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Food availability and physiological state of sea urchin larvae (Strongylocentrotus purpuratus)

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Abstract

Food availability is highly variable in the ocean. Many species of marine invertebrates have a larval form that depends upon exogenous nutrients for growth, yet there are few biochemical and physiological indices for determining changes in the nutritional status of larvae. In this study, the effects of food availability on biochemical compositions and metabolic processes of larvae of the sea urchin, Strongylocentrotus purpuratus, were determined. Larvae were cultured under different food concentrations (fed-to-excess and unfed) and a suite of biological processes assayed, ranging from measurements at the level of the whole organism to that of specific molecules. These data were normalized to DNA content (an index of cell number) to allow comparisons of physiological rates in larvae of different sizes. Changes in the following were measured during larval growth: free amino acid pool, protein, lipid classes (cholesterol, free fatty acids, hydrocarbons, phospholipids, triacylglycerol), enzyme activities (Na+, K+-ATPase and citrate synthase), and respiration rates. In growing larvae, the two key components that showed differential cell-specific content relative to unfed larvae were glycine in the free amino acid pool and phospholipids. Additionally, several lipid classes were detectable only in fed larvae (cholesterols, free fatty acids, and hydrocarbons). While triacylglycerols were present in eggs and utilized during pre-feeding development, they were not re-accumulated at detectable levels in feeding larvae. Respiration rates, protein content, and enzyme activities were all similar on a cell-specific basis, showing that these variables did not provide useful indices of differences in physiological state between fed and unfed larvae. In contrast, measurements of the cell-specific content of glycine and certain lipid classes did provide useful indices of physiological state of larvae. Application of these indices could potentially allow for determinations of nutritional state of larvae in the ocean.

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References

  • Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1994) Molecular biology of the cell, 3rd edn. Garland Publishing, New York

  • Anger K (1995) Starvation resistance in larvae of a semiterrestrial crab, Sesarma curacaoense (Decapoda: Grapsidae). J Exp Mar Biol Ecol 187:161–174

    Article  Google Scholar 

  • Anger K, Dawirs RR (1981) Influence of starvation on the larval development of Hyas areneus (Decapoda: Majidae). Helgol Meeresunters 34:287–311

    Article  Google Scholar 

  • Blaxter JHS, Hempel G (1963) The influence of egg size on herring larvae (Clupea harengus L.). J Cons Int Explor Mer 28:211–240

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Boidron-Metairon IF (1988) Morphological plasticity in laboratory-reared echinoplutei of Dendraster excentricus (Eschscholtz) and Lytechinus variegates (Lamarck) in response to food conditions. J Exp Mar Biol Ecol 119:31–41

    Article  Google Scholar 

  • Brunk CF, Jones KC, James TW (1979) Assay for nanogram quantities of DNA in cellular homogenates. Anal Biochem 92:497–500

    Article  PubMed  CAS  Google Scholar 

  • Buckley LJ (1984) RNA–DNA ratio: an index of larval fish growth in the sea. Mar Biol 80:291–298

    Article  CAS  Google Scholar 

  • Cameron RA, Britten RJ, Davidson EH (1989) Expression of two actin genes during larval development in the sea urchin Strongylocentrotus purpuratus. Mol Reprod Dev 1:149–155

    Article  PubMed  CAS  Google Scholar 

  • Childress JJ, Somero GN (1990) Metabolic scaling: a new perspective based on scaling of glycolytic enzyme activities. Am Zool 30:161–173

    CAS  Google Scholar 

  • Clarke ME, Calvi C, Domeier M, Edmonds M, Walsh PJ (1992) Effects of nutrition and temperature on metabolic enzyme activities in larval and juvenile red drum, Sciaenops ocellatus, and lane snapper, Lutjanus synagris. Mar Biol 112:31–36

    Article  CAS  Google Scholar 

  • Crisp DJ (1974a) Factors influencing the settlement of marine invertebrate larvae. In: Grant PT, Mackie AN (eds) Chemoreception in marine organisms. Academic, London, pp 177–265

    Google Scholar 

  • Crisp DJ (1974b) Energy relations of marine invertebrate larvae. Thalassia Jugoslavica 10:103–120

    Google Scholar 

  • Davidson EH (1976) Gene activity in early development, 2nd edition. Academic, New York

    Google Scholar 

  • Davidson EH (1986) Gene activity in early development, 3rd edition. Academic, New York

