Skip to main content

Improvement of non-specific immunity, growth, and activity of digestive enzymes in Carassius auratus as a result of apple cider vinegar administration to diet

Fish Physiology and Biochemistry volume 46, pages 1387–1395 (2020)Cite this article

Abstract

This study was conducted to evaluate the effects of apple cider vinegar (ACV) administration on non-specific immunity of serum and skin mucus, growth indices, and activity of digestive enzymes (amylase, lipase, and protease) in Carassius auratus. For this purpose, 180 fish (weighing 7.35 ± 0.19 g) were allocated to 4 treatment groups with 3 replications in a completely randomized design. Fish were fed for 105 days using a basal diet supplemented with 0% (control), 1% (T 1), 2% (T 2), and 4% (T 3) ACV (contained 5% acetic acid). Results showed a significant increase in lysozyme activity, ACH50, and total immunoglobulin of skin mucus in fish fed with T2 diet (p < 0.05). Total immunoglobulin and lysozyme activity were significantly lower in the serum of fish fed with control diet than those fed with the mentioned treatment (p < 0.05). The highest value was observed in fish fed with T2 diet. Minimum (p < 0.05) complement activity (1.52 ± 0. 25 U ml−1) was observed in fish fed with control diet. The mean of the final weights (17.35 ± 1.39 g), daily growth (1.0 ± 0.01 g), and specific growth rate (2.19 ± 0.14) was significantly higher in T3 diet group than the controls (p < 0.05). While the highest amylase-specific activity was observed in the controls (p < 0.05), there was a significant increase in specific activity of protease, lipase, and alkaline phosphatase in T2 diet group (p < 0.05). According to the results of this study, the inclusion of a limited quantity of ACV (4%) into the diet can improve immunity and growth parameters in C. auratus.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1

References

  • Ahmadniaye Motlagh H, Safari O, Paolucci M (2019a) Effect of different levels of Calotropis persica seed powder on the growth parameters, immunity and gut microbiota of Oncorhynchus mykiss. Iran J Vet Sci Technol 11:43–50

  • Ahmadniaye Motlagh H, Safari O, Selahvarzi Y et al (2019b) Non-specific immunity promotion in response to garlic extract supplemented diets in female guppy (Poecilia reticulata). Fish Shellfish Immunol. https://doi.org/10.1016/j.fsi.2019.12.007

  • Ali TE-S, El-Sayed AM, Eissa MA-R, Hanafi HM (2018) Effects of dietary biogen and sodium butyrate on hematological parameters, immune response, and histological characteristics of Nile tilapia (Oreochromis niloticus) fingerlings. Aquac Int 26:139–150

    Article  Google Scholar 

  • Amar EC, Kiron V, Satoh S et al (2000) Effects of dietary βcarotene on the immune response of rainbow trout Oncorhynchus mykiss. Fish Sci 66:1068–1075

    Article  CAS  Google Scholar 

  • Baruah K, Pal AK, Sahu NP et al (2005) Dietary protein level, microbial phytase, citric acid and their interactions on bone mineralization of Labeo rohita (Hamilton) juveniles. Aquac Res 36:803–812

    Article  CAS  Google Scholar 

  • Bernfeld P (1951) Enzymes of starch degradation and synthesis. Adv Enzymol Relat Areas Mol Biol 12:379–428

    CAS  Google Scholar 

  • Castillo S, Rosales M, Pohlenz C, Gatlin DM (2014) Effects of organic acids on growth performance and digestive enzyme activities of juvenile red drum Sciaenops ocellatus. Aquaculture 433:6–12. https://doi.org/10.1016/j.aquaculture.2014.05.038

    Article  CAS  Google Scholar 

  • Chiu S-T, Tsai R-T, Hsu J-P et al (2008) Dietary sodium alginate administration to enhance the non-specific immune responses, and disease resistance of the juvenile grouper Epinephelus fuscoguttatus. Aquaculture 277:66–72

    Article  CAS  Google Scholar 

  • Chuchird N, Rorkwiree P, Rairat T (2015) Effect of dietary formic acid and astaxanthin on the survival and growth of Pacific white shrimp (Litopenaeus vannamei) and their resistance to Vibrio parahaemolyticus. SpringerPlus 4:440

    Article  Google Scholar 

  • Da Silva BC, do Nascimento Vieira F, JLP M et al (2013) Salts of organic acids selection by multiple characteristics for marine shrimp nutrition. Aquaculture 384–387:104–110. https://doi.org/10.1016/j.aquaculture.2012.12.017

    Article  CAS  Google Scholar 

  • Dai J, Li Y, Yang P et al (2018) Citric acid as a functional supplement in diets for juvenile turbot, Scophthalmus maximus L.: effects on phosphorus discharge, growth performance, and intestinal health. Aquaculture 495:643–653

    Article  CAS  Google Scholar 

  • Duan Y, Wang Y, Zhang J, Sun Y, Wang J (2018) Dietary effects of succinic acid on the growth, digestive enzymes, immune response and resistance to ammonia stress of Litopenaeus vannamei. Fish Shellfish Immunol 78:10–17

