Anatomical, histochemical and immunohistochemical characterisation of the cardiac outflow tract of the silver arowana, Osteoglossum bicirrhosum (Teleostei: Osteoglossiformes)

Lorenzale, Miguel; López‐Unzu, Miguel A.; Fernández, M.C.; Durán, Ana C.; Fernández, Borja; Soto-Navarrete, María Teresa; Sans‐Coma, V.

doi:10.1016/j.zool.2016.09.004

Cited by 7 publications

(7 citation statements)

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“…The gross anatomy, histology, ultrastructure, embryology and physiology of the bulbus arteriosus of teleosts has generated a vast literature (see Icardo, and Lorenzale et al ., ). As expressed by Icardo (), the structure of this cardiac segment is highly variable, ‘close to being species‐specific.’…”

Section: Current Understandingmentioning

confidence: 97%

The anatomical components of the cardiac outflow tract of chondrichthyans and actinopterygians

et al. 2018

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The outflow tract of the fish heart is the segment interposed between the ventricle and the ventral aorta. It holds the valves that prevent blood backflow from the gill vasculature to the ventricle. The anatomical composition, histological structure and evolutionary changes in the fish cardiac outflow tract have been under discussion for nearly two centuries and are still subject to debate. This paper offers a brief historical review of the main conceptions about the cardiac outflow tract components of chondrichthyans (cartilaginous fish) and actinopterygians (ray-finned fish) which have been put forward since the beginning of the nineteenth century up to the current day. We focus on the evolutionary origin of the outflow tract components and the changes to which they have been subject in the major extant groups of chondrichthyans and actinopterygians. In addition, an attempt is made to infer the primitive anatomical design of the heart of the gnathostomes (jawed vertebrates). Finally, several areas of further investigation are suggested. Recent work on fish heart morphology has shown that the cardiac outflow tract of chondrichthyans does not consist exclusively of the myocardial conus arteriosus as classically thought. A conus arteriosus and a bulbus arteriosus, devoid of myocardium and mainly composed of elastin and smooth muscle, are usually present in cartilaginous and ray-finned fish. This is consistent with the suggestion that both components coexisted from the onset of the gnathostome radiation. There is evidence that the conus arteriosus appeared in the agnathans. By contrast, the evolutionary origin of the bulbus is still unclear. It is almost certain that in all fish, both the conus and bulbus develop from the embryonic second heart field. We suggest herein that the primitive anatomical heart of the jawed vertebrates consisted of a sinus venosus containing the pacemaker tissue, an atrium possessing trabeculated myocardium, an atrioventricular region with compact myocardium which supported the atrioventricular valves, a ventricle composed of mixed myocardium, and an outflow tract consisting of a conus arteriosus, with compact myocardium in its wall and valves at its luminal side, and a non-myocardial bulbus arteriosus that connected the conus with the ventral aorta. Chondrichthyans have retained this basic anatomical design of the heart. In actinopterygians, the heart has been subject to notable changes during evolution. Among them, the following two should be highlighted: (i) a decrease in size of the conus in combination with a remarkable development of the bulbus, especially in teleosts; and (ii) loss of the myocardial compact layer of the ventricle in many teleost species.

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Section: Current Understandingmentioning

confidence: 97%

The anatomical components of the cardiac outflow tract of chondrichthyans and actinopterygians

et al. 2018

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“…In addition to the characteristics of the ventricle, the bulbus arteriosus had numerous longitudinal ridges extending along its entire length, with two prominent main ridges, ventral and dorsal, connecting the distal portions of the conus valves. Lorenzale et al (2017) described the same arrangement in O. bicirrhosum and suggested that the elasticity of the ridges, combined with the presence of smooth muscle, allows the ridges to play an active role in opening and closing the valves. Since this arrangement has been found so far only in the bulbus arteriosus of A. gigas and O. bicirrhosum, both belonging to the monophyletic group of Osteoglossomorpha, the question arises as to whether this feature could be a synapomorphy of this group.…”

Section: Discussionmentioning

confidence: 85%

“…Lorenzale et al. () described the same arrangement in O. bicirrhosum and suggested that the elasticity of the ridges, combined with the presence of smooth muscle, allows the ridges to play an active role in opening and closing the valves. Since this arrangement has been found so far only in the bulbus arteriosus of A. gigas and O. bicirrhosum , both belonging to the monophyletic group of Osteoglossomorpha, the question arises as to whether this feature could be a synapomorphy of this group.…”

