doriae appears to be correlated with temperature and rainfall (Fig.

22, Tables 11 and 12). Precipitation in driest month (variable BIO14 of WorldClim), precipitation in driest quarter

(BIO17), precipitation in warmest quarter (BIO18), temperature seasonality (BIO4), and latitude were the variables

having the strongest correlation with size. This suggests that individuals are larger in regions having a more seasonal

climate, or at higher latitudes, and in areas with greater rainfall (Appendix 5).

Subspecies. We recognize two subspecies in Chiroderma doriae.

C. d. doriae Thomas, 1891

Synonyms:

[Phyllostoma] dorsale Lund, 1842a: 134; nomen nudum.

C[hiroderma]. pictum Gray, 1866: 117; nomen nudum.

Chiroderma villosum: Dobson, 1878: 534; not Chiroderma villosum Peters, 1860.

Ch[iroderma]. doriae Thomas, 1891: 881; type locality “Minas Geraes.” (State of Minas Gerais, Brazil).

Chiroderma villosum: Winge, 1892: 9; not Chiroderma villosum Peters, 1860.

[Chiroderma] doriai Trouessart, 1904: 118; unjustified emendation of Chiroderma doriae Thomas.

Chiroderma sp. Pedro, Passos and Lim, 2001: 138.

Chiroderma doria Wagner et al., 2015: 1016; incorrect subsequent spelling of Chiroderma doriae Thomas, 1891.

Distribution and Habitat. The nominal subspecies is distributed in Brazil from the northeastern state of Rio Grande

do Norte, to Santa Catarina in the south, and westward into the states of Mato Grosso do Sul, Goiás, and the Distrito

Federal. The subspecies also occurs in eastern Paraguay (departments of La Cordillera and San Pedro; Fig. 23). Fu-

ture studies may reveal C. d. doriae in Bolivia, as it is recorded in adjacent Corumbá, Mato Grosso do Sul, Brazil.

The subspecies occurs in the Atlantic rainforest and associated formations such as the restinga, and has been

found in Cerrado and Pantanal habitats (Taddei 1979; Gregorin 1998; Bordignon 2005). C. d. doriae is also pres-

ent in urban parks of large cities and in other altered landscapes (Esbérard et al. 1996; Nogueira & Peracchi 2003;

Nunes et al. 2017). This subspecies occurs at elevations from sea level (e.g. São Sebastião, São Paulo, Brazil) to

approximately 1,200 m (e.g. Diamantina, Minas Gerais, Brazil).

C. d. vizottoi Taddei and Lim, 2010

Synonyms:

Chiroderma nov. sp. Cruz, Martínez, and Fernandes, 2007: 615.

Chiroderma sp. Gregorin, Carmignotto, and Percequillo, 2008: 372.

Chiroderma vizottoi Taddei and Lim, 2010: 384; type locality “Teresina (ca. 05° 02 ′ S and 42° 45 ′ W), in the State of Piauí,

Brazil.”

Distribution and Habitat. This subspecies is in the Brazilian states of Ceará, Maranhão, and Piauí (Fig. 23). A

specimen from the Caatinga of Piauí was captured in an area with low xerophytic trees (3 to 5 meters high), next to

a rocky outcrop (Gregorin et al. 2008). Two specimens from Maranhão were captured in mist nets set on the beach,

in a mosaic of sandbank and mangrove vegetation.

Remarks. Lund (1842a: 134, 1842b: 200), in his studies on the extant and fossil fauna of Lagoa Santa, Minas

Gerais, recorded Phyllostoma dorsale among the living species of the region. In both publications, Lund clearly

uses Phyllostoma dorsale as a new name, as evidenced by the “m.” (= mihi) following the name. Because the name

is present only in a faunal list, and no formal description is given, Phyllostoma dorsale Lund is considered a nomen

nudum for nomenclatural purposes (see article 12 of the ICZN 1999).

Gray (1866), in his revision of Phyllostomidae, listed two species in Chiroderma, C. villosum and C. pictum.

The latter name is a nomen nudum, because it lacks a description. We include Chiroderma pictum in the synonymy

of Chiroderma doriae because, in the Dobson’s (1878) catalogue of bats in the British Museum, the only specimen

GARBINO ET AL.

of Chiroderma in the collection at the time of Gray’s (1866) publication was the specimen that later became the

type of Chiroderma doriae. The Latin word pictus means “painted”, or “decorated”, suggesting that Gray referred

to the conspicuous facial stripes, observable that specimen, a characteristic differentiating this species from Peters’

C. villosum, which was the only other Chiroderma known at that time.

Dobson (1878), in his description of Chiroderma salvini, compared the type with a specimen from Minas Gerais

(Brazil) identified by him as Chiroderma villosum. However, Thomas (1891), based on an unpublished plate by Wil-

helm Peters, available in the Genova Natural History Museum, recognized that the Minas Gerais specimen Dobson

identified as Chiroderma villosum did not represent Chiroderma villosum Peters, 1860. Thomas (1891) described

that specimen as Chiroderma doriae.

Winge (1892), studying the material sent by Lund to the Copenhagen museum, identified as Chiroderma vil-

losum the material referred to Lund as Phyllostoma dorsale. Winge (1892: 9) located, among the Lagoa Santa speci-

mens representing extant taxa, five fluid-preserved specimens, two skeletons, and three skins. Among the fossil

material, Winge mentioned only post-cranial elements from Lapa da Escrivaninha and a cave he did not identify.

Thomas (1893), after receiving part of the Lagoa Santa material Winge identified as Chiroderma villosum,

correctly identified the skull as belonging to C. doriae. This publication is the first to ascertain that Phyllostoma

dorsale of Lund was the same taxon that Thomas (1891) described as Chiroderma doriae. The specimen collected

by Lund at Lagoa Santa (BMNH 93.1.9.16) and examined by us is probably the same specimen donated by Winge

to the British Museum and mentioned by Thomas (1893).

Aside from the Lagoa Santa specimens and the holotype, all from Minas Gerais, no additional specimen of C.

doriae were mentioned in the literature for 86 years. Probably for this reason, publications that mentioned the spe-

cies cited only Minas Gerais as a locality of occurrence and repeated the morphological characteristics mentioned

in the original description (Vieira 1942; Cabrera 1958). It is important to note, however, that the BMNH houses

specimens of C. doriae collected in the beginning of the 20th century, by Alphonse Robert in Ypanema, currently

Floresta Nacional de Ipanema, São Paulo (BMNH 3.7.1.163), and by Wilhelm Ehrhardt in Joinville, Santa Catarina

(BMNH 9.11.19.15).

Taddei (1979) published the first study including new data on C. doriae since Thomas’s report in 1893. When

he redescribed the taxon based on 39 specimens of C. d. doriae collected in northwestern São Paulo, Taddei (1979)

confirmed the presence of a conspicuous dorsal stripe previous authors had considered to be absent.

Natural History. C. d. doriae is secondarily granivorous, specialized in chewing and grinding seeds of the

fruits of Ficus to extract their nutritional content (Taddei 1980; Nogueira & Peracchi 2001, 2003). Four species of

Ficus have been documented in the diet of C. d. doriae: Ficus clusiaefolia, F. cyclophylla, F. organensis, and F.

tomentella (Sipinski & Reis 1995; Esbérard et al. 1996; Nogueira & Peracchi 2001). Individuals of C. d. doriae

have been captured near to or visiting fruiting trees of Cecropia glaziovii (Urticaceae), Ficus enormis, F. gomeleira,

and Muntingia calabura (Muntingiaceae), suggesting that this bat also consumes the fruits of these species (Taddei

1980; Esbérard et al. 1996). In addition to figs, fruits and infructescences of Cecropia pachystachya, Chlorophora

tinctoria (Moraceae), Piper sp., and Psychotria suterella (Rubiaceae) are also consumed (Taddei 1973; Esbérard

et al. 1996; Nogueira & Peracchi 2001; Novaes et al. 2010; Laurindo et al. 2017). Individuals of C. d. doriae have

been found covered in the pollen of Mabea fistulifera (Euphorbiaceae) and of an unidentified species, suggesting

that the bat also feeds on flowers (Esbérard et al. 1996; Olmos & Boulhosa 2000).

Day roosts used by C. d. doriae are not known (see review in Garbino & Tavares 2018b), but there are two re-

cords from caves, the use of which may be occasional: one in the state of São Paulo (Arnone 2008) and the other in

Minas Gerais (information on specimen UFMG 4953). In the Cerrado of São Carlos, southeastern Brazil, the species

was found in pellets of the Stygian Owl (Asio stygius) by Motta-Junior & Taddei (1992).

At localities in southeastern Brazil where they occur in sympatry, C. d. doriae is usually captured in much

higher numbers than C. v. villosum when mist nets are set at ground level. At the Rio de Janeiro Botanical Garden,

eight nights of ground-level mist netting resulted in the capture of 49 C. d. doriae and 5 C. v. villosum (Nogueira &

Peracchi 2003). In Mirassol, São Paulo, 24 C. d. doriae and 6 C. v. villosum were captured in ground-level nets (Tad-

dei 1979). In contrast, Gregorin et al. (2017), using canopy mist nets placed between 11 and 19.5 m above ground

in the Parque Estadual do Rio Doce, Minas Gerais, captured 1 C. d. doriae and 24 C. v. villosum. The anecdotical

report of Taddei (1980) describes the approach by C. d. doriae to fruiting trees as a low flight. Although the litera-

ture on the ecology of C. d. doriae is scarce when compared to that for C. gorgasi, C. trinitatum, and C. villosum, it

suggests that the species is not as much a canopy frugivore as the other species.

Five species of ectoparasites are known from C. d. doriae: Aspidoptera falcata (Streblidae), Megistopoda prox-

ima (Streblidae), Strebla guajiro (Streblidae), and Trichobius joblingi (Streblidae) in Sergipe; and the mite Periglis-

chrus iheringi (Spinturnicidae) recorded on individuals from Mato Grosso do Sul, Rio de Janeiro, and in Paraguay

(Presley 2004; Lourenço et al. 2016; Lima Silva et al. 2017; Soares et al. 2017). Lourenço et al. (2018) found a

trypanosomatid parasite in the blood of C. d. doriae from Distrito Federal, Brazil.

