Structural Organization of the Blood-sinus Systems in Lampreys and Hagfish: Functional and Evolutionary Interpretations

Abstract The head and branchial regions of larval and adult lampreys and hagfish were studied histologically in serial sections. The most remarkable feature in these extant agnathans was the occurrence of large blood-sinuses. In larval lampreys, blood-sinuses are well developed in the velum, an organ that functions to introduce water and accompanying food particles from the mouth into the gill and alimentary regions. The sinuses in the velum may act to transduce the force of contraction of velar muscles to the stroke-like movement of the velum; without these sinuses muscular contractions might simply cause the velum to collapse. In adult lampreys, blood-sinuses are well developed in the peribranchial space that surrounds the branchial (gill) sac and is surrounded by the branchial pouch. It is possible that the force of contractions of the branchial-pouch muscles is transduced effectively to the branchial sac via the peribranchial blood-sinus and facilitates the expiration of water through the external gill pores. If the peribranchial sinus were absent, the muscular contraction might deform the branchial sac in an inappropriate manner. In the hagfish, the blood-sinus system is also well developed in the velum and peribranchial space, although the peribranchial sinus lies outside the muscular branchial pouch. In agnathans, the blood-sinus system may function, at least in part, as a kind of hydrostatic skeleton that transduces the force generated by muscular contraction.     

A radiological study of the central circulation in the lungfish, Protopterus aethiopicus

The dipnoan heart is only in part structurally developed to support a separated circulation in pulmonary and systemic circuits. In the present investigation biplane angiocardiography has been used to describe the extent of such a double circulation and the factors which may modify it in the African lungfish, Protopterus aethiopicus. Contrast injections in the pulmonary vein revealed a clear tendency for aerated blood returing from the lungs to be selectively dispatched to the anterior branchial arteries giving rise to the major systemic circulation. Contrast injections in the vena cava delineated the sinus venosus as a large receiving chamber for systemic venous blood. Contraction of the sinus venosus discharged blood into the right, posterior part of the partially divided atrial space. Contrast injection in the pulmonary vein showed that vessel to pass obliquely from right to left such that blood was emptied distinctly into the left side of the atrium. During contraction the atrial space tended to retain a residual volume in its anterior undivided part which minized mixing. Ventricular filling occurred through separate right and left atrio-ventricular connections. Right-left separation in most of the ventricle was maintained by the partial ventricular septum, the trabeculated, spongelike myocardium and the mode of inflow from the atria. Mixing in the anterior undivided portion of the ventricle during the ejection phase was slight due to a streamlined ejection pattern. The outflow through the bulbus cordis occurred in discrete streams which in part were structurally separated by well developed spiral folds. In the anterior bulbus segment the spiral folds are fused and make completely separate dorsal and ventral outflow tracts. The ventral bulbus channel provides blood to the three anterior branchial arteries. The second and third branchial arteries are large and represent direct shunts to the dorsal aorta. The fourth and fifth branchial arteries are gill bearing and receive blood form the dorsal bulbus channel. The most posterior epibranchial vessels give rise to the pulmonary arteries.     

