Microanatomy of the major airway mucosa of the bowhead whale, Balaena mysticetus

In the bowhead whale, Balaena mysticetus, the mucosa of the major airways from the blowholes through the rostral portion of the larynx is lined with parakeratotic, pigmented, stratified squamous epithelium. Scattered enlarged connective tissue papillae of the lamina propria of the nasal vestibules and the palatopharyngeal sphincter contain encapsulated nerve endings. Abundant papillae in the mucosa covering the epiglottic and arytenoid cartilages contain similar nerve endings. The remainder of the laryngeal cavity and laryngeal sac is lined by a variably pigmented, stratified squamous epithelium, which is not keratinized. At the laryngotracheal junction the lining changes to ciliated pseudostratified columnar epithelium which continues through the trachea and principal bronchi. Scanning electron microscopy (SEM) indicates that this epithelium is typically mammalian, with approximately half of the surface cells bearing cilia and slender microvilli. The remaining cells are mucus producing and have thicker microvilli. The valvular mass regulating the external nares consists of irregular, dense white fibrous connective tissue with numerous adipose cells and is penetrated by skeletal muscle cords ranging from 2-4 mm in diameter. The septal mass between the blowholes is composed of irregular, dense white fibrous connective tissue containing large tendinous bundles, clusters of adipose cells, and several large arteries and thick-walled veins. The lamina propria of the nasal vestibules is irregular, dense white fibrous connective tissue. That of the larynx is not as dense and contains proportionately more elastic fibers. The laryngeal sac does not contain elastic laminae, but does have a tunica muscularis of skeletal muscle bundles. Within the trachea and principal bronchi, the lamina propria possesses laminae of longitudinally oriented elastic fibers and simple, branched tubuloalveolar mucous glands. The nasal, laryngeal, tracheal, and bronchial cartilages are hyaline with vascular channels.     

Macroanatomy of the renicule of the bowhead whale (Balaena mysticetus)

The macroanatomy of renicules and surrounding tissues from the kidneys of five Eskimo-harvested bowhead whales, Balaena mysticetus, was examined. These renicules are similar in overall structure to those of other cetaceans and intermediate in size. There are several important differences including the presence of arcuate vessels within the sporta perimedularis, the extension of connective tissue from the sporta deep into the peripheral cortex, and the presence of very large, thin-walled veins that occupy the interrenicular spaces. Arterial and venous plexuses outside the substance of the sporta reported in other cetaceans were not observed in the bowhead.     

Gross anatomy of the respiratory system of the bowhead whale, Balaena mysticetus

Components of the respiratory system from seven bowhead whales have been examined. The paired and laterally curved external nares are passively closed by a valve-like mass located in the rostral, lateral, and ventral walls of the nasal vestibules. Nasal septal cartilages are paired smooth plates rostrally changing to accordion-like folds caudally. The epiglottic and arytenoidal protuberances of the larynx are typically cetacean, but blunt. The cricoid cartilage is not a complete ring, but an elongated, inverted, trough-shaped structure. The thyroid cartilage is trough-shaped with elongated cranial cornua curving dorsocaudally from each thyroid lamina. A conical mass of skeletal muscle serves as the floor of the short trachea and also surrounds the termination of the laryngeal sac. The trachea is dorsoventrally compressed, lacks a tracheal bronchus, and its width equals its length. The principal bronchi give rise to lobar bronchi at obtuse angles. Large segmental bronchi branch extensively from lobar bronchi near the mediastinal lung surface. The lungs are rectangular and of nearly uniform thickness throughout, without external or internal lobulation.     