The reproductive pattern is seasonal polyestry (Taddei 1980). Pregnancies were recorded in June through Octo-

ber, with earlier stages reported in June and July, and females with advanced fetuses recorded from August through

October (Taddei 1980; Esbérard et al. 1996). Births of single young occur between October and January, suggesting

a gestation period of at least three and half months (Taddei 1980). Females simultaneously pregnant and lactating

are common, indicating postpartum estrus and the production of two young per year, with a second birth period in

February and March (Taddei 1976, 1980; Esbérard et al. 1996).

The natural history of C. d. vizottoi is poorly known. In Ceará, seven specimens were mist netted close to an

unidentified fruiting Moraceae; one was pregnant and another lactating when captured in January (Silva et al. 2015).

In Maranhão, a male and female were caught in a mist net placed along the beach in a small fishing community next

to a mangrove swamp near regenerating rain forest and a “babaçual” (Attalea speciosa [Arecaceae]) palm grove.

The mist-net was set in front of a tree locally called “agarra” or “amapá” (Apocynaceae?), and one of the bats had

its abdomen covered with a sticky material resembling a milky sap, or latex. Almeida et al. (2016) recorded the mite

Periglischrus iheringi (Spinturnicidae) on C. d. vizottoi in Ceará.

Specimens Examined (N = 136): Brazil: Alagoas, Mata da Cachoeira, São José da Lage (UFPB 4348); Bahia,

Reserva Particular do Patrimônio Natural Serra Bonita ([UFMG]RSB 21, [UFMG]RSB 22); Ceará, Reserva Natu-

ral Serra das Almas (ALP 10196, 10418, 10421, 10423, 10440, 10451, 10464); Goiás, Itumbiara (MCN-MQ 145);

Maranhão, São Luís (ALP 6633–6635, [UFMG]VCT 373, 374); Mato Grosso do Sul, Corumbá ([UFMG]VCT

6069, [UFMG]VCT 6081), Fazenda Barma (MZUSP 28591, 28688), Morro do Paxixi (ZUFMS 2300), Parque Es-

tadual Matas do Segredo (ZUFMS 493), Urucum (ZUFMS 800, 1058–1062, 1069), Urucum, Morro São Domingos

(ZUFMS 912); Minas Gerais, without specific locality (BMNH 44.9.2.6 [holotype of doriae]), Área de Proteção

Ambiental Coqueiral (CMUFLA 163), Barão de Cocais ([UFMG]VCT 5831), Belo Horizonte (UFMG 3537), Es-

tação Ecológica de Pirapitinga in Morada Nova de Minas (UFMG 3383), Estação Ecológica de Pirapitinga in Três

Marias (ALP 9154), Gruta do Salitre in Diamantina (UFMG 4953), João Monlevade (CMUFLA 965), Lagoa Santa

(BMNH 93.1.9.16); Mariana (CMUFLA 938, [UFMG]VCT 6058), Parque Estadual do Rio Doce (CMUFLA 1157),

Pompéu (MCN-MQ 253), Usina Hidrelétrica Retiro Baixo (CMUFLA 1415), Valos (CMFULA 496); Pará (not

mapped; BMNH 7.1.1.723 [probably an error]); Paraíba, Fazenda Pacatuba, 10 km NE Sapé (UFPB 3), Reserva Bi-

ológica Guaribas (UFPB 7327, 7341); Pernambuco, Reserva de Saltinho ([MZUSP] AD119); Piauí, Parque Nacio-

nal de Sete Cidades (DZSJRP 11460 [paratype of vizottoi]), Teresina (DZSJRP 18054 [holotype of vizottoi]); Rio de

Janeiro, Ilha da Marambaia (ALP 6121), Jardim Botânico do Rio de Janeiro (7508–7511, 7513–7515, 7517, 7519,

7520, 8059, 8062, 8064, 8077, 8079–8081), Morro Azul (ALP 9142), Parque Estadual da Pedra Branca (ALP 5784),

Parque Natural Municipal da Prainha (ALP 6650); Rio Grande do Norte, Mata da Estrela (MZUSP 35027); Santa

Catarina, Joinville (BMNH 9.11.19.15); São Paulo, Barra do Ribeirão Onça Parda (MZUSP 10632), Barão Geraldo

(ZUEC 783), Cachoeira dos Índios (DZSJRP 3140, 3141), Cananéia (MZUSP 26354), Estação Experimental de

Pindorama (DZSJRP 16506), Fazenda João XXIII ([LMUSP]GTG 01), Fazenda Paraguassu (ZUEC 1002), Fazenda

Santa Carlota (MZUSP 35028), Fazenda Silvio Fazoli in Irapuã (DZSJRP 2924, 2937, 2945, 2946, 3611, 3728),

Grota de Mirassol (DZSJRP 2640, 3997, 3998, 3999, 4029), Iguape (MZUSP 21802), Ilha do Cardoso (MZUSP

28037, ZUFMS 395, 397), Instituto de Biologia Marinha in São Sebastião (DZSJRP 10050), Itapetininga (USNM

542616), Parque Estadual da Ilha Anchieta (MZUSP 29456, 31582), Parque Estadual de Ilhabela (MZUSP 35029),

Parque Estadual Turístico do Alto Ribeira (MZUSP 34012), São José do Rio Preto (DZSJRP 2469), São Roque

(MZUSP 15112), Sítio Progresso (DZSJRP 3810, 3825, 3921, 4271–4273, 4381–4385, 4445), Ypanema (BMNH

3.7.1.163), Sergipe, Estação Ecológica de Itabaiana (ALP 6545), Floresta Nacional do Ibura (CMUFS SSB1-FNI,

SSB2-FNI, SSB376-FNI, SSB377-FNI, SSB20-FNI, SSB33-FNI), Mata do Junco (CMUFS 51, 71, 73, 94), Parque

Nacional Serra de Itabaiana (CMUFS 65). Paraguay: La Cordillera, Estancia Sombrero (TTU 75275, 99569); San

Pedro, Yaguarete Forests, 0.5 km W headquarters (TTU 95747). Locality unknown: BMNH 7.1.1.698.

GARBINO ET AL.

FIGURE 23. Collecting localities of the analyzed specimens of Chiroderma doriae doriae, C. d. vizottoi, C. gorgasi, and C.

trinitatum. The locality numbers are referenced in the gazetteer (Appendix 1).

Chiroderma trinitatum Goodwin, 1958

Synonyms:

Chiroderma trinitatus Goodwin, 1958:1; type locality “Cumaca, Trinidad, British West Indies.”

Chiroderma trinitatum: Handley, 1960:466; correct gender concordance.

Chiroderma trinitatum trinitatum: Barriga-Bonilla, 1965: 247; name combination.

Chiroderma trinitratum Linares and Moreno-Mosquera, 2010: 275; incorrect subsequent spelling of Chiroderma trinitatum

Goodwin, 1958.

Type Material. The holotype, designated in the original publication, is specimen AMNH 175325, a female pregnant

when collected in a well-lit cave, by L. Venus and B. Smith on March 22, 1956, in Cumaca, Trinidad and Tobago.

The skin is preserved in fluid and nearly all hair has fallen out. There is a transversal cut on the abdomen. The skull

has been removed and is in good condition, with all the teeth and cranial bones preserved. The fetus, removed from

the type, has a distinct median dorsal stripe and a crown-rump length of approximately 20 mm.

Distribution and Habitat. Specimens are known form Guyana; Suriname; French Guiana; Trinidad; northern,

central and western Brazil; northern and eastern Bolivia; eastern Perú; eastern Ecuador; southern and eastern Co-

lombia; and southern Venezuela (Fig. 23).

Records are from humid tropical forests, in the Amazon basin, Orinoco basin, and the Guianas. Some records

are from ecotonal areas between humid forests and drier, more seasonal formations, such as in Serra do Roncador

(central Brazil), and in San Ramón (northeastern Bolivia). C. trinitatum have been collected from approximately

20 m above sea level (e.g. Belém, Brazil) to elevations near 1,050 m, in the Andean foothills (e.g. Santa Bibiana,

Perú), corroborating the altitudinal amplitude given in the literature (e.g. Handley 1976; Ascorra et al. 1996; Solari

et al. 2006, 2019).

Description and Comparisons. Dorsal pelage may be pale brown, dark brown, or grayish brown (Fig. 24). A

completely white C. trinitatum was recorded in the Peruvian Amazon by Tello et al. (2014). Dorsal hairs are tricol-

ored, the base about ¼ of the hair length and dark brown, middle portion about ½ of the hair length and pale buff

or pale gray, and tips about ¼ of the hair length and pale brown, dark brown, or grayish brown. Facial stripes are

always present with the interocular pair wider (> 2 mm) than the genal stripes. A median dorsal stripe was present in

111 of the 113 specimens examined (98%). When present, the stripe was barely visible in 13 of 95 specimens (13%).

The stripe usually begins in the interscapular region and reaches the posterior rump of the body. In some specimens,

the dorsal stripe began more anteriorly in the region immediately behind the nape. The ears have yellowish margins

and base, with the remainder brownish. The spear of the noseleaf has a simple tip, is brown in color, with paler

lateral borders of the horseshoe.

FIGURE 24. Dorsal view of the pelage of Chiroderma trinitatum. A) USNM 361723 from Brazil, Pará; B) USNM 393709 from

Brazil, Mato Grosso.

The skull is similar to that of C. gorgasi and it is smaller than every other species of Chiroderma (Tables 7 and

8). The braincase is globose, standing above the frontonasal region in lateral view. A sagittal crest was absent in 37

of 126 specimens (29.4%), weakly developed in 86 (68.2%), and well developed in 3 (2.3%). The nasal notch is

relatively short, not reaching the interorbital region (Fig. 25). C. trinitatum has relatively small orbits; the anterior

border approximating the mesial margin of M1 (Fig. 26). Post orbital processes are present, but rhomboid instead

of pointed as in the other species.

A posterior palatine process was absent in 110 (90.9%) of the 121 specimens examined. A small process was

present in 10 specimens, and one (AMNH 264076) had an anomalous notch in place of a projection on the margin

of the palate. Paraoccipital processes are absent. When cranium and mandible are in occlusion, there is a lateral gap

bordered by the C, P3, P4, p2 and p4 (Fig. 9).

