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Energy metabolism of eggs during embryogenesis in Balanus balanoides

Published online by Cambridge University Press:  11 May 2009

M. I. Lucas  and
D. J. Crisp†
M. I. Lucas
Affiliation:
N.E.R.C. Unit of Marine Invertebrate Biology, Marine Science Laboratories, Menai Bridge, Gwynedd LL59 5EH
D. J. Crisp†
Affiliation:
N.E.R.C. Unit of Marine Invertebrate Biology, Marine Science Laboratories, Menai Bridge, Gwynedd LL59 5EH
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Abstract

The partitioning and utilization of energy reserves during embryogenesis were followed in the cirripede Balanus balanoides and related to the described sequence of developmental stages. Egg volume and dry weights were measured. Between the recently fertilized egg and eggs containing well-developed embryos at the end of natural incubation there is a doubling of egg volume.

The biochemical composition of the newly fertilized egg is dominated by TCA-insoluble protein (55 %). Neutral lipid accounts for 17 % of the dry weight, while phospholipid and polysaccharide contribute 3–5% and 5–7% respectively. About 36% of the TCA-insoluble protein is utilized during in vivo development, accounting for about three-quarters of the energy expenditure. During this time 40% of the carbohydrate and 20% of the neutral lipid reserves are also utilised. However, when starved adults retain their mature egg masses beyond the normal term, egg metabolism occurs largely at the expense of the remaining lipid reserves. These would be exhausted in a further 6–7 weeks and the embryos unable to survive. The ability of adults to postpone hatching may therefore have important implications for the energy reserves and viability of the newly hatched nauplii. Protein supplies most of the energy during embryogenesis, with neutral lipid assuming increased importance after development has been completed.

Oxygen consumption of the egg masses measured in vitro was converted through aerobic oxycalorific equivalent into biochemical loss. This showed good agreement with direct measurement of summed energy losses of the biochemical components. It was apparent that oxygen uptake rate in the later stages was restricted by diffusion resistance due to egg packing, since eggs freed from the egg mass matrix showed a 30% increase in oxygen uptake and a reduction in development time.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 67 , Issue 1 , February 1987 , pp. 27 - 54
Copyright
Copyright © Marine Biological Association of the United Kingdom 1987

