Energetic tradeoffs control the size distribution of aquatic mammals.

Four extant lineages of mammals have invaded and diversified in the water: Sirenia, Cetacea, Pinnipedia, and Lutrinae. Most of these aquatic clades are larger bodied, on average, than their closest land-dwelling relatives, but the extent to which potential ecological, biomechanical, and physiological controls contributed to this pattern remains untested quantitatively. Here, we use previously published data on the body masses of 3,859 living and 2,999 fossil mammal species to examine the evolutionary trajectories of body size in aquatic mammals through both comparative phylogenetic analysis and examination of the fossil record. Both methods indicate that the evolution of an aquatic lifestyle is driving three of the four extant aquatic mammal clades toward a size attractor at ∼500 kg. The existence of this body size attractor and the relatively rapid selection toward, and limited deviation from, this attractor rule out most hypothesized drivers of size increase. These three independent body size increases and a shared aquatic optimum size are consistent with control by differences in the scaling of energetic intake and cost functions with body size between the terrestrial and aquatic realms. Under this energetic model, thermoregulatory costs constrain minimum size, whereas limitations on feeding efficiency constrain maximum size. The optimum size occurs at an intermediate value where thermoregulatory costs are low but feeding efficiency remains high. Rather than being released from size pressures, water-dwelling mammals are driven and confined to larger body sizes by the strict energetic demands of the aquatic medium.

Adaptations for amphibious vision in sea otters (Enhydra lutris): structural and functional observations.

Sea otters (Enhydra lutris) are amphibious mammals that maintain equal in-air and underwater visual acuity. However, their lens-based underwater accommodative mechanism presumably requires a small pupil that may limit sensitivity across light levels. In this study, we consider adaptations for amphibious living by assessing the tapetum lucidum, retina, and pupil dynamics in sea otters. The sea otter tapetum lucidum resembles that of terrestrial carnivores in thickness and fundic coverage. A heavily rod-dominated retina appears qualitatively similar to the ferret and domestic cat, and a thick outer nuclear layer relative to a thinner inner nuclear layer is consistent with nocturnal vertebrates and other amphibious carnivores. Pupil size range in two living sea otters is smaller relative to other amphibious marine carnivores (pinnipeds) when accounting for test conditions. The pupillary light response seems slower than other aquatic and terrestrial species tested in comparable brightness, although direct comparisons require further assessment. Our results suggest that sea otters have retained features for low-light vision but rapid adjustments and acute underwater vision may be constrained across varying light levels by a combination of pupil shape, absolute eye size, and the presumed coupling between anterior lens curvature and pupil size during accommodation.

Eye Optics in Semiaquatic Mammals for Aerial and Aquatic Vision.

Based on anatomical measurements of refractive structures in the eye, the positions of focused images were computed for several groups of semiaquatic mammals: rodents, a nonpinniped semiaquatic carnivore (the sea otter), and pinniped carnivores (seals, sea lions, and the walrus). In semiaquatic rodents, eye optics enable emmetropia in the air but cause substantial hypermetropia in the water. In semiaquatic carnivores, there are several mechanisms for amphibious vision that focus images on the retina in both air and water. These mechanisms include the potential for a substantial change in the lens shape of sea otters and the presence of the corneal emmetropic window in pinnipeds. The results suggest that several groups of mammals that independently adapted to aquatic environments vary in how their visual systems adapted to aquatic vision.

New data on Mustelidae (Carnivora) from Southeast Asia: Siamogale thailandica, a peculiar otter-like mustelid from the late middle Miocene Mae Moh Basin, northern Thailand.

