ZOOTAXA

ISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)Copyright © 2013 Magnolia Press

Zootaxa 3718 (3): 267–276

www.mapress.com/zootaxa/Article

http://dx.doi.org/10.11646/zootaxa.3718.3.3

http://zoobank.org/urn:lsid:zoobank.org:pub:F25FFE68-1F6B-4144-9326-CE20E57F4EDC

On the phylogenetic position of Carollia manu Pacheco et al., 2004

(Chiroptera: Phyllostomidae: Carolliinae)

PAÚL M. VELAZCO1, 2

1Department of Mammalogy, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA.

E-mail: pvelazco@amnh.org2Science & Education, Field Museum of Natural History, 1400 S. Lake Shore Drive, Chicago, IL 60605, USA

Abstract

The Neotropical bat genus Carollia (Phyllostomidae: Carolliinae) currently includes eight species. Carollia manu was de-

scribed in 2004 and is distributed in montane forests in southern Peru and Bolivia. The phylogenetic affinities of C. manu

have never been assessed before. Phylogenetic analyses of cytochrome b sequences of seven of the eight known species

of the genus place C. manu sister to C. subrufa. The analyses also suggest hidden diversity in the genus.

Key words: Carollia, Neotropics, Phyllostomidae, Phylogeny, Systematics

Introduction

The Neotropical bat genus Carollia Gray, 1838 includes some of the most abundant species of mammals found in the Neotropics, where they play important roles in seed dispersal and forest regeneration (Fleming 1988; Lim & Engstrom 1998). This genus of small to medium-sized bats (forearm 33.7–44.6 mm, greatest length of skull 18.7–23.5 mm; Solari & Baker 2006; McLellan & Koopman 2008) is distributed from central Mexico to southern Brazil (Simmons 2005; McLellan & Koopman 2008). The genus Carollia currently includes eight species: C. benkeithi

Solari and Baker, 2006; C. brevicauda (Schinz, 1821); C. castanea Allen, 1890; C. manu Pacheco et al., 2004; C.

monohernandezi Muñoz et al., 2004; C. perspicillata (Linnaeus, 1758); C. sowelli Baker et al., 2002; and C.

subrufa (Hahn, 1905).The most extensive revision of the genus was performed by Pine (1972). He recognized four species (C.

brevicauda, C. castanea, C. perspicillata, and C. subrufa). Additionally Pine (1972) suggested that some specimens that he was unable to assign to the four aforementioned species could represent undescribed species (i.e., Carollia sp.? (1), Carollia sp.? (2), Carollia sp.? (3), and Carollia sp.). McLellan (1984) extended Pine’s (1972) work by using morphometric techniques, including multivariate analyses, to examine geographic and nongeographic variation in cranial morphology. McLellan (1984) found that all the species included in her analyses (C. brevicauda, C. castanea, C. perspicillata, and C. subrufa) were easily separated by the multivariate analyses; additionally she found that sexual dimorphism was present in all species, where males were consistently larger than females.

During the past decade, the systematics of the genus has changed dramatically: C. benkeithi and an undescribed species were recognized from populations usually assigned to C. castanea (see Solari & Baker 2006); C. colombiana Cuartas et al. 2001 was described from specimens from northern Colombia, but later synonymized with C. brevicauda (see Zurc & Velazco 2010); C. manu Pacheco et al. 2004, the Carollia sp.? (3) of Pine (1972), was described from montane forests in southern Peru and Bolivia (Fig. 1); C. monohernandezi Muñoz et al. 2004 was described from several localities in Colombia, but later restricted to the type locality—Colombia: Caquetá, Florencia, Villaraz (Zurc & Velazco 2010); and C. sowelli Baker et al. 2002 was described to include Central American populations north of central Panama that had been previously assigned to C. brevicauda.

Several hypotheses of phylogenetic relationships of the species of Carollia have been published in different

Accepted by M. Weksler: 16 Sept. 2013; published: 4 Oct. 2013 267

contexts: phylogeographic studies (Hoffmann & Baker 2003; Pavan et al. 2011), systematics (Wright et al. 1999), and the description of new species (Baker et al. 2002; Solari & Baker 2006). The five aforementioned studies used the mitochondrial cytochrome b to reconstruct the phylogenetic relationships and found similar results. Two major clades were recovered: one including the smaller species (i.e., C. benkeithi and C. castanea), while the other clade contained the medium to large species (C. subrufa, (C. sowelli, (C. brevicauda + C. perspicillata))).

