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Histological Studies on the Skin of a Freshwater Goby Rhinogobius brunneus (Gobiidae) Related to Cutaneous Respiration

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Abstract

The Korean freshwater goby, Rhinogobius brunneus, prefers shallow water bodies with pebble bottoms, which are easily exposed to air due to the lack of water in droughts or the decline of water level after rainfall. Histological studies using microscopic researches revealed its skin consisting of two large parts, the epidermis and dermis with modified vascularization and intraepithelial blood capillaries, considering such environmental habitat conditions. The epidermis (38.4–156.8 µm in thickness) is classified into three parts; the outermost surface layer contained: stratified squamous and polygonal cells, mucous cells, and taste buds. The middle layer includes stratified polygonal cells and finally, the stratum germinativum consisting of a single layer of stratified polygonal cells and intraepithelial blood capillaries. In particular, there are very interesting findings that a small number of blood capillaries are situated at the stratum germinativum of the epidermis and dermal vascularization develops at the stratum laxum of the dermis. Consequently, the presence of the intraepithelial and intradermal blood capillaries, abundant mucous cells, well-developed dermal vascularization, a thick epidermis, as well as the reduced diffusion distance in some skin regions may be considered useful histological evidence to support cutaneous respiration during hypoxic conditions in stagnant water or during the periodic dry season.

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REFERENCES

  1. Ángeles Esteban, M., An overview of the immunological defenses in fish skin, ISRN Immunol., 2012, vol. 2012, art. ID 853470. https://doi.org/10.5402/2012/853470

    Article  Google Scholar 

  2. Beon, M.S., Oh, M.K., Lee, Y.J., et al., A comparative study on vascularization and the structure of the epidermis of an amphibious mudskipper fish, Scartelaos gigas (Gobiidae, Teleostei), on different parts of the body and the appendages, J. Appl. Ichthyol., 2013, vol. 29, pp. 410–415. https://doi.org/10.1111/jai.12038

    Article  Google Scholar 

  3. Bond, C.E., Biology of Fishes, New York: Saunders College, 1996.

    Google Scholar 

  4. Dash, S., Das, S.K., Samal, J., and Thatoi, H.N., Epidermal mucus, a major determinant in fish health: a review, Iran. J. Vet. Res., 2018, vol. 19, no. 2, pp. 72.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. de Moraes, M.F., Höller, S., da Costa, O.T., et al., Morphometric comparison of the respiratory organs in the South American lungfish Lepidosiren paradoxa (Dipnoi), Physiol. Biochem. Zool., 2005, vol. 78, pp. 546–559.

    PubMed  Google Scholar 

  6. Fänge, R., Gas exchange in fish swim bladder, Rev. Physiol. Biochem. Pharmacol., 1983, vol. 97, pp. 111–158.

    PubMed  Google Scholar 

  7. Fernandes, M.N., Moron, S.E., and Sakuragui, M.M., Gill morphological adjustments to environment and the gas exchange function, in Fish Respiration and Environment, Boca Raton, FL: CRC Press, 2007, pp. 93–120.

    Google Scholar 

  8. Fernandes, M.N., da Cruz, A.L., da Costa, O.T.F., and Perry, S.F., Morphometric partitioning of the respirator surface area and diffusion capacity of the gills and swim bladder in juvenile Amazonian air-breathing fish, Arapaima gigas, Micron, 2012, vol. 43, no. 9, pp. 961–970.

    PubMed  Google Scholar 

  9. Ghosh, S.K., Ghosh, B., and Chakrabarti, P., Fine anatomical structures of the intestine in relation to respiratory function of an air-breathing loach, Lepidocephalichthys guntea (Actinopterygii: Cypriniformes: Cobitidae), Acta Ichthyol. Piscatoria, 2011, vol. 41, pp. 1–5.

    Google Scholar 

  10. Glover, C.N., Bucking, C., and Wood, C.M., The skin of fish as a transport epithelium: a review, J. Comp. Physiol., 2013, vol. 183, no. 7, pp. 877–891. https://doi.org/10.1007/s00360-013-0761-4

    Article  CAS  Google Scholar 

  11. Goncaves, A.F., Castro, L.F.C., Pereira-Wilson, C., et al., Is there a compromise between nutrient uptake and gas exchange in the gut of Misgurnus anguillicaudatus, an intestinal air-breathing fish? Comp. Biochem. Physiol., Part D: Genomics Proteomics, 2007, vol. 2, no. 4, pp. 345–355.

