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Antioxidant enzyme activities and immune responses in rainbow trout (Onchorhynchus mykiss) juveniles fed diets supplemented with dandelion (Taraxacum officinalis) and lichen (Usnea barbata) extracts

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Abstract

In the present study, antioxidant activity, immune responses, and growth performance of rainbow trout (Onchorhynchus mykiss) juveniles fed with diets supplemented with dandelion (Taraxacum officinalis) and lichen (Usnea barbata) extracts were assessed. Four different concentrations of aqueous methanolic extract of the plants (0% (control), 0.1%, 0.5%, and 1% (D, dandelion; L, lichen) were added to the diets, and fish were fed for 75 days. On the 15th, 45th, and 75th day of the study, liver antioxidant enzyme activities were determined, and immune responses were determined every 15th day. The results showed that SOD activity increased in the fish group of 0.1% D on the 15th and 45th day compared to control; however, it was lower in all the lichen extract-treated groups than in control at almost all sampling times, except on the 15th day in the 0.1% L group. CAT activity showed an increased value (P < 0.05) in 0.5% L and 1% L treated fish groups on the 15th day, in fish of 1% D and 1% L groups on 45th and on 75th day in 0.1% D group. GPX activity increased on the 15th day of the study in fish of 0.1% D group, on the 45th day in 1% D and 1% L groups and on the 75th day in fish of 0.5% D, 0.1% D, and 0.5% L groups (P < 0.05). G6PDH enhanced in all treatment groups compared to control on the 15th day, except in 0.1% L and 0.5% L groups. An elevated G6PDH activity was also observed on the 75th day of the study in 0.5% D, 1% D, and 0.5% L fish groups. An increase on lipid peroxidation (LP) was observed in all L groups on the 45th day of the study. Lysozyme activity was determined to be the highest in 0.5% and 1% L on the 45th day, in 0.1% L on the 60th day and in the 0.5% L fish group on the 75th day compared to control (P < 0.05). Myeloperoxidase was found to be the highest at the end of the study in 1% L fish group compared to the control (P < 0.05). In conclusion, we suggest the use of dandelion to combat oxidative stress and to lower FCR and the use of lichen to modulate the immune response in rainbow trout. The use of such products will be economical for aquaculture and harmless for the environment.

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Data are available from corresponding author upon reasonable request.

References

  • Almabrok AA, Amhamed ID, Mohamed GA, Bilen S, Altief TAS (2018) Effect of Tilia tomentosa methanolic extract on growth performance, digestive enzyme activity, immune system and haematological indices of common carp (Cyprinus carpio). Mar Sci Tech Bull 7(1):12–20

    Article  Google Scholar 

  • Amhamed ID, Mohamed GA, Almabrok AA, Altief TAS, Bilen S (2018) Efficacy of dietary Chenopodium album extract on some health parameters, digestive enzymes and growth performance in juvenile Cyprinus carpio. Alınteri Zirai Bilimler Dergisi 33(2):165–176

    Google Scholar 

  • Amer SA (2016) Effect of Spirulina platensis as feed supplement on growth performance, immune response and antioxidant status of mono-sex Nile tilapia (Oreochromis niloticus). Benha Vet Med J. 30:1–10. https://doi.org/10.21608/bvmj.2016.31332

  • Arslan G, Sönmez AY, Yanık T (2018) Effects of grape Vitis vinifera seed oil supplementation on growth, survival, fatty acid profiles, antioxidant contents and blood parameters in rainbow trout Oncorhynchus mykiss. Aquac Res 49(6):2256–2266. https://doi.org/10.1111/are.13686

    Article  CAS  Google Scholar 

  • Bilen S, Bulut M (2010) Effects of laurel (Laurus nobilis) on the non-specific immune responses of rainbow trout (Oncorhynchus mykiss, Walbaum). J Anim Vet Adv 9(8):1275–1279. https://doi.org/10.3923/javaa.2010.1275.1279

