Abstract
Teleost scales are extremely diverse in morphology, with different categories (cycloid, crenate, spinoid, ctenoid) once used to define major groups of fish. We describe these different classical categories of scales and discuss the structure and potential function of small features of scale morphology such as spines, ctenii, radii, and circuli. Modern techniques now make analysis of scale morphology using three-dimensional quantitative data possible. This ability is crucial because many of the hydrodynamic and protective hypotheses concerning the function of scales are dependent on three-dimensional structure. We discuss different techniques to investigate and image the structure of fish scales and skin, and we highlight gel-based surface profilometry as a new valuable tool for studying fish skin. In addition to bony scales, fish skin is also covered by an epidermis that secretes mucus that can coat the exterior of scales. Fish scales are often studied in isolation with the epidermis removed; here we present topographic, three-dimensional, analyses of fish skin surfaces from seven species with the mucus, epidermis, and relative positions of scales intact. We compare these images qualitatively and quantitatively to the same individuals with the epidermis and mucus removed to show a previously unexplored axis of diversity in fish: how mucus and epidermis interact with scale morphology to create surface texture. The three-dimensional structure of fish skin has important implications for hydrodynamic function during locomotion, but this remains a largely unexplored area.
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References
Aleyev, Y. G. (1977). Nekton. Hague: Dr. W. Junk b.v. Publishers.
Anderson, E. J., McGillis, W. R., & Grosenbaugh, M. A. (2001). The boundary layer of swimming fish. The Journal of Experimental Biology, 204, 81–102.
Batts, B. S. (1964). Lepidology of the adult pleuronectiform fishes of Puget Sound, Washington. Copeia, 4, 666–673.
Beardsley, G. L. (1967). Age, growth, and reproduction of the Dolphin, Coryphaena hippurus, in the Straits of Florida. Copeia, 1967, 441.
Bereiter-Hahn, J., & Zylberberg, L. (1993). Regeneration of teleost fish scale. Comparative Biochemistry and Physiology, 105A, 625–641.
Bergman, J. N., Lajeunesse, M. J., & Motta, P. J. (2017). Teeth penetration force of the tiger shark Galeocerdo cuvier and sandbar shark Carcharhinus plumbeus. Journal of Fish Biology, 91, 460–472.
Bernadsky, G., Sar, N., & Rosenberg, E. (1993). Drag reduction of fish skin mucus: Relationship to mode of swimming and size. Journal of Fish Biology, 42, 797–800.
Besseau, L., & Bouligand, Y. (1998). The twisted collagen network of the box-fish scutes. Tissue & Cell, 30, 251–260.
Bone, Q. (1972). Buoyancy and hydrodynamic functions of integument in the Castor oil fish, Ruvettus pretiosus (Pisces: Gempylidae). Copeia, 1972, 78–87.
Browning, A., Ortiz, C., & Boyce, M. C. (2013). Mechanics of composite elasmoid fish scale assemblies and their bioinspired analogues. Journal of the Mechanical Behavior of Biomedical Materials, 19, 75–86.
Burdak, V. D. (1986). Morphologie fonctionnelle du tegument ecailleux des poissons. Cybium, 10, 1–128.
Casselman, J. M. (1990). Growth and relative size of calcified structures of fish growth and relative size of calcified structures of fish. Transactions of the American Fisheries Society, 119, 673–688.
Chintapalli, R. K., Mirkhalaf, M., Dastjerdi, A. K., & Barthelat, F. (2014). Fabrication, testing and modeling of a new flexible armor inspired from natural fish scales and osteoderms. Bioinspiration & Biomimetics, 9, 36005.
Daniel, T. L. (1981). Fish mucus: In situ measurements of polymer drag reduction. The Biological Bulletin, 160, 376–382.
Daniels, R. A. (1996). Guide to the identification of scales of inland fishes of northeastern North America. New York State Museum Bulletin, 488, 1–93.
Dapar, M. L. G., Torres, M. A. J., Fabricante, P. K., & Demayo, C. G. (2012). Scale morphology of the Indian goatfish, Parapeneus indicus (Shaw, 1803) (Perciformes: Mullidae). Advance Envirronmental Biologico, 6, 1426–1432.
Descamps, E., Sochacka, A., de Kegel, B., Van Loo, D., Hoorebeke, L., & Adriaens, D. (2014). Soft tissue discrimination with contrast agents using micro-ct scanning. Belgian Journal of Zoology, 144, 20–40.