As a product of the 1999–2001 Field Museum Manu Biosphere Reserve expeditions, several individuals of Carollia manu were collected (Solari et al. 2006). In this paper, I use some of these specimens to place C. manu in a phylogenetic context in order to improve our understanding of the evolution and diversification of this ecologically important group.

FIGURE 1. Photograph of an adult male Carollia manu captured at Pampa Grande, Ayopaya, Cochabamba, Bolivia, in

September 2006 (MHNC-M 149 [Museo de Historia Natural Alcide d'Orbigny, Cochabamba, Bolivia]). Photograph by Lizette

Siles.

Material and methods

To evaluate the phylogenetic position of Carollia manu among other species of the genus, I sequenced the complete cytochrome b gene of two specimens from southern Peru meeting the morphological description of C.

manu: large size, long fur, broad rostrum, flattened anterorbital region, broad interorbital region, massive upper and lower premolars and molars, first upper premolar broadly in contact with the canine. I also sequenced additional specimens from Peru corresponding to other species of the genus. In addition, Cytb sequences of Carollia used in the analysis of Wright et al. (1999), Hoffmann and Baker (2003), Solari and Baker (2006), Velazco and Patterson (2008), Pavan et al. (2011), McDonough et al. (2011), and Velazco and Patterson (2013) were obtained from GenBank. Glyphonycteris silvestris, Rhinophylla fischerae, and Trinycteris nicefori were used as outgroup taxa to root the trees. The locality and voucher information of the sequences produced in this study, GenBank accession nos. KF019701–KF019724, together with the sequences from other studies (GenBank accession nos. AF187023–AF187024, AF511951–AF512006, DQ177279–DQ177282, FJ154120, FJ589651–FJ589715, JF442120, JF442123–JF442124, JF442129–JF442132, JF442134, JF442137, JF442157, JF442187, and KC753898) are presented in the Appendix.

VELAZCO268 · Zootaxa 3718 (3) © 2013 Magnolia Press

Voucher specimens for the samples are deposited in the following mammal collections:

ASNHC (ASK) Angelo State Natural History Collection, San Angelo, Texas, USA.CM Carnegie Museum of Natural History, Pittsburgh, Pennsylvania, USA.FMNH Field Museum of Natural History, Chicago, Illinois, USA.IEPA Instituto Estadual de Pesquisas do Amapá, Amapá, Brazil.INPA Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil.MSB (NK) Museum of Southwestern Biology, University of New Mexico, Albuquerque, New Mexico, USA.MVZ Museum of Vertebrate Zoology, University of California, Berkeley, California, USA.MZUSP Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil.QCAZ Museo de Zoología, Pontificia Universidad Católica del Ecuador, Quito, Ecuador.ROM (F, FN) Royal Ontario Museum, Toronto, Ontario, Canada.TTU (TK) Museum of Texas Tech University, Lubbock, Texas, USA.UFES Universidade Federal de Espírito Santo, Vitória, Espírito Santo, Brazil.UFMG Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.

DNA isolation and sequencing for the samples were performed in the Pritzker Laboratory for Molecular Systematic and Evolution of the Field Museum of Natural History. Total genomic DNA from tissue samples was isolated from small (~0.05 g, wet weight) portions of liver or muscle that had been frozen or preserved in lysis buffer. DNA was extracted using a Puregene DNA isolation kit (Gentra System, Minneapolis, Minnesota). Polymerase chain reaction (PCR) and sequencing reactions were carried out with primers L14724 and H15915 from Irwin et al. (1991). PCR conditions include an initial denaturation step at 95ºC for 2 min, followed by 35 cycles of PCR (denaturation at 95ºC for 30 s, annealing at 50ºC for 30 s, polymerization at 72ºC for 2 min), and a final extension at 72ºC at 8 min. The PCR reagents in a 25 μl sample were 2 μl of FMNH Taq, 2.5 μl 10X reaction buffer, 2.5 μl of 8 mM premixed deoxynucleotide triphosphates, 15 μl of ddH2O, 1 μl per primer (10 μM), and 1 μl genomic DNA. The PCR bands were cut, and intact DNA was melted at 70°C for 10 min, and then 1.5 μl of GELaseTM (Epicentre Technologies, Madison, WI) was added and incubated for at least 2 h at 45°C. The PCR products were cycle-sequenced using ABI PRISM BigDyeTM Terminators v. 3.1 cycle sequencing kit (Applied Biosystems, Foster City, CA). The cycling protocol used involved an initial denaturation step at 96ºC for 60 s, followed by 25 cycles of denaturation at 96ºC for 10 s, annealing at 50ºC for 5 s, and extension at 60ºC for 4 min. Cycle-sequencing products were purified through an Ethanol/EDTA precipitation protocol and run on an ABI PRISM 3730 Genetic Analyzer (Applied Biosystems, Foster City, CA).

