Year 2018, Volume 7 , Issue 1, Pages 12 - 20 2018-06-30

Effect of Tilia tomentosa methanolic extract on growth performance, digestive enzyme activity, immune system and haematological indices of common carp (Cyprinus carpio)

Ahmed Alhadi Almabrok [1] , Iman Daw Amhamed [2] , Gamaia Ali Mohamed [3] , Soner Bilen [4] , Tarek Abdalsalam Salem Altief [5]

This study was conducted to determine the effect of dietary supplementation with Tilia tomentosa on the growth performance, digestive enzyme activity, haematological indices and nonspecific immune indices of juvenile common carp (Cyprinus carpio). Fish with an average weight of 4.35 ± 0.16 g were fed a diet supplemented with an aqueous methanolic extract of T. tomentosa at a dose of 0% (control), 0.01%, 0.05% or 0.1% over 45 days. By the end of the study, the final weight, weight gain and specific growth rate were observed to be significantly higher for the 00.1% and 0.1% groups compared with the control group (P < 0.05). The feed conversion ratio was significantly decreased in the 0.05% and 0.1% groups compared with the control (P < 0.05). The activities of various digestive enzymes (amylase, lipase and trypsin) were also measured and no significant differences were observed compared to the control (P > 0.05). The mean cell volume of the 0.01% group was significantly increased compared to the control (P < 0.05) and increased lysozyme activity was observed in the 0.05% and 0.1% groups. Respiratory burst activity was significantly increased (P < 0.05) on days 15 and 30 for the 0.1% and 0.05% groups, respectively. No differences were observed for myeloperoxidase activity among the four groups. These results suggest that aqueous methanolic extract of T. tomentosa has a growth-promoting and immunostimulatory effect on common carp.

