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Mammalia

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Volume 82, Issue 1

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Albinism in the striped spear-nosed bat Gardnerycteris crenulatum (Chiroptera: Phyllostomidae) with an updated list of albino bats in the World

Marlon Zortéa
  • Corresponding author
  • Programa de Pós-graduação em Biodiversidade Animal, Universidade Federal de Goiás, Regional Jataí, Br. 364 Km 195, Jataí, Goiás, 75801-615, Brazil
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  • De Gruyter OnlineGoogle Scholar
/ Michelly Cristina Silva
Published Online: 2017-01-20 | DOI: https://doi.org/10.1515/mammalia-2016-0080

Abstract

Albinism is a pigmentation anomaly present in all of the main vertebrate groups, including about 4% of bat species. In this article, we described a new case in a Neotropical bat Gardnerycteris crenulatum collected in a savanna of northern Brazil. This bat is an adult male with white and pale yellow fur, red eyes, and white skin on its entire body. We perform a review of the world list of bat species with albinism, which totals 60 species in six continents to this date.

Keywords: albinism; bats; Brazil; Mammalia; Neotropical

Pigmentation anomalies have been described in all of the main vertebrate groups (Uieda 2000). Bats, like other mammals, are susceptible to genetic disorders that affect pigmentation. These include albinism, leucism, flavism, and melanism (Uieda 2000, Zamolo et al. 2013, Tello et al. 2014). Among these conditions, albinism stands out as a rare phenomenon arising from a genetic condition that inhibits or substantially reduces melanin production in the body. This consequentially results in the development of white fur and skin and red eyes (Griffiths et al. 2000, Uieda 2000, Hernández-Mijangos 2009, Tello et al. 2014). Many bat species are known to exhibit cases of albinism, though this condition is rare, affecting less than 4% of the known population (Uieda 2000).

Albinism has been recorded in 11 bat species in four countries of South America: Argentina, Brazil, Peru, and Venezuela (Setzer 1950, Moreira et al. 1992, Soriano et al. 1993, Veiga and Oliveira 1995, Uieda 2000, Barquez et al. 2003, Oliveira and Aguiar 2008, Pautasso et al. 2009, Ramírez et al. 2010, Falcão 2014, Rengifo et al. 2014, Tello et al. 2014, Romano et al. 2015). Of them, six are phyllostomids (Artibeus planirostris, Carollia perspicillata, Dermanura cinerea, Glossophaga longirostris, Desmodus rotundus, and Sturnira erythromos), four are molossids (Eumops glaucinus, Molossus molossus, Molossus rufus, and Tadarida brasiliensis), and one is a vespertilionid (Eptesicus furinalis). Zalapa et al. (2016) recently reviewed the atypical coloring bats of North and Central America and the Caribbean islands, recording 10 albino species.

A bat survey was carried out every 3 months near the municipality of Barra do Ouro (7°45′14″S, 47°50′25″W, 170 m) from 2012 to 2015 in the state of Tocantins, Brazil. Eight mist nets (9×2.5 m) were placed at ground level and opened for 6 h after sunset. This study was conducted under the permission of the Brazilian Federal Wildlife Agency (IBAMA) (license number #024/2011, process number #02029.000555/2011-20) and was in accordance with guidelines of the American Society of Mammalogists for use of wild mammals in research (Gannon and Sikes 2007). A voucher specimen of Gardnerycteris crenulatum was deposited in the Animal Biodiversity Laboratory of the Goiás Federal University (number CJ 1006).

Of the nearly 2000 bats captured, 11 of them belonged to Gardnerycteris crenulatum (six male, and five female). On February 23, 2015, we captured one striped spear-nosed bat with exceptional pigmentation. This bat was an adult male with white and pale yellow fur, red eyes, and white skin on its entire body (Figure 1). The region around the ear and neck had some prominent yellowish fur. The other individuals captured in the same region had the normal color of the species: dark upperparts; blackish brown midback with a pale stripe down from crown to rump; underparts frosted silvery buff; and washed orange (yellowish) around throat (Emmons and Feer 1997). The albino specimen presented a forearm of 44.3 mm and a body mass of 10.1 g. Both these measurements were close to the other five normal male individuals captured in the same area [FA=45.2–45.9 mm (n=4); body mass=9.5–11.3 g (n=3)].

An albino male Gardnerycteris crenulatum with details of red eyes, white skin, and translucent ears.
Figure 1:

An albino male Gardnerycteris crenulatum with details of red eyes, white skin, and translucent ears.

Although the specimen shown in this study did not present the completely white fur, it can be classified as albino according to the phenotypic classification of Lamoreux et al. (2010). The yellow fur of Gardnerycteris crenulatum is different from that attributed to flavism’ cases. Flavism is a type of hypochromatism, with animals presenting yellow or red hair on the insufficiently pigmented skin (Červený 1980). The yellowing color observed in our specimen resembled the color of an individual of Hipposideros diadema recorded by Aul and Marimuthu (2006).