Sequences were edited and compiled using SequencherTM 4.1.2 software (Gene Codes). The sequence data were analyzed using Maximum Likelihood (ML) and Bayesian inference (BI) methods. jModelTest version 2.1.1 (Darriba et al. 2012) was used to find the best model for the ML and Bayesian analyses under the Akaike information criterion. The ML analyses were conducted using GARLI 1.0 (Zwickl 2006) using a TVM+I+Γ model with the following parameters: rate matrix (0.5969, 0.7270, 0.5416, 0.3351, 6.7270, 1.0000); base frequencies (A = 0.3124, C = 0.3374, G = 0.1088, T = 0.2415); proportion of invariable sites (0.4260); gamma distribution shape parameter (0.7430). GARLI was used to generate 1000 ML nonparametric bootstrap replicates; the replicates were used to calculate a majority-rule consensus tree in PAUP* v.4.0b10 (Swofford 2003) to assess clade support.

Bayesian inference analysis was used to estimate a phylogeny using a TVM+I+Γ model of nucleotide substitution. Bayesian inference analysis was conducted using MrBayes version 3.1.2 (Huelsenbeck & Ronquist 2001) with random starting trees without constraints; four simultaneous Markov chains were run for 10 million generations, trees were sampled every 1000 generations, stationarity was assessed by examining the standard deviation of split frequencies and by plotting the –ln L per generation using Tracer v. 1.5 (Rambaut & Drummond, 2003), and trees generated before stationarity were discarded as “burn-in.”

To determine the relationships among the haplotypes of Carollia perspicillata, a median-joining network was calculated in SplitsTree4 (Huson & Bryant 2006). Only complete sequences were included in this analysis. To detect the presence of geographic structure in C. perspicillata, the haplotypes were coded based on their geographic region: Amazonia, Andes, Brazilian Shield, Caribbean lowlands, Central America, Chocó, and Guianan Shield.

The alignment and resulting tree were deposited in TreeBASE under ID 14307 (http://purl.org/phylo/treebase/phylows/study/TB2:S14307).

Zootaxa 3718 (3) © 2013 Magnolia Press · 269PHYLOGENY OF CAROLLIA (CHIROPTERA: PHYLLOSTOMIDAE)

Results

Complete cytochrome b (1140 bp) analyses included 167 specimens of Carollia and outgroups (Appendix). Base composition across this data set was homogeneous, except for low values of guanine (28% A, 30% C, 14% G, and 28% T). There are 310 (27%) parsimony-informative sites in the data set.

FIGURE 2. Cytochrome b maximum likelihood phylogram for the genus Carollia. Support statistics from a maximum

likelihood bootstrap analysis and a Bayesian analysis are indicated at each resolved node. For the maximum likelihood analysis

(ML), white indicates bootstrap frequencies ≤ 50%, grey indicates bootstrap frequencies between 50% and 75%, and black

indicates bootstrap frequencies ≥ 75%. For the Bayesian analysis (BPP), white indicates posterior probabilities < 0.95, whereas

black indicates posterior probabilities ≥ 0.95.