Microanatomy of the renicule of Balaena mysticetus

Renicules from twelve bowhead whales (Balaena mysticetus) were examined utilizing light, scanning electron, and transmission electron microscopes. The basic organization of the renicule into capsule, cortex, sporta perimedullaris, medulla, and calyx is described. Despite less than perfect preservation resulting from environmental and logistical conditions at the collecting sites, it has been possible to document the basic microstructure of most components of the renicule of this endangered species. Several unusual features were observed. The absence of smooth muscle fibers (other than in vessel walls) from the capsule, sporta perimedullaris, and calyx wall is a departure from what is reported in other cetaceans as is the consistent presence of arcuate arteries in the substance of the sporta perimedullaris. Large subcapsular veins are present but do not appear to represent connecting elements in an alternative venous return through capsular and interrenicular veins. Elastic fibers are seen only in the sporta perimedullaris and the calyx wall, whereas reticular fibers are most abundant in the medullary stroma. Finally, enlarged cells with clear cytoplasm are seen in the tunica media of the glomerular afferent arterioles extending a variable, but always considerable, distance toward the interlobular arteriole. These cells are presumed to represent an extended array of the epithelioid cells common in the afferent arterioles of the juxtaglomerular apparatus of other mammalian kidneys.     

Epidermal and papillary dermal characteristics of the bowhead whale (Balaena mysticetus)

Skin samples from most body regions of the bowhead whale were examined. The epidermis is 2.7 to 50 times thicker than that reported in other cetaceans with both regional and individual variations in thickness. The thinnest areas examined (1 mm) occur on the eyelid margins and the thickest (25 mm) occur on the lower jaw. A distinctive parakeratotic stratum corneum with a thick underlying stratum spinosum (without a stratum granulosum) extends over the entire body surface. From a few dozen to several hundred epidermal lesions are present on all whales studied. A typical stratum basale of germinative keratinocytes (with melanocytes in pigmented areas) rests upon a well-defined basal lamina. Epidermal rod arrays arise from the basal keratinocytes which cover highly elongated dermal papillae and extend to the epidermal surface through the distal stratum spinosum and the stratum corneum. At least four diatom genera occur on and in the stratum corneum and lesion areas of different whales. The superficial dermis consists of a papillary layer with long (up to 13 mm) dermal papillae interdigitating with the epidermis from a basal area that is 2-4 mm in thickness. The number of dermal papillae per mm2 varies inversely with the thickness of the epidermis. Large diameter, sensory papillae packed with tortuous, highly elongated, encapsulated nerve end organs also interdigitate with the thin epidermal areas of the ventral surface of the rostrum, the upper and lower lip margins, and the upper and lower eyelid margins. Scattered, single, stiff hairs emerge from the skin only in specific, pigmented regions of the head.     

Observations on the anatomy of the stomach and duodenum of the bowhead whale,Balaena mysticetus

Gastric and cranial duodenal structure of the bowhead whale (Balaena mysticetus) was examined grossly and microscopically. The stomach was arranged in a series of four compartments. The first chamber, or forestomach, was a large nonglandular sac. lined by a keratinized stratified squamous epithelium. It was followed by the fundic chamber, a large, somewhat globular and entirely glandular compartment. At the entrance of the fundic chamber, a narrow cardiac gland region could be defined. The remaining onucosa of the chamber contained the proper gastric glands. A narrow, tubular connecting channel, the third distinct gastric division, was lined by mucous glands and joined the fundic chamber with the final stomach compartment, or pyloric chamber. This fourth chamber was also tubular and lined by mucous glands but was of a diameter considerably larger than the connecting channel. The stomach terminated at the pyloric sphincter which consisted of a v/ell-developed band of circular smooth-muscle bundles effecting a division between the pyloric chamber and small intestine. The small intestine began with the duodenal ampulla, a dilated sac considerably smaller than the fundic chamber of the stomach. The rnucosa of this sac contained mucous glands throughout. The ampulla led without a separating sphincter into the duodenum proper which continued the intestine in a much more narrow tubular fashion. The mucosal lining of the duodenum was composed of villi and intestinal crypts. Although their occurrence varied among whales, enteroendocrine cells were identified within the mucous glands of the cardiac region, connecting channel, pyloric chamber, and cranial duodenum. The hepatopancreatic duct entered the wall of the duodenum shortly after the termination of the duodenal ampulla and continued intramurally along the intestine before finally joining the duodenal lumen.     

