Skip to main content
Log in

Effect of Dietary Inorganic and Chelated Trace Mineral Supplementation on the Growth Performance and Skeletal Deformities of European Seabass and Senegalese Sole Post-larvae

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Trace elements such as Cu, Fe, Mn and Zn are essential minerals in fish diets, especially important at early larval stages. The chemical speciation of these elements directly influences their uptake efficiency and metabolic utilization. In order to optimize the form of trace elements incorporated into larval feed, two experiments were conducted using two commercial fish species, European seabass (Dicentrarchus labrax) and Senegalese sole (Solea senegalensis), and two chemical forms (inorganic and glycinate chelates). Several fish performance parameters were measured, as well as bone status parameters to assess which form of mineral results in optimal fish biological performance. European seabass and Senegalese sole post-larvae were unresponsive (P > 0.05) to dietary treatments in terms of dry weight (DW), standard length (SL), relative growth rate (RGR) or feed conversion rates (FCR) when fed diets supplemented with chelated over inorganic trace minerals. This study suggests that replacing dietary inorganic mineral supplementation by their organic glycinate-chelated forms brings no beneficial effects on somatic growth and bone development in Senegalese sole and European seabass post-larvae fed high-quality commercial microdiets. Additionally, we show that mineral leaching from diets can be significant, but the use of chelated minerals can potentially mitigate this leaching phenomenon. Therefore, the selection of the dietary mineral form should take into account not only their economic value, but also their biological effect and environmental impact. Data generated in this trial provides new knowledge in trace mineral nutrition of early-stage marine 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
Fig. 4
Fig. 5

Similar content being viewed by others

Data Availability

The data are available from the corresponding author based on reasonable requests.

References

  1. Georgakopoulou E, Katharios P, Divanach P, Koumoundouros G (2010) Effect of temperature on the development of skeletal deformities in Gilthead seabream (Sparus aurata Linnaeus, 1758). Aquaculture 308:13–19. https://doi.org/10.1016/j.aquaculture.2010.08.006

    Article  Google Scholar 

  2. Boglione C, Gavaia P, Koumoundouros G et al (2013) Skeletal anomalies in reared European fish larvae and juveniles. Part 1: normal and anomalous skeletogenic processes. Rev Aquac 5:S99–S120. https://doi.org/10.1111/raq.12015

    Article  Google Scholar 

  3. Boglione C, Gisbert E, Gavaia P et al (2013) Skeletal anomalies in reared European fish larvae and juveniles. Part 2: main typologies, occurrences and causative factors. Rev Aquac 5:S121–S167. https://doi.org/10.1111/raq.12016

    Article  Google Scholar 

  4. Lall SP, Lewis-McCrea L (2007) Role of nutrients in skeletal metabolism and pathology in fish - an overview. Aquaculture 267:3–19. https://doi.org/10.1016/j.aquaculture.2007.02.053

    Article  CAS  Google Scholar 

  5. Cahu C, Zambonino Infante J, Takeuchi T (2003) Nutritional components affecting skeletal development in fish larvae. Aquaculture 227:245–258. https://doi.org/10.1016/S0044-8486(03)00507-6

    Article  CAS  Google Scholar 

  6. Mazurais D, Darias MJ, Le Gall MM et al (2008) Dietary vitamin mix levels influence the ossification process in European sea bass (Dicentrarchus labrax) larvae. Am J Physiol Integr Comp Physiol 294:R520–R527. https://doi.org/10.1152/ajpregu.00659.2007

    Article  CAS  Google Scholar 

  7. Darias MJ, Mazurais D, Koumoundouros G et al (2010) Dietary vitamin D3 affects digestive system ontogenesis and ossification in European sea bass (Dicentrachus labrax, Linnaeus, 1758). Aquaculture 298:300–307. https://doi.org/10.1016/j.aquaculture.2009.11.002

    Article  CAS  Google Scholar 

  8. Hamre K, Yúfera M, Rønnestad I et al (2013) Fish larval nutrition and feed formulation: knowledge gaps and bottlenecks for advances in larval rearing. Rev Aquac 5:S26–S58. https://doi.org/10.1111/j.1753-5131.2012.01086.x

    Article  Google Scholar 

  9. Lall SP, Kaushik SJ (2021) Nutrition and metabolism of minerals in fish. Animals 11(9):2711

    Article  PubMed  PubMed Central  Google Scholar 

  10. Lall SP (2002) The minerals. In: Hardy JE, Halver R (eds) Fish nutrition, 3rd edn. Academic Press, San Diego, pp 259–308