Gill ultrastructure of the Pacific hagfish Eptatretus stouti

At the gross anatomical level, hagfish gills show unusual features not seen in any other fish gills. Our study was undertaken to determine if peculiarities also characterize the microscopic anatomy and ultrastructure of hagfish gills. To the contrary, branchial respiratory lamellae of Pacific hagfish were found to resemble the lamellae of lampreys, elasmobranchs, and teleosts, often down to the finest subcellular details. As in other fish, hagfish lamellae are lined by epithelium containing pavement cells with organelles indicative of a secretory function, basal cells showing undifferentiated cell features, and branchial ionocytes. The ionocytes are identical to chloride cells of teleosts in cytostructure, distribution, and abundance. There are pillar and marginal capillaries in hagfish gill lamellae. Pillar cells contain bundles of 5-nm microfilaments, and they associate with collagen columns as in other fish. Hagfish pillar cells do exhibit odd features, however: They cluster (groups of up to nine were seen), and their extracellular collagen columns are rarer than in other fish gills (averaging only two columns per three pillar cells). Other special features of hagfish gills are the following: lipid droplets and smooth endoplasmic reticulum are well developed in all cell types; pavement cells secrete a lipomucous product (stains with periodic acid-Schiff, Alcian blue, and Sudan black B); and goblet cells are absent. The presence of "chloride cells" in hagfish is puzzling, as hagfish body fluids are iso-osmotic to seawater and there is no need to osmoregulate for sodium chloride; the ionocytes contain carbonic anhydrase, suggesting a function in acid/base regulation.     

Degradation, receptor binding affinity, and potency of insulin from the Atlantic hagfish (Myxine glutinosa) determined in isolated rat fat cells

Insulin from the Atlantic hagfish, Myxine glutinosa, a primitive vertebrate, was studied with respect to degradation, receptor binding, and stimulation of glucose transport and metabolism in isolated rat adipocytes. The degradation was studied in a concentrated suspension with about 100mul of cells/ml of suspension. 125I-labeled hagfish insulin and 125I-labeled pig insulin were degraded at the same rate when present in concentrations of 0.3nM. Native hagfish insulin inhibited the rate of degradation of 125I-labeled pig insulin half-maximally at a concentration of 12+/-2 nM (S.D., n=6) as compared to 130+/-32 nM (S.D.,n=6) for pig insulin. Native hagfish insulin in a concentration of 130 nM was biologically inactivated at a rate several times slower than pig insulin in the same concentration. The results indicate that the maximal velocity (Vmax) of degradation of hagfish insulin as well as the concentration causing half-maximal velocity (Km) are about 10 times lower for hagfish insulin than for pig insulin. The receptor binding and the biological effects of hagfish insulin were studied in dilute cell suspensions where the degradation of hormone in the medium was negligible. The receptor binding affinity of hagfish insulin was 23+/-7 per cent (S.D., n=10) of that of pig insulin. Hagfish insulin was able to elicit the same maximal stimulation of both 3-o-methylglucose exchange and lipogenesis from glucose as pig insulin. However, the potency of hagfish insulin with respect to activation of lipogenesis was only 4.6+/-0.6 per cent (S.D., n=15) of that of pig insulin. Hagfish insulin thus constitutes the first described insulin which exhibits a discrepancy between relative binding affinity and relative potency. This discrepancy was not due to the methionine residue (B31) at the COOH-terminal end of the B chain of hagfish insulin, since removal of this residue caused no marked change in the binding affinity or the potency. The results indicate that the receptor occupancy must be 5 times higher with hagfish insulin than with pig insulin to cause a particular degree of activation of lipogenesis. Hagfish insulin might therefore be characterized as a "partial antagonist" on the receptors. However, it was not possible to demonstrate antagonistic properties of hagfish insulin on the cells. The effect of hagfish insulin plus pig insulin in submaximally stimulating concentrations was additive. Furthermore, the decay of activation of adipocytes after incubation with hagfish insulin followed the same time course as the decay of activation after incubation with pig insulin in a concentration of equal potency. These phenomena are in agreement with the concept that adipocytes possess a large excess of receptors which can mediate the effect of insulin on lipogenesis from glucose.     

