Abstract
  1. Phyllostomid bats exhibit great diversity in skull size and morphology that reflects the degree of resource division and ecological overlap in the group. In particular, Stenodermatinae has high morphological diversification associated with cranial and mandibular traits that is associated with the ability to consume the full range of available fruits (soft and hard). In terms of morphology, performance (bite force) appears to play an important role in niche partitioning among bat species, however, very few studies have confirmed these relationships using functional cranial traits.
  2. Here, we analyzed craniodental traits and their relationship to the bite force in 309 specimens distributed in seven species of stenodermatine bats with two foraging types: nomadic and sedentary frugivorous bats. We evaluated 19 functional traits of the skull and jaw related to feeding and bite force in live animals by correcting bite force with body size. We used a GLM model and post hoctests to determine possible relationships and differences between cranial traits, species, and sex.
  3. The results showed that there is significant interspecific variation between stenodermatines that are nomadic and sedentary. The greatest variation in bite force within species was explained by the mandibular toothrow length (MANDL) between sexes, which was greater in females. The larger species of Artibeus , together withPlatyrrhinus helleri , Uroderma convexum andSturnira giannae , which have a greater length of the skull, condylo-incisor, condylo-canine, mandibular toothrow and height of the coronoid, exhibit greater bite force. By contrast, the smaller speciesA. anderseni and A. phaeotis have short skulls and the lowest values of bite force, which suggests that the size of the skull confers a biomechanical advantage.
  4. Our results highlight the usefulness of analyzing functional traits related to feeding to establish the performance of bats in terms of the bite force.
KEYWORDS
Ecomorphology, frugivores, morphometry, Stenodermatinae, skull, trophic performance.
1. INTRODUCTION
The skull of vertebrates is a complex assembly that is closely related to the resource collection, food processing, behavior, and ecology of the species (Bels & Herrel, 2019). Examining the patterns and mechanisms that lead to cranial variation, including shape and traits, enables an understanding of the morphology, ecology, and general fitness of animals (Santana, Dumont, & Davis, 2010). Bats have variation in cranial morphology attributed to evolutionary processes of ecological specialization, which result in a niche division between ecomorphologically similar species (Santana, Grosse, & Dumont, 2012). This variation responds mainly to functional requirements related to nutritional performance and the sensory system (Thiagavel et al., 2018).
Among chiropterans, New World leaf-nosed bats (Phyllostomidae) represents one of the largest and most morphologically diverse mammal families (Rossoni et al., 2017). Ecological diversification in Phyllostomidae is related to bite performance and mechanical demands of different diets, including frugivores, insectivores, nectarivores, carnivores, and sanguinivores (Dumont, 2007, Nogueira, Peracchi, & Monteiro, 2009; Manhães, Nogueira, & Monteiro, 2017). Dietary differences require specific mechanical modifications, including variation in the rostral length and height of the skull (Santana, Dumont, & Davis, 2010). However, there is a lack of understanding about the patterns in the variation of the shape and performance (López-Aguirre & Pérez-Torres, 2015). The remarkable specializations seen in these bats provide a unique opportunity for studying the relationship between cranial morphology, feeding performance, and dietary ecology (Aguirre, Herrel, Van Damme, & Matthysen, 2002; Rossoni et al., 2017).
The bite force is a biomechanical trait that determines various vital functions, such as feeding, mating, defense, and competition, and is closely related to body size and feeding performance (Santana, Dumont, & Davis, 2010). Therefore, an increase in bite force allows for a broader spectrum of food available (Santana & Dumont, 2009). Phylostomid exhibit bite forces associated with the size and hardness of food (Aguirre, Herrel, Van Damme, & Matthysen, 2003), resulting in strong morphological heterogeneity due to the particularities of the diet (Dumont & O’Neil, 2004).
Although various studies have addressed the relationships of craniodental morphology, bite force and diet (e.g., Aguirre, Herrel, Van Damme, & Matthysen, 2002; Dumont, Herrel, Medellín, Vargas-Contreras, & Santana, 2009: Santana, Grosse, & Dumont, 2012; Santana & Miller 2016), the evaluation of these variables has been carried out separately, evaluating each variable independently (Shi et al., 2020). Likewise, the information related to the craniodental traits responsible for generating bite forces in bats is limited without much attention to the functionally relevant components of the craniodental system and the musculature of the jaw (Herrel, Smet, Aguirre, & Aerts, 2008). The specific hardness of food and the bite force required to process food play an important role in the division of resources within frugivore bat communities (Dumont, 2007). According to Soriano (2000) and Giannini & Kalko (2004), fruit bats can be categorized as nomadic or sedentary, with preference for a specific type of plant, morphological diversity reflected in the physical properties of the fruits, and a tendency of specialization towards a specific fruit or group of fruits (Santana, Dumont, & Davis, 2010; Santana, Grosse, & Dumont, 2012).
Frugivorous bats provide an excellent model to study the relationship between craniodental morphology and bite force because they consume both hard and soft fruits, the result of adaptive pressures related to mandibular morphology (see Murillo-García, & De la Vega, 2018). We selected the members of the family Phyllostomidae due to the fact that they have the highest diversity of mammals with more than 70 species that are found sympatrically and serve as nocturnal predators, pollinators and predominant seed dispersers (Giannini & Kalko, 2004; Reid et al., 2015), and within this family, the Stenodermatinae subfamily, contains > 43% of all described New World leaf-nosed bat species (Shipley & Twining, 2020) and in central Colombia, department of Tolima, these chiropterans represent near the 13% in the sampled areas (see García-Herrera, Ramírez-Fráncel, & Flórez, 2019).
Our objective was to identify the functional traits associated with bite force in seven representative species of the Stenodermatinae subfamily occurring in Colombia. We hypothesize that large species and small-sized nomadic frugivorous species with narrow faces, wide palates and shorter length between molars will have a greater biomechanical advantage of stronger bite force in relation to sedentary frugivorous bats.
2. MATERIALS AND METHODS