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Swimming Effects on Developing Zebrafish

  • Sander Kranenbarg
  • Bernd Pelster
Chapter

Abstract

Zebrafish represent an important vertebrate model species in developmental biology. This chapter reviews the effects of exercise on the development of the musculoskeletal system, the cardiovascular system, metabolic capacities of developing zebrafish, and regulation of these processes on the gene expression level. Zebrafish larvae display a high amount of developmental plasticity, enabling an adaptive response to training. This adaptive response is apparent in both the morphology and physiology of the musculoskeletal system. Given the multitude of (molecular) tools available for the zebrafish, this species promises to be very useful in further elucidating the mechanisms of muscle, skeletal, and cardiovascular adaptations to prolonged exercise.

Keywords

Zebrafish Embryo Adult Zebrafish Zebrafish Larva Swimming Exercise Vertebral Centra 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors thank Stephen Devoto, David Parichy, and Paula Mabee for making their original high quality artwork available for reproduction in this chapter.

References

  1. Alexander RM (1969) The orientation of muscle fibres in the myomeres of fishes. J Mar Biol Assoc UK 49:263–290CrossRefGoogle Scholar
  2. Ameln H, Gustafsson T, Sundberg CJ, Okamoto K, Jansson E, Poellinger L, Makino Y (2005) Physiological activation of hypoxia inducible factor-1 in human skeletal muscle. FASEB J 19(8):1009–1011PubMedGoogle Scholar
  3. Augustine S, Gagnaire B, Floriani M, Adam-Guillermin C, Kooijman SALM (2011) Developmental energetics of zebrafish, Danio rerio. Comp Biochem Physiol A Mol Integr Physiol 159(3):275–283PubMedCrossRefGoogle Scholar
  4. Avaron F, Hoffman L, Guay D, Akimenko MA (2006) Characterization of two new zebrafish members of the hedgehog family: a typical expression of a zebrafish indian hedgehog gene in skeletal elements of both endochondral and dermal origins. Dev Dyn 235(2):478–489PubMedCrossRefGoogle Scholar
  5. Backiel T, Kokurewicz B, Ogorzalek A (1984) High incidence of skeletal anomalies in carp, Cyprinus carpio, reared in cages in flowing water. Aquaculture 43:369–380CrossRefGoogle Scholar
  6. Bagatto B, Pelster B, Burggren WW (2001) Growth and metabolism of larval zebrafish: effects of swim training. J Exp Biol 204(24):4335–4343PubMedGoogle Scholar
  7. Bainbridge R (1958) The speed of swimming of fish as related to size and to the frequency and amplitude of the tail beat. J Exp Biol 35:109–133Google Scholar
  8. Bartman T, Walsh E, Wen KK, McKane M, Ren J, Alexander J, Rubenstein P, Stainier D (2004) Early myocardial function affects endocardial cushion development in zebrafish. PLoS Biol 2(5):e129PubMedCrossRefGoogle Scholar
  9. Beamish FWH (1978) Swimming capacity. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 7. Academic Press, New York, chap 2, pp 101–187Google Scholar
  10. Bird NC, Mabee PM (2003) Developmental morphology of the axial skeleton of the zebrafish, Danio rerio (ostariophysi: cyprinidae). Dev Dyn 228(3):337–357PubMedCrossRefGoogle Scholar
  11. Bonewald LF, Johnson ML (2008) Osteocytes, mechanosensing and wnt signaling. Bone 42(4):606–615PubMedCrossRefGoogle Scholar
  12. Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Res Board Can 21:1183–1226CrossRefGoogle Scholar
  13. Brustein E, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Drapeau P (2003) Steps during the development of the zebrafish locomotor network. J Physiol Paris 97(1):77–86PubMedCrossRefGoogle Scholar