Duro-Royo, J., Zolotovsky, K., Mogas-Soldevila, L., Varshney, S., Oxman, N., Boyce, M. C., & Ortiz, C. (2015). MetaMesh: A hierarchical computational model for design and fabrication of biomimetic armored surfaces. Computer-Aided Design, 60, 14–27.
Esmaeili, H. R., Gholamifard, A., Zarei, N., & Arshadi, A. (2012). Scale structure of a cyprinid fish, Garra rossica (Nikol’skii, 1900) using scanning electron microscope (SEM). International Journal of Science, Technology and Society, 4, 487–492.
Esteban, M. Á. (2012). An overview of the immunological defenses in fish skin. ISRN Immunology, 2012, 1–29.
Fast, M. D., Sims, D. E., Burka, J. F., Mustafa, A., & Ross, N. W. (2002). Skin morphology and humoral non-specific defence parameters of mucus and plasma in rainbow trout, coho and Atlantic salmon. Comparative Biochemistry and Physiology A, 132, 645–657.
Ghosh, R., Ebrahimi, H., & Vaziri, A. (2014). Contact kinematics of biomimetic scales. Applied Physics Letters. 105, 233701-1-233701-5.
Gignac, P. M., Kley, N. J., Clarke, J. A., Colbert, M. W., Morhardt, A. C., Cerio, D., Cost, I. N., Cox, P. G., Daza, J. D., Early, C. M., et al. (2016). Diffusible iodine-based contrast-enhanced computed tomography (diceCT): An emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. Journal of Anatomy, 228, 889–909.
Hawkes, J. W. (1974). The structure of fish skin I. General organization. Cell and Tissue Research, 149, 147–158.
Hill, K. T., Cailliet, G. M., & Radtke, R. L. (1989). A comparative analysis of growth zones in four calcified structures of Pacific Blue Marlin, Makaira nigricans. Fishery Bulletin, 87, 829–843.
Huysseune, A., & Sire, J.-Y. (1998). Evolution of patterns and processes in teeth and tooth-related tissues in non-mammalian vertebrates. European Journal of Oral Sciences, 106, 437–481.
Ibañez, A. L., Cowx, I. G., & O’Higgins, P. (2007). Geometric morphometric analysis of fish scales for identifying genera, species, and local populations within the Mugilidae. Canadian Journal of Fisheries and Aquatic Sciences, 1100, 1091–1100.
Ibañez, A. L., Cowx, I. G., & O’Higgins, P. (2009). Variation in elasmoid fish scale patterns is informative with regard to taxon and swimming mode. Zoological Journal of the Linnean Society, 155, 834–844.
Jawad, L. A. (2005). Comparative scale morphology and squamation patterns in triplefins (Pisces: Teleostei: Perciformes: Tripterygiidae). Tuhinga, 16, 137–167.
Jawad, L. A., & Al-Jufaili, S. M. (2007). Scale morphology of greater lizardfish Saurida tumbil (Bloch, 1795) (Pisces: Synodontidae). Journal of Fish Biology, 70, 1185–1212.
Jimenez, J. (2004). Turbulent flows over rough walls. Annual Review of Fluid Mechanics, 36, 173–196.
Johal, M. S., Esmaeili, H. R., & Sharma, M. L. (2006). Scale structure of a cobitid fish, Cobitis linea (Heckel, 1849) using different modes of SEM. Current Science, 91, 1464–1466.
Johnson, M.K. and Adelson, E.H. (2009). Retrographic sensing for the measurement of surface texture and shape. In: 2009 IEEE Conference on Computer Vision and Pattern Recognition, 1070–1077.
Johnson, M. K., Cole, F., Raj, A., & Adelson, E. H. (2011). Microgeometry capture using an elastomeric sensor. ACM Transactions on Graphics, 30, 46.
Lauder, G. V., Wainwright, D. K., Domel, A. G., Weaver, J., Wen, L., & Bertoldi, K. (2016). Structure, biomimetics, and fluid dynamics of fish skin surfaces. Physical Review Fluids, 1, 060502.
Li, R., & Adelson, E. H. (2013). Sensing and recognizing surface textures using a GelSight sensor. In: 2013 IEEE Conference on Computer Vision and Pattern Recognition, pp. 1241–1247.
Liyan, W. U., Zhibin, J., Yuqiu, S., Wentao, R., Shichao, N., & Zhiwu, H. (2017). Water-trapping and drag-reduction effects of fish Ctenopharyngodon idellus scales and their simulations. Science China Technological Sciences, 60, 1111–1117.
