The Rete tibiotarsale and Arteriovenous Association in the Hind Limb of Birds: A Compartive Morphological Study on Counter-current Heat Exchange Systems

Arterio-venous association was investigated in the tibial region of 66 bird species representing 21 orders. An intermingled network of arteries and veins (rete tibiotarsale) was found in all stages of complication, ranging from the most simple with only 3 arteries and 5–7 veins (tinamou and owl) to the most elaborate types with more than 60 arteries and 40 veins (flamingo). As opposed to what has hitherto been believed, elaborate retia are present in many short-legged species, while most of the long-legged wading birds only have retia of a very simple type. Arctic forms of eider ducks were found to possess elaborate retia comparable to those in other ducks. In species lacking the rete tibiotarsale, the single artery and its counter-current veins are forming a venae comitantes system. The number of counter-current veins increases with foot size and in ravens and crows up to 8 veins were surrounding the artery, resembling the pattern described in the fins of whales. In species of gulls and guillemots, the contact surface between the veins and the artery appeared to be higher in arctic forms than in more southerly distributed birds. The findings are discussed in relation to heat economy, foot size, and ecology of the species. Further, theories for the evolution of the different types of heat exchange systems are presented. It is concluded that no single selective factor can explain the evolution and occurrence of the rete tibiotarsale.     

Microanatomy of retia mirabilia of bowhead whale foramen magnum and mandibular foramen

The morphology of vessels of the cervical rete mirabile near the region of the foramen magnum of the bowhead whale, Balaena mysticetus, as well as of retial vessels of the mandibular foramen was studied by light and transmission electron microscopy. A comparison of arterial and venous components of the mandibular rete revealed considerable arterial branching and arteriovenous anastomoses. Although the small arteries of bowhead retia contained the same layers found in nonretial arteries, several distinctive morphologic features were evident. These included wide separation by collagenous connective tissue and small size of individual smooth muscle cells of the tunica media. These myocytes also contained considerable perinuclear glycogen and communicated minimally with adjacent myocytes by small foot-like cytoplasmic appendages as well as branching of basement membranes. Ganglia-like neural plexuses were observed within the tunica media of arterial retia. Endothelial cells lining the intima demonstrated loose peripheral edges which frequently projected into the vessel lumen, and these cells rested upon a subjacent layer of reticular fibers. It is known for some species that the retial supply to the brain in whales largely supplants an internal carotid arterial supply and that the spinal cord is supplied by retia. The physiologic role of the bowhead mandibular retia remains unknown. The retia mirabilia of cetaceans are considered as one of the morphologic adaptations which modulate hemodynamics during diving and resurfacing. The morphologic features of these vessels in the bowhead whale, as revealed by electron microscopy, appear to reflect the capability to respond in a slow but sustained manner to diving, and the large glycogen deposits may help sustain vascular myocyte metabolism during prolonged submersion.     

The cardiac ventricles of a baleen whale (Balaenoptera acutorostrata: Minke whale) and a toothed whale (Hyperoodon ampullatus: Bottlenose whale)

Fifteen minke whale (Balaenoptera acutorostrata: Mysticeti) and three bottlenose whale (Hyperoodon ampullatus: Odontoceti) hearts were obtained from Norway. Only the ventricular mass and the base of the great arteries were available for study. The shape of the heart, the double apex, the narrowness of the interventricular septum in the dorsiventral plane, the side-to-side position of the ventricles, the relative thickness of the wall of the right ventricle, and the heavy trabeculation agree with other, brief reports of whale heart morphology. Coronary artery tortuosity, which has been described in sperm whales by others, was found in the bottlenose but not in the minke whales. It is suggested that the shape of the heart is associated with depth and duration of dives and that the pattern of trabeculation may be related to the size of the animal.     

