Introduction
Diverse faunal groups can show atypical or abnormal coloration on the body; these abnormalities have been classified according to their phenotypic characteristics as albinism, leucism and melanism. In albinism, the pelage and skin are whitish, and the coloration of the eyes is red; in leucism, white spots appear on various regions of the body, but the coloration of the eyes is normal; and in melanism, hyperpigmentation or darkening of hair tones is present (Uieda 2000, Sánchez-Hernández et al. 2010, Tello et al. 2014, Lucati & LópezBaucells 2016, Zortéa & Silva 2018). These pigmentary disorders are attributed to the expression of mutant alleles (Bensch et al. 2000, Moller & Mousseau 2001) or the enzyme tyrosinase absence, which produces melanin in vertebrates (Lucati & López-Baucells 2016, Zalapa et al. 2016). The colour abnormalities have also been attributed to environmental or biological factors (Holyoak 1978, Lucati & López-Bauchells 2016, Moller & Mousseau 2001) such as geographic isolation that limits connectivity between populations, inducing inbreeding (Bensch et al. 2000, Chętnicki et al. 2007).
These chromatic disorders have been reported in individuals of the Phyllostomidae, Mormoopidae, Molossidae, and Vespertilionidae families from North and South America (Caire & Thies 1988, Geiger & Pacheco 2006, Hernández-Mijangos 2009, Idoeta et al. 2011, García-Morales et al. 2012, 2013, Ruelas et al. 2016, Zortéa & Silva 2018, Hernández-Aguilar & Santos-Moreno 2018). For example, in South America, cases of these conditions have been reported in molossids in the genera Molossus, Eumops, Nyctinomops, and Tadarida in Peru (Tello et al. 2014), Brazil (Veiga & Oliveira 1995, Sodré et al. 2004, Geiger & Pacheco 2006, Nascimento et al. 2018), Venezuela (Soriano et al. 1993, Muñoz-Romo et al. 2014), and Argentina (Romano et al. 2015). In frugivorous phyllostomids, these cases have been reported in Venezuela (Muñoz-Romo et al. 2014, Melo-Torres & Salazar-Candelle 2016), Colombia (Roncancio & Ramírez-Chaves et al. 2008, Marín-Vasquez et al. 2010, Velandia-Perilla et al. 2013, Olarte-González et al. 2014, Chacón et al. 2015, Calderón-Álvarez & Marín-Vásquez 2018), Peru (Medina & López 2008, Ruelas et al. 2016), Argentina (Barquez et al. 2003), and Brazil (Oliveira & Aguiar 2008, Souza et al. 2013, Rocha et al. 2013, Falcão 2014, Rosa et al. 2017) in various species in the genera Sturnira, Artibeus, and Carollia.
In Ecuador, three cases of atypical colorations have been recorded in bats, all belonging to the Phyllostomidae family: leucism in Carollia perspicillata (Boada & Tirira 2010) and Artibeus fraterculus (Fernández de Córdova et al. 2017) and albinism in Vampyrum spectrum (Brito & León 2014). Here, we report new cases of leucism in Molossus molossus Pallas, 1766 and Stunira bakeri Velazco and Patterson, 2014 from the lowland of western Ecuador; these are the first documented cases of leucism in these bat species in Ecuador.
Materials and methods
The leucism cases were recorded in three localities from lowland of western Ecuador:
Bosque Protector Cerro Blanco (2°10’S; 80°0’W). This is a private reserve, managed by Fundación ProBosque, and it is located at the southernmost end of the Chongón-Colonche Range on the edge of the urban area of the city of Guayaquil, in the province of Guayas. The predominant vegetation is secondary dry forest, with disturbed areas and small mature patches. Sampling was conducted near an artificial refuge, which is close to the main road and residential areas and a less than one kilometer from a mining area. The refuge is an abandoned house built of cement block walls and pillars and roofed with palm leaves, locally known as “cade”. The bats were captured during the rainy season in February 2016.
Cerro Cacharí (1°46’S, 79°27’W). This is private land located eight kilometers from the city of Babahoyo in the province of Los Ríos. This is a forested remnant located in a transition zone between deciduous (dry) forests and evergreen (humid) forests. Cacharí is formed by a small rocky outcrop with fractured plutonic rocks, including a main cave and numerous cracks. The structure forms a small hill in the midst of a floodplain, and there are large areas of rice crops around it. Non-systematic samplings were carried out from December 2016 to June 2018, both in the cave and around the rest of the forest remnant.
Isla Santay National Recreation Area (2°13’S; 79°52’W). This protected area is managed by the Ministerio de Ambiente y Agua de Ecuador. It comprises a wetland located in the Guayas River and has flooded areas, shrub, and dry forest remnants towards the center; it is surrounded by mangroves. Isla Santay is between two large cities, Guayaquil y Eloy Alfaro (Durán), in the province of Guayas. The island contains a small community, called “Ecoaldea”; the M. molossus individuals were captured in the houses of this community. The sampling was carried out in November of 2019.
