Skeletal deformities in gilthead seabream (Sparus aurata): exploring the association between mechanical loading and opercular deformation

Authors

  • Vincent Vermeylen Laboratory of Aquaculture and Artemia Reference Center, Ghent University, Coupure Links 653, 9000 Gent and Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, 9000 Gent
  • Barbara De Kegel Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, 9000 Gent
  • Tania De Wolf INVE, Maricoltura di Rosignano Solvay, srl, Via P. Gigli (Loc Lillatro), 57013 Rosignano Solvay
  • Dominique Adriaens Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, 9000 Gent

DOI:

https://doi.org/10.26496/bjz.2023.110

Keywords:

operculum, deformation, Sparus aurata

Abstract

Fish aquaculture is frequently confronted with skeletal abnormalities. In gilthead seabream (Sparus aurata (Linnaeus, 1758)), opercular deformities are one of the most common types of deformities. Many studies point at potential causal factors, mainly genetic or nutritional. However, no clear consensus has surfaced yet, and other factors known to affect bone formation remain unexplored, including mechanical stressors by external forces or muscle contraction. In this study, we investigated whether an altered mechanical use of the gill cover could be associated with opercular deformities, by inducing a change in the respiratory rate and thus gill ventilation. Juvenile seabreams were reared under 80, 100 or 200% dissolved oxygen (DO) to trigger altered respiration behaviour, and the effect on body and opercular shape was analysed. The main hypothesis was that hypoxic conditions would increase opercular ventilation, which would result in a higher prevalence of opercular deformities. The results show that the hypoxic condition (80% DO) did not trigger a significantly higher prevalence of opercular deformations, though the opposite is true for the hyperoxic condition (200% DO). No effect of oxygen treatment was observed on overall body shape, though deformed opercles showed a pronounced, but non-significant difference in shape across treatments. Morphometric results and µCT scans reveal that deformations mainly occur in the dorsocaudal region of the opercular bone. Although no causal link could be demonstrated, we discuss how these results can indirectly suggest that an altered mechanical loading on the operculum could explain its deformation.

References

Adams D.C. & Otárola-Castillo E. (2013). geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution 4: 393–399. https://doi.org/10.1111/2041-210X.12035

Adams D., Collyer M. & Kaliontzopoulou A. (2018). Geometric Morphometric Analyses of 2D/3D Landmark Data. Available from https://rdrr.io/cran/geomorph/ [accessed 17 July 2023].

Andrades J.A., Becerra J. & Fernandez-Llebrez P. (1996). Skeletal deformities in larval, juvenile and adult stages of cultured gilthead sea bream (Sparus aurata L.). Aquaculture 141: 1–11. https://doi.org/10.1016/0044-8486(95)01226-5

Atkins A., Milgram J., Weiner S. & Shahar R. (2015). The response of anosteocytic bone to controlled loading. Journal of Experimental Biology 218: 3559–3569. https://doi.org/10.1242/jeb.124073

Beraldo, P. & Canavese, B. (2011). Recovery of opercular anomalies in gilthead sea bream, Sparus aurata L.: morphological and morphometric analysis. Journal of Fish Diseases 34: 21–30. https://doi.org/10.1111/j.1365-2761.2010.01206.x

Beraldo P., Pinosa M., Tibaldi E. & Canavese B. (2003). Abnormalities of the operculum in gilthead sea bream (Sparus aurata): morphological description. Aquaculture 220: 89–99. https://doi.org/10.1016/S0044-8486(02)00416-7

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. Reviews in Aquaculture 5: S121–S167. https://doi.org/10.1111/raq.12016

Bonewald L.F. (2011). The amazing osteocyte. Journal of Bone and Mineral Research 26: 229–238. https://doi.org/10.1002/jbmr.320

Bonhomme V., Picq S., Gaucherel C. & Claude J. (2014). Momocs: outline analysis using R. Journal of Statistical Software 56: 1–24. https://doi.org/10.18637/jss.v056.i13

