First record of albinism in Lesser Woolly Horseshoe Bat Rhinolophus beddomei (Chiroptera: Rhinolophidae) with an updated list of chromatic aberrations in bats in India

: There have been worldwide reports of chromatic aberrations in bats, most striking among which is albinism. Albinism is an inherited, hypo-pigmentary state characterised by a complete lack of melanin. Albinistic individuals have pale skin, white fur, and pinkish-red eyes. Here we report the first record of albinism in Lesser Woolly Horseshoe Bat Rhinolophus beddomei. During a bat survey in Goa, India; a single individual of albino Lesser Woolly Horseshoe Bat was recorded along with a normally coloured conspecific individual from a small shelter with tiled roof. We confirm the species identity of this bat based on its morphology, and acoustic characteristics of its echolocation call. We further update the list of colour aberrations in bats reported from India.


INTRODUCTION
Abnormal pigmentation of skin and its derivatives are results of chromatic disorders (Rook et al. 1998).They are caused either by a deficiency or an excess of melanin (Hofreiter & Schöneberg 2010; Abreu et al. 2013).These are reported in many vertebrate groups and classified under broad terms such as hypopigmentation and hyperpigmentation (Uieda 2000).Based on the mutations and phenotypic effects, pigmentation disorders can be classified as albinism, leucism, piebaldism, hypomelanism and melanism (Lucati & Lopez-Baucells 2016).Hypopigmentation cases are, however, most easily detected.Pigmentation disorders and unusual coloration occur because of mutations in genes expressing for skin and fur coloration in animals (Fertl & Rosel 2002;Alexis & Marin-Vasquez 2018).
Albinism is an inherited, hypo-pigmentary disorder characterised by a complete lack of melanin.It is caused by absence of the enzyme tyrosinase that causes individuals to have pale skin, white fur or feathers, and pinkish -red eyes ( van Grouw 2006van Grouw , 2013;;Hofreiter & Schöneberg 2010).Albinism is controlled by an autosomal recessive gene ( van Grouw 2006;Falcão 2014).Due to their nocturnal and cryptic habits, bats with atypical colouration are difficult to observe, and reports on aberrant bat skin and hair colouration are very infrequent.Though many reports of albino bats have come from different parts of the world, records of albinism in Indian bat species are scarce (Khajuria 1972(Khajuria , 1984;;Karim 1983;Bhati 1988;Senacha & Purohit 2005;Aul & Marimuthu 2006;Devkar et al. 2011;Dhanya et al. 2015;Singh & Yadav 2016;Mahabal et al. 2019).Also, some workers have suggested that albinism is rare in bats (Uieda 2000;Devkar et al. 2011;Tello et al. 2014).According to recent reviews, of the approximately 1,300 species of bats in the world, chromatic aberrations have been reported from 115 species belonging to 11 families (Lucati & Lopez-Baucells 2016) and albinism has been described in 60 species (Zortea & Silva 2017).
Here we report a case of albinism in the Lesser Woolly Horseshoe Bat Rhinolophus beddomei.This paper presents the first record of chromatic aberration seen in this species.We provide an updated list of chromatic aberrations in bats reported from India for referral purpose.

MATERIALS AND METHODS
During a reconnaissance survey of bats in South Goa on 29 October 2023 at 1630 h (IST), we observed a pair of Lesser Woolly Horseshoe Bat Rhinolophus beddomie Andersen, 1905 roosting in a small shelter with tiled roof (15.24643056˚N & 74.21220833˚ E) in a horticultural landscape (Figure 1 & Image 1).The shelter had two rooms with one used as a pump house, and the other as an unused lavatory.The temperature and humidity of the roost site were measured using a digital thermohumidity meter (Aceteq).Echolocation calls were recorded using Echo Meter Touch 2 (Wildlife Acoustics, USA).The recorded calls were analysed using Raven Pro 1.6.5 software.Frequency of maximum energy (FMAXE, in kHz) and duration (d, in ms) were considered as bioacoustics parameters (Wordley et al. 2014).

