Skip to main content

Effect of Dietary Manganese and Zinc Levels on Growth and Bone Status of Senegalese Sole (Solea senegalensis) Post-Larvae

Abstract

Essential dietary trace elements, such as zinc (Zn) and manganese (Mn), critically influence a wide range of physiological, metabolic, and hormonal processes in fish larvae and post-larvae. Despite their importance for normal fish growth and skeletal development, trace mineral nutrition has not been extensively studied in the early stages of development of fish. Post-larvae of an emergent aquaculture species, Senegalese sole (Solea senegalensis), were the subject of this study in order to better understand the effects of diet supplementation of trace minerals upon fish larval development and performance. Sole post-larvae were fed a combination of organic Mn (45 and 90 mg kg−1 feed) and organic Zn (100 and 130 mg kg−1 feed) and survival, growth, mineral deposition rates, and vertebral bone status were assessed. Our results showed that although no significant effect was found on the growth performance of Senegalese sole post-larvae, Mn and Zn supplementation to a commercial microdiet for marine fish larvae at higher dietary levels (Mn at 90 mg kg−1 and Zn at 130 mg kg−1) improved larval survival, decreased the severity of vertebral malformations, and increased the deposition of Mn in bone.

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

Fig. 1

References

  1. Boglione C, Gisbert E, Gavaia P, E. Witten P, Moren M, Fontagné S, Koumoundouros G (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 

  2. 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 

  3. de Azevedo AM, Losada AP, Barreiro A, Vázquez S, Quiroga MI (2018) Skeletal anomalies in Senegalese sole (Solea senegalensis), an anosteocytic boned flatfish species. Vet Pathol 56:307–316. https://doi.org/10.1177/0300985818800027

    Article  PubMed  Google Scholar 

  4. Sfakianakis DG, Georgakopoulou E, Papadakis IE, Divanach P, Kentouri M, Koumoundouros G (2006) Environmental determinants of haemal lordosis in European sea bass, Dicentrarchus labrax (Linnaeus, 1758). Aquaculture 254:54–64. https://doi.org/10.1016/j.aquaculture.2005.10.028

    Article  Google Scholar 

  5. Fragkoulis S, Printzi A, Geladakis G et al (2019) Recovery of haemal lordosis in gilthead seabream (Sparus aurata L.). Sci Rep 9:9832. https://doi.org/10.1038/s41598-019-46334-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Witten PE, Obach A, Huysseune A, Baeverfjord G (2006) Vertebrae fusion in Atlantic salmon (Salmo salar): development, aggravation and pathways of containment. Aquaculture 258:164–172. https://doi.org/10.1016/j.aquaculture.2006.05.005

    Article  Google Scholar 

  7. Gisbert E, Skalli A, Fernández I, Kotzamanis Y, Zambonino-Infante JL, Fabregat R (2012) Protein hydrolysates from yeast and pig blood as alternative raw materials in microdiets for gilthead sea bream (Sparus aurata) larvae. Aquaculture 338–341:96–104. https://doi.org/10.1016/j.aquaculture.2012.01.007

    CAS  Article  Google Scholar 

  8. Cahu CL, Gisbert E, Villeneuve LAN, Morais S, Hamza N, Wold PA, Zambonino Infante JL (2009) Influence of dietary phospholipids on early ontogenesis of fish. Aquac Res 40:989–999. https://doi.org/10.1111/j.1365-2109.2009.02190.x

    CAS  Article  Google Scholar 

  9. Kjørsvik E, Olsen C, Wold P-A, Hoehne-Reitan K, Cahu CL, Rainuzzo J, Olsen AI, Øie G, Olsen Y (2009) Comparison of dietary phospholipids and neutral lipids on skeletal development and fatty acid composition in Atlantic cod (Gadus morhua). Aquaculture 294:246–255. https://doi.org/10.1016/j.aquaculture.2009.06.012

    CAS  Article  Google Scholar 

  10. Villeneuve L, Gisbert E, Zambonino-Infante JL, Quazuguel P, Cahu CL (2005) Effect of nature of dietary lipids on European sea bass morphogenesis: implication of retinoid receptors. Br J Nutr 94:877–884. https://doi.org/10.1079/BJN20051560

    CAS  Article  PubMed  Google Scholar 

  11. Izquierdo MS, Socorro J, Roo J (2010) Studies on the appearance of skeletal anomalies in red porgy: effect of culture intensiveness, feeding habits and nutritional quality of live preys. J Appl Ichthyol 26:320–326. https://doi.org/10.1111/j.1439-0426.2010.01429.x

    Article  Google Scholar 

  12. Fernández I, Gisbert E (2011) The effect of vitamin A on flatfish development and skeletogenesis: a review. Aquaculture 315:34–48. https://doi.org/10.1016/j.aquaculture.2010.11.025

    CAS  Article  Google Scholar 

  13. Darias MJ, Mazurais D, Koumoundouros G, Glynatsi N, Christodoulopoulou S, Huelvan C, Desbruyeres E, le Gall MM, Quazuguel P, Cahu CL, Zambonino-Infante JL (2010) Dietary vitamin D 3 affects digestive system ontogenesis and ossification in European. Aquaculture 298:300–307. https://doi.org/10.1016/j.aquaculture.2009.11.002

