The effects of hand-stripping on some epidermal mucus immune parameters in rainbow trout, Oncorhynchus mykiss
Downloads
Fish epidermis functions as the first defense barrier against physical, chemical, and biological stressors. However, the effects of hand-stripping on fish mucosal immune responses have been hardly investigated. The present study investigated the effects of stripping procedures on skin mucosal immune responses of rainbow trout (Oncorhynchus mykiss) breeders. The skin mucus was sampled from six male and six female trout before and one week after the stripping handling. The results showed that stripping had significant effect on all parameters except protease activity, but gender had a significant effect only on the mucosal protease and alkaline phosphatase activity. The results did not show any effect of the interaction between stripping and gender on mucosal lysozyme activity. The data revealed that enzymatic activities of alkaline phosphatase, lysozyme, esterase, as well as the total immunoglobulin level and bactericidal activity were significantly reduced in the skin mucus of fish one week after the stripping. The reduction of immune parameters in the skin mucus could be related to immunosuppression caused by stripping stress which, in turn, might have made the fish more susceptible to microbial infections and diseases. Therefore, care should be taken during stripping to minimize the manipulation stress.
Downloads
Aranishi F., Mano N. (2000). Response of skin cathepsins to infection of Edwardsiella tarda in Japanese flounder. Fisheries Science, 66: 169-170.
Aranishi F., Nakane M. (1997). Epidermal proteases of the Japanese eel. Fish Physiology and Biochemistry, 16: 471-478.
Aranishi F., Mano N., Nakane M., Hirose H. (1999). Effects of thermal stress on skin defense lysins of European eel, Anguilla anguilla. Journal of Fish Diseases, 22: 227-230.
Aranishi F., Mano N., Hirose H. (1998). Fluorescence localization of epidermal cathepsins L and B in the Japanese eel. Fish Physiology and Biochemistry, 19: 205-209.
Balfry S.K., Iwama G.K. (2004). Observations on the inherent variability of measuring lysozyme activity in coho salmon (Oncorhynchus kisutch). Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology, 138: 207-211.
Bartelme T.D. (2004). Reducing losses associated with transport and handling in marine teleost fish. Advanced Aquarist's Online Magazine, 3(5).
Bergsson G., Agerberth B., Jörnvall H., Gudmundsson G.H. (2005). Isolation and identification of antimicrobial components from the epidermal mucus of Atlantic cod (Gadus morhua). The FEBS Journal, 272(19): 4960-4969.
Böckelmann P.K., Ochandio B.S., Bechara I.J. (2010). Histological study of the dynamics in epidermis regeneration of the carp tail fin (Cyprinus carpio, Linnaeus,1758). Brazilian Journal of Biology, 70: 217-223.
Bonga S.W. (1997). The stress response in fish. Physiological Reviews, 77: 591-625.
Bradford M.M. (1979). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 249-254.
Caruso G., Denaro M.G., Caruso R., Mancari F., Genovese L., Maricchiolo G. (2011). Response to short term starvation of growth, haematological, biochemical and non-specific immune parameters in European sea bass (Dicentrarchus labrax) and blackspot sea bream (Pagellus bogaraveo). Marine Environmental Research, 72(1-2): 46-52.
Dash S., Das S.K., Samal J., Thatoi H.N. (2018). Epidermal mucus, a major determinant in fish health: a review. Iranian Journal of Veterinary Research, 19(2): 72-81.
Demers N.E., Bayne C.J. (1997). The immediate effects of stress on hormones and plasma lysozyme in rainbow trout. Developmental and Comparative Immunology, 21(4): 363-373.
Dhanaraj M., Haniffa M.A., Sv A.S., Manikandaraja D. (2009). Antibacterial activity of skin and intestinal mucus of five different freshwater fish species viz., Channa striatus, C. micropeltes, C. marulius, C. punctatus and C. gachua. Malaysian Journal of Science, 28(3): 257-262.
Easy R.H., Ross N.W. (2010). Changes in Atlantic salmon Salmo salar mucus components following short"and long"term handling stress. Journal of Fish Biology, 77(7): 1616-1631.
Ellis A. (2001). Innate host defense mechanisms of fish against viruses and bacteria. Developmental and Comparative Immunology, 25: 827-839.
Esteban M.í. (2012). An overview of the immunological defenses in fish skin. ISRN Immunology, 1-29.
Fernandes J.M.O., Smith V.J. (2002). A novel antimicrobial function for a ribosomal peptide from rainbow trout skin. Biochemical and Biophysical Research Communications, 296: 167-171.
Ghafoori Z., Heidari B., Farzadfar F., Aghamaali M. (2014). Variations of serum and mucus lysozyme activity and total protein content in the male and female Caspian kutum (Rutilus frisii kutum, Kamensky 1901) during reproductive period. Fish and Shellfish Immunology, 37: 139-146.
