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.