Skip to main content
Log in

Significance of extrinsic factors for the optimization of dietary cobalt supplementation in Tor putitora fingerlings

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Extrinsic factors play a significant role during aquaculture feed manufacturing practices. Herein, a 90-day feeding trial was designed in triplicate under controlled environmental conditions to evaluate the efficiency of different chemical forms of dietary cobalt at different dosage levels on growth performance, hematological, and immunological indices of Tor putitora fingerlings. Firstly, cobalt chloride nanoparticles (Co-NPs) and cobalt methionine chelated complex (Co-Met) were synthesized via physical and chemical methods respectively and then characterized for their size, surface morphology, and elemental composition analysis by using X-rays diffraction spectroscopy (XRD), scanning electron microscopy (SEM), and energy dispersive spectroscopy (EDS). Results indicated the crystalline nature of Co-NPs with spherical shape having an average size < 20 nm while Co-Met appeared as an amorphous complex with a honey-comb-like octahedral structure with an average size of 82.69 nm. Afterward, a feeding experiment was executed and fish were divided into three groups, i.e., control group (CG; fed 40% crude protein diet with no mineral added), while the other two groups were fed graded levels (0.5–3 mg/kg; increment of 0.5 mg Co/group) of Co-NPs and Co-Met supplemented diets. Statistical analysis of results by using two-way ANOVA indicated significant (P < 0.001) effect of both chemical forms, dosage levels, and their interaction level on fish indicating a dose-dependent significant effect of different chemical forms of dietary cobalt on fish. Additionally, Co-Met supplemented group of fish at supplementation level of 3 mg/kg diet showed highest growth performance, and improved hemato-immunological as compared to other experimental and control group of fish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Not applicable.

Code availability

Not applicable.

References

  • Abdel-Hammed MM, Allam SA, Metwally AA, El-Deeb KF, Abdel-Aziz M (2019) A comparative study of nano-iron and zinc as feed additive on growth performance, feed efficiency and chemical body composition of Nile tilapia fingerlings (Oreochromis nilotiucs). Egypt J Aqua Biol Fish 23(5):367–380

    Article  Google Scholar 

  • Al-Ghanem KA (2011) Effect of cobalt-supplemented diets on bioaccumulation, digestive enzyme activities and growth of Cyprinus carpio. Toxicol Environ Chem 93(5):985–995

    Article  CAS  Google Scholar 

  • Al-Habsi K, Johnson EH, Kadim IT, Srikandakumar A, Annamalai K, Al-Busaidy R, Mahgoub O (2007) Effects of low concentrations of dietary cobalt on liveweight gains, haematology, serum vitamin B12 and biochemistry of Omani goats. Vet J 173(1):131–137. https://doi.org/10.1016/j.tvjl.2005.10.002

    Article  CAS  PubMed  Google Scholar 

  • Anadu D, Anozie O, Anthony A (1990) Growth responses of Tilapia zillii fed diets containing various levels of ascorbic acid and cobalt chloride. Aquaculture 88(3–4):329–336

    Article  CAS  Google Scholar 

  • Anderson DP, Siwicki AK (1995) Basic hematology and serology for fish health programs. In: M. Shariff JR, Subasinghe RP (eds) Diseases in Asian aquaculture II. Fish Health Section, Asian Fisheries Society, Manila, pp 185–202

  • Anderson DP, Zeeman MG (1995) Immunotoxicology in fish. Fundamentals Aqua Toxicol 2:371–404

    Google Scholar 

  • Apines-Amar MJS, Satoh S, Caipang CMA, Kiron V, Watanabe T, Aoki T (2004) Amino acid-chelate: a better source of Zn, Mn and Cu for rainbow trout. Oncorhynchus Mykiss Aquaculture 240(1–4):345–358

    Article  CAS  Google Scholar 

  • Ashmead HD (2012). Amino acid chelation in human and animal nutrition: Taylor and Francis, CRC Press.ISBN 978–1–4398–9767–6.

  • Ashry GME, Melegy KME. (2015). Synthesis, characterization and effectiveness of chelated mineral as aflatoxin absorbents. Journal of Chemical Biology and Therapeutics, 1(1), 1–5, ISSN: 2572–0406.