  14. Bryson-Richardson RJ, Currie PD (2008) The genetics of vertebrate myogenesis. Nat Rev Genet 9(8):632–646PubMedCrossRefGoogle Scholar
  15. Burggren WW, Territo PR (1995) Early development of blood oxygen transport. In: Sutton J, Houston C, Coats G (eds) Hypoxia and the Brain, Queen City Printers, Burlington, pp 85–89Google Scholar
  16. Buss RR, Drapeau P (2001) Synaptic drive to motoneurons during fictive swimming in the developing zebrafish. J Neurophysiol 86(1):197–210PubMedGoogle Scholar
  17. Chandrasekhar A, Moens CB, Warren JT, Kimmel CB, Kuwada JY (1997) Development of branchiomotor neurons in zebrafish. Development 124(13):2633–2644PubMedGoogle Scholar
  18. Cloutier R, Caron A, Grünbaum T, François NRL (2010) Effect of water velocity on the timing of skeletogenesis in the arctic charr, Salvelinus alpinus (salmoniformes: teleostei): an empirical case of developmental plasticity. Int J Zool 2010:1–15CrossRefGoogle Scholar
  19. Colwill RM, Creton R (2011) Locomotor behaviors in zebrafish (Danio rerio) larvae. Behav Process 86(2):222–229CrossRefGoogle Scholar
  20. Cubbage C, Mabee P (1996) Development of the cranium and paired fins in the zebrafish Danio rerio (ostariophysi, cyprinidae). J Morphol 229(2):121–160Google Scholar
  21. Dahm R, Geisler R (2006) Learning from small fry: the zebrafish as a genetic model organism for aquaculture fish species. Mar Biotechnol 8(4):329–345PubMedCrossRefGoogle Scholar
  22. Danos N, Staab K (2010) Can mechanical forces be responsible for novel bone development and evolution in fishes. J Appl Ichthyol 26(2):156–161CrossRefGoogle Scholar
  23. Davison W (1997) The effects of exercise training on teleost fish, a review of recent literature. Comp Biochem Physiol A Mol Integr Physiol 117(1):67–75Google Scholar
  24. Devoto S, Melançon E, Eisen J, Westerfield M (1996) Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122(11):3371–3380PubMedGoogle Scholar
  25. Drapeau P, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Brustein E (2002) Development of the locomotor network in zebrafish. Prog Neurobiol 68(2):85–111PubMedCrossRefGoogle Scholar
  26. 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 238:239–246PubMedCrossRefGoogle Scholar
  27. Egg M, Tischler A, Schwerte T, Sandbichler A, Folterbauer C, Pelster B (2012) Endurance exercise modifies the circadian clock in zebrafish (Danio rerio) temperature independently. Acta Physiol 205:167–176CrossRefGoogle Scholar
  28. Egginton S (2009) Invited review: activity-induced angiogenesis. Pflüg Arch 457(5):963–977CrossRefGoogle Scholar
  29. Engeszer RE, Patterson LB, Rao AA, Parichy DM (2007) Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 4(1):21–40PubMedCrossRefGoogle Scholar
  30. Fiaz A, van Leeuwen J, Kranenbarg S (2010) Phenotypic plasticity and mechano-transduction in the teleost skeleton. J Appl Ichthyol 26(2):289–293CrossRefGoogle Scholar
  31. Fiaz A, Léon-Kloosterziel KM, Gort G, Schulte-Merker S, van Leeuwen JL, Kranenbarg S (2012) Swim-training differentially affects the timing of chondrogenesis and osteogenesis in zebrafish larva (Danio rerio). PLoS ONE 7(4):e34072PubMedCrossRefGoogle Scholar
  32. Fischer-Rousseau L, Cloutier R, Zelditch M (2009) Morphological integration and developmental progress during fish ontogeny in two contrasting habitats. Evol Dev 11(6):740–753PubMedCrossRefGoogle Scholar
  33. Fleming A, Keynes R, Tannahill D (2004) A central role for the notochord in vertebral patterning. Development 131(4):873–880PubMedCrossRefGoogle Scholar
  34. Fuiman L, Webb P (1988) Ontogeny of routine swimming activity and performance in zebra danios (teleostei: cyprinidae). Anim Behav 36(1):250–261CrossRefGoogle Scholar