    Article  CAS  Google Scholar 

  • Elala NMA, Ragaa NM (2015) Eubiotic effect of a dietary acidifier (potassium diformate) on the health status of cultured Oreochromis niloticus. J Adv Res 6:621–629

    Article  Google Scholar 

  • Gao Y, Storebakken T, Shearer KD et al (2011) Supplementation of fishmeal and plant protein-based diets for rainbow trout with a mixture of sodium formate and butyrate. Aquaculture 311:233–240

    Article  CAS  Google Scholar 

  • Gawlicka A, Parent B, Horn MH et al (2000) Activity of digestive enzymes in yolk-sac larvae of Atlantic halibut (Hippoglossus hippoglossus): indication of readiness for first feeding. Aquaculture 184:303–314

    Article  CAS  Google Scholar 

  • Hamer HM, Jonkers D, Venema K et al (2008) The role of butyrate on colonic function. Aliment Pharmacol Ther 27:104–119

    Article  CAS  Google Scholar 

  • Hernández AJ, Satoh S, Kiron V (2013) The effect of citric acid supplementation on growth performance, phosphorus absorption and retention in rainbow trout (Oncorhynchus mykiss) fed a low-fishmeal diet. Cienc E Investig Agrar 40:397–406

    Article  Google Scholar 

  • Hoseinifar SH, Zoheiri F, Caipang CM (2016) Dietary sodium propionate improved performance, mucosal and humoral immune responses in Caspian white fish (Rutilus frisii kutum) fry. Fish Shellfish Immunol 55:523–528

    Article  CAS  Google Scholar 

  • Jun-sheng L, Jian-lin L, Ting-ting W (2006) Ontogeny of protease, amylase and lipase in the alimentary tract of hybrid juvenile tilapia (Oreochromis niloticus$\times$ Oreochromis aureus). Fish Physiol Biochem 32:295–303

    Article  Google Scholar 

  • Kondo T, Kishi M, Fushimi T, Kaga T (2009) Acetic acid upregulates the expression of genes for fatty acid oxidation enzymes in liver to suppress body fat accumulation. J Agric Food Chem 57:5982–5986

    Article  CAS  Google Scholar 

  • Li JS, Li JL, Wu TT (2009) Effects of non-starch polysaccharides enzyme, phytase and citric acid on activities of endogenous digestive enzymes of tilapia (Oreochromis niloticus × Oreochromis aureus). Aquac Nutr 15:415–420

    Article  CAS  Google Scholar 

  • Li L, He M, Xiao H et al (2018) Acetic acid influences BRL-3A cell lipid metabolism via the AMPK signalling pathway. Cell Physiol Biochem 45:2021–2030

    Article  CAS  Google Scholar 

  • Luckstadt C (2008) The use of acidifiers in fish nutrition. Perspect Agric Vet Sci Nutr Nat Resour 3:1–8

    Google Scholar 

  • Lückstädt C (2008) Effect of organic acid containing additives in worldwide aquaculture–sustainable production the non-antibiotic way. Acidifiers Anim Nutr 71

  • Motlagh H, Sarkheil M, Safari O, Paolucci M (2020) Supplementation of dietary apple cider vinegar as an organic acidifier on the growth performance, digestive enzymes and mucosal immunity of green terror (Andinoacara rivulatus). Aquac Res 51:197–205

    Article  Google Scholar 

  • Najdegerami EH, Baruah K, Shiri A et al (2015) Siberian sturgeon (Acipenser baerii) larvae fed Artemia nauplii enriched with poly-β-hydroxybutyrate (PHB): effect on growth performance, body composition, digestive enzymes, gut microbial community, gut histology and stress tests. Aquac Res 46:801–812

    Article  CAS  Google Scholar 

  • Nazıroğlu M, Güler M, Özgül C, Saydam G, Küçükayaz M, Sözbir E (2014) Apple cider vinegar modulates serum lipid profile, erythrocyte, kidney, and liver membrane oxidative stress in ovariectomized mice fed high cholesterol. J Membr Biol 247:667–673. https://doi.org/10.1007/s00232-014-9685-5

    Article  CAS  PubMed  Google Scholar 

  • Ng WK, Koh CB, Sudesh K, Siti-Zahrah A (2009) Effects of dietary organic acids on growth, nutrient digestibility and gut microflora of red hybrid tilapia, Oreochromis sp., and subsequent survival during a challenge test with Streptococcus agalactiae. Aquac Res 40:1490–1500. https://doi.org/10.1111/j.1365-2109.2009.02249.x

    Article  CAS  Google Scholar 

  • Ng WK, Koh CB, Teoh CY, Romano N (2015) Farm-raised tiger shrimp, Penaeus monodon, fed commercial feeds with added organic acids showed enhanced nutrient utilization, immune response and resistance to Vibrio harveyi challenge. Aquaculture 449:69–77. https://doi.org/10.1016/j.aquaculture.2015.02.006