<Emphasis Type="Italic">Hoxa3</Emphasis> regulates the proliferation and differentiation of the third pharyngeal arch mesenchyme in mice

Genetic disruption of Hoxa3 results in bilateral defects of the common carotid artery, which is derived from the third branchial arch artery. The tunica media of the great arteries derived from the arch arteries is formed by the ectomesenchymal neural crest cells. To examine the etiology of the regression of the third arch artery, we generated Hoxa3 homozygous null mutant embryos that expressed a lacZ marker transgene driven by a connexin43 (Cx43): promoter in the neural crest cells. The expression of -galactosidase in these mouse embryos was examined by both whole-mount X-gal staining and immunohistochemistry with the monoclonal -galactosidase antibody on sections. The migration of neural crest cells from the neural tube to the third branchial arch was not affected in the Hoxa3 homozygotes. The initial formation of the third arch artery was also not disturbed. The artery, however, regressed at embryonic day 11.5 (E11.5), when differentiation of the third pharyngeal arch began. The internal and external carotid arteries arose from the dorsal aorta in E12.5 null mutants, which showed an abnormal persistence of the ductus caroticus. The third pharyngeal arch of wild-type mice fuses with the fourth and second arches at E12.0. In the Hoxa3 null mutants, however, the fusion was delayed, and the hypoplastic third pharyngeal arch was still discerned at E12.5. Moreover, the number of proliferating cells in the third arch of the null mutants was small compared with that in the wild-type. Thus, Hoxa3 is required for the growth and differentiation of the third pharyngeal arch. The defective development of the third pharyngeal arch may induce the anomalies of the carotid artery system. This work was supported in part by a grant (no. 14570026) from the Ministry of Education of Japan to Y.K.     

Vascular corrosion replicas of chemo-baroreceptors in fish: The carotid labyrinth in Ictaluridae and Clariidae

Summary Scanning electron microscopy of vascular corrosion replicas and light microscopy revealed a pair of highly vascularized tissues, the carotid labyrinths, in the dorsal head region of the channel catfish, Ictalurus punctatus, the black bullhead, I. melas, and the walking catfish, Clarias batrachus. The labyrinth consists of a myriad of arterioles that arise from the common carotid artery immediately distal to the origin of the common carotid from the efferent branchial (epibranchial) artery of the first gill arch. The arterioles anastomose with each other to form: (1) the internal carotid artery which supplies the brain, and (2) several anteriolateral arteries that extend into the anterior head. In the ictalurids the common carotid artery emerges from the labyrinth intact and continues anteriorly as the large olfactory artery, whereas in Clarias all postlabyrinthine vessels result from arborization of the common carotid and subsequent anastomosis of the arterioles. Similarities between piscine and amphibian carotid labyrinths and the anatomical proximity of the former with the gills suggest that, in Ictaluridae, the labyrinth has a chemoor baroreceptor function.Supported by NSF Grant No. PCM 79-23073The authors wish to thank K. Drajus, D. Kullman, E. Boland and Dr. J. O'Malley for their most capable help. The authors also express their gratitude to P. Shafland and the Florida Game and Fresh Water Fish Commission for providing Clarias     

Homeobox gene hoxa3 is essential for the formation of the carotid body in the mouse embryos

Homeobox gene Hoxa3 is strongly expressed in the third pharyngeal arch and pouch. We found that Hoxa3 homozygous null mutant mice had the lack of the carotid body. In all late-term mutant embryos examined (n = 10), no carotid body was present. The carotid body rudiment is formed in the wall of the third branchial artery, which develops into the common carotid artery and the first part of the internal carotid artery. The symmetrical patterns of the third, fourth, and sixth arch arteries were observed in wild-type littermates at embryonic day (E) 10.5-12.5. In Hoxa3 homozygous mutant embryos, however, the third arch artery began to degenerate at E10.5 and almost disappeared at E11.5. Furthermore, the bifurcation of the common carotid artery at the normal position, i.e., at the upper end of the larynx, was never detected in the mutant embryos at E16.5-E18.5. The common carotid artery of the homozygous mutants was separated into the internal and external carotid arteries immediately after its origin. Thus, the present study evidenced that the absence of the carotid body in Hoxa3 homozygous mutants is due to the defect of development of the third arch artery, resulting in malformation of the carotid artery system. During fetal development, the carotid body of mice is in close association with the superior cervical ganglion of the sympathetic trunk. The superior cervical ganglion rather showed hypertrophic features in Hoxa3 homozygous mutants lacking the carotid body.     