RESULTS
The temperature and humidity in the room where the bats roosted were 33.2˚C and 75%, respectively.The pair of bats was clinging on to the Coconut Palm Cocos nucifera wood frame beneath the roof tiles at the height of 2.5 m above ground.Each individual occupied a separate wood frame, separated by a distance of 0.5 m (Image 1).The pelage and patagium of the normally coloured individual were typically dark greyish-brown and woolly, rough-textured, and notably grizzled on the upper side (Image 2).The albino individual had white skin, fur on its entire body and pale pinkish ears and eyes.In this individual, the blood vessels were seen through the skin of the patagium (Image 3).Both the individuals of the pair had similar body sizes, and were identified as the Lesser Woolly Horseshoe Bat, based on the distinctive morphological features (Bates & Harrison 1997;Srinivasulu et al. 2010) (Images 2 & 3).The owner of this shelter revealed that this albino individual has been roosting in this place since last five years.
Lesser Woolly Horseshoe Bat echolocation call has Frequency-modulated (FM) and Constant-frequency (CF) components.Since bat ultrasonic sounds are species specific, we also recorded the bioacoustics aspect.The characteristics of recorded calls were typical FM/CF/FM, emitted by Rhinolophid bats; with a short upward FM sweep followed by a long CF component, followed by a short downward FM sweep as previously corroborated (Raghuram et al. 2014;Srinivasulu et al. 2023) (Image 4).The calls (n = 20 pulses) had a mean FMAXE of 41.00 kHz, and a mean duration of 84.11 ± 7.6 ms.The observed  attributes tally with acoustic signature of Rhinolophus beddomei.
In India, chromatic aberrations in bats have been reported among eight species, one of Megachiroptera and seven species of Microchiroptera.Thus far a total of 14 individuals have been reported with cases of chromatic aberrations, 11 of albinism and three of piebaldism.