  • Atamanalp M, Aksakal E, Kocaman EM, Uçar A, Şişman T, Türkez H (2011) The alterations in the hematological parameters of rainbow trout, Oncorhynchus mykiss, exposed to cobalt chloride. J Faculty Veterinary 17:73–76

    Google Scholar 

  • Ayub M (2007) Freshwater fish seed resources in Pakistan. Assess Freshwater Fish Seed Res Sustain Aquacul, Fish Aquacul Dept 501:381

    Google Scholar 

  • Behera T, Swain P, Rangacharulu P, Samanta M (2014) Nano-Fe as feed additive improves the hematological and immunological parameters of fish. Labeo Rohita h Appl Nanosci 4(6):687–694

    Article  CAS  Google Scholar 

  • Berntssen MHG, Sundal T, Olsvik P, Amlund H, Rasinger J, Ørnsrud R (2017) Sensitivity and toxic mode of action of dietary organic and inorganic selenium in Atlantic salmon (Salmo salar). Aquat Toxicol 192:116–126

    Article  CAS  PubMed  Google Scholar 

  • Beyersmann D, Hartwig A (2008) Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch Toxicol 82(8):493

    Article  CAS  PubMed  Google Scholar 

  • Bharadwaj AS, Patnaik S, Browdy CL, Lawrence AL (2014) Comparative evaluation of an inorganic and a commercial chelated copper source in Pacific white shrimp Litopenaeus vannamei (Boone) fed diets containing phytic acid. Aquaculture 422–423:63–68. https://doi.org/10.1016/j.aquaculture.2013.11.025

    Article  CAS  Google Scholar 

  • Blust R (2011) Cobalt. Fish Physiology 31(A):291–326

    Article  Google Scholar 

  • Chanda S, Paul B, Ghosh K, Giri S (2015) Dietary essentiality of trace minerals in aquaculture—a review. Agric Rev 36(2):100–112

    Article  Google Scholar 

  • Chris UO, Singh N, Agarwal A (2018) Nanoparticles as feed supplement on growth behaviour of cultured catfish (Clarias gariepinus) fingerlings. Mater Today: Proceed 5(3):9076–9081

    CAS  Google Scholar 

  • Craig S, Helfrich LA, Kuhn D, Schwarz MH (2017). Understanding fish nutrition, feeds, and feeding. Virginia Copperative extension. Publication 420-256 2002

  • DeForest DK, Meyer JS (2015) Critical review: toxicity of dietborne metals to aquatic organisms. Crit Rev Environ Sci Technol 45(11):1176–1241

    Article  CAS  Google Scholar 

  • Elks PM, van Eeden FJ, Dixon G, Wang X, Reyes-Aldasoro CC, Ingham PW, Renshaw SA (2011) Activation of hypoxia-inducible factor-1α (Hif-1α) delays inflammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafish inflammation model. Blood, J Am Soc Hematol 118(3):712–722

    CAS  Google Scholar 

  • EM K (2011) The alterations in the hematological parameters of rainbow trout, Oncorhynchus mykiss, exposed to cobalt chloride. Kafkas Üniversitesi Veteriner Fakültesi Dergisi 17(1):73–76

    Google Scholar 

  • Faiz H, Zuberi A, Nazir S, Rauf M, Younus N (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 (Ctenopharyngodonidella). Int J Agri Biol 17(3):568–574

    CAS  Google Scholar 

  • Fazio F (2019) Fish hematology analysis as an important tool of aquaculture: a review. Aquaculture 500:237–242

    Article  Google Scholar 

  • Fernandes J, Murakami A, Sakamoto M, Souza L, Malaguido A, Martins E (2008) Effects of organic mineral dietary supplementation on production performance and egg quality of white layers. Brazilian J Poultry Sci 10(1):59–65

    Article  Google Scholar 

  • Finley BL, Monnot AD, Gaffney SH, Paustenbach DJ (2012) Dose-response relationships for blood cobalt concentrations and health effects: a review of the literature and application of a biokinetic model. J Toxicol Environ Health, Part B 15(8):493–523