<Emphasis Type="Italic">Hoxa3</Emphasis> and signaling molecules involved in aortic arch patterning and remodeling

Anomalies of the aortic arch have long been of anatomicoclinical interest. Recent studies on gene-targeted mice have identified the candidate genes that are involved in the patterning and remodeling of the pharyngeal arch arteries. In this review, we discuss our present knowledge with regard to the signaling molecules that regulate specific aspects of arch artery development. We focus first on Hoxa3, because it plays a critical role in the regulation of the differentiation of the third pharyngeal arch. Hoxa3 is expressed by the neural crest cells that originate from the rhombomeres, viz., (r)5, r6, and r7, and populate the third pharyngeal arch; it is also expressed in the third pharyngeal pouch. In Hoxa3 homozygous null mutant mice, the third arch artery degenerates bilaterally at embryonic day 11.5, resulting in the malformation of the carotid artery system. Complex combinatorial signals among the neural crest cells, pharyngeal mesoderm, ectoderm, and pouch endoderm are required for the proper development of the arch arterial system. Therefore, we highlight the numerous signaling pathways and individual genes expressed by the ectomesenchymal neural crest cells and also by the other epithelial and mesodermal cells of the pharynx. Defects in these genes result in malformations of the arch artery derivatives. This review should deepen our understanding of congenital human syndromes with abnormal patterns of pharyngeal arch arteries.     

The homologies of the lorisoid internal carotid artery system

The development of the “internal carotid” arterial system of the lesser galago (Galago senegalensis senegalensis)is described. The first artery to be formed is a typical promontory artery which runs through the middle-ear cavity and gives off the stapedial artery. It terminates in the cranial cavity by dividing into the middle cerebral, anterior cerebral, and two ophthalmic arteries. It is accompanied by the internal carotid nerve. A medially directed artery to the external carotid rete arises from the commencement of the promontory artery and joins the caudal end of the rete, whose cranial end lies in the foramen lacerum. As the promontory artery enters the cranial cavity, it communicates with the cranial end of the rete. The promontory artery, between the origin of the artery to the rete and its connection with the rete, becomes narrowed and eventually disappears. Thus the internal carotid artery is formed from the commencement of the promontory artery, the artery to the rete, the external carotid rete, and the terminal intracranial part of the promontory artery. The relationships of the artery to the rete indicate that it is the homologue of the human ascending pharyngeal artery.     

Dense granule-containing cells in arterial chemoreceptor areas of the tortoise (Testudo hermanni)

Light- and electron-microscopic observations of the chemosensory areas of the arteries of the tortoise (Testudo hermanni) reveal that clusters of nonmuscular cells are found in the adventitial layer of restricted regions of the carotid artery, aortic arch, and pulmonary artery. In these clusters, three types of cells are complexly interwoven: the G-cell closely resembles the glomus cell, which has been found in the arterial chemoreceptor area of several animal species; the LG-cell has very large electron-dense granules; the third type is a G- and LG-cell supporting cell. Membrane specializations are often observed at apposing membranes between G-cells. Two kinds of nerve endings synapse with G-cells, one with numerous clear synaptic vesicles, the other without vesicles. Some G-cells are in membrane-to-membrane contact with smooth-muscle cells (g-s connection), and here a membrane thickening is visible. Nerve terminals with numerous synaptic vesicles synapse with the LG-cells. The G-cell in the carotid artery, the aorta, and the pulmonary artery is a chemoreceptor element ultrastructurally the same as the glomus cell in the arterial chemoreceptor area of various vertebrate species.     

An immunohistochemical study on the innervation of SP-IR nerves in the cerebral arteries of the bent-winged bat

Summary The overall distribution of substance P (SP) immunoreactive (IR) nerves surrounding the cerebral arteries of the bent-winged bat were investigated immunohistochemically. In this microchiropteran species, the walls from the vertebral artery to the caudal part of the basilar artery have considerably well-developed plexuses of SP-IR nerves, whereas no demonstrable SP-IR fibers were found in the crostral part of the basilar artery, and in more rostrally located arteries the nerve supply was very sparse or occasionally lacking. This innervation pattern has not yet been established for the cerebral arterial systems of other mammals that have been studied under normal conditions, but it is very similar to the pattern of SP-IR innervation observed in the guinea pig and cat of which the trigeminal ganglia have been destroyed. From the combination of this and other immunohistochemical findings, it is suggested that SP-IR nerves innervating the vertebral and basilar arteries of the bent-winged bat originate from the upper cervical dorsal root ganglia (DRG) and enter the cranial cavity along the vertebral artery and through the meninges.Abbreviations BA basilar artery - CSN cervical spinal nerves - ICS internal carotid system - SCG superior cervical ganglion - SNB sympathetic nerve bundle - VA vertebral artery - VBS vertebro-basilar system     