  35. Gallaugher P, Thorarensen H, Kiessling A, Farrell A (2001) Effects of high intensity exercise training on cardiovascular function, oxygen uptake, internal oxygen transport and osmotic balance in chinook salmon (Oncorhynchus tshawytscha) during critical speed swimming. J Exp Biol 204(16):2861–2872PubMedGoogle Scholar
  36. Gomez C, David V, Peet NM, Vico L, Chenu C, Malaval L, Skerry TM (2007) Absence of mechanical loading in utero influences bone mass and architecture but not innervation in myoD-myf5-deficient mice. J Anat 210(3):259–271PubMedCrossRefGoogle Scholar
  37. Granato M, van Eeden FJ, Schach U, Trowe T, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Nüsslein-Volhard C (1996) Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 123:399–413PubMedGoogle Scholar
  38. Grande T, Young B (2004) The ontogeny and homology of the weberian apparatus in the zebrafish Danio rerio (ostariophysi: cypriniformes). Zool J Linn Soc 140(2):241–254CrossRefGoogle Scholar
  39. Grotmol S, Kryvi H, Keynes R, Krossøy C, Nordvik K, Totland GK (2006) Stepwise enforcement of the notochord and its intersection with the myoseptum: an evolutionary path leading to development of the vertebra. J Anat 209(3):339–357PubMedCrossRefGoogle Scholar
  40. Gustafsson T, Puntschart A, Kaijser L, Jansson E, Sundberg CJ (1999) Exercise-induced expression of angiogenesis-related transcription and growth factors in human skeletal muscle. Am J Physiol 276:H679–H685PubMedGoogle Scholar
  41. Hamilton MT, Booth FW (2000) Skeletal muscle adaptation to exercise: a century of progress. J Appl Physiol 88(1):327–331PubMedGoogle Scholar
  42. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, OxfordGoogle Scholar
  43. 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(2):207–219PubMedCrossRefGoogle Scholar
  44. Hoppeler H, Howald H, Conley K (1985) Endurance training in humans: aerobic capacity and structure of skeletal muscle. J Appl Physiol 59(2):320–327PubMedGoogle Scholar
  45. Hove J, Köster R, Forouhar A, Acevedo-Bolton G, Fraser S, Gharib M (2003) Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421(6919):172–177PubMedCrossRefGoogle Scholar
  46. Johnston I, Bower N, Macqueen D (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214(10):1617–1628PubMedCrossRefGoogle Scholar
  47. Jonz MG, Nurse CA (2005) Development of oxygen sensing in the gills of zebrafish. J Exp Biol 208(8):1537–1549PubMedCrossRefGoogle Scholar
  48. Kihara M, Ogata S, Kawano N, Kubota I, Yamaguchi R (2002) Lordosis induction in juvenile red sea bream, Pagrus major, by high swimming activity. Aquaculture 212:149–148CrossRefGoogle Scholar
  49. Kimmel CB, Patterson J, Kimmel RO (1974) The development and behavioral characteristics of the startle response in the zebrafish. Dev Psychobiol 7(1):47–60PubMedCrossRefGoogle Scholar
  50. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203(3):253–310PubMedCrossRefGoogle Scholar
  51. Kopp R, Köblitz L, Egg M, Pelster B (2011) HIF signaling and overall gene expression changes during hypoxia and prolonged exercise differ considerably. Physiol Genomics 43(9):506–516PubMedCrossRefGoogle Scholar
  52. Kranenbarg S, van Cleynenbreugel T, Schipper H, van Leeuwen J (2005a) Adaptive bone formation in acellular vertebrae of sea bass (Dicentrarchus labrax L.). J Exp Biol 208:3493–3502PubMedCrossRefGoogle Scholar
  53. Kranenbarg S, Waarsing JH, Muller M, Weinans H, van Leeuwen JL (2005b) Lordotic vertebrae in sea bass (Dicentrarchus labrax L.) are adapted to increased loads. J Biomech 38(6):1239–1246PubMedCrossRefGoogle Scholar