    Google Scholar 

  • Davidson EH, Hough-Evans BR, Britten RJ (1982) Molecular biology of the sea urchin embryo. Science 217:17–26

    Article  PubMed  CAS  Google Scholar 

  • Fenaux L, Strathmann MF, Strathmann RR (1994) Five tests of food-limited growth of larvae in coastal waters by comparisons of rates of development and form of echinoplutei. Limnol Oceanogr 39:84–98

    Article  Google Scholar 

  • Fiske CH, Subbarow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375–400

    CAS  Google Scholar 

  • Fry BJ, Gross PR (1970) Patterns and rates of protein synthesis in sea urchin embryos. II. The calculation of absolute rates Dev Biol 21:125–146

    Article  PubMed  CAS  Google Scholar 

  • Gallager SM, Mann R, Sasaki GC (1986) Lipid as an index of growth and viability in three species of bivalve larvae. Aquaculture 56:81–103

    Article  CAS  Google Scholar 

  • Gnaiger E (1983) Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In: Gnaiger E, Forstner H (eds) Polarographic oxygen sensors: aquatic and physiological applications. Springer, Berlin, pp 337–345

    Google Scholar 

  • Graeve M, Kattner G, Hagen W (1994) Diet-induced changes in the fatty acid composition of artic herbivorous copepods: experimental evidence of trophic markers. J Exp Mar Biol Ecol 182:97–110

    Article  CAS  Google Scholar 

  • Hadfield MG, Carpizo-Ituarte EJ, del Carmen K, Nedved BT (2001) Metamorphic competence, a major adaptive convergence in marine invertebrate larvae. Am Zool 41:1123–1131

    Article  Google Scholar 

  • Hinegardner R (1974) Cellular DNA content of the echinodermata. Comp Biochem Physiol B 49:219–226

    Article  PubMed  Google Scholar 

  • His E, Seaman MNL (1992) Effects of temporary starvation on the survival, and on subsequent feeding and growth, of oyster (Crassostrea gigas) larvae. Mar Biol 114:277–279

    Article  Google Scholar 

  • Hochachka PW, Somero GN (1984) Biochemical adaptation. Princeton University Press, Princeton

    Google Scholar 

  • Hoegh-Guldberg O, Emlet RB (1997) Energy use during the development of a lecithotrophic and a planktotrophic echinoid. Biol Bull 192:27–40

    Article  Google Scholar 

  • Hoegh-Guldberg O, Manahan DT (1995) Coulometric measurement of oxygen consumption during development of marine invertebrate embryos and larvae. J Exp Biol 198:19–30

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Holland DL, Gabbott PA (1971) A micro-analytical scheme for the determination of protein, carbohydrate, lipid and RNA levels in marine invertebrate larvae. J Mar Biol Ass UK 51:659–668

    Article  CAS  Google Scholar 

  • Hurlbert SH, White MD (1993) Experiments with freshwater invertebrate zooplanktivores: quality of statistical analyses. Bull Mar Sci 53:128–153

    Google Scholar 

  • Jaeckle WB, Manahan DT (1989) Growth and energy imbalance during the development of a lecithotrophic molluscan larva (Haliotis rufescens). Biol Bull 177:237–246

    Article  Google Scholar 

  • Kattner G, Graeve M, Calcagno JA, Lovrich GA, Thatje S, Anger K (2003) Lipid, fatty acid and protein utilization during lecithotrophic larval development of Lithodes santolla (Molina) and Paralomis granulose (Jacquinot). J Exp Mar Biol Ecol 292:61–74

    Article  CAS  Google Scholar 

  • Lee JJ, Calzone FJ, Britten RJ, Angerer RC, Davidson EH (1986) Activation of sea urchin actin genes during embryogenesis. Measurement of transcript accumulation from five different genes in Strongylocentrotus purpuratus. J Mol Biol 188:173–183

    Article  PubMed  CAS  Google Scholar 

  • Leong PK, Manahan DT (1997) Metabolic importance of Na+, K+-ATPase activity during sea urchin development. J Exp Biol 200:2881–2892

    PubMed  CAS  Google Scholar 

  • Manahan DT (1990) Adaptations by invertebrate larvae for nutrient acquisition from seawater. Am Zool 30:147–160

    Google Scholar 

  • Manahan DT, Davis JP, Stephens GC (1983) Bacteria-free sea urchin larvae take up neutral amino acids selectively from seawater. Science 220:204–206

