4.2 Interspecific bite force variation
Stenodermatinae represents a subfamily of Phyllostomidae bats with a diet that contains significantly more fruit than other family’s bats (Santana, Grosse, & Dumont, 2012). They are morphologically diverse with cranial and mandibular traits that overlap with other feeding guilds (Santana, Grosse, & Dumont, 2012), which is reflected in the variety of foods as well as in the tendency of these species to specialize in a group of particular fruits (Rojas, Vale, Ferrero, & Navarro, 2012; Rossoni, Assis, Giannini, & Marroig, 2017). Several craniodental traits contribute to generate a greater bite force and the differences between these particular traits had showed a clear segregation between the species (Santana, Grosse, & Dumont, 2012).
The association in craniodental features and bite force by species can be explained by the type of fruit consumed. A. phaeotis , P. helleri and S. giannae (small-sized and sedentary nomadic fruit bats) formed an independent group. These species have a short skull and a shorter distance from the teeth to the jaw joint, which allows them to consume hard and soft fruits (Dumont et al., 2012), P. helleri and S. giannae are characterized by elongated and narrow snouts (Santana, Grosse, & Dumont, 2012), which is associated with the consumption of soft and smaller fruits such as those of Solanaceae (Arias & Pacheco, 2019; García-Herrera, Ramírez-Fráncel and Flórez, 2019). Species that share cranial and nutritional traits with D. anderseni. For its part, Uroderma convexum was distinguished from the other species studied here by having a parallel rostrum and a short face that abruptly expands from the apex to the edges of the lacrimal bone (Mantilla-Meluk, 2014). These characteristics allow them to exploit mainly hard fruits of plant species such as Ficus spp. (Sagot and Stevens, 2012).
All the big and small-sized nomadic frugivorous bat species studied here, except for A. anderseni and A. phaeotis had a stronger bite force, which was correlated to a greater length of the skull, shorter palate, narrower width between molars, dentary length, and higher coronoid process. These traits have been recognized as predictors of a biomechanical advantage for higher feeding performance (Dumont et al., 2012). Shortening and widening of the rostrum inA. anderseni and A. phaeotis was negatively correlated to bite force, although it should confer a greater biomechanical advantage; a pattern that has been repeatedly observed in placental and marsupial carnivores (Wroe & Milne, 2007). This is probably due to the fact that the variation in size could be the most dominant factor and it has been shown that the differential proportions of the skull determine the maximum value of the bite force (Herrel, Podos, Huber, & Hendry, 2005; Nogueira et al., 2009; Dollion et al., 2016). Recent studies have suggested that among closely related mammals, larger taxa exhibit relatively longer faces, whereas smaller taxa exhibit paedomorphic traits such as proportionally shorter faces and larger brains (Cardini & Polly, 2013; Cardini, Polly, Dawson, & Milne, 2015; Tamagnini, Meloro, & Cardini, 2017). This pattern called cranial evolutionary allometry, has been seen in antelopes, squirrels, fruit bats, cats and kangaroos (Tamagnini, Meloro, & Cardini, 2017).
Previous studies have demonstrated that skull size is important in determining interspecific differences in bite force, specifically, Nogueira, Peracchi & Monteiro (2009) found that, in phyllostomids, size‐corrected bite forces were correlated with shorter rostra, alignment of the molars along the masseter insertion region, and expansion of the anterior zygomatic arch and angular process. On the contrary, our study determined that the variation in bite force in Stenodermatinal bats is better explained by the length of the skull, condylo-incisor, condylo-canine, mandibular toothrow and height of the coronoid, results similar to those reported by Herrel et al.,(2008) in a sample of bat species (including non-phylostomids).
Shortening and widening of the rostrum in A. anderseni and A. phaeotis was negatively correlated to bite force, although it should confer a greater biomechanical advantage; a pattern that has been repeatedly observed in placental and marsupial carnivores (Wroe & Milne, 2007). This is probably due to the fact that the variation in size could be the most dominant factor and it has been shown that the differential proportions of the skull determine the maximum value of the bite force (Herrel, Podos, Huber, & Hendry, 2005; Nogueira et al., 2009; Dollion et al., 2016). Recent studies have suggested that among closely related mammals, larger taxa exhibit relatively longer faces, whereas smaller taxa exhibit paedomorphic traits such as proportionally shorter faces and larger brains (Cardini & Polly, 2013; Cardini, Polly, Dawson, & Milne, 2015; Tamagnini, Meloro, & Cardini, 2017). This pattern called cranial evolutionary allometry, has been seen in antelopes, squirrels, fruit bats, cats and kangaroos (Tamagnini, Meloro, & Cardini, 2017).
Another factor that could explain our results is that bats modulate the force of the bite according to the exploited resources of soft and hard food (Santana & Dumont, 2009). Artibeus vary in the size and texture of the fruits they prefer (Wendeln, Runkle, & Kalko, 2000) and may exhibit differential maximum bite force, which can potentially increase by more than 10% when consuming hard fruits (Santana & Dumont, 2009). Another factor to consider is the possible variation in the intraspecific bite force in response to the temporal or geographical variation of food resources or the hormonal status of bats, as proposed by Irschick et al. (2006). Since the bats included in our study are composed of individuals from different localities and data (fieldwork and voucher specimens; Appendix I), our data could be susceptible to this source of variation and therefore a more detailed study is needed to test this hypothesis and further improve our understanding of the relationships of bite force and craniodental traits.
Given that nomad bats consume similar fruits, they could require the same force to process, so we expected that all bats grouped in this category would present similar bite forces, however our results established that the species Artibeus lituratus , A. planirostris , followed U. bilobatum and P. hellerirecorded the highest bite force, probably because these bats feed on food resources that clearly have different mechanical demands when consuming even other resources other than the fruits.
All Stenodermatinae are frugivores with short and wide rostrum, but our results show that can occur some divergent morphologies within the clade, which is seen in the large number of species within the subfamily and highly diverse genera (Murillo-García & De la Vega, 2018). As has been documented in other vertebrates, closely related species exhibit strong positive relationships between large skulls and greater biomechanical advantage (Maestri et al., 2016; Santana & Miller, 2016). Our findings illustrate that skull size is a determining factor in the bite force and emphasizes that the use of functional traits is relevant to establishing the feeding performance of bat species. This highlights the importance of studying the relationships between morphology, bite force and the ecology of the species to get a better understanding of evolutionary adaptions of highly diverse Neotropical bat groups.