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Permanent atypical coloration in mammals can occur by a congenital condition or environmental causes, but it is expressed by defects in melanocytes (melanin-producing cells) number or function. Around the world, bats have been reported with abnormal coloration, but only a handful of cases are from México. We report records of chromatic disorders in several species captured from different locations in México. Bats were captured with mist nets outside roosting sites or in trails with vegetation. All individuals were released at the capture site. We recorded 9 individuals of Phyllostomidae and 3 of Molossidae with chromatic disorders: 11 white-spotted individuals and 1 with albinism. White spotting is recorded for the first time in Mimon cozumelae and the first record for Leptonycteris yerbabuenae and Nyctinomops laticaudatus in México. Individuals with pigmentary disorders records are rare in nature and reporting the occurrence of these events in bats increases the knowledge of the natural history of species.
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THERYA NOTES 2021, Vol. 2 : 112-116 DOI: 10.12933/th erya_notes-21-46
Noteworthy records of abnormal coloration in Mexican bats
Registros notables de coloración anormal en murciélagos
mexicanos
Melany aguilar-lópez1*, pedro adrián aguilar-rodríguez1, Juan Cruzado-Cortés2, M. Cristina MaCswiney g.3, and Jorge ortega4
1ECOYDES A. C. Belisario Domínguez 105-2, Colonia Centro, C. P. 42186. Pachuca, Hidalgo, México. E-mail: m.aguilar@ecoydesac.org
(MA-L); pedroaguilarr@gmail.com (PAA-R).
2Biólogo independiente. Calle 33 número 451, Francisco de Montejo, C. P. 97203. Mérida, Yucatán, México. E-mail:
juancruzado@outlook.com (JC-C).
3Centro de Investigaciones Tropicales, Universidad Veracruzana. Calle José María Morelos y Pavón 44 y 46, Centro, C. P. 91000.
Xalapa, Veracruz, México. E-mail: cmacswiney@uv.mx (MCMG).
4Laboratorio de Bioconservación y Manejo, Posgrado de Ciencias Quimicobiológicas, Departamento de Zoología, Escuela Na-
cional de Ciencias Biológicas, Instituto Politécnico Nacional. Plan de Ayala esquina Carpio s/n, C. P. 11340. Ciudad de México,
México. E-mail: artibeus2@aol.com (JO).
*Corresponding author
Permanent atypical coloration in mammals can occur by a congenital condition or environmental causes, but it is expressed by defects in
melanocytes (melanin-producing cells) number or function. Around the world, bats have been reported with abnormal coloration, but only a
handful of cases are from México. We report records of chromatic disorders in several species captured from dierent locations in México. Bats
were captured with mist nets outside roosting sites or in trails with vegetation. All individuals were released at the capture site. We recorded 9
individuals of Phyllostomidae and 3 of Molossidae with chromatic disorders: 11 white-spotted individuals and 1 with albinism. White spotting
is recorded for the rst time in Mimon cozumelae and the rst record for Leptonycteris yerbabuenae and Nyctinomops laticaudatus in México.
Individuals with pigmentary disorders records are rare in nature and reporting the occurrence of these events in bats increases the knowledge
of the natural history of species.
Key words: Albinism; Chiroptera; hypopigmentation; Molossidae; Phyllostomidae.
La coloración atípica permanente en mamíferos puede ocurrir por una condición congénita o por causas ambientales, pero se expresa por
defectos en el número o función de los melanocitos (células productoras de melanina). Alrededor del mundo, se han reportado murciélagos
con coloración anormal en la piel, pero en México se conocen pocos casos. Aquí, presentamos registros de trastornos cromáticos en varias es-
pecies capturadas en diferentes lugares de México. Los murciélagos fueron capturados con redes de niebla afuera de los sitios de percha o en
senderos con vegetación. Todos los individuos fueron liberados en el sitio de captura. Registramos 9 individuos de la familia Phyllostomidae y
3 de Molossidae con trastornos cromáticos: 11 individuos con manchas blancas y 1 con albinismo. El fenotipo de manchas blancas se reporta
por primera vez en Mimon cozumelae y el primer registro para Leptonycteris yerbabuenae y Nyctinomops laticaudatus en México. Los registros
de individuos con trastornos pigmentarios son raros en la naturaleza, e informar la ocurrencia de estos eventos en murciélagos aumenta el
conocimiento de la historia natural de las especies.