Disruption of the Hoxa3 homeobox gene results in anomalies of the carotid artery system and the arterial baroreceptors

Homeobox gene Hoxa3 is expressed in the third pharyngeal arch and pouch and is required for development of the third arch artery in addition to the thymus, parathyroid gland and carotid body. We therefore statistically analyzed malformations of the carotid artery system in Hoxa3 homozygous mutant mice, in comparison with wild-type and heterozygous littermates. To identify the carotid artery system, red carbon ink was injected, or vascular casts were made by injection of Mercox resin and observed by scanning electron microscopy. Furthermore, innervation of the carotid sinus and baroreceptor regions in the aortic arch and right subclavian artery were studied in the Hoxa3 null mutants having an abnormal carotid artery system by immunohistochemistry with TuJ1 and protein gene product (PGP) 9.5 antibodies, which recognize nerve fibers and neurons. The common carotid artery of Hoxa3 homozygous mutants was absent or very short and therefore the internal and external carotid artery arose from a more proximal level than those of wild types. The baroreceptor innervation, however, persisted in the mutants, although vascular targets were changed. These results indicate that Hoxa3 gene is crucial for the formation of the common carotid artery and the null mutant mice are the first useful animal models to show that the third arch arteries on both sides specifically degenerate but the fourth and sixth arch arteries are normal.     

The structure of the carotid bifurcation in the lizards Tiliqua occipitalis and Trachysaurus rugosus

The origin of the internal carotid artery in the lizards Tiliqua occipitalis and Trachysaurus rugosus has been shown to be both extremely variable and complex. In the dense connective tissue investing the junction of the internal carotid artery and the summit of the carotid arch are groups of cells associated with sinusoids derved from arterioles arising from the neighboring great vessels. The conspicuous epithelioid cells in these groups resemble the mammalian carotid body glomus and amphibian α cells. Nerve fibers showing no obvious synaptic specializations pass to and over these cell groups. It is suggested that these cell groups and sinusoids are comparable to mammalian carotid body glomeruli. A similar group of cells has been described in the concavity of the summit of the fourth aortic arch. This cell group, however, gives a distinct chromaffin reaction.     

Cytoplasmic and Mitochondrial Creatine Kinases from the Skeletal Muscle of Sperm Whale (Physeter macrocephalus). Molecular Cloning and Enzyme Characterization

We have amplified two cDNAs, coding for creatine kinases (CKs), from the skeletal muscle of sperm whale Physeter macrocephalus by PCR, and cloned these cDNAs into pMAL plasmid. These are the first CK cDNA and deduced amino acid sequences from cetaceans to be reported. One of the two amino acid sequences is a cytoplasmic, muscle-type isoform (MCK), while the other was identified as a sarcomeric, mitochondrial isoform (sMiCK) that included a mitochondrial targeting peptide. The amino acid sequences of sperm whale MCK and sMiCK showed 94–96% sequence identity with corresponding isoforms of mammalian CKs, and all of the key residues necessary for CK function were conserved. The phylogenetic analyses of vertebrate CKs with three independent methods (neighbor-joining, maximum-likelihood and Bayes) supported the clustering of sperm whale MCK with Bos and Sus MCKs, in agreement with the contemporary view that these groups are closely related. Sperm whale MCK and sMiCK were expressed in Escherichia coli as a fusion protein with maltose-binding protein, and the kinetic constants (K _m, K _d and k _cat) were determined for the forward reaction. Comparison of kinetic constants with those of human and mouse CKs indicated that sperm whale MCK has a comparable affinity for creatine (K _m^Cr = 9.38 mM) to that of human MCK, and the sMiCK has two times higher affinity for creatine than the human enzyme. Both the MCK and sMiCK of sperm whale display a synergistic substrate binding (K _d /K _m = 3.1–7.8) like those of other mammalian CKs.     

