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Growth Performance, Antioxidative Capacity, and Intestinal Histomorphology of Grey Mullet (Liza ramada)–Fed Dietary Zinc Nanoparticles

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Abstract

Zinc is one of the essential microelements involved in vital physiological and biological functions in the fish body. The study evaluated the growth performance, antioxidative capacity, and intestinal histomorphology of Grey Mullet (Liza ramada)–fed dietary zinc nanoparticles (ZnO-NPs) at 0, 10, 20, and 40 mg/kg for the first time. The final weight and specific growth rate (SGR) of Grey Mullet–fed dietary ZnO-NPs at 20 and 40 mg/kg were meaningfully enhanced (p < 0.05). Further, the weight gain (WG) was significantly higher in fish treated with ZnO-NPs than the control, and fish fed 20–40 mg/kg had the highest WG (p < 0.05). The feed conversion ratio (FCR) was meaningfully reduced in fish fed 20–40 mg ZnO-NPs/kg (p < 0.05). The histomorphology of the intestines revealed a significant improvement in villus height, villus width, and goblet cells by ZnO-NPs. The lysozyme activity, phagocytic activity, and phagocytic index showed higher levels in Grey Mullet–fed dietary ZnO-NPs at 20 mg/kg than fish fed 0, 10, and 40 mg/kg (p < 0.05). Superoxide dismutase (SOD) and catalase (CAT) were markedly improved in Grey Mullet treated with ZnO-NPs compared with the control, and the group of fish treated with 20 mg/kg had the highest SOD and CAT (p < 0.05). Glutathione peroxidase (GPx) was significantly higher in fish fed 20–40 mg/kg ZnO-NPs than fish fed 0–10 mg/kg and fish fed 40 mg ZnO-NPs/kg showing the highest GPx value (p < 0.05). The concentration of malondialdehyde was markedly lowered in Grey Mullet fed ZnO-NPs at varying levels (p < 0.05). Based on the overall results, the regression analysis suggests that ZnO-NPs can be included at 24.61–35.5 mg/kg for the best performances of Grey Mullet.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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References

  1. FAO, Food and Agriculture Organization of the United Nations (2018) Aquaculture Department, The state of world fisheries and aquaculture. Rome, p 2430

  2. Tacon AGJ, Metian M, McNevin AA (2021) Future feeds: suggested guidelines for sustainable development. Rev Fish Sci Aquac: 1–13. https://doi.org/10.1080/23308249.2021.1898539

  3. Dawood MAO et al (2021) The influence of coconut oil on the growth, immune, and antioxidative responses and the intestinal digestive enzymes and histomorphometry features of Nile tilapia (Oreochromis niloticus). Fish Physiol Biochem. https://doi.org/10.1007/s10695-021-00943-8

  4. Mugwanya M et al (2021) Biofloc systems for sustainable production of economically important aquatic species: a review. Sustainability 13(13). https://doi.org/10.3390/su13137255

  5. Tacon AGJ (2020) Trends in global aquaculture and aquafeed production: 2000–2017. Rev Fish Sci Aquac 28(1):43–56

    Article  Google Scholar 

  6. Mzengereza K et al (2021) Effect of substituting fish oil with camelina oil on growth performance, fatty acid profile, digestibility, liver histology, and antioxidative status of red seabream (Pagrus major). Animals 11(7). https://doi.org/10.3390/ani11071990

  7. Cottrell RS et al (2020) Global adoption of novel aquaculture feeds could substantially reduce forage fish demand by 2030. Nature Food 1(5):301–308

    Article  Google Scholar 

  8. Pierri BdS et al (2021) Different levels of organic trace minerals in diets for Nile tilapia juveniles alter gut characteristics and body composition, but not growth. Aquac Nutr 27(1):176–186

    Article  CAS  Google Scholar 

  9. Watanabe T, Kiron V, Satoh S (1997) Trace minerals in fish nutrition. Aquaculture 151(1):185–207

    Article  CAS  Google Scholar 

  10. Dawood MAO (2021) Nutritional immunity of fish intestines: important insights for sustainable aquaculture. Rev Aquac 13(1):642–663