The I1s have converging tips in most of the specimens (112 out of 122) we examined. The I1s may be in contact

at the base, along approximately ⅔ of their length, or only at their tips, the most frequent state. In some C. trinitatum,

the I1s are separated throughout their length. The P3 is wider (buccolingually) than long (mesiodistally) and does

not touch P4.

GARBINO ET AL.

FIGURE 25. Dorsal (A) and ventral (C) views of the skull of Chiroderma trinitatum (USNM 581934—Perú, Amazonas) and

dorsal (B) and ventral (D) view of C. gorgasi (USNM 335294—Panamá, San Blas).

FIGURE 26. Skull and mandible, in lateral view, of A) Chiroderma trinitatum (USNM 581934—Perú, Amazonas) and B) C.

gorgasi (USNM 335294—Panamá, San Blas).

The crown of the lower canine is relatively short, clearly below the level of the tip of the coronoid, in lateral

view (Fig. 26). The p2 is large, approximately ¾ of the height of p4, and higher than long. The p2 may be close to

or in contact with the canine, or it may lie approximately equidistant between c and p4 (Fig. 26).

Chiroderma trinitatum is easily differentiated from C. doriae and C. improvisum by its much smaller size (Ta-

bles 7 and 8). The intermediate-sized species, e.g. C. salvini, C. scopaeum, and C. villosum, are distinguishable from

C. trinitatum by having their longer nasal notch that reaches the interorbital region, pointed post-orbital processes

and the short p2, which is approximately ¼ the crown height of p4.

The species most similar to C. trinitatum is C. gorgasi. C. trinitatum has relatively shorter lower canines, the

tips of which are clearly below the level of the top of the coronoid process in lateral view. The lower canines have

higher crowns in C. gorgasi, being on the same level or higher than the tip of the coronoid process (Fig. 26). The

base of lower canines of C. trinitatum is also longer, but shorter in C. gorgasi. The p2 of C. trinitatum is usually

higher than long mesiodistally; whereas, in C. gorgasi the p2 is longer than high (Fig. 27). As recently described by

Lim et al. (2020), C. trinitatum tends to have a wider braincase and typically has a third cuspid on p4 that is absent

in C. gorgasi.

FIGURE 27. Right dentary of A) Chiroderma trinitatum (USNM 460124—Brazil, Pará) and B) C. gorgasi (USNM 335294—

Panamá, San Blas).

Geographic Variation and Phylogeography. Phylogenetic analyses of 68 sequences of C. trinitatum resulted

in two highly-supported clades (Fig. 21). One of the clades is based on sequences from 26 specimens from the Gui-

anas (French Guiana, Guyana, and Suriname), and the island of Trinidad. The other clade consists of 42 specimens,

from the Guianas (Guyana and Suriname) and the Amazon basin (Bolivia, Brazil, Ecuador, and Perú) (Fig. 21).

However, we could not find any morphological differences between the two clades.

Subspecies. C. trinitatum is monotypic.

Natural History. C. trinitatum is frugivorous and is known to consume fruits and infructescences of at least

five species: Cecropia obtusifolia, Piper elongatum, Solanum riparium (Solanaceae), Ficus sp., and Vismia sp. (Hy-

pericaceae) (Reis & Peracchi 1987; Loayza et al. 2006; Linares & Moreno-Mosquera 2010). C. trinitatum has also

been recorded drinking the mineral-rich water at clay licks (“collpas”) in the Peruvian Amazon (Bravo et al. 2008,

2010; Ghanem et al. 2013; Ghanem & Voigt 2014).

In most studies comparing the relative abundance of species in the canopy and understory, C. trinitatum was

more commonly netted in the higher forest strata, at approximately 20 m, suggesting that the species is a canopy

frugivore (Ascorra et al. 1996; Simmons & Voss 1998; Charles-Dominique & Cockle 2001; Kalko & Handley Jr.

2001; Delaval et al. 2005; Rex et al. 2011). Day roosts of C. trinitatum are unknown, and the only information avail-

able comes from the type specimen, which was collected on the island of Trinidad in a cave described by Goodwin

& Greenhall (1961) as well-lit and co-inhabited by Micronycteris megalotis.

In Venezuela, two species of ectoparasites were documented on C. trinitatum, the mite Periglischurus iheringi

(Spinturnicidae) and a species of Streblidae of the genus Paratrichobius (salvini complex) (Herrin & Tipton 1975;

Wenzel 1976). In Colombia, the tick Ornithodoros azteci (Argasidae) was recorded from C. trinitatum by Marin-

kelle & Grose (1981). The endoparasite Hasstilesia tricolor (Nematoda) was recorded by Nogueira et al. (2014) in

C. trinitatum from Acre, Brazil.

Reproductive data suggest seasonal polyestry. Pregnant females are recorded from December through March in

the Amazon of Colombia, Perú, and Venezuela, and on the island of Trinidad. Pregnancies are recorded from June

through September in Guyana and the Amazon of Brazil, Perú, and Venezuela. Lactating females were documented

in February, April, May, and July. Apparently, gestation peaks during the rainy season (December to March), with

one birth peak from the middle to the end of the rainy season, and a second during the dry season (June to Septem-

ber) with births occurring close to the beginning of the rainy season.

Specimens Examined (N = 146): Bolivia: Beni, Estancia Yutiole (AMNH 210810), Remansos (AMNH

209520, 209521); La Paz, Río Coraico Valley (AMNH 246646), Santa Ana de Madidi (AMNH 261632, 261641);

GARBINO ET AL.

Santa Cruz, 10 km N San Ramón (AMNH 261674), Parque Nacional Noel Kempff Mercado, 23 km S Campa-

mento Los Fierros (AMNH 264077), Parque Nacional Noel Kempff Mercado, 27.5 km S Campamento Los Fierros

(AMNH 264076), Parque Nacional Noel Kempff Mercado, 3 km S Campamento Los Fierros (AMNH 264075),

Parque Nacional Noel Kempff Mercado, El Refugio (USNM 584492). Brazil: Acre, Parque Nacional da Serra do

Divisor (ALP 7020, 7088, 7099, 7124, 7134, 7143, 7144, 7195, 7295, 7311); Amazonas, Comunidade Cachoeirinha

(LMSUP[ICA033]), opposite to Comunidade São Pedro (LMUSP[ICA173]); Mato Grosso, 264 km N Xavantina

(USNM 393704–393711), Parque Nacional do Juruena, Serra dos Apiacás (CMUFLA 1284), São José do Rio Claro

(MZUSP[PEV 896–897]); Pará, Fazenda Bocaina (UFMG[VCT1437]), Fazenda Fartura (MZUSP 36012, 36013),

Floresta Nacional de Carajás (UFMG[VCT6342]), rio Xingu, Linha de Transmissão Jurupari (MZUSP 35033),

Sta. A, IAN (USNM 361723, 460127), Várzea, Belém (USNM 460124, 460125, 460126); Rondônia, Monte Ne-

gro (MZUSP 35026, ZUFMS 1342). Colombia: Amazonas, Puerto Nariño (USNM 483766–483769); Vichada,

Territorio Faunistico Tuparro (IAvH-M 2083). Guyana: Cuyuni-Mazaruni, Maz 3 (BMNH 1980.751, 1980.752).

Namai Creek (ROM 108144); Potaro-Siparuni, Iwokrama Reserve (ROM 109026); Upper Demerara-Berbice, 3.2

km W Kurupukari (BMNH 1997.39), Tropenbos (ROM 103486). French Guiana: Sinnamary, Paracou (AMNH

266255, 266256, 267189, 268532, 269118). Perú: Amazonas, Cordillera del Condor (USNM 581934); Cusco,

Camisea, Armihuari (MUSM 13619, 13622, 13623, USNM 582837), Camisea, Pagoreni (MUSM 13624–13626,

USNM 582838), Consuelo (MUSM 19670); Huánuco, Puerto Inca (MUSM 36692); Junín, Santa Bibiana (MUSM

40606); Loreto, Jenaro Herrera (MUSM 4219, 5594), km 22,7 da rodovia Iquitos-Nauta (MUSM 29559), Peña

Negra (MUSM 29557), Quebrada Grande (MUSM 21134, 21135), Río Lagartococha (MUSM 21138); Madre de

Dios, Albergue Maskoitania (MUSM 19669), Pakitza (MUSM 678), Quebrada Aguas Calientes (MUSM 16651),

Refugio Juliaca (MUSM 11662); Pasco, Campamento Río Lobo (MUSM 10229), Cerro Chontiya (MUSM 10226,

10227), Cerro Jonatán (MUSM 10228), San Pablo (AMNH 230656), Yanahuanca (MUSM 10881); Puno, Curva

Alegre (MUSM 26658), San Fermín (MUSM 26659); Ucayali, Concesión de Conservación Río La Novia (MUSM

44185); Suriname: Brokopondo, Brownsberg Nature Park (ROM 114213); Sipaliwini, Kushere Landing (ROM

120168). Trinidad and Tobago: Trinidad, Arima (AMNH 205373), Cumaca (AMNH 175325 [holotype of trini-

tatum]), Fillete (AMNH 205375), Las Cuevas (BMNH 1971.121). Venezuela: Amazonas, Boca Mavaca (USNM

405159), Capibara (USNM 415245), Cerro Neblina base camp (USNM 560764–560766), Guayabal (USNM

415256, 415257), Río Cunucunuma (MZUSP 27166, 27167, USNM 405132–405139, 405141–405148, 405156,

405157), Río Manapiare (USNM 415250–415254); Apure, La Blanquita (USNM 440348); Barinas, Altamira

(USNM 418121); Bolívar, 85 km SSE El Dorado (USNM 387192), El Manaco (USNM 387193–387198, 387202,

387203); Yaracuy, Minas de Aroa (USNM 440747).

Chiroderma gorgasi Handley, 1960

Synonyms:

Chiroderma gorgasi Handley, 1960: 464; type locality “Tacarcuna Village, 3,200 ft., Río Pucro, Darién, Panama.”

