Innervation patterns of mystacial vibrissae support active touch behaviors in California sea lions (Zalophus californianus).

Vibrissae or follicle-sinus complexes (F-SCs) are highly developed mammalian sensory structures. These blood-filled sinuses are richly innervated and possess novel mechanoreceptors. Although much is known regarding the function of F-SCs in terrestrial mammals, much less is known regarding marine carnivores such as pinnipeds. Pinnipeds possess the largest, most highly innervated vibrissae of any mammal. One such pinniped is the California sea lion, which are generalist marine predators that rely heavily upon tactile discrimination capabilities. Psychophysical studies demonstrate that haptic tactile discrimination using F-SCs is exceptionally sensitive. However, our knowledge of the structure and function of F-SCs in otariids is limited. Our objectives were to investigate the innervation and microstructure of F-SCs across the mystacial vibrissal field and infer function from haptic performance studies in California sea lions. Innervation and microstructure of vibrissae differed considerably compared to similar data available for phocids. Total innervation of mystacial vibrissae was estimated to be 86,042 axons. Investigations of innervation density and investment of microvibrissae versus macrovibrissae demonstrated a significantly increased axon density per F-SC in medial microvibrissal regions compared to lateral macrovibrissae, which supports psychophysical data and somatotopic organization of the central nervous system involved with tactile discrimination capability. Innervation increased from medial microvibrissae (705 ± 125 axons/F-SC) to lateral macrovibrissae (1,447 ± 154) as well as from dorsal (541 ± 60) to ventral (1,493 ± 327) vibrissal regions. These data provide a more complete picture of the sensory ecology of this important aquatic mammalian lineage; the specialization of peripheral sensory structures, central nervous structures with demonstrated enhanced haptic capabilities behaviorally has likely led to the ecological success of California sea lions.

A cerebellar substrate for cognition evolved multiple times independently in mammals.

Given that complex behavior evolved multiple times independently in different lineages, a crucial question is whether these independent evolutionary events coincided with modifications to common neural systems. To test this question in mammals, we investigate the lateral cerebellum, a neurobiological system that is novel to mammals, and is associated with higher cognitive functions. We map the evolutionary diversification of the mammalian cerebellum and find that relative volumetric changes of the lateral cerebellar hemispheres (independent of cerebellar size) are correlated with measures of domain-general cognition in primates, and are characterized by a combination of parallel and convergent shifts towards similar levels of expansion in distantly related mammalian lineages. Results suggest that multiple independent evolutionary occurrences of increased behavioral complexity in mammals may at least partly be explained by selection on a common neural system, the cerebellum, which may have been subject to multiple independent neurodevelopmental remodeling events during mammalian evolution.

The tympanic region of Otaria byronia (Otariidae, Carnivora) - morphology, ontogeny, age classes and dimorphism.

Here we describe and explore for the first time the ontogeny and sexual dimorphism of the auditory region of Otaria byronia. We studied the tympanic region of skulls of 237 specimens of different ages and sexes. Geometric morphometric methods were used to analyze the tympanic bulla. In addition, 3D reconstructions of the tympanic bulla were performed using computed tomography analysis scans and a serial wearing technique. We provide a description of the external and internal morphology of the tympanic bulla in both sexes and across different stages (bioclasses). The average shape of the bulla in O. byronia has a subtriangular contour, with variations between sexes and ages. Each stage (bioclasses I, II, and III) is characterized by the respective mean shape of the tympanic bulla and designated as a morphoclass (1, 2, and 3). In all cases, the ectotympanic shows greater surface area than the endotympanic, as in other otariids, in contrast to Phocidae. During ontogeny, the relative size of the ectotympanic increases, growing in all directions and covering the endotympanic. This pattern is seen to the greatest extent in adult males, in which the ectotympanic forms an extremely well-developed apophysis jugulare. No differences in internal morphology of the tympanic cavity were recorded between ages and sexes. The bulla does not increase in thickness in successive age classes; in fact, the walls are extremely thin in the adult stages, despite the extensive development of its processes. This pattern is opposite that observed in Phocidae. In morphoclass 3, adult males older than 7 years undergo hypermorphic change that results in a peramorphic condition when compared to adult females. These changes probably follow the same pattern shown by the rest of the skull and contribute to the marked sexual dimorphism of the species.