    Article  CAS  PubMed  Google Scholar 

  • Marsh AG, Manahan DT (1999) Accurate measurements of the respiration rates of marine invertebrate embryos and larvae. Mar Ecol Prog Ser 184:1–10

    Google Scholar 

  • Marsh AG, Leong PK, Manahan DT (1999) Energy metabolism during embryonic development and larval growth of an Antarctic sea urchin. J Exp Biol 202:2041–2050

    PubMed  CAS  Google Scholar 

  • McEdward LR, Herrera JC (1999) Body form and skeletal morphometrics during larval development of the sea urchin Lytechinus variegatus (Lamarck). J Exp Mar Biol Ecol 232:151–176

    Article  Google Scholar 

  • Moran AL, Manahan DT (2004) Physiological recovery from prolonged starvation in larvae of the Pacific oyster Crassostrea gigas. J Exp Mar Biol Ecol 306:17–36

    Article  CAS  Google Scholar 

  • Olson RR, Olson MH (1989) Food limitation of planktotrophic marine invertebrate larvae: does it control recruitment success? Ann Rev Ecol Syst 20:225–247

    Google Scholar 

  • Paulay G, Boring L, Strathmann RR (1985) Food limited growth and development of larvae: experiments with natural seawater. J Exp Mar Biol Ecol 93:1–10

    Article  Google Scholar 

  • Platt T, Fuentes-Yaco C, Frank KT (2003) Marine ecology: spring algal bloom and larval fish survival. Nature 423:398–400

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. Available at http://www.R-project.org

  • Schmidt-Nielsen K (1986) Scaling: why is animal size so important? Cambridge University Press, New York

  • Sewell MA (2005) Utilization of lipids during early development of the sea urchin Evechinus chloroticus. Mar Ecol Prog Ser 304:133–142

    Google Scholar 

  • Sewell MA, Cameron MJ, McArdle BH (2004) Developmental plasticity in larval development in the echinometrid sea urchin Evechinus chloroticus with varying food ration. J Exp Mar Biol Ecol 309:219–237

    Article  Google Scholar 

  • Shilling FM, Manahan DT (1990) Energetics of early development for the sea urchins Strongylocentrotus purpuratus and Lytechinus pictus and the crustacean Artemia sp. Mar Biol 106:119–127

    Article  Google Scholar 

  • Shilling FM, Manahan DT (1994) Energy metabolism and amino acid uptake during early development of antarctic and temperate echinoderms. Biol Bull 187:398–407

    Article  CAS  Google Scholar 

  • Srere PA (1969) Citrate synthase. In: Lowenstein JM (ed) Methods in enzymology, vol 13. Academic, New York, pp 3–11

  • Starr M, Himmelman JH, Therriault JC (1990) Direct coupling of marine invertebrate spawning with phytoplankton blooms. Science 247:1070–1074

    Article  Google Scholar 

  • Taylor JG (1982) An introduction to error analysis. University Science, Mill Valley

  • Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45

    Article  Google Scholar 

  • Vardeman SB, Jobe JM (2001) Statistical quality assurance methods for engineers. Wiley, New York

    Google Scholar 

  • Weiss GM, McManus GB, Harvey HR (1996) Development and lipid composition of the harpacticoid copepod Nitrocra spinipes reared on different diets. Mar Ecol Prog Ser 132:57–61

    CAS  Google Scholar 

  • Yasumasu I, Hino A, Suzuki A, Mita A (1984) Change in the triglyceride level in sea urchin eggs and embryos during early development. Dev Growth Diff 26:525–532

    Article  CAS  Google Scholar 

  • Younger MS (1979) Handbook for linear regression. Duxbury Press, North Scituate

    Google Scholar 

Download references

Acknowledgments

The authors are grateful to Drs. Simon Tavaré and Claudia Rangel Escareño of the University of Southern California for their advice on error propagation and statistical analysis. All experiments included in this study comply with current US laws regarding biological research on marine invertebrates. This work was supported by National Science Foundation Grant Number 0130398.

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Correspondence to D. T. Manahan.

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Communicated by J.P. Grassle.

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Meyer, E., Green, A.J., Moore, M. et al. Food availability and physiological state of sea urchin larvae (Strongylocentrotus purpuratus). Mar Biol 152, 179–191 (2007). https://doi.org/10.1007/s00227-007-0672-6

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