Tilia tomentosa, common carp, growth, haematology, digestive enzyme activity
  • Aklakur, M., Rather, M. A., Kumar, N. (2015). Nano delivery: an emerging avenue for nutraceuticals and drug delivery. Critical reviews in food science and nutrition, 56(14), 2352-2361.
  • Alexander, C. P., Kirubakaran, C. J. W., & Michael, R. D. (2010). Water soluble fraction of Tinospora cordifolia leaves enhanced the non-specific immune mechanisms and disease resistance in Oreochromis mossambicus. Fish & shellfish immunology, 29(5), 765-772.
  • Alishahi, M., Ranjbar, M., Ghorbanpoor, M., Peyghan, R., & Mesbah, M. (2010). Effects of dietary Aloe vera on some specific and nonspecific immunity in the common carp (Cyprinus carpio). Iranian Journal of Veterinary Medicine, 4(3),189–195.
  • Awad, E., Austin, D., & Lyndon, A. R. (2013). Effect of black cumin seed oil (Nigella sativa) and nettle extract (Quercetin) on enhancement of immunity in rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture, 388, 193-197.
  • Baser, K.H.C., Tümen,G., Malyer, H., and Kirimer,N. (2006). Plants used for common cold in Turkey. In Proceedings of the IVth International Congress of Ethnobotany (ICEB 2005) (Vol. 133, p. 137).
  • Bilen, S., Biswas, G., Otsuyama, S., Kono, T., Sakai, M., & Hikima, J. I. (2014). Inflammatory responses in the Japanese pufferfish (Takifugu rubripes) head kidney cells stimulated with an inflammasome-inducing agent, nigericin. Developmental & Comparative Immunology, 46(2), 222-230.
  • Bilen, S., Ünal, S., & Güvensoy, H. (2016). Effects of oyster mushroom (Pleurotus ostreatus) and nettle (Urtica dioica) methanolic extracts on immune responses and resistance to Aeromonas hydrophila in rainbow trout (Oncorhynchus mykiss). Aquaculture, 454, 90-94.
  • Bilen, S., & Bulut, M. (2010). Effects of laurel (Laurus nobilis) on the non-specific immune responses of rainbow trout (Oncorhynchus mykiss, Walbaum). Journal of Animal and Veterinary Advances, 9(8), 1275-1279.
  • Bilen, S., Bulut, M., & Bilen, A. M. (2011). Immunostimulant effects of Cotinus coggyria on rainbow trout (Oncorhynchus mykiss). Fish & shellfish immunology, 30(2), 451-455.
  • Bilen, S., Yılmaz, S., & Bilen, A. M. (2013). Influence of tetra (Cotinus coggygria) extract against Vibrio anguillarum infection in koi carp, Cyprinus carpio with reference to haematological and immunological changes. Turkish Journal of Fisheries and Aquatic Sciences, 13(3),517–522.
  • Bilen, S., Yılmaz, S., Bilen, A. M., & Biswas, G. (2014). Effects of Dietary Incorporation of Tetra (Cotinus coggygria) Extract on Immune Response and Resistance to Aeromonas hydrophila in Koi Carp (Cyprinus carpio). The Israeli Journal of Aquaculture-Bamidgeh, 66, 1-6.
  • Biswas, G., Korenaga, H., Nagamine, R., Kawahara, S., Takeda, S., Kikuchi, Y., ... & Sakai, M. (2013). Cytokine mediated immune responses in the Japanese pufferfish (Takifugu rubripes) administered with heat-killed Lactobacillus paracasei spp. paracasei (06TCa22) isolated from the Mongolian dairy product. International immunopharmacology, 17(2), 358-365.
  • Blaxhall, P. C., & Daisley, K. W. (1973). Routine haematological methods for use with fish blood. Journal of fish biology, 5(6), 771-781.
  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 72(1-2), 248-254.
  • Casillas, E., & Smith, L. S. (1977). Effect of stress on blood coagulation and haematology in rainbow trout (Salmo gairdneri). Journal of Fish Biology, 10(5), 481-491.
  • Cech Jr, J. J., & Wohlschlag, D. E. (1982). Seasonal patterns of respiration, gill ventilation, and hematological characteristics in the striped mullet, Mugil cephalus L. Bulletin of Marine Science, 32(1), 130-138.
  • Chakrabarty, P., & Banerjee, V. (1988). Effect of organophosphorus pesticides on the peripheral hemogram of the fish Channa punctatus. Environment and Ecology, 6(2), 390-394.
  • Chakrabarti, R., & Vasudeva, R. Y. (2006). Achyranthes aspera stimulates the immunity and enhances the antigen clearance in Catla catla. International Immunopharmacology, 6(5), 782-790.
  • Choi, S. H., Park, K. H., Yoon, T. J., Kim, J. B., Jang, Y. S. & Choe, C. H. (2008). Dietary Korean mistletoe enhances cellular non-specific immune responses and survival of Japanese eel (Anguilla japonica). Fish & shellfish immunology, 24(1), 67-73.