    Google Scholar 

  12. Graham, J.B., Air-Breathing Fishes: Evolution, Diversity, and Adaptation, San Diego: Academic, 1997.

    Google Scholar 

  13. Graham, J.B., Respiratory adaptations for air-breathing fishes, in Encyclopedia of Fish Physiology, Vol. 3: Energetics, Interactions with the Environment, Lifestyles, and Applications, New York: Elsevier, 2011, pp. 1861–1874.

  14. Gurr, E., A Practical Manual of Medical and Biological Staining Techniques, New York: Wiley, 1956.

    Google Scholar 

  15. Harabawy, A.S. and Mekkawy, I.A., Skin characteristics and organization of the air-breathing fish, Alticus kirkii (Gunther, 1868) along different body regions, J. Biol. Sci., 2011, vol. 11, no. 8, pp. 466–474. https://doi.org/10.3923/jbs.2011.466.474

    Article  Google Scholar 

  16. Hawkes, J.W., The structure of fish skin, Cell Tissue Res., 1974, vol. 149, no. 2, pp. 147–158.

    CAS  PubMed  Google Scholar 

  17. Hughes, G.M. and Munshi, J.S.D., Scanning electron microscopy of the accessory respiratory organs of the snake-headed fish, Channa striata (Bloch) (Channidae, Channiformes), J. Zool., 1986, vol. 209, no. 3, pp. 305–317. https://doi.org/10.1111/j.1469-7998.1986.tb03593.x

    Article  Google Scholar 

  18. Hwang, P.P. and Lin, L.Y., Gill ionic transport, acid-base regulation, and nitrogen excretion, in The Physiology of Fishes, Boca Raton, FL: CRC Press, 2013, pp. 205–233.

    Google Scholar 

  19. Kang, C.K. and Lee, T.H., The pharyngeal organ in the buccal cavity of the male Siamese fighting fish, Betta splendens, supplies mucus for building bubble nests, Zool. Sci., 2010, vol. 27, no. 11, pp. 861–866. https://doi.org/10.2108/zsj.27.861

    Article  Google Scholar 

  20. Killgore, K.J. and Hoover, J.J., Effects of hypoxia on fish assemblages in a vegetated waterbody, J. Aquat. Plant Manage., 2001, vol. 39, no. 1, pp. 40–44.

    Google Scholar 

  21. Kim, H.T., A comparative anatomy and histology of the olfactory organ of 17 fishes in South Korea, PhD Thesis, Jeonju: Chonbuk Natl. Univ., 2018.

  22. Kim I.S. and Park, J.Y., Freshwater Fish of Korea, Seoul: Kyo-Hak, 2002.

    Google Scholar 

  23. Kim, C.H. and Park, J.Y., Modified organs of air breathing fishes in Korea, Korean J. Ichthyol., 2011, vol. 23, no. 3, pp. 250–254.

    Google Scholar 

  24. Kim, G.B., Kil, H.K., Yu, B.T., et al., Long-term changes of the fish fauna and community structure in the Jungrang Creek, Seoul, Korea, Korean J. Limnol., 2002, vol. 35, no. 2, pp. 63–70.

    Google Scholar 

  25. Ko, M.H., Jang, S.L., and Won, Y.J., Fish distribution characteristics of Mudeungsan National Park, Korean J. Limnol., 2018, vol. 32, no. 2, pp. 154–164.

    Google Scholar 

  26. Lane, E.B. and Whitear, M., Sensory structures at the surface of fish skin: I. Putative chemoreceptors, Zool. J. Linn. Soc., 1982, vol. 75, no. 2, pp. 141–151.

    Google Scholar 

  27. Lauder, G.V., Wainwright, D.K., Domel, A.G., et al., Structure, biomimetics, and fluid dynamics of fish skin surfaces, Phys. Rev. Fluids, 2016, vol. 1, no. 6, art. ID 060502. https://doi.org/10.1103/PhysRevFluids.1.060502

    Article  Google Scholar 

  28. Liem, K.F., Functional morphology of the integumentary, respiratory, and digestive systems of the synbranchoid fish, Monopterus albus, Copeia, 1967, no. 2, pp. 375–388.

  29. Magoulick, D.D. and Kobza, R.M., The role of refugia for fishes during drought: a review and synthesis, Freshwater Biol., 2003, vol. 48, no. 7, pp. 1186–1198.

    Google Scholar 

  30. Maina, J.N. and Maloiy, G.M.O., The morphology of the respiratory organs of the African air-breathing catfish (Clarias mossambicus): a light, electron and scanning microscopic study, with morphometric observations, J. Zool., 1986, vol. 209, no. 3, pp. 421–445.