We report new dental remains of Mustelidae from the late middle Miocene of Mae Moh Basin, northern Thailand, improving the poor fossil record of the family in Southeast Asia. Siamogale thailandica is a poorly known mustelid, previously recorded from just a single tooth. Here we present over a hundred new specimens attributable to this species. S. thailandica shows a combination of primitive and convergent features of the dentition that makes its original subfamilial assignment to Lutrinae doubtful. Evidence from the dental morphology suggests that it belongs to a bunodont otter-like mustelid that evolved in convergence with "true" otters (Lutrinae) toward a semi-aquatic way of life. Autapomorphic features such as the height and the position of the m1 metaconid and the shape of the P4 lingual shelf make S. thailandica unique among Mustelidae. The morphology of this species is mostly similar to Mionictis species and Lartetictis dubia, reported in the Miocene of North America and Europe, respectively. These similarities could imply immigration events to Thailand in the early or middle Miocene. Alternately, the lineage leading to Siamogale might have deeper origins from an endemic early Miocene Southeast Asian mustelid.

A note on the specific cuticle structure of wool hairs in otters (Lutrinae).

The cuticle structure of the wool hairs (secondary hairs) of six otter species was examined by scanning electron microscopy to clarify the specific function of this hair type in the Lutrinae. The species studied were chosen according to the different genera, climatic regions, and degrees of association to water of the Lutrinae. Independent of their preferred habitats, the cuticle of every wool hair examined exhibited in all animals a rather similar shape and arrangement of the scales. This specific adaptive feature allows a flexible interlocking of adjacent wool hairs, which also helps to form thin wool hair bundles that surround small oval shaped spaces. Thus, the trapping of an effective insulating air layer is facilitated and heat loss from the body is reduced.

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.

Bite force is a measure of feeding performance used to elucidate links between animal morphology, ecology, and fitness. Obtaining live individuals for in vivo bite-force measurements or freshly deceased specimens for bite force modeling is challenging for many species. Thomason's dry skull method for mammals relies solely on osteological specimens and, therefore, presents an advantageous approach that enables researchers to estimate and compare bite forces across extant and even extinct species. However, how accurately the dry skull method estimates physiological cross-sectional area (PCSA) of the jaw adductor muscles and theoretical bite force has rarely been tested. Here, we use an ontogenetic series of southern sea otters (Enhydra lutris nereis) to test the hypothesis that skeletomuscular traits estimated from the dry skull method accurately predicts test traits derived from dissection-based biomechanical modeling. Although variables from these two methods exhibited strong positive relationships across ontogeny, we found that the dry skull method overestimates PCSA of the masseter and underestimates PCSA of the temporalis. Jaw adductor in-levers for both jaw muscles and overall bite force are overestimated. Surprisingly, we reveal that sexual dimorphism in craniomandibular shape affects temporalis PCSA estimations; the dry skull method predicted female temporalis PCSA well but underestimates male temporalis PCSA across ontogeny. These results highlight the importance of accounting for sexual dimorphism and other intraspecific variation when using the dry skull method. Together, we found the dry skull method provides an underestimation of bite force over ontogeny and that the underlying anatomical components driving bite force may be misrepresented.

Sexual dimorphism of craniomandibular size in the Eurasian otter, Lutra lutra, from South Korea.

Sexual size dimorphism of craniomandibular morphology of the Eurasian otter Lutra lutra in South Korea was analyzed using linear measurements. In total, 32 skulls (18 males and 14 females) and 22 linear measurements (16 cranial and 6 mandibular measurements) were used. Our results showed statistically significant sexual dimorphism between male and female skull size. Multivariate analyses using the cranial and mandibular traits showed significant differences between the sexes, respectively. The most dimorphic trait was ectorbital breadth (EOB), and the EOB of the male was approximately 10% greater than that of the female. This type of sexual size dimorphism, in which males are generally larger than females, is a general pattern shown in family Mustelidae. Several researchers have suggested various hypotheses about the factors causing sexual size dimorphism, i.e., 'resource partitioning model' and 'sex-specific pressure model'. Our results are consistent with these hypotheses, and we suggest that these factors would have affected the sexual size dimorphism of the Eurasian otter in Korea.

Geographic variation of craniodental morphology of the Eurasian otter (Lutra lutra) in East Asia.

