Skip to main content
SpringerLink
Log in

Changes in yolk total proteins and lipid components and embryonic growth rates during lobster (Homarus americanus) egg development under a simulated seasonal temperature cycle

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

From August 2000 to June 2001, seven egg-carrying female lobster (Homarus americanus) from the Îles de la Madeleine population (Gulf of St. Lawrence, Canada) were held under a simulated seasonal temperature cycle to monitor egg development from extrusion to hatching. For the first time, changes in the yolk components (total lipids and major lipid classes, total proteins) and embryo growth of single eggs were monitored separately over the entire development period. Under the controlled temperature conditions, egg development proceeded in three phases. (1) Autumn, from extrusion to early December, was marked by a rapid increase in the Perkins’s eye index and rapid declines in yolk total proteins and triacylglycerols (TAG). Embryo daily growth rate was estimated between 1 and 2 µg proteins day−1. (2) Winter, from late December to early April (temperature stable at ca. 1°C) was characterized by a stationary phase in the evolution of the eye index and yolk lipid use, and embryo growth slowed significantly. (3) Spring, from late April to hatching in June was the period with the most rapid changes in yolk TAG and embryo growth rates >6 µg proteins day−1 were recorded. Almost 65% of the live biomass (total proteins) of the hatching larvae was accumulated during the last few weeks of development. An index of embryo growth efficiency was estimated as the slope of the relationship between embryo total proteins and yolk TAG during egg development. A relationship was found between the initial mean egg dry weight and the embryo growth efficiency index suggesting that under the same experimental conditions bigger eggs used yolk lipids more efficiently and sustained faster embryonic growth than smaller eggs. The relationship may also explain why larger larvae originate from larger eggs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aiken DE, Waddy SL (1980) Reproductive Biology. In: Cobb JS, Phillips BF (eds) The biology and management of lobsters, vol 1 Physiology and behavior. Academic Press, New York, pp 215–276

  • Aiken DE, Waddy SL (1982) Cement gland development, ovary maturation, and reproductive cycles in the American lobster Homarus americanus. J Crustacean Biol 2:315–327

    Google Scholar 

  • Attard J (1985) Fécondité individuelle et production d’oeufs par recrue du homard (Homarus americanus) sur les côtes nord et sud des Iles-de-la-Madeleine, Golfe du Saint-Laurent. Can Tech Rep Fish Aquat Sci 1417:1–14

    Google Scholar 

  • Attard J, Hudon C (1987) Embryonic development and energetic investment in egg production in relation to size of female lobster (Homarus americanus). Can J Fish Aquat Sci 44:1157–1164

    Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  Google Scholar 

  • Brooks S, Tyler CR, Sumpter JP (1997) Egg quality in fish: what makes a good egg? Rev Fish Biol Fish 7:387–416

    Article  Google Scholar 

  • Capuzzo JM, Lancaster BA (1979) Some physiological and biochemical considerations of larval development in the American lobster, Homarus americanus Milne Edwards. J Exp Mar Biol Ecol 40:53–62

    Article  CAS  Google Scholar 

  • Clarke A, Shadsheim A, Holmes LJ (1985) Lipid biochemistry and reproductive biology in two species of Gammaridae (Crustacea: Amphipoda). Mar Biol 88:247–263

    CAS  Google Scholar 

  • Clarke A, Brown JH, Holmes LJ (1990) The biochemical composition of eggs from Macrobrachium rosenbergii in relation to embryonic development. Comp Biochem Physiol 96B:505–511

    CAS  Google Scholar 

  • Cobb JS, Phillips BF (1980) The biology and management of lobsters, vol I Physiology and behavior. Academic Press, New York

  • Dehn PF, Aiken DE, Waddy SL (1983) Aspects of vitellogenesis in the lobster Homarus americanus. Can Tech Rep Fish Aquat Sci 1161:1–28

    Google Scholar 

  • DeLeersynder M, Dhainaut A, Porcheron P (1980) La vitellogenèse chez le crabe Eriocheir sinensis. Bull Soc Zool Fr 105:413–418

    Google Scholar 

  • Factor JR (ed) (1995) Biology of the lobster Homarus americanus. Academic Press, San Diego

  • Fraser AJ, Tocher DR, Sargent JR (1985) Thin-layer chromatography – flame ionization detection and the quantitation of marine neutral lipids and phospholipids. J Exp Mar Biol Ecol 88:91–99

