This study indicates that the development of the vertebrae in the Atlantic salmon requires the orchestration of two sources of metameric patterning, derived from the notochord and the somite rows, respectively. Before segmentation of the salmon notochord, chordoblasts exhibit a well-defined cell axis that is uniformly aligned with the cranio-caudal axis. The morphology of these cells is characterised by a foot-like basal projection that rests on the notochordal sheath. Notochordal segments are initially formed within the chordoblast layer by metameric change in the axial orientation of groups of chordoblasts. This process results in the formation of circular bands of chordoblasts, with feet perpendicular to the cranio-caudal axis, the original chordoblast orientation. Each vertebra is defined by two such chordoblast bands, at the cranial and caudal borders, respectively. Formation of the chordoblast segments closely precedes formation of the chordacentra, which form as calcified rings within the adjacent notochordal sheath. Sclerotomal osteoblasts then differentiate on the surface of the chordacentra, using them as foundations for further vertebral growth. Thus, the morphogenesis of the rudiments of the vertebral bodies is initiated by a generation of segments within the chordoblast layer. This dual segmentation model for salmon, in which the segmental patterns of the neural and haemal arches are somite-derived, while the vertebral segments seem to be notochord-derived, contrasts with current models for avians and mammals.
The teleost backbone consists of amphicoelous vertebrae and intervertebral ligaments, both of which include notochord-derived structures. On the basis of a sequential developmental study of the vertebral column of Atlantic salmon ( Salmo salar L.) from the egg stage up to early fry stage (300-2500 day-degrees) we show that the vertebral body consists of four layers or compartments, two of which are formed through mineralization of preformed collagenous tissue (the notochordal sheath and the intervertebral ligament) and two of which are formed through ossification. The three inner layers have ordered lamellar collagen matrixes, which alternate perpendicularly from layer to layer, whereas the outer layer consists of cancellous bone with a woven matrix. The bone layers also differ in osteocyte content. In this study we describe the structural details of the layers, and their modes of formation.The results are compared with previous descriptions, and possible phylogenetic implications are discussed.
This study investigates the effect of different smolt production strategies on vertebral morphology (radiology), composition (mineral content) and mechanical strength (load-deformation testing) in Atlantic salmon (Salmo salar). Rapid-growing underyearling (0+) smolt were compared with slower-growing yearling (1+) smolt and a reference group of wild smolt (w). The underyearling and yearling smolt were transferred to seawater in October 2002 and May 2003, respectively. The underyearling smolt were reared under continuous light and the yearling smolt under natural light during the first twelve weeks in seawater, at ambient temperatures. Thus, the underyearling smolt hit seawater at 13 °C and were reared at 10-13 °C during the early seawater phase, whereas the yearling smolt hit seawater at 7 °C and were reared at 7-10 °C during the early seawater phase. All groups displayed increased longitudinal growth (up to 9% increase in relative length) of the caudal vertebrae during parr-smolt transformation. However, at transfer to seawater, the underyearling smolt had significantly lower vertebral mineral content (0+ 44%, 1+ 47%, w 50%) and higher incidence of deformed vertebrae (0+ 1.5%, 1+ 0%, w 0%), and at twelve weeks after transfer to seawater significantly lower vertebral mineral content (0+ 36%, 1+41%, w 43%), yield-load (0+6492 g, 1+8797 g, w 9150 g) and stiffness (0+7578 g/mm, 1+ 15,161 g/mm, w 20,523 g/mm), and significantly higher incidence of deformed vertebrae (0+ 2.5%, 1+ 0.3%, w 0%). There was a significant correlation between the mineral content and mechanical properties of the vertebrae. The underyearling smolt had significantly elevated plasma concentrations of total Ca, and P and Ca2+ during the parr-smolt transformation and in the early seawater phase.The results show that underyearling smolt may have an increased risk of developing vertebral deformities. It is possible that this risk can be reduced by postponing the start of the short-day treatment. This will reduce the temperature during smoltification, the temperature and daylength during the early seawater phase, and increase the age at smoltification.
Reared larval and juvenile Atlantic halibut H~ppoglossus hippoglossus collected during incidences of mass mortality in 2 hatcheries were studied by light and electron microscopy. A vacuolating encephalopathy and retinopathy as well as endocardial lesions were observed. By transmission electron microscopy isometric, spherical, unenveloped virus particles with mean capsid diameters of approximately 25 nm were detected. The virions were found intracytoplasmically in semicrystalline arrays or as membrane-associated aggregates and single particles. Infection could be observed in neurons, astrocytes, oligodendrocytes, microglia/macrophages, lymphocyte-like cells, vascular endothelium, endocardial endothelium, myocardial myocytes and in the mesothelium of the epicardium. Specific immunolabeling was obtained in affected tissues on immunohistochemistry applying primary antisera against nodaviruses isolated from the striped jack Pseudocaranx dentex and the sea bass Dicentrarchus labrax. We suggest that the mortality was caused by a nodavirus-like agent and that this disease of the Atlantic halibut is closely related to diseases termed viral nervous necrosis (VNN), viral encephalopathy and retinopathy, and fish encephalitis, which have been associated with mass mortality in numerous cultured marine teleost species. In Atlantic halibut, viral endocardial lesions were a constant finding, suggesting that viremia may be an important factor in the pathogenesis of the infection.