Vascular anatomy of the gills of the stingarees Urolophus mucosus and U. paucimaculatus (Urolophidae,Elasmobranchii)

The branchial vascular anatomy of Urolophus mucosus and U. paucimaculatus was studied by scanning electron microscopical examination of critical-point-dried tissue or of vascular corrosion casts. The vasculature could be divided into arterioarterial and arteriovenous pathways, which channel the flow of blood through the gills. The arterioarterial pathway consists of an afferent branchial artery which gives rise to afferent distributing arteries that run through the tissues of the interbranchial septum and supply the afferent filament arteries of several filaments. Afferent filament arteries open regularly into a corpus cavernosum in the core of the filament; unlike other elasmobranchs no septal corpora cavernosa are found. At the tip of the filament, channels of the corpus cavernosum connect to a channel which passes across the distal end of the filament from afferent to efferent side. This channel always connects to the afferent filament artery, and in many filaments it connects to the efferent filament artery as well. In addition, a vascular arcade connects all the afferent filament arteries along the entire length of each hemibranch. The filament corpus cavernosum supplies the secondary lamellae. The lamellae drain into efferent lamellar arterioles which in turn drain into the efferent filament artery and the efferent branchial artery. The vascular anatomy of the arteriovenous pathway is similar to that described in other elasmobranchs and consists of arteriovenous anastomoses, found only arising from efferent arterial circulation, and the venolymphatic system, which is composed of the central venous sinus and the companion vessels.     

Branchial vascular pathways in two species of Tetraodontiformes and the concept of secondary vessels and nutrient arteries

The vascular organisation of the branchial basket was examined in two Tetraodontiform fishes; the three-barred porcupinefish, Dicotylichthys punctulatus and the banded toadfish, Marylina pleurosticta by scanning electron microscopy of vascular casts and standard histological approaches. In D. punctulatus, interarterial anastomoses (iaas) originated at high densities from the efferent filamental and branchial arteries, subsequently re-anastomosing to form progressively larger secondary vessels. Small branches of this system entered the filament body, where it was interspersed between the intrafilamental vessels. Large-bore secondary vessels ran parallel with the efferent branchial arteries, and were found to constitute an additional arterio–arterial pathway, in that these vessels exited the branchial basket in company with the mandibular, the carotid and the afferent and efferent branchial arteries, from where they gave rise to capillary beds after exit. Secondary vessels were not found to supply filament muscle; rather these tissues were supplied by single specialised vessels running in parallel between the efferent and afferent branchial arteries in both species examined. Although the branchial vascular anatomy was generally fairly similar for the two species examined, iaas were not found to originate from any branchial component in the banded toadfish, M. pleurosticta, which instead showed a moderate frequency of iaas on other vessels in the cephalic region. It is proposed that four independent vascular pathways may be present within the teleostean gill filament, the conventional arterio–arterial pathway across the respiratory lamellae; an arterio–arterial system of secondary vessels supplying the filament and non-branchial tissues; a system of vessels supplying the filament musculature; and the intrafilamental vessels (central venous sinus). The present study demonstrates that phylogenetic differences in the arrangement of the branchial vascular system occur between species of the same taxon.     

Current knowledge of hagfish reproduction: implications for fisheries management

This review briefly summarizes the latest findings on reproductiveendocrinology of Atlantic hagfish (Myxine glutinosa) and implicationsfor fisheries management. In response to a major decline orcollapse of the fisheries (groundfish and anadromous species)industry in the Northeast, species that were once consideredalternative or underutilized have and are being identified thatmay be suitable for commercial harvest, one such example isthe hagfish. Hagfish in recent years have been sought afteras valuable fish not only for their flesh, but also their skin.Currently, there are no regulations governing the harvestingof hagfish along the East Coast. There has been little to noinformation of the life history of hagfish including growthrate, age determination, reproductive biology, life span, andlarval size at hatching. Thus, the level at which a sustainablefisheries for this species can be maintained is unknown. Insome parts of the world, hagfish stocks are being depleted dueto overfishing. In order for fisheries management to manageits hagfish stocks and develop a sustainable commercial hagfishfishery, critical information is needed to assist in determiningthe optimal use of this valuable resource. Key elements of the reproductive system have not been elucidatedin hagfish. However, there is new evidence from recent reproductivestudies that Atlantic hagfish may have a seasonal reproductivecycle. These data include seasonal changes in gonadotropin-releasinghormone (GnRH), gonadal steroids, estradiol and progesterone,corresponding to gonadal reproductive stages along with theputative identity of a functional corpus luteum. This newlyacquired data may provide important information to fisheriesmanagers of the East Coast.     