    CAS  Google Scholar 

  • Fyhn HJ (1993) Multiple functions of FAA during embryogenesis in marine fishes. In: Walther BT, Fyhn HJ (eds) Physiological and biochemical aspects of fish development. University of Bergen, Norway, pp 299–308

  • Galois R (1987) Les lipides neutres chez les crustacés décapodes: métabolismes et besoins. Océanis 13:197–215

    Google Scholar 

  • Gardner C (2001) Composition of eggs in relation to embryonic development and female size in giant crabs (Pseudicarcinus gigas (Lamarck)). Mar Freshwat Res 52:333–338

    Article  Google Scholar 

  • Gendron L (2002) Le homard des eaux côtières du Québec en 2001. MPO Science, Rapport sur l’État des Stocks C4–05 (2001)

  • Giménez L, Anger K (2001) Relationships among salinity, egg size, embryonic development, and larval biomass in the estuarine crab Chasmagnathus granulata Dana, 1851. J Exp Mar Biol Ecol 260:241–257

    PubMed  Google Scholar 

  • Harrison KE (1990) The role of nutrition in maturation, reproduction and embryonic development of decapod crustaceans: a review. J Shellfish Res 9:1–28

    Google Scholar 

  • Helluy SM, Beltz BS (1991) Embryonic development of the American lobster (Homarus americanus): quantitative staging and characterization of an embryonic molt cycle. Biol Bull 180:355–371

    Google Scholar 

  • Herring PJ (1974) Observations on the embryonic development of some deep-living decapod crustaceans, with particular reference to species of Acanthephyra. Mar Biol 25:25–33

    Google Scholar 

  • Holland DL (1978) Lipid reserves and energy metabolism in the larvae of benthic marine invertebrates. In: Malins DC, Sargent JR (eds) Biochemical and biophysical perspectives in marine biology, vol 4. Academic Press, London, pp 85–123

  • Latrouite D, Morizur Y, Raguenes G (1984) Fécondités individuelles et par recrue du homard européen Homarus gammarus (L.) des côtes françaises. C.I.E.M.C.M 1984/K:38

  • MacKenzie B (1988) Assessment of temperature effects on interrelationships between stage durations, mortality, and growth in laboratory-reared Homarus americanus Milne Edwards larvae. J Exp Mar Biol Ecol 116:87–98

    Article  Google Scholar 

  • Marangos C (1988) Variations des concentrations des acides aminés libres et des protéines totales dans les oeufs de la crevette grise Crangon crangon (Crustacea : Decapoda) au cours de l’embryogenèse. Umi La Mer Tokyo 26:61–68

    Google Scholar 

  • Mellinger J (1995) Les réserves lipidiques de l’oeuf des poissons. Annee Biol 34:63–90

    CAS  Google Scholar 

  • Morais S, Narciso L, Calado R, Nunes ML, Rosa R (2002) Lipid dynamics during the embryonic development of Plesionika martia (Decapoda; Pandalidae) and Palaemon serratus (Decapoda; Palaemonidae): relation to metabolic consumption. Mar Ecol Prog Ser 242:195–204

    CAS  Google Scholar 

  • Nates SF, McKenney CL Jr (2000) Ontogenic changes in biochemical composition during larval and early postlarval development of Lepidophtalmus louisianensis, a ghost shrimp with abbreviated development. Comp Biochem Physiol 127B:459–468

    CAS  Google Scholar 

  • O’Connor JD, Gilbert LI (1968) Aspects of lipid metabolism in crustaceans. Am Zool 8:529–539

    CAS  PubMed  Google Scholar 

  • Ouellet P, Taggart CT, Frank KT (1992) Lipid condition and survival in shrimp (Pandalus borealis) larvae. Can J Fish Aquat Sci 49:368–378

    Google Scholar 

  • Ouellet P, Allard JP (2002) Seasonal and interannual variability in larval lobster Homarus americanus size, growth and condition in the Magdalen Islands, southern Gulf of St. Lawrence. Mar Ecol Prog Ser 230:241–251

    Google Scholar 

  • Pandian TJ (1970) Yolk utilization and hatching time in the Canadian lobster Homarus americanus. Mar Biol 7:249–254

    Google Scholar 

  • Parrish CC (1987) Separation of aquatic lipid classes by chromarod thin-layer chromatography with measurement by Iatroscan flame ionisation detection. Can J Fish Aquat Sci 44:722–731

