Albinism in Carollia perspicillata ( Chiroptera ; Phyllostomidae ) , in the state of Rondônia , Brazil . A brief review of albinism in bats

Albinism is a phenomenon that is not very common in bats. In the literature, sixty-seven bat species with this mutation have been reported. The purpose of this paper is to report a case of complete albinism in Carollia perspicillata. A young male albino bat was captured in a culvert under the BR 364 highway, located within an anthropogenic area in the district of Caiçara, municipality of Porto Velho, in the northern Brazilian state of Rondônia. The animal was apparently well integrated into the group, healthy and of normal size for the species. A brief review of albinism in bats is also provided.


Introduction
Albinism is caused by a rare gene mutation that provides instructions for the synthesis of proteins involved in melanin production.Melanin is produced by melanocyte cells, which are found in the skin and eyes.Animals with albinism show a signifi cant reduction in the amount of melanin (partial albinism) or no pigment in the eyes, skin, or hair (true or complete albinism) (NOAH, 2015).In addition, the red eyes of albino animals are caused by the refl ection of red blood cells in the retinal blood vessels (MILLER, 2005).
Another pigmentation variation in mammals is leucism, which is characterized by individuals with partial or total discoloration of the skin and/or fur.However, the pigmentation of eyes and claws is normal.Leucism has on occasion been confused with partial albinism and results from a reduction in all types of pigment, while albinism results from only a reduction in melanin production (MILLER, 2005).Worldwide, complete albinism in bats has been recorded in 64 individuals of 38 species (UIEDA, 2000).Most of the recent cases were published in Latin American and Asian countries.
The neotropical bat genus Carollia (GRAY, 1838) currently includes eight species, fi ve of which are known from Brazil.This genus includes some of the most abundant species of mammals and plays an important role in seed dispersal and regeneration of forests.There are three reports of albinism in C. perpicillata (CHARLES-DOMINIQUE et al., 2001;BOADA;TIRIRA, 2010;FALCÃO, 2014).The purpose of this paper is to report a case of complete albinism in Carollia perspicillata (LINNAEUS, 1758), from the Brazilian state of Rondônia, and to provide a brief review of albinism in bats.

Materials and Methods
The review was developed based on a database search of international (PubMed, ScienceDirect and LILACS) and national (SciELO) literature and annals of the most important events related to Chiroptera, between 2001 and 2015, using the following key words: bats, In all three surveyed districts, culverts under the BR364 highway were used as shelters by C. perspicillata colonies.The culvert where the albino specimen was found (UTM 0315841 8963087) is in the Caiçara District, is made of iron and has an internal diameter of 2 m for its entire 20 m length.It has a double opening and was built in the 1980s (Figure 1).Selected individuals roosting in this culvert were tagged with metal rings and their sex, age and reproductive condition were recorded.The environment around the shelter includes a perennial lake originating from the enlargement of the stream on both sides of the shelter, in an Amazon rainforest remnant within an anthropic area.The immediate area contains abundant Piperaceae plants, which constitute the main food source for this species (MIKICK et al., 2003).
The region is categorized as a rainy tropical climate.The average annual temperature ranges from 24°C to 26°C, with little variation throughout the year (only 10°C).The summer is hot and rainy, while the winters are dry and mild.The annual precipitation ranges from 1400 to 2600 mm (INMET, 2017).

Results
Table 1 lists the cases of albinism (complete or partial) recorded for bats worldwide since the review by Uieda (2000), totaling sixty-seven species (151 individuals) from 40 countries.The collected albino individual of C. perspicillata (Zoology Museum of the University of São Paulo, Brazil-MZUSP35367) was a young male (right forearm 40 mm; left forearm 39.5 mm; weight 10 g).It was roosting in a colony of approximately one hundred normally pigmented C. perspicillata.Of these, 39 were females (9 were pregnant, 14 were young, 6 were lactating and had their 10 pups with them) and 12 were males (8 adults and 4 young).

