Print
First record of albinism for the doglike bat, Peropteryx kappleri Peters, 1867 (Chiroptera, Emballonuridae)
expand article infoLeopoldo Ferreira de Oliveira Bernardi, Xavier Prous§, Mariane S. Ribeiro§, Juliana Mascarenhas|, Sebastião Maximiano Correa Genelhú, Matheus Henrique Simões§, Tatiana Bezerra§
‡ Universidade Federal de Lavras, Minas Gerais, Brazil
§ Vale, Environmental Licensing and Speleology, Nova Lima, Brazil
| Unaffiliated, Nova Lima, Brazil
¶ Unaffiliated, Belo Horizonte, Brazil
Open Access

Abstract

Albinism is a type of deficient in melanin production could be the result of genetic anomalies that are manifest as the absence of coloration of part or the entire body of an organism. This type of chromatic disorder can affect several vertebrate species, but is rarely found in nature. Among bats, more than 450 cases of total or partial loss of body pigmentation have been reported. Herein we provide the first report of albinism for the bat species Peropteryx kappleri (Chiroptera: Emballonuridae) with two such specimens being observed from iron formation caves in a conservation unit “Floresta Nacional de Carajás”, Amazon forest, northern of Brazil.

Keywords

Chiroptera, Peropteryx, hypopigmentation, Neotropics, Amazonia, cave

Deficiency in melanin production is a rare among vertebrates. Such a condition can cause changes in the coloration of specific body parts, such as skin, hair, feathers, scales or the eye, and can even reach extreme cases where there is complete absence of pigmentation throughout the entire body. Changes in body color caused by deficient melanin production can generate several conditions, which (Lucati and López-Baucells 2017) has classified into four types: true albinism, leucism, piebaldism and hypomelanism. All types of melanin production deficiency are hereditary and genetic (congenital) abnormalities. Such disorders have been observed in numerous species of wild mammals throughout the world, including marine (Fertl and Rosel 2002, Abreu et al. 2013), terrestrials (Lopucki and Mróz 2010, Abreu et al. 2013, Neves et al. 2013, Xu et al. 2013, Camargo et al. 2014, Nedyalkov et al. 2014, Sayyed et al. 2015, Kumar et al. 2016, Romero et al. 2018, Oliveira et al. 2019) and bats (Uieda 2000, Murariu and Chisamera 2006, McCardle 2012, López-Baucells et al. 2013, Ramasindrazana et al. 2014, Rengifo et al. 2014, Smirnov et al. 2014, Zalapa et. al. 2016, Lucati and López-Baucells 2017).

Chromatic aberrations that lead to albinism in bats have been reported in 61 species of 10 families (Rhinolophidae, Hipposideridae, Rhinopomatidae, Emballonuridae, Nycteridae, Phyllostomidae, Mormoopidae, Molossidae, Miniopteridae, and Vespertilionidae), in a great number of countries worldwide, but they continue to be a rarely observed event (Uieda 2000, Rosa et al. 2017, Nascimento et al. 2018, Zortéa and Silva 2018). Although these aberrations interfere with the coloration of the animals, there have been, to date, no marked negative effects of this genetic inheritance that could compromise the survival of bats in the natural environment (Uieda 2001).

There have been 31 reports of the absence of melanin pigmentation for 17 species of bats in Brazil (Uieda 2000, Rosa et al. 2017, Nascimento et al. 2018, Zortéa and Silva 2018). Of these records, 20 were cases of albinism (t-inherited, hypopigmentary disorder characterized by a complete lack of melanin caused by the absence of the enzyme tyrosinase; it results in pale skin, white fur or feathers, and red eyes) and 11 case of piebaldism (total lack of melanin in part of the skin and/or hair follicles due to the absence of melanocytes in the affected part) (Lucati and López-Baucells 2017; Rosa et al. 2017; Uieda 2000; Zortéa and Silva 2018). This article reports the observations of two albino individuals of Peropteryx kappleri Peters, 1867, which increases the number of individual records of albinism in bats in Brazil to 33. Furthermore, it represents the first report of albinism for the genus Peropteryx and the third report in the world for the family Emballonuridae (Zortéa and Silva 2018) (Table 1).