Palabras clave: Albinismo; Chiroptera; hipopigmentación; Molossidae; Phyllostomidae.
© 2021 Asociación Mexicana de Mastozoología,www.mastozoologiamexicana.org
Skin coloration in vertebrates is the result of pigments, an
extremely varied group of large molecules that reect light
rays (Hoekstra 2006). Melanin is one of the most important
pigments and it is found in skin, hair, or fur, and eyes. There
are two types of melanin, pheomelanin and eumelanin
(Solano 2014), which are produced in the cells called mela-
nocytes, located at the basal layer of the epidermis (Hick-
man et al. 2001; Cappai et al. 2015; Ali and Naaz 2018). The
pigmentation phenotypes derived from melanocytes are
regulated by over 200 gene loci (Lamoreux et al. 2010).
However, sometimes the phenotype expressed diers
from the chromatic patterns that characterize the species.
Cases of atypical coloration can occur for various reasons.
Some abnormal colorations could be the result of environ-
mental conditions (i.e., roost atmosphere; Constantine
1958) or the diet (MacSwiney et al. 2012), but they are not
permanent, and other phenotypes might be related to a
genetic condition (Jackson 1997; Lamoreux et al. 2010).
Hypopigmentation in mammals is the result of pig-
ment-cell death or the failure in the development of these
cells (Lamoreux et al. 2010) and includes white spotting,
vitiligo, progressive graying, and albinism. White spot-
ting is the congenital absence of viable melanocytes
from some or all the areas where they would be regularly
present, thus forming white spots among the normally
colored skin, and is evident at the birth of the individual
(Lamoreux et al. 2010). Meanwhile, albinism is the con-
genital absence of melanin throughout the body due to
113 THERYA NOTES Vol. 2 :112-116
Abnormal coloration in Mexican bats
an inability of viable melanocytes to produce pigments
(with the resulting phenotype of absence of integumen-
tary and retinal pigmentation; Lamoreux et al. 2010) result-
ing by several recessive genes interacting (Summers 2009).
Both atypical colorations are the most frequently reported
in bats (Uieda 2000; Gamba-Ríos 2010; Lucati and López-
Baucells 2016; Zalapa et al. 2016; Martínez-Coronel et al.
2020). To capture an animal with some condition of chro-
matic disorder has been always of special interest due to
the rarity of which these specimens are registered. Here,
we present noteworthy mentioning records of abnormal
coloration in several bat species captured during dierent
eld trips in México.
We compiled records of abnormal coloration in dierent
bat species. These are the results of eld captures made
by the authors, either by mist-netting in their habitat or
recorded at their roost. In all the captured individuals, we
measured forearm length, weight, and determined the sex
and reproductive status, before taking pictures of their skin
condition. We identied the individuals using the guide by
Medellín et al. (2008). After that, we released them. Due to
the lack of agreement in chromatic disorder terminology in
bats, we used the terms suggested by Zalapa et al. (2016)
to name the skin pigmentation abnormalities for this study.
We recorded 12 bats with chromatic disorders, from 9
species. Of these, 7 species belong to the Phyllostomidae
family and 2 species to the Molossidae family (Appendix):
Artibeus jamaicensis, A. lituratus, Desmodus rotundus, Glos-
sophaga soricina, Leptonycteris yerbabuenae, Mimon cozu-
melae, Sturnira hondurensis (Phyllostomidae); Nyctinomops
laticaudatus and Tadarida brasiliensis (Molossidae; Figures
1A-1F, 2A-2E). The bats were captured in the Mexican states
of Guanajuato (1), Hidalgo (2), Oaxaca (2), Tlaxcala (1), Vera-
cruz (1), Quintana Roo (1), and Yucatán (4).
