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.     

Structure and function of the velar muscle in the New Zealand hagfish Eptatretus cirrhatus: response to temperature change and hypoxia

The rate of velar movement in Eptatretus cirrhatus, as determined by electromyography, increased with Q(10) 3·2 during exposure to temperatures between 7 and 19° C and increased 3·9 fold during exposure to hypoxia (oxygen partial pressure = 6·67 kPa). This confirms the role of the velum in generating respiratory currents and modification of its activity in response to changes in metabolic demand or environmental oxygen availability. The maximum velar rate observed was 168 beats min(-1) , higher than that recorded in any hagfish species to date. Fibres of musculus craniovelaris were exclusively small, red (slow-twitch) fibres, consistent with a high aerobic capacity required by fibres involved in rhythmic, ongoing activity.     

Early Development of the Hagfish Pituitary Gland: Evidence for the Endodermal Origin of the Adenohypophysis

The adenohypophysis in early head fold stage hagfish embryosis at first a distinct differentiated thickening of the archentericroof where it contacts the developing infundibular portion ofthe brain. This portion of the archenteron eventually becomesthe dorsal epithelium of the nasopharyngeal duct. The laterdevelopment of the adenohypophysis involves formation of multipleacinar outgrowths of the dorsal nasopharyngeal epithelium whichtogether form a layered mass of follicular tissue adjacent tothe neurohypophysis. This mode of origin of the adenohypophysisby endodermal polyinvagination and delamination differs fromall other vertebrates, including the lampreys. The pertinenceof this new information for considerations of monophyletic versusdiphyletic evolutionary origins of the modern cyclostome groupsis pointed out. The unusual development of the hagfish adenohypophysispresents some new and unanticipated puzzles within the generalquestion of pituitary evolution.     

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.     

Insulin in Invertebrates and Cyclostomes

It seems increasingly clear that insulin is a hormone that doesnot occur exclusively in vertebrates. Several independent reportsnow exist giving evidence of insulin production in the digestivetissues of both deuterostomian and protostomian invertebrates.Cells with some light-microscopical and ultrastructural characteristicsof vertebrate B-cells have also been observed. Recently, evidencehas been obtained that insulin can act as a hypoglycemic hormone,promoting glycogen synthesis, also in a protostomian invertebrate,the gastropod mollusc, Strophocheilus oblongus. The endocrine pancreas of the cyclostomes occupies a key positionin the comparative endocrinology of the islet parenchyma andin the evolution of insulin production. It may represent anevolutionary link between the presumably gut-connected dispersedinsulin-producing cells of deuterostomian invertebrates andthe pancreatic islets of gnathostomian vertebrates. This hypothesiswas supported by the fact that cells with light-microscopicaland ultrastructural similarities to the islet B-cells were observedin the bile duct mucosa of the hagfish, Myxine glutinosa. However,immunofluorescent studies with antisera against human insulinand C-peptide did not show any immunoreactive material outsidethe B-cells of the endocrine pancreas. Particular attentionwas paid to elucidate the biological significance of the largecystic cavities that are so typical for the cyclostomian isletparenchyma. The working hypothesis that they may contain storedinsulin, proinsulin (or even "proto-proinsulin") was not supportedby immunofluorescence, autoradiographic, or ultrastructuralinvestigations, nor by proinsulin assays. It is possible thathagfish islet B-cells contain zinc, despite the fact that theamino acid residue in B₁₀-position is aspartic acid insteadof histidine. The biosynthesis of hagfish insulin shows a patternsimilar to that in gnathostomes. Its rate is related to theambient temperature and at 11 C the conversion of proinsulinto insulin lasts several days.     

On the Origin of Thymic Lymphocytes

In the leopard frog (Rana pipiens), thymic lymphocytes do notoriginate from blood-borne stem cells that migrate into thethymus anlage; rather they arise in situ from elements in thethymic rudiment itself. After thymic differentiation, the lymphocytes(or their descendants) leave the thymus and extensively seedthe peripheral lymphoid organs. Indeed, virtually all the lymphocytesin the spleen, kidney, and bone marrow are ontogenically derivedfrom thymic cells. In postmetamorphic life, the thymus representsan organ in which lymphopoiesis is genuinely self-sustaining.Throughout the juvenile life of the frog, there is no indicationof an inward afferent stream of cells entering the intact thymus.     