    Article  CAS  Google Scholar 

  • Förstner, U., Wittmann, G. T. (2012). Metal pollution in the aquatic environment: Springer Science and Business Media.2nd edition, ISBN:978–3–540–12856–4

  • Gharibzahedi SMT, Jafari SM (2017) The importance of minerals in human nutrition: bioavailability, food fortification, processing effects and nanoencapsulation. Trends Food Sci Technol 62:119–132

    Article  CAS  Google Scholar 

  • Ghiuţă I, Cristea D, Munteanu D (2017) Synthesis methods of metallic nanoparticles—an overview Bulletin of the Transilvania University of Brasov. Eng Sci Series I 10(2):133–140

    Google Scholar 

  • Gräslund S, Bengtsson BE (2001) Chemicals and biological products used in south-east Asian shrimp farming, and their potential impact on the environment—a review. Sci Total Environ 280(1–3):93–131

    Article  PubMed  Google Scholar 

  • Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber DS (2008) Effects of particle composition and species on toxicity of metallic nanomaterials in aquatic organisms. Environ Toxicol Chem: an Int J 27(9):1972–1978

    Article  CAS  Google Scholar 

  • Handy RD, Henry TB, Scown TM, Johnston BD, Tyler CR (2008) Manufactured nanoparticles: their uptake and effects on fish—a mechanistic analysis. Ecotoxicol 17(5):396–409

    Article  CAS  Google Scholar 

  • Harvey L (2001) Mineral bioavailability. Nutri Food Sci 31(4):179–182

    Article  Google Scholar 

  • Hellwig-Bürgel T, Stiehl DP, Wagner AE, Metzen E, Jelkmann W (2005) Hypoxia-inducible factor-1 (HIF-1): a novel transcription factor in immune reactions. J Interferon Cytokine Res 25(6):297–310

    Article  PubMed  Google Scholar 

  • Hojman P., Brolin C., Gissel H., Brandt C., Zerahn B., Pedersen B. K., Gehl J. (2009). Erythropoietin over-expression protects against diet-induced obesity in mice through increased fat oxidation in muscles. PloS one, 4(6).

  • Ilham I, Siddik MAB, Fotedar R (2016) Effects of organic selenium supplementation on growth, accumulation, haematology and histopathology of juvenile barramundi (Lates calcarifer) fed high soybean meal diets. Biol Trace Elem Res 174(2):436–447

    Article  CAS  PubMed  Google Scholar 

  • Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7(2):60–72

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jahanian R, Moghaddam HN, Rezaei A (2008) Improved broiler chick performance by dietary supplementation of organic zinc sources. Asian Australas J Anim Sci 21(9):1348–1354

    Article  CAS  Google Scholar 

  • Jiang W, Kim BY, Rutka JT, Chan WC (2007) Advances and challenges of nanotechnology-based drug delivery systems. Expert Opin Drug Deliv 4(6):621–633

    Article  CAS  PubMed  Google Scholar 

  • Joye IJ, Davidov-Pardo G, McClements DJ (2014) Nanotechnology for increased micronutrient bioavailability. Trends Food Sci Technol 40(2):168–182

    Article  CAS  Google Scholar 

  • Kanwal Z, Raza MA, Manzoor F, Riaz S, Jabeen G, Fatima S, Naseem S (2019) A comparative assessment of nanotoxicity induced by metal (silver, nickel) and metal oxide (cobalt, chromium) nanoparticles in Labeo rohita. Nanomaterials 9(2):309

    Article  CAS  PubMed Central  Google Scholar 

  • Katya K, Lee S, Bharadwaj AS, Browdy CL, Vazquez-Anon M, Bai SC (2017) Effects of inorganic and chelated trace mineral (Cu, Zn, Mn and Fe) premixes in marine rockfish, Sebastes schlegeli (Hilgendorf), fed diets containing phytic acid. Aquac Res 48(8):4165–4173

    Article  CAS  Google Scholar 

  • Ke Q, Costa M (2006) Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70(5):1469–1480

    Article  CAS  PubMed  Google Scholar 

  • Kishawy AT, Roushdy EM, Hassan FA, Mohammed HA, Abdelhakim TM (2020) Comparing the effect of diet supplementation with different zinc sources and levels on growth performance, immune response and antioxidant activity of tilapia. Oreochromis Niloticus Aquacul Nutri 26(6):1926–1942