Long, J. H., Hale, M. E., McHenry, M. J., & Westneat, M. W. (1996). Functions of fish skin: Flexural stiffness and steady swimming of longnose gar Lepisosteus osseus. The Journal of Experimental Biology, 199, 2139–2151.
Margraf, F. J., & Riley, L. M. (1993). Evaluation of scale shape for identifying spawning stocks of coastal Atlantic striped bass (Morone saxatilis). Fisheries Research, 18, 163–172.
Meunier, F. J. (1981). “Twisted plywood” structure and mineralization in the scales of a primitive living fish Amia calva. Tissue & Cell, 13, 165–171.
Meunier, F. J. (2011). The Osteichtyes, from the Paleozoic to the extant time, through histology and palaeohistology of bony tissues. Comptes Rendus Palevol, 10, 347–355.
Meunier, F. J., & Brito, P. M. (2004). Histology and morphology of the scales in some extinct and extant teleosts. Cybium, 28, 225–235.
Meyer, W., & Seegers, U. (2012). Basics of skin structure and function in elasmobranchs: A review. Journal of Fish Biology, 80, 1940–1967.
Motta, P., Habegger, M. L., Lang, A., Hueter, R., & Davis, J. (2012). Scale morphology and flexibility in the shortfin mako Isurus oxyrinchus and the blacktip shark Carcharhinus limbatus. Journal of Morphology, 273, 1096–1110.
Rakers, S., Gebert, M., Uppalapati, S., Meyer, W., Maderson, P., Sell, A. F., Kruse, C., & Paus, R. (2010). “Fish matters”: The relevance of fish skin biology to investigative dermatology. Experimental Dermatology, 19, 313–324.
Roberts, C. D. (1993). Comparative morphology of spined scales and their phylogenetic significance in the Teleostei. Bulletin of Marine Science, 52, 60–113.
Rosen, M. W., & Cornford, N. E. (1971). Fluid friction of fish slimes. Nature, 234, 49–51.
Sagong, W., Kim, C., Choi, S., Jeon, W.-P. and Choi, H. (2008). Does the sailfish skin reduce the skin friction like the shark skin? Physics of Fluids, 20, 101510-1-101510-10.
Sankar, S., Sekar, S., Mohan, R., Rani, S., Sundaraseelan, J., & Sastry, T. P. (2008). Preparation and partial characterization of collagen sheet from fish (Lates calcarifer) scales. International Journal of BIological Macromolecules, 42, 6–9.
Schönbörner, A. A., Boivin, G., & Baud, C. A. (1979). The mineralization processes in teleost fish scales. Cell and Tissue Research, 202, 203–212.
Schultz, M. P., & Flack, K. A. (2007). The rough-wall turbulent boundary layer from the hydraulically smooth to the fully rough regime. Journal of Fluid Mechanics, 580, 381.
Shephard, K. L. (1994). Functions for fish mucus. Reviews in Fish Biology and Fisheries, 4, 401–429.
Sire, J.-Y. (1986). Ontogenic development scales in a cichlid Hemichromis bimaculatus (Cichlidae). Journal of Fish Biology, 28, 713–724.
Sire, J.-Y., & Akimenko, M.-A. (2004). Scale development in fish: A review, with description of sonic hedgehog (shh) expression in the zebrafish (Danio rerio). The International Journal of Developmental Biology, 48, 233–247.
Sire, J.-Y., & Arnulf, I. (1990). The development of squamation in four Teleostean fishes with a survey of the literature. Jpn. Journal of Ichthyology, 37, 133–143.
Sire, J., & Arnulf, I. (2000). Structure and development of the ctenial spines on the scales of a teleost fish, the cichlid Cichlasoma nigrofasciatum. Acta Zoologica, 81, 139–158.
Sire, J.-Y., & Huysseune, A. (2003). Formation of dermal skeletal and dental tissues in fish: A comparative and evolutionary approach. Biological Reviews of the Cambridge Philosophical Society, 78, 219–249.
Smits, A. J. (2000). A physical introduction to fluid mechanics. New York: John Wiley and Sons.
Song, J., Ortiz, C., & Boyce, M. C. (2011). Threat-protection mechanics of an armored fish. Journal of the Mechanical Behavior of Biomedical Materials, 4, 699–712.
