Five albino bats from Guerrero and Colima, Mexico

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1 Five albino bats from Guerrero and Colima, Mexico Cornelio Sánchez-Hernández 1*, María de Lourdes Romero-Almaraz 2, Alejandro Taboada-Salgado 3, José Alberto Almazán-Catalán 1, Gary D. Schnell 4, and Leobardo Sánchez-Vázquez 1 1. Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, A.P , Coyoacán, C.P , México. 2. Escuinapa No. 92 bis. Col. Pedregal de Santo Domingo, C.P , México, D.F., México. 3. Recursos Genéticos y Productividad-Ganadería, Colegio de Posgraduados, Montecillo 56230, Texcoco, Estado de México, México. 4. Sam Noble Oklahoma Museum of Natural History and Department of Zoology, 2401 Chautauqua Avenue, University of Oklahoma, Norman, Oklahoma, 73072, USA. *Corresponding author: cornelio@servidor.unam.mx Abstract Albinism, a hypopigmentary congenital disorder, can be partial (leucism) or complete (amelanism or true albinism). To date worldwide, 70 specimens of 43 bat species have been recorded as complete albinos, with three Pteronotus parnellii, Macrotus waterhousii, and Artibeus intermedius reported from Mexico. We document additional Mexican albinos, including four complete-albino Desmodus rotundus (one male and three females) from the state of Guerrero, and one partial-albino Artibeus jamaicensis from the state of Colima. Albino D. rotundus are known from Trinidad and Brazil, and our four records increase to 11 the known number of albinos, thus making D. rotundus the best represented bat species with the anomaly. Guerrero, with four albino bats, is the only place where more than a single albino bat has been found at the same locality. A subadult male D. rotundus, caught in October 2008, had clean pelage and was unaggressive; it likely had not entered into competitive interactions with other males for females. One adult female D. rotundus, captured in December 2008, was soiled, had several bruises on wings, and was aggressive, possibly reacting to previous agonistic interactions with colony members. She was lactating, suggesting that males in the wild do not discriminate against albino females, as apparently they do in captivity. This bat, released at point of capture, was seen again later in December 2008, as well as in March, May, and June In August 2009, we caught two more female albino D. rotundus, a young juvenile and a lactating adult. The adult was released and caught again in October and December A partial-albino Artibeus jamaicensis, caught in January 2001, was an adult pregnant female, the fourth record of a partial-albino and pregnant bat in Mexico, the first being an Artibeus phaeotis. Keywords: Albinism, Desmodus rotundus, Artibeus jamaicensis, Mexico. Introduction Albinism is a hypopigmentary congenital disorder known to affect a variety of mammals and Aguiar 2008). In the Americas, complete albinism in bats has been recorded in 31 specimens of 16 species (Pteronotus parnellii, and other vertebrates (Allen 1939; Uieda 2000). Rhinophylla pumilio, Desmodus rotundus, It can be partial (leucism) with hypomelanism Macrotus waterhousii, Sturnira erythromos, resulting in a variable distribution of melanin on the body and animals displaying white spots on the skin or white fur tufts on the body (Herreid and Davis 1960; Quay 1970). Albinism also can be complete (amelanism or true albinism), which is characterized by lack of melanin pigment in the Glossophaga longirostris, Artibeus intermedius, A. planirostris, A. cinereus, Antrozous pallidus, Myotis lucifugus, M. sodalis, M. velifer, Eumops glaucinus, Molossus molossus, and Tadarida brasiliensis) in 10 countries (Canada, United States, Mexico, Puerto Rico, French Guyana, eyes, skin, and hair. Given that melanin provides Venezuela, Argentina, Brazil, Cuba, and some protection from ultraviolet radiation, Trinidad; Brigham and James 1993; Uieda 2000; albinos can sunburn easily from overexposure (Uieda 2000). In bats, partial and complete albinism are rare phenomena. Worldwide only 70 complete-albino bats of 43 species have been recorded and, in 24 countries, only a single albino bat has been noted Charles-Dominique et al. 2001; Barquez et al. 2003; Sodre et al. 2004; Oliveira and Aguiar 2008). For Mexico, only three complete-albino bats and four partial-albino bats have been reported (Sánchez et al. 1989; Pozo and Escobedo-Cabrera (Brigham and James 1993; Uieda 2000; Charles- 1998; Hernández-Mijangos 2009). Given Dominique et al. 2001; Barquez et al. 2003; Sodre et al. 2004; Aul and Marimuthu 2006; Oliveira albinism is rare in bats in general and those in Mexico in particular, our purpose is to document 522