  54. Lamb KJ, Lewthwaite JC, Lin JP, Simon D, Kavanagh E, Wheeler-Jones CPD, Pitsillides AA (2003) Diverse range of fixed positional deformities and bone growth restraint provoked by flaccid paralysis in embryonic chicks. Int J Exp Pathol 84(4):191–199PubMedCrossRefGoogle Scholar
  55. Lauschke J, Maisch B (2009) Athlete’s heart or hypertrophic cardiomyopathy? Clin Res Cardiol 98(2):80–88PubMedCrossRefGoogle Scholar
  56. van Leeuwen J, van der Meulen T, Schipper H, Kranenbarg S (2008) A functional analysis of myotomal muscle-fibre reorientation in developing zebrafish Danio rerio. J Exp Biol 211(8):1289–1304PubMedCrossRefGoogle Scholar
  57. LeMoine CMR, Craig PM, Dhekney K, Kim JJ, McClelland GB (2010) Temporal and spatial patterns of gene expression in skeletal muscles in response to swim training in adult zebrafish (Danio rerio). J Comp Physiol [B] 180(1):151–160CrossRefGoogle Scholar
  58. Mabee PM, Trendler TA (1996) Development of the cranium and paired fins in Betta splendens (teleostei: percomorpha): intraspecific variation and interspecific comparisons. J Morphol 227:249–287CrossRefGoogle Scholar
  59. Mably JD, Childs SJ (2010) Developmental physiology of the zebrafish cardiovascular system. In: Perry SF, Ekker M, Farrell AP, Brauner CJ (eds) Zebrafish, fish physiology, vol 29. Academic Press, chap 6, pp 249–287Google Scholar
  60. 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(9):2442–2448PubMedCrossRefGoogle Scholar
  61. Mauro A (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9:493–495PubMedCrossRefGoogle Scholar
  62. McClelland GB, Craig PM, Dhekney K, Dipardo S (2006) Temperature- and exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J Physiol London 577(Pt 2):739–751Google Scholar
  63. Montgomery J, Baker C, Carton A (1997) The lateral line can mediate rheotaxis in fish. Nature 389(6654):960–963CrossRefGoogle Scholar
  64. Mook D (1977) Larval and osteological development of the sheepshead, Archosargus probatocephalus (pisces: sparidae). Copeia 1:126–133CrossRefGoogle Scholar
  65. Morris S, Gaudin A (1982) Osteocranial development in the viviparous surfperch Amphistichus argenteus (pisces: embiotocidae). J Morphol 174(1):95–120CrossRefGoogle Scholar
  66. Müller UK, van Leeuwen JL (2004) Swimming of larval zebrafish: ontogeny of body waves and implications for locomotory development. J Exp Biol 207:853–868PubMedCrossRefGoogle Scholar
  67. Nowlan NC, Murphy P, Prendergast PJ (2007) Mechanobiology of embryonic limb development. Ann N Y Acad Sci 1101:389–411PubMedCrossRefGoogle Scholar
  68. Nowlan NC, Prendergast PJ, Murphy P (2008) Identification of mechanosensitive genes during embryonic bone formation. PLoS Comput Biol 4(12):e1000250PubMedCrossRefGoogle Scholar
  69. Osse J, van den Boogaart J (1999) Dynamic morphology of fish larvae, structural implications of friction forces in swimming, feeding and ventilation. J Fish Biol 55(suppl A):156–174Google Scholar
  70. Osse J, van den Boogaart J, van Snik G, van der Sluys L (1997) Priorities during early growth of fish larvae. Aquaculture 155:249–258CrossRefGoogle Scholar
  71. Palstra AP, Tudorache C, Rovira M, Brittijn SA, Burgerhout E, van den Thillart GEEJM, Spaink HP, Planas JV (2010) Establishing zebrafish as a novel exercise model: swimming economy, swimming-enhanced growth and muscle growth marker gene expression. PLoS ONE 5(12):e14483Google Scholar
  72. Parichy DM, Elizondo MR, Mills MG, Gordon TN, Engeszer RE (2009) Normal table of postembryonic zebrafish development: staging by externally visible anatomy of the living fish. Dev Dyn 238(12):2975–3015PubMedCrossRefGoogle Scholar