Guardiola F.A., Cuesta A., Esteban M.í. (2016). Using skin mucus to evaluate stress in gilthead seabream (Sparus aurata L.). Fish and Shellfish Immunology, 59: 323-330.
Guardiola F.A., Cuesta A., Arizcun M., Meseguer J., Esteban M.í. (2014). Comparative skin mucus and serum humoral defense mechanisms in the teleost gilthead seabream (Sparus aurata). Fish and Shellfish Immunology, 36: 545-551
Guardiola F.A., Dioguardi M., Parisi M.G., Trapani M.R., Meseguer J., Cuesta A., Esteban M.A. (2015). Evaluation of waterborne exposure to heavy metals in innate immune defences present on skin mucus of gilthead seabream (Sparus aurata). Fish and Shellfish Immunology, 45(1): 112-123.
Guardiola F.A., Cuesta A., Esteban M.í. (2016). Using skin mucus to evaluate stress in gilthead seabream (Sparus aurata L.). Fish and Shellfish Immunology, 59: 323-330.
Hellio C., Pons A.M., Beaupoil C., Bourgougnon N., Gal Y.L. (2002). Antibacterial, antifungal and cytotoxic activities of extracts from fish epidermis and epidermal mucus. International Journal of Antimicrobial Agents, 20: 214-219.
Hjelmeland K., Christie M., Raa J. (1983). Skin mucus protease from rainbow-trout, Salmo gairdneri Richardson, and its biological significance. Journal of Fish Biology, 23: 13-22.
Huang Z.H., Ma A.J., Wang X. (2011). The immune response of turbot, Scophthalmus maximus (L.), skin to high water temperature. Journal of Fish Diseases, 34: 619-627.
Iger Y., Abraham M. (1990). The process of skin healing in experimentally wounded carp. Journal of Fish Biology, 36: 421-437.
Iger Y., Abraham M. (1997). Rodlet cells in the epidermis of fish exposed to stressors. Tissue Cell, 29: 431-438.
Ingram G. (1980). Substances involved in the natural resistance of fish to infection A- review. Journal of Fish Biology, 16: 23-60.
Iwama G.K., Pickering A., Sumpter J., Schreck C. (2011). Fish Stress and Health in Aquaculture, Cambridge University Press. 290 p.
Jia R., Liu B.L., Feng W.R., Han C., Huang B., Lei J.L. (2016). Stress and immune responses in skin of turbot (Scophthalmus maximus) under different stocking densities. Fish and Shellfish Immunology, 55: 131-139.
Jung T.S., del Castillo C.S., Javaregowda P.K., Dalvi R.S., Nho S.W., Park S.B., Aoki T. (2012). Seasonal variation and comparative analysis of non-specific humoral immune substances in the skin mucus of olive flounder (Paralichthys olivaceus). Developmental and Comparative Immunology, 38(2): 295-301.
Kennedy J., Baker P., Piper C., Cotter P.D., Walsh M., Mooij M.J., Hill C. (2009). Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Marine Biotechnology, 11(3): 384-396.
Khansari A.R., Parra D., Reyes-López F.E., Tort L. (2017). Modulatory in vitro effect of stress hormones on the cytokine response of rainbow trout and gilthead sea bream head kidney stimulated with Vibrio anguillarum bacterin. Fish and Shellfish Immunology, 70: 736-749.
Khansari A.R., Balasch J.C., Vallejos-Vidal E., Parra D., Reyes-López F.E., Tort L. (2018). Comparative immune-and stress-related transcript response induced by air exposure and Vibrio anguillarum bacterin in rainbow trout (Oncorhynchus mykiss) and gilthead seabream (Sparus aurata) mucosal surfaces. Frontiers in immunology, 9: 856.
Kuppulakshmi C., Prakash M., Gunasekaran G., Manimegalai G., Sarojini S. (2008). Antibacterial properties of fish mucus from Channa punctatus and Cirrhinus mrigala. European Review for Medical and Pharmacological Sciences, 12: 149-153.
Ledy K., Giamberini L., Pihan J. (2003). Mucous cell responses in gill and skin of brown trout Salmo trutta fario in acidic, aluminium-containing stream water. Diseases of Aquatic Organisms, 56: 235- 240.
Lindenstrí¸m T., Secombes C.J., Buchmann K. (2004). Expression of immune response genes in rainbow trout skin induced by Gyrodactylus derjavini infections. Veterinary Immunology and Immunopathology, 97: 137-148.
Lí¼ A., Hu X., Xue J., Zhu J., Wang Y., Zhou G. (2012). Gene expression profiling in the skin of zebrafish infected with Citrobacter freundii. Fish and Shellfish Immunology, 32: 273-283.