cDNA cloning of a mannose-binding lectin-associated serine protease (MASP) gene from hagfish (Eptatretus burgeri)

Hagfish, agnathan cyclostome, is the most primitive extant vertebrate and its complement (C) system seems to be a primordial system in comparison with a well-developed C system in gnathostome vertebrates. From a phylogenic perspective of defense mechanisms, we have isolated complement C3 from the serum of hagfish (Eptatretus burgeri). In this study, we first attempted to identify a hagfish Bf or C2 as a C3 convertase by RT-PCR using degenerative primers designed on the basis of the conserved amino acid stretches among the several kinds of serine proteases. Contrary to our expectation, homology search of cloned RT-PCR product suggested that there was a partial cDNA encoding the homologue of neither Bf nor C2 but a mannose-binding lectin-associated serine protease (MASP). Analyses of a full-length cDNA clone isolated from a hagfish liver cDNA library by using the partial cDNA as a probe indicated that this cDNA encoded hagfish MASP 1. This evidence strongly suggests that the hagfish defends itself against pathogens at least by the complement system composed of lectin pathway.     

Different sensitivities of arteries and veins to vasoactive drugs in a hagfish, Eptatretus cirrhatus

We used myography on five different arteries and three veins of the hagfish, Eptatretus cirrhatus, to test the response of vessels to vasoactive drugs. Concentration-response curves were generated for carbachol, endothelin-1, arginine vasotocin and the adrenergic agonists, phenylephrine and isoprenaline. pEC50 values indicated that veins were more sensitive to endothelin-1 than were arteries, but the arteries were more sensitive to the cholinergic agonist, carbachol. Segmental arteries did not react to arginine vasotocin, but all other vessels did, and on a molar basis it was the most potent agonist tested. That ventral and dorsal aortas were more sensitive to arginine vasotocin than smaller vessels might indicate that this neurohypophysial peptide has the potential to exert a profound influence on branchial vascular resistance and cardiac output in hagfishes. The results also demonstrate the potential for a variety of endogenous peptides to contribute to central venous tone.     

Fine structure of the excretory system of Amphioxus (Branchiostoma floridae) and its response to osmotic stress

Summary The excretory organs of Amphioxus occur as segmentally arranged structures throughout the pharyngeal region and may be divided into three components: the solenocytes, the renal tubule, and the renal glomerulus.The solenocytes possess foot processes that rest upon the coelomic surface of the ligamentum denticulatum. The tubular apparatus of the solenocytes consists of ten triangular rods surrounding a central flagellum. The distal end of the tubular apparatus enters branches of the renal tubule. The renal tubule eventually opens into the atrial cavity of Amphioxus. The renal glomerulus is a sinus within the connective tissue of the ligamentum dentieculatum where it connects elements of the branchial circulation with the dorsal aorta. The renal glomerulus, like other blood vessels of Amphioxus, lacks an endothelial lining.If Amphioxus is adapted to artificial sea water at different concentrations there is no change in kidney morphology suggesting that Amphioxus is either is osmotic with its environment or is osmoregulating with other organs.This work was supported by U.S. Public Health Service Grant 5-T01-GM 00582.     