  73. Pelster B (2008) Fish larval physiology. Science Publishers, Enfield, USA, chap Gas exchange, pp 91–118Google Scholar
  74. Pelster B, Bagatto B (2010) Respiration. In: Perry SF, Ekker M, Farrell AP, Brauner CJ (eds) Zebrafish, fish physiology series, vol 29. Elsevier, Amsterdam, Chap 7, pp 290–309Google Scholar
  75. Pelster B, Sänger A, Siegele M, Schwerte T (2003) Influence of swim training on cardiac activity, tissue capillarization, and mitochondrial density in muscle tissue of zebrafish larvae. Am J Physiol 285(2):R339–R347Google Scholar
  76. Pette D, Staron R (2001) Transitions of muscle fiber phenotypic profiles. Histochem Cell Biol 115(5):359–372PubMedGoogle Scholar
  77. Pitsillides AA (2006) Early effects of embryonic movement: ‘a shot out of the dark’. J Anat 208(4):417–431PubMedCrossRefGoogle Scholar
  78. Plaut I (2000) Effects of fin size on swimming performance, swimming behaviour and routine activity of zebrafish Danio rerio. J Exp Biol 203(4):813–820PubMedGoogle Scholar
  79. Prior B, Yang H, Terjung R (2004) What makes vessels grow with exercise training. J Appl Physiol 97(3):1119–1128PubMedCrossRefGoogle Scholar
  80. van Raamsdonk W, van der Stelt A, Diegenbach PC, van de Berg W, de Bruyn H, van Dijk J, Mijzen P (1974) Differentiation of the musculature of the teleost Brachydanio rerio. i. myotome shape and movements in the embryo. Z Anat Entwicklungsgesch 145:321–342CrossRefGoogle Scholar
  81. van Raamsdonk W, Pool CW, Mijzen P, Mos W, van der Stelt A (1977) On the relation between movements and the shape of somites in early embryos of the teleost Brachydanio rerio. Contrib Zool 46:261–274Google Scholar
  82. van Raamsdonk W, Pool CW, te Kronnie G (1978) Differentiation of muscle fiber types in the teleost Brachydanio rerio. Anat Embryol (Berl) 153(2):137–155CrossRefGoogle Scholar
  83. van Raamsdonk W, Mos W, te Kronnie G, Pool CW, Mijzen P (1979) Differentiation of the musculature of the teleost Brachydanio rerio. ii. effects of immobilization on the shape and structure of somites. Acta Morphol Neerl Scand 17:259–273PubMedGoogle Scholar
  84. Rodríguez J, Garcia-Alix A, Palacios J, Paniagua R (1988) Changes in the long bones due to fetal immobility caused by neuromuscular disease. a radiographic and histological study. J Bone Joint Surg 70(7):1052–1060PubMedGoogle Scholar
  85. Rombough P (2002) Gills are needed for ionoregulation before they are needed for O2 uptake in developing zebrafish, Danio rerio. J Exp Biol 205(12):1787–1794Google Scholar
  86. Rombough P, Drader H (2009) Hemoglobin enhances oxygen uptake in larval zebrafish (Danio rerio) but only under conditions of extreme hypoxia. J Exp Biol 212(6):778–784PubMedCrossRefGoogle Scholar
  87. Saint-Amant L, Drapeau P (1998) Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol 37(4):622–632Google Scholar
  88. Scarpulla RC (2008) Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann N Y Acad Sci 1147:321–334PubMedCrossRefGoogle Scholar
  89. Schilling TF (2002) The morphology of larval and adult zebrafish. In: Nüsslein-Volhard C, Dahm R (eds) Zebrafish, no. 261 in the practical approach series, Oxford University Press, Oxford, Chap 3, pp 59–94Google Scholar
  90. Schilling TF, Kimmel CB (1997) Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development 124(15):2945–2960PubMedGoogle Scholar
  91. Schwerte T (2009) Cardio-respiratory control during early development in the model animal zebrafish. Acta Histochem 111(3):230–243PubMedCrossRefGoogle Scholar
  92. Spoorendonk K, Hammond C, Huitema L, Vanoevelen J, Schulte-Merker S (2010) Zebrafish as a unique model system in bone research: the power of genetics and in vivo imaging. J Appl Ichthyol 26(2):219–224CrossRefGoogle Scholar