Discussion
The albino C. perspicillata reported in this study was roosting in a culvert.According to a review of albino bats published by Uieda (2000), only six of 64 bats were captured with mist nets while fl ying, and 39 were captured in daytime roosts, such as caves, mines, galleries, buildings, tree holes and bird boxes.The author proposed that these enclosed roosts may be important for the survival of albino bats because they offer protection against sunlight, water loss and predation; this could explain why there are no records of albinism from bat species that preferentially use external roosts.Of the albino specimens reported since the review by Uieda (2000), the majority have been found in enclosed roosts (35 individuals) and just eleven were captured with mist nets or a harp trap (Table 2).
In the review of Uieda (2000) a similar proportion between males (47.4%) and females (52.6%) was observed.Among the reports with information about sex since that review, 27 were females (61.4%) and 17 were males (38.6%) (Table 2).In some species, females live in maternity colonies segregated from the males.This fact suggests that females are more easily captured in relation to males, who live in small groups or in various shelters and locations or are segregated from the colony by dominant males, and could explain the predominance of females over males.Romano et al. (2015) reported an albino individual of Tadarida brasiliensis in an attic inhabited by females during the fi nal stages of pregnancy, parturition, and lactation.
The bat subject of this paper was apparently well integrated into the group, healthy and of normal size for the species.Although albinism may bring disadvantages (UIEDA, 2000), some authors have reported that albino bats live long lives (UIEDA, 2000;PRÉVOST et al., 2011).Among 45 bats where the age was reported, 18 (40%) were classifi ed as adults.This indicates that albino bats can live until an adult age and become integrated into their colonies.
In relation to reproduction of albino bats, Sánches-Hernández et al. (2010) found two reproductively active adult females of D. rotundus and one pregnant A. jamaicensis.Acosta et al. (2011) reported two females, one pregnant and one lactant, of Micronycteris microtis.Miranda et al. (2012) reported two lactant females of Myotis levis.However, an albino female maintained in captivity by Uieda (2001) for 28 months with normally colored males and females did not become pregnant, unlike other females in the group.Based on the review, the majority of the 151 albino individuals, in 27 species, were from the family Vespertilionidae (40.9%).This was also observed by Uieda (2000), probably because of the high species diversity in the family.The number of cases of albinism in D. rotundus is greater than in other species, and includes 12 individuals, considering all records since UIEDA (2000).However, it is unlikely that this represents a higher incidence of albinism in the species, and probably reflects the high sampling rates of a species targeted by a rabies control program.

Albinism in bats
Within the subfamily Carolliinae, there have been reports of albinism in Rhinophylla pumilio (CHARLES-DOMINIQUE et al., 2001), Carollia brevicauda (Soriano et al, 1993) and Carollia sowelli (HERNÁNDEZ-MIJANGOS, 2009).Among the three reported cases of albinism in C. perspicillata, two were cases of complete albinism (FALCÃO, 2014): an adult female, captured in a mist net; and a young male, captured in a shelter of this study.Boada and Tirira (2010) used leucism as a synonym for partial albinism for an adult female captured by a mist net.This work reports the second record of albinism for C. perspicillata in Brazil.Given that albinism is a rare hypopigmentary disorder, cases should be reported to increase the knowledge of such variation in bats.

A
. R. Rosa et al.When making the eight collections in this shelter where the albino bat (Figure 2) was found, the population of C. perpicillata varied from 50 and 200 individuals.While collecting in August 2011 and July 2014, cohabitation of C. perspicillata with a few (5 to 10) specimens of Glossophaga soricina (Pallas's long tongued bat) and 10 to 50 specimens of Trachops cirrhosus (fringe-lipped bat) was recorded.

FIGURE 2 :
FIGURE 2: Albino specimen of Carollia perspicillata showing the presence of translucent dactylopatagium and red eyes (Photograph by Patrício Rocha).
Chiroptera, albinism and hypopigmentation.This period was selected because the last list of rabies positive bats for Brazil byUIEDA et al. was published in 2000.

TABLE 1 :
Records of albinism (complete or partial) in bats according country of collection.
* AccordingMarin-Vasques et al. (2010), some of these reports represent cases of leucism.** These authors used leucism as a synonym for partial albinism.

TABLE 2 :
Data of records of albino bats according type of shelter and capture, sex and type of albinism.