    Google Scholar 

  31. Mittal, A.K. and Munshi, J.D., A comparative study of the structure of the skin of certain air-breathing fresh-water teleosts, J. Zool., 1971, vol. 163, no. 4, pp. 515–532.

    Google Scholar 

  32. Null, S.E., Mouzon, N.R., and Elmore, L.R., Dissolved oxygen, stream temperature, and fish habitat response to environmental water purchases, J. Eviron. Manage., 2017, vol. 197, pp. 559–570.

    CAS  Google Scholar 

  33. Ostrander, G.K. and Hopkins, J., The Laboratory Fish, San Diego: Academic, 2000, pp. 79–91.

    Google Scholar 

  34. Palzenberger, M. and Pohla, H., Gill surface area of water-breathing freshwater fish, Rev. Fish Biol. Fish., 1992, vol. 2, no. 3, pp. 187–216.

    Google Scholar 

  35. Park, J.Y., Morphology and histochemistry of the skin of the Korean spined loach, Iksookimia koreensis (Cobitidae), in relation to respiration, Folia Zool., 2002a, vol. 51, no. 3, pp. 241–247.

    Google Scholar 

  36. Park, J.Y., Structure of the skin of an air-breathing mudskipper, Periophthalmus magnuspinnatus, J. Fish Biol., 2002b, vol. 60, no. 6, pp. 1543–1550.

    Google Scholar 

  37. Park, J.Y. and Kim, I.S., Histology and mucus cytochemistry of the gastro-intestinal tract of a mud loach, in relation to respiration, J. Fish Biol., 2001, vol. 58, pp. 861–872.

    Google Scholar 

  38. Park, J.Y., Kim, I.S., and Kim, S.Y., Histology of skin of the amphibious esh, Periophthalmus modestus, Korean J. Biol. Sci., 2000, vol. 4, no. 4, pp. 315–318.

    Google Scholar 

  39. Park, J.Y., Lee, Y.J., Kim, I.S., and Kim, S.Y., A comparative study of the regional epidermis of an amphibious mudskipper fish, Boleophthalmus pectinirostris (Gobiidae, Pisces), Folia Zool., 2003a, vol. 52, no. 4, pp. 431–440.

    Google Scholar 

  40. Park, J.Y., Kim, I.S., and Kim, S.Y., Structure and mucous histochemistry of the intestinal respiratory tract of a mud loach, Misgurnus anguillicaudatus (Cantor), J. Appl. Ichthyol., 2003b, vol. 19, pp. 215–219.

    Google Scholar 

  41. Park, J.Y., Kim, I.S., and Kim, S.Y., Structure and histochemistry of the skin of a torrent catfish, Liobagrus mediadiposalis, Environ. Biol. Fish., 2003c, vol. 66, no. 1, pp. 3–8.

    Google Scholar 

  42. Park, J.Y., Lee, Y.J., Kim, I.S., and Kim, S.Y., Morphological and cytochemical study on the skin of Korean eel goby, Odontamblyopus lacepedii (Pisces, Gobiidae), Korean J. Biol. Sci., 2003d, vol. 7, no. 1, pp. 43–47.

    Google Scholar 

  43. Park, J.Y., Oh, M.K., Kang, E.J., et al., On the vascularization and structure of the skin of a Korean bullhead Pseudobagrus brevicorpus (Bagridae, Teleostei) based on its entire body and appendages, J. Appl. Ichthyol., 2010, vol. 26, no. 1, pp. 64–70. https://doi.org/10.1111/j.1439-0426.2009.01354.x

    Article  Google Scholar 

  44. Perry, S.F. and Gilmour, K.M., Acid-base balance and CO2 excretion in fish: unanswered questions and emerging models, Respir. Physiol. Neurobiol., 2006, vol. 154, pp. 199–215. https://doi.org/10.1016/j.resp.2006.04.010

    Article  CAS  PubMed  Google Scholar 

  45. Randall, D.J., Ip, Y.K., Chew, S.F., and Wilson, J.M., Air breathing and ammonia excretion in the giant mudskipper, Periophthalmodon schlosseri, Physiol. Biochem. Zool., 2004, vol. 77, no. 5, pp. 783–788.

    CAS  PubMed  Google Scholar 

  46. Reverter, M., Tapissier-Bontemps, N., Lecchini, D., et al., Biological and ecological roles of external fish mucus: a review, Fishes, 2018, vol. 3, no. 4, art. ID 41. https://doi.org/10.3390/fishes3040041

    Article  Google Scholar 

  47. Sato, M., Histology of barbels of Blepsias cirrhosus draciscus (Cottidae), Jpn. J. Ichthyol., 1977, vol. 23, no. 4, pp. 220–224.