    Article  CAS  Google Scholar 

  • Bilen S, Bilen MA (2012) Tetra (Cotinus coggygria) ve defne (Laurus nobilis) bitkilerinin alabalıklarda (Oncorhynchus mykiss) büyümeyi teşvik edici etkileri. Alinteri J Agr Sci 22(B):26–33

    Google Scholar 

  • Bilen S, Kızak V, Gezen AM (2013) Floating fish farm unit (3FU) Is it an appropriate method for Salmonid production. Mar Sci Tech Bull 2(1):9–13

    Google Scholar 

  • Bilen S, Altunoğlu ÇY, Ulu F, Biswas G (2016) Innate immune and growth promoting responses to caper (Capparis spinosa) extract in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immun 57:206–212. https://doi.org/10.1016/j.fsi.2016.08.040

    Article  CAS  Google Scholar 

  • Bilen S, Elbeshti HTAG (2019) A new potential therapeutic remedy against Aeromonas hydrophila infection in rainbow trout (Oncorhynchus mykiss) using tetra, Cotinus coggygria. J Fish Dis 42(10):1369-1381. https://doi.org/10.1111/jfd.13061

  • Bilen S, Altief TAS, Özdemir KY, Salem MOA, Terzi E, Güney K (2020a) Effect of lemon balm (Melissa officinalis) extract on growth performance, digestive and antioxidant enzyme activities, and immune responses in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 46(1):471–481

    Article  CAS  Google Scholar 

  • Bilen S, Karga MK, Altunoğlu YÇ, Ferhat ULU, Biswas G (2020b) Immune responses and growth performance of the aqueous methanolic extract of malva sylvestris in Oncorhynchus mykiss. Mar Sci Tech Bull 9(2):159–167

    Article  Google Scholar 

  • Elbesthi RTA, Özdemir KY, Taştan Y, Bilen S, Sönmez AY (2020) Effects of ribwort plantain (Plantago lanceolata) extract on blood parameters, immune response, antioxidant enzyme activities, and growth performance in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 46(4):1295–1307. https://doi.org/10.1007/s10695-020-00790-z

    Article  CAS  PubMed  Google Scholar 

  • Elgaml SA, Khalil R, Hashish EA, El-Murr A (2015) Protective effects of selenium and alpha-tocopherol against lead-induced hepatic and renal toxicity in Oreochromis niloticus. J Aquacult Res Dev 6:1. https://doi.org/10.4172/2155-9546.1000299

    Article  CAS  Google Scholar 

  • Ellis AE (1990) Lysozyme assays. In: Stolen JS, Fletcher TC, Anderson DP, Roberson BS, Van Muiswinkel WB (eds) Techniques in fish immunology, 1st edn. SOS Publications, New Jersey, pp 101–103

    Google Scholar 

  • Engel K, Schmidt U, Reuter J, Weckesser S, Simon-Haarhaus B, Schempp CM (2007) Usnea barbata extract prevents ultraviolet-B induced prostaglandin E2 synthesis and COX-2 expression in HaCaT keratinocytes. J Photochem Photobiol, B 89(1):9–14

    Article  CAS  Google Scholar 

  • FAO (2018) Aquaculture Department. The state of world fisheries and aquaculture, Rome

    Google Scholar 

  • Gülçin O, Beydemir S, Hisar O, Köksal E, Reiter RJ (2009) Melatonin administration increases antioxidant enzymes activities and reduces lipid peroxidation in the rainbow trout (Oncorhynchus mykiss, Walbaum) erythrocytes. Turk J Vet Anim Sci 33:241–245

    Google Scholar 

  • Keleştemur GT, Özdemir Y (2013) Effects of dietary vitamin a and e on growth performance and antioxidant status in blood of juvenile rainbow trout (Oncorhynchus mykiss, w. 1792) exposed to flow rate stress. J Anim Plant Sci 23:821–827

