DOI 10.1515/mammalia-2013-0019      Mammalia 2014; 78(2): 191–197

Carlos Tello*, Daniel G. Streicker, Jorge Gomez and Paúl M. Velazco

New records of pigmentation disorders in molossid and phyllostomid (Chiroptera) bats from Peru

Abstract: Pigmentation disorders, either from the com-plete absence (albinism), partial (leucism), or excess ( melanism) of melanin, are rare in vertebrates. Worldwide, only a few records of these disorders had been reported for bats. Thanks to recent fieldwork and examination of museum specimens of the collections of the AMNH and MUSM, we report five species with those conditions in Peru. In this study, we report the first cases of leucism in Artibeus anderseni, Chiroderma trinitatum, and Desmodus rotundus and partial melanism in Carollia perspicillata. Additionally, we report the first record of an albino bat (Molossus molossus) for Peru.

Keywords: albinism; bats; leucism; melanism; Neotropics.

*Corresponding author: Carlos Tello, Programa de Investigación, Yunkawasi, Av. Mariscal Castilla 582, Lima 33, Perú; and Programa de Conservación de Murciélagos del Perú, Lima, Peru, e-mail: carlos.tello.ch@gmail.comDaniel G. Streicker: Odum School of Ecology, University of Georgia, Athens, GA 30602, USAJorge Gomez: Dirección General de Epidemiología, Ministerio de Salud, Lima, PeruPaúl M. Velazco: Department of Mammalogy, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA

IntroductionPigmentation disorders, like albinism, leucism, or mela-nism, are considered as rare, although they have been recorded in several vertebrate taxa (Ulmer 1941, Edgren 1957, Haedo and Esteban 1972, Kettlewell 1973, Veiga 1994, Majerus 1998, Rodrigues et al. 1999, Bowman and Curran 2000, Teixeira and Araújo 2002, Ramírez and Arana 2005, Tedesco et al. 2005, Alarcos et al. 2006, Tortato and Althoff 2007, Tizón et al. 2008, Oliveira 2009). Albinism is a genetic condition caused by a gene mutation. It is char-acterized by a complete lack of melanin; so in animals with this condition, the fur is white and the eyes are red due to the reflection of the color of the capillary vessels

of the retina (Quay 1970, Buchanan 1985, Griffiths et  al. 2000). Leucism is characterized by a reduction in or lack of pigmentation in different parts of the body and is caused by the expression of mutant alleles (Jehl 1985, Bensch et al. 2000). Animals with this condition usually display atypical white spots on the skin and/or pure white fur and normal colored eyes and claws (Quay 1970, Miller 2005) different from albinistic individuals. Melanism is a phenotypic condition linked to recessive alleles or muta-tions that make individuals darker than the typical form (Kettlewell 1973, Majerus and Mundy 2003, Kingsley et al. 2009). It is present in a wide variety of animal taxa includ-ing mammalian species (Kettlewell 1973, Majerus 1998), but in bats, it is even more rare than albinism and leucism (Buchanan 1985).

The appearance of pigmentation disorders in noc-turnal mammals such as bats is particularly interesting because such mutations are expected to increase the risk of predation (Smith 1968, Caire and Thies 1988), but rela-tively few cases of these disorders have been described. On the other hand, the presence of these disorders could be indirect evidence of genetic variability in populations (Jehl 1985). In South America, there have been reports of seven species with albinism (Artibeus cinereus, Artibeus planirostris, Glossophaga longirostris, Desmodus rotun-dus, Sturnira erythromos, Eumops glaucinus, and Molos-sus molossus) in three countries: Argentina (Barquez et al. 2003, Ramírez et al. 2010), Brazil (Moreira et al. 1992, Veiga and Oliveira 1995, Uieda 2000, Geiger and Pacheco 2006, Oliveira and Aguiar 2008), and Venezuela (Setzer 1950). Leucism has been reported in 15 bat species in South America (Anoura caudifer, Artibeus jamaicensis, Carollia brevicauda, Carollia perspicillata, Lophostoma silvicolum, Micronycteris microtis, Sturnira erythromos, Sturnira lilium, Eptesicus furinalis, Myotis riparius, Eumops bonariensis, Eumops glaucinus, Eumops patagonicus, Nyctinomops lat-icaudatus, and Tadarida brasiliensis) in seven countries (Linares 1967, Barquez et  al. 2003, Geiger and Pacheco 2006, Roncancio and Ramírez-Chaves 2008, Boada and Tirira 2010, Marin-Vasquez et al. 2010, Medina and López 2010, Acosta et al. 2011, Idoeta et al. 2011). Melanism has been reported in two bat species (Myotis lucifugus and