Chiroderma trinitatum gorgasi: Barriga-Bonilla, 1965: 246; name combination.

Type Material. The type of C. gorgasi, USNM 309903, consists of a stuffed skin, skull and mandible, collected in

Tacarcuna Village, Panamá, on March 6, 1959 by C. O. Handley and B. R. Feinstein (field number COHJR 5436).

It is an adult male, captured in a mist net over water.

The skin is in good condition with the facial and dorsal stripes observable in the specimen. The skull and man-

dible are in good condition and every tooth is present. The I1 have convergent tips.

Distribution and Habitat. Specimens are known from Panamá, western Colombia, and northwestern Ecuador

(Fig. 23), and there is a record from eastern Honduras (Turcios-Casco et al. 2020). The unconfirmed record for

Costa Rica is based on a bat captured and released by R. LaVal in Tortuguero (Timm & LaVal 1998). Also in Costa

Rica, Harvey & González-Villalobos (2007) reported the capture of 18 “Chiroderma trinitatum” in Talamanca, but

we could not verify if there are voucher specimens to support this claim. The occurrence of the species in Costa Rica

is expected, as C. gorgasi has been recorded in western Panamá and eastern Honduras (Handley 1966b; Turcios-

Casco et al. 2020).

The records of C. gorgasi are from the humid forests of the Chocó of Colombia, the Darién of Panamá, Caribbe-

an lowland forests of Honduras, and montane forests of the Rio Magdalena valley in Colombia. The altitude where

specimens have been obtained ranges from 30 m in Esmeraldas, Ecuador, to 975 m, in Tacarcuna, Panamá. There

are Colombian records of the species occurring at 2,100 in Tolima and between 1,600 and 2,300 m in Risaralda

(Galindo-Espinosa et al. 2010; Castaño et al. 2018).

Description and Comparisons. Dorsal pelage may vary from pale to dark brown. Individual hairs of the dor-

sum are tricolored: the base is approximately ¼ of the hair length and dark brown, the middle band is approximately

½ of the length of the hair and varies from buff to pale gray, and the tip is about ¼ of the hair length and varies from

pale to dark brown. Both pairs of facial stripes are conspicuous. The dorsal stripe is conspicuous in approximately

half of the sample (47%, n=8); whereas, it is barely visible in nine specimens. The ear margins and base are paler

than the remainder of the ear conch. The noseleaf has a simple tip, is brown in color, with pale margins on the

horseshoe.

Dimensions of the skull are similar to those of C. trinitatum, and the two species are the smallest Chiroderma

(Tables 7 and 8). Braincase is globose, clearly distinguishable in profile from the frontonasal region. The sagittal

crest is poorly developed and was not detected in 9 of the 17 specimens we scored for this character. The nasal notch

is short and either does not reach the interorbital region, or extends only the level of the anterior border of the orbit.

Similar to C. trinitatum, the post-orbital processes are rhomboid and not pointed as in the other Chiroderma. The

posterior palatine process was absent in 13 of 15 specimens and in the other 2, the process was only a small bump.

When cranium and mandible are in occlusion, a lateral gap is visible, bordered by C, P3, P4, p2 and p4.

The I1s are convergent and their tips are usually in contact. The mandibular condyle is level with or slightly

below the toothrow. The lower canines are relatively narrow and high-crowned, with the crown tip level with the

top of the coronoid process, when viewed laterally. The p2 is in contact with c, but not with p4, or if not in contact

with the lower canine, p2 may be either closer to the lower canine or equidistant from c and p4. The p2 usually is

longer mesiodistally than high and the protoconid is shifted anteriorly, not aligned with the base of the tooth when

viewed laterally (Fig. 27).

Chiroderma gorgasi differs from every other Chiroderma, except C. trinitatum, by its smaller size and nasal

notch usually not reaching the interorbital region. Comparisons with C. trinitatum were made in the previous sec-

tion.

Geographic Variation and Phylogeography. Sequences of three individuals of C. gorgasi were analyzed in

the phylogeny, precluding making inferences on geographical structuring. Within-species variation was 1.04%, the

second highest value in Chiroderma after C. villosum (1.17%).

Subspecies. C. gorgasi is monotypic.

Remarks. Handley (1960) described Chiroderma gorgasi based on five specimens from Panamá and one C.

trinitatum from Trinidad, the type and only known specimen at the time. In the original description, Handley (1960:

465) suggested that, as the sample size increased, the two taxa could prove to be conspecific. Shortly after its de-

scription, C. gorgasi was treated as a subspecies of C. trinitatum, based on their morphological similarity (Barriga-

Bonilla 1965; Jones & Carter 1976; Hall 1981). Simmons (2005) recognized a monotypic trinitatum with gorgasi as

a junior synonym. Recently, Lim et al. (2020) recognized C. gorgasi as a distinct species, because it does not share

a most recent common ancestor with C. trinitatum, and has distinguishing morphological characters.

Natural History. C. gorgasi is a frugivore, specialized on fruits of Ficus (Bonaccorso 1979). Four species of

fruits and infructescences have been recorded in the diet of C. gorgasi: Ficus popenoei , Piper aduncum, Solanum

umbellatum, and Vismia sp. (Bonaccorso 1979; Castaño et al. 2018). The vertical distribution suggests that C.

gorgasi is a canopy and sub-canopy frugivore, more frequently captured in nets between 3 and 12 m above ground

(Bonaccorso 1979).

The few reproductive data for the species suggest a pattern of seasonal polyestry. A pregnant female was cap-

tured in June in Colombia and lactating individuals were recorded in February and March in Panamá. Literature data

for Panamá report pregnancies in February, May and between September and November; whereas lactating females

are documented from May and September (Fleming 1973; Bonaccorso 1979). Births apparently occur toward the

end of the dry season, between February and May, and in the middle of the rainy season, between July and Septem-

ber, when fruits are most abundant.

Specimens Examined (N = 18): Colombia: Antioquia, La Tirana (IAvH-M 917, 934, 974, USNM 499475,

499477, 499479); Chocó, Corregimiento Gilgal (IAvH-M 4932), Finca El Recurso (IAvH-M 3260, 3299, 3323);

Valle del Cauca, Río Zabaletas (USNM 483764). Panamá: Darién, Parque Nacional Darién (ROM 104342), Ta-

carcuna Village Camp (USNM 309902, 309903 [holotype of gorgasi], 309904); San Blas, Armila (USNM 335294,

335296, 335297).

GARBINO ET AL.

Chiroderma improvisum Baker and Genoways, 1976

Synonyms:

Chiroderma improvisum Baker and Genoways, 1976: 1; type locality “Guadeloupe: Basse-Terre; 2 km. S, 2 km. E Baie-Ma-

hault.”

Type Material. The type, TTU 19900 (not seen), is a skin, skull and mandible, collected by R. J Baker and H. H.

Genoways (field number J. C. Patton 552) in July 29, 1974 on the Basse-Terre island, Guadalupe (Baker & Geno-

ways 1976). It is an adult male captured in a mist net set in a pasture adjacent to gallery forest. The karyotype of the

specimen is deposited with the tissue collection of the Texas Tech University under the number TK 8285. The skin,

skull, and mandible were examined by means of photographs and are in good condition.

Distribution and Habitat. The species is known from four islands in the Lesser Antilles: Guadeloupe, Mont-

serrat, Saint Kitts, and Nevis (Fig. 28). There is also a subfossil specimen collected on the island of Marie-Galante,

south of Guadeloupe (Lenoble 2019). Records of C. improvisum are from areas of dry forests and humid forests,

from sea level up to approximately 350 m. The few known specimens were captured in mist nets set over streams, in

gallery forests, in secondary forests surrounded by pasture and plantations, and in urban and peri-urban areas (Baker

et al. 1978; Jones Jr. & Baker 1979; Pierson et al. 1986; Pedersen et al. 2010; Beck et al. 2016). However, a harp

trap set across a dry ravine caught the first specimen of C. improvisum from Nevis (Lim et al., 2020).

FIGURE 28. Collecting localities of the analyzed specimens of Chiroderma improvisum, C. v. villosum and C. v. jesupi. The

locality numbers are referenced in the gazetteer (Appendix 1).

Description and Comparisons. Dorsal pelage varies from grayish to dark brown. Dorsal pelage is long (ap-

proximately 13 mm). Individual hairs of the dorsum are tricolored with a grayish base and buff middle band. The

interocular stripes are weakly developed and the genal pair was not visible in the two skins we examined, but its

presence can be verified in photographs of live animals (Baker & Genoways 1976; Jones Jr. & Baker 1980; Lim et

al. 2020). The dorsal stripe is inconspicuous, visible from the mid dorsum to near base of the uropatagium. The ear

is moderate to dark brown along most of its length; the base is yellowish. The noseleaf is uniformly dark to medium

brown, and the tip may be simple or notched, as evident in the figure in Jones & Baker (1980). The posterior border

of the uropatagium has a V-shaped notch.

The skull of C. improvisum is the largest among Chiroderma (Tables 7 and 8). The braincase is low and slopes

evenly to the frontonasal region in profile. The sagittal and lambdoid crests are conspicuous in both specimens

examined and in the type. The nasal notch extends behind the anterior margin of the orbits (Fig. 29). Post-orbital

processes are distinct, but not pointed. The orbits are relatively small and the posterior margin approximates the

level of the mesial margin of M1 (Fig. 30). A medial accessory foramen between incisive foramina is lacking. There

is no posterior palatine process. When skull and mandible are in occlusion, there is a small lateral gap bordered by

C, P3, p2, and p4 (Fig. 9). In addition, there is a frontal gap surrounded by I1, I2, c, i1, and i2 (Fig. 14).

The I1s are convergent and their tips may or may not be in contact. P3 is separated from P4 by a small gap,

or the two teeth contact each other (Fig. 29). The mandibular condyle is above or level with the tooth row. Lower

canines are relatively short, their tips below the level of the top of the coronoid process. The basal cingulum of the

lower canines is well developed and crowding the lower incisors. The p2 is mesiodistally longer than tall, and is

approximately ⅓ of the height of p4 (Fig. 30). The p2 is in contact with lower canines, either touches p4 or the two

lower premolars are separated by a small gap. The p4 protoconid is robust, with its distal margin sloping evenly to

the tooth’s, not abruptly as in the other species.

