Mammalia 2023; aop

Original Study

Sebastián García-Restrepo*, María José Andrade-Erazo, Paula Juliana Castiblanco-Camacho,

Yuliana Escobar-Aguirre, Paula Daniela Herreño-Rodríguez and Juan Esteban Carrero-Herrera

New reports of morphological anomalies in leaf-

nosed bats (Chiroptera: Phyllostomidae) from
Colombia
https://doi.org/10.1515/mammalia-2022-0067 continent (P. elongatus, G. commissarisi, and H. thomasi).
Received June 21, 2022; accepted January 23, 2023; We also recorded the broken digits anomaly on two
published online February 6, 2023 individuals from two species: Platyrrhinus sp. and Sturnira
sp. from Chocó collected in 2019. In addition, we found one
Abstract: Morphological anomalies in bats are rarely
case of the absence of pinnae and tragus in C. perspicillata
reported. We present new reports of three types of
from Santander collected in 2018; an absence not previ-
morphological anomalies (chromatic, wing, and ear) from
ously reported in bats. We encourage researchers to report
specimens in a biological collection and from individuals
their observations of bats with morphological anomalies,
captured during field sampling. We recorded piebaldism on
as this information could be useful in estimating occur-
seven individuals from six species: Carollia perspicillata,
rence rates and addressing questions about its effects on
Glossophaga commissarisi, Hsunycteris thomasi, Phyllosto-
populations.
mus elongatus, and Trachops cirrhosus from Guaviare
collected in 2022, and Tonatia saurophila from Casanare Keywords: chromatic anomalies; leucism; pinnae; tragus;
collected in 2020. These represent three new reports for the wing defects.

*Corresponding author: Sebastián García-Restrepo, Semillero de

Investigación de Mastozoología de la Universidad de los Andes (SIMUA),
Bogotá DC, C.P. 111711, Colombia; Laboratorio de Ecología de Bosques
Tropicales y Primatología, Universidad de los Andes, Bogotá DC, C.P. 111711,
Colombia; and Fundación Habitando Conservación, Medellín, C.P. 050026,
Colombia, E-mail: s.garciar@uniandes.edu.co. https://orcid.org/0000-
0003-1441-3749
María José Andrade-Erazo, Semillero de Investigación de Mastozoología
de la Universidad de los Andes (SIMUA), Bogotá DC, C.P. 111711, Colombia;
and Fundación Habitando Conservación, Medellín, C.P. 050026, Colombia,
E-mail: mj.andrade1@uniandes.edu.co. https://orcid.org/0000-0003-3269-
4687
Paula Juliana Castiblanco-Camacho and Paula Daniela Herreño-
Rodríguez, Semillero de Investigación de Mastozoología de la Universidad
de los Andes (SIMUA), Bogotá DC, C.P. 111711, Colombia,
E-mail: pj.castiblanco@uniandes.edu.co (P.J. Castiblanco-Camacho),
p.herreno@uniandes.edu.co (P.D. Herreño-Rodríguez). https://orcid.org/
0000-0001-7220-465X (P.J. Castiblanco-Camacho). https://orcid.org/0000-
0002-8731-746X (P.D. Herreño-Rodríguez)
Yuliana Escobar-Aguirre, Programa de Biología, Departamento de
Ciencias Biológicas, Universidad de Caldas, Manizales, Caldas, C.P. 170004,
Colombia, E-mail: yuliana.1711813178@ucaldas.edu.co. https://orcid.org/
0000-0002-0863-5540
Juan Esteban Carrero-Herrera, Semillero de Investigación de
Mastozoología de la Universidad de los Andes (SIMUA), Bogotá DC, C.P.
111711, Colombia; and Laboratorio de Ecología de Bosques Tropicales y
Primatología, Universidad de los Andes, Bogotá DC, C.P. 111711, Colombia,
E-mail: je.carrero@uniandes.edu.co
1 Introduction
Bats can present different types of morphological anomalies:
chromatic, osteological, dental, and tail (Caire and Thies
1988; Esquivel-Melo et al. 2017, 2021; Kunz and Chase 1983;
López-Aguirre 2014; Lucati and López-Baucells 2016; Mitchell
and Smith 1966; Phillips and Jones 1970; Ramírez-Pulido and
Müdespacher 1987). Regarding chromatic anomalies, there
is no consensus on the term that describes the absence of
melanocytes in certain areas of the body. Lucati and López-
Baucells (2016) proposed six categories to distinguish
between albinism, leucism, piebaldism, hypomelanism,
melanism, and partial melanism. For individuals with white
spots, they suggest the term “piebald”; however, Zalapa et al.
(2016) used four categories including the term “white spots”.
Later, Martínez-Coronel et al. (2020) suggested that the broad
category termed “piebald”, proposed by Lucati and López-
Baucells (2016), is not properly defined, as there are no
studies that support a precise classification (Martínez-
Coronel et al. 2020). Nevertheless, recent publications have
used the term piebald (de Almeida et al. 2022; García et al.
2020; Marín 2021; Veloso-Frías et al. 2020). Thus, in this article
we use the term piebald only for individuals with white fur
2 S. García-Restrepo et al.: Anomalies in leaf-nosed bats from Colombia