    Article  CAS  Google Scholar 

  • Kubrak OI, Rovenko BM, Husak VV, Vasylkiv OY, Storey KB, Storey JM, Lushchak VI (2012) Goldfish exposure to cobalt enhances hemoglobin level and triggers tissue-specific elevation of antioxidant defenses in gills, heart and spleen. Comp Biochem Physiol c: Toxicol Pharmacol 155(2):325–332

    CAS  Google Scholar 

  • Kwon YM, Xia Z, Glyn-Jones S, Beard D, Gill HS, Murray DW (2009) Dose-dependent cytotoxicity of clinically relevant cobalt nanoparticles and ions on macrophages in vitro. Biomed Mater 4(2):1–8

    Article  CAS  Google Scholar 

  • Lall, S. P. (2003). The minerals. In Fish nutrition, Academic press, 3rd edition, ISBN: 9780080494920, 259–308.

  • Lin YH, Wu JY, Shiau SY (2010) Dietary cobalt can promote gastrointestinal bacterial production of vitamin B12 in sufficient amounts to supply growth requirements of grouper. Epinephelus Malabaricus Aquaculture 302(1–2):89–93

    Article  CAS  Google Scholar 

  • Little EE, Calfee RD, Theodorakos P, Brown ZA, Johnson CA (2007) Toxicity of cobalt-complexed cyanide to Oncorhynchus mykiss, Daphnia magna, and Ceriodaphnia dubia. Environ Sci Pollu Res-Int 14(5):333–337

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  PubMed  Google Scholar 

  • Mancino A, Schioppa T, Larghi P, Pasqualini F, Nebuloni M, Chen IH, Sica A (2008) Divergent effects of hypoxia on dendritic cell functions. Blood, J Am Soc Hematol 112(9):3723–3734

    CAS  Google Scholar 

  • Mansour ATE, Goda AA, Omar EA, Khalil HS, Esteban MÁ (2017) Dietary supplementation of organic selenium improves growth, survival, antioxidant and immune status of meagre, Argyrosomus regius, juveniles. Fish Shellfish Immunol 68:516–524

    Article  CAS  PubMed  Google Scholar 

  • Maxwell P, Salnikow K (2004) HIF-1, an oxygen and metal responsive transcription factor. Cancer Biol Ther 3(1):29–35

    Article  CAS  PubMed  Google Scholar 

  • Miles RD, Henry PR (2000) Relative trace mineral bioavailability. Ciência Animal Brasileira 1(2):73–93

    Google Scholar 

  • Mirzaie M, Rahmani Z, Taherkhani A (2013) Synthesis, characterization and thermal behavior studies of nanoparticles cobalt (II) chloride. J Basic Appl Sci Res 3(1):183–186

    Google Scholar 

  • Momin JK, Jayakumar C, Prajapati JB (2013) Potential of nanotechnology in functional foods. Emirates J Food Agri (EJFA) 25(1):10–19

    Article  Google Scholar 

  • Mukherjee S, Kaviraj A (2009) Evaluation of growth and bioaccumulation of cobalt in different tissues of common carp, Cyprinus carpio (Actinopterygii: Cypriniformes: Cyprinidae), fed cobalt-supplemented diets. Acta Ichthyol Piscat 39(2):87–93

    Article  Google Scholar 

  • Mukherjee S, Kaviraj A (2011) Bioaccumulation of cobalt, digestive enzyme activities, and growth of freshwater catfish, Heteropneustes fossilis (Bloch), fed cobalt-supplemented diets. Toxicol Environ Chem 93(3):575–584

    Article  CAS  Google Scholar 

  • Oda T, Hirota K, Nishi K, Takabuchi S, Oda S, Yamada H, Adachi T (2006) Activation of hypoxia-inducible factor 1 during macrophage differentiation. Am J Physiol Cell Physiol 291(1):104–113

    Article  CAS  Google Scholar 

  • Oliva-Teles A (2012) Nutrition and health of aquaculture fish. J Fish Dis 35(2):83–108