    Google Scholar 

  11. Watanabe T, Kiron V, Satoh S (1997) Trace minerals in fish nutrition. Aquaculture 151:185–207. https://doi.org/10.1016/S0044-8486(96)01503-7

    Article  CAS  Google Scholar 

  12. NRC (National Research Council) (2011) Minerals. In: Nutrient requirements of fish and shrimp. The National Academies Press, Washington, DC, pp 163–185

  13. Apines MJS, Satoh S, Kiron V et al (2003) Availability of supplemental amino acid-chelated trace elements in diets containing tricalcium phosphate and phytate to rainbow trout, Oncorhynchus mykiss. Aquaculture 225:431–444. https://doi.org/10.1016/S0044-8486(03)00307-7

    Article  CAS  Google Scholar 

  14. Apines-Amar MJS, Satoh S, Caipang CMA et al (2004) Amino acid-chelate: a better source of Zn, Mn and Cu for rainbow trout, Oncorhynchus mykiss. Aquaculture 240:345–358. https://doi.org/10.1016/j.aquaculture.2004.01.032

    Article  CAS  Google Scholar 

  15. Katya K, Lee S, Bharadwaj AS et al (2016) 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 48:1–9. https://doi.org/10.1111/are.13236

    Article  CAS  Google Scholar 

  16. Paripatananont T, Lovell RT (1997) Comparative net absorption of chelated and inorganic trace minerals in channel catfish Ictalurus punctatus diets. J World Aquac Soc 28:62–67. https://doi.org/10.1111/j.1749-7345.1997.tb00962.x

    Article  Google Scholar 

  17. Wang C, Lovell RT (1997) Organic selenium sources, selenomethionine and selenoyeast, have higher bioavailability than an inorganic selenium source, sodium selenite, in diets for channel catfish (Ictalurus punctatus). Aquaculture 152:223–234. https://doi.org/10.1016/S0044-8486(96)01523-2

    Article  CAS  Google Scholar 

  18. Antony Jesu Prabhu P, Schrama JW, Kaushik SJ et al (2016) Mineral requirements of fish: a systematic review. Rev Aquac 8:172–219. https://doi.org/10.1111/raq.12090

    Article  Google Scholar 

  19. Terova G, Rimoldi S, Izquierdo M et al (2018) Nano-delivery of trace minerals for marine fish larvae: influence on skeletal ossification, and the expression of genes involved in intestinal transport of minerals, osteoblast differentiation, and oxidative stress response. Fish Physiol Biochem 44(5):1375–1391. https://doi.org/10.1007/s10695-018-0528-7

    Article  CAS  PubMed  Google Scholar 

  20. Izquierdo MS, Ghrab W, Roo J et al (2016) Organic, inorganic and nanoparticles of Se, Zn and Mn in early weaning diets for gilthead seabream (Sparus aurata; Linnaeus, 1758). Aquac Res 48:1–16. https://doi.org/10.1111/are.13119

    Article  CAS  Google Scholar 

  21. Viegas MN, Salgado MA, Aguiar C 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 199:2012–2021. https://doi.org/10.1007/s12011-020-02307-4

    Article  CAS  PubMed  Google Scholar 

  22. Navarro DB, Rubio VC, Luz RK et al (2009) Daily feeding rhythms of Senegalese sole under laboratory and farming conditions using self-feeding systems. Aquaculture 291:130–135. https://doi.org/10.1016/j.aquaculture.2009.02.039

    Article  Google Scholar 

  23. AOAC (ed) (2006) Official methods of analysis: revision 1, 2006, 18th edn. AOAC International, Gaithersburg Maryland, USA

    Google Scholar 

  24. Bassett JHD, van der Spek A, Gogakos A, Williams G (2012) Quantitative X-ray imaging of rodent bone by Faxitron. In: Helfrich MH, Ralston SH (eds) Bone Research Protocols SE - 29. Humana Press, pp 499–506

    Chapter  Google Scholar 

  25. Mabilleau G, Mieczkowska A, Irwin N et al (2013) Optimal bone mechanical and material properties require a functional glucagon-like peptide-1 receptor. J Endocrinol 219:59–68. https://doi.org/10.1530/JOE-13-0146

    Article  CAS  PubMed  Google Scholar 

  26. Boglione C, Pulcini D, Scardi M et al (2014) Skeletal anomaly monitoring in rainbow trout (Oncorhynchus mykiss, Walbaum 1792) reared under different conditions. PLoS One 9:e96983. https://doi.org/10.1371/journal.pone.0096983