    Article  CAS  Google Scholar 

  • Pereira SA, Jesus GFA, Cardoso L et al (2019) The intestinal health of silver catfish Rhamdia quelen can be changed by organic acid salts, independent of the chelating minerals. Aquaculture 505:118–126

    Article  CAS  Google Scholar 

  • Pourmozaffar S, Hajimoradloo A, Miandare HK (2017) Dietary effect of apple cider vinegar and propionic acid on immune related transcriptional responses and growth performance in white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 60:65–71. https://doi.org/10.1016/j.fsi.2016.11.030

    Article  CAS  PubMed  Google Scholar 

  • Pourmozaffar S, Hajimoradloo A, Paknejad H, Rameshi H (2019) Effect of dietary supplementation with apple cider vinegar and propionic acid on hemolymph chemistry, intestinal microbiota and histological structure of hepatopancreas in white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 86:900–905

    Article  CAS  Google Scholar 

  • Reda RM, Mahmoud R, Selim KM, El-Araby IE (2016) Effects of dietary acidifiers on growth, hematology, immune response and disease resistance of Nile tilapia, Oreochromis niloticus. Fish Shellfish Immunol 50:255–262

    Article  CAS  Google Scholar 

  • Romano N, Koh CB, Ng WK (2015) Dietary microencapsulated organic acids blend enhances growth, phosphorus utilization, immune response, hepatopancreatic integrity and resistance against Vibrio harveyi in white shrimp, Litopenaeus vannamei. Aquaculture 435:228–236. https://doi.org/10.1016/j.aquaculture.2014.09.037

    Article  CAS  Google Scholar 

  • Safari R, Hoseinifar SH, Kavandi M (2016) Modulation of antioxidant defense and immune response in zebra fish (Danio rerio) using dietary sodium propionate. Fish Physiol Biochem 42:1733–1739

    Article  CAS  Google Scholar 

  • Safari R, Hoseinifar SH, Nejadmoghadam S, Khalili M (2017) Apple cider vinegar boosted immunomodulatory and health promoting effects of Lactobacillus casei in common carp (Cyprinus carpio). Fish Shellfish Immunol 67:441–448. https://doi.org/10.1016/j.fsi.2017.06.017

    Article  CAS  PubMed  Google Scholar 

  • Salem AM, Amin RA (2012) Evaluation of some organic acids as potential decontaminants of Vibrio parahaemolyticus in fresh shrimp. World J Dairy Food Sci 7:41–48

    Google Scholar 

  • Sankaran K, Gurnani S (1972) On the variation in the catalytic activity of lysozyme in fishes. Indian J Biochem Biophys 9:162–165

    CAS  PubMed  Google Scholar 

  • Silva BC, Nolasco-Soria H, Magallón-Barajas F et al (2016) Improved digestion and initial performance of whiteleg shrimp using organic salt supplements. Aquac Nutr 22:997–1005

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Subramanian S, MacKinnon SL, Ross NW (2007) A comparative study on innate immune parameters in the epidermal mucus of various fish species. Comp Biochem Physiol B Biochem Mol Biol 148:256–263. https://doi.org/10.1016/j.cbpb.2007.06.003

    Article  CAS  PubMed  Google Scholar 

  • Sugiura SH, Dong FM, Hardy RW (1998) Effects of dietary supplements on the availability of minerals in fish meal; preliminary observations. Aquaculture 160:283–303

    Article  CAS  Google Scholar 

  • Walter K, Schütt C (1974) Alkaline phosphatase in serum: continuous assay. In: Methods of enzymatic analysis. Elsevier, Amsterdam, pp 860–864

    Chapter  Google Scholar 

  • Worthington CC (1988) Worthington enzyme manual: enzymes and related biochemicals. Worthington Biochemical Corporation

Download references

Acknowledgments

The authors are grateful to the staff at the Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad and the students Mr. Ali Baghalian, Mr. Erfan Parsa, and Mr. Mahammad Zarepor for their kind help.

Funding

This work was supported by Ferdowsi University of Mashhad [Research numbers 2/44318].

Author information

Authors and Affiliations

  1. Department of Fisheries, Faculty of Natural Resources and Environment, Ferdowsi University of Mashhad, Mashhad, Iran

    Hamidreza Ahmadniaye Motlagh & Omid Safari

  2. Department of Animal Science, Faculty of Agriculture, Ferdowsi University of Mashhad, Mashhad, Iran

    Ali Javadmanesh

Authors
  1. Hamidreza Ahmadniaye Motlagh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ali Javadmanesh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Omid Safari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hamidreza Ahmadniaye Motlagh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ahmadniaye Motlagh, H., Javadmanesh, A. & Safari, O. Improvement of non-specific immunity, growth, and activity of digestive enzymes in Carassius auratus as a result of apple cider vinegar administration to diet. Fish Physiol Biochem 46, 1387–1395 (2020). https://doi.org/10.1007/s10695-020-00797-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00797-6

Keywords

  • Non-specific immunity
  • Apple cider vinegar
  • Organic acids
  • Digestive enzyme