Cerezo J. & García García B. (2004). The effects of oxygen levels on oxygen consumption, survival and ventilatory frequency of sharpsnout sea bream (Diplodus puntazzo Gmelin, 1789) at different conditions of temperature and fish weight. Journal of Applied Ichthyology 20: 488–492. https://doi.org/10.1111/j.1439-0426.2004.00601.x

Chatain B. (1994). Abnormal swimbladder development and lordosis in sea bass (Dicentrarchus labrax) and sea bream (Sparus auratus). Aquaculture 119: 371–379. https://doi.org/10.1016/0044-8486(94)90301-8

Divanach P.B.C.M.B., Boglione C., Menu B., Koumoundouros G., Kentouri M. & Cataudella S. (1996). Abnormalities in finfish mariculture: an overview of the problem, causes and solutions. Special Publication/European Aquaculture Society 45–66.

Domenici P., Herbert N.A., Lefrançois C., Steffensen J.F. & McKenzie D.J. (2013). The effect of hypoxia on fish swimming performance and behaviour. Swimming Physiology of Fish: Towards Using Exercise to Farm a Fit Fish in Sustainable Aquaculture 129–159. https://doi.org/10.1007/978-3-642-31049-2_6

Ekanayake S. & Hall B. K. (1988). Ultrastructure of the osteogenesis of acellular vertebral bone in the Japanese medaka, Oryzias latipes (Teleostei, Cyprinidontidae). American Journal of Anatomy 182: 241–249. https://doi.org/10.1002/aja.1001820305

EUMOFA (2022). The EU Fish Market. Luxembourg: Publications Office of the European Union. https://doi.org/10.2771/716731

Faustino M. & Power D.M. (2001). Osteologic development of the viscerocranial skeleton in sea bream: alternative ossification strategies in teleost fish. Journal of Fish Biology 58: 537–572. https://doi.org/10.1111/j.1095-8649.2001.tb02272.x

Fernández I., Darias M., Andree K.B., Mazurais D., Zambonino-Infante J.L. & Gisbert E. (2011). Coordinated gene expression during gilthead sea bream skeletogenesis and its disruption by nutritional hypervitaminosis A. BMC Developmental Biology 11: 7. https://doi.org/10.1186/1471-213X-11-7

Ferrer M.A., Calduch-Giner J.A., Díaz M., Sosa J., Rosell-Moll E., Abril J.S.,Sosa G.S., Delgado T.B., Carmona C., Martos-Sitcha J.A., Cabruja E., Afonso J.M., Vega A., Lozano M., Montiel-Nelson J.A. & Pérez-Sánchez J. (2020). From operculum and body tail movements to different coupling of physical activity and respiratory frequency in farmed gilthead sea bream and European sea bass. Insights on aquaculture biosensing. Computers and Electronics in Agriculture 175: 105531. https://doi.org/10.1016/j.compag.2020.105531

Galeotti M., Beraldo P., De Dominis S., D’angelo L., Ballestrazzi R., Musetti R., Pizzolito S. & Pinosa M. (2000). A preliminary histological and ultrastructural study of opercular anomalies in gilthead sea bream larvae (Sparus aurata). Fish Physiology and Biochemistry 22: 151–157. https://doi.org/10.1023/A:1007883008076

García-Celdrán M., Ramis G., Manchado M., Estévez A., Afonso J. M., María-Dolores E., Peñalver J. & Armero E. (2015). Estimates of heritabilities and genetic correlations of growth and external skeletal deformities at different ages in a reared gilthead sea bream (Sparus aurata L.) population sourced from three broodstocks along the Spanish coasts. Aquaculture 445: 33–41. https://doi.org/10.1016/j.aquaculture.2015.04.006

García-Celdrán M., Cutáková Z., Ramis G., Estévez A., Manchado M., Navarro A., María-Dolores E., Peñalver J., Sánchez J.A. & Armero E. (2016). Estimates of heritabilities and genetic correlations of skeletal deformities and uninflated swimbladder in a reared gilthead sea bream (Sparus aurata L.) juvenile population sourced from three broodstocks along the Spanish coasts. Aquaculture 464: 601–608. https://doi.org/10.1016/j.aquaculture.2016.08.004