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192      C. Tello et al.: Pigmentation disorders in Peruvian bats

Pipistrellus subflavus), only from North America (Osgood 1936, Trapido and Crowe 1942, Buchanan 1985). In this study, we report for the first time cases of albinism and melanism in bat species from Peru.

Materials and methodsWe reviewed specimens belonging to the scientific collec-tions of the American Museum of Natural History, New York, USA (AMNH) and the Museo de Historia Natural de la Universidad Nacional Mayor de San Marcos, Lima, Peru (MUSM). In addition to those, we have records from recent expeditions in Peru in which the specimens were captured, photographed, and released.

The specimens were captured using mist nets and an aerial insect net. The records are presented with their locality information and natural history data if available. Standard field measurements and reproductive condition information were recorded or taken from the field notes for bats from the museum collections. Field measurements included TL, total length (including tail); T, tail length; HF, hind foot length; E, ear; FA, forearm; and W, weight. We used a digital caliper to take nine craniodental meas-urements to the nearest 0.01 mm as follows: GLS, greatest length skull; CBL, condylobasal length; CCL, condyloca-nine length; BB, braincase breadth; PL, palatal length; ZB, zygomatic breadth; MTL, maxillary toothrow length.

Procedures for the capture and handling of bats were approved by the University of Georgia’s Animal Care and Use Committee (A2011-04-009-R1), and collection permits were obtained from the Division of Flora and Fauna of the Ministry of Agriculture of Peru (RD-0299-2010-AG-DGFFS-DGEFFS and RD-038-2012-AG-DGFFS-DGEFFS).

ResultsWe found one specimen with albinism (Molossus molos-sus), seven specimens with leucism (Artibeus anderseni, Chiroderma trinitatum, and Desmodus rotundus), and one specimen with partial melanism (Carollia perspicillata).

Albinism

Molossus molossus – An adult male specimen (AMNH 278458, Figure 1) was collected at the Centro of Investi-gaciones Jenaro Herrera (CIJH) located approximately 2.5 km east of the Ucayali River and 140 km SSW of Iquitos

Figure 1 An albino male Molossus molossus (AMNH 278458), ventral (A) and dorsal (B) views showing the presence of white fur-skin and translucent dactylopatagium; head (C) view showing red eyes (Photograph by Marco Tschapka).

in the Province of Requena, Department of Loreto (4°55′ S, 73°45″ W, 150 m), on January 21, 2012. This bat was cap-tured using a canopy net set at 30  m above the ground during the “International Bat Course 2012” organized by Centro de Ecología y Biodiversidad (CEBIO). The habitat where the mist net was set is a forest edge between a sec-ondary growth forest and an open area where the CIJH facilities are located. The specimen had white fur and skin on the entire body (Figure 1A and B) and red eyes (Figure 1C). The normal fur for this species is chestnut brown to blackish; some individuals could be brown to reddish on the back, with ventral fur slightly lighter than dorsal fur (Fabian and Gregorin 2007). Other species captured in the same mist net were Carollia perspicillata, Chiroderma trinitatum, and Platyrrhinus brachycephalus. External and cranial measurements of our specimens (Table 1) are within the range of measurements reported for M. molos-sus (Freeman 1981, Simmons and Voss 1998, Barquez et al. 1999, Genoways et al. 2005).