    Google Scholar 

  • Kızak MK, Celik HT (2012) The effects of different dosage of kefir with different durations on growth performances and antioxidant system in the blood and liver tissues of Çoruh trout (Salmo coruhensis). Turk J Fish Aquat Sc 12:1–2. https://doi.org/10.4194/1303-2712-v12_2_12

    Article  Google Scholar 

  • Li ZH, Li P, Randak T (2010) Effect of a human pharmaceutical carbamazepine on antioxidant responses in brain of a model teleost in vitro: an efficient approach to biomonitoring. J Appl Toxicol 30:644–648. https://doi.org/10.1002/jat.1534

    Article  CAS  PubMed  Google Scholar 

  • Lushchak VI (2014) Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact 224:164–175

    Article  CAS  Google Scholar 

  • Madamombe IT, Afolayan AJ (2003) Evaluation of antimicrobial activity of extracts from South African Usnea barbata. Pharm Biol 41(3):199–202

    Article  Google Scholar 

  • Mir MA, Sawhney SS, Jassal MMS (2013) Qualitative and quantitative analysis of phytochemicals of Taraxacum officinale. Wudpecker J Pharm Pharmocol 2(1):1–5

    CAS  Google Scholar 

  • Özlüer-Hunt A, Özkan-Yılmaz F, Berköz M, Engin K, Gündüz SG, Yalın S (2016) Effects of dietary nucleotide yeast on immune responses and antioxidant enzyme activities of rainbow trout juveniles (Oncorhynchus mykiss). Isr J Aquacult Bamidgeh 68:1264–1276

    Google Scholar 

  • Ricker WE (1979) Growth rates and models. In: Hoar WS, Randall DJ, Brett JR (eds) Fish Physiology. Academic Press, New York, pp 677–743

    Google Scholar 

  • Şahan A, Duman S, Çolak SÖ, Çınar E, Bilgin R (2017) Determination of some hematological and non-specific immune defences, oxidative stress and histopathological status in rainbow trout (Oncorhynchus mykiss) fed rosehip (Rosa canina) to Yersinia ruckeri. Turk J Fish Aquat Sc 17:91–100. https://doi.org/10.4194/1303-2712-v17_1_11

    Article  Google Scholar 

  • Sahoo PK, Kumari J, Mishra BK (2005) Non-specific immune responses in juveniles of Indian major carps. J Appl Ichthyol 21:151–155. https://doi.org/10.1111/j.1439-0426.2004.00606.x

    Article  Google Scholar 

  • Siwicki AK, Anderson DP, Rumsey GL (1994) Dietary intake of immunostimulants by rainbow trout effects non-specific immunity and protection against furuncluosis. Vet Immunol Immunopathol 41:125–139

    Article  CAS  Google Scholar 

  • Sönmez AY, Bilen S, Albayrak M, Yılmaz S, Biswas G, Hisar O, Yanık T (2015a) Effects of dietary supplementation of herbal oils containing 1, 8-cineole, carvacrol or pulegone on growth performance, survival, fatty acid composition, and liver and kidney histology of rainbow trout (Oncorhynchus mykiss) fingerlings. Turk J Fish Aquat Sc 15:813–819. https://doi.org/10.4194/1303-2712-v15_4_04

    Article  Google Scholar 

  • Sönmez AY, Bilen S, Alak G, Hisar O, Yanık T, Biswas G (2015b) Growth performance and Antioxidant Enzyme Activities in rainbow trout (Oncorhynchus mykiss) Juveniles Fed Diets Supplemented with Sage, Mint and Thyme Oils. Fish Physiol Biochem 41:165–175. https://doi.org/10.1007/s10695-014-0014-9

    Article  CAS  PubMed  Google Scholar 

  • Terzi E, Kucukkosker B, Bilen S, Kenanoglu ON, Corum O, Özbek M, Parug SS (2021) A novel herbal immunostimulant for rainbow trout (Oncorhynchus mykiss) against Yersinia ruckeri. Fish Shellfish Immunol 110:55–66