patches and usually colored eyes and will not discuss other Table : Previous reports of piebaldism from Colombia.
chromatic anomalies.
Regarding wing anomalies, Törne (1913) and Davis Subfamily Species Department Source
(no. of records)
(1968) proposed three categories of defects: (a) accessory
cartilage, defined as an additional structure in some region Carollinae Carollia Caquetá Marin-Vasquez
brevicauda et al. ()
of the dactylopatagium; (b) nonsymmetrical digit, as in the
Cauca (PNN Isla Velandia-Perilla
nonsymmetrical forearms; and (c) broken digit, charac-
Gorgona) () et al. ()
terized by a reddened swelling at the site of the injury that Valle del Cauca Velandia-Perilla
occurs in the phalanges and metacarpals (Castillo-Figueroa et al. ()
and Pérez-Torres 2018; Davis 1968). The most common Stenodermatinae Artibeus amplus Caquetá Marín-Vásquez
break involves the third digit, although breaks can also et al. ()
Artibeus Valle del Cauca Velandia-Perilla
occur in digits 2–5 (Davis 1968).
lituratus et al. ()
The outer ear of most bat species consists of two main Magdalena Olarte-Gonzalez
parts, the pinnae and the tragus. The pinnae contributes et al. ()
greatly to directionality of the auditory system, while the Artibeus Caquetá Marin-Vasquez
tragus functions as a reflecting surface generating acoustic planirostris et al. ()
Córdoba () Chacón et al.
cues (Chiu and Moss 2007; Jen and Chen 1988; Lawrence and
()
Simmons 1982). It has been suggested that pinnae-to-tragus
Dermanura Valle del Cauca Velandia-Perilla
produces reflections that contribute to the vertical localiza- rosenbergi et al. ()
tion of sound sources (Lawrence and Simmons 1982). Due to Sturnira Caldas Roncancio and
their morphological and ecological importance, anomalies in erythromos Ramírez-Chaves
these structures could threaten the individual’s survival. ()
Uroderma Magdalena () Mantilla-Meluk
Piebaldism has been reported from eight Colombian
bilobatum and Jiménez-
departments (Table 1) in 22 individuals bats belonging to five Ortega ()
subfamilies and 12 species of Phyllostomid bats (Chacón et al. Uroderma Magdalena Mantilla-Meluk
2015; Mantilla-Meluk and Jiménez-Ortega 2011; Marin-Vas- magnirostrum and Jiménez-
quez et al. 2010; Olarte-Gonzalez et al. 2014; Roncancio and Ortega ()
Glossophaginae Anoura caudifer Valle del Cauca Velandia-Perilla
Ramírez-Chaves 2008; Velandia-Perilla et al. 2013). In addi-
et al. ()
tion, wing defects have been reported in seven Phyllostomid
Lonchophyllinae Lonchophylla Chocó Velandia-Perilla
species (Castillo-Figueroa and Pérez-Torres 2018), including robusta et al. ()
three records of broken digits from two departments: Arti- Phyllostominae Lophostoma Amazonas Marin-Vasquez
beus planirostris (Spix 1823) and Sturnira bogotensis (Shamel silvicolum et al. ()
1927) from Córdoba, and Sturnira lilium (Geoffroy-Saint- Phyllostomus Caquetá () Marin-Vasquez
discolor et al. ()
Hilaire 1810) from Cundinamarca (according to Velazco and
Patterson (2013). S. lilium is not present in Colombia, so this
specimen needs to be reviewed for accurate identification
(Castillo-Figueroa and Pérez-Torres 2018). Anomalies of the 2 Materials and methods
outer ear previously reported correspond to ears with less
than half normal length in Tadarida brasiliensis (Geoffroy 2.1 Field sampling
1824) from the USA (Caire and Thies 1988), hypertrophy of
the tragus in Artibeus lituratus (Olfers 1818) from Colombia, Bat sampling was carried out during teaching activities in three local-
ities, where each bat was sampled using five mist nets (two 12 × 3 m, one
the squared-eared anomaly in Myotis grisescens (Howell
9 × 3 m, and two 6 × 3 m) between 18:00 and 22:00 h. We captured