Anion- and pH-linked effects on the heme-iron geometry in ferrous nitrosylated monomeric myoglobins

 The cooperative effect of anions and proton concentration on the EPR spectroscopic properties of the ferrous nitrosylated derivative of monomeric Mb from loggerhead sea turtle (Caretta caretta), sperm whale (Physeter catodon), and horse (Caballus caballus) has been investigated between pH 4.5 and 9.0, at 100 K. In the absence of anions, an EPR spectrum characteristic of the hexa-coordinated species of ferrous nitrosylated Mb with an axial geometry is observed, which is unaffected by pH. On the other hand, a transition toward a species characterized by an EPR spectrum corresponding to a hexa-coordinated rhombic geometry takes place in the presence of phosphate, acetate, citrate, sulfate, and chloride. Only the hexa-coordinated form characterized by the rhombic EPR spectrum appears then to undergo a pH-dependent transition toward the penta-coordinated species. Present results show clear-cut evidence for the spectroscopic coupling of proton and anion binding sites with the Mb reactive center, indicating that an allosteric mechanism might modulate the proximal HisF8-heme-NO geometry in monomeric hemoproteins. Received: 15 December 1997 / Accepted: 15 June 1998     

Endothelin regulates neural crest deployment and fate to form great vessels through Dlx5/Dlx6-independent mechanisms

Endothelin-1 (Edn1), originally identified as a vasoconstrictor peptide, is involved in the development of cranial/cardiac neural crest-derived tissues and organs. In craniofacial development, Edn1 binds to Endothelin type-A receptor (Ednra) to induce homeobox genes Dlx5/Dlx6 and determines the mandibular identity in the first pharyngeal arch. However, it remains unsolved whether this pathway is also critical for pharyngeal arch artery development to form thoracic arteries. Here, we show that the Edn1/Ednra signaling is involved in pharyngeal artery development by controlling the fate of neural crest cells through a Dlx5/Dlx6-independent mechanism. Edn1 and Ednra knock-out mice demonstrate abnormalities in pharyngeal arch artery patterning, which include persistent first and second pharyngeal arteries, resulting in additional branches from common carotid arteries. Neural crest cell labeling with Wnt1-Cre transgene and immunostaining for smooth muscle cell markers revealed that neural crest cells abnormally differentiate into smooth muscle cells at the first and second pharyngeal arteries of Ednra knock-out embryos. By contrast, Dlx5/Dlx6 knockout little affect the development of pharyngeal arch arteries and coronary arteries, the latter of which is also contributed by neural crest cells through an Edn-dependent mechanism. These findings indicate that the Edn1/Ednra signaling regulates neural crest differentiation to ensure the proper patterning of pharyngeal arch arteries, which is independent of the regional identification of the pharyngeal arches along the dorsoventral axis mediated by Dlx5/Dlx6.     

The arterial circle of the brain,its branches and connections in selected representatives of the Antilopinae

The arterial circle of the brain, that is, the circle of Willis, and its branches in ruminants have been chiefly described in farm animals and only in selected wild species. In view of the deficit of information about this vascular region in numerous other species of the Ruminantia, the arteries of the encephalic base were analyzed in five antelope species representing different genera of the Bovidae, Antilopinae. Specimens of the following species were examined: springbuck (Antidorcas marsupialis), blackbuck (Antilope cervicapra), dik‐dik (Madoqua kirkii), saiga (Saiga tatarica), and oribi (Ourebia ourebi). Post‐autopsy material received from domestic zoological gardens was used to inject the bilateral common carotid arteries with a stained acetone solution of vinyl superchloride. When the material was polymerized, the specimens were macerated enzymatically. The process resulted in casts of arteries of the head and encephalic base on a skeletal scaffold. The investigations revealed that the bilateral components of the arterial circle of the brain, that is, the rostral cerebral artery and caudal communicating artery, arose from the division of the intracranial segment of the internal carotid artery, which emerges from the rostral epidural rete mirabile. The extracranial segment of the internal carotid artery was obliterated. In consequence of this process, the blood reaches the brain chiefly from the maxillary artery. The research proved that the arteries of the encephalic base in the Antilopinae are most similar to the vessels described in antelopes of Tragelaphus, Taurotragus, and Boselaphus genera and small domestic ruminants. However, they are different from the arterial pattern of the encephalic base in bovines and other species classified as the Bovini. J. Morphol. 276:766–771, 2015. © 2015 Wiley Periodicals, Inc.     