Optic nerve, superior colliculus, visual thalamus, and primary visual cortex of the northern elephant seal (Mirounga angustirostris) and California sea lion (Zalophus californianus).

The northern elephant seal (Mirounga angustirostris) and California sea lion (Zalophus californianus) are members of a diverse clade of carnivorous mammals known as pinnipeds. Pinnipeds are notable for their large, ape-sized brains, yet little is known about their central nervous system. Both the northern elephant seal and California sea lion spend most of their lives at sea, but each also spends time on land to breed and give birth. These unique coastal niches may be reflected in specific evolutionary adaptations to their sensory systems. Here, we report on components of the visual pathway in these two species. We found evidence for two classes of myelinated fibers within the pinniped optic nerve, those with thick myelin sheaths (elephant seal: 9%, sea lion: 7%) and thin myelin sheaths (elephant seal: 91%, sea lion: 93%). In order to investigate the architecture of the lateral geniculate nucleus, superior colliculus, and primary visual cortex, we processed brain sections from seal and sea lion pups for Nissl substance, cytochrome oxidase, and vesicular glutamate transporters. As in other carnivores, the dorsal lateral geniculate nucleus consisted of three main layers, A, A1, and C, while each superior colliculus similarly consisted of seven distinct layers. The sea lion visual cortex is located at the posterior side of cortex between the upper and lower banks of the postlateral sulcus, while the elephant seal visual cortex extends far more anteriorly along the dorsal surface and medial wall. These results are relevant to comparative studies related to the evolution of large brains.

A Robotic Platform to Study the Foreflipper of the California Sea Lion.

The California sea lion (Zalophus californianus), is an agile and powerful swimmer. Unlike many successful swimmers (dolphins, tuna), they generate most of their thrust with their large foreflippers. This protocol describes a robotic platform designed to study the hydrodynamic performance of the swimming California sea lion (Zalophus californianus). The robot is a model of the animal's foreflipper that is actuated by motors to replicate the motion of its propulsive stroke (the 'clap'). The kinematics of the sea lion's propulsive stroke are extracted from video data of unmarked, non-research sea lions at the Smithsonian Zoological Park (SNZ). Those data form the basis of the actuation motion of the robotic flipper presented here. The geometry of the robotic flipper is based a on high-resolution laser scan of a foreflipper of an adult female sea lion, scaled to about 60% of the full-scale flipper. The articulated model has three joints, mimicking the elbow, wrist and knuckle joint of the sea lion foreflipper. The robotic platform matches dynamics properties-Reynolds number and tip speed-of the animal when accelerating from rest. The robotic flipper can be used to determine the performance (forces and torques) and resulting flowfields.

Microvasculature of the California sea lion (Zalophus californianus) eye and its functional significance.

OBJECTIVE: To examine the ocular circulation in California sea lions (Zalophus californianus). ANIMALS STUDIED: Eyes were obtained postmortem from three sea lions that died while in captivity. PROCEDURES: Specimens from sea lions were investigated using scanning electron microscopy (SEM) of vascular corrosion casts. The thermal characteristics of live animal eyes were measured using an infrared imaging system. RESULTS: The major orbital artery of the sea lion was the ophthalmic artery. The artery was remarkably thick in diameter, showed a marked convolution and formed an ophthalmic rete around the optic nerve at the posterior pole of the eyeball. The long posterior ciliary artery terminates to form a prominent inner arterial circle at the pupillary margin. The iridial arteries originated from the arterial circle showing either a crimped or somewhat coiled course, extending toward the root of the iris and formed a root supplying a large amount of blood to the iris and ciliary bodies. The venules in the conjunctiva formed a well-developed venous plexus. The vortex veins showed a dilation and constriction at the site passing through the sclera. Thermographic examination revealed that the eye showed a higher degree of thermal emission than adjacent skin areas. CONCLUSIONS: These characteristics suggest that the ocular vasculature might play roles in thermoregulation as well as in hemodynamics by draining a large amount of blood so that the appropriate operating temperature for the eye can be maintained in a deep and cold aquatic environment.

Somatosensory brainstem, thalamus, and cortex of the California sea lion (Zalophus californianus).