Sudo, S., Tsuyuki, K., Ito, Y., & Ikohagi, T. (2002). A study on the surface shape of fish scales. Trans. Jpn. Soc. Mechanical Engineering, 45, 1100–1105.
Suzuki, T. (1971). Some scale patterns of the scad, Decapterus maruadsi (Temminck et Schlegel), and their variations with body parts. Bulletin of the Japan Sea Regional Fisheries Research Laboratory 23, 1–19.
Szewciw, L., Zhu, D., & Barthelat, F. (2017). The nonlinear flexural response of a whole teleost fish: Contribution of scales and skin. Journal of the Mechanical Behavior of Biomedical Materials, 17, 30252–30257.
Taylor, H. F. (1916). The structure and growth of the scales of the squeteague and the pigfish as indicative of life history. Fishery Bulletin, 34, 285–330.
Thomson, J. M. (1956). Interpretation of the scales of the yellow-eye mullet, Aldrichetta forsteri (Cuvier & Valenciennes) (Mugilidae). Australian Journal of Marine and Freshwater Research, 8, 14–30.
Vernerey, F. J., & Barthelat, F. (2010). On the mechanics of fishscale structures. International Journal of Solids and Structures, 47, 2268–2275.
Vernerey, F. J., & Barthelat, F. (2014). Skin and scales of teleost fish: Simple structure but high performance and multiple functions. Journal of the Mechanics and Physics of Solids, 68, 66–76.
Wainwright, D. K., & Lauder, G. V. (2016). Three-dimensional analysis of scale morphology in bluegill sunfish, Lepomis macrochirus. Zoology, 119, 182–195.
Wainwright, D. K., Lauder, G. V., & Weaver, J. C. (2017). Imaging biological surface topography in situ and in vivo. Methods in Ecology and Evolution. in press.
Walters, V. (1963). The Trachipterid integument and an hypothesis on its hydrodynamic function. Copeia, 1963, 260–270.
Wen, L., Weaver, J. C., & Lauder, G. V. (2014). Biomimetic shark skin: Design, fabrication and hydrodynamic function. The Journal of Experimental Biology, 217, 1656–1666.
Wen, L., Weaver, J. C., Thornycroft, P. J. M., & Lauder, G. V. (2015). Hydrodynamic function of biomimetic shark skin: Effect of denticle pattern and spacing. Bioinspiration & Biomimetics, 10, 066010.
Whitear, M. (1970). The skin surface of bony fishes. Journal of Zoology, 4, 437–454.
Whitehouse, D. J. (1994). Handbook of surface metrology. Philadelphia: Institute of Physics Publishing.
Xu, Z., Parra, D., Gomez, D., Salinas, I., Zhang, Y.-A., von Gersdorff Jørgensen, L., Heinecke, R. D., Buchmann, K., LaPatra, S., & Sunyer, J. O. (2013). Teleost skin, an ancient mucosal surface that elicits gut-like immune responses. Proceedings of the National Academy of Sciences of the United States of America, 110, 13097–13102.
Yanase, K., & Saarenrinne, P. (2015). Unsteady turbulent boundary layers in swimming rainbow trout. The Journal of Experimental Biology, 218, 1373–1385.
Zaccone, G., Kapoor, B. G., Fasulo, S., & Ainis, L. (2001). Structural, histochemical and functional aspects of the epidermis of fishes. Advnces in Marine Biology, 40, 253–348.
Zylberberg, L., Bereiter-Hahn, J., & Sire, J. Y. (1988). Cytoskeletal organization and collagen orientation in the fish scales. Cell and Tissue Research, 253, 597–607.
Acknowledgements
We would like to acknowledge James Weaver for his imaging expertise (in particular for the images in Fig. 10.5), and Kimo Johnson for his assistance with GelSight profilometry measurements. We acknowledge Karsten Hartel and Andrew Williston with assistance in accessing specimens and Dr. Lex Smits for introducing us to k+. The research reported here was supported by ONR MURI Grant N000141410533 monitored by Dr. Bob Brizzolara, HFSP Young Investigators Grant (RGY0067- 2013) to James Weaver, and NSF GRF 2014162421 awarded to D.K.W.
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Wainwright, D.K., Lauder, G.V. (2017). Mucus Matters: The Slippery and Complex Surfaces of Fish. In: Gorb, S., Gorb, E. (eds) Functional Surfaces in Biology III. Biologically-Inspired Systems, vol 10. Springer, Cham. https://doi.org/10.1007/978-3-319-74144-4_10
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