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. 2020 Apr 27:11:260.
doi: 10.3389/fphys.2020.00260. eCollection 2020.

Morphology of the Amazonian Teleost Genus Arapaima Using Advanced 3D Imaging

Miriam Scadeng  1   2 , Christina McKenzie  3 , Weston He  1   4 , Hauke Bartsch  1   5 , David J Dubowitz  1   2 , Dominik Stec  1 , Judy St Leger  6
Affiliations

Morphology of the Amazonian Teleost Genus Arapaima Using Advanced 3D Imaging

Miriam Scadeng et al. Front Physiol. .

Abstract

The arapaima is the largest of the extant air-breathing freshwater fishes. Their respiratory gas bladder is arguably the most striking of all the adaptations to living in the hypoxic waters of the Amazon basin, in which dissolved oxygen can reach 0 ppm (0 mg/l) at night. As obligatory air-breathers, arapaima have undergone extensive anatomical and physiological adaptations in almost every organ system. These changes were evaluated using magnetic resonance and computed tomography imaging, gross necropsy, and histology to create a comprehensive morphological assessment of this unique fish. Segmentation of advanced imaging data allowed for creation of anatomically accurate and quantitative 3D models of organs and their spatial relationships. The deflated gas bladder [1.96% body volume (BV)] runs the length of the coelomic cavity, and encompasses the kidneys (0.35% BV). It is compartmentalized by a highly vascularized webbing comprising of ediculae and inter-edicular septa lined with epithelium acting as a gas exchange surface analogous to a lung. Gills have reduced surface area, with severe blunting and broadening of the lamellae. The kidneys are not divided into separate regions, and have hematopoietic and excretory tissue interspersed throughout. The heart (0.21% BV) is encased in a thick layer of lipid rich tissue. Arapaima have an unusually large telencephalon (28.3% brain volume) for teleosts. The characteristics that allow arapaima to perfectly exploit their native environment also make them easy targets for overfishing. In addition, their habitat is at high risk from climate change and anthropogenic activities which are likely to result is fewer specimens living in the wild, or achieving their growth potential of up to 4.5 m in length.

Keywords: MRI; air-breathing; arapaima; imaging; morphology; osteoglossid; pirarucu.