Pinnipeds (sea lions, seals, and walruses) are notable for many reasons, including their ape-sized brains, their adaptation to a coastal niche that combines mastery of the sea with strong ties to land, and the remarkable abilities of their trigeminal whisker system. However, little is known about the central nervous system of pinnipeds. Here we report on the somatosensory areas of the nervous system of the California sea lion (Zalophus californianus). Using stains for Nissl, cytochrome oxidase, and vesicular glutamate transporters, we investigated the primary somatosensory areas in the brainstem, thalamus, and cortex in one sea lion pup and the external anatomy of the brain in a second pup. We find that the sea lion's impressive array of whiskers is matched by a large trigeminal representation in the brainstem with well-defined parcellation that resembles the barrelettes found in rodents but scaled upward in size. The dorsal column nuclei are large and distinct. The ventral posterior nucleus of the thalamus has divisions, with a large area for the presumptive head representation. Primary somatosensory cortex is located in the neocortex just anterior to the main vertical fissure, and precisely locating it as we do here is useful for comparing the highly gyrified pinniped cortex with that of other carnivores. To our knowledge this work is the first comprehensive report on the central nervous system areas for any sensory system in a pinniped. The results may be useful both in the veterinary setting and for comparative studies related to brain evolution.

Health Status of Galápagos Sea Lions (Zalophus wollebaeki) on San Cristóbal Island Rookeries Determined by Hematology, Biochemistry, Blood Gases, and Physical Examination.

The Galápagos sea lion, Zalophus wollebaeki, is an endemic and endangered species subject to population decline associated with environmental variability, such as El Niño events, constant feeding stress, and exposure to diseases through contact with introduced species. Reference blood parameter intervals have been published for some pinniped species, but baseline biochemical and blood gas values are lacking from Z. wollebaeki. We analyzed blood samples from 30 juvenile Galápagos sea lions (19 females, 11 males) captured in two rookeries on San Cristóbal Island. A portable blood analyzer (iSTAT) was used to obtain near-immediate field results for pH, partial pressure of O2, partial pressure of CO2, bicarbonate (HCO3(-)), hematocrit (Hct), hemoglobin, Na, K, ionized Ca, and glucose, and blood lactate was measured using a portable Lactate Plus(TM) analyzer. Average heart rate, biochemistry, and hematology parameters were comparable with healthy individuals of other pinniped species. Hemoglobin was significantly correlated with body condition of juvenile Galápagos sea lions. When compared with available blood values of clinically healthy California sea lions, Galápagos sea lions had higher total protein and Hct and lower Ca and K levels. Our results provide baseline data that may be useful in comparisons among populations and in detecting changes in health status among Galápagos sea lions.

Morphology of the lingual surface of South American fur seal (Arctocephalus australis) and sea lion (Otaria flavescens).

In this study, we aimed to describe the morphological characteristics of the lingual papillae in two species of Otariidae family by stereomicroscopy and scanning electron microscopy. We used tongues of two South American Otariidae species. The tongues were elongated and terminated in bifid apex and there was no median sulcus on the dorsal lingual surface. The most numerous type of lingual papilla was filiform in the South American fur seal (SASL) and entire dorsal lingual surface was covered by these filiform papillae but the dorsal surface of the tongue of the South American sea lion was covered by numerous polygonal projections, which were different in size. Fungiform papillae were detected in only SASL and they randomly distributed on the lingual apex and body, and some fungiform papillae were collected into twosome or threesome groups on the posterior part of the lingual body. Circumvallate papilla was found in the center of the lingual radix of South American sea lion. Thread-like conical papillae were common for both species and they located on the lingual radix. We determined that lingual surface morphology was completely different in each species, although they were members of the same family, Otariidae.

Applicability of single-camera photogrammetry to determine body dimensions of pinnipeds: Galapagos sea lions as an example.