Records of albino bats in Brazil.

Species Disorder No individuals Location Reference
Artibeus cinereus Albinism 1♂ flyway Oliveira and Aguiar 2008
Artibeus concolor Piebaldism 1♂ flyway Zortéa and Silva 2018
Artibeus jamaicensis Albinism 1? tree Uieda 2000
Artibeus planirostris Albinism 1 Uieda 2000
Artibeus lituratus Piebaldism 1♂ flyway Souza et al. 2013
Carollia perspicillata Piebaldism 1♀ cave Rocha et al. 2013
Carollia perspicillata Albinism 1♀ flyway Falcão 2014
Carollia perspicillata Piebaldism 1♀ flyway Zortéa and Silva 2018
Carollia perspicillata Albinism 1? tunnel Rosa et al. 2017
Dermanura cinerea Albinism 1? Oliveira and Aguiar 2008
Desmodus rotundus Albinism 2♂, 1♀, 1? 1 cave, 1 flyway, 1? Uieda 2000, 2001
Desmodus rotundus Albinism 1♂ cave Uieda 2000, 2001
Desmodus rotundus Albinism 1? flyway Moreira et al. 1992
Eumops glaucinus Albinism 1♂ Sodré et al. 2004
Gardnerycteris crenulatum Albinism 1 flyway Zortéa and Silva 2018
Molossus molossus Albinism 1 hollow tree Veiga and Oliveira 1995
Molossus molossus Albinism 1♀ hollow tree Uieda 2000
Molossus molossus Albinism 1♀ flyway Nascimento et al. 2018
Myotis levis Albinism 1? Miranda et al. 2012
Nyctinomops laticaudatus Piebaldism 2 ♂, 3 ♀ building Geiger and Pacheco 2006
Peropteryx kappleri Albinism 1♂ cave Present data
Peropteryx kappleri Albinism 1 young cave Present data
Phyllostomus discolor Piebaldism 1♀ flyway Treitler et al. 2013
Tadarida brasiliensis Piebaldism 1? Zortéa and Silva 2018
Tonatia saurophila Piebaldism 1? flyway Zortéa and Silva 2018

The albino bats were observed in Floresta Nacional de Carajás (FLONA-Carajás), which is located completely within the Amazon Forest domain in the state of Pará, North Brazil. (Figure 1). The FLONA-Carajás, created by Decree No. 2,486 of February 2, 1998, has more than 390,000 hectares and is a Conservation Unit for sustainable and diversified use of forest resources and scientific research. The main vegetation cover of the region is the Ombrophilous Forest, with local variations, the majority associated with changes in the relief. The forest areas are intercepted by rock outcrops of iron ore, which has a high economic interest. In these outcrops are concentrated the caves of the region, with mining being the main impact on this important habitat for some species of bats. One of the main purposes for creating FLONA-Carajás was to protect the environment and allow multiple uses of the forest, including the extraction of iron ore in a way that is minimally damaging to the environment, with emphasis on methods for sustainable exploitation of native forests (ICMBIO 2017). However, during the iron ore extraction some caves have been supressed, this proceeds are allowed in this type of conservation unit area. And with the intention of keeping some forest areas and caves undisturbed, was established around of FLONA-Carajás the Carajás Ferruginous Fields National Park, created on June 5, 2017, with 80,000 hectares (Figure 1). In this new protected area are inserted hundreds of caves preserved as an environmental compensation and the iron ore extraction is commercial use of the forest is not allowed.

Figure 1. 

Location of the caves where the specimens of Peropteryx klaperi were observed in the municipalities of Parauapebas (cavern PESE–0004) and Canaã dos Carajas (cavern S11D–0007), in southeastern Pará, Brazil.

Species surveys at the site have been routine, but since 2008 faunal studies have intensified in the caves of the region, mainly in association with environmental licensing and monitoring. As a result, knowledge of the local chiropterofauna has increased and to date faunal surveys have been carried out in more than 1,000 caves in FLONA-Carajás, in addition to several projects involving the survey of chiroptera in epigeal environments. To date, a total of 75 species of bats have been recorded in FLONA-Carajás, of which 23 were recorded in caves, including those of the genus Peropteryx (Tavares et al. 2012).