FIGURE 29. Dorsal (A) and ventral (C) views of the skull of Chiroderma improvisum (TTU 31403—Montserrat) and dorsal

(B) and ventral (D) views of C. villosum (USNM 520557—Panamá).

Compared with C. doriae, which has a similar size, C. improvisum is larger, has grayish or dark brown dorsal

pelage (medium brown in doriae), faint facial stripes (bright in doriae), and unicolored noseleaf and ears (in doriae

the horseshoe of the noseleaf has pale borders and the ears also have whitish margins). Cranially, C. improvisum

can be diagnosed by its wider nasal notch and by the broader posterior border of the palate, not narrow inverted-U

shaped as in C. doriae. The P3 of C. improvisum is not expanded buccolingually and is in contact with P4, differing

GARBINO ET AL.

from C. doriae in both aspects. The lower canines of C. improvisum are relatively larger than in C. doriae. The p2

of C. improvisum is mesiodistally longer than tall; whereas, in C. doriae, p2 is taller exceeding ⅔ the height of p4.

The p4 of C. improvisum is more robust than in C. doriae, and the protoconid is long mesiodistally. A frontal gap is

present in C. improvisum, but lacking in C. doriae.

FIGURE 30. Skull and mandible, in lateral view, of A) Chiroderma improvisum (TTU 31403—Montserrat) and B) C. villosum

(USNM 520557—Panamá).

The species most similar to C. improvisum in qualitative characters is C. villosum, from which improvisum can

be differentiated by the much larger size, darker pelage (pale brown in villosum), absence of a posterior palatine

process, convergent I1s (parallel and separate in villosum), relatively smaller lower canines (taller and more pointed

in villosum), large p2 in contact with p4 (gap between p2 and p4 in villosum).

Geographic Variation and Phylogeography. The genetic distance between the two specimens of C. improvi-

sum in our molecular analysis was 0.22% (Fig. 4). Due to the small sample, we cannot make inferences either on

geographic structuring or morphological variation in the taxon.

Subspecies. C. improvisum is monotypic.

Natural History. There is no information on the diet of C. improvisum, but it probably feeds on fruits, infruc-

tescences and their seeds, as the other species of Chiroderma. The type was collected approximately 6 m above the

ground and near a forest having a 15-meter-high canopy (Baker et al. 1978), suggesting that the species may be ac-

tive in the canopy as is the closely-related C. villosum. A mite, Periglischrus iheringi (Spinturnicidae), was recorded

on C. improvisum from Saint Kitts (Beck et al. 2016). We lack information on reproduction in C. improvisum.

Specimens Examined (N = 2): Montserrat: Saint Anthony Parish, 0.8 km above mouth of Belham river (TTU

31403). Saint Kitts and Nevis: Saint Thomas Parish (Nevis)¸ Barnes Ghaut (ROM 126002).

Chiroderma villosum Peters, 1860

Synonyms: See under subspecies.

Type Material. The lectotype of Chiroderma villosum (ZMB 408), designated by Thomas (1891), is a stuffed skin.

The skull is inside the skin and the skin around the lips is everted, exposing all of the teeth except M2 and m2. The

free portion of the noseleaf spear is broken. The wing patagia are crumbly and several fragments have fallen off. The

tips of the ears are also crumbly. The skin appears to preserve the original color, the interocular stripes are barely

visible, but the genal pair is not visible. Dorsal pelage is pale brown and three bands can be distinguished: a dark

brown base, and buff middle. The dorsal stripe appears to be lacking.

The I1s are parallel to each other, not in contact, and have slightly diverging tips. The p2 is small and clearly

separated from p4. The forearm measures 47.9 mm. According to Thomas (1891), the individual depicted in Peters’

(1906) plate, published posthumously, is probably the type. In the illustration, the skull is separate from the skin,

suggesting that the skull could have been removed and later re-inserted in the skin (Fig. 31). The other possibility

is that the skull Peters illustrated belonged to the partial skeleton referred to, but not examined by Carter & Dolan

(1978:59).

FIGURE 31. Plate of the lectotype of Chiroderma villosum by Wilhelm Peters, published posthumously.

Distribution. See under subspecies.

Description and Comparisons. Dorsal pelage may be pale brown, dark brown, reddish brown, or grayish

brown. Most of the 328 specimens we examined have a pale brown dorsum (61%, n=201). The second most com-

mon color of the dorsal pelage is dark brown (38%, n=125). Dorsal hairs are tri-banded, the base is always dark

brown, and the middle band is pale buff. Facial stripes were not detected in 191 (58%) of the 328 analyzed speci-

mens. In 36.2% of the sample (n=119), the stripes were detected, but not conspicuous. The interocular pair was

the only pair of facial stripes detected in 82.3% of the specimens, while both pairs were present in 17.7%. Only 13

specimens (3.9% of the sample) had conspicuous facial stripes, with the interocular pair more conspicuous than

the genal. The dorsal stripe was not detected in 152 of 333 specimens (45.6%) scored for this character. The stripe

was faint in 154 specimens (46.2%), and, in some the only evidence of a stripe was a short white mid-dorsal line.

Only 22 specimens (6.6%) had a conspicuous dorsal stripe. Five specimens (1.5%) had a median dorsal stripe, but

they were not scored as to conspicuousness. The tragus and base of the ears are yellow, but the remainder is uni-

formly brownish. The tip of the noseleaf is notched in 49 (74.2%) of the 66 specimens scored for this character. The

noseleaf is nearly uniformly pale brown, with the central rib of the spear having a more pinkish tone and the lateral

margin of the horseshoe slightly paler.

The skull of C. villosum is similar in size to C. d. vizottoi and C. scopaeum, and measurements have some

overlap with small C. d. doriae, C. salvini, and large C. trinitatum (Tables 7 and 8). The braincase is relatively deep

and globose. A sagittal crest is present in 356 (85.5%) of the 416 C. villosum crania scored for this character, and

varied from high and conspicuous to low and inconspicuous. The orbits are relatively large. The nasal notch is long,

extending back into the interorbital region close to post-orbital processes.

A posterior palatine process was present in 280 (83%) of the 336 skulls scored for this character, and varied

from a long and conspicuous to a small nub. When cranium and mandible are in occlusion, a wide lateral gap,

GARBINO ET AL.

bordered by C, P3 and P4, and p2 and p4, is evident (Fig. 9). The occluded teeth also form a W-shaped frontal gap

rimmed by lower canines, lower incisors, and upper inner incisors (Fig. 14).

The I1s were parallel to each other (76.2%, n=314), medially convergent (22.3%, n=92) or divergent (1.4%,

n=6) in the 512 crania scored for this character (Fig. 32). M2 usually has a cingulum around the protocone, which

projects lingually. Lower canines are narrow and tall, with the tips level with the top of the coronoid process when

the mandible is viewed laterally. The crown of p2 is approximately ¼ the height of p4. The p2 is in contact with the

canine, but not with p4. Compared to the other species of Chiroderma, the protoconid of p4 is narrow.

FIGURE 32. Individual variation in the disposition of the inner upper incisors in Chiroderma villosum. A) parallel (USNM

520558, Panamá); B) convergent (USNM 520557, Panamá); C) divergent tips (USNM 540676, Trinidad); and D) base and tips

divergent (USNM 499481, Colombia).

The subspecies C. v. jesupi and C. v. villosum differ in size, with the former averaging smaller in forearm length

and in every cranial dimension we analyzed (Table 9). As previously mentioned, our decision to recognize two

subspecies was mainly due to the presence of haplotypes exclusive to the trans-Andean portion of the distribution

of C. villosum.

The two smallest Chiroderma (C. gorgasi and C. trinitatum) differ from C. villosum by size, presence of con-

spicuous facial and dorsal stripes, bicolored noseleaf, shorter nasal notch, convergent I1s, and taller p2. The insular

C. improvisum is easily distinguished from C. villosum by its larger size, relatively lower braincase, longer rostrum,

more robust dentition, and p2 in contact with p4.

Among similar-sized species, C. villosum can be differentiated by the weaker facial and dorsal stripes (conspic-

uous in C. doriae, C. salvini, and C. scopaeum), paler dorsal pelage (usually darker in C. d. doriae and C. salvini),

notched tip of noseleaf (simple tip in C. doriae, C. salvini, and C. scopaeum), deeper braincase (shallow in C. d.

doriae), longer nasal notch (shorter in C. doriae, C. salvini, and C. scopaeum), larger orbits (smaller in C. doriae,

C. salvini, and C. scopaeum), I1s parallel or divergent (convergent in C. doriae, C. salvini, and C. scopaeum),

smaller p2 (large in C. doriae), narrower and taller canines (wider and shorter in C. doriae and C. scopaeum), and

presence of a frontal gap when cranium and mandible are in occlusion (gap absent in C. doriae, C. salvini, and C.

scopaeum).

Geographic Variation and Phylogeography. Phylogenetic analyses of sequences of COI representing 133 C.

villosum recovered a clade composed of sequences exclusively from México, Central America, and trans-Andean

South America (Figs. 33, 35). The samples from cis-Andean South America, however, form a polytomy, which does

not suggest geographic structuring because specimens from distant regions, such as Bolivia and Trinidad, group

together.

FIGURE 33. Haplotype network of Chiroderma villosum and C. improvisum, built using the “Median Joining” algorithm (ep-

silon = 0; 2,000 iterations).

There is geographic variation in size among the subpopulations of C. villosum. Specimens from the Atlantic

rainforest of eastern Brazil (n=48) are larger than the other geographic groups (Table 13, Fig. 34). Specimens from

Trinidad and Tobago also had larger dimensions; however, the sample size was smaller (n=7). Populations from

the Amazon north of the Amazonas River and from México and Central America and trans-Andean South America

had the smaller dimensions. We suggest there is clinal variation in size, with larger specimens in the extreme east

and southeast part of the distribution and smaller individuals in the northwestern part of the range. There is overlap

between measurements from adjacent geographic groups, but the populations from the western portion of the distri-

bution, which would correspond to subspecies C. v. jesupi, are significantly smaller than the others (Fig. 34).