Craniodental morphology of the Eurasian otter (Lutra lutra) in the Korean Peninsula, Japanese islands and Kinmen Island (Taiwan) was studied using geometric morphometrics to identify the skull variations between the populations. Forty adult skulls were examined (29 specimens from the Korean Peninsula, six from Shikoku, Honshu and Hokkaido of Japan, and five from Kinmen Island). Images of the dorsal and ventral views of the skull and the right lateral view of the mandible were analyzed. Specimens from the Korean Peninsula were larger than those from the Japanese islands and Kinmen Island. However, no correlation was observed between the shape variations in the three populations and the centroid size of the skull. The Mann-Whitney U-test showed that relative warps (RWs) RW1, RW2 and RW4 of the dorsal view and RW2 of the ventral view of the skull differed significantly between the populations. Some craniodental differences between the populations were seen in the dorsal and ventral views of the skull, mostly at the snout and parietal regions. The MANOVA test revealed significant differences between the specimens from the Japanese islands and Korean Peninsula and between the specimens from the Korean Peninsula and Kinmen Island. RWs plots showed an overlap of all three populations. In conclusion, the comparisons of the three examined populations revealed significant differences in their craniodental morphology.

The fetal membranes of the otter shrews and a synapomorphy for afrotheria.

The otter shrews of mainland Africa are the closest relatives of the Madagascar tenrecs. We sought for similarities in placentation between the two groups and, in a wider context, with other mammals of the Afrotheria clade. Specimens of the Nimba otter shrew (Micropotamogale lamottei) were obtained from the Ivory Coast and examples of the giant otter shrew (Potamogale velox) from the Hill Collection. The Nimba otter shrew has a central haemophagous organ similar to that in tenrecs. The labyrinth of the Nimba otter shrew, however, is endotheliochorial with syncytial trophoblast enclosing the maternal vessels. On the other hand tenrecs have cellular haemomonochorial placentae and an associated spongy zone, which is not present in the Nimba otter shrew. The placenta of the giant otter shrew is also endotheliochorial. The central region of its placenta is particularly interesting, since the juxtafetal portion is clearly a haemophagous region whereas the labyrinth feeding this region is endotheliochorial. Thus there is considerable variation in placental morphology within Tenrecidae. Importantly, however, both otter shrews have a large allantoic sac divided into four intercommunicating lobes by two pairs of septal folds. A similar arrangement has been described for representatives of each of the remaining five orders within Afrotheria. This is significant because previous anatomical studies have failed to establish a single synapomorphy in support of Afrotheria.

Morphology of the lingual papillae of the Asian short-clawed otter.

We examined the dorsal lingual surface of an adult Asian short-clawed otter (Aonyx cinerea) by using scanning electron microscopy. The filiform papilla on the lingual apex had some pointed processes. The connective tissue core of the filiform papillae consisted of several rod-like processes, and the connective tissue core with a long process was rarely observed. The filiform papilla on the lingual body had several pointed processes and the fungiform papilla had smooth surface. The connective tissue core of the filiform papillae consisted of a large main and several small processes. The vallate papillae were surrounded by a groove and some pads, and many processes were observed on this surface. The tongue of the Asian short-clawed otter was different from that of the Japanese marten belong to family Mustelidae.

Sexual dimorphism of the Eurasian otter (Lutra lutra) in South Korea: Craniodental geometric morphometry.

Sexual dimorphism of the craniodental morphology of the Eurasian otter in South Korea was studied with geometric morphometrics. 29 adult skulls (15 males and 14 females) were used. Images of the dorsal and ventral view of the cranium and right lateral view of the mandible were taken and then digitized, and measurements were taken on the right side. Results showed that size difference between males and females was significant. Correlations between the size and shape variations have not been observed in this study. The bivariate plots with centroid size showed size dimorphism between males and females with some overlapping. Most relative warp (RW) scores were not significantly different between males and females. We observed only RW2 for dorsal and ventral view of the skull, and only RW1 for mandible was significantly different between the sexes. Shape dimorphisms were revealed at the postorbital constriction, temporal-mandibular joint, coronoid process, mandibular condyle and angular process of the skull. Based on our study, sexual dimorphism exists in Eurasian otter from the South Korean population in terms of both the size and shape. Furthermore, the degree of size dimorphism is greater than shape dimorphism.