The ML and BI analyses recovered similar topologies, with some strongly supported clades (Fig. 2). Nine different lineages were recovered, two of them unnamed. Carollia manu was recovered as sister to C. subrufa with high bootstrap and posterior probabilities values (Fig. 2). Other relationships confirm the results of Hoffmann and Baker (2003). Two major clades were recovered: one containing the smaller size species and the other the medium to large size species of the genus. The small-bodied clade included 4 lineages, C. benkeithi is sister to an unnamed

VELAZCO270 · Zootaxa 3718 (3) © 2013 Magnolia Press

clade from Ecuador and Peru, this relationship is weakly supported, and is joined to the strongly supported clade conformed by C. castanea and another unnamed lineage (Fig. 2). The clade of larger species contains a sister group of C. manu and C. subrufa that is sister to the remaining larger species—this final group consists of a weakly supported basal relationship of C. sowelli sister to the weakly supported pairing of C. brevicauda and C.

perspicillata (Fig. 2).The average Cytb pairwises distance among the nine recovered clades of Carollia ranges from 3.75% (C.

brevicauda–C. perspicillata) to 12.6% (C. perspicillata–C. benkeithi) (Table 1). The pairwise distance between C.

manu and its sister taxon C. subrufa is 5% (Table 1).The median-joining network of 82 complete sequences (76 unique haplotypes) of Carollia perspicillata is

shown in figure 3. There was significant haplotype overlap between geographic regions (Fig. 3). Only one subgroup of the network was formed completely by haplotypes from one region (Brazilian Shield), but additional haplotypes from the Brazilian Shield were present everywhere (Fig. 3).

FIGURE 3. Median-joining network showing the phylogenetic relationships between haplotypes of Carollia perspicillata.

Mutations are indicated by the numbers next to the branches. Missing intermediate haplotypes are added to the network and are

illustrated with small black squares. Branches not proportional to number of mutations.

Discussion

As expected, the fast-evolving cytochrome b gene supported all recent diversification events but fail to support many of the deeper nodes on the Carollia phylogeny (Fig. 2). The monophyly of Carollia was strongly supported, as well as that of nine species, two of them unnamed. One of the unnamed forms, a small Carollia, was recovered as sister to C. benkeithi but that relationship exhibited low bootstrap and posterior probabilities values (Fig. 2). It was first discovered by Solari and Baker (2006) and is distributed in Ecuador and Peru, and is currently being

Zootaxa 3718 (3) © 2013 Magnolia Press · 271PHYLOGENY OF CAROLLIA (CHIROPTERA: PHYLLOSTOMIDAE)

described by Solari and collaborators. C. castanea was found to contain two species, one of them unnamed. Based on the data on hand, it is difficult to assign to which of these lineages the name castanea should be applied to, as the type locality of castanea is Costa Rica and the species have overlapping distributions, with one distributed in Honduras, Costa Rica, Panama, and western Ecuador, and the other known from Panama. A more comprehensive study including revision of specimens and the generation of more molecular data (mtDNA and nDNA) from other specimens in Central America is needed to correctly assign castanea to one of these forms and to describe the other as a new species.

TABLE 1. Pair-wise uncorrected percentage of Cytb sequence divergence ( ± SD) within and among Carollia species.

TABLE 1. (Continued)

Carollia manu was recovered as sister to C. subrufa, represented here by specimens from El Salvador and Mexico (Fig. 2). This relationship, which is strongly supported by both bootstrap and posterior probabilities values, was unexpected since a sister relationship of bat species with those distributions has not been observed before (Hoffmann & Baker 2003; Lim et al. 2004; Solari & Baker 2006; Hoofer et al. 2008a,b; Lim et al. 2008; Redondo et al. 2008; Velazco & Patterson 2008; Pavan et al. 2011; Velazco & Patterson 2013). The only species of Carollia

missing from this study is Carollia monohernandezi; it is known only from the holotype located east of the Andes in southern Colombia (Zurc & Velazco 2010). It is possible that the inclusion of this species might increase the support for the basal branches of the phylogeny.

Low intraspecific genetic variability characterized the two most widespread species of the genus, Carollia

brevicauda and C. perspicillata, which are also sister species. C. brevicauda, represented by 28 individuals distributed from Panama to Bolivia and Brazil, exhibit an intraspecific Cytb divergence of only 1.79% and C.

perspicillata represented by 90 individuals distributed from southern Mexico to southern Brazil, exhibit an intraspecific Cytb divergence of just 1.67% (Table 1). Additionally, the Cytb divergence between Carollia

brevicauda and C. perspicillata was only 3.75% (Table 1), suggesting that the split and subsequent diversification occurred recently during the Pleistocene, as suggested by Hoffmann and Baker (2003) and Pavan et al. (2011). These numbers fall far below the 5% value commonly regarded as a hallmark of species-level divergence (cf.