Of the records, 1 individual (a female pregnant D. rotun-
dus) was an albino (Figure 2B), while most of the individu-
als presented the phenotype of non-symmetrical or single
“white spots” in their skin and fur, either in their back or
shoulder (Figures 1A, 1D, 2A, 2C, 2E), the crown of the head
(Figure 2D), or in their nose and lips (Figure 1C). The mul-
tiple white spots presented in both wings of A. jamaicensis,
L. yerbabuenae, and S. hondurensis (Figures 1B, 1E, 1F) were
visible in the inner and upper face of the patagium.
Abnormal colorations have been widely reported in
bats, and in México, so far 40 individuals from 15 species in
Chiapas, Colima, Hidalgo, Jalisco, Oaxaca and Sonora (Caire
and Thies 1988; Zalapa et al. 2016; Hernández-Aguilar and
Santos-Moreno 2018; Martínez-Coronel et al. 2020). Here,
we added 11 individuals and 2 species to the previous stud-
ies, as well as the states of Guanajuato, Tlaxcala, Quintana
Roo, Veracruz, and Yucatán.
There are several records about abnormal skin color-
ation in bats from around the world (i.e., Uieda 2000; López-
Baucells et al. 2013; Treitler et al. 2013; Zalapa et al. 2016;
Fernández de Córdoba et al. 2017), and frequently reported
in cave-dwelling species that conform big colonies or gre-
garious family groups, especially from the Phyllostomidae
and Molossidae families (Lucati and López-Baucells 2016;
Zalapa et al. 2016). All the species here reported show
these specic characteristics. Atypical skin pigmentation
has been considered problematic to conspecic com-
munication or to avoid predators, thus, impacting the t-
ness of the individual (Uieda 2000; Caro 2005), but in bats,
reproductive individuals with chromatic disorders have
been frequently reported (Sánchez-Hernández et al. 2010;
García-Morales et al. 2012; Zalapa et al. 2016; this study),
and no behavioral changes associated to the condition are
known so far (Harada et al. 1991; Uieda 2001; Moreno et al.
2020). Protected roost, such as caves, may be benecial to
the survival of bats with chromatic disorders, protecting
them from sun burns and being easily spotted by predators
(Uieda 2000; Barquez et al. 2003; Mantilla-Meluk and Jimé-
nez-Ortega 2011). Also, the bat’s nocturnal habits should
play a role in the low impact of abnormal pigmentation in
their survival.
Figure 1. A) Two adults of Artibeus jamaicensis with notorious white spots cov-
ering most of their back, individual 1 was not captured, individual 2 is an adult male
(Photograph of J. Cruzado); B) Adult female of Artibeus jamaicensis with white spots at
the middle and edge of the plagiopatagium and uropatagium (Photograph of C. Mac-
Swiney); C) Adult female of Artibeus lituratus with white spots in noseleaf and upper edge
of dactylopatagium (Photograph of P. Aguilar-Rodríguez); D) Mimon cozumelae with no-
table white spot in the upper back (Photograph of Z. Vallado); E) Remarkable white spots
in plagiopatagium, uropatagium and ears of Leptonycteris yerbabuenae (Photograph of
M. Aguilar); F) Specimen of Sturnira hondurensis with multiple white spots in both wings
(Photograph of M. Aguilar).
www.mastozoologiamexicana.org 114
Aguilar-López et al.
tus (reported as A. intermedius), D. rotundus, and G. soricina
(Pozo and Escobedo-Cabrera 1998; García-Morales et al.
2010; Sánchez-Hernández et al. 2010).
