Divergent Skull Morphology Supports Two Trophic Specializations in Otters (Lutrinae)

Abstract

Variation in terrestrial mammalian skull morphology is known to constrain feeding performance, which in turn influences dietary habits and ultimately fitness. Among mustelids, otters have evolved two feeding specializations: underwater raptorial capture of prey (mouth-oriented) and capture of prey by hand (hand-oriented), both of which have likely associations with morphology and bite performance. However, feeding biomechanics and performance data for otters are sparse. The first goal of this study was to investigate the relationships between feeding morphology and bite performance among two mouth-oriented piscivores (Pteronura brasiliensis and Lontra canadensis) and two hand-oriented invertebrate specialists (Enhydra lutris and Aonyx cinerea). Since other vertebrate taxa that are mouth-oriented piscivores tend to possess longer skulls and mandibles, with jaws designed for increased velocity at the expense of biting capability, we hypothesized that mouth-oriented otters would also possess long, narrow skulls indicative of high velocity jaws. Conversely, hand-oriented otters were expected to possess short, blunt skulls with adaptations to increase bite force and crushing capability. Concomitant with these skull shapes we hypothesized that sea otters would possess a greater mandibular bluntness index, providing for a greater mechanical advantage compared to other otter species investigated. A second goal was to examine morphological variation at a finer scale by assessing variation in cranial morphology among three sea otter subspecies. Since diet varies among these subspecies, and their populations are isolated, we hypothesized that the magnitude of mandibular bluntness and concomitant mechanical advantage, as well as occlusal surface area would also vary within species according to their primary food source (fish versus hard invertebrates). Functional expectations were met for comparisons among and within species. Among species the phylogeny suggests a deeply rooted transition to alternative foraging types. Yet within foraging types alternative species were also strongly variable, suggesting either selective differences in the extent or nature of realized foraging mode, or an accumulation of non-adaptive changes during the long independent evolutionary history. At the finest scale, variation among subspecies indicates that trophic adaptation occurred rapidly, making it interesting that we happened to find both deeply and shallowly-rooted transformations associated with diet type in otter species and subspecies.

Chew, shake, and tear: Prey processing in Australian sea lions (Neophoca cinerea)

“…However, there are some important differences between the feeding behaviors used by Australian sea lions and those used by otters when processing large food. Piscivorous otters generally have sharp carnassial teeth that enable them to effectively cut their food, while invertebrate feeding otters have broad molars that are used to crush shellfish and crustaceans (Timm-Davis et al 2015). In both of these cases the food is held stationary by the forelimbs over specific specialized teeth to enable effective processing of the food item.…”

Dry versus wet and gross: Comparisons between the dry skull method and gross dissection in estimations of jaw muscle cross‐sectional area and bite forces in sea otters

“…Specifically, we test the hypotheses that bite force derived from photographs of osteological specimens with estimated PCSA and in‐lever lengths of jaw adductor muscles accurately predicts variables derived from dissection‐based measurements of PCSA and in‐lever lengths of jaw adductor muscles and overall theoretical bite force in the same individuals. We test these relationships using an ontogenetic series of southern sea otters ( Enhydra lutris nereis ) as our model species because of the availability of a large sample of fresh specimens with intact craniomandibular musculature for dissections and the known morphological specializations for consuming hard prey such as short, blunt skulls, taller and wider mandibular rami, and bunodont dentition (Constantino et al, ; Law, Baliga, Tinker, & Mehta, ; Riley, ; Timm‐Davis, DeWitt, & Marshall, ). We acknowledge that in vivo bite force measurements are critical in validating both modeling approaches.…”

Ontogenetic Scaling of Theoretical Bite Force in Southern Sea Otters (Enhydra lutris nereis)

“…These durophagous marine mustelids feed on a variety of hard-shelled invertebrates such as chitinous crabs and calcifying bivalves and gastropods (Riedman and Estes 1990). Like many durophagous mammals, sea otters exhibit several cranial adaptations that facilitate durophagy including short, blunt skulls (Riley 1985); taller and wider mandibular rami (Timm-Davis et al 2015; bunodont dentition (Fisher 1941;Constantino et al 2011); and fracture-resistant dental enamel (Ziscovici et al 2014). Recent work on adult southern sea otters indicated that although size is the primary axis of craniomandibular variation, a handful of craniomandibular traits demonstrated significant shape differences between the sexes (Law et al, forthcoming).…”