    Google Scholar 

  48. Sayer, M.D., Adaptations of amphibious fish for surviving life out of water, Fish Fish., 2005, vol. 6, no. 3, pp. 186–211.

    Google Scholar 

  49. Scheid, P., Pelster, B., and Kobayashi, H., Gas exchange in the fish swimbladder, Adv. Exp. Med. Biol., 1990, vol. 277, pp. 735–742. https://doi.org/10.1007/978-1-4684-8181-5_84

    Article  CAS  PubMed  Google Scholar 

  50. Seo, J.W., Fish founa and ecological characteristics of dark chub (Zacco termminckii) population in the mid-upper region of Gam stream, Korean J. Limnol., 2005, vol. 38, no. 2, pp. 196–206.

    Google Scholar 

  51. Sullivan, J.P., Lundberg, J.G., and Hardman, M., A phylogenetic analysis of the major groups of catfishes (Teleostei: Siluriformes) using rag1 and rag2 nuclear gene sequences, Mol. Phylogenet. Evol., 2006, vol. 41, no. 3, pp. 636–662.

    CAS  PubMed  Google Scholar 

  52. Suzuki, N. and Hiraki, M., Intraepithelial blood capillaries in fish species, Rep. Kanagawa Nat. Preserv. Soc., 1991, vol. 10, pp. 1–11.

    Google Scholar 

  53. Turko, A.J., Rossi, G.S., and Wright, P.A., More than breathing air: evolutionary drivers and physiological implications of an amphibious lifestyle in fishes, Physiology, 2021, vol. 36, no. 5, pp. 307–314.

    PubMed  Google Scholar 

  54. Ultsch, G.R. and Gros, G., Mucus as a diffusion barrier to oxygen: possible role in O2 uptake at low pH in carp (Cyprinus carpio) gills, Comp. Biochem. Physiol., Part A: Physiol., 1979, vol. 62, no. 3, pp. 685–689.

    Google Scholar 

  55. van Doan, H., Hoseinifar, S.H., Jaturasitha, S., et al., The effects of berberine powder supplementation on growth performance, skin mucus immune response, serum immunity, and disease resistance of Nile tilapia (Oreochromis niloticus) fingerlings, Aquaculture, 2020, vol. 520, art. ID 734927. https://doi.org/10.1016/j.aquaculture.2020.734927

    Article  CAS  Google Scholar 

  56. Winemiller, K.O. and Yan, H.Y., Obligate mucus-feeding in a South American trichomycterid catfish (Pisces: Ostariophysi), Copeia, 1989, vol. 1989, no. 2, pp. 511–514.

    Google Scholar 

  57. Wu, H., Hu, X., Sun, S., et al., Effect of increasing of water level during the middle of dry season on landscape pattern of the two largest freshwater lakes of China, Ecol. Indic., 2020, vol. 113, art. ID 106283.

    Google Scholar 

  58. Yang, S.G., Cho, Y.C., Yang, H., and Kang, E.J., Characteristics of fish fauna and community structure in Yongdam reservoir by inhabiting environment changes, Korean J. Environ. Biol., 2012, vol. 30, no. 1, pp. 15–25.

    Google Scholar 

  59. Zhang, J., Taniguchi, T., Takita, T., and Ali, A.B. A study on the epidermal structure of Periophthalmodon and Periophthalmus mudskippers with reference to their terrestrial adaptation, Ichthyol. Res., 2003, vol. 50, no. 4, pp. 310–317.

    Google Scholar 

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ACKNOWLEDGMENTS

We thank our laboratory members who helped us collect specimens and conduct fieldwork.

Funding

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (project no. 2020R1A6A3A0109608211).

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Authors and Affiliations

  1. Jeonju National University of Education, Jeonju, Republic of Korea

    H. T. Kim

  2. Department of Biological Science and Institute for Biodiversity Research, College of Natural Sciences, Jeonbuk National University, Jeonju, Republic of Korea

    S. W. Yun & J. Y. Park

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Hyun Tae Kim and Seung Woon Yun wrote text, made the figures and contributed equally to this work. Jong Young Park edited and approved the manuscript for publication.

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Correspondence to J. Y. Park.

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Statement of the welfare of animal. We followed the rules of Jeonbuk National University Institutional Animal Care and Use Committee for animal’s ethics (2016-12ET-0097).

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Kim, H.T., Yun, S.W. & Park, J.Y. Histological Studies on the Skin of a Freshwater Goby Rhinogobius brunneus (Gobiidae) Related to Cutaneous Respiration. J. Ichthyol. 62, 495–502 (2022). https://doi.org/10.1134/S0032945222030067

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