The albino bats were observed in 2016 and 2017 in two caves located in FLONA-Carajás; one in a cave in the municipality Parauapebas and the other in the municipality of Canaã dos Carajás, both in the state of Pará, Brazil (Figure 1). The first observation was made on 04 September 2016 and was of an adult male P. kappleri found in cave PESE–0004 (06°06'19.22"S; 50°09'5.96"W) (forearm measurement; 47,5 cm). The second observation was made on 23 October 2017 and was of a young P. kappleri found in cave S11D–0007 (06°24'06.42"S, 50°21'06.09"W) (no measurements were made).

The specimens were observed hanging on walls inside the caves and last than 5 metres from the entrance. The adult male was solitary, while the juvenile was close to other conspecific individuals with normal coloration. Both individuals had complete albinsm, including reddish eyes, which are typical features of albinism (Figure 2). Aside from the obvious morphological differences of albino bats (i.e., coloration), no other differences were observed for the individuals during the brief period during which they were observed in the field (not more than 30 minutes), not even in their behavior. The observed individuals were not euthanized since the legal authorization of the research only permitted the capture of bats for purposes of identification, with the collection of specimens being allowed only for cases of taxonomic doubt (ABIO 639/2015 and ABIO 455/2014). The adult specimen were captured and measurement were taken to confirm the condition, but the juvenile was simply observed during campaigns to monitor cave fauna.

Figure 2. 

Albino specimens of Peropteryx observed in caves of Floresta Nacional de Carajás. A–C male specimen of Peropteryx kappleri D juvenile specimen of Peropteryx kappleri.

Bats of the genus Peropteryx spp. are very common in the entrances to caves in the region of Carajás, and have been observed in more than 600 caves. Nonetheless, despite this significant effort, there have been no other reports of albino specimens, which are testimony to the rarity of this condition in this group of animals, as demonstrated by Uieda (2000) and Lucati and López-Baucells (2017), highlighting the importance of these records.

The influence or not of albinism in bat individual fitness should be better evaluated, that’s because lack of skin pigmentation could promote a major disadvantage to animals in the wild habitat, the most obvious being an animal’s lack of crypsis with its surroundings, protects sun rays and lost of accuracy of eyesight (Uieda 2000, Sandoval-Castilho et al. 2006, Acevedo et al. 2009). However, bat animals have prevalent are nocturnal behaviour so the absence of pigment may not be interfere is significantly with individual fitness. Furthermore, bats seek for a daytime shelter in a variety of habitats, and caves could offer protection against sunlight, water loss, and visual hunting predators (Uieda 2001), promoting better chances to survive.

Acknowledgements

We thank Reginaldo Marins, Paulo Leite, José Macedo and Bruno Henrique for assistance during field activities; Carlos Frederico for help to the elaboration of the map of the study area; VALE S.A. for financial support and the promotion of research; and Brandt Meio Ambiente e Ativo Ambiental for logistic support during field activities in FLONA Carajás. We also thank IBAMA and ICMBIO for authorizing the research, and the Federal University of Lavras (UFLA), the Coordination of Improvement of Higher Level Personnel (CAPES) and the National Council for Scientific and Technological Development (CNPq) for providing financial support and scholarships.

