Chris J. Law

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

Sexual dimorphism attributed to niche divergence is often linked to differentiation between the sexes in both dietary resources and characters related to feeding and resource procurement. Although recent studies have indicated that southern sea otters (Enhydra lutris nereis) exhibit differences in dietary preferences as well as sexual dimorphism in skull size and shape, whether these intersexual differences translate to differentiation in feeding performances between the sexes remains to be investigated. To test the hypothesis that scaling patterns of bite force, a metric of feeding performance, differ between the sexes, we calculated theoretical bite forces for 55 naturally deceased male and female southern sea otters spanning the size ranges encountered over ontogeny. We then used standardized major axis regressions to simultaneously determine the scaling patterns of theoretical bite forces and skull components across ontogeny and assess whether these scaling patterns differed between the sexes. We found that positive allometric increases in theoretical bite force resulted from positive allometric increases in physiological cross-sectional area for the major jaw adductor muscle and mechanical advantage. Closer examination revealed that allometric increases in temporalis muscle mass and relative allometric decreases in out-lever lengths are driving these patterns. In our analysis of sexual dimorphism, we found that scaling patterns of theoretical bite force and morphological traits do not differ between the sexes. However, adult sea otters differed in their absolute bite forces, revealing that adult males exhibited greater bite forces as a result of their larger sizes. We found intersexual differences in biting ability that provide some support for the niche divergence hypothesis. Continued work in this field may link intersexual differences in feeding functional morphology with foraging ecology to show how niche divergence has the potential to reinforce sexual dimorphism in southern sea otters.

Sexual dimorphism in craniomandibular morphology of southern sea otters (Enhydra lutris nereis)

The niche divergence hypothesis suggests that if a species exhibits intersexual differences in diet, selection should favor divergence in the feeding apparatus between the sexes. Recent work revealed that male and female southern sea otters (Enhydra lutris nereis) utilize different dietary resources in response to increased population density; females exhibit more specialized diets as a function of smaller home ranges, whereas males exhibit larger home ranges, potentially allowing them to expand their dietary breadths by feeding on prey items that are not found in female home ranges. These dietary differences suggest the potential for sexual dimorphism of the feeding apparatus (i.e., the skull). Here, we tested the hypothesis that male and female southern sea otters exhibit differences in craniomandibular traits directly related to biting ability. Univariate and multivariate analyses of 12 craniomandibular traits showed that size is the primary axis of skull variation, whereas only a handful of craniomandibular traits demonstrated significant shape differences between the sexes. Relative postorbital constriction breadth, masseter in-lever length, and cranial height differed significantly between the sexes. These 3 traits can increase the surface area of jaw muscle attachment sites and thus are directly linked to the mechanics of biting ability. Collectively, these morphological differences indicate that niche divergence may be an important mechanism maintaining sexual dimorphism in southern sea otters.

Lineage diversity and size disparity in Musteloidea: testing patterns of adaptive radiation using molecular and fossil-based methods.

Abstract. Adaptive radiation is hypothesized to be a primary mechanism that drives the remarkable species diversity and morphological disparity across the Tree of Life. Tests for adaptive radiation in extant taxa are traditionally estimated from calibrated molecular phylogenies with little input from extinct taxa. With 85 putative species in 33 genera and over 400 described extinct species, the carnivoran superfamily Musteloidea is a prime candidate to investigate patterns of adaptive radiation using both extant‐ and fossil‐based macroevolutionary methods. The species diversity and equally impressive ecological and phenotypic diversity found across Musteloidea is often attributed to two adaptive radiations coinciding with two major climate events, the Eocene‐Oligocene transition and the Mid‐Miocene Climate Transition. Here, we compiled a novel time‐scaled phylogeny for 88% of extant musteloids and used it as a framework for testing the predictions of adaptive radiation hypotheses with respect to rates of lineage diversification and phenotypic evolution. Contrary to expectations, we found no evidence for rapid bursts of lineage diversification at the origin of Musteloidea, and further analyses of lineage diversification rates using molecular and fossil‐based methods did not find associations between rates of lineage diversification and the Eocene‐Oligocene transition or Mid‐Miocene Climate Transition as previously hypothesized. Rather, we found support for decoupled diversification dynamics driven by increased clade carrying capacity in the branches leading to a subclade of elongate mustelids. Supporting decoupled diversification dynamics between the subclade of elongate mustelids and the ancestral musteloid regime is our finding of increased rates of body length evolution, but not body mass evolution, within the decoupled mustelid subclade. The lack of correspondence in rates of body mass and length evolution suggest that phenotypic evolutionary rates under a single morphological metric, even one as influential as mass, may not capture the evolution of diversity in clades that exhibit elongate body shapes. The discordance in evolutionary rates between body length and body mass along with evidence of decoupled diversification dynamics suggests that body elongation might be an innovation for the exploitation of novel Mid‐Miocene resources, resulting in the radiation of some musteloids.