Finally, we emphasize that individuals with pigmentary
disorders records are rare in nature and reporting the occur-
rence of these events in bats increases the knowledge of
the natural history of species. Future research will improve
our understanding about the causes and implications of
these conditions.
Acknowledgements
We thank J. L. Monter Vargas, E. Andablo Amador, E. Gutiér-
rez, Z. Vallado, A. Tzab, K. Romo and all the eld assistants
who participated during the eld trips and whose invalu-
able help we were able to obtain these records. Par-
tial nancial support was provided by Centro de Inves-
tigaciones Tropicales, Universidad Veracruzana (Project
#342612019193) and Comisión Nacional de Áreas Natura-
les Protegidas (CONANP)- Dirección Regional de Centro y
Eje Neovolcánico. The valuable feedback from three anony-
mous reviewers helped improve the manuscript.
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Associated editor: Cristian Kraker-Castañeda
Submitted: May 4, 2021; Reviewed: August 25, 2021.
Accepted: September 1, 2021; Published on line: September 14, 2021.
www.mastozoologiamexicana.org 116
Aguilar-López et al.
Appendix
List of the captured bats with chromatic disorders.
Family Phyllostomidae
1) Artibeus jamaicensis
Locality: Hacienda Misnebalam, 10 km north of Mérida,
Yucatán (21° 09’ 02.9’’ N, 89° 35’ 42.4’ W, 6 m). Colony inside
an abandoned building, surrounded by low deciduous for-
est.
Date: December 14th, 2020.
Specimen: Adult male. Forearm length 59 mm.
A second individual was registered in the same roost
but not captured (individual 2 in the inset of Figure 1A).
Chromatic disorder: White spotting (Figure 1A).
2) Artibeus jamaicensis
Locality: 3.5 km from Felipe Carrillo Puerto, Quintana
Roo (19° 36’ 23.3’’ N, 88° 03’ 50.3’W, 30 m). Captured with
a mist-net in a trail surrounded by medium semi-evergreen
forest.
Date: February 5th, 2011.
Specimen: Adult female. Forearm length 57.8 mm, and
weight 40 g.
Chromatic disorder: White spotting (Figure 1B).
3) Artibeus lituratus
Locality: Rancho Viejo, Tlalnelhuayocan, Veracruz (19°
31’ 53.71’’ N, 96° 58’ 46.86’W, 1,460 m). Captured in second-
ary growth of montane cloud forest, with a river nearby.
Date: March 27th, 2018.
Specimen: Adult female. Forearm length 69.8 mm, and
weight 54 g.
Chromatic disorder: White spotting (Figure 1C).
4) Mimon cozumelae
Locality: Cave near Pixoy, Valladolid, Yucatán (20° 42’
1.07’’ N, 88° 17’ 30.4’’ W, 27 m).
Date: January 11th, 2021. Captured during the emer-
gence from the roost. The cave is surrounded by secondary
growth of medium semi-evergreen forest.
Specimen: Adult male. Forearm length 58.4 mm, and
weight 25 g.
Chromatic disorder: White spotting (Figure 1D).
5) Leptonycteris yerbabuenae
Locality: La Ventosa, Juchitán, Oaxaca (16° 30’ 19.192’’ N,
100° 57’ 06.405’’ W, 20 m). Captured in a vegetation patch
with columnar cacti with water nearby.
Date: May 17th, 2017.
Specimen: Adult female. Forearm length 58 mm and
weight 26 g.
Chromatic disorder: White spotting (Figure 1E).
6) Sturnira hondurensis
Locality: Durango, Zimapán, Hidalgo (20° 54’ 03.539’’ N,
99° 14’ 26.444’’ W, 2,041 m). Captured in a mist-net over a
temporal stream, close to a cabin, in a coniferous forest.
Date: August 22th, 2017.
Specimen: Adult male. Forearm length 42.8 mm and
weight 20 g.
Chromatic disorder: White spotting (Figure 1F).