References

  • Abreu MSL, Machado R, Barbieri F, Freitas NS, Oliveira LR (2013) Anomalous colour in Neotropical mammals: a review with new records for Didelphis sp (Didelphidae, Didelphimorphia) and Arctocephalus australis (Otariidae, Carnivora). Brazilian Journal of Biolology 73(1): 185–194. https://doi.org/10.1590/S1519-69842013000100020
  • Camargo I, Rios E, Cornejo-Latorre C, Álvarez-Castañeda ST (2014) First Record of Leucism in the Genus Peromyscus (Mammalia: Rodentia). Western North American Naturalist 74(3): 366–368. https://doi.org/10.3398/064.074.0301
  • Falcão FC (2014) First record of complete albinism in Carollia perspicillata (Chiroptera, Phyllostomidae). Chiroptera Neotropical 20(1): 1234–2136.
  • Fertl D, Rosel P (2002) Albinism. In: Perrin WF, Würsig B, Thewissen JGM (Eds) Encyclopedia of Marine Mammals, Academic Press, San Diego, 16–18.
  • Geiger D, Pacheco SM (2006) Registro de albinismo parcial em Nyctinomops laticaudatus (E. Geoffroy, 1805) (Chiroptera: Molossidae) no sul do Brasil. Chiroptera Neotropical 12(1): 250–254.
  • ICMBIO [Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis] (2017) Plano de pesquisa geossistemas ferruginosos da Floresta Nacional de Carajás: Temas prioritários para pesquisa e diretrizes para ampliação do conhecimento sobre os geossistemas ferruginosos da Floresta Nacional de Carajás e seu entorno. Brazil, 82 pp.
  • Kumar K, Vaishnav V, Ojha AP, Parihar P, Barmera R, Parihar GR (2016) Occurrence of Albino Gazella bennetti in Viratra mata Oran (Sacred land) of Chohtan, Barmer (Thar Desert of Rajasthan). India International Journal of Environmental & Agriculture Research 2(11): 87–90.
  • López-Baucells A, Mas M, Puig-Montserrat X, Flaquer C (2013) Hypopigmentation in vespertilionid bats: the first record of a leucistic soprano pipistrelle Pipistrellus pygmaeus Barbastella 6(1): 66–72. https://doi.org/10.14709/BarbJ.6.1.2013.09
  • Lopucki R, Mróz I (2010) Cases of colouration anomalies in small mammals of Poland, and reasons for their incidence. Annales Universitatis Mariae Curie-Sklodowska 65(1): 67–76. https://doi.org/10.2478/v10067-011-0006-4
  • Lucati F, López-Baucells A (2017) Chromatic disorders in bats: a review of pigmentation anomalies and the misuse of terms to describe them. Mammal Review 47: 112–123. https://doi.org/10.1111/mam.12083
  • McCardle H (2012) Albinism in wild vertebrates. Texas State University, San Marcos 72pp.
  • Miranda JMD, Kaku-Oliveira NY, Munster LC (2012) Primeiros dados de uma colônia reprodutiva de Myotis levis (I. Geoffroy, 1824) nos campos de Palmas, Paraná, Brasil (Vespertilionidae). Chiroptera Neotropical 16(2): 762–768.
  • Moreira EC, Silva MCP, Veloso JG (1992) Albinismo em Desmodus rotundus rotundus, Chiroptera (E. Geofroy, 1810). Arquivo Brasileiro de Medicina Veterinária de Zootecnia 44: 549–552.
  • Murariu D, Chisamera G (2006) Partial albinism in noctule bat – Nyctalus noctula (Schreiber, 1774) (Mammalia: Chiroptera) from Romania. Travaux du Muséum National d’Histoire Naturelle 49: 353–357.
  • Nascimento ACS, Dourado ÂCM, Trevelin LC, Bezerra AMR (2018) First record of total albinism in Molossus molossus (Chiroptera: Molossidae) from northeastern Brazil. Boletim do Museu Paraense Emílio Goeldi. Ciências Naturais 13: 273–277.
  • Nedyalkov N, Koshev Y, Raykov I, Bardarov G (2014) Color variation of small mammals’s (Mammalia: Rodentia and Insectivora) coats from Bulgaria. North-western Journal of Zoology 10(2): 1–4.
  • Neves ACSA, Coutinho LC, Oliveira MB, Pessôa LM (2013) First report of partial albinism in genus Thrichomys (Rodentia: Echimyidae). Papéis Avulsos de Zoologia 54(9): 107–110. https://doi.org/10.1590/0031-1049.2014.54.09