    Article  CAS  PubMed  Google Scholar 

  • Onuegbu C, Aggarwal A, Singh N (2018) ZnO nanoparticles as feed supplement on growth performance of cultured African Catfish fingerlings ZnO nanoparticles as feed supplement on growth performance of cultured african catfish fingerlings. J Sci Industrial Res 77(4):213–218

    CAS  Google Scholar 

  • Ørnsrud R, Lorentzen M (2002) Bioavailability of selenium from raw or cured selenomethionine-enriched fillets of Atlantic salmon (Salmo salar) assessed in selenium-deficient rats. Br J Nutr 87(1):13–20

    Article  PubMed  CAS  Google Scholar 

  • Paik I (2001) Application of chelated minerals in animal production. Asian Australasian J Animal Sci 14:191–198

    CAS  Google Scholar 

  • Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73(6):1712–1720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palazon A, Goldrath AW, Nizet V, Johnson RS (2014) HIF transcription factors, inflammation, and immunity. Immunity 41(4):518–528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prabhu PAJ, Lock E-J, Hemre G-I, Hamre K, Espe M, Olsvik PA, Sissener NH (2019) Recommendations for dietary level of micro-minerals and vitamin D3 to Atlantic salmon (Salmo salar) parr and post-smolt when fed low fish meal diets. Aquat Biol 7:6996–7018

    Google Scholar 

  • Pohlenz C, Gatlin DM III (2014) Interrelationships between fish nutrition and health. Aquaculture 431:111–117

    Article  CAS  Google Scholar 

  • Rider S, Davies S, Jha A, Clough R, Sweetman J (2010) Bioavailability of co-supplemented organic and inorganic zinc and selenium sources in a white fishmeal-based rainbow trout (Oncorhynchus mykiss) diet. J Anim Physiol Anim Nutr 94(1):99–110

    Article  CAS  Google Scholar 

  • Sajid M, Ilyas M, Basheer C, Tariq M, Daud M, Baig N, Shehzad F (2015) Impact of nanoparticles on human and environment: review of toxicity factors, exposures, control strategies, and future prospects. Environ Sci Pollut Res 22(6):4122–4143

    Article  Google Scholar 

  • Sakai M (1999) Current research status of fish immunostimulants. Aquaculture 172(1–2):63–92

    Article  CAS  Google Scholar 

  • Saravi SS, Karami S, Karami B, Shokrzadeh M (2009) Toxic effects of cobalt chloride on hematological factors of common carp (Cyprinus carpio). Biol Trace Elem Res 132(1–3):144

    Article  CAS  Google Scholar 

  • Sarkar B, Jaisai M, Mahanty A, Panda P, Sadique M, Nayak B, Dutta J (2015) Optimization of the sublethal dose of silver nanoparticle through evaluating its effect on intestinal physiology of Nile tilapia (Oreochromis niloticus L). J Environ Sci Health, Part A 50(8):814–823

    Article  CAS  Google Scholar 

  • Sharif MK, Butt MS., Sharif HR (2017). Role of nanotechnology in enhancing bioavailability and delivery of dietary factors.Elsevier. In Nutrient delivery, 587–618.

  • Sen S, Pathak Y (2016). Nanotechnology in nutraceuticals: production to consumption: Chemical Rubber Company (CRC) Press.

  • Shaalan M, Saleh M, El-Mahdy M, El-Matbouli M (2016) Recent progress in applications of nanoparticles in fish medicine: a review. Nanomed Nanotechnol Biol Med 12(3):701–710

    Article  CAS  Google Scholar 

  • Shahpar Z, Johari SA (2019) Effects of dietary organic, inorganic, and nanoparticulate zinc on rainbow trout, Oncorhynchus mykiss larvae. Biol Trace Elem Res 190(2):535–540

    Article  CAS  PubMed  Google Scholar 

  • Shaw BJ, Handy RD (2011) Physiological effects of nanoparticles on fish: a comparison of nanometals versus metal ions. Environ Int 37(6):1083–1097

    Article  CAS  PubMed  Google Scholar 

  • Sevcikova M, Modra H, Slaninova A, Svobodova Z (2011) Metals as a cause of oxidative stress in fish: a review. Vetrinary Med 56(11):537–546