Bradley & Baker 2001), but the species are sympatric and have been morphologically distinguished since the 19th

century.

1 2 3 4 5

1—Carollia benkeithi 1.80 ± 1.09

2—Carollia brevicauda 12.32 ± 0.64 1.79 ± 0.94

3—Carollia castanea A 8.15 ± 0.98 11.80 ± 0.62 1.51 ± 0.90

4—Carollia castanea B 8.14 ± 0.87 12.30 ± 0.54 5.22 ± 0.27 0.26

5—Carollia manu 12.38 ± 0.88 6.22 ± 0.42 11.73 ± 0.39 12.06 ± 0.15 0

6—Carollia new 7.26 ± 0.87 11.33 ± 0.77 7.86 ± 0.67 7.37 ± 0.58 11.51 ± 0.42

7—Carollia perspicillata 12.60 ± 0.73 3.75 ± 0.46 11.42 ± 0.44 12.03 ± 0.41 6.55 ± 0.27

8—Carollia sowelli 11.92 ± 0.54 4.96 ± 0.56 11.18 ± 0.40 11.31 ± 0.16 6.68 ± 0.23

9—Carollia subrufa 12.32 ± 0.87 7.38 ± 0.34 11.41 ± 0.34 11.36 ± 0.15 5.00 ± 0.10

6 7 8 9

1—Carollia benkeithi

2—Carollia brevicauda

3—Carollia castanea A

4—Carollia castanea B

5—Carollia manu

6—Carollia new 1.23 ± 0.59

7—Carollia perspicillata 10.64 ± 0.68 1.67 ± 0.73

8—Carollia sowelli 10.52 ± 0.79 4.73 ± 0.48 1.61 ± 1.66

9—Carollia subrufa 11.43 ± 0.44 7.63 ± 0.33 6.71 ± 0.26 1.67

x

VELAZCO272 · Zootaxa 3718 (3) © 2013 Magnolia Press

Carollia perspicillata is the only species of the genus thought to have subspecies: azteca, perspicillata, and tricolor (McLellan & Koopman 2008). However, no subspecies should be recognized within C. perspicillata, due to the low intraspecific Cytb divergence (1.67%, Table 1) and the lack of geographic structure in the haplotypes (Fig. 3).

Further analyses of additional genes (mitochondrial and nuclear) and samples from Colombia need to be included in order to investigate the timing of the split between these two species and to have a more robust understanding of the evolution and diversification of this ecologically important group.

Acknowledgments

For access to tissues under their care I thank Bruce D. Patterson and John Phelps (FMNH). I thank Lizette Siles for the photograph of figure 1. For critical comments on an early draft of this manuscript, I thank Kerry Kline, Bruce D. Patterson, Miguel Pinto, and two anonymous reviewers. Funding for this project was provided by an NSF Doctoral Dissertation Enhancement Grant (OISE 0630149) to Bruce D. Patterson and PMV, the Gerstner and Roosevelt postdoctoral fellowships (AMNH) and the Barbara E. Brown Fund for Mammal Research (FMNH). The specimens of Carollia manu were collected thanks to funding provided by NSF (DEB 9870191 to Bruce D. Patterson and colleagues).

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VELAZCO274 · Zootaxa 3718 (3) © 2013 Magnolia Press

APPENDIX

The following list includes all the specimens used in this study (Museum number, collector number, GenBank number), with

their respective localities. See Material and Methods for abbreviations. Coordinates for the localities of the sequences produced

by this study are provided.

Carollia benkeithi (14)

BOLIVIA: Beni: Yacuma (MSB 68356 / NK 25385 / AF512002). Cochabamba: Sajta (MSB 70297 / NK 30150 /

AF512004); Villa Tunaria (MSB 70298 / NK 30033 / AF512003). PERU: Huánuco: Leoncio Prado, Tingo Maria (TTU 46187

/ TK22892 / DQ177279). Madre de Dios: Albergue Maskoitania, Río Alto Madre de Dios (FMNH 174603 / TK125124 /

DQ177280, FMNH 174605 / TK 125125 / DQ177281, FMNH 174609 / TK 125127 / DQ177282). San Martín: Moyobamba,

