Hydraulic control of tuna fins: A role for the lymphatic system in vertebrate locomotion

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Science  21 Jul 2017:
Vol. 357, Issue 6348, pp. 310-314
DOI: 10.1126/science.aak9607
  • Fig. 1 Morphology of the musculo-vascular system in Pacific bluefin tuna median fins.

    (A) Cross section of the second dorsal fin (SDF) sinus. Top left inset: A dissecting scope image of the SDF cross section. Bar, 1 mm. Abbreviations: fin rays (FR), expandable vascular channels (VC), incompressible chamber of the vascular sinus (VS), scales (SC), inclinator muscles (IM) surround lateral vessels connected with VS, epaxial musculature (EPM), proximal parts of pterygiophores (PT), erector muscles (ERM), and depressor muscles (DM). (B) Cross section of the depressed (left) and erected (right) SDF shows collapsed and expanded VC between fin rays. (C) Three-dimensional structure of the musculo-vascular system in SDF. PT and some FR have been removed for illustrative purposes. FR, connective tissue (CT) sheath between skin and IM, EPM, and compressible vascular channels (CVC) continue around the first dorsal fin (FDF). (D) Cross section of the FDF. FR of the folded FDF in the groove on the fish’s back, CVC beneath the SC layer, IM, ERM and DM, and EPM. (E) Blue Microfil injection into the incompressible chamber of the VS at the base of the SDF; skin with the scales has been removed. Bar, 2 cm. FR of the erected FDF, CVC around the FDF, and connection of the CVC with the VS incompressible chamber at the base of the SDF; blue Microfil compound injected into the sinus reveals the expanded vascular channels between FR of the SDF.

  • Fig. 2 Biomechanics and hydrodynamics of tuna median fins.

    (A and B) Schematic of the hydraulic effect in the second dorsal fin (SDF) of tuna. (A) Depressed fin: compressible vascular channels (CVC), fin rays (FR), expandable vascular channels (VC) between the FR, relaxed inclinator muscles (IM), and incompressible chamber with vascular sinus (VS). (B) Erected fin: solid arrows indicate collapsed CVC caused by contraction of the IM. Dashed arrow indicates outflow of liquid from CVC to the VS and VC. (C) Isometric view of a CAD model of tuna shows the simulated flow pattern associated with the SDF and anal fin (AF) at 6 m/s and a yaw angle of 11°. (D and E) Top view of a tuna CAD model shows the velocity V, lift vector L, and drag vector D; α is the yaw angle formed by the fin plane and the velocity vector. (D) Enlarged view of the second dorsal fin without associated flow.

  • Fig. 3 Vascular sinuses of median fins are connected to the lymphatic system.

    (A) Blood and lymphatic vessels after blue Microfil injection into the VS of the anal fin. Internal lining of the peritoneal cavity (left), H&E histological section of the lining of the peritoneal cavity (right). Examples of arteries, veins, and vessels staining positive for Microfil; melano-macrophage centers (MMCs) are labeled. Bars, 1 cm (left panel); 150 μm (right panel). (B) Image of longitudinal section of VS. Veins and MMCs in the endothelium of the VS are labeled; ruler in mm. (C) Cells were isolated from the VS, blood, and spleen. Upper panels, live cells; lower panels, methanol-fixed and Giemsa-stained cells. Examples of the main three cell types are labeled: red blood cells, lymphocytes, and myeloid cells. Bars, 40 μm. (D) Hematocrit analysis of the VS liquid (left) and blood (right). Plasma, hematocrit (RBCs), and buffy coat (white blood cells and platelets) are labeled. (E) Cells were isolated from blood (left) and the VS (right) and analyzed by flow cytometry using forward scatter (FSC) and side scatter (SSC) for populations of RBCs, lymphocytes, and myeloid cells. (F and G) Cells were cocultured with beads and analyzed by green fluorescence for phagocytosis and FL4 (unstained). Representative analysis of blood samples with gated positive cells (left) and VS (right). (G) Normalized analysis of fold change of cells positive for phagocytosis from three different experiments. *P <0.005, single-factor ANOVA.

  • Fig. 4 The lymphatic sinus in the Scombridae family.

    (A) Dissecting scope images of sections taken from the base of the second dorsal fin from Pacific mackerel, Spanish mackerel, bonito, and yellowfin tuna. The vascular sinus (VS) is labeled in Spanish mackerel, bonito, and yellowfin tuna with a black arrow but is not detected in Pacific mackerel. Bars, 1 mm. (B) Hypothesized development of the VS in the Scombridae family cladogram. The cladogram of the four scombridae tribes is reproduced with permission from a whole–mitochondrial genome analysis (22), based on 18 species of scombroid fishes. Hypothesized development of the vascular sinus based on the detection of VS in two species of Thunnini tribe (Thunnus albacares and Thunnus orientalis), one species of Sardini tribe (Sarda chiliensis), and one species of Scomberomorini tribe (Scomberomorus sierra) and the lack of the VS in one species of Scombrini tribe (Scomber australasicus).

Supplementary Materials

  • Hydraulic control of tuna fins: A role for the lymphatic system in vertebrate locomotion

    Vadim Pavlov, Benyamin Rosental, Nathaniel F. Hansen, Jody M. Beers, George Parish, Ian Rowbotham, Barbara A. Block

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods 
    • Figs. S1 to S9 
    • Tables S1 to S3 
    • Captions for Movies S1 and S2 
    • Captions for Tables S4 and S5 
    • References 
    Table S4
    Measurements data of swimming behavior and median fins erection of captive bluefin tuna in TRCC, in Excel spreadsheet.
    Table S5
    CFD flow simulation data of the Pacific bluefin tuna model median fins performance, in Excel spreadsheet.

    Images, Video, and Other Media

    Movie S1
    Examples of erected and depressed median fins related with tuna swimming behaviors taken at the Tuna Research and Conservation Center with a Phantom camera.
    Movie S2
    In-vitro experiment on the hydraulic effect on the second dorsal fin of Pacific bluefin tuna.

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