2 five additional albinos - four complete albinos and one partial - from Mexico. Material and Methods In 2008 and 2009, as part of an ecological mark-recapture study of bats in Mezcala, Guerrero (municipality Eduardo Neri, 4.3 km southeast of Mezcala, 509m asl, 17º N, 99º W), we visited a 168-m tunnel. It has a single opening and was built in the 1970s by a power-and-light company (Comisión Federal de Electricidad) as part of a planned dam complex that was never completed. Dimensions of the tunnel entrance are 3 3m, with basically the same dimensions throughout the tunnel. At the distal end of the tunnel there is a substantial rock collapse. The tunnel is close to the edge of the Mezcala River (formally Balsas River). Topography in the area is very rough, with hills up to 500 m in height and slopes ranging from Dominant vegetation is tropical deciduous forest, with associations of thorny chaparral and columnar cactus such as Pachycereus weberi and Neobuxbaumia mezcalaensis, and dominant trees of genera Bursera, Pithecellobium, and Acacia. Average temperature ( C) and humidity (%), respectively, inside the tunnel were as follows: October 2008, 29.4 and 86.3%; December 2008; 29.3 and 54.2%; June 2009, 30.1 and 65.4%; August 2009, 29.8 and 70.2%; October 2009, 29.7 and 66.1%; and December 2009, 29.1 and 54.1%. Average annual outside temperature is 28.9ºC, with mean annual precipitation of mm (Meza and López-García 1997). The climate is warm and subhumid with rains in summer. We used insect nets during the day to capture bats at roosting sites in the tunnel. To prevent bats from escaping, the entrance of the tunnel was blocked with a plastic net curtain. One other specimen came from Colima, Manzanillo, 4 km NE La Rosa, 650 m ( N, W). The climate in the area is semiwarm and subhumid with rains in summer. Average annual temperature is 26ºC; January is the coldest month (24.3ºC) and July the warmest (28.5ºC). Mean annual precipitation is mm (Instituto Nacional de Estadística, Geografía e Informática 2009) Results On 24 October 2008, we caught a subadult, albino male D. rotundus (Figures 1 and 2) with abdominal testes in Mezcala, Guerrero (preserved as skin and skull, CNMA [Colección Nacional de Mamíferos, Instituto de Biología, Universidad Nacional Autónoma de México], collector number 2296, J. A. Almazán-Calatán). The bat was located inside the tunnel 75 m from the entrance and was part of a group of about 40 individuals; overall, the colony included about 200 of the species located m from the entrance in groups of individuals. Most D. rotundus in the group with the albino flew away when our presence was noted, while the other bats faced us with open mouths exhibiting classic aggressiveness and a defensive position typical of vampires. The albino tried to hide itself among the others, which was only partially successful; this submissive attitude made it easy to catch with the insect net. Figure 1. Subadult male Desmodus rotundus shown at roost site (left) and after capture (right). In our presence after the upper photograph was taken, he attempted to hide among the other bats that were exhibiting aggressive and defensive positions. On 12 December 2008, in the same tunnel and under similar conditions, we caught an albino female D. rotundus (Figure 2) with welldeveloped mammary glands and with milk secretion. She was in a group of about 30 individuals 100 m from the tunnel entrance and 523 took flight several times before we successfully captured her. This bat was marked and released in the same roost after we recorded measurements and other information. She was observed four more times - 27 December 2008, 27 March 2009, 15 May 2009, and 27 June On 27