  • Citarasu, T. (2010). Herbal biomedicines: a new opportunity for aquaculture industry. Aquaculture International, 18(3), 403-414.
  • Cockson, A., & Bourne, D. (1972). Enzymes in the digestive tract of two species of euryhaline fish. Comparative Biochemistry and Physiology--Part A: Physiology, 41(4), 715-718.
  • Collazos, M. E., Ortega, E., Barriga, C., & Rodrìguez, A. B. (1998). Seasonal variation in haematological parameters in male and female Tinca tinca. Molecular and cellular Biochemistry, 183(1-2), 165-168.
  • Dalmo, R. A., Ingebrigtsen, K., & Bøgwald, J. (1997). Non‐specific defence mechanisms in fish, with particular reference to the reticuloendothelial system (RES). Journal of Fish Diseases, 20(4), 241-273.
  • Erlanger, B. F., Kokowsky, N., & Cohen, W. (1961). The preparation and properties of two new chromogenic substrates of trypsin. Archives of biochemistry and biophysics, 95(2), 271-278.
  • Evelyn, T. P. T. (2002). Finfish immunology and its use in preventing infectious diseases in cultured finfish. Diseases in Asian Aquaculture IV,(CR Lavilla-Pitogo & ER Cruz-Lacierda ed.), 303-324.
  • Farahi, A., Kasiri, M., Sudagar, M., Soleimani Iraei, M., & Zorriehzahra, S. M. J. (2012). Effect of dietary supplementation of Melissa officinalis and aloe vera on hematological traits, lipid oxidation of carcass and performance in rainbow trout (Oncorhynchus mykiss). Online Journal of Animal and Feed Research, 1, 1-5.
  • Fukumoto, L. R., & Mazza, G. (2000). Assessing antioxidant and prooxidant activities of phenolic compounds. Journal of agricultural and food chemistry, 48(8), 3597-3604.
  • Furne, M., Hidalgo, M. C., Lopez, A., Garcia-Gallego, M., Morales, A. E., Domezain, A., Domezaine´, J. & Sanz, A. (2005). Digestive enzyme activities in Adriatic sturgeon Acipenser naccarii and rainbow trout Oncorhynchus mykiss. A comparative study. Aquaculture, 250(1-2), 391-398.
  • Garcia, M. P., Echevarria, G., Martinez, F. J., & Zamora, S. (1992). Influence of blood sample collection on the haematocrit value of two teleosts: rainbow trout (Oncorhynchus mykiss) and European sea bass (Dicentrarchus labrax L.). Comparative biochemistry and physiology. Comparative physiology, 101(4), 733-736.
  • Gawlicka, A., Parent, B., Horn, M. H., Ross, N., Opstad, I., & Torrissen, O. J. (2000). Activity of digestive enzymes in yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding. Aquaculture, 184(3-4), 303-314.
  • Gjedrem, T., Robinson, N., Rye, M. (2012). The importance of selective breeding in aquaculture to meet future demands for animal protein: a review. Aquaculture, 350, 117-129.‏Gudding, R., Lillehaug, A., & Evensen, Ø. (1999). Recent developments in fish vaccinology. Veterinary Immunology and Immunopathology, 72(1-2), 203-212.
  • Haghighi, M., & Rohani, M. S. (2013). The effects of powdered ginger (Zingiber officinale) on the haematological and immunological parameters of rainbow trout Oncorhynchus mykiss. Journal of medicinal Plant and Herbal therapy research, 1(1), 8-12.
  • Haghighi, M., Sharif Rohani, M., Samadi, M., Tavoli, M., Eslami, M., & Yusefi, R. (2014). Study of effects Aloe vera extract supplemented feed on hematological and immunological indices of rainbow trout (Oncorhynchus mykiss). International Journal of Advanced Biological and Biomedical Research, 2(6), 2143-2154.
  • Harikrishnan, R., Balasundaram, C., & Heo, M. S. (2011). Impact of plant products on innate and adaptive immune system of cultured finfish and shellfish. Aquaculture, 317(1-4), 1-15.
  • Harikrishnan, R., Jin, C. N., Kim, M. C., Kim, J. S., Balasundaram, C., & Heo, M. S. (2010). Effectiveness and immunomodulation of chemotherapeutants against scuticociliate Philasterides dicentrarchi in olive flounder. Experimental parasitology, 124(3), 306-314.
  • Hickey, C. R. (1976). Fish hematology, its uses and significance. NY Fish Game J, 23(2), 170-175.
  • Ieri, F., Innocenti, M., Possieri, L., Gallori, S., & Mulinacci, N. (2015). Phenolic composition of “bud extracts” of Ribes nigrum L., Rosa canina L. and Tilia tomentosa M. Journal of pharmaceutical and biomedical analysis, 115, 1-9.