Morphological features correlate with many life history traits and are therefore of high interest to behavioral and evolutionary biologists. Photogrammetry provides a useful tool to collect morphological data from species for which measurements are otherwise difficult to obtain. This method reduces disturbance and avoids capture stress. Using the Galapagos sea lion (Zalophus wollebaeki) as a model system, we tested the applicability of single-camera photogrammetry in combination with laser distance measurement to estimate morphological traits which may vary with an animal's body position. We assessed whether linear morphological traits estimated by photogrammetry can be used to estimate body length and mass. We show that accurate estimates of body length (males: ±2.0%, females: ±2.6%) and reliable estimates of body mass are possible (males: ±6.8%, females: 14.5%). Furthermore, we developed correction factors that allow the use of animal photos that diverge somewhat from a flat-out position. The product of estimated body length and girth produced sufficiently reliable estimates of mass to categorize individuals into 10 kg-classes of body mass. Data of individuals repeatedly photographed within one season suggested relatively low measurement errors (body length: 2.9%, body mass: 8.1%). In order to develop accurate sex- and age-specific correction factors, a sufficient number of individuals from both sexes and from all desired age classes have to be captured for baseline measurements. Given proper validation, this method provides an excellent opportunity to collect morphological data for large numbers of individuals with minimal disturbance.

Predictive equations for the estimation of body size in seals and sea lions (Carnivora: Pinnipedia).

Body size plays an important role in pinniped ecology and life history. However, body size data is often absent for historical, archaeological, and fossil specimens. To estimate the body size of pinnipeds (seals, sea lions, and walruses) for today and the past, we used 14 commonly preserved cranial measurements to develop sets of single variable and multivariate predictive equations for pinniped body mass and total length. Principal components analysis (PCA) was used to test whether separate family specific regressions were more appropriate than single predictive equations for Pinnipedia. The influence of phylogeny was tested with phylogenetic independent contrasts (PIC). The accuracy of these regressions was then assessed using a combination of coefficient of determination, percent prediction error, and standard error of estimation. Three different methods of multivariate analysis were examined: bidirectional stepwise model selection using Akaike information criteria; all-subsets model selection using Bayesian information criteria (BIC); and partial least squares regression. The PCA showed clear discrimination between Otariidae (fur seals and sea lions) and Phocidae (earless seals) for the 14 measurements, indicating the need for family-specific regression equations. The PIC analysis found that phylogeny had a minor influence on relationship between morphological variables and body size. The regressions for total length were more accurate than those for body mass, and equations specific to Otariidae were more accurate than those for Phocidae. Of the three multivariate methods, the all-subsets approach required the fewest number of variables to estimate body size accurately. We then used the single variable predictive equations and the all-subsets approach to estimate the body size of two recently extinct pinniped taxa, the Caribbean monk seal (Monachus tropicalis) and the Japanese sea lion (Zalophus japonicus). Body size estimates using single variable regressions generally under or over-estimated body size; however, the all-subset regression produced body size estimates that were close to historically recorded body length for these two species. This indicates that the all-subset regression equations developed in this study can estimate body size accurately.

Comparative anatomy of the ophthalmic rete and its relationship to ocular blood flow in three species of marine mammal.

OBJECTIVE: To examine the blood supply to the eyes of bottlenose dolphin (Tursiops truncatus), spotted seal (Phoca largha), and California sea lion (Zalophus californianus). Emphasis is placed on exploring the anatomic function in the context of aquatic life. PROCEDURE: Methyl methacrylate casts were prepared and studied using a scanning electron microscope. Infrared images of the eye were recorded using a thermocamera. RESULTS: In all three marine species, blood is supplied to the ophthalmic rete. The main source of blood supply to the rete is the basilar rete via the spinal rete in the dolphin and via the ophthalmic artery in the seal and sea lion. The retinal and choroidal arteries are derived from the rete. The dolphin rete showed a very well-developed arterial network occupying most of the orbit. The rete in pinnipeds was less developed with several entwining arteries, unlike that in cetaceans. Thermographic examination revealed that the eye shows a higher degree of thermal emission than adjacent areas of the skin in these 3 species. DISCUSSION: The role of the rete in aquatic mammals appears to conserve ocular temperature so that the appropriate operating temperature for photoreceptors and ocular muscles can be maintained in a cold ambient temperature. Additionally, the rete might have a flow-damping effect by maintaining resistance to blood flow in the orbit. This study highlights the special nature of ocular vascular anatomy and function that enabled the unique adaptation of aquatic mammals to life in aquatic habitats.

Testing Bergmann's rule and the Rosenzweig hypothesis with craniometric studies of the South American sea lion.