New aspects of the intrafilamental vascular system in gills of a euryhaline teleost,Tilapia mossambica

Summary The non-respiratory vascular system of T. mossambica gill filaments was studied in serial longitudinal and cross sections. Comparatively few scattered vascular communications occur between the afferent filament artery and the central venous sinus (AVA_aff). The efferent filament artery, however, is connected by regularly arranged anastomoses (AVA_eff), directly, and sometimes indirectly via nutritive vessels, to the central sinus. These AVA_eff are about as numerous as lamellae counted on one side of each filament, although they diminish slightly in number towards the filament base. The relation AVA_eff to AVA_aff was 17.6:1 in the distal and 17.8:1 in the basal filamental region, while in the tip region of 7 filaments 126 AVA_eff but only 1 AVA_aff were encountered. No direct connection between the lamellar lacunae and the central sinus was detected. According to these results, non-respiratory intrafilamental blood shunting appears unlikely. AVA_eff are assumed to be the main route for blood entering the central venous sinus which would consequently flow into the branchial veins.The authors wish to express their sincere thanks to Miss Angelika Krauß for her valuable technical assistance and to Miss Erna Finger for making the photographs. Thanks are also due to Mr. W. Zeltmann for drawing Figs. 2, 5, and 8 and to Mr. K. Herzog for Fig. 7.     

Functional Organization of the Teleost Gill

The circulation of the gills has been studied in the perch, trout and eel combining the conventional histological methods and casting techniques. The existence of two blood pathways in each gill arch was confirmed. 1 — An arterio-arterial pathway assuming the respiratory function. It includes the afferent branchial artery and in each primary lamella the afferent primary artery, the secondary lamellae capillaries and the primary and branchial efferent arteries. 2 — An arterio-venous pathway arising from both the branchial artery, in the gill arch, and the primary arteries in each primary lamella. This pathway includes the central venous sinus of the primary lamella, several small veins and is finally connected with the branchial veins. 3 — The lack of connections between afferent primary arteries and cvs in the trout and the perch makes impossible a direct blood flow from the afferent to the efferent artery (shunt). In the eel connections between cvs and both afferent and efferent arteries do not mean that a shunt is operating according to the pressure gradient.     

Land crabs with smooth lungs: Grapsidae,Gecarcinidae, and Sundathelphusidae ultrastructure and vasculature

The highly terrestrial grapsids and gecarcinids and the amphibious sundathelphusids all have large, expanded branchial chambers. The lining of the branchial chambers is smooth and well vascularized, and it functions as a lung. The respiratory membrane and the cuticle lining the lung are extremely thin (200–350 nm). The blood vessels within the lung are formed from connective tissue cells supported by collagen fibres and lined by a basal lamina. The major vessels in the lung are embedded deep in the branchiostegite and lie just beneath the thick outer carapace. These vessels branch towards the respiratory membrane, where they eventually lose their connective tissue coverings to form thin, flattened lacunae directly below the respiratory epithelium. The lacunae (exchange sites) are bordered by specialized connective tissue cells, which either bear microvilli on their apical surface (fimbriated cells) or are very smooth. The respiratory circulation in the lung is very complex, with two portal systems present between the afferent and efferent systems, producing a total of three lacunal exchange beds. Portal systems increase the surface area available for gas exchange. The major distributing vessel in the lung is the branchiostegal vein, which runs along the inner margin of the branchiostegite. The main venous supplies come anteriorly from the infraorbital and ventral sinuses and posteriorly from the procardial sinus. The main collecting vessel is the pulmonary vein, which arises anteriorly and which runs around the ventral perimeter of the branchiostegite before emptying into the pericardial sinus. © 1993 Wiley-Liss, Inc.     

Baroreceptor control of pressure-flow relationships during hypoxemia

In the absence of peripheral chemoreceptors, the effects of graded hypoxemia on the carotid sinus control of central and regional hemodynamics were studied in anesthetized mongrel dogs. Baroreceptor stimulation was effected by carotid sinus isolation and perfusion under controlled pressure. Blood flows were measured in the aorta and the celiac, mesenteric, left renal, and right iliac arteries. Carotid sinus reflex set-point pressures were well maintained until hypoxemia was severe. Carotid sinus reflex set-point gain was maximal during mild hypoxemia. Reflex operating point regional flows were unaffected by hypoxemia. A factorial analysis of overall reflex increases in mean aortic pressure, flow, and power during reduced baroreceptor stimulation showed potentiation by increasing hypoxemia. Corresponding effects of baroreceptor stimulation and hypoxemia on aortic resistance and heart rate were additive. Celiac, renal, and iliac blood flows increased during both hypoxemia and reduced baroreceptor stimulation. Only in the celiac bed were blood flow changes independent of concomitant changes in cardiac output. Thus, at maximum sympathetic stimulation (low carotid sinus pressure) during hypoxemia, the cardiovascular system maintained both central and regional blood flows at high systemic blood pressures independent of the peripheral chemoreceptors.     