Subspecies. We recognize two subspecies in Chiroderma villosum.

GARBINO ET AL.

FIGURE 34. Predefined groups of C. villosum used in the geographic variation analysis (above). Boxplot of the first princi-

pal component (PC1), extracted from the variance-covariance matrix of a principal component analysis of 13 cranio-dental

measurements (below). A = México/Central America/trans-Andean South America; B = northern Venezuela; C = Trinidad and

Tobago; D =northern Amazonia and the Guianas; E = Southern Amazonia; F = Chaco and Cerrado; G = Atlantic coast.

FIGURE 35. Phylogenetic relationships between Chiroderma improvisum and C. villosum, based on 141 sequences of the cyto-

chrome c oxidase subunit 1 gene. Localities in parentheses are detailed in the gazetteer (Appendix 1). This subtree is a detailed

version of the clades named “improvisum” and “villosum” in figure 4.

GARBINO ET AL.

TABLE 13. Loadings of the first and second principal components, extracted from the variance-covariance matrix of a

principal component analysis of 13 cranio-dental measurements of Chiroderma villosum.

Measurements PC 1 PC 2

GLS 0.91 -0.01

CIL 0.93 0.00

CCL 0.94 -0.02

PB 0.66 0.21

BB 0.68 0.08

MB 0.82 -0.07

ZB 0.89 0.07

MTRL 0.90 0.09

M1–M1 0.88 0.30

M2–M2 0.88 0.28

MANDL 0.89 0.09

DENL 0.90 -0.07

CAL 0.77 -0.61

Eigenvalues 9.50 0.62

Proportion of variation 73.10% 4.79%

C. v. villosum Peters, 1860

Synonyms:

Chiroderma villosum Peters, 1860:748; type locality “Brasilia.”

Chiroderma villosa Jones, 1951: 224; incorrect gender concordance.

Chiroderma villosum villosum: Handley, 1960:466; first use of current name combination.

Chiroderma trinitatum: Pirlot, 1972: 76, not Chiroderma trinitatum Goodwin, 1958.

Chiroderma sp. Nowak, 1994: 160.

Chiroderma salvini Nowak, 1994: 160, not Chiroderma salvini Dobson, 1878.

Chiroderma [sp.] Czaplewski & Cartelle, 1998: 794. see Garbino & Tavares (2018a)

Chiroderma salvini: Medina et al., 2015: 204, not Chiroderma salvini Dobson, 1878.

Chiroderma salvini: Rocha et al., 2016: 573; not Chiroderma salvini Dobson, 1878.

Chiroderma salvini: Maas et al., 2018: 672; not Chiroderma salvini Dobson, 1878.

Distribution and Habitat. The nominal subspecies, C. v. villosum, is known from the tropical region of cis-Andean

South America. The taxon has been recorded in Colombia, Venezuela, Trinidad and Tobago, Guyana, Suriname,

French Guiana, Brazil, Ecuador, Perú, and Bolivia (Fig. 28). The southern limit of the subspecies is in the Brazilian

state of Paraná (not mapped; Reis et al. 1998).

The subspecies occurs in a wide variety of environments, including humid and seasonal forests (e.g. Amazonia,

Atlantic rainforest), flooded plains (e.g. Pantanal, Llanos), and dry formations (e.g. Caatinga, Cerrado) (Handley

1976; Gregorin et al. 2008; Luz et al. 2011; Fischer et al. 2015). C. v. villosum apparently tolerates some habitat

disturbance, as it occurs in small forest fragments and urban areas (Nogueira & Peracchi 2003; Ferreira et al. 2010;

Nunes et al. 2017).

Chiroderma villosum villosum occurs from sea level to approximately 1,000 m. In Venezuela, 99% of the speci-

mens of C. v. villosum were captured below 500 m (Handley 1976). In the Peruvian Amazonia (Madre de Dios), the

species was recorded between 340 and 950 m (Solari et al. 2006).

C. v. jesupi Allen, 1900

Synonyms:

Chiroderma jesupi Allen, 1900: 88; type locality “Cacagualito, Colombia.”

Chiroderma isthmicum Miller, 1912: 25; type locality “Cabima, Panama.”

Chiroderma isthmica Hall and Jackson, 1953: 645; incorrect gender concordance.

Chiroderma villosum jesupi: Handley, 1960:466; first use of current name combination.

Distribution and Habitat. The subspecies C. v. jesupi occurs in the tropical region of trans-Andean South America

and also in Central America and México. The taxon has been recorded in México (Oaxaca, Hidalgo, Veracruz, and

states to the south), Guatemala, Belize, El Salvador, Honduras, Nicaragua, Costa Rica, Panamá (including Islas

Perlas), western Colombia, western Ecuador, and extreme northwestern Perú (Tumbes; Fig. 28).

Collecting sites of C. v. jesupi are in dry and humid tropical forests. The taxon has been recorded from sea

level up to approximately 970 m. In northwestern Perú (Tumbes), specimens were captured at 350 m (Novoa et al.

2011). In Colombia (Tolima), the taxon was captured at 900 m (Galindo-Espinosa et al. 2010). In southern México

(Chiapas), the maximum capture elevation was 915 m (Davis et al. 1964).

Remarks. The original description of Chiroderma villosum was based on specimen ZMB 408 and on a skeleton

from the anatomical collection of the Berlin museum that is probably lost (Turni & Kock 2008; Garbino & Nogueira

2017). From the two syntypes, Turni & Kock (2008: 44) selected specimen ZMB 408 as the lectotype, but Thomas

(1891: 882) had already designated the same specimen, i.e. the one represented in Peters’ plate, as the lectotype.

In the species description, Peters (1860: 748) mentioned only “Brasilia” as the locality and suggested that the

lectotype was collected by Friedrich Sellow. In the collection catalogue of the Museum für Naturkunde, the local-

ity of the specimen, handwritten by Peters reads just “Brasilien”, and there is no note indicating who collected it

(Garbino & Nogueira 2017). Due to the impossibility to further restrict the type locality and the lack of evidence

that it was indeed collected by Sellow, we follow most authors in citing “Brazil” as the type locality of Chiroderma

villosum (Handley 1960; Husson 1962; Carter & Dolan 1978; Simmons 2005; Gardner 2008a; Turni & Kock 2008;

Garbino & Nogueira 2017).

Cabrera (1958: 85) erroneously designated “Venezuela” as the type locality of Chiroderma villosum, followed

by Goodwin & Greenhall (1961), and probably by Vieira (1942, 1955), who did not include the species among the

Brazilian mammals. Cabrera may have altered the type locality based on the mention of a specimen from St. Este-

ban, Venezuela by Thomas (1891: 56), which was the first subsequent precise locality reported for the species.

Natural History. C. villosum is a secondarily granivorous frugivore, specializing in chewing the seeds of fruits

of Ficus to extract nutritive content (Nogueira & Peracchi 2003; Wagner et al. 2015). The species apparently has

preference for Ficus, and fruits of this genus may compose 100% of the diet of C. villosum in Panamá (Bonaccorso

1979). Nine species of Ficus have been recorded in the diet of C. villosum in Panamá: Ficus citrifolia, F. dugandii,

F. insipida, F. nymphaefolia, F. obtusifolia, F. paraensis, F. pertusa, F. popenoei, and F. trigonata (Bonaccorso 1979;

Handley et al. 1991; Wendeln et al. 2000; Wagner et al. 2015). Consumption of infructescences of Cecropia obtusa

was recorded in the diet of C. villosum from French Guiana (Lobova et al. 2003; Suárez-Castro & Montenegro

2015). C. villosum have been captured at mineral-rich clay licks (“collpas”) in the Peruvian Amazon (Bravo et al.

2008; Ghanem & Voigt 2014).

In the Guianas, Amazonia, and in the Atlantic rainforest, the species was captured more frequently in the

canopy, suggesting that C. villosum is a canopy frugivore (Ascorra et al. 1996; Simmons & Voss 1998; Charles-

Dominique & Cockle 2001; Kalko & Handley Jr. 2001; Delaval et al. 2005; Gregorin et al. 2017). The only natural

day roost recorded for the species are tree hollows in Venezuela (Handley 1976). In addition to natural shelters, C.

villosum has been found in buildings in Brazil, Panamá, and Venezuela (Goldman 1920; Handley 1976; data from

the DZSJRP collection catalogue).

The following ectoparasites have been documented on C. v. jesupi: Aspidoptera busckii (Streblidae), Tricho-

bius joblingi (Streblidae), Paratrichobius sp. A (Wenzel et al. 1966). In Venezuela, two species of streblid bat flies

(Trichobius parasiticus and Metelasmus pseudopterus), two spinturnicid mites (Periglischurus acustidens and P.

iheringi), and a species of trombiculid mite (Whartonia nudosetosa), are known from C. v. villosum (Herrin & Tip-

ton 1975; Reed & Brennan 1975; Wenzel 1976). Marinkelle & Grose (1981) recorded Megistopoda proxima and

Strebla carolliae, two species of streblid bat flies from Colombian C. villosum. The absence or rarity of spinturnicid

mites on C. villosum was noted in some studies: in Panamá no mite was recorded on any specimen, in the Peru-

vian Amazon no mite was collected from 33 specimens, and only two mites were collected from a sample of 724

Venezuelan C. villosum (Furman 1966; Herrin & Tipton 1975; Gettinger 2018). Two flesh fly larvae of the genus

Sarcophaga (Sarcophagidae), were found in the abdominal cavity of a freshly-dead female, suggesting that they

parasitized the live animal (Goodwin & Greenhall 1961).

Blood parasites of the family Trypanosomatidae, subfamily Leishmaninae, are known from C. v. villosum from

GARBINO ET AL.

central Brazil, and Trypanosoma (Schizotrypanum) is documented in this species from Colombia (Marinkelle 1982;

Lourenço et al. 2018). One C. v. villosum from southeastern Brazil had traces of hantavirus infection, making C.

villosum one of the few species of frugivorous bat to host this virus (Sabino-Santos et al. 2015).