A.C.M. Mishquiyacu Rumiyacu-Almendra, Orquidiario Waqanki (06° 04’ 30” S, 76° 58’ 33” W) (FMNH 203350 / RCO 0931

/ KF019701, FMNH 203543 / BDP 4699 / KF019702, FMNH 203544 / BDP 4702 / KF019703, FMNH 203546 / SVS 0316 /

KF019704); Rioja, Pardo Miguel, Naranjos, Caserio El Diamante (05° 45’ 12” S, 77° 31’ 34” W) (FMNH 203351 / PMV 2367

/ KF019705, FMNH 203353 / RCO 0970 / KF019706, FMNH 203547 / SVS 0380 / KF019707).

Carollia brevicauda (28)

BOLIVIA: Santa Cruz: Buen Retiro (MSB 55142 / NK 12171 / AF511951); 27 km SE Santa Cruz (MSB 59775 / NK

15417 / AF511952). BRAZIL: Amazonas: Santa Isabel do Rio Negro (MZUSP / AD 911 / FJ589653, MZUSP / AD 878 /

FJ589654). Mato Grosso: Aripuanã (UFMG / ARI 01 / FJ589651, UFMG / ARI 04 / FJ589652). ECUADOR: Esmeraldas:

San Lorenzo (TTU 85302 / TK 104530 / AF511953). Napo: Parque Nacional Yasuní (ROM 103977 / FN 37059 / AF511954,

ROM 103978 / FN 37060 / AF511956). Orellana: Coca (QCAZ 8484 / ASK 7651 / JF442129). Sucumbíos: Marian, Puente

del Cuyabeno (ASNHC 14047 / ASK 7654 / JF442132). GUYANA: Barima-Waini: Baramita (— / TK 86502 / AF511958).

PANAMA: Panamá: Parque Nacional Altos de Campana (–– / FN 38117 / AF511960). PERU: Cuzco: Paucartambo,

Consuelo (13° 01’ 25” S, 71° 29’ 30” W) (FMNH 174595 / BDP 4040 / FJ154120, FMNH 174596 / BDP 4035 / KF019708,

FMNH 174598 / BDP 4036 / KF019709). Madre de Dios: Manu, Maskoitania (12° 46’ 18” S, 71° 23’ 8” W) (FMNH 174597 /

BDP 4029 / KF019710). San Martín: Moyobamba, A.C.M. Mishquiyacu Rumiyacu-Almendra, Orquidiario Waqanki (06° 04’

30” S, 76° 58’ 33” W) (FMNH 203549 / RCO 0896 / KF019711, FMNH 203552 / SVS 0327 / KF019712); Moyobamba,

Tingana (05° 54’ 38” S, 77° 06’ 43” W) (FMNH 203364 / PMV 2403 / KF019713, FMNH 203559 / SVS 0390 / KF019714);

Rioja, Pardo Miguel, Naranjos, Caserio El Diamante (05° 45’ 12” S, 77° 31’ 34” W) (FMNH 203360 / PMV 2364 / KF019715,

FMNH 203361 / RCO 0968 / KF019716, FMNH 203553 / RCO 0944 / KF019717, FMNH 203557 / PMV 2358 / KF019718).

SURINAME: Saramacca: Raleigh Falls (CM 63727 / TK 10218 / AF511955). VENEZUELA: Barinas: Barinitas (CM

78409 / TK 19316 / AF511959). Bolívar: El Palmar (CM 78400 / TK 19273 / AF511957).

Carollia castanea A (8)

COSTA RICA: Limón: Tortuga Lodge (ROM 108291 / FN 44016 / AF511994); Estación Biológica Caño Palma (ROM

108303 / FN 44029 / AF511995). ECUADOR: Esmeraldas: San Lorenzo (TTU 85278 / TK 104506 / AF511998, TTU 85280

/ TK 104508 / AF511999, TTU 85453 / TK 104681 / AF512000). HONDURAS: Atlántida: Lancetilla (TTU 84037 / TK

101378 / AF511996, TTU 84121 / TK 101462 / AF511997). PANAMA: Chiriquí: Santa Clara (ROM 104315 / FN 38166 /

AF512001).

Carollia castanea B (2)

PANAMA: Darién: Parque Nacional Darién (ROM 104341 / FN 38195 / AF511992, ROM 104353 / FN 38212 /

AF511993).