    Article  CAS  PubMed Central  Google Scholar 

  27. Losada AP, de Azevedo AM, Barreiro A et al (2014) Skeletal malformations in Senegalese sole (Solea senegalensis Kaup, 1858): gross morphology and radiographic correlation. J Appl Ichthyol 30:804–808. https://doi.org/10.1111/jai.12524

    Article  Google Scholar 

  28. Ennos R (2007) Statistical and data handling skills in biology. Pearson Prentice Hall

    Google Scholar 

  29. SA MVDCE, Pezzato LE, Barros MM, Padilha PM (2005) Relative bioavailability of zinc in supplemental inorganic and organic sources for Nile tilapia Oreochromis niloticus fingerlings. Aquac Nutr 11:273–281. https://doi.org/10.1111/j.1365-2095.2005.00352.x

    Article  Google Scholar 

  30. Fountoulaki E, Morgane H, Rigos G et al (2010) Evaluation of zinc supplementation in European sea bass (Dicentrarchus labrax) juvenile diets. Aquac Res 41:208–216. https://doi.org/10.1111/j.1365-2109.2010.02503.x

    Article  CAS  Google Scholar 

  31. Savolainen LC, Gatlin DM (2010) Evaluation of sulfur amino acid and zinc supplements to soybean-meal-based diets for hybrid striped bass. Aquaculture 307:260–265. https://doi.org/10.1016/j.aquaculture.2010.07.027

    Article  CAS  Google Scholar 

  32. Domínguez D, Rimoldi S, Robaina LE et al (2017) Inorganic, organic, and encapsulated minerals in vegetable meal based diets for Sparus aurata (Linnaeus, 1758). PeerJ 5:e3710. https://doi.org/10.7717/peerj.3710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Silva MS, Kröckel S, Jesu Prabhu PA et al (2019) Apparent availability of zinc, selenium and manganese as inorganic metal salts or organic forms in plant-based diets for Atlantic salmon (Salmo salar). Aquaculture 503:562–570. https://doi.org/10.1016/j.aquaculture.2019.01.005

    Article  CAS  Google Scholar 

  34. Zhang H, Gilbert ER, Zhang K et al (2017) Uptake of manganese from manganese–lysine complex in the primary rat intestinal epithelial cells. J Anim Physiol Anim Nutr (Berl) 101:147–158. https://doi.org/10.1111/jpn.12430

    Article  CAS  PubMed  Google Scholar 

  35. Yúfera M, Darías MJ (2007) Changes in the gastrointestinal pH from larvae to adult in Senegal sole (Solea senegalensis). Aquaculture 267:94–99. https://doi.org/10.1016/j.aquaculture.2007.02.009

    Article  CAS  Google Scholar 

  36. Rønnestad I, Yúfera M, Ueberschar B et al (2013) Feeding behaviour and digestive physiology in larval fish: current knowledge, and gaps and bottlenecks in research. Rev Aquac 5:S59–S98. https://doi.org/10.1111/raq.12010

    Article  Google Scholar 

  37. García-Casal MN, Layrisse M (2001) The effect of change in pH on the solubility of iron bis-glycinate chelate and other iron compounds. Arch Latinoam Nutr 51:35–36

    PubMed  Google Scholar 

  38. López-alvarado J, Langdonb CJ, Teshima S, Kanazawa A (1994) Effects of coating and encapsulation of crystalline amino acids on leaching in larval feeds. Aquaculture 122:335–346

    Article  Google Scholar 

  39. Yúfera M, Kolkovski S, Fernández-Díaz C, Dabrowski K (2002) Free amino acid leaching from a protein-walled microencapsulated diet for fish larvae. Aquaculture 214:273–287. https://doi.org/10.1016/S0044-8486(01)00902-4

    Article  Google Scholar 

  40. Nordgreen A, Yúfera M, Hamre K (2008) Evaluation of changes in nutrient composition during production of cross-linked protein microencapsulated diets for marine fish larvae and suspension feeders. Aquaculture 285:159–166. https://doi.org/10.1016/j.aquaculture.2008.08.011

    Article  CAS  Google Scholar 

  41. Önal U, Langdon C (2004) Characterization of lipid spray beads for delivery of glycine and tyrosine to early marine fish larvae. Aquaculture 233:495–511

    Article  Google Scholar 

  42. Kvåle A, Yúfera M, Nygård E et al (2006) Leaching properties of three different micropaticulate diets and preference of the diets in cod (Gadus morhua L.) larvae. Aquaculture 251:402–415. https://doi.org/10.1016/j.aquaculture.2005.06.002

