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Effects of the embryonic thermal environment on haddock (Melanogrammus aeglefinus) developmental trajectories through exogenous feeding stages

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Abstract

Detailed development of haddock (Melanogrammus aeglefinus) embryos and larvae was studied in several embryonic thermal rearing environments. Using defined reference points (landmarks), development of various tissues including muscle was mapped throughout early ontogeny. The onset of most landmarks was unaffected by temperature as a proportion of time to the initiation of exogenous feeding (standardized developmental time). However, blastopore closure, notochord vacuolation, retinal pigmentation, the appearance of blood cells, and hatching occurred later in development at lower temperatures. Appearance of the optic lumen, neural tube cavitation, and increased myofibril density per deep cell occurred earlier at lower temperatures. Changes in relative order and temporal sequence of developmental events were observed among temperature groups. Notochord (from 30 to 7% of developmental time) and eye development (from 45 to 33% developmental time) was accelerated with increased embryonic temperature, while myofibrillargenesis (from 60 to 88% developmental time) and neural tube development was similarly slowed (71–85% developmental time). The rate of gut development continued to be greater in larvae from higher incubation temperature groups beyond hatch in spite of the absence of temperature variation. Incubation temperature was found to have had a differential but significant effect on the development of various tissues and structures that affected the form and, possibly, function of exogenous feeding haddock.

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References

  • Adriaens D, Verraes W (2002) An empirical approach to study the relation between ontogeny, size and age using geometric morphologies. In: Aerts P, D’Août K, Herrel A, Van Damme R (eds) Topics in functional and ecological vertebrate morphology. Shaker Publishing, Maastricht, pp 293–324

    Google Scholar 

  • Aiken DE (ed) (2003) Early rearing of haddock: state of the art. Aqua Assoc Can, Spec Pub 7: 136p

  • Atchley WR, Xu S, Cowley DE (1997) Altering developmental trajectories in mice by restricted index selection. Genetics 146:629–640

    CAS  PubMed  PubMed Central  Google Scholar 

  • Atchley WR, Wei R, Crenshaw P (2000) Cellular consequences in the brain and liver of age-specific selection for rate of development in mice. Genetics 155:1347–1357

    CAS  PubMed  PubMed Central  Google Scholar 

  • Balon EK (1999) Alternative ways how to become a definitive phenotype or a juvenile (and on some persisting linguistic offences). Environ Biol Fish 56:17–38

    Article  Google Scholar 

  • Blaxter JHS (1992) The effect of temperature on larval fishes. Neth J Zool 42:336–357

    Article  Google Scholar 

  • Devoto SH, Melancon E, Eisen JS, Westerfield M (1996) Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 22:3371–3380

    Google Scholar 

  • Fauconneau B, Paboeuf G (2001) Muscle satellite cells in fish. In: Johnston IA (ed) Fish physiology, vol 18. Muscle development and growth. Academic, London, pp 73–101

    Google Scholar 

  • Fijan N (2002) Morphogenesis of blood cell lineages in channel catfish. J Fish Biol 60:999–1014

    Article  Google Scholar 

  • Fuiman LA, Poling KR, Higgs DM (1998) Quantifying developmental progress for comparative studies of larval fishes. Copeia 1998:602–611

    Article  Google Scholar 

  • Galloway TF, Kjørsvik E, Kryvi H (1998) Effect of temperature on viability and axial muscle development in embryos and yolk sac larvae of the Northeast Arctic cod (Gadus morhua). Mar Biol 132:559–567

    Article  Google Scholar 

  • Galloway TF, Kjørsvik E, Kryvi H (1999) Muscle growth and development in Atlantic cod larvae (Gadus morhua L.) related to different somatic growth rates. J Exp Biol 202:2111–2120

    CAS  PubMed  Google Scholar 

  • Gibson S, Johnston IA (1995) Temperature and development in larvae of the turbot Scophthalmus maximus. Mar Biol 124:17–25

    Article  Google Scholar 

  • Hall TE, Johnston IA (2003) Temperature and developmental plasticity during embryogenesis in the Atlantic cod Gadus morhua L. Mar Biol 142:833–840

    Article  Google Scholar 

  • Hall BK, Olsen WM (eds) (2003) Keywords and concepts in evolutionary developmental biology. Harvard University Press, Cambridge

  • Hall TE, Smith P, Johnston IA (2004) Stages of embryonic development in the Atlantic cod Gadus morhua. J Morphol 259:255–270