Bats were caught using mist nets. External morphometric measurements (in mm) were taken using a digital caliper as follows: forearm length (FA), tail length (T), head-body length (HB), foot length (F), and ear length (E). The age class (juvenile, subadult, or adult) was determined by observing the epiphyseal-diaphyseal fusion (Brunet-Rossinni & Wilkinson 2009); the reproductive condition was determined by direct observation of primary sexual characteristics (Racey 2009). We followed the guidelines of the American Society of Mammalogists (Sikes et al. 2016) for animal handling.
The molossids were identified as Molossus molossus based on the following morphological and morphometric characteristics: smooth upper lip without grooves, small, rounded ears rising from the same point on the forehead, antitragus taller than wide, bicolored fur, and forearm length (FA) between 35 - 40 mm. These characteristics distinguish M. molossus from other species in the same genus that also inhabit western Ecuador, such as M. bondae, which has fur of a single color, and M. rufus, which has a FA greater than 50 mm (Eger 2008; Díaz et al. 2016; Tirira 2017). The populations of M. molossus that dwell in the western Andes in Ecuador are recognized as M. m. daulensis (Brosset 1965; Eger 2008). Before release, each individual was photographed, except for MZUGM-605.
The specimen of Sturnira was identified as S. bakeri due to the following characteristics: tetracolored dorsal hair, observable in stereo microscope, short and woolly fur approximately 5 mm in length between the shoulders, tricolor ventral hair, sparsely hairy forearm, dorsal surface of the femur, tibia, and foot densely covered by long hairs, IV metacarpal shorter than III metacarpal, and somatic measurements (FA, T, HB, F, E) in accordan-
ce with those described for the species. Cranio-dental diagnostic features observed were oval sphenorbital fissure, globular cranial box, narrow face, well-developed sagittal crest, absent anterior process of the glenoid fossa, and metaconid and entoconid in well-defined M1 and M2, separated from each other by a deep notch (Velazco & Patterson 2014; Sánchez & Pacheco 2016; MontoyaBustamante et al. 2017). The collected specimens were deposited in the mammal collection of the Museo de Zoología of the Universidad de Guayaquil (MZUGM).
Results
The caught leucistic individuals of Molossus molossus were six individuals (♀ = 5; ♂ = 1) from Cerro Blanco, one sub-adult female (MZUGM-605) from Cerro Cacharí inside the cave, and ten individuals (♀ = 8, ♂ = 2) from Isla Santay. Table 1 shows external measurements, age, and reproductive conditions of these individuals. The specimens of M. molossus presented white spots or patches on the head, ears, legs, throat, propatagium, and uropatagium; bats from Isla Santay also presented dorsal and ventral fur with silverish tips.
Notes: * Silver-tipped fur on back, ** various small spots on back and underside of right-wing, *** Fuzzy, silver-tipped fur on back, chin, and head.
The specimen of Sturnira bakeri was a pregnant female (MZUGM-705; FA= 44; HB=64.3; F= 17.7; E=15.8; Weight: 31 g), captured with mist-nets in the forest remnant of Cerro Cacharí; the individual presented a whitish-yellowish patch on its dorsal region, from the top of the upper left scapular region to the apophysis of the scapula, in contrast to the coloration normally present in yellow-shouldered bats. Figure 1 shows the individuals with leucism of both species.
Discussion
Bats with chromatic disorders have not been reported before in reserves from western Ecuador (Carrera et al. 2010, Fernández de Córdova et al. 2017, Parker & Carr 1992, Salas 2008). Our leucistic individuals from Guayas represent the first cases for this geographical region, and were not apparently related to external morphology, age or reproductive condition (Eger 2008; Velazco & Patterson 2014; Díaz et al. 2016; Tirira 2017; García-Morales et al. 2012, 2013; Sánchez-Hernández et al. 2010).
The chromatic abnormalities found in M. molossus were observed in different body regions (ears, tragus, throat, chest, abdomen, back, wings, legs, propatagium, uropatagium), and constitute the first known cases of leucism for this species. Previously, only albinism cases had been reported in M. molossus (Nascimiento et al. 2018, Soriano et al. 1993, Veiga & Oliveira 1995, Tello et al. 2014). The appearance of this condition in various individuals during a single sampling, near their known refuge was remarkable (Lucati & López-Baucells 2016, Uieda 2000, Zalapa et al. 2016), so it is likely they belonged to the same colony.
In contrast to the leucistic M. molossus individuals, the Sturnira bakeri specimen was not captured near its refuge, but rather on its flight path through the forest, which is infrequently recorded for bats (Rose et al., 2017). Our report of leucism in S. bakeri is the first for the species, since previous cases have been recorded in different species of Sturnira such as S. hondurensis (García-Morales et al. 2012), S. erytrhomos (Barquez et al. 2003; Roncancio & Ramírez-Chaves 2008), S. parvidens (Zalapa et al. 2016), and S. lilium (Medina & López 2008; Melo-Torres & Salazar-Candelle 2016), in pregnant females, males, and subadults of these species.
Although chromatic aberrations in bats seem to be a worldwide phenomenon, South America has a significant information gap (Lucati & López-Baucells 2016), and the little known comes from last few years (Hernández-Aguilar & Santos-Moreno 2018, Rose et al. 2017, Ruelas et al. 2016, Tello et al. 2014, Zortéa & Silva 2018). Therefore, these chromatic disorders and their causes should be investigated in order to complement available data on the subject.