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

Hughes G.M. (1960). A comparative study of gill ventilation in marine teleosts. Journal of Experimental Biology 37: 28–45. https://doi.org/10.1242/jeb.37.1.28

Kimmel C.B., DeLaurier A., Ullmann B., Dowd J. & McFadden M. (2010). Modes of developmental outgrowth and shaping of a craniofacial bone in zebrafish. PloS ONE 5: e9475. https://doi.org/10.1371/journal.pone.0009475

Koumoundouros G. (2010). Morpho-anatomical abnormalities in Mediterranean marine aquaculture. Recent Advances in Aquaculture Research 66: 125–148.

Koumoundouros G., Oran G., Divanach P., Stefanakis S. & Kentouri M. (1997). The opercular complex deformity in intensive gilthead sea bream (Sparus aurata L.) larviculture. Moment of apparition and description. Aquaculture 156: 165–177. https://doi.org/10.1016/S0044-8486(97)89294-0

Kranenbarg S., Waarsing J.H., Muller M., Weinans H. & van Leeuwen J.L. (2005). Lordotic vertebrae in sea bass (Dicentrarchus labrax L.) are adapted to increased loads. Journal of Biomechanics 38: 1239–1246. https://doi.org/10.1016/j.jbiomech.2004.06.011

Kuhl F.P. & Giardina C.R. (1982). Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing 18: 236–258. https://doi.org/10.1016/0146-664X(82)90034-X

Kuroki M., Okamura A., Takeuchi A. & Tsukamoto K. (2016). Effect of water current on the body size and occurrence of deformities in reared Japanese eel leptocephali and glass eels. Fisheries Science 82: 941–951. https://doi.org/10.1007/s12562-016-1015-7

MacArthur R.H. (1957). On the relative abundance of bird species. Proceedings of the National Academy of Sciences 43: 293–295. https://doi.org/10.1073/pnas.43.3.293

Magnoni L.J., Eding E., Leguen I., Prunet P., Geurden I., Ozório R.O. & Schrama J.W. (2018). Hypoxia, but not an electrolyte-imbalanced diet, reduces feed intake, growth and oxygen consumption in rainbow trout (Oncorhynchus mykiss). Scientific Reports 8: 1–14. https://doi.org/10.1038/s41598-018-23352-z

Martos-Sitcha J.A., Sosa J., Ramos-Valido D., Bravo F.J., Carmona-Duarte C., Gomes H.L., Calduch-Giner J.À., Cabruja E., Vega A., Ferrer M.Á., Lozano M., Montiel-Nelson J.A., Afonso J.M. & Pérez-Sánchez J. (2019). Ultra-low power sensor devices for monitoring physical activity and respiratory frequency in farmed fish. Frontiers in Physiology 10: 667. https://doi.org/10.3389/fphys.2019.00667

McArley T.J. Sandblom E. & Herbert N.A. (2021). Fish and hyperoxia—from cardiorespiratory and biochemical adjustments to aquaculture and ecophysiology implications. Fish and Fisheries 22: 324–355. https://doi.org/10.1111/faf.12522

Morel C., Adriaens D., Boone M., De Wolf T., Van Hoorebeke L. & Sorgeloos P. (2010). Visualizing mineralization in deformed opercular bones of larval gilthead sea bream (Sparus aurata). Journal of Applied Ichthyology 26: 278–279. https://doi.org/10.1111/j.1439-0426.2010.01420.x

Noble C., Jones H.A.C., Damsgård B., Flood M.J., Midling K.Ø., Roque A., Sæther B.-S. & Cottee S.Y. (2012). Injuries and deformities in fish: their potential impacts upon aquacultural production and welfare. Fish Physiology and Biochemistry 38: 61–83. https://doi.org/10.1007/s10695-011-9557-1