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Figures

FIGURE 1
FIGURE 1
Overview of specimen one. In all figures the traditional radiological convention is adopted with rostral end of fish to the left of the page for sagittal and coronal images and 3D reconstructions. For axial images, left side of image is right side of fish. Right (R), left (L), dorsal (D), ventral (V) marked for clarity. (A) 190 cm long female arapaima weighing 70.5 kg, volume of 68.85lt. The average density of the whole specimen is 1.02 g/cm3. Whole fish surface reconstructed from CT and MRI data (CT cranial 85% MRI caudal 15% as demarcated by blue arrows). (B) Semi transparent surface outline showing relative position of internal organs and skeleton reconstructed from CT data. Heart: purple, liver: brown, spleens: pink, ovary: magenta, esophagus and stomach: green, gut: turquoise, pyloric caeca: orange, respiratory tissue: blue, air in gas bladder: yellow, esophageal sphincter: red. Axial skeleton head and body surface: semi-transparent.
FIGURE 2
FIGURE 2
Respiratory system: The gill arches and filaments. (a) On each side there are four gill arches (GA) with associated cartilaginous filaments (F). (b) Photomicrograph of the boney gill arch, cartilaginous filaments. Note extensive blunting and broadening of the lamellae. (c) A higher magnification light micrograph of the lamellae of a gill filament. The epithelium of the lamellae is made up of ionocytes (filled arrowheads), mucocytes (empty arrowhead) and pavement cells (notched arrowhead). Note the collapse of the pillar cell system. (d) Coronal CT slice at level of the base of mouth demonstrating the gill arches and filaments. (e) 3D reconstruction of gill arches (blue) from CT as seen from caudal end of fish looking cranially into the fish.
FIGURE 3
FIGURE 3
Respiratory system: Esophageal Sphincter. (a) Midline sagittal, and (b,c) axial MRI image at level of upper esophagus through the muscular sphincter (MS), positioned in the dorsal aspect of the esophagus. White box on (b) indicates enlarged section (c). The sphincter is a triangular, disc-like shaped muscle through which air moves between the esophagus and the rostral aspect of the gas bladder (GB), which is not inflated at this level. A tiny longitudinal strip of tissue seen overlying the opening (yellow arrow in c), may act as a valve regulating the flow of air, or preventing water/food from entering the GB. In addition a localized thickening of tissue (red arrow) sited on the opposing side of the esophagus, possibly occludes the slit opening when the surfaces of the esophagus are opposed. (d,e) 3D reconstruction of muscular sphincter from CT data demonstrating relationship between the esophagus and the GB. Red: muscular sphincter, blue: rostral end of GB, green: esophagus, yellow: strip of tissue in valve opening. (d) From above sphincter, (e) from below sphincter, (f) lateral view.
FIGURE 4
FIGURE 4
Respiratory system: Respiratory gas bladder. (a) The gas bladder (GB) and respiratory tissue (RT) runs the length of the dorsal coelomic cavity and encompasses the kidneys (K). (b) The dorsal surface is covered by a mat of highly vascular tissue comprising of ediculae and inter-edicular septa. The inter-edicular septa are created by trabeculae made of smooth muscle and connective tissue. The interior surfaces of the gas bladder that are in contact with air are all covered with respiratory epithelium consisting of pavement and columnar epithelial cells. (c,d) A light micrograph stained with Masson’s Trichrome showing a blood vessel (BV), inter-edicular septa (IES) and ediculae (E). Collagen is stained blue. (e,f) Axial and zoomed axial MRI of respiratory tissue at level of mid of the GB demonstrating respiratory tissue (RT), gas in air bladder (A), Gas in stomach (G). The kidneys (K) are seen suspended in the GB, vertebrae (V) and gut (GU). Vertebral bodies appear to have spicules emanating from them (red arrow) – Similar appearance seen on CT in Figure 10. This feature is presumably to increase surface area for gas exchange and have not previously been described in this species. (g) Coronal CT scan at level of GB demonstrating relationships of contents of GB. (h–j) 3D reconstructions from CT data. (h) Air (A) fraction in GB (yellow), (i) Vascular respiratory tissue fraction (blue). (j) Reconstructions of GB showing the relationship of A to RT.
FIGURE 5
FIGURE 5
Ovary and kidneys. (a) Gross anatomy of ovary (O) in the peritoneal cavity. (b) Kidney- light micrograph showing hematopoietic tissue (H), renal tubules (T), capillary tuft (arrowhead) and melanomacrophages (empty arrowhead). (c) 3D reconstruction from CT data of kidneys (green) and ovary (magenta) as seen from left side and (d) from below looking up. Other organs as described above but semitransparent for orientation.
FIGURE 6
FIGURE 6
The heart. (a,b,d) The heart consists of the sinus venosus (SV), the atrium (At), the ventricle (V) and the bulbus arteriosis (BA). Some of the substantial lipid rich connective tissue that surrounds the heart can be seen (L). (c) Photomicrograph of the ventricular myocardium. (d) Sagittal MRI of the heart showing the ductus of Cuvier (arrowhead) connecting to the sinus venosus. A small amount of pericardial effusion (PE) can be seen at the apex of the heart. (e–i) e-3D reconstruction of heart superimposed on axial MRI for orientation of heart. (f) Ventral (seen from below), (g) Dorsal (from above), (h) Left lateral, (i) Right Lateral. Hepatic vein: yellow, sinus venosus: light blue), atrium: dark blue, ventricle: red, bulbus arteriosus: purple.
FIGURE 7
FIGURE 7
The digestive system. (a) Abdominal cavity with liver (L) and gut (G). (b) Several spleens. (c) Light micrograph of liver showing a bile duct (BD), blood vessel (BV), sinusoids (arrowhead) and hepatocytes (top half of image). (d,e) Sagittal midline and axial CT slice through head demonstrating how effective crushing of prey occurs between boney tongue and roof of mouth. (f) 3D reconstruction of head looking into mouth highlighting boney tongue (green). (g,h) 3D model of gut and liver reconstructed from CT data. The gut of the osteoglossomorpha is distinct from that of other fishes in that the intestine passes posteriorly to the left of the esophagus and stomach (Nelson, 1972) rather than to the right. (g) left lateral, (h) Right lateral. Esophagus and stomach: green, intestinal loops: turquoise, blind ending pyloric caeca originating from proximal gut: orange, liver: brown, spleens pink.
FIGURE 8
FIGURE 8
(a) Photomicrograph showing the cerebellum (Ce), medulla (M), optic tectum (OT), valvula cerebelli (VC) and telencephalon (Te). (b) Sagittal midline T2 MR image through brain showing the cerebellum, optic tectum, telencephalon, olfactory bulb (OB), pituitary (P), spinal cord (SC) and medulla. Surrounding high signal is expansive cerebro-spinal fluid (CSF) space in which the brain is suspended. (c,d) Dorsal and lateral view 3D reconstructions of the head from CT data showing the extent of the CSF space encasing the brain (green), optic nerves (blue) and olfactory nerves (orange). Eyes are red, and lining of olfactory pits yellow. Other bony head structures are semi transparent head. (e–i) 3D reconstructions of the brain with large and complex CSF space surrounding brain (semitransparent surface). (e) Dorsal, (f) Ventral, (g) lateral, (h) anterior, and (i) Posterior view. Olfactory bulbs: green, telencephalon: dark yellow, hypothalamus: brown, optic tectum: blue, cerebellum: light yellow, medulla and proximal spinal cord: red, and proximal optic tract: turquoise.
FIGURE 9
FIGURE 9
Musculoskeletal -Head. (A–C) 3D reconstructions from CT data, of the external bony armor plates of the head with integument overlain as transparent surface. Abbtp, anterior basibranchial toothplate; ang, angular; ant, antorbital; br, branchiostegal rays; chy, Ceratohyal; cl; d, dentary; dsp, dermosphenotic; fr, frontal; io 1–4, infraorbital 1–4; iop, interopercular; iop, infraopercular; mx, maxilla; n, nasal; op, opercle; pa, parietal; pmx, premaxilla; pop, preopercle; q, quadrate; s, suture; sop, subopercle; spop, suprapreopercle; u, urohyal; v, vomer. (Bones referenced as per Steward 2013).
FIGURE 10
FIGURE 10
Musculoskeletal and Integument. (a) Axial CT at level of GB demonstrating air partially encased between the bony cortices of the transvers processes of the vertebral bodies, and (b,c) shows spiculation of the vertebral body, possibly to increase surface area of respiratory epithelium exposed to air. (d) 3D rendering of vertebrae on background of coronal CT slice showing air density within part of the in the vertebral body between spicules. (e) Axial CT section demonstrating flexible dermal armor of elasmoid scales made from overlapping layers of type 1 collagen and a highly mineralized hydroxyapatite outer layer (Yang et al., 2014). Scales overlap with a thickness up to 9.7 mm. Single scale thickness is approximately 3.4 mm. (f,g) The muscle is divided in to left and right epaxial and hypaxial muscle by the vertical and horizontal septa. (h) Bony axial skeleton reconstructed from CT data (excluding distal tail).
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