1909), Myotis lucifugus (Le Conte 1831), Myotis septen- individuals with the piebald pattern in Puerto Amor, Playa Güio (San
trionalis (Trouessart 1897), Myotis sodalis (Miller and Allen José del Guaviare–Guaviare) between March 20 and 23, 2022 (Figure 1,
1928) from the USA, and Myotis albescens (Geoffroy 1806), Table 2). In this locality, the nets were arranged along forest edges,
and Myotis nigricans (Schinz 1821) from Costa Rica (Kurta flyways inside the forest, and streams.
and Kwiecinski 2007; LaVal and LaVal 1980; Tamayo-Zuluaga Individuals with broken digits were collected in Bahía del Agua-
cate, Capurganá (Acandí – Chocó) between November 07 and 10, 2019
et al. 2020). Here we report new cases of piebaldism, broken
(Figure 1, Table 2). In this locality, the nets were placed along waterways
digits, and absent pinnae and tragus in leaf-nosed bats in and forest edges of secondary forest.
Colombia, following the definition of piebaldism by Lucati Bone thickening, no swelling, redness, or loose movement of the
and López-Baucells (2016) and focused on a continental scale. digits, indicated that fractures occurred before handling the animals
 S. García-Restrepo et al.: Anomalies in leaf-nosed bats from Colombia
Figure 1: Collection localities of bats with piebaldism (Casanare, Guaviare), broken digits (Chocó), and outer ear absence (Santander) in Colombia.
(Davis and Doster 1972). Additionally, one specimen without pinnae and
tragus was collected in San Juan del Carare (Cimitarra – Santander) on
March 27, 2018 (Figure 1, Table 2). In this locality, the nets were placed in
a mosaic of forest fragments and grassland used for cattle ranching and
agricultural activities. All individuals were identified following Diaz
et al. (2016, 2021) and Gardner (2007), and deposited in the mammal
collection of the Natural History Museum C. J. Marinkelle (ANDES-M).
2.2 Revision of specimens deposited in the Natural
History Museum C. J. Marinkelle
During routine curatorial activities of the ANDES-M collection, we
found a piebald specimen (Tonatia saurophila) collected in the village
Belgrado (Maní–Casanare) in February 2020 (Figure 1, Table 2). A
systematic review of the entire collection was not conducted to reveal
the presence of other individuals with anomalous traits.
3 Results
On the whole we report ten specimens with morphological
anomalies: seven with a piebald pattern, two with broken
3
digits, and one with an outer ear deformity (Table 2). The
chromatic anomalies were recorded in seven adults (two
females, five males) from six species: Carollia perspicillata
(Linnaeus, 1758), Glossophaga commissarisi (Gardner 1962),
Hsunycteris thomasi (Allen 1904), Phyllostomus elongatus
(Geoffroy-Saint-Hilaire 1810), T. saurophila (Koopman and
Williams 1951), and Trachops cirrhosus (Spix 1823)
(Figure 2). None of the individuals showed additional
anomalies. The piebald pattern is observed in different
body parts, ranging from dorsal and ventral to the upper
shoulders and even the face (Table 2).
Records of wing defects correspond to two adult males
identified as Platyrrhinus sp. and Sturnira sp. The first
specimen had a fracture in the metacarpal of second digit
(right wing), and the second one had a defect in the second
phalanx of third digit (left wing) (Figure 3). None of the
individuals showed additional anomalies. An additional
individual of C. perspicillata (adult male) had no pinnae nor
tragus (Figure 4) but did not show signs of injury or physical
damage. In the same field sampling, another five bats were
captured (three Carollia perspicilla and two Carollia
4 S. García-Restrepo et al.: Anomalies in leaf-nosed bats from Colombia