Section: Discussionmentioning

confidence: 91%

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Heart structure in the Amazonian teleost Arapaima gigas (Osteoglossiformes, Arapaimidae)

et al. 2018

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The fish heart ventricle has varied morphology and may have a specific morpho-functional design in species adapted to extreme environmental conditions. In general, the Amazonian ichthyofauna undergoes constant variations in water temperature, pH and oxygen saturation, which makes these species useful for investigations of cardiac morphology. Arapaima gigas, a member of the ancient teleost group Osteoglossomorpha, is one of the largest freshwater fish in the world. This species has a specific heart metabolism that uses fat as the main fuel when O 2 supplies are abundant but also can change to glycogen fermentation when O 2 content is limiting. However, no information is available regarding its heart morphology. Here, we describe the heart of A. gigas, with emphasis on the ventricular anatomy and myoarchitecture. Specimens of A. gigas weighing between 0.3 and 4040 g were grouped into three developmental stages. The hearts were collected and the anatomy analyzed with a stereomicroscope, ultrastructure with a scanning electron microscope, and histology using toluidine blue, Masson's trichrome and Sirius red stains. The ventricle undergoes morphological changes throughout its development, from the initial saccular shape with a fully trabeculated myocardium and coronary vessel restricted to the subepicardium (Type I) (group 1) to a pyramidal shape with mixed myocardium and coronary vessels that penetrate only to the level of the compact layer (Type II) (groups 2 and 3). The trabeculated myocardium has a distinct net-like organization in all the specimens, differing from that described for other teleosts. This arrangement delimits lacunae with a similar shape and distribution, which seems to allow a more uniform blood distribution through this myocardial layer.

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“…Gegenbaur () and Stöhr () pointed out that the anterior, generally single row of cardiac outflow tract valves of teleosts is morphologically equivalent to the first transverse row of chondrichthyans and early actinopterigyans (polypteriforms, acipenseriforms, lepisosteiforms and amiiforms). The outflow tract valves of teleosts are attached proximally to the conal myocardium and distally to the bulbus arteriosus (Guerrero et al, ; Lorenzale et al, ). Birds and mammals have normally three pocket‐like valves at the base of the aorta and pulmonary trunk, respectively.…”

Section: Discussionmentioning

confidence: 99%

The valves of the cardiac outflow tract of the starry ray, Raja asterias (Chondrichthyes; Rajiformes): Anatomical, histological and evolutionary aspects

Lorenzale

Fernández

Durán

et al. 2018

Anat Histol Embryol

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The cardiac outflow tract of chondrichthyans is composed of the myocardial conus arteriosus, equipped with valves at its luminal side, and the bulbus arteriosus devoid of myocardium. Knowledge of the histomorphology of the conal valves is scarce despite their importance in preventing blood backflow to the heart. Current information on the subject refers to a single shark species. The present report is the first to describe the structure of the conal valves of a batoid species, namely, Raja asterias. Hearts from seven starry rays were examined using scanning electron microscopy and histochemical techniques for light microscopy. In all hearts, the conus showed four transverse rows of three pocket‐like valves each. Each valve was composed of a leaflet and its supporting sinus. The leaflet had a stout central body, rich in glycosaminoglycans, which contained fibroblasts, collagen and elastin. The central body was surrounded by two thin fibrous layers, outer and inner, formed mainly by collagen. The valves of the anterior row, which were the largest of the valvular system, were attached proximally to the conus arteriosus and distally to the bulbus arteriosus, and not to the ventral aorta as previously reported for chondrichthyans. The arrangement of the anterior valves in the starry ray is an anatomical pattern that apparently has been preserved throughout the evolution of vertebrates.

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Anatomical, histochemical and immunohistochemical characterisation of the cardiac outflow tract of the silver arowana, Osteoglossum bicirrhosum (Teleostei: Osteoglossiformes)

Cited by 7 publications

References 44 publications

The anatomical components of the cardiac outflow tract of chondrichthyans and actinopterygians

The anatomical components of the cardiac outflow tract of chondrichthyans and actinopterygians

Heart structure in the Amazonian teleost Arapaima gigas (Osteoglossiformes, Arapaimidae)

The valves of the cardiac outflow tract of the starry ray, Raja asterias (Chondrichthyes; Rajiformes): Anatomical, histological and evolutionary aspects

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