Morphological Analysis of Long Bones in Semi-aquatic Mustelids and their Terrestrial Relatives.

The locomotor environment and behavior of quadrupedal mammals exert functional constraints on their limbs. Therefore long bone shapes are thought to reflect at least partially the species' locomotor ecology. Semi-aquatic species move through two media with distinct density and viscosity and their locomotor apparatus should therefore reflect a trade-off between the divergent functional constraints it faces. Adaptation to a semi-aquatic lifestyle occurred independently in otters (Lutrinae) and minks (Mustelinae). Analyzing semi-aquatic mustelids and their terrestrial relatives, we investigate long bone shape diversity, describe changes in long bone shape associated with a semi-aquatic lifestyle, and discuss the functional consequences of these shape changes. The robustness of the otter bones is highlighted and its potential ballast role discussed. Large epiphyses are observed in otters but this trend seems associated with terrestrial more than with aquatic locomotion. Thus, the most aquatic species, Enhydra lutris, presents narrow knee articulations compared to similar sized less aquatic species. Enhydra lutris presents a fore- and hind limb shape that diverge from that in other otters. Minks show bone shapes similar to each other but only Neovison vison tends to differ from its terrestrial relatives. The evolution of limb shape in this group is strongly correlated with size, locomotor mode, and phylogenetic history, leading to a morphological pattern where the roles of each of these factors are difficult to disentangle.

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.

Comparative functional anatomy of hindlimb muscles and bones with reference to aquatic adaptation of the sea otter.

Although the sea otter (Enhydra lutris) is a complete aquatic species, spending its entire life in the ocean, it has been considered morphologically to be a semi-aquatic animal. This study aimed to clarify the unique hindlimb morphology and functional adaptations of E. lutris in comparison to other Mustelidae species. We compared muscle mass and bone measurements of five Mustelidae species: the sea otter, Eurasian river otter (Lutra lutra), American mink (Neovison vison), Japanese weasel (Mustela itatsi) and Siberian weasel (M. sibirica). In comparison with the other 4 species, E. lutris possessed significantly larger gluteus, popliteus and peroneus muscles, but smaller adductor and ischiopubic muscles. The popliteus muscle may act as a medial rotator of the crus, and the peroneus muscle may act as an abductor of the fifth toe and/or the pronator of the foot. The bundles of the gluteus superficialis muscle of E. lutris were fused with those of the tensor fasciae latae muscle and gluteofemoralis muscles, and they may play a role in femur abduction. These results suggest that E. lutris uses the abducted femur, medially rotated crus, eversion of the ankle and abducted fifth digit or extended interdigital web as a powerful propulsion generator. Therefore, we conclude that E. lutris is a complete aquatic animal, possessing differences in the proportions of the hindlimb muscles compared with those in other semi-aquatic and terrestrial mustelids.

Ontogeny of Oxygen Storage Capacity and Diving Ability in the Southern Sea Otter (Enhydra lutris nereis): Costs and Benefits of Large Lungs.

Small body size, large lungs, and dense pelage contribute to the unique challenges faced by diving sea otters (Enhydra lutris) when compared to other marine mammals. Here we determine the consequences of large lungs on the development of diving ability in southern sea otters (Enhydra lutris nereis) by examining the ontogeny of blood, muscle, and lung oxygen stores and calculating aerobic dive limits (cADL) for immature and mature age classes. Total oxygen storage capacity matures rapidly in sea otters, reaching adult levels by 2 mo postpartum. But this result is driven by exceptional lung capacity at birth, followed by a decrease in mass-specific lung volume with age. Blood and muscle oxygen stores remain well below adult values before weaning, with large pups exhibiting 74% and 54% of adult values, respectively. Slow muscle development limits the capacity of immature sea otters to dive against high positive buoyancy due to comparatively large lungs. Immature sea otters diving with total lung capacity (TLC) experience up to twice the mass-specific positive buoyancy as adults diving with TLC but can reduce these forces to comparable adult levels by using a smaller diving lung volume (DLV). The cADL of a juvenile with DLV is 3.62 min, while the cADL of an adult with TLC is 4.82 min. We find that the magnitude of positive buoyancy experienced by sea otters changes markedly with age and strongly influences the ontogeny of diving ability in this species.

