Results of the finite element simulations provided no support for increased functional differentiation (Fig. 3a), mechanical efficiency (Fig. 2), stiffness (Fig. 2), or consistent differences in stress distributions (Fig. 4) in living durophagous otter species compared to non-durophagous species. Therefore, our hypotheses of similarity between Siamogale and living durophagous otters, as well as predicted differences between living durophagous and non-durophagous otter species, are not supported by the data. In fact, the relationship between the unadjusted SE values and model volumes of living otter species is significantly linear (Fig. 3c, Table 3). This stiffness-volume linearity is a relationship expected from isometric scaling of a given finite element model with input forces set proportional to surface area5. In Dumont et al.’s derivation of proper scaling coefficients for maintaining proportional output values (i.e., isometric model scaling), a linear relationship is expected between strain energy and model volume given that input force to area ratio is held constant. This linear relationship is expected for models of identical geometry at different volumes, but such relationship is not necessarily a null expectation for a comparative species sample of varying geometry and varying volumes, such as the dataset analyzed in this study. All our models were assigned input forces proportional to the muscle attachment areas (highlighted on the mandible in Fig. 1), and simulations were conducted using original volumes of the jaw models. Given these modeling parameters, a significant linear relationship among the ten living otter species analyzed indicates that total strain energy-volume scaling relationships follow isometric model scaling principles regardless of the actual differences in dietary preference or mandibular morphology.

This strain energy-volume linearity is an unexpected result from a functional perspective, as living otter species exhibit a wide range of diets that differ significantly in prey material properties (from soft tissues to hard exoskeletons) and in hunting strategy (from snapping bites when capturing fish, to crushing bites when breaking hard-shell invertebrates)6,7,8,9,10,11,12,13. In addition, some of the general anatomical gradients previously identified in non-pinniped durophagous carnivorans compared to non-durophagous carnivorans are reflected in mandible shapes of molluscivorous lutrines14. For example, taller and broader coronoid processes and deeper mandibular corpi in the molluscivores Enhydra and A. capensis (Fig. 1a). A significantly linear strain energy-volume relationship suggests that such morphological differences do not relate to mandible stiffness (as measured by strain energy) differences. Nevertheless, the scatter around the linear regression lines indicates that small departures in mandible stiffness from linearity (which assumes identical geometry) could still be associated with biomechanical differences associated with mandible shape differences (although; as an example, Aonyx capensis, a crab-eater that has not been observed to use shell-breaking tools (i.e., hard-shelled prey items are processed orally), does exhibit a relatively stiff mandible model profile (Fig. 2) as well as lower than expected SE values given its model volume (Fig. 3b,c; values falling below the 95% CI). Along the same lines, the high stiffness values of the Siamogale models could be related to its robust mandibular corpus, which has thick cortical walls that increase the second moment of area and therefore resistance to bending (Fig. 1c)15.

In light of the linear relationship between SE and volume among the ten living otter species examined, the simulation outputs of Siamogale shows a remarkable departure from the typical otter pattern (Fig. 3b), and suggests that living otters are poor analogs for understanding the biomechanical adaptations of Siamogale. When the SE-volume relationship is analyzed in the broader context of other carnivoran species including omnivore (brown bear), hypercarnivore (wolf), and fossil species inferred to have diets involving high jaw loads (the extinct marine bear Kolponomos, and the extinct sabertooth Smilodon), the linear relationship appears to hold among the living species (Fig. 3f). The inferred molluscivore Kolponomos is roughly equidistant from the fitted regression line in vertical distance as Siamogale, indicating similar degrees of departure from the living carnivoran pattern, and a significant decrease in SE (or an increase in stiffness) relative to their jaw volumes. Kolponomos has previously been shown, using finite element simulations, to possess stiff mandibles with deep mandibular symphysis, both being structural characteristics consistent with a shell-prying hunting strategy followed by oral crushing of hard-shelled invertebrates16. The mandibular symphysis of Siamogale appears relatively deepened compared to living otters (Fig. 1), but to a lesser extent than Kolponomos. Furthermore, the deepening of the mandibular ramus at the m1-m2 location, rather than at the location of the symphysis, indicates that Siamogale was not adapted to prying hard-shelled invertebrates with the incisor tooth row to the extent inferred in Kolponomos. However, both Siamogale and Kolponomos have mandibular morphology (robust and deep rami) and biomechanics (high jaw stiffness relative to volume) consistent with extensive use of the jaw as a crushing tool.