Ofer L., Dumont M., Rack A., Zaslansky P. & Shahar R. (2019). New insights into the process of osteogenesis of anosteocytic bone. Bone 125: 61–73. https://doi.org/10.1016/j.bone.2019.05.013

Ortiz-Delgado J.B., Fernández I., Sarasquete C. & Gisbert E. (2014). Normal and histopathological organization of the opercular bone and vertebrae in gilthead sea bream Sparus aurata. Aquatic Biology 21: 67–84. https://doi.org/10.3354/ab00568

Paperna I., Ross B., Colorni A. & Colorni B. (1980). Diseases of marine fish cultured in Eilat mariculture project based at the Gulf of Aqaba, Red Sea. Studies and Reviews-General Fisheries Council for the Mediterranean (FAO) 57.

Pavlidis M.A. & Mylonas C.C. (2011). Sparidae: Biology and Aquaculture of Gilthead Sea Bream and Other Species. John Wiley & Sons.

Perry S.F., Jonz M.G. & Gilmour K.M. (2009). Oxygen sensing and the hypoxic ventilatory response. Fish Physiology 27: 193–253. https://doi.org/10.1016/S1546-5098(08)00005-8

Prestinicola L., Boglione C. & Cataudella S. (2014). Relationship between uninflated swim bladder and skeletal anomalies in reared gilthead seabream (Sparus aurata). Aquaculture 432: 462–469. https://doi.org/10.1016/j.aquaculture.2014.06.020

R Core Team (2018). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

Rahman M.S. & Thomas P. (2007). Molecular cloning, characterization and expression of two hypoxia-inducible factor alpha subunits, HIF-1alpha and HIF-2alpha, in a hypoxia-tolerant marine teleost, Atlantic croaker (Micropogonias undulatus). Gene 396: 273–282. https://doi.org/10.1016/j.gene.2007.03.009

Remen M., Nederlof M.A., Folkedal O., Thorsheim G., Sitjà-Bobadilla A., Pérez-Sánchez J., Oppedal F. & Olsen R.E. (2015). Effect of temperature on the metabolism, behaviour and oxygen requirements of Sparus aurata. Aquaculture Environment Interactions 7: 115–123. https://doi.org/10.3354/aei00141

Rohlf F.J. (2015). The tps series of software. Hystrix 26. https://doi.org/10.4404/hystrix-26.1-11264

Rohlf F.J. & Bookstein F.L. (1990). Proceedings of the Michigan Morphometrics Workshop. University of Michigan Museum of Zoology.

Rohlf F.J. & Slice D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology 39: 40–59. https://doi.org/10.2307/2992207

Roo J., Socorro J. & Izquierdo M.S. (2010). Effect of rearing techniques on skeletal deformities and osteological development in red porgy Pagrus pagrus (Linnaeus, 1758) larvae. Journal of Applied Ichthyology 26: 372–376. https://doi.org/10.1111/j.1439-0426.2010.01437.x

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.-Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P. & Tinevez J.Y. (2012). Fiji: an open-source platform for biological-image analysis. Nature Methods 9: 676. https://doi.org/10.1038/nmeth.2019

Schneider C.A., Rasband W.S. & Eliceiri K.W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671. https://doi.org/10.1038/nmeth.2089

Sfakianakis D.G., Renieri E., Kentouri M. & Tsatsakis A.M. (2015). Effect of heavy metals on fish larvae deformities: a review. Environmental research 137: 246–255. https://doi.org/10.1016/j.envres.2014.12.014

Shahar R. & Dean M. N. (2013). The enigmas of bone without osteocytes. BoneKEy Reports 2. https://doi.org/10.1038/bonekey.2013.77

Simon M.C. & Keith B. (2008). The role of oxygen availability in embryonic development and stem cell function. Nature Reviews Molecular Cell Biology 9: 285. https://doi.org/10.1038/nrm2354