3 December she was in a group of about 15 individuals, and we did not attempt to catch her. Figure 2. Adult female Desmodus rotundus when first caught in December She was released and observed on four subsequent visits to the tunnel. not aggressive and looked to be in good physical condition, with no injuries to his body, although the left wing had two small holes. In contrast, when caught in December, the female was very aggressive, apparently having no blood in her stomach; she looked thin, her pelage was short and bedraggled, and she had several bruises on her wings. However, when we caught her again in March, the pelage was relatively clean, and she was considerably less aggressive. In June, she again had several wing bruises, and her ears had been bitten and were bloody. The two females caught in August (with one recaptured in October and December) looked healthy and clean; the adult female had some bruises on her wings, but these apparently occurred when we caught her in an insect net. The bat was lactating and pregnant in March; by palpation, the length of the embryo was estimated to be 27 mm. In May the female was in the middle of a group of individuals, and we did not catch her. In June she was lactating and in a group of individuals located m from the tunnel entrance. On 21 August 2009 we caught two more female albino D. rotundus, a young juvenile (Figure 3) and a lactating individual. The juvenile bat (skin and skull, CNMA 44536; collector number 2560, J. A. Almazán-Calatán) could not fly by herself and had a milk-tooth incisor. In addition to incisors, canines, and premolars that had irrupted recently, she had two deciduous incisors (thin and hook-shaped) on each side and exterior to the canines. This juvenile was in a rock crevice about 80 m from the entrance with a group of about 20 individuals that partially covered her, but when the other bats flew she was left along. This zone in the tunnel had most of the D. rotundus (ca individuals), and an accumulation of feces on the tunnel floor confirmed that the site had been used for some time. In this area, D. rotundus were distributed in several groups, most individuals being adults. The captured adult female was released and recaptured at the same place on 17 October 2009, at which time she was sexually inactive. She was in a crevice about 150 m from the tunnel entrance in a group of 40 individuals (mostly adults), exhibiting aggressiveness and a defensive position like the other vampires in the group. She was recaptured again on 5 December 2009 and was lactating. The four D. rotundus were complete albinos, having white pelage and red eyes, as well as wings and uropatagium that were completely white. The veins in the wing were notably red, naked areas were pink, and nails were white. There was a marked difference in the behavior of the initial two albino bats captured. The male was 524 Figure 3. Juvenile female Desmodus rotundus captured in August The tunnel also harbored about 200 Balantiopteryx plicata, which occupied the initial 100 m of the tunnel. They were distributed in several groups of individuals. In addition, about 100 Macrotus waterhousii were present, starting 50 m from the entrance and being distributed through the rest of the tunnel; most were 100 m or more from the entrance. A partial-albino female Artibeus jamaicensis (Figure 4) was collected on 11 January 2001, in Colima (skin and skull, SNOMNH [Sam Noble Oklahoma Museum of Natural History, University of Oklahoma]; collector number 4547, C. Sánchez-Hernández). It was caught in a mist net placed in vegetation of a semideciduous tropical forest. This adult female had an embryo mm with a mass of 3.4 g. The adult had dorsal and ventral hair with white-yellowish tips and lighter bases. The eyes were dark, the rostral lines lighter, and the wings, uropatagium, and naked areas were light brown with white spots; veins were notably pinkish in color. Head, neck, and shoulders had unicolor gold-white hair. The specimen was missing a lower incisor, and all other teeth were worn. External measurements (in millimeters and grams) for the male, young female, and two adult