Table : Specimens with morphological anomalies reported in this study.

Species Museum Sampling site Land cover Coordinates (elevation: m Anomaly description
voucher above sea level)
(ANDES-M)

Piebaldism

Carollia perspi-  San José del Gua- Caquetá Moist .; −. () One white spot on the ventral region
cillata _ viare (Guaviare) Forest
Carollia perspi-  .; −. () Two white spots on the ventral region,
cillata \ one on each side. The spots are close to
the mammary glands
Glossophaga com-  One white spot between the neck and left
missarisi _ shoulder and a small one on the
forehead
Hsunycteris tho-  .; −. () One white spot on the ventral region, and
masi \ some scattered white hairs
Phyllostomus  Two white spots on the left shoulder
elongatus _
Trachops cirrhosus  One white spot on the dorsal region
_
Tonatia saurophila  Maní (Casanare) Llanos .; −. (-) One white spot on the ventral region
_

Broken digit

Platyrrhinus sp. _  Acandí (Chocó) Chocó - Darién .; −. () Fracture in the metacarpal of nd digit
Sturnira sp. _  Moist Forest Defect on the second phalanx of rd digit

Missing ear

Carollia perspi-  Cimitarra Magdalena- .; −. () Missing outer ear structure and tragus
cillata _ (Santander) Urabá Moist on the right side
Forest

Classification of land cover as presented in Sánchez-Cuervo et al. ().

brevicauda), and none presented anomalies. During field-
work for an undergraduate thesis in the same locality in
2018, another bat (Carollia sp.) with only one ear was
captured, but this bat was not collected (Gabriela Arias,
personal comment).
4 Discussion and conclusion
Piebaldism in America has been reported in at least 60 bat
species, Phyllostomidae being the family with most cases
of anomalies (38 spp.), followed by Vespertilionidae (10
spp.), Molossidae (10 spp.), Mormoopidae and Noctilioni-
dae (one species each one) (Flores Salazar 2021; Lucati and
López-Baucells 2016; Pereira et al. 2022; Rivero-Castro et al.
2020; Ruelas et al. 2016; Salas et al. 2021) (see Supplemen-
tary Table S1). Our findings add three bat species not pre-
viously reported with piebaldism in America: P. elongatus,
G. commissarisi, and H. thomasi. Although C. perspicillata
is one of the most abundant Neotropical bats (Arita 1993;
McLellan and Koopman 2007), there are only five records
of atypical coloration from Trinidad and Tobago (2), Brazil
(2), and Honduras (1) (Espinal et al. 2016; Goodwin and
Greenhall 1961; Lucati and López-Baucells 2016; Rocha
et al. 2013), and two records of partial leucism in Ecuador
and Costa Rica (Boada and Tirira 2010; Escobar-Anleu and
Mora 2018). T. saurophila has one record of piebaldism in
Brazil (through a personal comment by López-Baucells in
Lucati and López-Baucells 2016), while T. cirrhosus has one
record from Brazil and one from Ecuador (Borloti et al. 2019;
Bravo-Salinas and Salas 2022). The biological implications of
this abnormal pattern are still unknown; however, it could
reduce the individual’s fitness as well as make them more
conspicuous to predators and less attractive during the
breeding season (Caro 2005). Nevertheless, the record of
pregnant females of C. brevicauda in National Natural Park
Gorgona (Cauca, Colombia), Sturnira ludovici in Huasteca
region (Hidalgo, Mexico), as well as lactating females of
 S. García-Restrepo et al.: Anomalies in leaf-nosed bats from Colombia 5

Figure 2: Piebald individuals. (a) Carollia perspicillata (ANDES-M 2687); (b) Carollia perspicillata (ANDES-M 2688); (c) Glossophaga commissarisi; (d)
Hsunycteris thomasi; (e) Phyllostomus elongatus; (f) Tonatia saurophila; (g) Trachops cirrhosus. Red arrows indicate the white spots.