Reproductive data from specimens we examined and from the literature (Davis et al. 1964; Jones et al. 1971;

Taddei 1976; Bonaccorso 1979; Anderson 1997) suggest seasonal polyestry. In Central America (Nicaragua and

Panamá), pregnant females were recorded in January, February, and March, just before the beginning of the rainy

season, and lactating C. villosum were found in February, March, and April. In South America, pregnancies were

also recorded before the rainy season in July and August (Rondônia, Brazil) and in August and September (Boliv-

ian, Ecuadorian, and Peruvian Amazon). In southeastern Brazil (São Paulo), C. villosum were recorded as pregnant

in July and August. In Venezuela, pregnancies were recorded both before the rainy season in January, February,

March, and April, and during the rainy season in June, and July; whereas, lactating individuals were documented in

February, June, and July.

Specimens Examined (N = 509): Belize: Toledo, Bladen Nature Reserve (USNM 583035, 583036). Bolivia:

Beni, Río Iténez (AMNH 209529–209533), Vacadiaz (USNM 390606); La Paz, Santa Ana de Madidi (AMNH

261677); Pando, Independencia (AMNH 262526–262529), Río Nareuda (248884, 248885); Santa Cruz, Buenavis-

ta (AMNH 61754), Parque Nacional Noel Kempff Mercado (AMNH 264078, 264079). Brazil: without specific

locality (ZMB 408 [lectotype of villosum]); Acre, Seringal Lagoinha (DZSJRP 13029–13033), Parque Nacional da

Serra do Divisor (ALP 7011, 7018, 7022, 7023, 7050, 7059, 7160, 7308); Alagoas, Mata de Coimbra (UFPB 4349);

Amazonas, Comunidade Cachoeirinha (LMUSP[ICA048]), Humaitá (DZSJRP 14793), Igarapé Taracuá

(LMUSP[JAP76]), km 27 of BR319 (DZSJRP 14121, 14651), km 5 of BR230 (DZSJRP 13134), opposite to Comu-

nidade São Pedro (LMUSP[ICA169], LMUSP[ICA170]), Vila de Santa Fé (LMUSP[JAP84]); Bahia, Ilhéus (CMU-

FLA 1076, 1078, 1119); Espírito Santo, Aracruz Celulose (MZUSP 35032), Fazenda Santa Terezinha (MZUSP

35030, 35031), Reserva Natural Vale (ALP 2806, 2810, 3009, 3249, 3327, 3408, 4560, 4758); Mato Grosso, 264 km

N Xavantina (USNM 393712–393714), Aricá (MZUSP 6494), Cláudia (MZUSP[PEV 1225-1226]), Nossa Senhora

do Livramento (UFMT 1146, 1147), Parque Nacional do Juruena (CMUFLA 1290, 1299), Sinop (ALP 3419),

U.H.E. foz do Apiacás (UFMT 1952, 1953), Usina Teles Pires (UFMT 2137, 2138); Mato Grosso do Sul, Estação

Ecológica Dahma (ZUFMS 492), Maciço do Urucum (ZUFMS 208, 209), Pantanal de Aquidauana (ZUFMS 1904),

Pantanal de Nhecolândia (ZUFMS 244, 1896); Minas Gerais, Dores do Indaiá (UFMG 3760), Estação Ecológica de

Pirapitinga (ALP 9166, 9370), Fazenda Cabriúna (CMUFLA 465), Fazenda Marinheiro (DZSJRP 14480), Parque

Nacional do Peruaçu (CMUFLA 907, 1532–1536, 1676–1678, 1680, 1682, 1684, 1686), Parque Estadual do Rio

Doce (CMUFLA 1158, 1161, 1834, 1839–1841); Pará, 52 km SSW Altamira (MZUSP 22677), Centro Kaiapó de

Estudos Ecológicos (MZUSP 29150–29152), Floresta Nacional de Carajás (UFMG[VCT6305]), Floresta Nacional

de Carajás, Serra Norte (UFMG[VCT2303]), Floresta Nacional de Carajás, Serra Sul, Corpo A (UFMG[VCT1959],

UFMG[VCT5157]), Floresta Nacional de Carajás, Serra Sul, Corpo C (UFMG[VCT2019], UFMG[VCT5073],

UFMG[VCT5079]), Lago Jacaré (MZUSP 13335), Lago Leonardo (MZUSP 13209, 13197), Platô Greig (UFMG

3258), Platô Monte Branco (UFMG 3244), Porto Trombetas (UFMG 3212, 3214, 3221, 3246), Projeto Alemão

(UFMG[VCT4394], UFMG[VCT4444]), Rio Xingu, left bank (MPEG 4112), Sta. A, IAN (USNM 361724, 361725),

Várzea, Belém (USNM 460128–460130); Paraíba, Fazenda Pacatuba (UFPB 4), João Pessoa (UFPB 10333, 10335,

10336); Pernambuco, Recife (UFMG[M1], UFMG[M2], UFMG[M3]); Piauí, Boqueirão da Esperança (ZUEC

2066), Parque Nacional da Serra das Confusões (MZUSP 33502); Rio de Janeiro, Jardim Botânico (ALP 7419–

7424, 7426–7431, 8278), Parque Estadual Serra da Tiririca (ALP 5578, 5579); Rondônia, Calama (AMNH 37041),

Costa Marques (AMNH 209575), Pedra Branca (MZUSP 22827), Pedras Negras (AMNH 209576), Cachoeira de

Nazaré, Rio Machado (MZUSP 20200, 20201), U.H.E. Jirau (MZUSP 35408); Roraima, Estação Ecológica da Ilha

de Maracá (DZSJRP 11487); São Paulo, São José do Rio Preto (DZSJRP 4586, 4676), Engenheiro Schmidt (DZS-

JRP 4804), Fazenda São Paulo (DZSJRP 14302, 14305, 14319), Roberto (DZSJRP 16549), Parque Natural Mu-

nicipal Grota de Mirassol (DZSJRP 4000, 4032, 4033), Fazenda Paraguassu (ZUEC 968), Sítio Progresso (DZSJRP

3783, 3922, 4337, 4386–4390); Sergipe, Estação Ecológica de Itabaiana (CMUFS 64), Mata do Junco (CMUFS 97),

Parque Nacional Serra de Itabaiana (ALP 8971); Tocantins, U.H.E. São Salvador (MZUSP[SSI178]). Colombia: no

specific locality (USNM 598086); Amazonas, Puerto Nariño (USNM 483777); Antioquia, La Tirana (IAvH-M 930,

USNM 449480–499482), Vereda La Pola, Parque Nacional Natural Los Katíos (IAvH-M 4923); Chocó, Cor-

regimiento Gilgal, P.N.N. Los Katíos (IAvH-M 4924–4926), Reserva Florestal Especial Las Teresitas (IAvH-M

3257), Vereda El Tilupo, P.N.N. Los Katíos (IAvH-M 4927–4929); Magdalena, Cagualito (AMNH 14574 [holotype

of jesupi]), Parque Nacional Natural Tayrona (IAvH-M 4198), Vereda El Congo (IAvH-M M-9665); Putumayo,

Caño Caucayá (IAvH-M M-624); Sucre, Estación Primates (IAvH-M 9583), Quebrada El Sereno (IAvH-M 9593);

Valle del Cauca, Río Zabaletas (USNM 483770–483776); Vaupés, Caño Arara (IAvH-M 1550). Costa Rica: Pun-

tarenas, Corcovado National Park (USNM 565813). El Salvador: La Libertad, Deininger Park (TTU 63906); La

Paz, Hacienda Escuintla (TTU 63911); La Unión, El Tamarindo (TTU 63912). Ecuador: Los Ríos, Beata Elvira

(USNM 498921, 498922), El Papayo (USNM 498923, 522435–522437), Hacienda Santa Teresita (USNM 522438),

Lima Pareja (USNM 498924, 498925, 522434), Río Nuevo (USNM 534315, 534316), Vinces (USNM 534314);

Pastaza, Lorocachi (USNM 548240, 548241), Santiago (not located; USNM 548242), Tiguino (USNM 574537,

574539), Yosa (not located, USNM 548237–548239); Pichincha, Río Palenque Science Center (USNM 528541).

Guatemala: Jutiapa, Colonia Montufar (AMNH 217417), Santa Rosa, La Avellana (AMNH 235312–235315).

Guyana—Barima-Waini, North West, Santa Cruz (ROM 98850); Cuyuni-Mazaruni, 24 km along Potaro road from

Bartica (BMNH 1965.645), Namai Creek (ROM 108219); Upper Demerara-Berbice, Dubulay Ranch (USNM

582328); Upper Takutu-Upper Essequibo, Chodikar River (ROM 106644). French Guiana: Sinnamary, Paracou

(AMNH 267190, 267191, 268534–268536). México: Veracruz, Xalapa (= Jalapa) (BMNH 81.10.27.1). Nicara-

gua—Zelaya (currently Región Autónoma de la Costa Caribe Sur), 4,5 km NW Rama (TTU 12794). Panamá—Bo-

cas del Toro, Almirante (USNM 315559–315562), Isla Popa (USNM 464304), Sibube (USNM 335298, 335299);

Colón, Bohio Peninsula (USNM 503637); Darién, Cana (USNM 179619), El Real (USNM 338045), Jaqué (USNM

362920), Punta Piña (USNM 314718), Tacarcuna Village Camp (USNM 309894, 309896–309900); Los Santos,

Cerro Hoya (USNM 323451–323453), Guánico Arriba (USNM 323448–323450); Panamá, Barro Colorado Island

(USNM 304904, 304905, 304907–304909, 332053, 457954, 544896), Cabima (USNM 173834 [holotype of isthmi-

cum], USNM 173836), Cerro Azul (USNM 305386), Culebra (USNM 223402), Gamboa (USNM 520557, 520558),

Isla San José (USNM 448449), Punta de Cocos (USNM 314719, 314720, 314721), Río Mandinga (USNM 305385);

San Blas (currently Guna Yala), Armila (USNM 335300–335316); Veraguas, Isla Cébaco (USNM 360219). Perú:

Cusco, Camisea (USNM 582836), Camisea, Armihuari (MUSM 13606, 13631, 13634, 13636, 13637, 13639–

13641), Camisea, Konkariari (MUSM 14742), Camisea, Pagoreni (MUSM 13610, 13615, USNM 582839), Cami-

sea, San Martín (MUSM 13618, 13644, USNM 582840, 582841), Jenaro Herrera (MUSM 6791), Ridge Camp