Glomerular bypass shunts in the kidney of the Atlantic hagfish,Myxine glutinosa

Summary The vascular pathways associated with the glomerulus of the Atlantic hagfish, Myxine glutinosa have been studied by scanning electron microscopy of corroded resin casts of the vasculature. Although the overall pattern of the renal vasculature did not differ from earlier reports, a previously unreported vascular pathway which arose from the renal artery and bypassed the glomerular capillaries in 28% of glomeruli was clearly demonstrated. Glomerular bypass shunts either ran to join the loose capillary network around Bowman's capsule and thereby drain into the network of vessels associated with the mesonephric duct (ureter), or ran directly into the ureteral system of vessels and subsequently into the posterior cardinal veins. Glomerular bypass shunts which theoretically permit renal arterial blood to bypass the process of filtration may play a role in the regulation of body fluid volume.     

A new species of hagfish (Myxinidae: Eptatretus) from Papua New Guinea

A new species of seven‐gilled hagfish Eptatretus astrolabium (Myxinidae) is described from a 400 mm total length female trapped 1 km east from Planet Rock, Astrolabe Bay, Papua New Guinea, at c. 500 m depth. This is the first hagfish species reported from the waters around New Guinea. It can be distinguished from other hagfishes by a combination of characters including seven pairs of gill apertures, three‐cusp multicusps on the anterior and posterior rows of cusps, 10 posterior unicusps, 52 total cusps, 18–19 prebranchial pores, five branchial pores, 48–49 trunk pores, 83–84 total pores and no nasal‐sinus papillae.     

The morphology and vasculature of the lungs and gills of the soldier crab,Mictyris longicarpus

The five gill pairs of Mictyris longicarpus have the lowest weight specific area reported for any crab. The cuticle of the gill lamellae is lined with epithelial cells which have structural features characteristic of iontransporting cells. Pillar cells are regularly distributed in the epithelium and serve to maintain separation of the two faces of the lamellae. The central hemolymph space is divided into two sheets by a fenestrated septum of connective tissue cells. The dorsal portion of the marginal canal of each lamella receives hemolymph from the afferent branchial vessel and distributes it to the lamella while the ventral portion of the canal collects hemolymph and returns it to the efferent branchial vessel. The lung is formed from the inner lining of the branchiostegite and an outgrowth of this, the epibranchial membrane. Surface area is increased by invagination of the lining which forms branching, blind-ending pores, giving the lung a spongy appearance. The cuticle lining the lung is thin and the underlyng epithelial cells are extremely attenuated, giving a total hemolymph/gas distance of 90–475 nm. Venous hemolymph is directed close to the gas exchange surface by specialised connective tissue cells and by thin strands of connective tissue which run parallel to the cuticle. Air sacs are anchored in position by paired pillar cells filled with microtubules. Afferent hemolymph is supplied from the eye sinus, dorsal sinus, and ventral sinus. Afferent vessels interdigitate closely with efferent vessels just beneath the respiratory membrane. The two systems are connected by a “perpendicular system” which ramifies between the airways and emerges to form a sinus beneath the carapace and then flows back between the air sacs to the efferent vessels. The afferent side of the perpendicular system is the major site of gas exchange. Efferent vessels return via large pulmonary veins to the pericardial cavity. P_aO₂ levels were high (95.5 Torr), indicating highly efficient gas exchange.     

