Abstract
Turbot specimens were kept at three temperatures (T s ): warm (W) (21–22 °C), ambient (A) (17–18 °C) and cold (C) (13–14 °C) during the larval and early postlarval stages. At 90 days posthatching (dph), all of them were transferred to ambient T until 190 dph. At 2–3 dph, the specimens showed a monolayer of red muscle and immature white fibres; external or dermomyotome cells (presumptive myogenic cells) were observed on the surface of the red muscle. In the following stages, many myogenic cells and presumptive myogenic precursors were observed within the myotome, presumably derived of the dermomyotome. When comparing the growth at the same age (2, 10, 25, 37 dph), the body length and the muscle growth were positively influenced by the warm T, being the hyperplasia the muscle parameter more significantly influenced. The development rate was also positively correlated with the high T: the beginning of the metamorphosis took place at 15, 23 and 25 dph at W, A and C temperatures, respectively, with the highest body length values at ambient temperature. The metamorphosis finished at 25, 30 and 37 dph at W, A and C temperatures, respectively, with the highest body length values at warm temperature. However, the muscle cellularity was similar in all the groups at the end of the metamorphosis. At 90 and 190 dph, the largest body length was observed at W temperature. However, the muscle cellularity was similar between A and W; the number of fibres was similar in all the groups at 190 dph, which shows the beginning of a compensatory muscle growth in A and C, mainly in A.
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References
Atkinson D (1996) Ectotherm life-history responses to development temperature. In: Johnston IA, Bennett AF (eds) Phenotypic and evolutionary adaptation of organisms to temperature. Society for experimental biology seminar series. Cambridge University Press, Cambridge, pp 183–204
Ayala MD, López-Albors O, Gil F, Latorre R, Vázquez JM, García-Alcázar A, Abellán E, Ramírez G, Moreno F (2000) Temperature effects on muscle growth of the axial musculature of the sea bass (Dicentrarchus labrax L.). Anat Histol Embryol 29:235–241
Ayala MD, López-Albors O, Gil F, García-Alcázar A, Abellán E, Alarcón JM, Álvarez MC, Ramírez-Zarzosa G, Moreno F (2001) Temperature effects on muscle growth in two populations (Atlantic and Mediterranean) of sea bass, Dicentrachus labrax L. Aquaculture 202:359–370
Ayala MD, López-Albors O, García Alcázar A, Abellán E, Latorre R, JMª Vázquez, Ramírez Zarzosa G, Martínez F, Gil F (2003) Effect of two thermal regimes on the muscle growth dynamics of sea bass larvae, Dicentrarchus labrax L. Anat Histol Embryol 32:271–275
Ayala MD, Abellán E, Arizcun M, García-Alcázar A, Navarro F, Blanco A, López-Albors O (2013) Muscle development and body growth in larvae and early postlarvae of shi drum, Umbrina cirrosa L., reared under different larval photoperiod. Muscle structural and ultrastructural Study. Fish Physiol Biochem 39:807–827
Ayala MD, Gómez C, Santaella M, Cal R (2014) Lasting temperature effects on the muscle tissue, body growth and fillet texture of adult turbots, Scophthalmus maximus L. Aquaculture European Congress, San Sebastián (Spain), Abstracts book, pp 94–95
Ayala MD, MªJ Lago, Cal R (2015) Body and muscle growth of pre-larvae and larvae of turbot, Scophthalmus maximus reared under different temperatures. Open J Anim Sci. 5(4):402–410
Campos C, Fernandes JMO, Conceição LEC, Engrola S, Vousa V, Valente LMP (2013) Thermal conditions during larval pelagic phase influence subsequent somatic growth of Senegaleses sole by modulating gene expression and muscle growth dynamics. Aquaculture 414–415:46–55
García de la Serrana D, Vieira VLA, Andree KB, Darias M, Estévez A, Gisbert E, Johnston IA (2012) Development temperature has persistent effects on muscle growth responses in gilthead sea bream. PLoS One 7(12):1–11
Gibson S, Johnston I (1995) Temperature and development in larvae of the turbot scophthalmus maximus. Mar Biol 124:17–25
Hollway GE, Bryson-Richardson RJ, Berger S, Cole NJ, Hall TE, Currie PD (2007) Whole-somite rotation generates muscle progenitor cell compartments in the developing zebrafish embryo. Dev Cell 12:207–219
Johnston IA, Mclay HA (1997) Temperature and family effects on muscle cellularity at hatch and first feeding in Atlantic salmon (Salmo salar L.). Can J Zool 75:64–74
Johnston IA, Cole NJ, Vieira VLA, Davidson I (1997) Temperature and developmental plasticity of muscle phenotype in herring larvae. J Exp Biol 200:849–868
Johnston IA, Alderson R, Sandham C, Mitchell D, Selkirk C, Dingwall A, Nickell D, Baker R, Robertson B, Whyte F, Springate J (2000) Patterns of muscle growth in early and late maturing populations of Atlantic salmon (Salmo salar L.). Aquaculture 189:307–333
Johnston IA, Manthri S, Alderson R, Smart A, Campbell P, Nickell D, Robertson D, Paxton CM, Burt LM (2003) Freshwater environment affects growth rate and muscle fibre recruitment in seawater stages of Atlantic salmon (Salmo salar L.). J Exp Biol 206:1337–1351
Johnston IA, Bower NI, Macqueen DJ (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214:1617–1628