  • Iqbal, K. J., Ashraf, M., Javid, A., Khan, N., Abbas, F., Hafeez-ur-Rehman, M., Rafique, M. K., Rasool, F., Azmat, H., & Altaf, M. (2016). Effect of Different Plant and Animal Origin (Fishmeal) Feeds on Digestive Enzyme Activity and Haematology of Juvenile Labeo rohita. Pakistan J. Zool, 48(1), 201-207.
  • Iwama, G. K., Greer, G. L., & Larkin, P. A. (1976). Changes in some hematological characteristics of coho salmon (Oncorhynchus kisutch) in response to acute exposure to dehydroabietic acid (DHAA) at different exercise levels. Journal of the Fisheries Board of Canada, 33(2), 285-289.
  • Jian, J., and Wu, Z. (2004). Influences of traditional Chinese medicine on non-specific immunity of Jian carp (Cyprinus carpio var. Jian). Fish & shellfish immunology, 16(2), 185-191.
  • Johnston, J. R. (1978, November). Oxygen metabolism and the microbicidal activity of macrophages. In Federation Proceedings (Vol. 37, No. 13, pp. 2759-2764).
  • Kaleeswaran, B., Ilavenil, S., & Ravikumar, S. (2011). Dietary supplementation with Cynodon dactylon (L.) enhances innate immunity and disease resistance of Indian major carp, Catla catla (Ham.). Fish & shellfish immunology, 31(6), 953-962.
  • Kawai, S. and Ikeda, S., (1973). Studies in digestive enzymes of fishes. III. Development of the digestive enzymes of rainbow trout after hatching and the effect of dietary change on the activities of digestive enzymes in the juvenile stage. Bulletin of the Japanese Society for the Science of Fish., 38:265-270.
  • Khondoker, S., Hossain, M. M. M., Hasan-Uj-Jaman, M., Alam, M. E., Zaman, M. F. U., & Tabassum, N. (2016). Effect of Nigella sativa (Black Cumin Seed) to Enhance the Immunity of Common Carp (Cyprinus carpio) Against Pseudomonas fluorescens. American Journal of Life Sciences, 4(3), 87-92.
  • Kono, T., Hamasuna, S., Korenaga, H., Iizasa, T., Nagamine, R., Ida, T., & Sakai, M. (2012). The role of neuromedin U during inflammatory response in the common carp. Fish & shellfish immunology, 32(1), 151-160.‏
  • Kori-Siakpere, O., Ake, J. E. G., & Idoge, E. (2005). Haematological characteristics of the African snakehead, Parachanna obscura. African Journal of Biotechnology, 4(6), 527-530.
  • Kour, D., Sharma, L. L., & Sharma, B. K. (2004). Use of herb, Bala (Sida cordifolia Linn.) as growth promoter in the supplementary feed of Cirrhinus mrigala (Ham.). Indian Journal of Fisheries, 51(4), 501-504.
  • Kumar, I. V., Chelladurai, G., Veni, T., Peeran, S. S. H., & Mohanraj, J. (2014). Medicinal plants as immunostimulants for health management in Indian cat fish. Journal of Coastal Life Medicine, 2(6), 426-430.
  • Lee-Shing, F., & Shu-Fen, C. (1989). Effect of salinity on the activities of digestive proteases from the tilapia fish, Oreochromis niloticus in different culture environments. Comparative Biochemistry and Physiology Part A: Physiology, 93(2), 439-443.
  • Lewis, S. M., Bain, B. J., and Bates, I. (2001). Dacie and Lewis Practical Haematology, 9th ed. London: Churchill Livingstone;. p 633.
  • Mahdavi, M., Hajimoradloo, A., Ghorbani, R., (2013). Effect of Aloe vera extract on growth parameters of common carp (Cyprinus carpio). World Journal of Medical Sciences, 9, 55–60.
  • Moriarty, D. J. W. (1973). The physiology of digestion of blue‐green algae in the cichlid fish, Tilapia nilotica. Journal of Zoology, 171(1), 25-39.
  • Mostafa, A.A.Z.M., Ahmad, M.H., Mousallamy, A., Samir, A., (2009). Effect of using dried Fenugreek seeds as natural feed additives on growth performance, feed utilization, whole-body coMyeloperoxidase activity sition and entropathogenic Aeromonas hydrophila-challinge of monsex Nile tilapia O. niloticus (L) fingerlings. Australian Journal of Basic and Applied Sciences, 3(2), 1234-1245.
  • Ojha, M. L., Chadha, N. K., Saini, V. P., Damroy, S., & Chandraprakash, S. P. (2014). Effect of ethanolic extract of Mucuna pruriens on growth, metabolism and immunity of Labeo rohita (Hamilton, 1822) fingerlings. International Journalof Fauna & Biological Studies, 1(5), 1-9.
  • Oluyemi, K. G., Adecprusi, E. A., and Olanrewage, J. (2008). Basic hematological parameters in African cat fish, Clarias gariepinus(Burchell, 1822) FED ascribe acid supplemented diets. Res J Ani Sci 2(1), 17-21.