Carollia manu (2)

PERU: Cuzco: Paucartambo, San Pedro (13° 3’ 17” S, 71° 32’ 46” W) (FMNH 172077 / SS 2042 / KF019719, FMNH

172078 / PMV 588 / KC753898).

Carollia perspicillata (90)

BRAZIL: Amapá: Rio Anacuí (IEPA / MAP 482 / FJ589715). Amazonas: Barcelos (INPA / RZ 33 / FJ589689, INPA /

RZ 05 / FJ589690, INPA / RZ 28 / FJ589691); Santa Isabel do Rio Negro (MZUSP / AD 802 / FJ589705, MZUSP / AD 843 /

FJ589707, MZUSP / AD 851 / FJ589710, MZUSP / AD 907 / FJ589712, MZUSP / AD 913 / FJ589714, MZUSP / AD 833 /

FJ589706, MZUSP / AD 849 / FJ589708, MZUSP / AD 847 / FJ589709, MZUSP / AD 902 / FJ589711, MZUSP / AD 909 /

FJ589713). Bahia: Una (MZUSP / AD 200 / FJ589661, MZUSP / AD 199 / FJ589662). Espírito Santo: Aguia Branca (UFES

/ YL 334 / FJ589655, UFES / YL 364 / FJ589656, UFES / YL 365 / FJ589657, UFES / YL 391 / FJ589658); Aracruz (MZUSP

/ AD 342 / FJ589670, MZUSP / AD 341 / FJ589671); Cariacica (UFES / RF 04 / FJ589659, UFES / RF 05 / FJ589660);

Linhares (MZUSP / AD 355 / FJ589672). Maranhão: Cândido Mendes (UFMG / LK 14 / FJ589702, UFMG / LK 16 /

FJ589703, UFMG / LK 22 / FJ589704); São Luis (UFMG / VCT316 / FJ589695). Mato Grosso: Aripuanã (UFMG / ARI 10 /

FJ589692, UFMG / ARI 22 / FJ589693, UFMG / ARI 40 / FJ589694). Minas Gerais: Caratinga (MVZ 185533 / – / AF511974,

MZUSP / AD 370 / FJ589673, MZUSP / AD 371 / FJ589674); Itacarambi (UFMG / PNP 11 / FJ589682, UFMG / PNPBH 046

Zootaxa 3718 (3) © 2013 Magnolia Press · 275PHYLOGENY OF CAROLLIA (CHIROPTERA: PHYLLOSTOMIDAE)

/ FJ589683, UFMG / PNPBH043 / FJ589684, UFMG / PNPBH045 / FJ589685); Marliéria (UFMG / PERD18 / FJ589675,

UFMG / PERD04 / FJ589676, UFMG / PERD19 / FJ589677, UFMG / PERDBH024 / FJ589678, UFMG / PERDBH029 /

FJ589679); Santa Bárbara (UFMG / PETI 39 / FJ589680, UFMG / PETI 07 / FJ589681); Unaí (UFMG / MM 004 / FJ589686).

Pernambuco: Olinda (MZUSP / AD 152 / FJ589700, MZUSP / AD 153 / FJ589701); Tamandaré (MVZ 185518 / – /

AF511981, MZUSP / AD 122 / FJ589696, MZUSP / AD 121 / FJ589697). Rio de Janeiro: Mangaratiba (MZUSP / AD 281 /

FJ589688, MZUSP / AD 284 / FJ589687). Rio Grande do Norte: Baia Formosa (MVZ 185806 / – / AF511980, MZUSP / AD

108 / FJ589698). São Paulo: Embuguaçu (MZUSP / AD 975 / FJ589668); Ilhabela (MZUSP / AD 217 / FJ589663, MZUSP /

AD 238 / FJ589664); Jundiai (MZUSP / AD 444 / FJ589667); Mogi das Cruzes (MZUSP / AD 765 / FJ589669); Ribeirao

Grande (MZUSP / AD 244 / FJ589666); Salesópolis (MZUSP / AD 662 / FJ589665). Sergipe: Santo Amaro das Brotas (MVZ

185813 / – / AF511982, MZUSP / AD 162 / FJ589699). ECUADOR: Azuay: San Pedro, Río San Francisco (QCAZ 8477 /