    Article  Google Scholar 

  11. El-Sharawy ME et al (2021) Studying the influence of copper on the growth behavior, antioxidative status, and histology of the intestine and liver of Striped Catfish (Pangasianodon hypophthalmus). Biol Trace Elem Res. https://doi.org/10.1007/s12011-021-02717-y

  12. Viegas MN et al (2021) Effect of dietary manganese and zinc levels on growth and bone status of Senegalese sole (Solea senegalensis) post-larvae. Biol Trace Elem Res 199(5):2012–2021

    Article  CAS  PubMed  Google Scholar 

  13. Broom LJ, Monteiro A, Piñon A (2021) Recent advances in understanding the influence of zinc, copper, and manganese on the gastrointestinal environment of pigs and poultry. Animals 11(5). https://doi.org/10.3390/ani11051276

  14. Angeles-Hernandez JC et al (2021) Zinc supplementation improves growth performance in small ruminants: a systematic review and meta-regression analysis. Anim Prod Sci 61(7):621–629

    Article  CAS  Google Scholar 

  15. Davis DA, Gatlin DM (1996) Dietary mineral requirements of fish and marine crustaceans. Rev Fish Sci 4(1):75–99

    Article  Google Scholar 

  16. Kazemi E et al (2020) Effect of different dietary zinc sources (mineral, nanoparticulate, and organic) on quantitative and qualitative semen attributes of rainbow trout (Oncorhynchus mykiss). Aquaculture 515:734529

    Article  CAS  Google Scholar 

  17. Meiler KA et al (2021) Oxidative stress-related gene expression in diploid and triploid rainbow trout (Oncorhynchus mykiss) fed diets with organic and inorganic zinc. Aquaculture 533:736149

    Article  CAS  Google Scholar 

  18. Mohseni M, Hamidoghli A, Bai SC (2021) Organic and inorganic dietary zinc in beluga sturgeon (Huso huso): effects on growth, hematology, tissue concertation and oxidative capacity. Aquaculture 539:736672

    Article  CAS  Google Scholar 

  19. El-Saadony MT et al (2021) Impact of mycogenic zinc nanoparticles on performance, behavior, immune response, and microbial load in Oreochromis niloticus. Saudi J Biol Sci. https://doi.org/10.1016/j.sjbs.2021.04.066

  20. Nasr-Eldahan S et al (2021) A review article on nanotechnology in aquaculture sustainability as a novel tool in fish disease control. Aquac Int. https://doi.org/10.1007/s10499-021-00677-7

  21. DawitMoges F et al (2020) Mechanistic insights into diverse nano-based strategies for aquaculture enhancement: a holistic review. Aquaculture 519:734770

    Article  Google Scholar 

  22. Mohammady EY et al (2021) Comparative effects of dietary zinc forms on performance, immunity, and oxidative stress-related gene expression in Nile tilapia, Oreochromis niloticus. Aquaculture 532:736006

    Article  CAS  Google Scholar 

  23. Abdelnour SA et al (2021) Nanominerals: fabrication methods, benefits and hazards, and their applications in ruminants with special reference to selenium and zinc nanoparticles. Animals 11(7):1916

    Article  PubMed  PubMed Central  Google Scholar 

  24. Albanese A, Tang PS, Chan WCW (2012) The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu Rev Biomed Eng 14(1):1–16

    Article  CAS  PubMed  Google Scholar 

  25. Sallam AE et al (2020) Growth performance, anti-oxidative status, innate immunity, and ammonia stress resistance of Siganus rivulatus fed diet supplemented with zinc and zinc nanoparticles. Aquac Rep 18:100410

    Article  Google Scholar 

  26. Dawood MAO et al (2020) Marine-derived chitosan nanoparticles improved the intestinal histo-morphometrical features in association with the health and immune response of Grey Mullet (Liza ramada). Mar Drugs 18(12):611