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References

Achituv, Y. & Barnes, H., 1976. Studies in the biochemistry of cirripede eggs. V. Changes in the general biochemical composition during development of Chthamalus stellatus (Poli). Journal of Experimental Marine Biology and Ecology, 22, 263—267.CrossRefGoogle Scholar
Achituv, Y. & Barnes, H., 1978. Studies in the biochemistry of cirripede eggs. VI. Changes in the general biochemical composition during development of Tetraclita squamosa rufotincta Pilsbry, Balanus perfortus Brug., and Pollicipes cornucopia Darwin. Journal of Experimental Marine Biology and Ecology, 32, 171–176.CrossRefGoogle Scholar
Achituv, Y. & Wortzlavski, A., 1983. Studies in the biochemistry of cirripede eggs. VII. Changes in the general biochemical composition during development of Chthamalus dentatus Krauss and Octomeris angulosa Sowerby. Journal of Experimental Marine Biology and Ecology, 69, 137–144.CrossRefGoogle Scholar
Baldwin, E., 1937. An Introduction to Comparative Biochemistry. Cambridge University Press.CrossRefGoogle Scholar
Barnes, H., 1965. Studies in the biochemistry of cirripede eggs. I. Changes in general biochemical composition during development of Balanus balanoides and B. balanus. Journal of the Marine Biological Association of the United Kingdom, 45, 321–339.CrossRefGoogle Scholar
Barnes, H. & Blackstock, J., 1973. Estimation of the lipids in marine animals: detailed investigation of the sulphophosphovanillin method for ‘total’ lipids. Journal of Experimental Marine Biology and Ecology, 12, 103–118.CrossRefGoogle Scholar
Barnes, H. & Evens, R., 1967. Studies in the biochemistry of cirripede eggs. III. Changes in the amino-acid composition during development of Balanus balanoides and B. balanus. Journal of the Marine Biological Association of the United Kingdom, 47, 171–180.CrossRefGoogle Scholar
Crisp, D. J., 1954. The breeding of Balanus porcatus (da Costa) in the Irish Sea. Journal of the Marine Biological Association of the United Kingdom, 33, 473–496.CrossRefGoogle Scholar
Crisp, D. J., 1956. A substance promoting hatching and liberation of young in cirripedes. Nature, London, 178, 263.CrossRefGoogle Scholar
Crisp, D. J., 1959. The rate of development of Balanus balanoides (L.) embryos in vitro. Journal of Animal Ecology, 28, 119–132.CrossRefGoogle Scholar
Crisp, D. J., 1964. Plastron respiration. In Recent Progress in Surface Science, vol. 2 (ed. Danielli, J. F., Pankhurst, G. A. and Riddiford, A. C.), pp. 377–125. New York: Academic Press.Google Scholar
Crisp, D. J., 1974. Energy relations of marine invertebrate larvae. Thalassia jugoslavica, 10, 103–120.Google Scholar
Crisp, D. J., 1976. The rôle of the pelagic larva. In Perspectives in Experimental Biology, vol. 1. Zoology (ed. Spencer-Davies, P.), pp. 145–155. Oxford: Pergamon Press.Google Scholar
Crisp, D. J., 1984. Energy flow measurements. In Methods for the Study of Marine Benthos, 2nd ed. (ed. Holme, N. A. and McIntyre, A. D.), pp. 284–372. Oxford: Blackwell. [IBP Handbook no. 16.]Google Scholar
Crisp, D. J., 1986. A comparison between the reproduction of high- and low-latitude barnacles, including Balanus balanoides and Tetraclita (Tesseropora) pacifica. In Biology of Benthic Marine Organisms (ed. Thompson, M.-F., Sarojini, R. and Nagabhushanam, R.), pp. 69–84. Rotterdam: A. A. Balkema.Google Scholar
Crisp, D. J. & Clegg, D. J., 1960. The induction of the breeding condition in Balanus balanoides (L.) Oikos, 11, 265–275.CrossRefGoogle Scholar
Crisp, D. J. & Southward, A. T., 1961. Different types of cirral activity of barnacles. Philosophical Transactions of the Royal Society (B), 243, 271–308.Google Scholar
Crisp, D. J. & Spencer, C. P., 1958. The control of the hatching process in barnacles. Proceedings of the Royal Society (B), 148, 278–299.Google Scholar
Dawson, R. M. C. & Barnes, H., 1966. Studies in the biochemistry of cirripede eggs. II. Changes in lipid composition during development of Balanus balanoides and B. balanus. Journal of the Marine Biological Association of the United Kingdom, 46, 249—261.CrossRefGoogle Scholar
Holland, D. L., 1978. Lipid reserves and energy metabolism in the larvae of benthic marine invertebrates. In Biochemical and Biophysical Perspectives in Marine Biology, vol. 4 (ed. Malins, D. C. and Sargent, J. R.), pp. 85–119. London: Academic Press.Google Scholar
Holland, D. L. & Gabbott, P. A., 1971. A micro-analytical scheme for the determination of protein, carbohydrate, lipid and RNA levels in marine invertebrate larvae. Journal of the Marine Biological Association of the United Kingdom, 51, 659–668.CrossRefGoogle Scholar
Holland, D. L. & Hannant, P. J., 1973. Addendum to a micro-analytical scheme for the biochemical analysis of marine invertebrate larvae. Journal of the Marine Biological Association of the United Kingdom, 53, 833–838.CrossRefGoogle Scholar
Holland, D. L. & Walker, G., 1975. The biochemical composition of the cypris larvae of the barnacle Balanus balanoides L. Journal du Conseil, 36, 162–165.CrossRefGoogle Scholar
Lowry, O. M., Rosebrough, N. J., Farr, A. L. & Randall, R. J., 1951. Protein measurement with the folin phenol reagent. Journal of Biological Chemistry, 193, 265–275.CrossRefGoogle ScholarPubMed
Lucas, M. I., Walker, G., Holland, D. L., & Crisp, D. J., 1979. An energy budget for the free swimming and metamorphosing cypris larva of Balanus balanoides (L.) (Crustacea: Cirripedia). Marine Biology 55, 221–229.CrossRefGoogle Scholar
Manahan, D. T. & Crisp, D. J., 1982. The role of dissolved organic material in the nutrition of pelagic larvae: amino acid uptake by bivalve veligers. American Zoologist, 22, 635–646.CrossRefGoogle Scholar
Needham, J., 1942. Biochemistry and Morphogenesis. Cambridge University Press.Google Scholar
Pandian, T. J. & Schumann, K-H., 1967. Chemical composition and caloric content of egg and zoea of the hermit crab Eupagurus bernardus. Helgoländer wissenschaftliche Meeresuntersuchungen, 16, 225–230.CrossRefGoogle Scholar
Patel, B. & Crisp, D. J., 1960 a. The influence of temperature on the breeding and moulting activities of some warm-water species of operculate barnacles. Journal of the Marine Biological Association of the United Kingdom, 39, 667–680.CrossRefGoogle Scholar
Patel, B. & Crisp, D. J., 1960 b. Rates of development of the embryos of several species of barnacles. Physiological Zoology, 33, 104–119.CrossRefGoogle Scholar
Southward, A. J., 1976. On the taxonomic status and distribution of Chthamalus stellatus (Cirripedia) in the north-east Atlantic region: with a key to the common intertidal barnacles of Britain. Journal of the Marine Biological Association of the United Kingdom, 56, 1007–1028.CrossRefGoogle Scholar
Spencer-Davies, P., 1966. A constant pressure respirometer for medium sized animals. Oikos, 17, 108–112.CrossRefGoogle Scholar
Walley, L. J., 1965. The development and function of the oviducal gland in Balanus balanoides. Journal of the Marine Biological Association of the United Kingdom, 45, 115–128.CrossRefGoogle Scholar
White, K. N. & Walker, G. 1981. Rate of nitrogen excretion by the shore barnacle Balanus balanoides (L.). Comparative Biochemistry and Physiology, 69 A, 389–394.CrossRefGoogle Scholar