A histochemical study on the innervation of the cerebral blood vessels in bats

Summary The adrenergic and cholinergic nerves innervating the cerebral blood vessels of four species of Japanese chiropterids (Rhinolophus ferrumequinum, Murina leucogaster, Vespertilio superans and Miniopterus Schreibersi) have been investigated using specific histochemical techniques. In all these species of bats arteries of the internal carotid system are poorly developed, whereas those of the vertebro-basilar system are well developed. The adrenergic and cholinergic nerves innervating these cerebral arteries, however, all originate from the stem nerve bundles entering the cranial cavity along the internal carotid artery. Both nerve plexuses are among the densest of any vertebrate species so far investigated. Adrenergic nerve plexuses are usually composed of complicated meshworks of fine fibres, while cholinergic ones are composed of rather longitudinally arranging meshworks of both thick and thin fibres, exhibiting a very high acetylcholinesterase activity. Small parenchymal arteries and arterioles are also dually innervated by adrenergic and cholinergic nerve fibres of peripheral origin. Intracerebral capillaries, on the other hand, are in several places directly connected with both adrenergic and cholinergic fibres of parenchymal origin. Capillaries in the cerebral and cerebellar cortices, diencephalon and cochlear nucleus in V. superans exhibit a heavy non-nervous acetylcholinesterase activity in their walls, but in R.ferrumequinum and M. schreibersi, the response is weak or negative, except for that in the cochlear nucleus.     

The carotid sinus in lizards with an anatomical survey of the ventral neck region

The anatomy of the ventral neck region of the scincid lizards Chalcides ocellatus and Scincus scincus is presented and is found to be similar to that of other lizards as described in the literature. The internal carotid artery arises by 3-5 roots from the dorsal side of the ascending limb of the carotid arch. During its first part, the internal carotid artery is completely divided into two nearly equal channels. The carotid sinus is more complicated in Chalcides than in Scincus. In lizards, it may be homologous to the carotid labyrinth of fishes and amphibians. Around the origin of the internal carotid artery are two kinds of epithelioid cells scattered in the adventitial connective tissue: a- large cells with rounded, faintly stained nuclei, and little, clear cytoplasm; b- cells with small darkly stained nuclei. Both kinds of cells appear to represent different levels of secretory activity. The number of the large cells increases with greater complexity of the carotid sinus. The cells also increase in size and number during summer (sexual period); this is especially true in younger animals. The epithelioid cells are considered to be homologous to the carotid body of higher vertebrates. The carotid sinus and epithelioid cells together form a closely interrelated system which may be intermediate between the carotid labyrinth of fishes and amphibians, and the carotid body of birds and mammals.     

SPERM WHALE DISTRIBUTIONS AND COMMUNITY ECOLOGY ASSOCIATED WITH A WARM-CORE RING OFF GEORGES BANK

Sperm whale (Physeter macrocephalus) sighting rate in the vicinity of a thermal front on the eastern boundary of a Gulf Stream warm-core ring was five times greater than the pooled rate in the remainder of the study area. No sperm whales were sighted within the ring away from frontal boundaries. Sperm whale distribution patterns associated with the ring were examined using hydrographic and zooplankton data. Hydrographic structure and zooplankton densities and community composition differed between the high-use region and the remainder of the study area, suggesting that mesoscale patterns in the biological and physical environments regulate sperm whale habitat usage. Satellite thermal images indicated cool water associated with the eastern front was shelf or slope water entrained from the Scotian Shelf to the north. Interaction of the warm-core ring with the shelf or slope water is probably indirectly responsible for greater sperm whale presence on the eastern boundary of the ring, providing suitable habitat for their squid prey. Entrainment of shelf water by warm-core rings occurs frequently, providing potential sperm whale habitat in the vicinity of rings. Surveys of warm-core rings and other Gulf Stream features are needed to improve accuracy of sperm whale population estimates.