  • Örün, I., Dörücü, M., & Yazlak, H. (2003). Haematological parameters of three cyprinid fish species from Karakaya Dam Lake, Turkey. Online J. Biol. Sci, 3, 320-328.
  • Pakravan, S., Hajimoradloo, A., & Ghorbani, R. (2012). Effect of dietary willow herb, Epilobium hirsutum extract on growth performance, body composition, haematological parameters and Aeromonas hydrophila challenge on common carp, Cyprinus carpio. Aquaculture research, 43(6), 861-869.
  • Patra, B. B., Panda, R. P., and Patra, A. K., (2014). Seasonal Variations in Certain Hematological Factors of Catla Catla (Hamilton 1822). Journal of Applied Physics, 6, 1-7.
  • Rao, Y. V., Das, B. K., Jyotyrmayee, P. & Chakrabarti, R. (2006). Effect of Achyranthes aspera on the immunity and survival of Labeo rohita infected with Aeromonas hydrophila. Fish & Shellfish Immunology, 20(3), 263-273.
  • Rodríguez, A., Esteban, M., & Meseguer, J. (2003). Phagocytosis and peroxidase release by seabream (Sparus aurata L.) leucocytes in response to yeast cells. The Anatomical Record, 272(1), 415-423.
  • Sahoo, P. K., Kumari, J., & Mishra, B. K. (2005). Non‐specific immune responses in juveniles of Indian major carps. Journal of Applied Ichthyology, 21(2), 151-155.
  • Saurabh, S., & Sahoo, P. K. (2008). Lysozyme: an important defence molecule of fish innate immune system. Aquaculture research, 39(3), 223-239.
  • Secombes, C. J. (1996). The nonspecific immune system: cellular defenses. The fish immune system: organism, pathogen and environment, 63-103.
  • Secombes, C. J., & Fletcher, T. C. (1992). The role of phagocytes in the protective mechanisms of fish. Annual Review of Fish Diseases, 2, 53-71.
  • Seung-Cheol, J.I., Jeong, G., Gwang-Soon, I.M., Lee, S., Yoo, J., Takii, K., (2007). Dietary medicinal herbs improve growth performance, fatty acid utilization, and stress recovery of Japanese flounder. Fisheries Science, 73(1), 70-76.
  • Siddiqui, A. Q., & Naseem, S. M. (1979). The haematology of Rohu, Labeo rohita. Journal of fish Biology, 14(1), 67-72.
  • Tekinay, A.A. and Davies, S.J. (2001). Dietary carbohydrate level influencing feed intake, nutrient utilisation and plasma glucose concentration in the rainbow trout, Oncorhynchus mykiss. Journal of Veterinary and Animal Sciences, 25(5), 657-666.
  • Worthington, C., (1991). Worthington enzyme manual related Biochemical. Freehold, New Jersey, USA.
  • Xie, J., Liu, B., Zhou, Q., Su, Y., He, Y., Pan, L. Ge, X., Xu, P., (2008). Effects of anthraquinone extract from rhubarb Rheum officinale Bail on the crowding stress response and growth of common carp Cyprinus carpio var. Jian. Aquaculture, 281, 5–11.
  • Yin, G., Ardó, L. Á. S. Z. L. Ó., Thompson, K. D., Adams, A., Jeney, Z., & Jeney, G. (2009). Chinese herbs (Astragalus radix and Ganoderma lucidum) enhance immune response of carp, Cyprinus carpio, and protection against Aeromonas hydrophila. Fish & Shellfish Immunology, 26(1), 140-145.
  • Yılmaz, S., Ergün, S. & Çelik, E. S. (2012). Effects of herbal supplements on growth performance of sea bass (Dicentrarchus labrax): Change in body composition and some blood parameters. J. BioSci. Biotech, 1(3), 217-222.
Primary Language en
Subjects Marine and Freshwater Biology
Journal Section Research Article

Author: Ahmed Alhadi Almabrok
Institution: Kastamonu University, Institute of Science, Department of Aquaculture, Kastamonu, Turkey

Author: Iman Daw Amhamed
Institution: Kastamonu University, Institute of Science, Department of Aquaculture, Kastamonu, Turkey

Author: Gamaia Ali Mohamed
Institution: Kastamonu University, Institute of Science, Department of Aquaculture, Kastamonu, Turkey

Author: Soner Bilen
Institution: Kastamonu University, Faculty of Fisheries
Country: Turkey

Author: Tarek Abdalsalam Salem Altief (Primary Author)
Institution: Kastamonu University, Institute of Science, Department of Aquaculture, Kastamonu, Turkey


Application Date : May 4, 2018
Acceptance Date : May 23, 2018
Publication Date : June 30, 2018

APA Almabrok, A , Amhamed, I , Mohamed, G , Bilen, S , Altief, T . (2018). Effect of Tilia tomentosa methanolic extract on growth performance, digestive enzyme activity, immune system and haematological indices of common carp (Cyprinus carpio). Marine Science and Technology Bulletin , 7 (1) , 12-20 . DOI: 10.33714/masteb.421047