Systematization, distribution, and territories of the caudal cerebral artery on the surface of the brain in nutria (Myocastor coypus) / Sistematização, distribuição e territórios da artéria cerebral caudal na superfície do cérebro em Nutria (Myocastor coypus)

The nutria (Myocastor coypus) is a medium-sized, semi-aquatic rodent valued by the skin and meat industry. This study aimed to describe and systematize the caudal cerebral artery on the brain surface in nutria, establishing a standard model and its main variations in this species. The thirty animals used were euthanized according to animal welfare rules. The vessels were filled with latex stained with red pigment and the samples were fixed in formaldehyde. In nutria, the brain was vascularized by the vertebral basilar system. The terminal branches of the basilar artery originated the rostral cerebellar, caudal cerebral, rostral choroidal and middle cerebral arteries, and its terminal branch, the rostral cerebral artery. The terminal branch of the basilar artery projected the caudal cerebral artery, which is usually a single medium-caliber vessel, into the transverse fissure of the brain. The caudal cerebral artery was presented as a single (66.7% of the cases to the right and 76.7% to the left) and double vessel (33.3% of the cases to the right and 23.3% to the left). It originated the rostral mesencephalic artery, the proximal component, and the caudal inter-hemispheric artery. The terminal branches of the rostral and caudal tectal mesencephalic arteries formed a typical anastomotic network. The caudal inter-hemispheric artery emitted central branches, the caudal choroidal artery, hemispherical occipital arteries, rostral tectal mesencephalic branches and distal components, and anastomosed "in osculum" with the terminal branches of the rostral inter-hemispheric artery. The caudal choroidal artery anastomosed with the rostral choroidal artery, where it branched out on the thalamic mass, vascularizing all diencephalic structures and the hippocampus. The caudal cerebral artery and its terminal branches anastomosed with the terminal branches of the rostral and middle cerebral arteries in a restricted region of the caudal pole of the cerebral hemisphere. The vascularization area of the caudal cerebral artery and its central branches in the paleopallial of the piriform lobe is extremely restricted, caudomedially.(AU)

A nutria (Myocastor coypus) é um roedor semi-aquático de tamanho mediano, apreciado na indústria de peles e carne. Este trabalho tem por objetivo descrever e sistematizar a artéria cerebral caudal na superfície do cérebro em nutria, estabelecendo um modelo padrão e suas principais variações e territórios nesta espécie. Os trinta animais utilizados foram eutanasiados segundo as regras de bem-estar animal, os vasos foram preenchidos com látex, corado em vermelho e as peças foram fixadas em formoldeído. O cérebro foi vascularizado exclusivamente pelo sistema vértebro-basilar. Os ramos terminais da artéria basilar originaram as artérias cerebelar rostral, cerebral caudal, corióidea rostral, cerebral média e seu ramo terminal, a artéria cerebral rostral. O ramo terminal da artéria basilar lançou a artéria cerebral caudal, um vaso normalmente único, de médio calibre, para o interior da fissura transversa do cérebro. A artéria cerebral caudal foi um vaso único em 66,7% à direita e em 76,7% à esquerda e mostrou-se dupla em 33,3% à direita e em 23,3% à esquerda. Ela lançou a artéria tectal mesencefálica rostral, componente proximal e a artéria inter-hemisférica caudal. Os ramos terminais das artérias tectais mesencefálicas, rostral e caudal, formavam uma rede anastomótica típica. A artéria inter-hemisférica caudal lançou ramos centrais, a artéria corióidea caudal, as artérias hemisféricas occipitais, os ramos tectais mesencefálicos rostrais, componentes distais e anastomosou-se "em ósculo" com o ramo terminal da artéria inter-hemisférica rostral. A artéria corióidea caudal anastomosava-se com a artéria corióidea rostral, onde ramificavam-se sobre a massa talâmica, vascularizando todas as estruturas do diencéfalo e hipocampo. A artéria cerebral caudal com seus ramos terminais apresenta anastomoses com os ramos terminais das artérias cerebrais rostral e média em uma região restrita do pólo caudal do hemisfério cerebral. A área de vascularização da artéria cerebral caudal com seus ramos centrais no páleo-palio do lobo piriforme é extremamente restrita, caudo-medialmente ao mesmo.(AU)