(USNM 588033); Loreto, 13,6 km NW Albarenga (MUSM 26545), Alto Río Pauya (MUSM 17734), Centro de In-

vestigaciones Jenaro Herrera (MUSM 4221, 4222), Estación Biologica Allpahuayo (MUSM 16476), Ninarumi

(MUSM 29560, 29561), Paujil (MUSM 29562), Puesto de Vigilancia Castaña (MUSM 21136), Quistococha (USNM

337940), Río Lagartococha (MUSM 21137), Río Pisqui, Campamento Llanura (MUSM 17735), Río Samiria

(MUSM 29562), Río Samiria, Flor de Yarina (MUSM 1637), Río Samiria, Tacshacocha (MUSM 1638, 1639), San

Lorenzo (BMNH 1924.3.1.75, 1924.3.1.76), Zungarococha (MUSM 29563); Madre de Dios, CICRA (MUSM

26106), Cocha Salvador (MUSM 733), Estación Biológica Cocha Cashu (MUSM 15856), Explorer’s Inn Lodge

(MUSM 1640), Hacienda Amazonia (MUSM 9757), Maskoitania (MUSM 19671), Pakitza (MUSM 6781, USNM

566544), Quebrada Aguas Calientes (MUSM 16653, 16660, 16661, 16665–16667), Reserva Cuzco Amazónico

(MUSM 6168, 6169), Santuario Nacional Pampas del Heath (MUSM 12827); Pasco, Campamento Río Lobo

(MUSM 10232), Cerro Chontiya (MUSM 10225, 10230, 10231), San Juan (USNM 364418), Villa America (MUSM

1641); San Martín, Concesion de Conservación Valle del Biavo (MUSM 43843, 43844, 43485), Juanjuí (MUSM

1642), Saposoa (MUSM 1643), Yurac Yacu (BMNH 27.1.1.63); Tumbes, Carrizalillo (MUSM 22123), Parque Na-

cional Cerros de Amotape (MUSM 22121, 22122), Quebrada Las Pavas (MUSM 24479); Ucayali, 59 km W Pu-

callpa (USNM 461256), Concesión de Conservación Río La Novia (MUSM 44186, 44187, 44472). Suriname:

Brokopondo, Brownsberg Nature Park (ROM 114212); Sipaliwini, Kushere Landing (ROM 120226). Trinidad and

Tobago: Tobago, Charlotteville (USNM 540676); Trinidad, without specific locality (AMNH 256325), Diego Mar-

tin (AMNH 183167), Grande Riviere (AMNH 172149), Guaico Tamana (AMNH 172148), Maracas Valley (AMNH

175599), Waterloo (BMNH 1897.6.7.44). Venezuela: Amazonas, 9 km SE Puerto Ayacucho (MZUSP 27168), Cer-

ro Neblina base camp (USNM 560606, 560607, 560767, 560768, 560769, 560770, 560771, 560772), Río Cu-

nucunuma (USNM 405127, 405165, 405167–05171), Río Manapiare (USNM 408624–408660, 408662–408678),

Río Mavaca (USNM 405175), San Carlos de Rio Negro (USNM 560604, 560605), Tamatama (USNM 405176,

405177, 408611–408617); Bolívar, El Manaco (USNM 387205–387209, 387212, 387213, 387126, 387210, 387211,

387214, 387215), Hato La Florida (USNM 405164), Hato San José (USNM 405162), Río Supamo (USNM 387204);

Sucre, Manacal (USNM 408620); Yaracuy, 19 km NW Urama (USNM 372145, 372146, 372149, 372150).

GARBINO ET AL.

Key to the species and subspecies of genus Chiroderma

1 Size small, forearm equal to or less than 42 mm, greatest length of skull equal to or less than 23 mm . . . . . . . . . . . . . . . . . . . 2

- Size intermediate to large, forearm equal to or more than 43 mm, greatest length of skull equal to or more than 23 mm ......

...................................................................................................3

2 First lower premolar longer than high mesiodistally; third cuspid of first lower premolar absent; crown of lower canine at the

same level or higher than the tip of the coronoid process of the mandibular bone . . . . . . . . . . . . . . . . . . . . Chiroderma gorgasi

- First lower premolar higher than long mesiodistally; third cuspid of first lower premolar present; crown of lower canine clearly

below the level of the top of the coronoid process of the mandibular bone . . . . . . . . . . . . . . . . . . . . . . . . Chiroderma trinitatum

3 Size large, length of forearm equal to or more than 56 mm, greatest length of skull equal to or more than 28 mm; first lower

premolar in contact with the lower canine and second premolar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Chiroderma improvisum

- Size intermediate to large, forearm length equal to or less than 54 mm (43–54 mm), greatest length of skull usually equal to or

less than 28 mm (23–28 mm); diastema between first lower premolar and second lower premolar . . . . . . . . . . . . . . . . . . . . . . 4

4 Size large, forearm length 47–54 mm, greatest length of skull 26–29 mm; dorsal pelage brown or dark brown; basal and termi-

nal bands of the dorsal hairs of a same color ................................................................ 5

- Size intermediate, forearm length 43–50 mm, greatest length of skull 23–26 mm; dorsal pelage brown, light brown or buff; base

of dorsal hairs darker than terminal band ................................................................... 6

5 First lower premolar large, with approximately ⅔ the height of second lower premolar; crown of lower canine clearly below the

level of the top of the coronoid process of the mandibular bone; paraoccipital processes present . . . . . . . . . . . . . . . . . . . . . . . .

...............................................................................Chiroderma doriae doriae

- First lower premolar small, with approximately ¼ the height of second lower premolar; crown of lower canine approximately

the same height as the top of the coronoid process of the mandibular bone; paraoccipital processes absent . . . . . . . . . . . . . . . .

.....................................................................................Chiroderma salvini

6 Tip of noseleaf unnotched; facial stripes bright and conspicuous; posterior process of the palate absent; first upper incisors with

convergent tips .......................................................................................7

- Tip of noseleaf notched; facial stripes dark and inconspicuous; posterior process of the palate present; first upper incisors with

parallel or divergent tips ................................................................................8

7 Length of forearm usually more than 48 mm (45–50 mm); greatest length of skull equal to or more than 25 mm (25–27 mm);

high-crowned first lower premolar (⅔ the height of second lower premolar; low-crowned lower canine, with the tips clearly

below the level of the top of the coronoid process of the mandibular bone . . . . . . . . . . . . . . . . . . . . Chiroderma doriae vizottoi

- Length of forearm equal to or less than 47 mm (43–47 mm); greatest length of skull equal to or less than 25 mm (23–25 mm);

low-crowned first lower premolar (¼ the height of second lower premolar); high-crowned lower canine, with the tips approxi-

mately the same height as the top of the coronoid process of the mandibular bone . . . . . . . . . . . . . . . . Chiroderma scopaeum

8 Length of forearm 46 mm on average (41–52 mm); distributed east of the Andes ........... Chiroderma villosum villosum

- Length of forearm 44 mm on average (41–47 mm); distributed west of the Andes .............Chiroderma villosum jesupi

Acknowledgements

We are thankful to Adriano Peracchi, Luiz Gomes, Marcelo Nogueira, and Daniela Dias (ALP-UFRRJ), Sara Ke-

telsen and Robert Voss (AMNH), Roberto Portela (BMNH), Eliana Morielle-Versute (DZSJRP), Alexandre Per-

cequillo (ESALQ-USP), Andrés Cuervo and Maria del Socorro Sierra (IAvH), Jake Esselstyn and Donna Dittman

(LSU), Victor Pacheco (MUSM), Juliana Gualda, Mario de Vivo, and Luis F. Silveira (MZUSP), Claudia Costa

and Cástor Cartelle (PUC-MG), Heath Garner (TTU), Renato Gregorin (UFLA), Fernando Perini (UFMG), Gus-

tavo Graciolli and Thomaz Sinani (UFMS), Rogerio Rossi and Thiago Semedo (UFMT), Pedro Estrela, Anderson

Feijó, and Hannah Nunes (UFPB), Adriana Bocchiglieri, Patricio A. Rocha, and Raone Beltrão-Mendes (UFS),

Alfred Gardner, Suzanne Peurach and Darrin Lunde (USNM), Christiane Funk and Frieder Meyer (ZMB), and

Karina Rebelo and Ivan Sazima (ZUEC), for allowing us to examine specimens under their care. We also thank

Bruce Patterson (FMNH), Gerson Lopes and João Valsecchi (IDSM), Leonardo Trevelin and José de Souza e Silva-

Júnior (MPEG), Livia Paniagua and Giovani Hernández-Canchola (MZFC), Franger Garcia and Mariana Jaramillo

(MZUC), Ana Pavan (USP), and Bruna Fonseca and Albert Ditchfield (UFES), for providing tissue samples. We

are grateful to Giuliano Doria and Cristina Macciò for sending a digital copy of the Chiroderma villosum plate of

Peters. GSTG would like to thank Alfred Gardner and Marcelo Nogueira for the valuable discussions on the subject

of this paper. We would like to thank also Ana Paula Carmignotto Daniel Casali, Gisele Kawauchi, Livia Loureiro,

Ligiane Moras, Maria Clara Nascimento Costa, and Paul Velazco for the suggestions and comments on an early ver-

sion of this paper. DNA sequencing was done by Kristen Choffe and Maria Clara Nascimento Costa in the Labora-

tory of Molecular Systematics at the Royal Ontario Museum. Alfred Gardner and one anonymous referee provided

very helpful comments and suggestions on an earlier version of this paper and Paul Velazco kindly translated the

abstract to Spanish. GSTG received a predoctoral fellowship from the Coordenação de Aperfeiçoamento de Pes-

soal de Nível Superior, Brazil (CAPES; Code 001). VCT was funded by the Programa Nacional de Pós Doutorado

(PNPD/CAPES; Code 001, 2014-2018) during most of the period of her mentorship of GSTG.

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Systematics of big-eyed bats, genus Chiroderma Peters, 1860 (Chiroptera: Phyllostomidae)

Abstract and Figures