Development of Transplantation Immunity and Restoration Experiments in the Thymectomized Amphibian

This paper examines the thymic dependence of alloimmunity inamphibians. In Xenopus, the presence of a thymus during thefirst 2 weeks of life is essential for the development of normalfirst-set skin allograft immunity. Thymectomy during this earlyperiod always impairs the alloimmune response of young adulttoads. However, most of these thymectomized animals are ableto completely destroy skin allografts, albeit with prolongedrejection times. Chronic graft rejection, rather than tolerance,still occurs following thymectomy as early as 5 days, when thethymus contains no small lymphocytes. In contrast to the considerabledifferences in first-set allograft survival times in controland early-thymectomized Xenopus, second-set grafts, appliedsubsequent to first-set destruction, are rejected in acute fashion(<3 weeks) in both groups. That the defect in first-set alloimmunityis specifically related to absence of thymus has been confirmedby implanting allogeneic thymus 2 weeks post-thymectomy. Thedonor thymus remains healthy and restores the allograft responseto normal. In contrast, allogeneic spleen does not reconstituteand itself often undergoes destruction. Preliminary autoradiographicexperiments on lymphoid tissue involvement in first-set allograftrejection are also described.     

Ontogeny of the Immune System in Amphibians

SYNOPSIS. Experiments with amphibians have revealed that tissuesallografted in embryonic and early larval life may later succumbto a host immunological attack. In Xenopus, the ontogeny ofthis alloimmune response is correlated with the lymphoid maturationof the thymus. This article describes experiments primarilydesigned to ascertain if such a correlation exists in Rana pipiens. Initially, a histological study of the differentiation of thelymphomyeloid complex of the leopard frog was undertaken. At18–21°C lymphoid histogenesis is well under way inthe thymus and is beginning in many other organs during thethird week of larval life. Extensive growth and differentiationof these organs follow. Observations are also presented on thestructure, function and development of the lymphoid and Iymphomyeloidorgans from late larval life throughmetamorphosis to adulthood. Experiments were then performed to determine the onset of thealloimmune response to embryonically transplanted neural foldmaterial. At 18–21°C incompatibility phenomena, albeitslight, are first detected in these grafts as early as 17 daysafter fertilization, i.e. 15 days after transplantation. Thus,in the leopard frog, the alloimmune response develops soon afterlymphoid maturation of the thymus. At later stages of development,a more vigorous response is witnessed, concomitant with a rapidphase of lymphoid organ differentiation.     

Reproductive biology and ecology of Pacific hagfish (Eptatretus stoutii) and black hagfish (Eptatretus deani)

The reproductive biology of Pacific hagfish Eptatretus stoutii (Lockington, 1878) and black hagfish Eptatretus deani (Evermann & Goldsborough, 1907) was assessed using current and historical data. Our results found that the reproductive characteristics of both hagfish species reflect those of K-selected species, which tend to live long and exhibit slow growth rates, low fecundity (approximately 20 eggs per female) and late maturity. Additionally, females of both species commence maturation prior to males. This study provides a population profile for both species of hagfish, but further assessments are needed to effectively manage a sustainable hagfish fishery.     

THE ADDUCTOR AND RETRACTOR MUSCLES OF THE VELIGER OF PECTEN MAXIMUS (L.) (BIVALVIA)

In Pecten maximus (L.), retractor and adductor muscles becomefunctional in the early veliger larva. The twelve-day-old veligerhas four pairs of velar retractors, three pairs of retractorsattached to the posterior body wall and an anterior adductor.The pediveliger has in addition, pedal retractor muscles anda posterior adductor. The retractors consist of striated muscle:the adductors have both smooth and striated portions. The retractorsattach near the hinge, branch to a greater or lesser extent,then attach to specific areas of the velum, posterior body walland foot. Some features of the branching and of the dispositionof points of attachment form a pattern which exhibits mirrorsymmetry about the plane between the two shell valves. Thispattern is characteristic of the species. It is deduced thatretraction and protraction of the velum result from co-ordinatedsequences of muscle contractions. ^*Present address: Forest Products Research Centre, P.O. Box1358, Boroko, Papua New Guinea. (Received 15 June 1984;     

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.     