    Article  CAS  PubMed Central  Google Scholar 

  27. Tancioni L et al (2014) Anthropogenic threats to fish of interest in aquaculture: Gonad intersex in a wild population of thinlip grey Mullet Liza ramada (Risso, 1827) from a polluted estuary in central Italy. Aquac Res 47:1670–1674

  28. Li YLPX-J, Li Y-BHZ-Q, Qing-Song H-LL (2006) Determination of seven trace elements in tea samples by atomic absorption spectrometry [J]. Chin J Spectrosc Lab 5

  29. AOAC, Association of Official Analytical Chemists (1998) Official methods of analysis of official analytical chemists international, 16th ed. Washington, DC

  30. Gewaily MS, Abumandour MM (2020) Gross morphological, histological and scanning electron specifications of the oropharyngeal cavity of the hooded crow (Corvus cornix pallescens). Anat Histol Embryol 50(1):72–83

  31. Bancroft JD, Gamble M (2008) Theory and practice of histological techniques. Elsevier health sciences, Edinburgh

    Google Scholar 

  32. Cai W-Q, Li S-F, Ma J-Y (2004) Diseases resistance of Nile tilapia (Oreochromis niloticus), blue tilapia (Oreochromis aureus) and their hybrid (female Nile tilapia×male blue tilapia) to Aeromonas sobria. Aquaculture 229(1):79–87

    Article  Google Scholar 

  33. Kawahara E, Ueda T, Nomura S (1991) In vitro phagocytic activity of white-spotted char blood cells after injection with Aeromonas salmonicida Extracellular Products. Fish Pathol 26(4):213–214

    Article  Google Scholar 

  34. Ellis A et al (1990) Lysozyme assay in techniques in fish immunology. Technique in Fish Immunology. In Stolen JS (ed) Techniques in fish immunology, fair haven: SOS publication (1990), pp 101–103

  35. Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86(1):271–278

    Article  CAS  PubMed  Google Scholar 

  36. Yossa R, Verdegem M (2015) Misuse of multiple comparison tests and underuse of contrast procedures in aquaculture publications. Aquaculture 437:344–350

    Article  Google Scholar 

  37. Abd El-Kader MF et al (2021) Selenium nanoparticles act potentially on the growth performance, hemato-biochemical indices, antioxidative, and immune-related genes of European seabass (Dicentrarchus labrax). Biol Trace Elem Res 199:3126–3134. https://doi.org/10.1007/s12011-020-02431-1

  38. Abd El-Kader MF et al (2020) Evaluating the possible feeding strategies of selenium nanoparticles on the growth rate and wellbeing of European seabass (Dicentrarchus labrax). Aquac Rep 18:100539

    Article  Google Scholar 

  39. Kumar N, Krishnani KK, Singh NP (2020) Effect of zinc on growth performance and cellular metabolic stress of fish exposed to multiple stresses. Fish Physiol Biochem 46(1):315–329

    Article  CAS  PubMed  Google Scholar 

  40. Faiz H et al (2015) Zinc oxide, zinc sulfate and zinc oxide nanoparticles as source of dietary zinc: comparative effects on growth and hematological indices of juvenile grass carp (Ctenopharyngodon idella). Int J Agric Biol 17(3)

  41. Izquierdo MS et al (2017) Organic, inorganic and nanoparticles of Se, Zn and Mn in early weaning diets for gilthead seabream (Sparus aurata; Linnaeus, 1758). Aquac Res 48(6):2852–2867

    Article  CAS  Google Scholar 

  42. Mondal AH et al (2020) Nano zinc vis-à-vis inorganic zinc as feed additives: Effects on growth, activity of hepatic enzymes and non-specific immunity in rohu, Labeo rohita (Hamilton) fingerlings. Aquac Nutr 26(4):1211–1222

    Article  CAS  Google Scholar 

  43. Kumar N, Krishnani KK, Singh NP (2018) Effect of dietary zinc-nanoparticles on growth performance, anti-oxidative and immunological status of fish reared under multiple stressors. Biol Trace Elem Res 186(1):267–278

