Abstract
- 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.
- 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.
- 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.
- 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