We tested the validity of Bergmann's rule and Rosenzweig's hypothesis through an analysis of the geographical variation of the skull size of Otaria flavescens along the entire distribution range of the species (except Brazil). We quantified the sizes of 606 adult South American sea lion skulls measured in seven localities of Peru, Chile, Uruguay, Argentina, and the Falkland/Malvinas Islands. Geographical and environmental variables included latitude, longitude, and monthly minimum, maximum, and mean air and ocean temperatures. We also included information on fish landings as a proxy for productivity. Males showed a positive relationship between condylobasal length (CBL) and latitude, and between CBL and the six temperature variables. By contrast, females showed a negative relationship between CBL and the same variables. Finally, female skull size showed a significant and positive correlation with fish landings, while males did not show any relationship with this variable. The body size of males conformed to Bergmann's rule, with larger individuals found in southern localities of South America. Females followed the converse of Bergmann's rule at the intraspecific level, but showed a positive relationship with the proxy for productivity, thus supporting Rosenzweig's hypothesis. Differences in the factors that drive body size in females and males may be explained by their different life-history strategies. Our analyses demonstrate that latitude and temperature are not the only factors that explain spatial variation in body size: others such as food availability are also important for explaining the ecogeographical patterns found in O. flavescens.

Genital morphology of the male South American fur seal (Arctocephalus australis) and biological implications / Morfologia dos órgãos genitais do macho do Lobo marinho (Arctocephalus australis) e implicações biológicas

Male capacity for spreading genes to a great number of descendents and to determine population dynamics depend directly on the genital organs. Morphological studies in pinnipeds are scarce and the functional meaning of some characteristics has never been discussed. We hypothesized that Arctocephalus australis (A. australis) shows morphophysiological adaptations in order to guarantee the perpetuation of the species in the unique annual mating season. Seven males, dead from natural causes, had their genital organs collected and fixed for morphological description. Some features differ from other described mammalian males and are closely related to the biology and reproductive cycle of this species, as the scrotal epidermis, absence of glandular portion in the ductus deferens and spermatogenic epithelium suggest a recrudescent testis period. The corona glandis exhibits a singular arrangement: its erectile border looks like a formation of petals and its association with the os penis gives a "lily-flower" form to this region. We propose the name margo petaliformis to this particular erectile border of the corona glandis because of its similarity to a flower corola. The male genital organs of A. australis show morphological features compatible with adaptation to environment requirements and reproductive efficiency.(AU)

A capacidade do macho de espalhar seus genes a um grande número de descendentes e determinar a dinâmica populacional depende diretamente dos seus órgãos genitais. Estudos morfológicos em pinípedes são escassos e o significado funcional de algumas de suas características ecológicas ainda foi pouco discutido. Nossa hipótese é que Arctocephalus australis (A. australis) apresenta adaptações morfofisiológicas em seus órgãos genitais capazes de interagir com o meio e garantir a perpetuação da espécie que apresenta apenas uma época de acasalamento que ocorre uma vez a cada ano. Sete A. australis machos, mortos recentes por causas naturais, tiveram seus órgãos genitais coletados e fixados para a descrição macro, micro e ultraestrutural. Algumas características diferem de outros machos já descritos e estão intimamente relacionados com a biologia e ciclo reprodutivo da espécie, dentre elas podemos citar a alta queratinização da epiderme escrotal que pode se relacionar com as rotineiras lesões por atrito desta região nas pedras; a ausência da porção glandular do ducto deferente aqui descrita pela primeira vez, o epitélio espermatogênico sugere um período de testículo recrudescente. A glande apresenta um arranjo singular: a coroa da glande apresenta porção lateral de tecido esponjoso que são bordas livres com capacidade de intumescencia. O osso peniano se encontra no centro destas bordas e representa a extremidade mais distal do penis, levando consigo o óstio uretral externo. As bordas associadas ao osso peniano, dão uma forma de "Flor de lírio" a esta região. Utilizamos o nome margo petaliformis a margem erétil liliforme a particular morfologia da glande, pela sua semelhança a uma corola de flor. Os órgãos genitais masculinos de A. australis mostram características morfológicas compatíveis com uma adaptação aos requisitos ambientais e de eficiência reprodutiva.(AU)

Skin histology and its role in heat dissipation in three pinniped species.