    CAS  Article  Google Scholar 

  14. 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

    CAS  Article  Google Scholar 

  15. 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

    CAS  Article  Google Scholar 

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

    Google Scholar 

  17. 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 

  18. 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 

  19. Baeverfjord G, Antony Jesu Prabhu P, Fjelldal PG, Albrektsen S, Hatlen B, Denstadli V, Ytteborg E, Takle H, Lock EJ, Berntssen MHG, Lundebye AK, Åsgård T, Waagbø R (2019) Mineral nutrition and bone health in salmonids. Rev Aquac 11:740–765. https://doi.org/10.1111/raq.12255

    Article  Google Scholar 

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

    Google Scholar 

  21. Nguyen VT, Satoh S, Haga Y, Fushimi H, Kotani T (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

    CAS  Article  Google Scholar 

  22. Izquierdo MS, Ghrab W, Roo J, Hamre K, Hernández-Cruz CM, Bernardini G, Terova G, Saleh R (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

    CAS  Article  Google Scholar 

  23. Terova G, Rimoldi S, Izquierdo M, Pirrone C, Ghrab W, Bernardini G (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 44:1375–1391. https://doi.org/10.1007/s10695-018-0528-7

    CAS  Article  PubMed  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 M, Ralston S (eds) Bone research protocols. Methods in molecular biology (methods and protocols). Humana Press, Totowa, NJ, p 588

    Google Scholar 

  25. Mabilleau G, Mieczkowska A, Irwin N, Flatt PR, Chappard D (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

    CAS  Article  PubMed  Google Scholar 

  26. Gavaia PJ, Dinis MT, Cancela ML (2002) Osteological development and abnormalities of the vertebral column and caudal skeleton in larval and juvenile stages of hatchery-reared Senegal sole (Solea senegalensis). Aquaculture 211:305–323. https://doi.org/10.1016/S0044-8486(02)00167-9

    Article  Google Scholar 

  27. Losada BAP, 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. Du SJ, Frenkel V, Kindschi G, Zohar Y (2001) Visualizing normal and defective bone development in zebrafish embryos using the fluorescent chromophore calcein. Dev Biol 238:239–246. https://doi.org/10.1006/dbio.2001.0390

    CAS  Article  PubMed  Google Scholar 

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

  30. 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 

  31. Hamre K, Yúfera M, Rønnestad I, Boglione C, Conceição LEC, Izquierdo M (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 

  32. Pittman K, Yúfera M, Pavlidis M, Geffen AJ, Koven W, Ribeiro L, Zambonino-Infante JL, Tandler A (2013) Fantastically plastic: fish larvae equipped for a new world. Rev Aquac 5:5–S267. https://doi.org/10.1111/raq.12034

    Article  Google Scholar 

  33. Canada P, Engrola S, Mira S, Teodósio R, Fernandes JMO, Sousa V, Barriga-Negra L, Conceição LEC, Valente LMP (2016) The supplementation of a microdiet with crystalline indispensable amino-acids affects muscle growth and the expression pattern of related genes in Senegalese sole (Solea senegalensis) larvae. Aquaculture 458:158–169. https://doi.org/10.1016/j.aquaculture.2016.03.010

    CAS  Article  Google Scholar 

  34. Panserat S, Marandel L, Geurden I, Veron V, Dias K, Plagnes-Juan E, Pegourié G, Arbenoits E, Santigosa E, Weber G, Verlhac Trichet V (2017) Muscle catabolic capacities and global hepatic epigenome are modified in juvenile rainbow trout fed different vitamin levels at first feeding. Aquaculture 468:515–523. https://doi.org/10.1016/j.aquaculture.2016.11.021

    CAS  Article  Google Scholar 

  35. Pinto W, Engrola S, da Conceição LEC (2018) Towards an early weaning in Senegalese sole : a historical review. Aquaculture 496:1–9. https://doi.org/10.1016/j.aquaculture.2018.06.077

    Article  Google Scholar 

  36. Shahpar Z, Johari SA (2018) Effects of dietary organic, inorganic, and nanoparticulate zinc on rainbow trout, Oncorhynchus mykiss. Larvae Biol Trace Elem Res 190:37–40. https://doi.org/10.1007/s12011-018-1563-z

    CAS  Article  Google Scholar 

  37. Roberto VP, Martins G, Pereira A, Rodrigues S, Grenha A, Pinto W, Cancela ML, Dias J, Gavaia PJ (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

    CAS  Article  Google Scholar 

  38. Li MH, Robinson EH (1996) Comparison of chelated zinc and zinc sulfate as zinc sources for growth and bone mineralization of channel catfish (Ictalurus punctatus) fed practical diets. 146:237–243

  39. Do Carmo e Sá MV, Pezzato LE, Ferreira LMMB, Padilha PDM (2004) Optimum zinc supplementation level in Nile tilapia Oreochromis niloticus juveniles diets. Aquaculture 238:385–401. https://doi.org/10.1016/j.aquaculture.2004.06.011