    Article  Google Scholar 

  • Hamlin HJ, Hunt von Herbing I, Kling LJ (2000) Histological and morphological evaluations of the digestive tract and associated organs of haddock throughout post-hatching ontogeny. J Fish Biol 57:716–732

    Article  Google Scholar 

  • Hazel JR, Prosser CL (1974) Molecular mechanisms of temperature compensation in poikilotherms. Physiol Rev 54:620–677

    Article  CAS  Google Scholar 

  • Hill J, Johnston IA (1997) Photomicrographic atlas of herring development. J Fish Biol 51:960–977

    Article  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, Toronto

    Google Scholar 

  • Hunt von Herbing I (2001) Development of feeding structures in larval fish with different life histories: winter flounder and Atlantic cod. J Fish Biol 59:767–782

    Article  Google Scholar 

  • Hunt von Herbing I, Boutilier RG, Miyake T, Hall BK (1996) Effects of temperature on morphological landmarks critical to growth and survival in larval Atlantic cod (Gadus morhua). Mar Biol 124:593–606

    Article  Google Scholar 

  • Jobling M (1994) Fish bioenergetics. Chapman and Hall, Toronto

    Google Scholar 

  • Jobling M (1997) Temperature and growth: modulation of growth rate via temperature change. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 225–253

    Chapter  Google Scholar 

  • Johnston IA (1993) Temperature influences muscle differentiation and the relative timing of organogenesis in herring (Clupea harengus) larvae. Mar Biol 116:363–379

    Article  Google Scholar 

  • Johnston IA (1999) Muscle development and growth: potential implications for flesh quality in fish. Aquaculture 177:99–115

    Article  Google Scholar 

  • Johnston IA (2001) Genetic and environmental determinants of muscle growth patterns. In: Johnston IA (ed) Fish physiology, vol 18. Muscle development and growth. Academic, London, pp 141–184

    Google Scholar 

  • Johnston IA, Vieira VLA, Hill J (1996) Temperature and ontogeny in ectotherms: muscle phenotype in fish. In: Johnston IA, Bennett AF (eds) Phenotypic and evolutionary adaptations of organisms to temperature. Society for experimental biology seminar series. Cambridge University Press, Cambridge, pp 153–181

  • 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

    CAS  PubMed  Google Scholar 

  • Johnston IA, Vieira VLA, Temple GK (2001) Functional consequences and population differences in the developmental plasticity of muscle to temperature in Atlantic herring Clupea harengus. Mar Ecol Prog Ser 213:285–300

    Article  Google Scholar 

  • Kamler E (1992) Early life history of fish: an energetics approach. Chapman and Hall, London

    Book  Google Scholar 

  • Kennedy CJ, Walsh PJ (1997) Effects of temperature on xenobiotic metabolism. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 303–324

    Chapter  Google Scholar 

  • Killeen JR, McLay HA, Johnston IA (1999) Temperature and neuromuscular development in embryos of the trout (Salmo trutta L.)

  • Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310

    Article  CAS  Google Scholar 

  • Koumoundouros G, Divanach P, Kentouri M (1999) Ontogeny and allometric plasticity of Dentex dentex (Osteichthyes: Sparidae) in rearing conditions. Mar Biol 135:561–572

    Article  Google Scholar 

  • Kovác V (2002) Synchrony and heterochrony in ontogeny (of fish). J Theor Biol 217:499–507

    Article  Google Scholar 

  • Lancioni H, Lucentini L, Panara F (2005) Ontogentic changes of circulating erythroid cells and haemoglobin components in Esox lucius. J Fish Biol 66:1576–1588

    Article  CAS  Google Scholar 

  • Lindsey CC, Arnason AN (1981) A model for responses of vertebral numbers in fish to environmental influences during development. Can J Fish Aquat Sci 38:334–347

    Article  Google Scholar 

  • Mabee PM, Olmstead KL, Cubbage CC (2000) An experimental study of intraspecific variation, developmental timing, and heterochrony in fishes. Evolution 54:2091–2106

    Article  CAS  Google Scholar 

  • Martell DJ (2005) Temperature-affected phenotypic plasticity in haddock (Melanogrammus aegelfinus L.) development. PhD Thesis, University of New Brunswick

  • Martell DJ, Kieffer JD, Trippel EA (2005) Effects of temperature during early life history on embryonic and larval development and growth in haddock, Melanogrammus aeglefinus. J Fish Biol 66:1558–1575. DOI 10.1111/j.1095-8649.2005.00699.x