    Article  CAS  PubMed  Google Scholar 

  44. Wang ZL (2004) Zinc oxide nanostructures: growth, properties and applications. J Phys Condens Matter 16(25):R829

    Article  CAS  Google Scholar 

  45. Imamoğlu S et al (2005) Effect of zinc supplementation on growth hormone secretion, IGF-I, IGFBP-3, somatomedin generation, alkaline phosphatase, osteocalcin and growth in prepubertal children with idiopathic short stature. J Pediatr Endocrinol Metab 18(1):69–74

    Article  PubMed  Google Scholar 

  46. Uniyal S et al (2017) Comparative efficacy of zinc supplementation from different sources on nutrient digestibility, hemato-biochemistry and anti-oxidant activity in guinea pigs. Livest Sci 204:59–64

    Article  Google Scholar 

  47. Şıklar Z et al (2003) Zinc deficiency: a contributing factor of short stature in growth hormone deficient children. J Trop Pediatr 49(3):187–188

    Article  PubMed  Google Scholar 

  48. Zhao HX et al (2011) Effect of supplemental dietary zinc sources on the growth and carbohydrate utilization of tilapia Smith 1840, Oreochromis niloticus × Oreochromis aureus. Aquac Nutr 17(1):64–72

    Article  CAS  Google Scholar 

  49. Hu CH et al (2014) Effects of zinc oxide supported on zeolite on growth performance, intestinal barrier function and digestive enzyme activities of Nile tilapia. Aquac Nutr 20(5):486–493

    Article  CAS  Google Scholar 

  50. Richardson NL et al (1985) Influence of dietary calcium, phosphorus, zinc and sodium phytate level on cataract incidence, growth and histopathology in juvenile Chinook salmon (Oncorhynchus tshawytscha). J Nutr 115(5):553–567

    Article  CAS  PubMed  Google Scholar 

  51. Dawood MA, Koshio S (2020) Application of fermentation strategy in aquafeed for sustainable aquaculture. Rev Aquac 12(2):987–1002

    Article  Google Scholar 

  52. Saurabh S, Sahoo PK (2008) Lysozyme: an important defence molecule of fish innate immune system. Aquac Res 39(3):223–239

    Article  CAS  Google Scholar 

  53. Siwicki A, Studnicka M (1987) The phagocytic ability of neutrophils and serum lysozyme activity in experimentally infected carp, Cyprinus carpio L. J Fish Biol 31(sA):57–60

    Article  Google Scholar 

  54. Birnie-Gauvin K et al (2017) A comparative and evolutionary approach to oxidative stress in fish: a review. Fish Fish 18(5):928–942

    Article  Google Scholar 

  55. Dawood MAO, Noreldin AE, Sewilam H (2021) Long term salinity disrupts the hepatic function, intestinal health, and gills antioxidative status in Nile tilapia stressed with hypoxia. Ecotoxicol Environ Saf 220:112412

    Article  CAS  PubMed  Google Scholar 

  56. Vinagre C et al (2012) Effect of temperature on oxidative stress in fish: Lipid peroxidation and catalase activity in the muscle of juvenile seabass Dicentrarchus labrax. Ecol Indic 23:274–279

    Article  CAS  Google Scholar 

  57. Mao L et al (2020) Embryonic development and oxidative stress effects in the larvae and adult fish livers of zebrafish (Danio rerio) exposed to the strobilurin fungicides, kresoxim-methyl and pyraclostrobin. Sci Total Environ 729:139031

    Article  CAS  PubMed  Google Scholar 

  58. Ruas CBG et al (2008) Oxidative stress biomarkers of exposure in the blood of cichlid species from a metal-contaminated river. Ecotoxicol Environ Saf 71(1):86–93

    Article  CAS  PubMed  Google Scholar 

  59. Olechnowicz J et al (2018) Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. J Physiol Sci 68(1):19–31

    Article  CAS  PubMed  Google Scholar 

  60. Tapiero H, Tew KD (2003) Trace elements in human physiology and pathology: zinc and metallothioneins. Biomed Pharmacother 57(9):399–411