ABSTRACT. The susceptibility of the Atlantic halibut Hjppoglossus hippoglossus yolk-sac larvae to viral encephalopathy and retinopathy (VER) was investigated by waterborne challenge experiments with nodavuus. Transfer of VER was inhcated by several hnes of evidence. A sigluficantly higher cumulative mortality was observed after challenge with virus compared to mock challenge, and increasing doses of vlrus resulted in shorter incubation periods. When the challenge was performed on the day after hatchmg, the time from inoculation to the time when 50% of the larvae were dead (LT,,) ranged from 26 to 32 d. Postponement of challenge for 13 d reduced the LT,, to 14 d, inhcating that the susceptibility of the larvae to the present nodavirus strain was low during the first 2 wk after hatching. The progression of the infect~on was monitored by sequential unmunohistochemistry and electron mcroscopy. On Day 18 after hatching the initial signs of infection were observed as a prominent focus of immunolabelling in the caudal part of the brain stem. In the same larvae irnrnunolabelled single cell lesions were observed in the stratified epithelium of the cranial part of the intestine. The portal of entry into the larvae may thus have been the intestinal epithelium, while the route of infection to the CNS may have been axonal transport to the brain stem through cranial nerves such as the vagus nerves. Later in the infection, lesions became more severe and widespread and were also found throughout the b r a~n and spinal cord and in the retina, cranial ganglia, intestme, liver, olfactory epithelium, yolk-sac epithelium, gills and pectoral fins. The mortality in all virus-challenged groups was 100%. This study thus demonstrates that the present nodavirus strain is able to replicate and cause VER in Atlantic halibut yolk-sac larvae at temperatures as low as 6°C
This study describes the long-term effects of surgical ablation of the pineal gland on the spine of 3-yr-old Atlantic salmon (Salmo salar L.) with a mean weight of 3.2 kg. Radiographic examinations showed that 82% of the pinealectomized fish developed marked lateral (scoliosis) and dorso-ventral spinal curvatures. The proportions of the individual vertebral bodies and their mechanical properties were also altered. The stiffness, yield limit and resilience of the vertebral bodies, as measured by compression in the cranio-caudal direction, were significantly lower in the pinealectomized than in the sham-pinealectomized group. Calcium, phosphorous and total mineral content of the vertebral bodies were also significantly lower in the pinealectomized fish, while these parameters were similar in scales in the two groups. Alterations of the spinal curve accompanied by changes in the proportions, mechanical strength and mineral content of the vertebral bodies of the pinealectomized salmon indicate that melatonin has several functions related to vertebral bone growth. As the lesions found in salmon are similar to the spinal malformations observed in avian species and mammals after pinealectomy, this study strengthens the hypothesis of a phylogenetically conserved function of the pineal gland related to skeletal development.
The notochord constitutes the main axial support during the embryonic and larval stages, and the arrangement of collagen fibrils within the notochord sheath is assumed to play a decisive role in determining its functional properties as a fibre-wound hydrostatic skeleton. We have found that during early ontogeny in Atlantic salmon stepwise changes occur in the configuration of the collagen fibre-winding of the notochord sheath. The sheath consists of a basal lamina, a layer of type II collagen, and an elastica externa that delimits the notochord; and these constituents are secreted in a specific order. Initially, the collagen fibrils are circumferentially arranged perpendicular to the longitudinal axis, and this specific spatial fibril configuration is maintained until hatching when the collagen becomes reorganized into distinct layers or lamellae. Within each lamella, fibrils are parallel to each other, forming helices around the longitudinal axis of the notochord, with a tangent angle of 75-80 ° to the cranio-caudal axis.The helical geometry shifts between adjacent lamellae, forming enantiomorphous left-and right-handed coils, respectively, thus enforcing the sheath. The observed changes in the fibre-winding configuration may reflect adaptation of the notochord to functional demands related to stage in ontogeny. When the vertebral bodies initially form as chordacentra, the collagen lamellae of the sheath in the vertebral region are fixed by the deposition of minerals; in the intervertebral region, however, they represent a pre-adaptation providing torsional stability to the intervertebral joint. Hence, these modifications of the sheath transform the notochord per se into a functional vertebral column. The elastica externa, encasing the notochord, has serrated surfaces, connected inward to the type II collagen of the sheath, and outward to type I collagen of the mesenchymal connective tissue surrounding the notochord. In a similar manner, the collagen matrix of the neural and haemal arch cartilages is tightly anchored to the outward surface of the elastic membrane. Hence, the elastic membrane may serve as an interface between the notochord and the adjacent structures, with an essential function related to transmission of tensile forces from the musculature. The interconnection between the notochord and the myosepta is discussed in relation to function and to evolution of the arches and the vertebra. Contrary to current understanding, this study also shows that notochord vacuolization does not result in an increased elongation of the embryo, which agrees with the circular arrangement of type II collagen that probably only enables a restricted increase in girth upon vacuolization, not aiding elongation. As the vacuolization occurs during the egg stage, this type of collagen disposition, in combination with an elastica externa, also probably facilitates flexibility and curling of the embryo.
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