Introduction
Teeth allow most vertebrates to acquire food –and therefore
energy—from their environment (Lucas, 2004). As such, they are one of
the critical interfaces between an animal and its environment and their
evolution depends both on intrinsic and extrinsic constraints. Teeth
play different roles, from food acquisition to food processing, and have
different functions (e.g., cutting, crushing, grinding, piercing). These
functions depend on both food properties and/or food processing behavior
and are related to tooth shape (e.g., Crofts et al., 2020). Work by
Crofts and colleagues (2020), based on pioneering studies by Lucas
(2004) and Massare (1987), showed how tooth morphology is associated
with prey properties and dental biomechanics (e.g., toughness, bending
abilities, mode of failure). Rounded teeth, for example, allow to crush
hard prey items, they are tough, can barely bend and consequently are
susceptible to fragmentation (Crofts et al., 2020). Because of their
tight and reliable relationship with diet and their abundance in the
fossil record, teeth have been suggested to be good indicators of past
climate and paleoenvironments (e.g., Evans, 2013), and are used to make
inferences on the ecology of extinct species (Bellwood et al., 2014;
Evans & Pineda-Munoz, 2018; Fischer et al., 2022; Frederickson et al.,
2018; Massare, 1987). By extension, tooth morphology could also be used
to infer the feeding habits of secretive species that are sometimes only
known from museum specimens, providing the link between tooth shape and
food properties has been established. While most dental morphology
studies have focused on mammals, because they benefit from a large
variety of diets and tooth shapes (Berkovitz & Shellis, 2018; Ungar,
2010, 2015), a significant amount of work has been done on non-mammalian
vertebrates (Berkovitz & Shellis, 2017). Yet, quantitative comparisons
of tooth morphology and its link to dietary ecology, in a
phylogenetically and ecologically broad sample of species remain rather
scarce for non-mammalian vertebrates. In this study, we investigated the
relationship between dietary ecology and tooth shape in a group of
non-model vertebrates: snakes.
Among vertebrates, macrostomatan snakes are peculiar as they are the
only taxon able to ingest prey larger than their head without processing
it. This behavior is related to an extraordinary organization of the
skull that has become highly kinetic. Indeed, snakes must coordinate the
movements of eight pairs of cranial bones to catch, subdue, manipulate,
and swallow their prey (Cundall & Greene, 2000; Moon et al., 2019).
Despite the complexity of their feeding behavior, snakes have
independently adopted a wide variety of dietary preferences (gastropods,
mammals, birds, crustaceans) providing an opportunity to study possible
convergences in their feeding apparatus (Rhoda et al., 2020). In
addition to constraints related to the physical properties of their food
items, some feeding behaviors may impose high loads on snake teeth, such
as eating live and vigorous prey, with or without the support of a solid
substrate. These various mechanical challenges may have driven the
evolution of tooth shape in snakes. Despite their richness and
complexity in shape (Vaeth et al., 1985; Young & Kardong, 1996),
studies on snake tooth morphology are scarce and either lack of a
quantitative approach or are phylogenetically limited (Berkovitz &
Shellis, 2017; Britt et al., 2009; Evans et al., 2019; Rajabizadeh et
al., 2020; Ryerson & Van Valkenburgh, 2021). Fangs, and mostly front
fangs, have recently attracted some scientific attention (Broeckhoven &
du Plessis, 2017; Cleuren, Parker, et al., 2021; Crofts et al., 2019; du
Plessis et al., 2018; Kundanati et al., 2020; Palci et al., 2021). Yet,
fangs are phylogenetically and functionally limited; their only purpose
is to puncture the prey to deliver venom and consequently, fangs are not
representative of snake tooth diversity. Indeed, they are but two highly
derived teeth out of sometimes over 200 teeth (D. Rhoda pers. obs.).