    Article  CAS  PubMed  Google Scholar 

  61. Stanton RC (2012) Glucose-6-phosphate dehydrogenase, NADPH, and cell survival. IUBMB Life 64(5):362–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Taheri S et al (2017) Effects of dietary supplementation of zinc oxide nanoparticles on some biochemical biomarkers in common carp (Cyprinus carpio). Int J Aquat Biol 5(5):286–294

    Google Scholar 

  63. Tate JDJ, Miceli MV, Newsome DA (1997) Zinc induces catalase expression in cultured fetal human retinal pigment epithelial cells. Curr Eye Res 16(10):1017–1023

    Article  PubMed  Google Scholar 

  64. Dawood MAO et al (2020) The influences of ferulic acid on the growth performance, haemato-immunological responses, and immune-related genes of Nile tilapia (Oreochromis niloticus) exposed to heat stress. Aquaculture 525:735320

    Article  CAS  Google Scholar 

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Funding

The current work was funded by Taif University Researchers Supporting Project number (TURSP-2020/202), Taif University, Taif, Saudi Arabia.

Author information

Authors and Affiliations

  1. Department of Physiology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr el-Sheikh, 33516, Egypt

    Mustafa Shukry

  2. Department of Biotechnology, College of Science, Taif University, P.O. Box 11099, Taif, 21944, Saudi Arabia

    Sarah Albogami & Ahmed M. El-Shehawi

  3. Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Kafrelsheikh University, Kafr el-Sheikh, 33516, Egypt

    Mahmoud Gewaily

  4. Central Laboratory for Aquaculture Research, Sakha Aquaculture Research Unit, Abbassa, Sharkia, Kafrelsheikh, Egypt

    Asem A. Amer

  5. Fish Nutrition Laboratory, Aquaculture Division, National Institute of Oceanography and Fisheries, Alexandria, Egypt

    Ali A. Soliman

  6. Department of Fish Production, Faculty of Agriculture, Al-Azhar University, Nasr City, Cairo, 11651, Egypt

    Saad M. Alsaiad

  7. Animal Production Department, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Sheikh, Egypt

    Mahmoud A. O. Dawood

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  1. Mustafa Shukry
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  2. Sarah Albogami
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  8. Mahmoud A. O. Dawood
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Contributions

Conceptualization, Mustafa Shukry, Mahmoud A.O. Dawood; Data curation, Mahmoud A.O. Dawood; formal analysis, Mustafa Shukry, Sarah Albogami, Mahmoud Gewaily, Ahmed M. El-Shehawi, Mahmoud A.O. Dawood; funding acquisition, Sarah Albogami, Ahmed M. El-Shehawi, Mahmoud A.O. Dawood; Investigation, Mustafa Shukry, Mahmoud A.O. Dawood; methodology, Saad M. Alsaiad, Mahmoud A.O. Dawood; project administration, Mahmoud A.O. Dawood; Resources, Asem A. Amer, Ali A. Soliman, Saad M. Alsaiad, Mahmoud A.O. Dawood; supervision, Mahmoud A.O. Dawood; Validation, Mahmoud A.O. Dawood; writing—original draft, Mahmoud A.O. Dawood; writing—review and editing, Sarah Albogami, Mahmoud Gewaily, Saad M. Alsaiad, Ahmed M. El-Shehawi, Mahmoud A.O. Dawood. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Mahmoud A. O. Dawood.

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The experimental procedure was approved by the ethics review board of the Institutional Animal Care and Use Committee in Kafrelsheikh University (Kafrelsheikh, Egypt).

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Shukry, M., Albogami, S., Gewaily, M. et al. Growth Performance, Antioxidative Capacity, and Intestinal Histomorphology of Grey Mullet (Liza ramada)–Fed Dietary Zinc Nanoparticles. Biol Trace Elem Res 200, 2406–2415 (2022). https://doi.org/10.1007/s12011-021-02844-6

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