7) Glossophaga soricina
Locality: La Ventosa, Juchitán, Oaxaca (16° 30’ 19.192’’ N,
100° 57’ 06.405’’ W, 20 m). Captured in a vegetation patch
with columnar cacti with water nearby.
Date: October 11th, 2016.
Specimen: Adult male with scrotal testes. Forearm
length 36 mm and weight 10 g.
Chromatic disorder: White spotting (Figure 2A).
8) Desmodus rotundus
Locality: Paraje El Pinalito, El Carricillo, Atarjea, Guana-
juato (21° 13’ 00.192’ N, 99° 49’ 52.557’ W, 2,138 m). Cap-
tured during the emergence from the roost. The cave is
surrounded by semi-arid vegetation.
Date: April 20th, 2021.
Specimen: Pregnant female. Forearm length and weight
not measured.
Chromatic disorder: Albinism (Figure 2B).
Family Molossidae
9) Nyctinomops laticaudatus
Locality: Cenote Homún, Yucatán (20° 44’ 47.68’’ N, 89°
17’ 48.8’’ W, 14 m).
Date: October 24th, 2020. Captured during the emer-
gence from the roost. Secondary growth of low deciduous
forest.
Specimen: Adult male. Forearm length 43 mm and
weight 12 g.
Chromatic disorder: White spotting (Figure 2C).
10) Tadarida brasiliensis
Locality: Vaquerías, Metztitlán, Hidalgo (20° 22’
08.987’’N, 98° 33’ 25.113’’ W, 2,058 m). Captured during the
emergence from the roost, a non-active mine. The cave is
surrounded by semi-arid vegetation.
Date: October 2nd, 2018.
Specimen: Adult male. Forearm length 43.8 mm and
weight 10.6 g.
Chromatic disorder: White spotting (Figure 2D).
11) Tadarida brasiliensis
Locality: Ex Hacienda Mazapa, Calpulalpan, Tlaxcala (19°
32’ 21.49’’ N, 98° 33’ 27.49’’ W, 2,722 m). Captured during the
emergence from the roost. Colony inside of an abandoned
building.
Date: December 20nd, 2019.
Specimen: Adult male. Forearm length 41.1 mm.
Chromatic disorder: White spotting (Figure 2E).
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This review presents a general view of all types of melanin in all types of organisms. Melanin is frequently considered just an animal cutaneous pigment and is treated separately from similar fungal or bacterial pigments. Similarities concerning the phenol precursors and common patterns in the formation routes are discussed. All melanins are formed in a first enzymatically-controlled phase, generally a phenolase, and a second phase characterized by an uncontrolled polymerization of the oxidized intermediates. In that second phase, quinones derived from phenol oxidation play a crucial role. Concerning functions, all melanins show a common feature, a protective role, but they are not merely photoprotective pigments against UV sunlight. In pathogenic microorganisms, melanization becomes a virulence factor since melanin protects microbial cells from defense mechanisms in the infected host. In turn, some melanins are formed in tissues where sunlight radiation is not a potential threat. Then, their redox, metal chelating, or free radical scavenging properties are more important than light absorption capacity. These pigments sometimes behave as a double-edged sword, and inhibition of melanogenesis is desirable in different cells. Melanin biochemistry is an active field of research from dermatological, biomedical, cosmetical, and microbiological points of view, as well as fruit technology.
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Aberrant colorations resulting from colour pigment deficiencies are commonly described in the bat literature. In this study we report the first leucistic piebald of Phyllostomus discolor (Wagner, 1843) by describing an individual captured in Central Amazonia, Brazil, that presented a distinct white patch on its body but normally pigmented eyes. This is the first report of hypo-pigmentism in the species, but also in the genus. .
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Albinism in the common vampire bat Desmodus rotundus (E. Geoffrey, 1810) was already reported for seven individuals, six of them did in Brazil. Although this species is relatively easy to keep in captivity and many studies with normally pigmented bats were did under laboratory conditions, no reports on detailed observations of captive albino vampire bats were found in literature. This paper reports some behavioral observation of a single albino female D. rotundus kept in captivity in Brazil between 1991 and 1993. Information on feeding behavior, interactions with normally colored individuals and reproduction were recorded.