Olfactory epithelium and ontogeny of the nasal chambers in the bowhead whale (Balaena mysticetus)

In a species of baleen whale, we identify olfactory epithelium that suggests a functional sense of smell and document the ontogeny of the surrounding olfactory anatomy. Whales must surface to breathe, thereby providing an opportunity to detect airborne odorants. Although many toothed whales (odontocetes) lack olfactory anatomy, baleen whales (mysticetes) have retained theirs. Here, we investigate fetal and postnatal specimens of bowhead whales (Balaena mysticetus). Computed tomography (CT) reveals the presence of nasal passages and nasal chambers with simple ethmoturbinates through ontogeny. Additionally, we describe the dorsal nasal meatuses and olfactory bulb chambers. The cribriform plate has foramina that communicate with the nasal chambers. We show this anatomy within the context of the whole prenatal and postnatal skull. We document the tunnel for the ethmoidal nerve (ethmoid foramen) and the rostrolateral recess of the nasal chamber, which appears postnatally. Bilateral symmetry was apparent in the postnatal nasal chambers. No such symmetry was found prenatally, possibly due to tissue deformation. No nasal air sacs were found in fetal development. Olfactory epithelium, identified histologically, covers at least part of the ethmoturbinates. We identify olfactory epithelium using six explicit criteria of mammalian olfactory epithelium. Immunohistochemistry revealed the presence of olfactory marker protein (OMP), which is only found in mature olfactory sensory neurons. Although it seems that these neurons are scarce in bowhead whales compared to typical terrestrial mammals, our results suggest that bowhead whales have a functional sense of smell, which they may use to find prey.     

The role of desmosomes in the ear plug formation in the bowhead whale (Balaena mysticetus)

The external acoustic meatus (EAM) of most baleen whales accumulates cellular debris annually in the lumen as whales age, forming a lamellated ear plug. The bowhead whale ear plug is formed from annually molting lining of the EAM as the entire epithelium releases at the level of the stratum basale during the spring migration. Epithelial regeneration is mostly completed by the fall migration, remaining intact for 6–7 months before being torn off the following spring. Desmosomes are integral to cell–cell adhesion with connecting desmosomal cadherins desmoglein (dsg) and desmocollin (dsc). Paraffin sections of the oral cavity and EAM lining of spring and fall adult bowhead whales, as well as the EAM of spring-caught juvenile, were immunohistochemically examined for the presence of these cadherins. In all fall specimens, both cadherins occurred in all layers except the superficial keratinous layer of the oral cavity. In spring, three different conditions existed: (a) oral cavity of spring-caught adults had reduced cadherins, with superficial fissuring in its keratinized layer and vacuolation in the upper stratum spinosum; (b) EAM of juvenile spring-caught whales displayed fissuring with accompanying reduction of both cadherins in its superficial lining; and (c) EAM lining of spring-caught adults displayed deep fissures, reduced cadherins, and absence of dsc1 in the fissuring zone. These results suggest that shedding of skin layers in mammals, whether normal molting, pathological, or the result of injury and wound repair all revolve around desmosome function. The specific role, structure, and location of these two cadherins need to be further addressed.     

The anatomy of the larynx of the bowhead whale,Balaena mysticetus,and its sound‐producing functions

This study describes the morphology of the laryngeal apparatus in bowhead whales (Balaena mysticetus) with respect to respiration, deglutition, and vocalization. We also examined the intrinsic cricoarytenothyroid muscle (Musculus (M.) diverticuli laryngei) which forms the laryngeal diverticulum, to ascertain its interactions with the laryngeal cartilages during respiration and sound production. Five fetal larynges and four from adult whales were studied using noninvasive imaging, as well as macroscopic and microscopic techniques. The larynx extends from the skull base into the thoracic inlet. The dorsally curved laryngeal stalk, supported by epiglottis and the corniculate processes of arytenoid cartilages, is situated within the nasopharynx. The epiglottic cartilage exhibits a prominent medial ridge. The arytenoid cartilages are rod‐shaped, and extend through the laryngeal cavity. The thyroid cartilage possesses a prominent caudal horn with a fibrous articulation to the ventrally incomplete cricoid cartilage. The M. thyroepiglotticus forms the connection between epiglottic and thyroid cartilages. The M. cricothyroideus lateralis connects the caudal horn of the thyroid cartilage with the cricoid cartilage and the M. cricothyroideus medialis connects the cricoid and thyroid cartilage. An extensive laryngeal diverticulum (Diverticulum laryngis), formed by the laryngeal mucosa and M. diverticuli laryngei, is positioned caudo‐ventral to the laryngeal vestibule. The mucosa thickens into a fold medial to the vocal processes of the arytenoid cartilages. Experiments with airflow combined with histological and anatomical evidence strongly suggest a sound producing function for these (vocal) folds. This analysis provides the first account of sound producing structures and function in bowhead whales. Anat Rec, 297:1316–1330, 2014. © 2014 Wiley Periodicals, Inc.     