DISCUSSION
Pigmentation anomaly is a rare phenomenon in nature; however, studies have reported such cases in bats from different parts of the world.In their robust global review, Zortea & Silva (2017) have listed 60 species of bats with cases of albinism.Lucati & Lopez-Baucells (2016) have listed 269 individual records of piebaldism, 152 of albinism, 94 of melanism, 20 of hypomelanism, 11 of leucism, and three of partial melanism; in 60 bats the chromatic disorder being 'undetermined'.After both these reviews, there have been more reports of albino bats from across the world (Cichocki et al. 2017;Moreno et al. 2020;Aguilar-lopez et al. 2021;Leal & Ramalho 2021;Leal et al. 2021;Ventorin et al. 2021).
From India, including the present study, cases of chromatic aberrations have been reported in only eight species of bats (Table 1).Of the 14 individuals with chromatic aberrations listed, 11 are of albinism and three of piebaldism.Senacha & Purohit (2005) had incorrectly reported three individuals of Rhinopoma hardwickii as cases of partial albinism, however subsequently it has been revised as piebaldism (Lucati & Lopez-Baucells 2016;Mahabal et al. 2019).The reported cases from India are from families: Pteropodidae, Rhinolophidae, Hipposideridae, Rhinopomatidae, and Emballonuridae.In India most cases of albinism have been reported in Hipposideridae, followed by Rhinopomatidae.
The present study is the first record ever for albinism in Rhinolophus beddomei across the globe, and the first record of chromatic aberrations reported from bats in Goa, India; increasing the cases of albinism in rhinolophids to five.Chromatic aberrations are designated based on the phenotypic effect.The individual in this study presented pale pinkish coloured eyes.In albino individuals, the phenotype shows allwhite hairs, pale skin and pinkish-red eyes (Lucati & Lopez-Baucells 2016;Moreno et al. 2020).Previously for the Genus Rhinolophus, albinism has been reported from Little Japanese Horseshoe Bat Rhinolophus cornutus (Sawada 1990), Mediterranean horseshoe bat Rhinolophus euryale (Dorst 1957), Greater horseshoe bat Rhinolophus ferrumequinum (Allen 1939;Fontanel 2001;Frontera 2002;Prevost et al. 2011), and Lesser Horseshoe Bat Rhinolophus hipposideros (Horaček 1995;Redant 2002).
Efforts at compiling systematic records of pigmentary anomalies in bats is low, and the ecological implications of these anomalies remain unclear (Romano et al. 1999).Most of the bat species in which albino individuals were recorded, including the present study; occupy sheltered roosts like caves, mines, and buildings (Uieda 2000).The absence of pigmentation could present a disadvantage for concealment, communication, and physiological regulation (Caro 2005).Some workers theorise that hypopigmentation is detrimental to bats; due to poor J TT vision, greater predation risk, lower mating success and lower survival rates (Caire & Theis 1988;Caro 2005;Oliveira & Aguiar 2008).Also, Oliveira & Aguiar (2008) suggest that sheltered roosts offer a clear advantage for the survival of albino bats, providing them protection against sunlight, water loss, and predation.However, there is no validation of such putative effects in bats with hypopigmentation or any chromatic aberrations.López-Baucells et al. (2013) argue that pigmentary disorders hardly influence survival of species that are affected.
Insectivorous bats use echolocation for orientation and foraging; and as such hypopigmentation may have no effect on their survival (Lucati & Lopez-Baucells 2016).Though, a lack of pigment in the eyes may negatively affect vision in fruit eating bats, as they rely heavily on vision and olfaction to navigate and forage (Guillery 1996;Rydell & Eklöf 2003;Heiduschka & Schraermeyer 2008;Moreno et al. 2020).Albinism is a rare inherited abnormality and its frequency of occurrence could likely be increased with inbreeding (Stevens et al. 1997).For this reason, it could be more common in colonial species of bats where individuals have strong fidelity to their roosts.
That the albino bat reported in this study has been seen in the same place by the farm owner for the past five years, clearly hints at site fidelity, and this merits discussion.Brack & Johnson (1990)  in Guerrero (Mexico), all these reports highlighting no effect of colour aberration and establishing that albino bats can survive for several years.Likewise, there are several reports of pregnant or lactating albino bats, refuting the idea of lower mating success in bats with colour aberrations (Brigham & James 1993;Talerico et al. 2008;Sánchez-Hernández et al. 2010;Rocha et al. 2013).
Efforts towards systematic records of pigmentary anomalies in bats is low, and their ecological implications remain unclear (Romano et al. 1999).Recent times have seen an increased number of publications reporting pigmentation anomalies in bats (Cichocki et al. 2017;Moreno et al. 2020;Aguilar-lopez et al. 2021;Leal & Ramalho 2021;Leal et al. 2021;Ventorin et al. 2021).Such reports are important to understand the evolutionary cost and benefits arising from chromatic disorders.Continuous documentation of chromatic aberrant bats will help understand geographic trends of albinism and allied pigment anomalies in bats, and further appreciate ecological effects of these anomalies on bat survival rates in natural populations (Lucati & Lopez-Baucells 2016).

Figure 1 .
Figure 1.Map showing location of albino and normal coloured Lesser Woolly Horseshoe bat reported in the study.
observed same albino individual of Myotis sodalis in a cave in Indiana (USA) in 1985, 1987 and 1989, Sánchez-Hernández et al. (2010) recaptured the same two albino individuals of Desmodus rotundus bats in 2008-2009 in a tunnel

Table 1 . Summary of records of chromatic aberration in bats reported from India. Species Chromatic aberration n Sex Habitat Location State/ Union territory Biogeographic zone Reference Megachiroptera Pteropodidae
* One dead individual, no information on sex Journal of Threatened Taxa | www.threatenedtaxa.org| 26 June 2024 | 16(6):