Leucism

Artibeus anderseni – Three leucistic specimens were found in the MUSM mammal collection. An adult male speci-men (MUSM 9765, Figure 2A) was collected at the Palotoa river, Province of Manu, Department of Madre de Dios (12°35′23.9″ S, 71°27′51.8″ W, 490 m), on August 17, 1985. This specimen has two white patches of fur on the dorsum

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Table 1 External and craniodental measurements of bats with pigmentation disorders.

Molosus molossus

Artibeus anderseni

Chiroderma trinitatum

Desmodus rotundus

Carollia perspicillata

AMNH 278458

MUSM 9756 , 10887 , 12422

MUSM 4219

CT 664 , 1 MUSM 5107

W 15.5 12 (3) 40–52 (2) 17TL 102 48–53 (3) 53 83 (1) 78T 36 – – – 11HF 8 10–11 (3) 9.8 14 (1) 11E 12 15–16.5 (3) 18 20 (1) 20FA 40 36.0–36.8 (3) 38.1 62–68 (2) 42GLS 17.2 18.6–19.1 (3) 21.6 23.9 (1) 22.8CBL 16.1 16.8–17.1 (3) 19.5 21.8 (1) 20.7CCL 15.7 16.2–16.5 (3) 18.8 19.4 (1) 19.9BB 9.1 8.2–8.9 (3) 9.3 12.3 (1) 9.8PL 5.3 7.6–8.1 (3) 11.4 9.9 (1) 9.8ZB 11 11.1–11.7 (3) 13.0 12.3 (1) 11.5MTL 6.5 5.9–6.1 (3) 7.2 3.5 (1) 7.5

Measurements are in millimeters, except weights, which are in grams. 1Released specimen.

Figure 2 Leucistic specimens of Artibeus anderseni. (A) Dorsal view of MUSM 9756, showing two white patches; (B) ventral view of MUSM 10887, showing a white patch of fur on the inguinal region and presence of white skin on a section of the uropatagium next to the right tibia; (C) ventral view of MUSM 12422, showing a white patch of fur on the right abdominal area.

(Figure 2A). Other species registered at the same locality were Artibeus obscurus, Carollia brevicauda, Carollia ben-keithi, Platyrrhinus incarum, and Uroderma bilobatum. An adult male specimen (MUSM 10887, Figure 2B) was col-lected in Palmira, Province of Oxapampa, Department of Pasco (10°4′13.7″ S, 75°33′47.5″ W, 830 m), on February 13, 1996. This specimen has two white patches of fur, one dor-sally and the other ventrally, and part of the uropatagium is white (Figure 2B). Other species registered at the same locality were Artibeus glaucus, Carollia brevicauda, Carol-lia perspicillata, Desmodus rotundus, Mesophylla macco-nnelli, Sturnira oporaphilum, and Vampyrodes caraccioli. The other specimen, an adult female (MUSM 12422, Figure 2C) was collected at the Estación Biológica Pakitza in Manu

National Park, Province of Manu, Department of Madre de Dios (11°56′47″ S, 71°16′59.9″ W, 356 m), on March 9, 1992. This specimen has two white patches of fur, one dorsally and the other ventrally, and part of the uropatagium is white (Figure 2C). Other species registered at the same locality were Artibeus lituratus, Artibeus obscurus, Artibeus planirostris, Carollia benkeithi, C. brevicauda, C. perspicil-lata, Lophostoma silvicolum, Platyrrhinus incarum, Rhino-phylla pumilio, Molossus molossus, and Noctilio albiventris. External and cranial measurements of our specimens (Table 1) are within the range of measurements reported for A. anderseni (Osgood 1916, Anderson 1997).

Chiroderma trinitatum – An adult male specimen (MUSM 4219, Figure 3) was collected at the CIJH (same

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194      C. Tello et al.: Pigmentation disorders in Peruvian bats

locality information as the Molossus record) on September 22, 1989. This specimen differs from other individuals of C. trinitatum in that its fur is entirely white (Figure 3), but the skin is of the same color as the other specimens of this species, without pigmentation abnormalities. Normal individuals have a brownish-gray coloration on the facial and dorsal fur (Zortéa 2007). This specimen was collected along with specimens of Chiroderma villosum, Platyrrhinus fusciventris, Platyrrhinus incarum, Uroderma bilobatum, and Vampyressa thyone. External and cranial measurements of our specimen (Table 1) are within the range of measurements reported for C. trinitatum (Swanepoel and Genoways 1979, Anderson 1997, Simmons and Voss 1998).