    CAS  Article  Google Scholar 

  40. Buentello JA, Goff JB, Gatlin DM (2009) Dietary zinc requirement of hybrid striped bass, Morone chrysops × Morone saxatilis, and bioavailability of two chemically different zinc compounds. J World Aquac Soc 40:687–694. https://doi.org/10.1111/j.1749-7345.2009.00288.x

    Article  Google Scholar 

  41. Fountoulaki E, Morgane H, Rigos G, Antigoni V, Mente E, Sweetman J, Nengas I (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

    CAS  Article  Google Scholar 

  42. Luo Z, Tan XY, Zheng JL, Chen QL, Liu CX (2011) Quantitative dietary zinc requirement of juvenile yellow catfish Pelteobagrus fulvidraco, and effects on hepatic intermediary metabolism and antioxidant responses. Aquaculture 319:150–155. https://doi.org/10.1016/j.aquaculture.2011.06.047

    CAS  Article  Google Scholar 

  43. Liu K, Ai QH, Mai KS, Zhang WB, Zhang L, Zheng SX (2013) Dietary manganese requirement for juvenile cobia, Rachycentron canadum L. Aquac Nutr 19:461–467. https://doi.org/10.1111/j.1365-2095.2012.00979.x

    CAS  Article  Google Scholar 

  44. Liang JJ, Wang S, Han B, Tian LX, Yang HJ, Liu YJ (2015) Dietary manganese requirement of juvenile grass carp (Ctenopharyngodon idella Val.) based on growth and tissue manganese concentration. Aquac Res 46:2991–2998. https://doi.org/10.1111/are.12455

    CAS  Article  Google Scholar 

  45. Maage A, Lygren B, El-Mowafi AFA (2000) Manganese requirement of Atlantic salmon (Salmo salar) fry. Fish Sci 66:1–8

    CAS  Article  Google Scholar 

  46. Antony Jesu Prabhu P, Schrama JW, Kaushik SJ et al (2014) Mineral requirements of fish: a systematic review. Rev Aquac 8:172–219. https://doi.org/10.1111/raq.12090

    Article  Google Scholar 

  47. Gatlin DM, Wilson RP (1984) Studies on the manganese requirement of fingerling channel catfish. Aquaculture 41:85–92. https://doi.org/10.1016/0044-8486(84)90085-1

    CAS  Article  Google Scholar 

  48. Ye CX, Tian LX, Yang HJ et al (2009) Growth performance and tissue mineral content of juvenile grouper (Epinephelus coioides) fed diets supplemented with various levels of manganese. Aquac Nutr 15:608–614. https://doi.org/10.1111/j.1365-2095.2008.00628.x

    CAS  Article  Google Scholar 

  49. Huang F, Jiang M, Wen H, Wu F, Liu W, Tian J, Yang C (2015) Dietary zinc requirement of adult Nile tilapia (Oreochromis niloticus) fed semi-purified diets, and effects on tissue mineral composition and antioxidant responses. Aquaculture 439:53–59. https://doi.org/10.1016/j.aquaculture.2015.01.018

    CAS  Article  Google Scholar 

  50. Liang JJ, Yang HJ, Liu YJ et al (2012) Dietary zinc requirement of juvenile grass carp (Ctenopharyngodon idella) based on growth and mineralization. Aquac Nutr 18:380–387. https://doi.org/10.1111/j.1365-2095.2011.00935.x

    CAS  Article  Google Scholar 

  51. Seo H, Cho Y, Kim T et al (2010) Zinc may increase bone formation through stimulating cell proliferation, alkaline phosphatase activity and collagen synthesis in osteoblastic MC3T3-E1 cells. Nutr Res Pract 4:356–361. https://doi.org/10.4162/nrp.2010.4.5.356

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Callaway DA, Jiang JX (2015) Reactive oxygen species and oxidative stress in osteoclastogenesis, skeletal aging and bone diseases. J Bone Miner Metab 33:359–370. https://doi.org/10.1007/s00774-015-0656-4

    CAS  Article  PubMed  Google Scholar 

  53. Arai M, Shibata Y, Pugdee K, Abiko Y, Ogata Y (2007) Effects of reactive oxygen species (ROS) on antioxidant system and osteoblastic differentiation in MC3T3-E1 cells. IUBMB Life 59:27–33. https://doi.org/10.1080/15216540601156188

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Vanda Chaveiro for all her work performed with the rearing of the fish.

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 received financial support from FCT/MCTES (Portugal) through a doctoral fellowship (grant PDE/BDE/113672/2015) within the framework or the doctoral program SANFEED, PDE/0023/2013.

Author information

Authors and Affiliations

Authors

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 Amosfera (IPMA) (Project LARVAMIX approval no. 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 no. 113/2013, August 7th) legislation on the protection of animals for scientific purposes.

Conflict of Interest

The authors declare that they have no conflict of interest.

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

Viegas, M.N., Salgado, M.A., Aguiar, C. et al. 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 (2021). https://doi.org/10.1007/s12011-020-02307-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-020-02307-4

Keywords

  • Manganese
  • Zinc
  • Solea senegalensis
  • Post larvae
  • Growth
  • Malformations