Structure of the external auditory meatus of the Bowhead whale (Balaena mysticetus) and its relation to their seasonal migration

The external auditory meatus (EAM) in many species of mysticete whales is filled with a waxy ear plug. Though this lamellated structure is often used to age a whale, its formation and development remain undescribed. It is thought that growth layer groups (GLGs) are laid down annually, thereby increasing the size of this structure. Since some mysticete whales are migratory and many undergo molting, we hypothesized that the cyclical production of these GLGs may be related to these processes. The epithelia of both EAM and glove finger (a part of the tympanic membrane protruding into the EAM) of one juvenile and multiple adult bowhead whales from both fall (October: non‐molting) and spring (May: molting) seasons were dissected and examined anatomically and histologically. These tissue samples were compared with the adult oral epithelia at the same time periods. These epithelia shared a similar basic broad structure, though there were differences in thickness and presence of intraepithelial structures. All epithelia in the October specimens were rich in both glycogen and lipid. The parakeratinized epithelium of the oral cavity in the juvenile and some May specimens shed via the production of several superficial epithelial fissures. Other adult May specimens exhibited deep epithelial fissures, reminiscent of pressure ulcers, which would cause the detachment of the entire epithelium from the dermis. We propose that sloughed epithelial lining is the source of the GLGs in the ear plug. Correlating a potential molting sequence with these observations explained the presence of epidermal glycogen, deep epidermal fissures and dermal glycolipid, and to some extent calls into question the origin and structure of the ear plug itself. Further morphological characterization of ear plugs in bowheads is needed to better understand cell origin and ear plug formation.     

Morphometric Correlates of the Ovary and Ovulatory Corpora in the Bowhead Whale,Balaena mysticetus

Gross morphology and morphometry of the bowhead whale ovary, including ovulatory corpora, were investigated in 50 whales from the Chukchi and Beaufort seas off the coast of Alaska. Using the presence of ovarian corpora to define sexual maturity, 23 sexually immature whales (7.6–14.2 m total body length) and 27 sexually mature whales (14.2–17.7 m total body length) were identified. Ovary pair weights ranged from 0.38 to 2.45 kg and 2.92 to 12.02 kg for sexually immature and sexually mature whales, respectively. In sexually mature whales, corpora lutea (CLs) and/or large corpora albicantia (CAs) projected beyond ovary surfaces. CAs became increasingly less interruptive of the surface contour as they regressed, while remaining identifiable within transverse sections of the ovarian cortex. CLs formed large globular bodies, often with a central lumen, featuring golden parenchymas enfolded within radiating fibrous cords. CAs, sometimes vesicular, featured a dense fibrous core with outward fibrous projections through the former luteal tissue. CLs (never more than one per ovary pair) ranged from 6.7 to 15.0 cm in diameter in 13 whales. Fetuses were confirmed in nine of the 13 whales, with the associated CLs ranging from 8.3 to 15.0 cm in diameter. CLs from four whales where a fetus was not detected ranged from 6.7 to 10.6 cm in diameter. CA totals ranged from 0 to 22 for any single ovary, and from 1 to 41 for an ovary pair. CAs measured from 0.3 to 6.3 cm in diameter, and smaller corpora were more numerous, suggesting an accumulating record of ovulation. Neither the left nor the right ovary dominated in the production of corpora. Anat Rec, 299:769–797, 2016. © 2016 Wiley Periodicals, Inc.     