Anoura caudifer (Calima-Darién, Valle del Cauca), and A. lit-
uratus (Cali, Valle del Cauca), suggest that this condition does
not always affect reproduction in certain populations (Gar-
cía-Morales et al. 2012; Velandia-Perilla et al. 2013).
Records of broken digits in bats include A. planirostris,
Barbastella barbastellus, Myotis daubentonii, Myotis myotis,
Myotis nattereri, Plecotus auritus, Rhinolophus hipposideros,
S. bogotensis, S. lilium, and Sturnira parvidens (Castillo-Fig-
ueroa and Pérez-Torres 2018; Cichocki et al. 2019; Cornejo-
Latorre et al. 2020). The two records of broken digits we
report from the Pacific region of Colombia correspond to
new species of Phyllostomid bats with this kind of wing
defect (Platyrrhinus sp., and Sturnira sp.). The site of the
injuries in the individuals (metacarpal of second digit, and
second phalanx of third digit) align with those previously
reported (Castillo-Figueroa and Pérez-Torres 2018; Cornejo-
Latorre et al. 2020; Davis 1968). Apparently, it is more com-
mon for these bats to injure these metacarpals, which form
most of the support for the leading edge and the wing tip
(Davis 1968). Although we cannot determine the causes of
broken digits, it could be a common condition, considering
the high-risk flight habits of bats (i.e., physical damage
occurring during flight or foraging, intraspecific in-
teractions, or interactions with predators) (Cichocki et al.
2019; Cornejo-Latorre et al. 2020). Considering they are
frugivorous bats that collect fruits close to vegetation, it is
possible that some physical obstacles (i.e., trunks, blanches,
leaves, or other elements) could affect the flight perfor-
mance and damage their wings (Cornejo-Latorre et al. 2020).
Finally, in addition to other more commonly reported
anomalies, such as wing defects, changes in their dental
formula, and chromatic disorders, our findings suggest that
outer ear anomalies may be also relevant in bats. These
include ears less than half the normal length (Caire and
Thies 1988), tragus hypertrophy (Tamayo-Zuluaga et al.
2020), square ear anomaly (Kurta and Kwiecinski 2007;
LaVal and LaVal 1980), and our record of absent pinnae and
tragus. Regarding the ear length anomaly reported by Caire
and Thies (1988) for T. brasiliensis, they suggested this did
not seem to affect their ability to echolocate. Also, although
some research has suggested that tragus can facilitate sound
localization in the vertical plane by introducing spectral
6 S. García-Restrepo et al.: Anomalies in leaf-nosed bats from Colombia

Figure 3: Wing defects: (a) Platyrrhinus sp. (ANDES-M 2538), metacarpal of second digit; (b) Sturnira sp. (ANDES-M 2539), second phalanx of third digit.
Red arrows indicate the broken digits.

cues, there is also evidence that its contribution to localiza-
tion is limited (Lawrence and Simmons 1982; Wotton and
Simmons 2000). Chiu and Moss (2007) suggested that the
Eptesicus fuscus ability to capture its prey is not heavily
dependent on the tragus. Furthermore, individuals can
adapt to changes in the filtering characteristics of the
external ear. They also proposed that other external ear
parts, such as the bridge along the pinna, may also
contribute to sound localization. However, the extent to
which the lack of an external structure might affect the an-
imal’s ability to echolocate or perform other functions is
unclear. It is important to promote the report of bats with
every types of anomalies, both in the field and in collections.
Studies measuring their frequency in bat populations could
help assess their effects on bat fitness and survival.
Research ethics: The specimens were collected under
permit 1177 granted by the National Authority of Environ-
mental Licenses (ANLA) to Universidad de los Andes. The
procedures were reviewed and approved by Institutional
Animal Care and Use Committee at the Universidad de los
Andes, Colombia.
Acknowledgments: We thank the people in the commu-
nities visited for sharing their time and expertise, and for
facilitating access to the sampling sites. Undergraduate stu-
dents in the course Biological Collections (2019–2 and 2022–1)
from the Department of Biological Sciences, Universidad de
los Andes, participated in the field sampling work in
Capurganá and Playa Güio. The Center for Research in
Tropical Microbiology and Parasitology (CIMPAT) provided
the equipment to carry out the field sampling. Maria
 S. García-Restrepo et al.: Anomalies in leaf-nosed bats from Colombia
Figure 4: Absence of pinnae and tragus: Carollia perspicillata (ANDES-M 2487) in (a) right side view, and (b) frontal view. Red arrow indicates the
abnormal ear.
Lavanholle Ventorin and an anonymous reviewer contrib-
uted to the improvement of this manuscript.
Author contributions: SGR: conceptualization; SGR, MJAE,
YEA, PDHR, JECH: data curation; MJAE, SGR: literature
review; SGR: writing – original draft; SGR, MJAE, PJCC,
PDHR: writing – review and editing. All authors actively
participated in the fieldwork. They reviewed and approved
the final version of the paper.
Research funding: None declared.
Conflict of interest statement: The authors declare that
they have no conflicts of interest regarding this article.
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Supplementary Material: This article contains supplementary material
(https://doi.org/10.1515/mammalia-2022-0067).