    Article  CAS  Google Scholar 

  • Srinivasan V, Bhavan PS, Rajkumar G, Satgurunathan T, Muralisankar T (2016) Effects of dietary iron oxide nanoparticles on the growth performance, biochemical constituents and physiological stress responses of the giant freshwater prawn Macrobrachium rosenbergii post-larvae. Int J Fish Aquatic Stud 4(2):170–182

    Google Scholar 

  • Stănilă A, Braicu C, Stănilă S (2011) Antibacterial activity of copper and cobalt amino acids complexes. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 39(2):124–129

    Article  Google Scholar 

  • Suganthi P, Soundarya N, Stalin A, Nedunchezhiyan S (2015) Toxicological effect of cobalt chloride on freshwater fish Oreochromis mossambicus. Int J Appl Res 1(3):331–340

    Google Scholar 

  • Tamura J, Kubota K, Murakami H, Sawamura M, Matsushima T, Tamura T, Naruse T (1999) Immunomodulation by vitamin B12: augmentation of CD8+ T lymphocytes and natural killer (NK) cell activity in vitamin B12-deficient patients by methyl-B12 treatment. Clin Exp Immunol 116(1):28–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trichet VV (2010) Nutrition and immunity: an update. Aquacul Res 41(3):356–372

    Article  CAS  Google Scholar 

  • Uchida K, Mandebvu P, Ballard C, Sniffen C, Carter M (2001) Effect of feeding a combination of zinc, manganese and copper amino acid complexes, and cobalt glucoheptonate on performance of early lactation high producing dairy cows. Anim Feed Sci Technol 93(3–4):193–203

    Article  CAS  Google Scholar 

  • Wang C, Lovell RT, Klesius PH (1997) Response to Edwardsiella ictaluri challenge by channel catfish fed organic and inorganic sources of selenium. J Aquat Anim Health 9(3):172–179

    Article  Google Scholar 

  • Younus N, Zuberi A, Rashidpour A, Metón I (2020a) Dietary cobalt supplementation improves growth and body composition and induces the expression of growth and stress response genes in Tor putitora. Fish Physiol Biochem 46(1):371–381

    Article  CAS  PubMed  Google Scholar 

  • Younus N, Zuberi A, Mahmoood T, Akram W, Ahmad M (2020b) Comparative effects of dietary micro-and nano-scale chitosan on the growth performance, non-specific immunity, and resistance of silver carp Hypophthalmichthys molitrix against Staphylococcus aureus infection. Aquacult Int 28(6):2363–2378

  • Zinkernagel AS, Johnson RS, Nizet V (2007) Hypoxia inducible factor (HIF) function in innate immunity and infection. J Mol Med 85(12):1339–1346

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

The first author of the manuscript (Dr. Naima Younus) has planned, conducted the experimental work, analyzed the results, and prepared the manuscript, while the second author (Dr. Amina Zuberi) had helped in designing of research, analyzing of results, and helped in statistical analysis and interpretation and finalizing the final version of the manuscript.

Furthermore, the corresponding author is the sole contact for the Editorial process and is responsible for communicating with the other author about progress, submissions of revisions, and final approval of proofs. We confirm that we have provided a current, correct email address which is accessible by the corresponding author.

Corresponding author

Correspondence to Naima Younus.

Ethics declarations

Ethics approval

All experimental procedures were conducted after the approval of the Animal Welfare Committee of Quaid-i-Azam University (BEC-FBS-67-QAU-2017).

Consent to participate

Both authors have participated equally while conducting experiments, analyzing results, interpreting, and finalizing the manuscript.

Consent for publication

Both authors have agreed to the peer-review of the manuscript and for publication in fish physiology and biochemistry.

Conflict of interest

The authors declare no competing interests.

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

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Younus, N., Zuberi, A. Significance of extrinsic factors for the optimization of dietary cobalt supplementation in Tor putitora fingerlings. Fish Physiol Biochem 48, 883–897 (2022). https://doi.org/10.1007/s10695-022-01089-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-022-01089-x

Keywords

Navigation