Sensory Hairs in the Bowhead Whale,Balaena mysticetus (Cetacea,Mammalia)

We studied the histology and morphometrics of the hairs of bowhead whales (Balaena mysticetus). These whales are hairless except for two patches of more than 300 hairs on the rostral tip of the lower lip and chin, the rostral tip of the upper lip, and a bilateral row of approximately ten hairs caudal to the blowhole. Histological data indicate that hairs in all three of these areas are vibrissae: they show an outermost connective tissue capsule, a circumferential blood sinus system surrounding the hair shaft, and dense innervation to the follicle. Morphometric data were collected on hair diameters, epidermal recess diameters, hair follicle length, and external hair lengths. The main difference between the hairs in the different regions is that blowhole hairs have larger diameters than the hairs in the chin and rostrum regions. We speculate that the hair shaft thickness patterns in bowheads reflect functional specializations. Anat Rec, 298:1327–1335, 2015. © 2015 Wiley Periodicals, Inc.     

Seasonal and Ontogenetic Variation in Subcutaneous Adipose Of the Bowhead Whale (Balaena mysticetus)

Cetacean evolution was shaped by an extraordinary land‐to‐sea transition in which the ancestors of whales became fully aquatic. As part of this transition, these mammals evolved unusually thick blubber which acts as a metabolic reservoir as well as an insulator and provides buoyancy and streamlining. This study describes blubber stratification and correlates it to seasonal variation, feeding patterns, and ontogeny in an arctic‐adapted mysticete, the bowhead whale (Balaena mysticetus). Bowheads are unique among mammals for possessing the largest known blubber stores. We found that adipocyte numbers in bowheads, like other mammals, do not vary with season or feeding pattern but that adipocyte size and structural fiber densities do vary with blubber depth. Anat Rec, 298:1416–1423, 2015. © 2015 Wiley Periodicals, Inc.     

An Intraoral Thermoregulatory Organ in the Bowhead Whale (Balaena mysticetus), the Corpus Cavernosum Maxillaris

The novel observation of a palatal retial organ in the bowhead whale (Balaena mysticetus) is reported, with characterization of its form and function. This bulbous ridge of highly vascularized tissue, here designated the corpus cavernosum maxillaris, runs along the center of the hard palate, expanding cranially to form two large lobes that terminate under the tip of the rostral palate, with another enlarged node at the caudal terminus. Gross anatomical and microscopic observation of tissue sections discloses a web‐like internal mass with a large blood volume. Histological examination reveals large numbers of blood vessels and vascular as well as extravascular spaces resembling a blood‐filled, erectile sponge. These spaces, as well as accompanying blood vessels, extend to the base of the epithelium. We contend that this organ provides a thermoregulatory adaptation by which bowhead whales (1) control heat loss by transferring internal, metabolically generated body heat to cold seawater and (2) protect the brain from hyperthermia. We postulate that this organ may play additional roles in baleen growth and in detecting prey, and that its ability to dissipate heat might maintain proper operating temperature for palatal mechanoreceptors or chemoreceptors to detect the presence and density of intraoral prey. Anat Rec, 296:701–708, 2013. © 2013 Wiley Periodicals, Inc.     

Evolutionary aspects of the development of teeth and baleen in the bowhead whale

In utero, baleen whales initiate the development of several dozens of teeth in upper and lower jaws. These tooth germs reach the bell stage and are sometimes mineralized, but toward the end of prenatal life they are resorbed and no trace remains after birth. Around the time that the germs disappear, the keratinous baleen plates start to form in the upper jaw, and these form the food‐collecting mechanism. Baleen whale ancestors had two generations of teeth and never developed baleen, and the prenatal teeth of modern fetuses are usually interpreted as an evolutionary leftover. We investigated the development of teeth and baleen in bowhead whale fetuses using histological and immunohistochemical evidence. We found that upper and lower dentition initially follow similar developmental pathways. As development proceeds, upper and lower tooth germs diverge developmentally. Lower tooth germs differ along the length of the jaw, reminiscent of a heterodont dentition of cetacean ancestors, and lingual processes of the dental lamina represent initiation of tooth bud formation of replacement teeth. Upper tooth germs remain homodont and there is no evidence of a secondary dentition. After these germs disappear, the oral epithelium thickens to form the baleen plates, and the protein FGF‐4 displays a signaling pattern reminiscent of baleen plates. In laboratory mammals, FGF‐4 is not involved in the formation of hair or palatal rugae, but it is involved in tooth development. This leads us to propose that the signaling cascade that forms teeth in most mammals has been exapted to be involved in baleen plate ontogeny in mysticetes.     