Branchial and circulatory responses to serotonin and rapid ambient water acidification in rainbow trout

Although the branchial and cardiovascular effects of serotonin (5-hydroxytryptamine) have only partially been characterized, a physiological role for serotonin in the cardiorespiratory responses of fish to environmental changes such as reduced Ph has been suggested. Therefore, we have characterized and compared the effects of serotonin and a rapid reduction of Ph in the ambient water (from pH 8.8 to pH 4.0) on ventral and dorsal aortic blood pressures, heart rate, cardiac output, and arterial pH in rainbow trout, Onchorhynchus mykiss. In addition, the circulation in the branchial microvasculature was observed using in vivo epi-illumination microscopy. The fall in water Ph and injection of serotonin (100 nmol/kg) both increased the branchial resistance and reduced the efferent filamental artery (EFA) blood velocity. Nevertheless, quantitatively, the responses to the two stimuli were different. Although acid exposure caused a much more profound increase in branchial resistance compared with serotonin, the blood flow in the observable distal portion of the EFA was only reduced by 60% in acid water, while it stopped with serotonin. Regardless of the marked branchial resistance elevation, a constriction of the efferent filamental vasculature could not be seen during acid exposure, as occasionally was the case with serotonin. While methysergide completely abolished the serotonin-induced branchial events, it only modestly suppressed the acid-induced reduction of EFA blood velocity. In contrast, all of the systemic changes induced by serotonin and acidic water were insensitive to methysergide. In conclusion, acidic water and injected serotonin elevate the branchial resistance, but the involvement of a serotonergic component in the acidic response appears negligible.     

Die Vaskularisation der Kiemen von Myxine glutinosa L. (Cyclostomata)

The angioarchitecture of the gills in Myxine glutinosa L. was studied by scanning electron microscopy of vascular corrosion casts (methylmethacrylate). It was found that the afferent branchial artery may be connected to the sinus peribranchialis by a papilla. The sinus is connected to delicate vessels and sinuses, which are interposed between meridionally arranged radial arteries. These delicate vascular formations continue into the interior of the gill and form a plexus on both poles of the gill folds. Light and scanning electron microscopical studies on the vascular endothelium of the afferent vessels of the gill lamellae reveal rounded endothelial cells, which are characterized by a high content of granula, by long cellular processes and by bridge-formations towards neighbouring cells. Supporting columns within the vascular system of the lamellae were found to be set up by several spirally arranged cells. SEM observations reveal goblet cells and numerous superficial epithelial cells with various numbers of microvilli and microridges forming the epithelial surface of the gill folds.     

Digestion under duress: nutrient acquisition and metabolism during hypoxia in the Pacific hagfish

Hagfish feed by immersing themselves in the body cavities of decaying animals. This ensures a rich nutrient source for absorption via the gills, skin, and gut, but it may also subject hagfish to reduced levels of dissolved oxygen and elevated levels of the products of biological degradation. This study investigated the impacts of hypoxia and ammonia on the assimilation and metabolism of selected nutrients (glycine, l-alanine, and glucose) in Pacific hagfish (Eptatretus stoutii). Throughout exposure to hypoxia, plasma glucose levels increased. This was not accompanied by an increase in gut glucose transport, which suggests mobilization of glucose from body glycogen stores. Hypoxia preexposure enhanced glycine absorption across the gut and the gill, although l-alanine uptake was unchanged in these tissues. A 24-h period of exposure to hypoxia in hagfish concurrently exposed to waterborne radio-labeled glycine led to a large (5.7-fold) increase in brain glycine accumulation. Preexposure to high levels of waterborne ammonia (10 mM) for 24 h had no impact on gut or skin glycine uptake. These results indicate that hagfish are adapted to maintain nutrient assimilation despite environmental stressors and that tissue-specific absorption of key nutrients such as glycine can even be enhanced in order to sustain critical functions during hypoxia.