Seasonal concentrations of reproductive steroids in the gonads of the Atlantic hagfish, Myxine glutinosa

Changes in gonadal morphology, gonadal estradiol, and progesterone were examined in Atlantic hagfish, Myxine glutinosa, during a period of 17 months, beginning in April, 2001. Atlantic hagfish were captured from the ocean on a monthly basis. A total of 60 hagfish were divided into three different size classes of twenty hagfish each (small 20-35 cm, medium 35-45 cm, large 45-55+cm) and transported to the University of New Hampshire for sampling. Overall, in the medium and large size hagfish, estradiol and progesterone had significantly elevated peaks in January, 2001. There were significant increases in estradiol concentrations in January, with relatively low fluctuations in levels for the rest of the sampling period. Progesterone concentrations increased significantly in January, 2002, in medium and large hagfish, and remained elevated until June and April, 2002, for the two size classes respectively. The majority of hagfish sampled were females or hermaphrodites; few true males were identified in any of the samples. The number of females with large eggs increased following the estradiol peak in January and hermaphrodites with mature sperm were identified in the July, 2002, sample. These data represent the first evidence for a seasonal reproductive cycle in M. glutinosa and only the second seasonal reproductive cycle identified in any hagfish species.     

Complement-like protein from the phylogenetically primitive vertebrate,Eptatretus Stouti,is a Humoral Opsonin

• 1.1. Serum from the Pacific hagfish,Eptatretus stouti,contains a complement-like protein (CLP).
• 2.2. CLP from unfractionated hagfish serum and from affinity-purified preparations binds to yeast cell surfaces.
• 3.3. Incubation with CLP enhances the phagocytosis of yeast by hagfish leukocytes.
• 4.4. CLP-mediated opsonization can be inhibited by anti-CLP antibody, EDTA, d(+)mannose and l(+)rhamnose.
• 5.5. Additional opsomic factors are also in hagfish serum.

     

The Complete Mitochondrial Genome of the Hagfish Myxine glutinosa: Unique Features of the Control Region

The complete sequence of the mitochondrial DNA of the hagfish Myxine glutinosa has been determined. The hagfish mtDNA (18,909 bp) is the longest vertebrate mtDNA determined so far. The gene arrangement conforms to the consensus vertebrate type and differs from that of lampreys. The exceptionally long (3628-bp) control region of the hagfish contains the typical conserved elements found in other vertebrate mtDNAs but is characterized by a large number of putative hairpins, which can potentially fold into a highly compact secondary structure that appears to be unique to hagfish. The comparison of the mtDNAs of two M. glutinosa specimens, excluding the control region, shows a 0.6% divergence at the nucleotide level as a sample of intraspecies polymorphism. Received: 21 August 2000 / Accepted: 2 March 2001     

Structure and biological activity of hagfish insulin

An isomorphously phased electron density map of hagfish (Myxine glutinosa) insulin has been calculated at a resolution of 3·1 Å spacing. The molecule crystallises with one molecule per asymmetric unit but is organised as a symmetric dimer lying on a 2-fold crystal axis. The structure of the hagfish insulin monomer is much more similar to that of pig insulin molecule 2 than molecule 1 of the dimer that constitutes one third of the 2 Zn insulin hexamer. There are different conformations however at the N and C termini of the B-chain. At the C terminus the two final residues on hagfish insulin partially obscure the A1 glycine residue, which in pig insulin is exposed. This structural difference has been shown, however, not to be responsible for the reduced activity of the hagfish insulin.     