    Article  CAS  Google Scholar 

  43. Kvåle A, Nordgreen AH, Tonheim SK, Hamre K (2007) The problem of meeting dietary protein requirements in intensive aquaculture of marine fish larvae, with emphasis on Atlantic halibut (Hippoglossus hippoglossus L.). Aquac Nutr 13:170–185. https://doi.org/10.1111/j.1365-2095.2007.00464.x

    Article  Google Scholar 

  44. Hamre K (2006) Nutrition in cod (Gadus morhua) larvae and juveniles. ICES J Mar Sci 63:267–274. https://doi.org/10.1016/j.icesjms.2005.11.011

    Article  Google Scholar 

  45. Phillips MJ, Clarke R, Mowat A (1993) Phosphorus leaching from Atlantic salmon diets. Aquac Eng 12:47–54. https://doi.org/10.1016/0144-8609(93)90026-8

    Article  Google Scholar 

  46. Roy LA, Davis DA, Saoud IP, Henry RP (2007) Supplementation of potassium, magnesium and sodium chloride in practical diets for the Pacific white shrimp, Litopenaeus vannamei, reared in low salinity waters. Aquac Nutr 13:104–113. https://doi.org/10.1111/j.1365-2095.2007.00460.x

    Article  CAS  Google Scholar 

  47. Berillis P (2015) Factors that can lead to the development of skeletal deformities in fishes: a review. J Fish com 9:17–23

    Google Scholar 

  48. Chanda S, Paul BN, Ghosh K, Giri SS (2015) Dietary essentiality of trace minerals in aquaculture-a review. Agric Rev 36:100–112. https://doi.org/10.5958/0976-0741.2015.00012.4

    Article  Google Scholar 

  49. Nielsen FH (2000) Evolutionary events culminating in specific minerals becoming essential for life. Eur J Nutr 39:62–66. https://doi.org/10.1007/s003940050003

    Article  CAS  PubMed  Google Scholar 

  50. Nguyen VT, Satoh S, Haga Y et al (2008) Effect of zinc and manganese supplementation in Artemia on growth and vertebral deformity in red sea bream (Pagrus major) larvae. Aquaculture 285:184–192. https://doi.org/10.1016/j.aquaculture.2008.08.030

    Article  CAS  Google Scholar 

  51. Roberto VP, Martins G, Pereira A et al (2018) Insights from dietary supplementation with zinc and strontium on the skeleton of zebrafish, Danio rerio (Hamilton, 1822) larvae: from morphological analysis to osteogenic markers. J Appl Ichthyol 34:512–523. https://doi.org/10.1111/jai.13664

    Article  CAS  Google Scholar 

Download references

Funding

This research has been carried out with the financial support of the LARVAMIX project (grant no. 17925) supported by Portugal and the European Union through FEDER, COMPETE 2020 and CRESC Algarve 2020, in the framework of Portugal 2020. MV acknowledges the financial support by FCT/MCTES (Portugal) through a doctoral fellowship (grant PDE/BDE/113672/2015).

Author information

Authors and Affiliations

Authors

Contributions

J. D., P. P. and C. A. contributed to funding, resources acquisition and conceptualization and design of the study. P. P. supplied the fish rearing facilities. M. S. and A. A. contributed to mineral analysis. M. V. contributed to the conceptualization and design of the study, performed the analytical work and data analysis, and wrote the main manuscript text. All authors contributed to manuscript revision, read and approved the submitted version.

Corresponding author

Correspondence to Michael N. Viegas.

Ethics declarations

Ethics Approval

The experimental protocol was approved by the Animal Welfare Committee (ORBEA) of the Instituto Português do Mar e da Atmosfera (IPMA) (Project LARVAMIX approval n° 17935) and carried out in registered facilities (0421/2018). Experiments were conducted by trained scientists and in full compliance with the European (Directive 2010/63/EU) and Portuguese (Decreto-Lei n°. 113/2013, August 7) legislation on the protection of animals for scientific purposes.

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

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Viegas, M.N., Salgado, M.A., Aguiar, C. et al. Effect of Dietary Inorganic and Chelated Trace Mineral Supplementation on the Growth Performance and Skeletal Deformities of European Seabass and Senegalese Sole Post-larvae. Biol Trace Elem Res 201, 5389–5400 (2023). https://doi.org/10.1007/s12011-023-03581-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-023-03581-8

Keywords

Navigation