Kacperczyk A, Jedrzejowska I, Daczewska M (2011) Differentiation and growth of myotomal muscles in a non-model tropical fish Pterophyllum scalarae (Teleostei: cichlidae). Anat Histol Embryol 40:411–418
Kamler E (1992) Early life history of fish: an energetics approach. Chapman and Hall, London, p 267
Koumans JTM, Akster HA (1995) Myogenic cells in development and growth of fish. Comp Biochem Physiol 110A(1):3–20
López-Albors O, Gil F, Ramírez Zarzosa G, Vázquez JM, Latorre R, García Alcázar A, Arencibia A, Moreno F (1998) Muscle development in Gilthead Sea Bream (Sparus aurata, L.) and sea bass (Dicentrarchus labrax, L.): further histochemical and ultrastructural aspects. Anat Histol Embryol 27:223–229
López-Albors O, Ayala MD, Gil F, García-Alcázar A, Abellán E, Latorre R, Ramírez-Zarzosa G, Vázquez JMª (2003) Early temperature effects on muscle growth dynamics and histochemical profile of muscle fibres of sea bass Dicentrarchus labrax L., during larval and juvenile stages. Aquaculture 220:385–406
López-Albors O, Abdel I, MªJ Periago, MªD Ayala, García-Alcázar A, Martínez Graciá C, Nathanailides C, Vázquez JMª (2008) Temperature influence on the white muscle growth dynamics of the sea bass Dicentrarchus labrax, L. Flesh quality implications at commercial size. Aquaculture 277:39–51
López-Albors O, Arizcun M, Abellán E, Blanco A, Ayala MD, Pastor LM, Latorre R (2010) Posthatch development of the axial musculature of the common dentex Dentex dentex, L. (Teleostei). Histol Histopathol 25:1557–1571
Marschallinger J, Obermayer A, Sänger AM, Stoiber W, Steinbacher P (2009) Postembryonic fast muscle growth of teleost fish depends upon a nonuniformly distributed population of mitotically active pax7+ precursor cells. Dev Dyn 238:2442–2448
Nathanailides C, Lopez-Albors O, Stickland NC (1995) Influence of prehatch temperature on the development of muscle cellularity in posthatch Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 52:675–680
Rescan PY (2008) New insights into skeletal muscle development and growth in teleost fishes. J Exp Zool B Mol Dev Evol 310:541–548
Rowlerson A, Mascarello A, Radaelli G, Veggetti A (1995) Differentiation and growth of muscle in the fish Sparus aurata (L.) II. Hyperplastic and hypertrophic growth of lateral muscle from hatching to adult. J Muscle Res Cell Motil 16:223–236
Scapolo PA, Veggetti A, Mascarello F, Romanello MG (1988) Developmental transitions of myosin isoforms and organization of the lateral muscle in the teleost Dicentrarchus labrax (L.). Anat Embryol 178:287–295
Steinbacher P, Haslett JR, Six M, Gollmann HP, Sänger AM, Stoiber W (2006) Phases of myogenic cell activation and possible role of dermomyotome cells in teleost muscle formation. Dev Dyn 235:3132–3143
Steinbacher P, Haslett JR, Obermayer A, Marschallinger J, Bauer HC, Sänger AM, Stoiber W (2007) MyoD and Myogenin expression during myogenesis phases in brown trout: a precocious onset of mosaic hyperplasia is a prerequisite for fast somatic growth. Dev Dyn 236:1106–1114
Steinbacher P, Stadlmayr V, Marschallinger J, Sänger AM, Stoiber W (2008) Lateral fast muscle fibers originate from the posterior lip of the teleost dermomyotome. Dev Dyn 237(11):3233–3239
Stellabotte F, Devoto SH (2007) The teleost dermomyotome. Dev Dyn 236:2432–2443
Stickland NC, White RN, Mescall PE, Crook AR, Thorpe JE (1988) The effect of temperature on myogenesis en embryonic development of the Atlantic salmon (Salmo salar, L.). Anat Embryol 178:253–257
Stoiber W, Haslett JR, Goldschmid A, Sänger AM (1998) Patterns of superficial fibre formation in the European pearlfish (Rutilus frisii meidingeri) provide a general template for slow muscle development in teleost fish. Anat Embryol (Berl) 197:485–496
Torres-Núñez E, Cal R, Rotllant J (2014) Phenotypic plasticity during early ontogeny in cultured turbot (Scophthalmus maximus): changes in dorsal and anal fin ray counts by water temperature. J Appl Ichthyol 30:762–766
Usher ML, Stickland NC, Thorpe JE (1994) Muscle development in Atlantic salmon (Salmo salar) embryos and the effect of temperature on muscle cellularity. J Fish Biol 44:953–964
Veggetti A, Mascarello F, Scapolo PA, Rowlerson A (1990) Hyperplastic and hypertrophic growth of lateral muscle in Dicentrarchus labrax (L.): an ultrastructural and morphometric study. Anat Embryol 182:1–10
Vieira VLA, Johnston IA (1992) Influence of temperature on muscle-fibre development in larvae of the herring Clupea harengus. Mar Biol 112:333–341
Wanson JC, Drochman P (1968) Epoxi technique inclusion for electron microscopy. Cell Biol 38:130
Waterman RE (1969) Developmental of the lateral musculature in the teleost, Brachydanio rerio: a fine structural study. Am J Anat 125:457–494
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Ayala, M.D., Martínez, J.M., Hernández-Urcera, J. et al. Effect of the early temperature on the growth of larvae and postlarvae turbot, Scophthalmus maximus L.: muscle structural and ultrastructural study. Fish Physiol Biochem 42, 1027–1042 (2016). https://doi.org/10.1007/s10695-015-0194-y
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DOI: https://doi.org/10.1007/s10695-015-0194-y