Angiotensin I-converting enzyme-like activity in tissues from the Atlantic hagfish (Myxine glutinosa) and detection of immunoreactive plasma angiotensins

Using a highly sensitive fluorimetric assay, significant levels of angiotensin I -converting enzyme-like activity (ACELA) were detected in a range of tissues (branchial heart, gill, kidney with associated vasculature and archinephric duct, liver, whole brain and gut) from the Atlantic hagfish (Myxine glutinosa). The highest ACELA occurred in heart and gill (1.8 and 1.5 nmol His–Leu min⁻¹ mg protein⁻¹, respectively). The mammalian angiotensin I-converting enzyme (ACE) inhibitor, captopril, at 10⁻⁵ M was a potent inhibitor of the ACELA found in all hagfish tissues. Radioimmunoassay showed that immunoreactive angiotensins (251.8±11.8 pM) were detectable in hagfish plasma. The validity of the assay for measurement of hagfish angiotensins was indicated by the parallelism of the angiotensin II standard curve against serially diluted hagfish plasma. Measurement of immunoreactive plasma angiotensins and detection of significant levels of ACELA in a wide range of tissues gives indirect evidence for the presence of a renin–angiotensin system in hagfishes, the earliest evolved group of craniates.     

A REVIEW OF LARVAL DEVELOPMENT IN THE INTERTIDAL LIMPET GENUS SIPHONARIA (GASTROPODA: PULMONATA)

A compilation of distributional and life-history data relatingto mode of larval development is presented for 26 species ofSiphonana, a genus of intertidal pulmonates. Most species depositgelatinous benthic egg masses with two species releasing pelagicegg masses. Fifteen species hatch as planktonic-developing larvae,nine hatch as direct-developing juveniles, and in a furthertwo larvae hatch with both the swimming velar apparatus (associatedwith plank-tonic development) and a crawling foot (associatedwith direct development). Data on mode of larval developmentare interpreted with respect to some adaptive models. Despiteimportant exceptions, there is support for adaptive models basedupon egg capsule size (direct developers hatch from larger eggcapsules) and intertidal distribution (direct developers generallyoccur higher on the shore than planktonic developers). Worldwide,planktonic developers are more widespread than direct-developingspecies, and individual planktonic species have a greater meanlatitudinal range. The evidence for adaptive models relatinglatitudinal distribution to developmental mode is equivocal.There appears to be no clear relationship between body sizeand developmental mode in the genus, although the smallest specieshas direct development and the largest has planktonic development.In most siphonariid subgenera, developmental mode appears tobe constant, but two subgenera contain a mixture of developmentaltypes (Received 1 November 1993; accepted 15 April 1994)     

Radiographic and aerodynamic measures of velopharyngeal anatomy and function following Furlow Z-plasty

Recent studies have shown that the Furlow double-opposing Z-plasty has several advantages that make it an attractive procedure for cleft palate repair and treatment of velopharyngeal insufficiency in selected cases. The anatomic changes associated with this procedure have never been documented prospectively. The purpose of this study was to describe radiographic dimensions of the velopharynx and aerodynamic measures of velopharyngeal function in a group of patients before and after Furlow Z-plasty for the treatment of velopharyngeal insufficiency. Twelve consecutive patients with cleft palate and velopharyngeal insufficiency, ranging in age from 3 to 19 years, were selected as candidates for Furlow Z-plasty based on perceptual, endoscopic, and radiographic findings. Eight patients had repaired cleft palate with a residual muscle diastasis and four patients had unrepaired submucous cleft palate. Subjects received aerodynamic and cephalometric assessments before and after Z-plasty. Cephalometric x-rays were measured for velar length, thickness, and pharyngeal depth. Mean nasal airflow during pressure consonants (Vn) was calculated from pressure/flow studies, and patients were categorized as having complete closure (<10 cc/sec Vn) or incomplete closure (>10 cc/ sec Vn). After Z-plasty, there was a significant increase in velar length (p = 0.002) and velar thickness (p = 0.001). After surgery, patients with complete velopharyngeal closure had significantly greater velar length than the incomplete closure group (p = 0.05) with nearly twice the increase in length. Similarly, following surgery, the complete closure group had significantly greater thickness than the incomplete closure group (p = 0.01), with a greater postoperative increase in velar thickness (p = 0.005). Finally, there was a significant negative correlation between percent increase in length and percent increase in thickness for patients in the complete closure group (r = -0.91, p = 0.03). Findings demonstrate that following Furlow Z-plasty, patients with cleft palate and velopharyngeal insufficiency obtained significant increases in velar length and thickness. Greater velar length and greater velar thickness both were associated with complete velopharyngeal closure. Patients in the complete closure group tended to demonstrate large percent gains in either length or thickness or moderate gains in both. Patients in the incomplete closure group tended to demonstrate relatively small percent gains in both dimensions. Results suggest there may be important anatomic features (such as pharyngeal depth/velar length ratio) that can be evaluated before surgery to predict which patients may be most likely to benefit from Furlow Z-plasty as a form of treatment for velopharyngeal insufficiency.     