Desmodus rotundus – Three leucistic specimens of vampire bats were captured in three different depart-ments of Peru. The first individual, an adult female, was captured using an aerial insect net in a culvert near the town of Vilcahuaura, Province of Huaura, Department of Lima (11°4′40.092″ S, 77°27′33.768″ W, 307 m), on August 2, 2007. This specimen presented white dorsal and ventral fur (Figure 4A). This specimen was photographed and then released. Individuals without a pigmentation abnor-mality present brown to gray dorsal fur with lighter ventral fur in some individuals (Greenhall et al. 1983). The locality belongs to the Huaura River valley. The culvert was built to allow the flow of water between mountains to irrigate the farmlands. The tunnel was exclusively inhabited by other individuals of D. rotundus. The second individual, an adult male (CT 664) was collected using a ground level

A B

Figure 3 Leucistic specimen of Chiroderma trinitatum (MUSM 4219). Dorsal (A) and ventral (B) views showing the presence of white fur and dark skin.

A B

C

Figure 4 Leucistic specimens of Desmodus rotundus. (A) Ventral view of a specimen from the department of Lima, showing the whitish fur and skin, and dark eyes. (B) Ventral view of a specimen from the department of Amazonas, showing a whitish patch on the fur on the chest. (C) Ventral view of a specimen from the department of Apurimac, showing some whitish patches in plagiopatagium and dactylopatagium.

mist net in a pasture field with cattle in the community of Guambo, a community located in the Province of Rod-riguez de Mendoza, Department of Amazonas (6°34′58.4″ S, 77°23′25.3″ W, 1527 m), on December 4, 2011. This specimen presented a whitish patch on fur on the chest (Figure 4B) that is usually brown to gray in coloration, in normal specimens of the species. The community is located close to a montane forest habitat. Other species collected along with this leucistic specimen included Artibeus glaucus, Anoura fistulata, Carollia perspicillata, Chiroderma trinitatum, and Platyrrhinus incarum. The third leucistic vampire is an adult female captured using ground mist nets around crop fields in Pachachaca, a community located approximately 6 km SW of the city of Abancay in the Province of Abancay, Department of Apu-rimac (6°13′13″ S, 79°17′58″ W, 2042 m), on July 12, 2011. This specimen, photographed and released afterward, presented some whitish patches in plagiopatagium and dactylopatagium (Figure 4C). The mist net was placed around cornfields close to a cave. Other species captured together with this leucistic vampire were Myotis oxyotus and Sturnira erythromos. The measurements presented in Table 1 are from a collected specimen (CT 664 to be deposited in the MUSM) and from a released specimen

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(two external measurements only). Measurements of our specimens (Table 1) fall within the range reported for D. rotundus (Swanepoel and Genoways 1979, Anderson 1997, Barquez et al. 1999).

Melanism

Carollia perspicillata – An adult male (MUSM 5107, Figure 5) was collected at the Cocha Cashu Biological Station in Manu National Park, Province of Manu, Depart-ment of Madre de Dios (11°51′ S, 71°19″ W, 380 m), on April 3, 1989. This specimen presented a long black patch of fur on the left side of the dorsum (Figure 5). The pelage dorsal is brown to brown blackish in normal individuals (Ortêncio Filho et al. 2007). External and cranial measure-ments of our specimen (Table 1) are within the range of measurements reported for C. perspicillata (Simmons and Voss 1998).