Snake teeth are usually described as pointy and curved (Berkovitz &
Shellis, 2017). They would therefore be considered as “piercing”
specialists in the classification scheme as described in (Crofts et al.,
2020), and should be associated with a restricted diet composed of soft
invertebrates and small fish. Yet, as previously mentioned, snakes show
a broad variety of diets, but also a wide variety of feeding behaviors
that involve their teeth such as ‘chewing’ (Tumlison & Roberts, 2018),
ripping (Bringsøe et al., 2020; Jayne et al., 2002; Noonloy et al.,
2018), slicing (Cundall & Greene, 2000; Kojima et al., 2020), or
swallowing without piercing (e.g. Dasypeltis sp. ). Snake teeth
are also involved in the whole feeding sequence, from prey capture to
swallowing. Yet, the diversity of tooth morphology and function in
snakes remains under-explored. Here, we quantified and compared the
dentary tooth morphology of 63 species that cover the phylogenetic and
ecological breadth of snakes. We tested four factors related to feeding
that could be associated with morphological adaptations of the teeth:
- Prey hardness: Prey hardness is related to tooth shape in other
vertebrates (Berkovitz & Shellis, 2017, 2018). Teeth of durophagous
species are usually more blunt, and their shape is adapted to resist
high loads while crushing a prey (Crofts, 2015). Snakes do not crush
their prey (except the crustacean specialist Fordonia
leucobalia ), but they use their teeth to manipulate and swallow it
whole. Their teeth must resist high loads –albeit lower than other
crushing-durophagous animals. Durophagy has been associated with short
and blunt fangs (Cleuren, Hocking, et al., 2021) and dentary teeth (in
a study comparing four closely related species: Rajabizadeh et al.,
2020), while species feeding on soft prey have sharp and long fangs
whole (Cleuren, Hocking, et al., 2021). We expect dentary teeth to
present similar morphological adaptations to prey hardness as fangs.
- Prey shape: Snakes are vulnerable to predators during the manipulation
and swallowing of prey and must reduce the time and energy spent
during feeding (Arnold, 1993). The shape of the prey eaten involves
different biomechanical challenges for snakes (Vincent et al., 2006)
and is associated with different head shapes (Segall et al., 2020).
Bulky prey (e.g., anurans, mammals) require extensive manipulation
(Pough & Groves, 1983) and repositioning while long prey (e.g.,
snakes, eels) require more ‘pterygoid walks’ (i.e., protractions and
retractions of left and right tooth rows in alternating fashion
assuring intraoral transport). Manipulation and repositioning of bulky
prey requires a good grip, which can be provided by long, curved, and
sharp teeth. While having short teeth that are not easily embedded in
the prey at each pterygoid walk may allow to reduce the swallowing
duration when eating elongate prey.
- Foraging substrate: Feeding on the ground provides a solid substrate
for the snake to support either itself or the prey during capture,
subduction, manipulation, and swallowing (Moon et al., 2019). However,
feeding in an aquatic or arboreal context does not provide that
support, so we expect the teeth to play a larger role in those
ecological contexts. Aquatic snakes must deal with their own buoyancy
and that of their prey while feeding, so the forces applying on the
teeth may show a diversity of orientations. We expect teeth of aquatic
species to have a shape that allows some degree of bending. Arboreal
manipulation and swallowing usually happens with the snake hanging
from a branch, head down, with no substrate support and almost without
the help of the rest of its body. This behavior increases the chances
of dropping prey which may not be possible for the snake to retrieve ,
unlike in an aquatic or terrestrial environment. Thus, arboreal
feeding requires a good grip on the prey, which would be favored by
long, sharp, and curved teeth.
- Biomechanical challenge related to feeding ecology: The previous
factors are not mutually exclusive (e.g., eel-eaters eat elongated
prey under water) but are also restrictive as they do not account for
feeding behavior. For instance, terrestrial viperids can either
envenomate and release their prey, while others hold on to the prey
after striking (Glaudas et al., 2017). The first behavior involves
manipulating and swallowing a dead prey, while the prey is alive and
certainly fighting back in the second case. These two behaviors
certainly impose different loads on the teeth. We classified
characteristics associated with the prey and the feeding behavior that
impose mechanical challenges to the teeth. We consider that (1) hard
prey is the highest challenge for a tooth, followed by (2) elongated
prey that involve repeated loading, (3) slippery prey (secreting
mucus) that may impose loads in various direction and require a good
grip to prevent escape, (4) Holding a vigorous prey that is neither
hard, nor long, nor slippery, finally, (5) bulky prey that require
extensive tooth manipulation.
We dissected the dentary bone of 63 species of snakes and used micro-CT
scanning to obtain high resolution scans of the teeth. We then used 3D
geometric morphometrics to compare both the external and internal shape
of the teeth. Shape information on inner part of the teeth allowed us to
compare the thickness of the hard tissues that compose the tooth. We
also measured the length and maximal and average degrees of curvature.
Next, we used phylogenetic comparative methods to test the importance of
our predictive ecological factors as drivers of tooth shape to establish
the link between tooth shape variation and dietary ecology in snakes.