A Comparison of the Cortical Structure of the Bowhead Whale (Balaena mysticetus), a Basal Mysticete,with Other Cetaceans

Few studies exist of the bowhead whale brain and virtually nothing is known about its cortical cytoarchitecture or how it compares to other cetaceans. Bowhead whales are one of the least encephalized cetaceans and occupy a basal phylogenetic position among mysticetes. Therefore, the bowhead whale is an important specimen for understanding the evolutionary specializations of cetacean brains. Here, we present an overview of the structure and cytoarchitecture of the bowhead whale cerebral cortex gleaned from Nissl-stained sections and magnetic resonance imaging (MRI) in comparison with other mysticetes and odontocetes. In general, the cytoarchitecture of cetacean cortex is consistent in displaying a thin cortex, a thick, prominent layer I, and absence of a granular layer IV. Cell density, composition, and width of layers III, V, and VI vary among cortical regions, and cetacean cortex is cell-sparse relative to that of terrestrial mammals. Notably, all regions of the bowhead cortex possess high numbers of von Economo neurons and fork neurons, with the highest numbers observed at the apex of gyri. The bowhead whale is also distinctive in having a significantly reduced hippocampus that occupies a space below the corpus callosum within the lateral ventricle. Consistent with other balaenids, bowhead whales possess what appears to be a blunted temporal lobe, which is in contrast to the expansive temporal lobes that characterize most odontocetes. The present report demonstrates that many morphological and cytoarchitectural characteristics are conserved among cetaceans, while other features, such as a reduced temporal lobe, may characterize balaenids among mysticetes. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:745–760, 2019. © 2018 Wiley Periodicals, Inc.     

Microanatomy of the liver immune system

The critical metabolic functions of the liver often eclipse any perception of its role as an immune organ. However, the liver as a mediator of systemic and local innate immunity and an important site of immune regulation is now an accepted concept. Complex repertoires of lymphoid and non-lymphoid cells are key to hepatic defense and immunoregulation. Hepatic cells of myeloid lineage include Kupffer cells and dendritic cells. Intrahepatic lymphocytes are distinct both in phenotype and function from their counterparts in any other organ and include both conventional (CD4+ and CD8+ αβ T cell receptor (TCR)+ T cells, B cells, natural killer (NK) cells) and nonconventional lymphoid cells (natural killer T (NKT) cells, γδTCR+ T cells, CD4? CD8? T cells). Many hepatic T cells express the TCR at an intermediate level and the great majority of them either coexpress NK cell markers (NKT cells) or they are apoptosing peripheral T cells. The percentage of activated (CD69+) and memory (CD45RBlow+) lymphocytes is much higher while naïve (CD62Lhigh) and resting T cells as well as B lymphocytes are underrepresented in the liver. The discovery of major populations of lymphoid cells in the liver that differ phenotypically, functionally and even perhaps developmentally from populations in other regions has been key to the evolving perception of the liver as a regulatory lymphoid organ. This chapter will focus on these populations and how they contribute to immune surveillance against malignant, infectious and autoimmune disease of the liver.     

骨性颈静脉孔区的应用解剖

目的: 观察骨性颈静脉孔区的显微解剖,为临床提供解剖学资料.方法: 显微镜下观察20例成人颅骨标本颈静脉孔的位置、组成、形态,并测量其大小及与周围骨性结构的距离.结果: 颈静脉孔是由枕骨和颞骨岩部合围的一个骨性管道,85%的外口、75%的内口右侧大于左侧;颈静脉孔内有颞突、枕突、锥形窝、颈静脉窝等结构;内口的前方与岩下窦沟相连,后接乙状窦沟,内口的上方有内耳门和前庭小管外口;颈静脉孔的外侧有茎乳孔和茎突,茎乳孔外接鼓乳裂,后方有枕骨颈突.结论: 多数颈静脉孔右侧大于左侧,乙状窦沟前移以右侧多见;鼓乳裂可以定位茎乳孔及颈静脉孔外侧壁;枕骨颈突是确定颈静脉孔后壁的标志.