DiscussionAlbinism is considered a rare phenomenon in bats (Barquez et  al. 2003). An extended review reported 38 species around the word (Uieda 2000), and in the last years, some additional records have been added (Charles-Dominique et  al. 2001, Buys et  al. 2002, Barquez et  al. 2003, Sodre et al. 2004, Leblanc and Taupin 2005, Aul and Marimuthu 2006, Oliveira and Aguiar 2008, Alcalde 2009, García-Morales et  al. 2010, Sánchez-Hernández et  al. 2010). Our record, Molossus molossus, is the first specimen and species reported with this rare condition for Peru; previous records for this species come from Brazil, Cuba, and Puerto Rico (Heatwole et al. 1964, Veiga and Oliveira

Figure 5 Specimen of Carollia perspicillata (MUSM 5107) with partial melanism, the black fur covering a third part of the dorsum.

1995, Uieda 2000). The previous records were taken from roosts like buildings and hollow trees (Heatwole et  al. 1964, Veiga and Oliveira 1995) as most records of albino bats that were observed and/or captured in roosts (Uieda 2000); our record is one of the few cases that were mist netted along flyways.

As with albinism, leucism in bats is infrequent, although there are more records than for albino bats in South America. In Peru, the only previous report corre-sponds to a specimen of Sturnira lilium (Medina and López 2010); however, Díaz and Linares (2012) mentioned that they collected specimens in northeasten Peru of Phyllosto-mus hastatus and Molossus rufus with “albinism’s spots”. We are not sure if these are cases of leucism or just fine spots on the fur. They do not offer additional information or pictures of the specimens. Excluding these cases, our records represent the second report of leucism in Peru and the first descriptions for the species reported here.

Cases of leucism in phyllostomid bats seem to be fre-quent in the genus Artibeus, with five species, including the one reported here, that have been described with this disorder (Sánchez et al. 1989, Hernández-Mijangos 2009, Marin-Vasquez et  al. 2010, Sánchez-Hernández et  al. 2010, 2012, García-Morales et al. 2012, López-Wilchis and León 2012). Albinism has been more frequently reported in Desmodus (Moreira et  al. 1992, Uieda 2000, Sánchez-Hernández et al. 2010). However, our records are the first for leucism. Nonetheless, it is unclear if these disorders are more common in Desmodus rotundus than other bats or if the records are the result of a well-studied species (Sánchez-Hernández et  al. 2010). Sánchez-Hernández et  al. (2012) also suggested that inbreeding may be at least partially responsible for these disorders. We do not have any other record of leucism in D. rotundus, although we have monitored these bats in the same localities for several years.

Additional studies should determine whether these genera are unusually prone to pigmentation disorders, the specific genetic mutations responsible and whether other environmental or life history factors associated with low genetic diversity may increase their frequency.

Kettlewell (1973) called all the cases where an increase of dark pigmentation occurs melanic, not necessarily pro-ducing an all-black individual. In bats, some previous records are not all-black specimens (Trapido and Crowe 1942, Buchanan 1985). For our melanic record of Carol-lia perspicillata, it seems more appropriate to call this disorder “partial melanism”, instead, because it was not entirely black. We agree with Buchanan (1985) that some melanic specimens could easily be unnoticed in the field because a large majority of bats present darker skins.

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As we show here, natural history collections are very important because the specimens preserve their fur char-acteristics, including these particular disorders in pig-mentation. This allowed us, in this case, to report those color abnormalities even in the specimens collected over 20 years ago.

Acknowledgments: We thank all the participants of the “International Bat Course 2012” organized by CEBIO. Spe-cial thanks are for the course organizer, Erika Paliza. The following curators and collection staff graciously provided access to the specimens under their care: Nancy B. Simmons

and Eileen Westwig, AMNH; Erika Paliza, CEBIO; and Víctor Pacheco, MUSM. We are grateful to Marco Tschapka for the live photographs of the albino Molossus molossus and Kerry Kline and two anonymous reviewers for reading and improv-ing early versions of this report. Funding for this project was provided to PMV by the Gerstner and Roosevelt postdoctoral fellowships at the American Museum of Natural History, by NSF grant DEB 0949859 to Nancy B. Simmons, National Geographic Grant CRE-4-17-07 to DGS and NSF grant DEB-1020966 to Sonia Altizer and Pejman Rohani.

Received February 4, 2013; accepted July 31, 2013; previously published online September 4, 2013

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