Taylor E.W., Campbell H.A., Levings J.J., Young M.J., Butler P.J. & Egginton S. (2006). Coupling of the respiratory rhythm in fish with activity in hypobranchial nerves and with heartbeat. Physiological and Biochemical Zoology 79: 1000–1009. https://doi.org/10.1086/507663

Thuong N.P., Verstraeten B., Kegel B.D., Christiaens J., Wolf T.D., Sorgeloos P., Bonte D. & Adriaens D. (2017). Ontogenesis of opercular deformities in gilthead sea bream Sparus aurata: a histological description. Journal of Fish Biology 91: 1419–1434. https://doi.org/10.1111/jfb.13460

Thuong N.P., Dierick M., De Wolf T. & Adriaens D. (2018). A 3D quantitative method for analyzing bone mineral densities: a case study on skeletal deformities in the gilthead sea bream, Sparus aurata (Linnaeus, 1758). Belgian Journal of Zoology 148. https://doi.org/10.26496/bjz.2018.24

Totland G.K., Fjelldal P.G., Kryvi H., Løkka G., Wargelius A., Sagstad A., Hansen T. & Grotmol S. (2011). Sustained swimming increases the mineral content and osteocyte density of salmon vertebral bone. Journal of Anatomy 219: 490–501. https://doi.org/10.1111/j.1469-7580.2011.01399.x

Utting J.C., Robins S.P., Brandao-Burch A., Orriss I.R., Behar J. & Arnett T.R. (2006). Hypoxia inhibits the growth, differentiation and bone-forming capacity of rat osteoblasts. Experimental Cell Research 312: 1693–1702. https://doi.org/10.1016/j.yexcr.2006.02.007

Valverde J.C., López F.J.M. & García B.G. (2006). Oxygen consumption and ventilatory frequency responses to gradual hypoxia in common dentex (Dentex dentex): basis for suitable oxygen level estimations. Aquaculture 256: 542–551. https://doi.org/10.1016/j.aquaculture.2006.02.030

Verhaegen Y., Adriaens D., De Wolf T., Dhert P. & Sorgeloos P. (2007). Deformities in larval gilthead sea bream (Sparus aurata): A qualitative and quantitative analysis using geometric morphometrics. Aquaculture 268: 156–168. https://doi.org/10.1016/j.aquaculture.2007.04.037

Vlassenbroeck J., Dierick M., Masschaele B., Cnudde V., Van Hoorebeke L. & Jacobs P. (2007). Software tools for quantification of X-ray microtomography at the UGCT. Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment 580: 442–445. https://doi.org/10.1016/j.nima.2007.05.073

Wang T., Lefevre S., van Cong N. & Bayley M. (2009). The effects of hypoxia on growth and digestion. Fish Physiology 27: 361–396. https://doi.org/10.1016/S1546-5098(08)00008-3

Winterbottom R. (1973). A descriptive synonymy of the striated muscles of the Teleostei. Proceedings of the Academy of Natural Sciences of Philadelphia: 225–317.

Witten P.E. & Hall B.K. (2015). Teleost skeletal plasticity: modulation, adaptation, and remodelling. Copeia 103: 727–739. https://doi.org/10.1643/CG-14-140

Witten P.E. & Huysseune A. (2009). A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biological Reviews 84: 315–346. https://doi.org/10.1111/j.1469-185X.2009.00077.x

Wu Z., You F., Wen A., Ma D. & Zhang P. (2016). Physiological and morphological effects of severe hypoxia, hypoxia and hyperoxia in juvenile turbot (Scophthalmus maximus L.). Aquaculture Research 47: 219–227. https://doi.org/10.1111/are.12483

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Published

2023-07-20

How to Cite

Vermeylen, V., De Kegel, B., De Wolf, T., & Adriaens, D. (2023). Skeletal deformities in gilthead seabream (Sparus aurata): exploring the association between mechanical loading and opercular deformation. Belgian Journal of Zoology, 153. https://doi.org/10.26496/bjz.2023.110

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Vol. 153 (2023)

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