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Introduction
Among mammals, bats (Chiroptera) represent one of the most diverse groups with more than 1386 species (Burgin et al. 2018). Within this group there is an active and well-developed hearing system known as echolocation (Griffin 1958). This system allows to receive and process ambient sounds using high frequency sound signals, which are amplified and filtered by the outer ear and then oriented towards the middle ear (Moss 2019, Lawrence & Simmons 1982). The outer ear of most bat species consists of two main parts, the pinna and tragus. Tragus is a prominent skin vertical lobe inside the ear (Hutson et al. 2001). The shape and size of tragus vary among species to the extent that differences can be used in taxonomic differentiation of some species (Metzner 1991). According to studies aiming to understand the role of tragus (Müller 2004, Firzlaff & Schuller 2003, Wotton et al. 1995), it has been suggested that this structure can generate specific tracking signals for vertical sound localization to determinate the directionality of the rumbling echoes, although these vary according to the experiment and bat species (Chiu & Moss 2007, Metzner 1991). Alterations in the tragus can cause some degree of change in the transfer characteristics of sound and enough binaural differences to locate a target (Firzlaff & Schuller 2004, Chiu & Moss 2007). Therefore, an anomaly in the tragus can be a serious problem for individuals that develop it, threatening the survivability, but the latter can be influenced by their ecology. In an exceptional case for bats of the genus Rhinolophus that lack tragus, they can compensate the absence of this structure by using highly coordinated movements of the ears (Firzlaff & Schuller 2004).
Among Neotropical bat species, the family Phyllostomidae is characterized by the evolution of complex and differentiated structures for echolocation, and additional adaptation to frugivorous diets (Arias-Aguilar et al. 2016). In general members of the subfamily Stenodermatinae tend to be more colorful than other phyllostomids, and most of these bats are characterized by having white stripes on the face and some species have a white stripe in the middle of the back (Fleming 2003). The ears of Stenodermatinae bats are from small to medium size with rounded edges, often pale and having small tragus (Barquez et al. 1999).
Within Stenodermatinae, the common great fruiteating bat Artibeus lituratus (Olfers 1818) is a large species (forearm = 71.7 mm, weight = 66 g) which is distributed from Central Mexico to southern Brazil, Trinidad and Tobago and the Lesser Antilles (Gardner 2008, Rui et al. 1999). Artibeus lituratus feeds mainly on seeds of the genus Cecropia, Eriobothria, Ficus, Terminalia and Zyzygium (Heithaus et al. 1975, Galetti & Morellato 1994, Fatima & Marjorie 2007, Saldana-Vázquez et al. 2013, Montoya-Bustamante et al. 2016). This species uses as shelters tree trunks, palm leaves, caves, and occasionally human constructions (Morrison 1980). In Colombia,
A. lituratus is distributed throughout the country, from tropical forests to agriculture and livestock systems, between 0 and 2600 m (Solari et al. 2013, López-Aguirre & Pérez-Torres 2015).
Externally, the ears of A. lituratus is characterized by their rounded shape, shorter than the head, with a straight outer top margin and convex bottom margin. The tragus is well developed, leaf-shaped and having crenulation in the outer margin. The basal lobe is square. The tragus average size is between 5 and 7 mm, and in most specimens the tip of the tragus is yellow (Barquez et al. 1999, Tirira 2007, Reid 2009). In this work, we present evidence of an anomaly in the tragus of an individual of Artibeus lituratus, captured in the Central Andes of the department of Caldas, Colombia.
Material and methods
For the description of the anomaly, and to explore how common is the presence of anomalies in this structure we reviewed the tragus of 321 bat individuals of the families Phyllostomidae, Molossidae, and Vespertilionidae deposited at the Museum of Natural History at the University of Caldas (MHNU-Ca), Manizales, Colombia. In addition, we performed a literature search on the platforms Scopus, Web of Science and JSTOR using keywords such as anomalies, agrochemicals, bat, and malformation to locate publications that describe similar cases.
Results
During a field work in the vereda Alegrías, municipality Aranzazu, Caldas (5°18’21.28"N, 75°29’38.94"W; 1969 m) in June 2019, nine bats of the families Phyllostomidae, Vespertilionidae, and Molossidae were captured using mist nets. The sampling area is destinated to agricultural activities, specifically with monocultures of tree tomato, passion fruit, lulo, beans, and avocados. The cultures are treated every two weeks with agrochemicals (fertilizers and pesticides) to improve agricultural production; this activity has been done for over 20 years.
Of the five bat species captured, two were individuals of A. lituratus, and one of them had an unusual tragus morphology. The tragus presented cylindrical shape and differed in size (right tragus 9.1 mm and left tragus 11.8 mm). The shape and size differed drastically from a normal tragus of conspecifics (Fig. 1), captured during the same sampling. The individual corresponds to an adult male.
Figure 1 (A). Left side view of the tragus (11.8 mm) anomaly shape of A. lituratus. (B) Right side view of the tragus (9.1 mm) shape anomaly of A. lituratus. (C) Right side view with normal tragus shape (5.3 mm) of an individual of A. lituratus captured during the same sampling.
The specimen was preserved as skin and skull, with the body in 70% ETOH and deposited in the MHN-UCa (MHN-UCa 2726). The search for additional specimens with anomalies in the tragus was performed on 321 bat individuals. We could not find additional records of similar anomalies neither on the MHN-UCa collections nor during the literature search.
Discussion
Apparently, the anomaly reported here represents anew case for Chiroptera. Commonly morphological anomaly can be caused by congenital malformations, deformations or disruptions caused by environmental factors, genetic and unknown factors (Rojas & Walker 2012). In this case the main cause of the anomaly is unknown but could be associated to agrochemicals use, because is acknowledge declining bat populations due to pesticide usage (Frank 2017, Williams-Guillén et al. 2016), and furthermore, the exposure to insecticides may lead to hepatic and muscular toxicity with consequences in flight capacity, reproduction, and metabolism of the bats (Oliveira et al. 2018). However, new sampling efforts should be performed to test this hypothesis and to discard postnatal malformation of this structure.
Some of the most common anomalies described in bats are related to wing defects (Castillo-Figueroa & Perez-Torres 2018), unusual changes on the dental formula (Rui & Drehmer 2004), and the absence of pigmentation (Roncancio & Ramirez-Chaves 2008, Marin-Vasquez et al. 2010, Velandia-Perilla et al. 2013). Another type of anomalies less known as the conjoined twins (Nogueira et al. 2017), and skeletal deformities (Kunz & Chase 1983, Romero & Pedersen 2017). We recommend continuing documenting and reporting anomalies in bats to understand the potential negative effects that can generate in individuals that present this unusual condition, and the causes of these morphological alterations (Benítez-Leite et al. 2007, Hoy et al. 2015).