4 females of D. rotundus, as well as the female A. jamaicensis, respectively, were as follows: total length, 72, 68,,, 79; length of tail, 0, 0, 0, 0, 0; length of foot, 14, 16, 16, 17, 13; length of ear, 19, 15, 17, 18, 21; forearm length, 57.4, 51.0, 60.0, 62.0, 56.2; metacarpal length of third digit, 50.4, 35.2, 54.0, 54.0, 50.7; first phalange length of third digit, 10.3, 8.8, 11.0, 11.0, 16.3; second phalange length of third digit, 17.0, 11.8, 17.0, 18.0, 27.7; third phalange length of third digit, 22.9, 6.6, 16.0, 12.0, 11.6; fourth phalange length of third digit, 3.5, 3.9,, 3.0, 8.1; tibia length, 22.9, 21.8, 23.0, 23.0, 20.2; mass, 18.0, 20.0, 30.0 (lactating in December 2008; 46.0, lactating and pregnant in March 2009; 41.0, lactating in June 2009); 41.0 (lactating in August 2009; 45.0, inactive in October 2009; 42.0, lactating in December 2009), Cranial measurements for the male D. rotundus, juvenile female D. rotundus, and female A. jamaicensis, respectively, were as follows: greatest skull length, 24.20, 22.90, 27.56; condylo-canine length, 18.71, 18.00, 23.65; condylo-basal length, 19.80,, 24.74; braincase breadth, 12.05, 11.50, 11.91; mastoid breadth, 12.05, 11.90, 14.70; zygomatic breadth, 10.63, 8.10, 16.77; skull height, 12.85, 12.00, 12.29; skull depth, 10.50, 10.20, 10.34; interorbital breadth, 6.70, 6.90, 10.46; interorbital constriction, 5.14, 5.50, 6.67; maxillary tooth row length, 5.39, 3.70, 9.73; width across C-C, 5.93, 5.30, 7.15; mandible length, 14.60, 13.10, 18.22; mandibular toothrow length, 6.21, 6.00, 10.31; mandibular height at base of inner incisors, 5.54, 2.20, ; coronoid process height, 5.47, 4.60, 7. 68; and articular process height, 3.76, 2.90, Figure 4. Partial-albino Artibeus jamaicensis captured in January Discussion and Conclusions In Mexico, albinism in bats has been reported previously for seven specimens, three of which were complete albinos - P. parnellii and M. waterhousii cited by Sánchez et al. (1989), and A. intermedius noted by Pozo and Escobedo-Cabrera (1998). D. rotundus represents the fourth species recorded with complete albinism in the country. Albinism in bats is a rare phenomenon as 525 reflected by the fact that the four species represent only 2.9% of the 140 bat species recorded for Mexico. Albino D. rotundus have been recorded for Trinidad (n = 1) and Brazil (n = 6; Uieda 2000), and our four from Mexico increase to 11 the known number of albino vampires, making it the best-represented bat species with such an anomaly. It is unclear whether albinism is more common in D. rotundus than in other bats, or if the number reported reflects a sampling artifact. Given economic and health issues tied to vampires (Romero-Almaraz et al. 2006; Shwiff et al. 2007), the species is well studied, probably more so than any other bat species. The four individuals from Mezcala represent the first time more than a single albino bat has been reported from the same locality. D. rotundus occupies multiple roosts with a strong fidelity to these roosts and to their home range, resulting in stable colony membership (Wimsatt 1969; L.- Forment et al. 1971). Given the economic losses in tropical areas of Latin America due to D. rotundus, management of the species has focused on reducing population sizes in areas of outbreaks of bat rabies in domestic livestock, which could affect genetic diversity of vampire populations and result loss of genetic diversity (Piaggio et al. 2008). Albinism is inherited and its frequency of occurrence likely would be increased with inbreeding (Stevens et al. 1997); if there is in fact a higher incidence of albinism in D. rotundus than in other bats, inbreeding may be at least partly responsible. The two adult-female D. rotundus we found were reproductively active, indicating that males did not spurn them, as apparently was the case for an albino female D. rotundus kept in captivity for 28 months in Brazil with normal males and females (Uieda 2001); the captive albino did not become pregnant, while other females in the group did. Our field observations indicate that female albino bats can be reproductively capable, as also has been demonstrated for an albino female M. lucifugus in Canada that was pregnant (Brigham and James 1993) and an albino female A. intermedius in Mexico that was lactating (Pozo and Escobedo Cabrera 1998). Furthermore, one of the albino female D. rotundus was pregnant and lactating again when subsequently captured. As noted, behavior and physical condition of the initial two D. rotundus we captured were different, with the male being unaggressive and having well-kept pelage, while the female was aggressive and looked disheveled. The latter condition suggests that this female probably did not participate in social-grooming activities typical of vampire groups. Uieda (2001) noted that a female albino D. rotundus in captivity was submissive and had inferior rank within a group;