    CAS  Google Scholar 

  • Perkins HC (1972) Developmental rates at various temperatures of embryos of the northern lobster (Homarus americanus Milne-Edwards). Fish Bull 70:95–99

    Google Scholar 

  • Petersen S, Anger K (1997) Chemical and physiological changes during the embryonic development of the Spider Crab, Hyas araneus L. (Decapoda: Majidae). Comp Biochem Physiol 117B:299–306

    CAS  Google Scholar 

  • Pezzack (1996) Overview of the Canadian lobster (Homarus americanus) fishery: Recent trends in landings and management and the outlook for the future. J Shellfish Res 15:494

    Google Scholar 

  • Phillips BF, Cobb JS, George RW (1980) General Biology. In Cobb JS, Phillips BF (eds) The biology and management of lobsters, vol I Physiology and behavior. Academic Press, New York, pp 1–82

  • Quinn GP, Keough MJ (2002)Experimental design and data analysis for biologists. Cambridge University Press. Cambridge

  • Sasaki GC (1984) Biochemical changes associated with embryonic and larval development in the american lobster Homarus americanus Milne Edwards. PhD thesis, MIT, Cambridge, and WHOI, Woods Hole, Mass.

  • Sasaki GC, Capuzzo JM, Biesiot P (1986) Nutritional and bioenergetic considerations in the development of the American lobster Homarus americanus. Can J Fish Aquat Sci 43:2311–2319

    CAS  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem150:76–85

    Google Scholar 

  • Tocher DR, Fraser AJ, Sargent JR, Gamble JC (1985) Lipid class composition during embryonic and early larval development in Atlantic herring (Clupea harengus L.). Lipids 20:84–89

    CAS  PubMed  Google Scholar 

  • Tremblay MJ, Sainte-Marie B (2001) Symposium sur le programme integré sur le homard canadien et son evironnement (PINHCE): Résumés et sommaire des travaux. Can Tech Rep Fish Aquat Sci 2328:1–130

    Google Scholar 

  • Tully O, Roantree V, Robinson M (2001) Maturity, fecundity and reproductive potential of the European lobster (Homarus gammarus) in Ireland. J Mar Biol Assoc UK 81:61–68

    Google Scholar 

  • Wear RG (1974) Incubation in British decapod Crustacea, and the effects of temperature on the rate and success of embryonic development. J Mar Biol Assoc UK 54:745–762

    Google Scholar 

  • Wehrtmann IS, Graeve M (1998) Lipid composition and utilization in developing eggs of two tropical marine caridean shrimps (Decapoda: Caridea: Alpheidae, Palaemonidae). Comp Bioch Physiol 121B:457–463

    CAS  Google Scholar 

  • Wehrtmann IS, Kattner G (1998) Changes in volume, biomass, and fatty acids of developing eggs in Nauticaris magellanica (Decapoda: Caridea): a latitudinal comparison. J Crustacean Biol 18:413–422

    Google Scholar 

Download references

Acknowledgements

We thank Jean-Pierre Allard and Brigitte Desrosiers for the maintenance of the tank and the water circulation system and for their help during egg sampling from August 2000 to June 2001. We also thank Nathalie Côté for her assistance with the laboratory analyses. Laure Devine edited the English version of the text. We finally thank the Institut des Sciences de la Mer of Rimouski (ISMER) for its financial help during a part of the project. The comments by two anonymous referees greatly contributed to the preparation of this enhanced version of the initial manuscript.

Author information

Authors and Affiliations

  1. Institut des sciences de la mer de Rimouski (ISMER), Université du Québec à Rimouski (UQAR), 310 allée des Ursulines, Rimouski, Québec, G5L 3A1, Canada

    V. Sibert & J-C. Brêthes

  2. Maurice Lamontagne Institute, Fisheries and Oceans Canada, 850 route de la mer, Mont-Joli, Québec, G5H 3Z4, Canada

    P. Ouellet

Authors
  1. V. Sibert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Ouellet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J-C. Brêthes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. Sibert.

Additional information

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

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sibert, V., Ouellet, P. & Brêthes, JC. Changes in yolk total proteins and lipid components and embryonic growth rates during lobster (Homarus americanus) egg development under a simulated seasonal temperature cycle. Marine Biology 144, 1075–1086 (2004). https://doi.org/10.1007/s00227-003-1287-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-003-1287-1

Keywords

Search

Navigation