    Article  CAS  Google Scholar 

  • Thirunavukkarasu P, Ramkumar L, Ramanathan T, Silambarasan D (2010) Anti oxidant activity of selected coastal medicinal plants. World J Fish Mar Sci 2:134–137

    CAS  Google Scholar 

  • Yagi K (1984) Assay for plasma lipid peroxidase. Methods Enzymol 109:328–331

    Article  Google Scholar 

  • Yonar ME, Yonar SM, Pala A, Silici S, Sağlam N (2015) Trichlorfon-induced haematological and biochemical changes in Cyprinus carpio: ameliorative effect of propolis. Dis Aquat Organ 114:209–216. https://doi.org/10.3354/dao02866

    Article  CAS  PubMed  Google Scholar 

  • Vaglio A, Landriscina C (1999) Changes in liver enzyme activity in the Teleost Sparus aurata in response to cadmium intoxication. Ecotoxicol Environ Saf 43(1):111–116. https://doi.org/10.1006/eesa.1999.1778

    Article  CAS  PubMed  Google Scholar 

  • Zhang C-x, Huang F, Li J, Wang L, Song K, Mai K-s (2016) Interactive effects of dietary magnesium and vitamin E on growth performance, body composition, blood parameters and antioxidant status in Japanese sea bass (Lateolabrax japonicus) fed oxidized oil. Aquacult Nutr 22:708–722. https://doi.org/10.1111/anu.12393

    Article  CAS  Google Scholar 

  • Zhao Y, Jiang X, Kong X, Di G, Nie G, Li X (2017) Effects of hypoxia on lysozyme activity and antioxidant defences in the kidney and spleen of Carassius auratus. Aquac Res 48:223–235. https://doi.org/10.1111/are.12876

    Article  CAS  Google Scholar 

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Acknowledgements

The study was presented as a Master’s thesis of Mohamed Omar Abdalla SALEM at Kastamonu University, Institute of Science.

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Authors and Affiliations

  1. Department of Aquaculture, Kastamonu University Institute of Science, Kastamonu, Turkey

    Mohamed Omar Abdalla Salem & Tarek A. Salem

  2. Department of Biology, Faculty of Education, Bani Walid University, Bani Walid, Libya

    Mohamed Omar Abdalla Salem

  3. Department of Basic Sciences, Faculty of Fisheries, Kastamonu University, Kastamonu, Turkey

    Keriman Yürüten Özdemir & Adem Yavuz Sönmez

  4. Department of Aquaculture, Faculty of Fisheries, Kastamonu University, Kastamonu, Turkey

    Soner Bilen

  5. Department of Forest Botany, Faculty of Forestry, Kastamonu University, Kastamonu, Turkey

    Kerim Güney

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  1. Mohamed Omar Abdalla Salem
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  4. Adem Yavuz Sönmez
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  5. Soner Bilen
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Contributions

Mohamed Omar Abdalla Salem, Tarek A. Salem, and Keriman Yürüten Özdemir performed the work. Adem Yavuz Sönmez analyzed data and interpreted the results. Soner Bilen designed the study and interpreted the results. Kerim Güney provided the plants and created the conception.

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Correspondence to Adem Yavuz Sönmez.

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Study protocol was approved in advance by the local Ethics Committee for Animal Research Studies at the Kastamonu University (KUHADYEK-2016.10).

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Salem, M.O.A., Salem, T.A., Yürüten Özdemir, K. et al. Antioxidant enzyme activities and immune responses in rainbow trout (Onchorhynchus mykiss) juveniles fed diets supplemented with dandelion (Taraxacum officinalis) and lichen (Usnea barbata) extracts. Fish Physiol Biochem 47, 1053–1062 (2021). https://doi.org/10.1007/s10695-021-00962-5

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