First record of pigmentation disorder in the Fringe-lipped Bat Trachops cirrhosus (Spix, 1823) (Chiroptera: Phyllostomidae) from southeast Brazil

Abstract Piebaldism is a genetic pigmentation disorder, which is caused by absence of melanocytes in parts of the skin and/or hair follicles, with eyes and claws normally pigmented. The occurrence of piebaldism in natural populations is rare and the effects on fitness are still unknown. This article reports the first case of pigmentation disorders in the Fringe-lipped Bat Trachops cirrhosus (Spix, 1823) (Chiroptera: Phyllostomidae) caught in Barra do Triunfo, city of João Neiva, northeastern state of Espírito Santo, southeast Brazil.


Introduction
Records of the occurrence of pigmentation disorders in natural populations has grown worldwide (Uieda 2000;Zalapa et al. 2016). Piebaldism is the condition in which the absence of melanin is localized, caused by the absence of melanocytes as a result of genetic mutations, and affects skin and hair follicles. Piebald individuals have a variable distribution of white patches on the body, but the eyes are normally pigmented (Abreu et al. 2013). According to a review of pigmentation anomalies in bats proposed by Lucati and Lópes-Baucells (2016), this condition is normally misclassified as leucism, which is the complete absence of pigmentation in the entire body except on the eyes, which are always normally coloured.
The adaptive significance of coloration in mammals is associated with concealment from potential prey or predators, communication and regulation of physiological processes (Caro 2005). There is a lack of knowledge about evolutionary mechanisms responsible for these aberrant phenotypes and their possible costs and benefits (Bilandžija et al. 2013). Individuals that have pigmentation disorders are expected to show reduced fitness, because the phenotype appears at low frequency in natural populations. In fact, some authors consider that chromatic disorders lead to overexposure and higher predation risk (Marín-Vásquez et al. 2010). Other authors, however, argue that, in dark environments, selection for pigmentation is relaxed, resulting in a variety of colorless forms. Because bats generally select dark roosts and forage at night, their coloration may have no effect on predation or social behaviour (Buys et al. 2002).

Methods
The capture of bats was performed using mist nets placed at ground level inside a small cave in Barra do Triunfo, city of João Neiva, northeastern state of Espírito Santo, southeast Brazil (19°41'35"S and 40°22'17"W, elevation of 204 m), in May 2010. The climate is classified as Tropical (Am in Koppën's classification), with a rainy season in the summer and a short dry season in the winter. Part of the Atlantic Forest Biome, the dominant vegetation is tropical rainforest. The native vegetation of the region is highly fragmented and the cave is located at the edge of a forest fragment.
Two mist nets were opened before nightfall, to intercept the departure of bats from the shelter. Two individuals of T. cirrhosus were collected as voucher specimens and taken to the "Laboratório de Estudos em Quirópteros" (LABEQ) of Universidade Federal do Espírito Santo (UFES), where they were killed following the cervical dislocation protocol, fixed in 10% formalin and preserved in 70% ethanol in the mammal collection.
A female and a male of Trachops cirrhosus were captured and deposited in the collection with the acronyms VP192 and VP193, respectively. The female specimen has a forearm measuring 59.9 mm and weighed 24 g, while the male specimen has a forearm of 62.4 mm and weighed 28 g. The male and female have a similar overall pattern, a characteristic grayish brown coloration. However, while the female shows no trace of chromatic disorder, the male has fur and skin of the ventral region, around the genital area, completely white (Fig. 1). Neither shows signs of reproductive activity.

Discussion
Cases of pigmentation disorder reported in the literature are more frequent in closed habitats such as caves, mines, galleries, buildings and hollow trees (Uieda 2000). Such roosting strategies could enhancing their survival possibilities and increase the frequency of alleles for piebaldism. It also could be explained by the fact that both underground and urban roosts have been more intensively monitored and the number of aberrant bats in nature could be greatly underestimated (Kunz 1982). In this report, specimens of Trachops cirrohosus were captured when leaving their shelter in a cave, suggesting that such a roosting site could offer protection against predation. The species T. cirrhosus is a widely distributed and usually found during bat inventories (Gardner 2007). Due to this, the occurrence of aberrant coloration in this species seems to be very rare (Souza et al. 2013). The individuals of T. cirrhosus were captured in a highly fragmented habitat, and according to Bensch et al. 2004, individuals with piebaldism could be more common in small and isolated populations given that inbreeding increases the likelihood for recessive alleles to be expressed.
These phenotypes remain quite rare in wildlife. Nevertheless, this may have no effect on bats because they use echolocation and forage at night (Buys et al. 2002). As discussed by Souza et al. 2013, the occurrence of adult bats with this feature may mean that this property does not overly increase predation risk in the young to the point of never reaching adulthood. In fact, Brack and Johnson 1990 observed the same albino individual of Myotis sodalis for more than 5 years. Bartonička and Burič 2007 also observed the same albino individual of Rhinolophus hipposideros every year from 2000 to 2007. Sánchez-Hernández et al. 2010 recaptured the same two albino specimens of Desmodus rotundus during 2 years and captured a lactating albino of the same species. Moreover, many authors reported the occurrence of pregnant or lactating bats with abnormal coloration (Brigham and James 1993 ;Talerico et al. 2008;Sánchez-Hernández et al. 2010 ;García-Morales et al. 2012;Lopez-Wilchis and Leon 2012;. These examples indicate that pigmentation disorders may not have a negative effect on reproductive sucess in these species.