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To describe the clinical characteristics and recent findings in the heterogeneous group of inherited disorders of melanin biosynthesis grouped as "albinism." The current classification of albinism, and the cutaneous, ocular, and central nervous system characteristics are presented. Recent clinical findings are summarized. Albinism is now classified based on genes known to be responsible for albinism. Foveal hypoplasia is invariably present and individuals with albinism often have delayed visual development, reduced vision, nystagmus, a positive angle kappa, strabismus, iris transillumination, and absent or reduced melanin pigment in the fundi. A visual-evoked potential can document the excessive retinostriate decussation seen in albinism. Grating acuity can be used to document delayed visual development in preverbal children. Glasses are often needed to improve visual acuity and binocular alignment. Albinism is caused by several different genes. Heterogeneity in clinical phenotype indicates that expressivity is variable.
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Oculocutaneous albinism (OCA2) is the most common autosomal recessive disorder in the South African Negroid population, occurring with a prevalence of 1/3900 individuals. The OCA2 locus, P, has been mapped to chromosome 15q11-q13 and a 2.7-kb interstitial deletion has been found to be the common mutation in Africa. This study reports the detection of the deletion allele in OCA2-affected individuals from the southern African, Zambian and Central African Republic (CAR) Negroid populations (0.77, 131/170 OCA2 chromosomes; 0.79, 11/14; 0.33, 4/12, respectively). Normally pigmented individuals from different African countries were also tested. The deletion mutation was found at a frequency of 0.013 (10/780) in the normally pigmented southern African Negroid population and at a lower frequency in individuals from central Africa (0.002; 2/834), including individuals from Zambia, Cameroon, Zaire and the CAR. The study confirms the African origin of this deletion allele. Haplotype analysis suggests that the deletion mutation probably occurred only once and that it arose before the divergence of these African populations, which is estimated to be about 2000-3000 years ago. The unusually high frequency of OCA2 mutations, in particular the 2.7-kb deletion, suggests some selective agent or genetic drift.
Albinism in Artibeus intermedius
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Pozo, C., And J. e. eSCoBedo-CABrerA. 1998. Albinism in Artibeus intermedius. Bat Research News 39:27-28.
And l. SánChez-Vázquez. 2010. Five albino bats from Guerrero and Colima
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SánChez-hernández, C., M. l. roMero-AlMArAz, A. TABoAdA-SAlGAdo, J. A. AlMAzán-CATAlán, G. d. SChnell, And l. SánChez-Vázquez. 2010. Five albino bats from Guerrero and Colima, Mexico. Chiroptera Neotropical 16:522-527.
Atypical coloration in bats: frequency and phenotypes in North and Central America, and the Caribbean islands, and new cases from Mexico and Costa Rica
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uiedA, W. 2001. A review of complete albinism in bats with five new cases from Brazil. Acta Chiropterologica 2:97-105. zAlAPA, S. S., S. Guerrero, M. l. roMero-AlMArAz, And C. Sán-Chez-hernández. 2016. Atypical coloration in bats: frequency and phenotypes in North and Central America, and the Caribbean islands, and new cases from Mexico and Costa Rica. Revista Mexicana de Biodiversidad 87:474-482.
Specimen: Adult male with scrotal testes. Forearm length 36 mm and weight 10 g
  • Locality Glossophaga Soricina
Glossophaga soricina Locality: La Ventosa, Juchitán, Oaxaca (16° 30' 19.192'' N, 100° 57' 06.405'' W, 20 m). Captured in a vegetation patch with columnar cacti with water nearby. Date: October 11 th, 2016. Specimen: Adult male with scrotal testes. Forearm length 36 mm and weight 10 g. Chromatic disorder: White spotting (Figure 2A).