A neontological interpretation of conodont elements based on agnathan cyclostome tooth structire function, and development

Krejsa, R. J., Bringas, P. Jr. & Slavkin, H. C. 1990 10 15: A neontological interpretation of conodont elements based on agnathan cyclostome tooth structure, function, and development. Lethaia , Vol. 23, pp. 359–378. Oslo. ISSN 0024–1164.
Speculation about a conodont-cyclostome connection has led us to search for and establish a biological basis for various characteristic structures in conodont elements. Measurements of juvenile hagfish palatal and lingual teeth overlap those of representative conodont elements, demonstrating a size correspondence of conodonts with teeth of living vertebrates. When hagfish tooth histology is compared with internal and surface topography (SEM) of hagfish, keratinous teeth and mineralized conodont elements, microspaces and tubules similar to those found in hagfish functional tooth coverings and replacement elements are also found within the white matter' of conodont elements. It is provisionally suggested that the primary organic matrix of conodont elements could be keratin and/or keratin-related molecules, and that individual conodont elements could represent shed tooth coverings. The basal bodies' found in certain conodont elements could be replacement elements. These interpretations are contrary to several paradigms of orthodox conodontology. ▭ Agnatha, conodonts, cyclostomes, hagfish, keratin, paleo-biology, shedding, teeth .     

Hydrodynamic disturbances produced by small zooplankton: case study for the veliger larva of a bivalve mollusc

Zooplankton produce hydrodynamic disturbances during swimmingand feeding that enlarge their perceptive volume. From the standpointof both prey and predators, fluid disturbances increase theprobability that an organism is detected, identified and reactedto within appropriate time and space scales. Morphology andkinematics dictate the magnitude, symmetry and attenuation ofdisturbances in the fluid medium. Therefore, fluid disturbancesmay be species and age (size) specific. Normal and high-speedvideo microscopy was used to study flow-field generation byfree-swimming and tethered bivalve larvae. These organisms swimand feed using many highly coordinated and symmetrically distributedappendages (i.e. cilia). Larvae tethered in flow at variousfree stream velocities (U₀), simulating swimming activity, inducedparticle trajectories approximately parallel to the organism'sdorso-ventral axis. Velocity (v) and acceleration (a) were symmetricalin the transverse plane and asymmetrical in the vertical plane.Greatest velocity magnitudes ({small tilde}7, 3 and 6 mm s^–)occurred dorsal to the velum and attenuated with source distance(r) as 1/r, 1/r^1.9 and 1/r^2.9 at 10 s^– U₀ =, 3.1 and 6.4mm s^–1, respectively. For a larva in flow, but with velumretracted, simulating sinking, velocity attenuated at Mr towardsthe organism. Mean velocity gradients were on the order of 3,8 and 10 s^–1 for swimming, sinking and hovering larvae,respectively. The high-frequency (22 Hz) component of particlevelocity past free-swimming larvae was due to beat frequencyof the velar cilia. This attenuated rapidly with r leaving onlylow-frequency (1–3 Hz) disturbances 0.1 mm beyond thetips of the cilia. Comparisons of the kinetic energy dissipationrate for turbulence in coastal waters with the kinetic energyof laminar flow fields implied possible dominance of the flowfield of hovering, but not swimming, larvae to at least threebody diameters from the organism (–1 mm). These differencesin flow fields have important implications for larval survival.The perceptive volume of a hovering larva will be 40-fold greaterthan that of a swimming or sinking larva. However, a hoveringlarva U also more likely to be detected by a potential predatorthat uses mechanosensory organs to locate prey.