Pigmentation disorder is a rare phenomenon in nature, and its impact on the survival rate is unclear. The low frequency of chromatic aberrations in bats has been associated with negative effects on the fitness and survival of affected individuals. An example of this phenomenon is such as in cases where the albino animal does not meet life expectancy due to its conspicuous appearance. Nevertheless, due to their nocturnal habits and the dark roosts that they generally select, bats are probably less vulnerable to predation than most diurnal animals (Buys et al. 2002, Rocha et al. 2013). Most cases of albinism resulted from studies in enclosed roosts such as caves, mines, and buildings (see Uieda 2000), where that conspicuity provides easy location of the bats for the researchers. Shelters found in foliage and hollow trees are more difficult to locate and access, thus presenting few records of albinism. In fact, there are only two cases of albinism observed in outdoor roosts, Artibeus planirostris (Uieda 2000) and Rhinophylla pumilio (Charles-Dominique et al. 2001). Gardnerycteris crenulatum roost mainly in hollow trees (Goodwin and Greenhall 1961, Handley-Jr 1976), for they provide a shelter that offers protection against visually oriented predators. Hollow trees usually present low incidence of light. Thus, the albino contrast with normal individuals living in the same shelter is not important in these conditions.

Despite the apparent fragility of depigmented animals, several studies describe adult bats, which by itself is already a sign of success of these individuals. Moreover, some studies show that albino animals (or leucistics) have a body size similar to those with normal coloration. The albino bat registered in this study was an adult and had size and weight similar to normal individuals from the same site. Baucells et al. (2013) recorded a leucistic piebald Pipistrellus pygmaeus with weight and forearm length above average on a sample of over 100 individuals. Uieda (2000) mentioned several cases in which albino bats have been observed for several years, which shows that albinism does not necessarily imply a short lifespan for a bat (Buys et al. 2002). Despite these indications, there is not solid evidence that supports negative or positive effects of the albinism on bats (Baucells et al. 2013).

The first citation of albinism in bats appeared in Pryer (1884), a direct observation of three individuals of Nyctinomops plicatus (=Chaerephon plicatus) in a cave. Setzer (1950) in a short note commented superficially about albinism in bats. Walley (1971) conducted a review of species with albinism and leucism, listing 14 albino species. In his article, Walley (op. cit.) listed albinism in two distinct species of Molossus, Molossus fortis and M. tropidorhynchus, actually attributed today as Molossus molossus (Simmons 2005). More recently, Uieda (2000) performed a robust review listing 38 species of bats with albinism in the world. Leblanc and Taupin (2004) revaluated cases of albinism, especially in Europe, increasing to 52 species with this anomaly in the world. Le blanc and Taupin (op. cit.) included much information based on personal communication and even photographic record. Subsequent studies focusing on bats’ albinism include the following works: Buys et al. (2002), Barquez et al. (2003), Hsu (2003); Sodré et al. (2004), Aul and Marimuthu (2006), Oliveira and Aguiar (2008), Alcalde (2009), Pautasso et al. (2009); Gamba-Ríos (2010), García-Morales et al. (2010), Ramírez et al. (2010), Sánchez-Hernandez et al. (2010), Falcão (2014), Ramasindrazana et al. (2014), Rengifo et al. (2014), Tello et al. (2014), Romano et al. (2015), Zalapa et al. (2016); Uieda et al. (in prep.). These studies, including the present study, recognize 60 species of albino bats, i.e. 4.6% of the approximately 1300 species of bats total (Fenton and Simmons 2014).

Table 1 presents an updated list of albino bats of the world. To date, albinism has been described in 60 species of 11 families of bats.

Table 1:

Updated list of bat species with albinism recorded in the world.

There is only one record of Pteropodidae, the other 10 families are Rhinolophidae, Hipposideridae, Rhinopomatidae, Emballonuridae, Nycteridae, Phyllostomidae, Mormoopidae, Molossidae, Miniopteridae, and Vespertilionidae.

Of the seven world continents, albinism has been recorded in six of them (bats do not occur in Antarctica). North and South America had the highest number of species with albinism records with 14 each, followed by Europe with 13 species and Asia with 12 species. Africa and Australia have the lowest number of species of albinism, six and two respectively. One species (Miniopterus schreibersii) had albinism records in two continents (Asia and Australia). However, currently M. schreibersii has been restricted to Eurasian and North Africa populations (Hutson et al. 2008).

With 25 species, the Vespertilionidae family presents the largest number of albinism cases (Table 1). According to Baucells et al. (2013), this higher frequency is probably because most efforts in bat research have historically been carried out with this taxonomical group. However, it is worth highlighting that in addition to cosmopolitan, the Vespertilionidae family has the highest species richness in various regions, such as Europe and the United States. In the Neotropics, where the dominant family is the Phyllostomidae, most species with albinism were verified within this group with 13 species. Thus, in addition to historical aspects of studies, the greatest richness of species within a family is also related to the number of cases of albinism reported.

Acknowledgments

We thank the Estreito Energy Consortium (CESTE) and BIOTA-Projects and Environmental Consulting for carrying out the fieldwork in Barra do Ouro. Several colleagues sent articles and helped us with translations: Carmen Pozo, Christoph Meyer, Corinne Charvet, Cornelio Sánchez-Hernández, Dmitriy G. Smirnov, Jan Zukal, and Wilson Uieda. The Biodiversity Heritage Library for the old publications access. Wilson Uieda and collaborators kindly provided information about albinism in Diaemus youngi. We are grateful to Amanda A. de Melo and Bobbi Jo Bergum for English review, and the BIOTA team for field assistance.

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About the article

Received: 2016-06-15

Accepted: 2016-12-13

Published Online: 2017-01-20

Published in Print: 2017-12-20


Citation Information: Mammalia, Volume 82, Issue 1, Pages 78–84, ISSN (Online) 1864-1547, ISSN (Print) 0025-1461, DOI: https://doi.org/10.1515/mammalia-2016-0080.

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