Mustafa A., Mackinnon B.M., Piasecki W. (2005). Interspecific differences between Atlantic salmon and Artic charr in susceptibility to infection with larval and adult Caliguselongatus: Effect of skin mucus protein profiles and epidermal histological differences. Acta Ichthyologica et Piscatoria, 35: 7-13.
Mugnier C., Fostier A., Guezou S., Gaignon G.L., Quemener L. 1998. Effect of some repetitive factors on turbot stress response. Aquaculture International, 6(1): 33-45.
Nigam A.K., Kumari U., Mittal S., Mittal A.K. (2012). Comparative analysis of innate immune parameters of the skin mucous secretions from certain freshwater teleosts, inhabiting different ecological niches. Fish Physiology and Biochemistry, 38: 1245-1256.
Palaksha K.J., Shin G.W., Kim Y.R., Jung T.S. (2008). Evaluation of non-specific immune components from the skin mucus of olive flounder (Paralichthys olivaceus). Fish and Shellfish Immunology, 24: 479-488.
Parra D., Reyes-Lopez F.E., Tort L. (2015). Mucosal immunity and B Cells in teleosts: Effect of vaccination and stress. Frontiers in Immunology, 6: 354.
Rai A., Mittal A. (1983). Histochemical response of alkaline phosphatase activity during the healing of cutaneous wounds in a catfish. Experientia, 39: 520-522.
Reverter M., Tapissier-Bontemps N., Lecchini D., Banaigs B., Sasal P. (2018). Biological and ecological roles of external fish mucus: a review. Fishes, 3: 41.
Roosta Z., Hoseinifar H. (2016). The effects of crowing stress on some epidermal mucus immune parameters, growth performance and survival rate of tiger barb (Pentius tetrazona). Aquaculture Research, 47: 1682-86.
Roosta Z., Hajimoradloo A., Ghorbani R., Hoseinifar S.H. (2014). The effects of dietary vitamin C on mucosal immune responses and growth performance in Caspian roach (Rutilus rutilus caspicus) fry. Fish Physiology and Biochemistry, 40(5): 1601-1607.
Ross N.W., Firth K.J.F., Wang A., Burka J.F., Johnson S.C. (2000). Changes in hydrolytic enzyme activities of naive Atlantic salmon Salmo salar skin mucus due to infection with the salmon louse Lepeophtheirus salmonis and cortisol implantation. Diseases of Aquatic Organisms, 41: 43-51.
Salinas I. (2015). The mucosal immune system of teleost fish. Biology, 4: 525-539.
Schreck C.B. (2010). Stress and fish reproduction: the roles of allostasis and hormesis. General and Comparative Endocrinology, 165: 549-556.
Sheikhzadeh N., Heidarieh M., KarimiPashaki A., Nofouzi K., AhrabFarshbafi M., Akbari M. (2012). Hilyses, fermented (Saccharomyces cerevisiae), enhances the growth performance and skin non-specific immune parameters in rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology, 32: 1083-87.
Siwicki A.K. (1993). Nonspecific defense mechanisms assay in fish. II. Potential killing activity of neutrophils and macrophages, lysozyme activity in serum and organs and total immunoglobulin (Ig) level in serum. Fish Diseases Diagnosis and Preventions Methods. pp: 105-111.
Studnicka M., Siwicki A., Ryka B. (1986). Lysozyme level in carp (Cyprinus carpio L.). Bamidgeh, 38(1): 22-25.
Subramanian S., MacKinnon S., Ross N.A. (2007). Comparative study on innate immune parameters in the epidermal mucus of various fish species. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 148: 256-263.
Subramanian S., Ross N.W., MacKinnon S.L. (2008). Comparison of antimicrobial activity in the epidermal mucus extracts of fish. Comparative Biochemistry and Physiology, 150: 85-92.
Tacchi L., Lowrey L., Musharrafieh R., Crossey K., Larragoite E.T., Salinas I. (2015). Effects of transportation stress and addition of salt to transport water on the skin mucosal homeostasis of rainbow trout (Oncorhynchus mykiss). Aquaculture, 435: 120-127.
Takemura A., Takano K. (1995). Lysozyme in the ovary of tilapia (Oreochromis mossambicus): its purification and some biological properties. Fish Physiology and Biochemistry, 14: 415-421.
Thongprajukaew K., Kovitvadhi U. (2013). Effects of sex on characteristics and expression levels of digestive enzymes in the adult guppy Poecilia reticulata. Zoological Studies, 52(3): 1-8.
Tort L. (2011). Stress and immune modulation in fish. Developmental and Comparative Immunology, 35: 1366-1375.
Vatsos I., Kotzamanis Y., Henry M., Angelidis P., Alexis M. (2010). Monitoring stress in fish by applying image analysis to their skin mucous cells. European Journal of Histochemistry, 10: 54(2): e22.