The living otter species that is most significantly below the linear regression line is Aonyx capensis, an oral crusher without observed tool-using ability for breaking shells6. Compared to Aonyx, the tool-using sea otter Enhydra lutris has a mandible with a level of stiffness expected from isometric model scaling (i.e., mandible geometry has weak or no effect on simulated stiffness). Given this observation, we interpret the linearly-scaling mandibular stiffness-volume ratio of Enhydra as evidence of a ‘functional release’ of the mandible as a crushing tool by delegating crushing function to the hands. Enhydra are known to have dexterous hands that can handle rock tools to pre-process (by smashing) large shelled prey before mastication. The lack of hand tool-use for shell-crushing in Aonyx would place the functional demand of crushing large shells entirely on the masticatory system (cranium and mandible). If this interpretation is correct, then the stiff mandible of Siamogale suggests this extinct otter likely crushed most or all of its prey using its jaws and did not have the ability to manually process its prey before mastication.

Given the conserved range of ME values across otter species and the significant departure of Siamogale in stiffness, we interpret the functional adaptation in Siamogale to have occurred by increasing bone strength, rather than by improving the mechanical efficiency of its masticatory system. Such increase in strength, combined with its large size, implies that Siamogale was capable of crushing much larger and harder prey than observed in any of the living otter species (roughly six-fold increase in stiffness relative to expectation from linearity). This interpretation is supported by the low stress observed on the Siamogale model during bite simulations, especially in the strength of the anterior mandibular corpus and symphyseal regions (Fig. 4). Previous research on rodent ecomorphology suggests that body size alone may be an important axis of ecological diversification and niche partitioning17. This may have been the case with Siamogale, whose increase in jaw strength appears to be associated only with jaw volume increase and not changes in efficiency. In absence of morphological shape modifications to significantly alter the mechanical efficiency of the masticatory system, the large size of Siamogale melilutra would have been critical in allowing the extinct otter to access larger prey in a faunal community where large-bodied predators are essentially unknown in the local fossil record (see below).

The contemporaneous fauna at Shuitangba, where the type specimens of Siamogale melilutra were discovered, contains common mammalian species of southeast Asian late Miocene forested habitats (deer, tapir, proboscideans, beavers) as well as aquatics plants such as fox nuts3. The abundance of aquatic and near-water environments in that region18 may have allowed aquatic carnivorans such as Siamogale to become the dominant predators of their ecological communities, outcompeting the larger, more cursorial carnivorans commonly found in more open environments outside of the Shuitangba area. A highly molluscivorous diet was likely for Siamogale given the great strength of its jaws, allowing the extinct otters to access foods unavailable to carnivorans without bulbous crushing dentitions (such as felids and ursids, which are known from the same fauna) or are not adapted to living in forested, humid environments (e.g., hyaenids, which are currently not recorded in the Shuitangba fauna)18.

In conclusion, our engineering simulation analyses suggest a linear scaling relationship between jaw stiffness and jaw volume in living otters; departure from this linear trend seems to indicate increased mechanical demand for oral processing of hard food items. This linear relationship may be a broader trend among carnivorans not specialized for oral-crushing durophagy. However, extinct carnivorans thought to be specialized in heavily loading their mandibles all exhibit higher mandibular stiffness (lower total strain energy) than expected from isometric model scaling. In particular, the degree of stiffness increase from linear trends observed in extant species is similar between the giant otter Siamogale and the marine bear Kolponomos. Both Siamogale and Kolponomos are inferred to have been durophagous molluscivores with emphasis on oral crushing rather than tool-use, suggesting that the acquisition of tool use by living durophagous sea otters functionally released their mandibles from having to deviate from the stiffness-volume isometric model scaling. Low stresses on the mandible during biting also characterize those extinct durophagous molluscivores (Fig. 4g)16. Our findings suggest that Siamogale does not have a living analog, but exhibits limited similarity to the living oral-crusher Aonyx in having significantly stiffer than expected mandibles among otters. Thus, Siamogale represents a novel freshwater carnivoran ecomorphology that is lacking in modern ecosystems and exhibits specialization for durophagy by large size and high jaw bone volume instead of increased efficiency.