5 she ate alone only after the normally pigmented bats in the group had fed, although no agonistic interactions were observed. The partial-albino A. jamaicensis is the fifth record for an albino phyllostomid in Mexico, the others being partial-albino Artibeus phaeotis (Sánchez et al. 1989), A. jamaicensis, A. watsoni, and Carollia sowelli (Hernández-Mijangos 2009). The relative lack of records of bats exhibiting this condition is surprising. It may be more common than implied by the number of records but simply unreported. Albino humans usually are sensitive to light (photophobia). Although this has not been demonstrated to be the case in bats, most albino bats have been from sheltered roosts rather than external roosts (Uieda 2000). When we shined light on the group with the albino male D. rotundus, he attempted to hide himself within the group, but whether this was due to light sensitivity or a response to our approach, or possibly both, was not determined. When we took four of the albino D. rotundus outside the tunnel for several minutes to record data and take pictures, they did not close their eyes when exposed to sunlight. Acknowledgements We thank authorities of Mezcala, Guerrero, for facilitating our studies. In addition, we appreciate participation in the field of Michael L. Kennedy, Troy L. Best, Ezequiel Guerrero-Ibarra, Santiago Corona-Salgado, Froylan Cruz-Martínez, Rocío Lumbreras-Ramos, Yuriria Castañeda-Sánchez, Sara Beatriz González-Pérez, and Lizbeth Montoya-Neri. Manuel Espino-Ocampo also was helpful in the field and generously provided a photograph of a roost (Figure 1). Laura Lara- Ortiz and Anacaren Morales-Ortiz provided useful comments on the manuscript, as did two anonymous reviewers. Permits for the study were provided by the Instituto Nacional de Ecología, Dirección General de Vida Silvestre FAUT.0103 to Cornelio Sánchez-Hernández. References Allen G.M Bats. Harvard University Press, Cambridge, Massachusetts. Aul B. and Marimuthu G Sighting of an albino bat in a colony of cave-dwelling microchiropteran, Hipposideros diadema nicobarensis at the Nicobar Islands. Current Science 90: Barquez R.M.; Carrizo L.V.; Ferro L.I.; Flores D.A.; Mollerach M.I.; Sánchez M.S. and García López. A.P Primer caso de albinismo total para Sturnira erythromos (Tschudi, 1844) (Chiroptera-Phyllostomidae). Chiroptera Neotropical 9: Brigham M. and James A.K A true albino little brown bat, Myotis lucifugus, from Saskatchewan. Blue Jay 51: Charles-Dominique P.; Brosset A. and Jouard S Atlas des chauves-souris de Guyane. No. 49. Service du Patrimoine Naturel, Museum d Histoire Naturelle, Paris. Hernández-Mijangos L.A Registros de albinismo parcial en tres species de murciélagos filostómidos (Chiroptera: Phyllostomidae) en Chiapas, México. Chiroptera Neotropical 15: Herreid C.F. II and Davis R.B Frequency and placement of white fur on free-tailed bats. Journal of Mammalogy 41: Instituto Nacional de Estadística, Geografía e Informática Accessed 19 March espanol/estados/col/temp_med_an.cfm?c=1211 &e=06&cfid=737476&cftoken= L.-Forment W.; Schmidt U. and Greenhall A.M Movement and population studies of the vampire bat (Desmodus rotundus) in Mexico. Journal of Mammalogy 52: Meza L. and López-García J Vegetación y mesoclimas de Guerrero. In: Estudios florísticos en Guerrero (edited by Diego N. and Fonseca R.M.), pp Facultad de Ciencias, Universidad Nacional Autónoma de México, México. Oliveira H.F.M. and Aguiar L.M.S A new case of complete albinism in a bat from Brazil. Chiroptera Neotropical 14: Piaggio A.J.; Johnston J.J. and Perkins S.L Development of polymorphic microsatellite loci for the common vampire bat, Desmodus rotundus (Chiroptera: Phylostomidae). Molecular Ecology Resources 8: Pozo C. and Escobedo-Cabrera J.E Albinism in Artibeus intermedius. Bat Research News 39: Q uay W.B Integument and derivatives. In: Biology of bats: Vol. II (edited by Wimsatt W.A.), pp Academic Press, New York. Romero-Almaraz M.L.; Aguilar-Setién Á. and Sánchez-Hernández C Murciélagos benéficos y vampiros: características, importancia, rabia, control y conservación. AGT Editor, S.A., México. 526

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