BACKGROUND: Pinnipeds have a thick blubber layer and may have difficulty maintaining their body temperature during hot weather when on land. The skin is the main thermoregulatory conduit which emits excessive body heat. METHODS: Thorough evaluation of the skin histology in three pinniped species; the California sea lion-Zalophus californianus, the Pacific harbor seal-Phoca vitulina richardsi, and the Northern elephant seal-Mirounga angustirostris, was conducted to identify the presence, location and distribution of skin structures which contribute to thermoregulation. These structures included hair, adipose tissue, sweat glands, vasculature, and arteriovenous anastomoses (AVA). Thermal imaging was performed on live animals of the same species to correlate histological findings with thermal emission of the skin. RESULTS: The presence and distribution of skin structures directly relates to emissivity of the skin in all three species. Emissivity of skin in phocids (Pacific harbor and Northern elephant seals) follows a different pattern than skin in otariids (California sea lions). The flipper skin in phocids tends to be the most emissive region during hot weather and least emissive during cold weather. On the contrary in otariids, skin of the entire body has a tendency to be emissive during both hot and cold weather. CONCLUSION: Heat dissipation of the skin directly relates to the presence and distribution of skin structures in all three species. Different skin thermal dissipation patterns were observed in phocid versus otariid seals. Observed thermal patterns can be used for proper understanding of optimum thermal needs of seals housed in research facilities, rescue centers and zoo exhibits.

Anatomy of the California sea lion globe.

OBJECTIVE: This study analyzed the morphology of the California sea lion globe to determine what features may contribute to their characteristic visual abilities. PROCEDURE: Globes from the Comparative Ocular Pathology Laboratory of Wisconsin (COPLOW) collection were examined from gross photographs and microscopic sections stained with hematoxylin and eosin, trichrome, smooth muscle actin, and alcian blue periodic acid-Schiff (PAS). Transmission electron microscopy of the cornea and iris was also performed. CLINICAL RESULTS: There was a round, flattened area ventromedial to the axial cornea. The pupil was tear-drop shaped. Pectinate ligaments were visible without magnification. The retina was holangiotic, containing numerous spoke-like venules and arterioles. The tapetum was green encompassing the entire fundus. The optic nerve was unmyelinated. HISTOLOGICAL RESULTS: The sclera was thinnest equatorially and thickest at the limbus and posterior pole. Bowman's layer was difficult to see by light microscopy but clear with transmission electron microscopy. The cornea had a thick epithelium, thin endothelium and Descemet's membrane, and the stroma thinned axially. The dilator muscle was absent near the pupil, but enlarged and mingled with the sphincter muscle near the iris base. A large, wide ciliary cleft with prominent trabeculae and a single continuous pectinate ligament was present. The corneoscleral trabecular meshwork was discontinuous. A round lens attached to the ciliary body via direct attachment to ciliary processes and delicate zonular ligaments. There was a circumferential muscle at the base of the ciliary processes. A thick tapetum covered the entire fundus except peripherally. The retina was characterized by sparse, large ganglion cells.

Harbor seal vibrissa morphology suppresses vortex-induced vibrations.

Harbor seals (Phoca vitulina) often live in dark and turbid waters, where their mystacial vibrissae, or whiskers, play an important role in orientation. Besides detecting and discriminating objects by direct touch, harbor seals use their whiskers to analyze water movements, for example those generated by prey fish or by conspecifics. Even the weak water movements left behind by objects that have passed by earlier can be sensed and followed accurately (hydrodynamic trail following). While scanning the water for these hydrodynamic signals at a swimming speed in the order of meters per second, the seal keeps its long and flexible whiskers in an abducted position, largely perpendicular to the swimming direction. Remarkably, the whiskers of harbor seals possess a specialized undulated surface structure, the function of which was, up to now, unknown. Here, we show that this structure effectively changes the vortex street behind the whiskers and reduces the vibrations that would otherwise be induced by the shedding of vortices from the whiskers (vortex-induced vibrations). Using force measurements, flow measurements and numerical simulations, we find that the dynamic forces on harbor seal whiskers are, by at least an order of magnitude, lower than those on sea lion (Zalophus californianus) whiskers, which do not share the undulated structure. The results are discussed in the light of pinniped sensory biology and potential biomimetic applications.