Refractive state, ocular anatomy, and accommodative range of the sea otter (Enhydra lutris).

Sea otters are carnivorous, amphibious mammals that are active both above and under water. Accordingly, it might be expected that their eyes are adapted for both aerial and aqueous vision. We examined the anatomy and physiological optics of the sea otter eye with a view towards describing and explaining its amphibious visual characteristics. We employed photokeratoscopy to measure the refractive power of the sea otter cornea, which we found to be 59 D. Using video dynamic photorefraction, we found that sea otters can focus targets clearly both in air and water, relying on accommodation to compensate for the refractive loss of their corneas upon immersion in water. Our anatomical investigations revealed that the anterior epithelium of the cornea is extensively developed, as is the iris musculature, meridional ciliary muscle, and the corneoscleral venous plexus. The first feature is most likely an adaptation to the salinity of the marine environment. We believe the latter features are part of a novel, well-developed lenticular accommodative mechanism.

Age-related change and allometry of skull and canine of sea otters, Enhydra lutris.

Skulls and canines of 460 sea otters from Lopatka Cape, Kamchatka, were examined to assess development patterns, individual variation and sexual differences. An allometric formula was applied to morphometrical data, and the relative growth of each character to total length of skull was analyzed. In both sexes, most morphometrical characters ceased growth at about 2 years of age. Canine root length increased rapidly during the first year of life, while crown length decreased due to remarkable wear. There was large individual variation in the feeding and breathing/sniffing apparatus, while there was little variation in braincase size. There were sexual differences in most characteristics, although males and females showed similar growth patterns. The coronoid process of the mandible showed positive allometry in both sexes, and we attributed this finding to feeding habits. The fact that only male mastoids showed positive allometry may be due to the need for male otters to maintain a passing territory.

Differences in blood haptoglobin and length-mass relationships in river otters (Lutra canadensis) from oiled and nonoiled areas of Prince William Sound, Alaska.

Significant differences in levels of blood haptoglobin occurred between river otters (Lutra canadensis) inhabiting oiled (mean = 361 mg/100 ml, SD = 38, n = 6) and nonoiled (mean = 306 mg/100 ml, SD = 87, n = 8) areas of Prince William Sound, Alaska (USA) following the Exxon Valdez oil spill in 1989. Additionally, male river otters from oiled areas had significantly lower body mass (1.13 kg) than male otters from nonoiled areas. We propose oil-related causes for these differences.

Evidence for recovery of body mass and haptoglobin values of river otters following the Exxon Valdez oil spill.

Levels of blood haptoglobin (Hp) and interleukin-6 immunoreactive protein (IL-6 ir) were significantly elevated in river otters (Lutra canadensis) inhabiting oiled areas of Prince William Sound, Alaska (USA) following the Exxon Valdez oil spill in 1989. By May and June 1992, however, such differences were not apparent. Mean body mass of otters, adjusted for sex, age-class, and total length with analysis of covariance, differed between oiled and non-oiled areas from 1990 to 1992, but were nearly identical by May and June 1992. We propose that river otters may be recovering from chronic effects that we observed in 1990 and 1991 following the 1989 Exxon Valdez oil spill, but further research is necessary to test this hypothesis.