Revisiting the behavioural framework of feeding in predatory aquatic mammals

Hocking et al . [1] (hereafter HEA) present a framework for defining and evaluating feeding strategies in predatory aquatic mammals. While we appreciate the review, we address three difficulties with the framework: (i) the tetrapod feeding cycle needs minimal revision to accommodate aquatic mammals, (ii) the proposed feeding strategies need further clarification and (iii) evolution should not be described as a logical sequence. Our goal is to clarify and expand on HEAs feeding framework to ensure that predatory aquatic mammals can be examined in a comparative framework with other tetrapods.nnFirst, HEA argue that the four stages of the tetrapod feeding cycle—ingestion, intraoral transport, processing and swallowing [2]—do not adequately address the problems faced by air-breathing aquatic mammals. HEA, therefore, propose an alternative feeding cycle: (I) prey capture, (IIa) prey manipulation and transport and (IIb) prey processing, (III) water removal and (IV) swallowing. These changes constrain our ability to compare feeding behaviour across tetrapod lineages. The tetrapod feeding cycle is already sufficiently flexible to accommodate behaviourally diverse clades, so we propose using the existing tetrapod feeding cycle [2] with some revisions based on HEA (figurexa01). nnnnFigure 1. nModified feeding cycle of aquatic tetrapods based on Schwenk [2] and Hocking et al . [1]. (Online version in colour.)nnnnIn the tetrapod feeding cycle, ingestion encompasses all behaviours used to capture, subdue, kill and process prey before it enters the oral cavity [2]. Therefore, HEAs stages I, IIa and IIb are already included in ingestion and can distinguish between different behaviours prior to prey entering the mouth (figurexa01). For example, sea otters ( Enhydra lutris ) dive to grab benthic prey (prey capture), move prey using their mouth/forepaws (prey manipulation) and use tools/teeth to open hard-shelled prey (external prey processing) [3]. …

Carnivory maintains cranial dimorphism between males and females: Evidence for niche divergence in extant Musteloidea: BRIEF COMMUNICATION

The evolution and maintenance of sexual dimorphism has long been attributed to sexual selection. Niche divergence, however, serves as an alternative but rarely tested selective pressure also hypothesized to drive phenotypic disparity between males and females. We reconstructed ancestral social systems and diet and used Ornstein–Uhlenbeck (OU) modeling approaches to test whether niche divergence is stronger than sexual selection in driving the evolution of sexual dimorphism in cranial size and bite force across extant Musteloidea. We found that multipeak OU models favored different dietary regimes over social behavior and that the greatest degree of cranial size and bite force dimorphism were found in terrestrial carnivores. Because competition for terrestrial vertebrate prey is greater than other dietary groups, increased cranial size and bite force dimorphism reduces dietary competition between the sexes. In contrast, neither dietary regime nor social system influenced the evolution of sexual dimorphism in cranial shape. Furthermore, we found that the evolution of sexual dimorphism in bite force is influenced by the evolution of sexual dimorphism in cranial size rather than cranial shape. Overall, our results highlight niche divergence as an important mechanism that maintains the evolution of sexual dimorphism in musteloids.

Lutra lutra (Carnivora: Mustelidae)

Abstract: n Lutra lutra (Linnaeus, 1758), commonly known as the Eurasian otter, is the most widely distributed of the lutrinids (otters). L. lutra is primarily a piscivorous predator but also preys on amphibians, crustaceans, small mammals, birds, and reptiles. Extant populations of this semiaquatic mustelid occur in a wide variety of aquatic freshwater and marine habitats throughout Asia, all of Europe, and parts of northern Africa. Despite the large distribution, habitat loss has led to dwindling L. lutra populations, particularly in Asia, and the species is currently listed as “Near Threatened” by the International Union for Conservation and Nature and Natural Resources.