ASK 7644 / JF442124). Esmeraldas: San Lorenzo (TTU 85385 / TK 104613 / AF511975, TTU 85403 / TK 104631 /

AF511976). Napo: Jatun Sacha Biological Station Headquarters (QCAZ 8498 / ASK 7665 / JF442137); Parque Nacional

Yasuní (ROM 103997 / FN 37084 / AF511990, ROM 104013 / FN 37107 / AF511991). Orellana: Coca (ASNHC 14051 / ASK

7653 / JF442131, QCAZ 8485 / ASK 7652 / JF442130). Sucumbíos: Reserva de Producción Faunística Cuyabeno, Cuyabeno

Lodge (ASNHC 14052 / ASK 7643 / JF442123, ASNHC 14053 / ASK 7638 / JF442120, ASNHC 1409 / ASK 7782 /

JF442187). GUATEMALA: El Petén: Poptún (ROM 99259 / FN 31809 / AF511988). GUYANA: Barima-Waini: Baramita

(–– / TK 86503 / AF511977). Upper Demerara-Berbice: Dubulay Ranch (— / TK 86671 / AF511978, –– / TK86691 /

AF511979). MEXICO: Campeche: Escarcega (ROM 97725 / FN 33206 / AF511989). Chiapas: Agua Azul (MSB 55643 / NK

8645 / AF511985, MSB 55645 / NK 8644 / AF511984). Quintana Roo: Laguna Noh-Bec (ROM 97498 / FN 30973 /

AF511987); Tulum (–– / MDE 6004 / AF511986). PERU: San Martín: Moyobamba, A.C.M. Mishquiyacu Rumiyacu-

Almendra, Orquidiario Waqanki (06° 04’ 30” S, 76° 58’ 33” W) (FMNH 203369 / RCO 0913 / KF019720, FMNH 203370 /

SVS 0328 / KF019721); Moyobamba, Tingana (05° 54’ 38” S, 77° 06’ 43” W) (FMNH 203390 / RCO 0997 / KF019722);

Rioja, Pardo Miguel, Naranjos, Caserio El Diamante (05° 45’ 12” S, 77° 31’ 34” W) (FMNH 203381 / PMV 2363 /

KF019723). VENEZUELA: Barinas: Barinitas (CM 78397 / TK 19315 / AF511983).

Carollia sowelli (13)

COSTA RICA: Limón: Estación Biológica Caño Palma (–– / FN 44027 / AF511973); Tortuga Lodge (–– / FN 44017 /

AF511972). GUATEMALA: El Petén: Poptún (ROM 99219 / FN 31769 / AF511962); Tikal (ROM 99274 / FN 31824 /

AF511965). HONDURAS: Comayagua: Cueva de Taulabé (TTU 82495 / TK 101341 / AF511969, TTU 82498 / TK 101377 /

AF511970). Francisco Morazán: Parque Nacional La Tigra (TTU 82496 / TK 101010 / AF511967, TTU 82497 / TK 101013 /

AF511968, TTU 83668 / TK 101005 / AF511966). MEXICO: Chiapas: Agua Azul (MSB 55644 / NK 8641 / AF511964).

Quintana Roo: Laguna Noh-Bec (ROM 97501 / FN 30976 / AF511961). Tabasco: Jonuta (ROM 96187 / FN 30002 /

AF511963). PANAMA: Chiriquí: Ojo de Agua (–– / FN38140 / AF511971).

Carollia new species (5)

ECUADOR: Napo: Jatun Sacha Biological Station Headquarters (ASNHC 14048 / ASK 7686 / JF442157, QCAZ 8493 /

ASK 7660 / JF442134); Parque Nacional Yasuní (ROM 103979 / FN 37061 / AF512006, ROM 103983 / FN 37065 /

AF512005). PERU: San Martín: Rioja, Pardo Miguel, Naranjos, Caserio El Diamante (05° 45’ 12” S, 77° 31’ 34” W) (FMNH

203398 / SVS 0384 / KF019724).

Carollia subrufa (2)

EL SALVADOR: Ahuachapán: El Refugio (ROM 35506 / TK 15818 / AF187024). MEXICO: Jalisco: 22 km S

Chamela (TTU 37719 / TK19550 / AF187023).

VELAZCO276 · Zootaxa 3718 (3) © 2013 Magnolia Press