  • Oliveira HFM, Aguiar LMS (2008) A new case of complete albinism in a bat from Brazil. Chiroptera Neotropical 14: 421–423.
  • Oliveira LS, Varjão LCG, Pereira LCM, Nicola-Pereira PA (2019) Primeiro registro de leucismo no cachorro-do-mato Cerdocyon thous (Linnaeus, 1766) (Carnivora: Canidae) no Brasil. Biotemas 32(1): 93–98. https://doi.org/10.5007/2175-79252019v32n1p93
  • Ramasindrazana B, Wilkinson DA, Beral M, Dietrich M (2014) An albino molossid bat from the southwestern Indian Ocean region Malagasy. Nature 8: 103–104.
  • Rengifo EM, Linares V, Díaz F, Panaifo J (2014) First record of albinism in the Black mastiff bat Molossus rufus E Geoffroy, 1805. Chiroptera Neotropical 20(2): 1288–1291.
  • Rocha PA, Feijó JA, Donato CR, Ferrari SF (2013) Leucism in Seba’s short-tailed bat, Carollia perspicillata (Linnaeus, 1758), from a rock shelter in northeastern Brazil. Chiroptera Neotropica 19: 1151–1153.
  • Romero V, Racines-Márquez CE, Britob J (2018) A short review and worldwide list of wild albino rodents with the first report of albinism in Coendou rufescens (Rodentia: Erethizontidae). Mammalia 82(5): 509–515. https://doi.org/10.1515/mammalia-2017-0111
  • Rosa AR, Martorelli LFA, Almeida MF de, Aires CC (2017) Albinism in Carollia perspicillata (Chiroptera; Phyllostomidae), in the state of Rondônia, Brazil. A brief review of albinism in bats. Revista Biotemas 30: 71–77. https://doi.org/10.5007/2175-7925.2017v30n3p71
  • Sandoval-Castilho J, Mariano-Melendez E, Villavicencio-Garayzar C (2006) New records of albinism in two elasmobranchs: the tiger shark, Galeocerdo cuvier and the giant electric ray, Narcine entemedor. Cybium 30(2): 191–192.
  • Sayyed A, Mahabal A, Nale A (2015) A first record of albinism in Jungle Palm Squirrels Funambulus tristriatus (Rodentia: Sciuridea) from India. ZOO’s PRINT 30(12): 18–19.
  • Smirnov DG, Vekhnik VP, Kurmaeva NM, Baishev FZ (2014) The Detection of Partial Albinism at Three Species of Bats (Mammalia: Chiroptera) in European Part of Russia. Open Journal of Animal Sciences 4: 291–296. https://doi.org/10.4236/ojas.2014.45037
  • Sodré MM, Uieda W, Baldim M (2004) First record of albinism in the bat Eumops glaucinus (Molossidae) from southeastern Brazil. Chiroptera Neotropical 10(1–2): 200–201.
  • Tavares VC, Palmuti CFS, Gregorin R, Dornas TT (2012) Morcegos. In: Martins FD, Castilho A, Campos J, Hatano FM, Rolim SG (Eds) Fauna da Floresta Nacional de Carajás: estudos sobre vertebrados terrestres. Nitro Editora, São Paulo. 156–173.
  • Treitler JT, López-Baucells A, Gomes FS, Tenaçol JF, Rocha R (2013) First record of a leucistic piebald Phyllostomus discolor (Chiroptera: Phyllostomidae). Chiroptera Neotropical 19: 1179–1181.
  • Uieda W (2000) A review of complete albinism in bats with five new cases from Brazil. Acta Chiropterologica 1: 97–105.
  • Xu X, Dong GX, Hu XS, Miao L, Zhang XL, Zhang DL, Yang HD, Zhang TY, Zou ZT, Zhang TT, Zhuang Y (2013) The genetic basis of white tigers. Current Biology 23: 1031–1035. https://doi.org/10.1016/j.cub.2013.04.054
  • Zalapa RSS, Guerrero S, Romero-Almaraz ML, Sánchez-Hernández C (2016) Coloración atípica en murciélagos: frecuencia y fenotipos en Norte yCentroamérica e islas del Caribe y nuevos casos para México y Costa Rica. Revista Mexicana de Biodiversidad 87: 474–482. https://doi.org/10.1016/j.rmb.2016.04.007
  • Zortéa M, Silva MC (2018) Albinism in the striped spear-nosed bat Gardnerycteris crenulatum (Chiroptera: Phyllostomidae) with an updated list of albino bats in the World. Mammalia 82: 78–84. https://doi.org/10.1515/mammalia-2016-0080