  93. 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):3233–3239PubMedCrossRefGoogle Scholar
  94. Stellabotte F, Devoto SH (2007) The teleost dermomyotome. Dev Dyn 236(9):2432–2443PubMedCrossRefGoogle Scholar
  95. Stellabotte F, Dobbs-McAuliffe B, Fernández DA, Feng X, Devoto SH (2007) Dynamic somite cell rearrangements lead to distinct waves of myotome growth. Development 134(7):1253–1257PubMedCrossRefGoogle Scholar
  96. Stemple DL (2005) Structure and function of the notochord: an essential organ for chordate development. Development 132(11):2503–2512PubMedCrossRefGoogle Scholar
  97. te Kronnie G, Reggiani C (2002) Skeletal muscle fibre type specification during embryonic development. J Muscle Res Cell Motil 23(1):65–69PubMedCrossRefGoogle Scholar
  98. Thirumalai V, Cline HT (2008) Endogenous dopamine suppresses initiation of swimming in prefeeding zebrafish larvae. J Neurophysiol 100(3):1635–1648PubMedCrossRefGoogle Scholar
  99. Timmons JA, Larsson O, Jansson E, Fischer H, Gustafsson T, Greenhaff PL, Ridden J, Rachman J, Peyrard-Janvid M, Wahlestedt C, Sundberg CJ (2005) Human muscle gene expression responses to endurance training provide a novel perspective on duchenne muscular dystrophy. FASEB J 19(7):750–760PubMedCrossRefGoogle Scholar
  100. van der Meulen T (2005) Epigenetics of the locomotory system in zebrafish. PhD thesis, Wageningen UniversityGoogle Scholar
  101. van der Meulen T, Schipper H, van Leeuwen J, Kranenbarg S (2005) Effects of decreased muscle activity on developing axial musculature in nic b107mutant zebrafish (Danio rerio). J Exp Biol 208(19):3675–3687PubMedCrossRefGoogle Scholar
  102. van der Meulen T, Schipper H, van den Boogaart J, Huising M, Kranenbarg S, van Leeuwen J (2006) Endurance exercise differentially stimulates heart and axial muscle development in zebrafish (Danio rerio). Am J Physiol 291(4):R1040–R1048CrossRefGoogle Scholar
  103. van der Stelt A (1968) Spiermechanica en myotoombouw bij vissen. PhD thesis, University of AmsterdamGoogle Scholar
  104. Verraes W (1975) Some functional aspects of ossifications in the cartilaginous ceratohyale during postembryonic development in Salmo gairdneri Richardson, 1836 (teleostei: salmonidae). Form Funct 8:27–32Google Scholar
  105. Weisel G (1967) Early ossification in the skeleton of the sucker (Catostomus macrocheilus) and the guppy (Poecilia reticulata). J Morphol 121(1):1–18PubMedCrossRefGoogle Scholar
  106. Westerfield M (2007) The zebrafish book—a guide for the laboratory use of zebrafish (Danio rerio), 5th edn. University of Oregon press, Eugene, Chap 2, Breeding, p 2.2Google Scholar
  107. Wieser W (1995) Energetics of fish larvae, the smallest vertebrates. Acta Physiol Scand 154(3):279–290PubMedCrossRefGoogle Scholar
  108. Witten PE, Huysseune A (2009) A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol Rev 84(2):315–346PubMedCrossRefGoogle Scholar
  109. Witten PE, Gil-Martens L, Hall BK, Huysseune A, Obach A (2005) Compressed vertebrae in atlantic salmon Salmo salar: evidence for metaplastic chondrogenesis as a skeletogenic response late in ontogeny. Dis Aquat Org 64(3):237–246PubMedCrossRefGoogle Scholar
  110. Wolff J (1892) Das Gesetz der Transformation der Knochen. No.4 in Reprints medizinhistorischer Schriften, Hirschwald, BerlinGoogle Scholar

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Authors and Affiliations

  1. 1.Experimental Zoology GroupWageningen UniversityWageningenThe Netherlands
  2. 2. Institut für ZoologieUniversität InnsbruckInnsbruckAustria

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