    Article  Google Scholar 

  • Martin JH, Lynn JA, Nickey WM (1966) A rapid polychrome stain for epoxy-embedded tissue. Am J Clin Path 46:250–251

    Article  CAS  Google Scholar 

  • Martinez GM, Bolker JA (2003) Embryonic and larval staging of summer flounder (Paralichthys dentatus). J Morphol 255:162–176

    Article  Google Scholar 

  • Morrison CM (1993) Histology of the Atlantic cod: an atlas. Part IV. Eleutheroembryo and larva. Can Spec Publ Fish Aquat Sci 119:1–496

    Google Scholar 

  • Morrison CM, Miyake T, Wright JR Jr (2001) Histological study of the development of the embryo and early larva of Oreochromis niloticus (Pisces: Cichlidae). J Morphol 247:172–195

    Article  CAS  Google Scholar 

  • Ojanguren AF, Braña F (2003) Thermal dependence of embryonic growth and development in brown trout. J Fish Biol 62:580–590

    Article  Google Scholar 

  • Pavlov DA (1984) Effect of temperature during early ontogeny of Atlantic salmon, Salmo salar. 1 Variability of morphological characters and duration of development of Atlantic salmon under different temperatures. J Ichthyol 24:30–38

    Google Scholar 

  • Presnell JK, Schreibman MP (1997) Humason’s animal tissue techniques, 5 edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Radmilovich M, Fernández A, Trujillo-Cenóz O (2003) Environmental temperature affects cell proliferation in the spinal cord and brain of juvenile turtles. J Exp Biol 206:3085–3093

    Article  Google Scholar 

  • Rideout RM, Trippel EA, Litvak MK (2004) Paternal effects on haddock early life history traits. J Fish Biol 64:695–701. DOI 10.1046/j.1095-8649.2003.00335.x

    Article  Google Scholar 

  • Rombough PJ (1997) The effects of temperature on embryonic and larval development. In: Wood CM, McDonald DG (eds) Global warming: implications for freshwater and marine fish. Cambridge University Press, Cambridge, pp 177–223

    Chapter  Google Scholar 

  • Sänger AM, Stoiber W (2001) Muscle fibre diversity and plasticity. In: Johnston IA (ed) Fish physiology, vol 18. Muscle development and growth. Academic, London, pp 187–250

  • Scott WB, Scott MG (1988) Atlantic fishes of Canada. Can Bull Fish Aquat Sci 219:731 p

    Google Scholar 

  • Spicer JI, Burggren WW (2003) Development of physiological regulatory system: altering the timing of crucial events. Zool 106:1–9

    Article  Google Scholar 

  • Spurlock BO, Skinner MS, Kattine AA (1966) A simple rapid method for staining epoxy-embedded specimens for light microscopy with the polychromatic stain, Paragon-1301. Am J Clin Path 46:252–258

    Article  CAS  Google Scholar 

  • Trippel EA (1998) Egg size and viability and seasonal offspring production of young Atlantic cod. Trans Am Fish Soc 127:339–359

    Article  Google Scholar 

  • Veggetti A, Rowlerson A, Radaelli S, Arrighi S, Domeneghini C (1999) Post-hatching development of the gut and lateral muscle in the sole. J Fish Biol 55A:44–65

    Article  Google Scholar 

  • Zapata A, Diez B, Cejalvo T, Gutiérrez-de Frías C, Cortés A (2005) Ontogeny of the immune system of fish. Fish Shellfish Immun (in press)

  • Zar JH (1999) Biostatistical analysis. Prentice-Hall Canada Inc, Toronto

    Google Scholar 

Download references

Acknowledgements

The authors acknowledge the financial and logistical support provided to D.J.M. and E.A.T. by Fisheries and Oceans Canada (St. Andrews Biological Station, St. Andrews, NB). Also J.D.K. thanks the Natural Sciences and Engineering Research Council for funding and the MADSAM fish group for continued support. We also wish to thank Drs. J. Castell and D. MacLatchy for invaluable advice and guidance on the research, E. Heikkila for her support and skilful editorial guidance, and two anonymous reviewers for helpful comments on the manuscript. All experimental protocols followed CCAC guidelines for the care and use of experimental animals.

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Correspondence to D. J. Martell.

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Communicated by R.J. Thompson, St. John's

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Martell, D., Kieffer, J. & Trippel, E. Effects of the embryonic thermal environment on haddock (Melanogrammus aeglefinus) developmental trajectories through exogenous feeding stages. Marine Biology 149, 177–187 (2006). https://doi.org/10.1007/s00227-005-0190-3

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