Eat whole and less often: ontogenetic shift reveals size specialization on kelp bass by the California moray eel, Gymnothorax mordax

Despite the importance of predation in many ecosystems, gaps remain in our understanding of nocturnal marine predators. Although the kelp forests of Southern California are some of the most well-studied ecosystems, California morays, Gymnothorax mordax, are predominately nocturnal predators that have remained largely unstudied and their predatory effects on the kelp forest ecosystem are unknown. We use a multi-year data set to examine the dietary breadth of G. mordax and to determine the functional role of this predator. We also quantify bite force to examine the potential performance limitations of morays in exploiting prey. Stomach content analyses and linear selectivity index values indicate that G. mordax specializes on kelp bass, Paralabrax clathratus. Average size of kelp bass consumed varies across years, suggesting that morays respond to fluctuations in prey size availability. The scaling relationship of kelp bass standard length and moray head length reveals an ontogenetic shift, where maximum prey size increases with moray size and small prey are dropped from the diet of larger individuals. Moray bite force exhibited strong positive allometry with moray head size, suggesting that larger morays exhibit greater bite forces for their head and body size. However, we found no relationship between prey size and bite force, suggesting that a disproportional increase in bite force does not facilitate the consumption of disproportionately larger prey. Our results indicate that while G. mordax of Catalina Island is a dietary specialist, it is capable of exhibiting functional shifts in prey size and species based on their abundance.

Mustela sibirica (Carnivora: Mustelidae)

Abstract: Mustela sibirica Pallas, 1773, commonly known as the Siberian weasel, is a widely distributed Palearctic musteline with natural populations ranging from west of the Ural Mountains of Siberia to the Far East and south to Taiwan and the Himalayas. A key characteristic that distinguishes M. sibirica from most sympatric musteline species is the occurrence of a black mask on its face that surrounds the eyes, a white muzzle and chin, and the presence of a nearly completely monotone yellowish-brown coat. Although M. sibirica is hunted to make “kolinsky stable-hair” paintbrushes, populations remain stable and the species is currently listed as “Least Concern” by the International Union for Conservation and Nature and Natural Resources. Version of Record, first published online September 27, 2018, with fixed content and layout in compliance with Art. 8.1.3.2 ICZN

Differentiation of craniomandibular morphology in two sympatric Peromyscus mice (Cricetidae: Rodentia)

In the Santa Cruz Mountains of California, dietary partitioning is believed to allow Peromyscus californicus (California mouse) and Peromyscus truei (pinyon mouse) to occur sympatrically; P. californicus feeds primarily on arthropods, whereas P. truei feeds primarily on acorns. To better understand how these species partition resources, we examine if these dietary differences extend to differences in craniomandibular morphology. We use a geometric morphometric approach to test the hypothesis that P. californicus and P. truei exhibited size and shape differences in craniomandibular morphology, in particular, regions of the skulls that pertain to biting ability and mechanical advantage of the jaw adductor muscles. We found that P. truei exhibited relatively wider zygomatic arches, relatively broader, more robust masseteric fossa and coronoid process, and a higher mechanical advantage of the masseter jaw muscle. These craniomandibular traits suggested that P. truei exhibits a relatively stronger bite force that is more suitable to access hard-shelled acorns despite its smaller body size.

Effects of diet on cranial morphology and biting ability in musteloid mammals

Size and shape are often considered important variables that lead to variation in performance. In studies of feeding, size‐corrected metrics of the skull are often used as proxies of biting performance; however, few studies have examined the relationship between cranial shape in its entirety and estimated bite force across species and how dietary ecologies may affect these variables differently. Here, we used geometric morphometric and phylogenetic comparative approaches to examine relationships between cranial morphology and estimated bite force in the carnivoran clade Musteloidea. We found a strong relationship between cranial size and estimated bite force but did not find a significant relationship between cranial shape and size‐corrected estimated bite force. Many‐to‐one mapping of form to function may explain this pattern because a variety of evolutionary shape changes rather than a single shape change may have contributed to an increase in relative biting ability. We also found that dietary ecologies influenced cranial shape evolution but did not influence cranial size nor size‐corrected bite force evolution. Although musteloids with different diets exhibit variation in cranial shapes, they have similar estimated bite forces suggesting that other feeding performance metrics and potentially nonfeeding traits are also important contributors to cranial evolution. We postulate that axial and appendicular adaptations and the interesting feeding behaviours reported for species within this group also facilitate different dietary ecologies between species. Future work integrating cranial, axial and appendicular form and function with behavioural observations will reveal further insights into the evolution of dietary ecologies and other ecological variables.