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The dual functions of sea urchin gonads are reflected in the temporal variations of their biochemistry

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Abstract

Fatty acid analyses are emerging as a powerful technique to probe trophic interactions between organisms. In this paper, the application of both this procedure and gonad index (GI) determination on two populations (intertidal and subtidal) of the echinoid Psammechinus miliaris is reported. The investigation spanned the 3-month spawning period of Scottish west coast populations. In both populations a progressive decrease in the GI was found, coupled with an increasing maturity stage (from mature to spent). Sexual maturation and decrease in GI was synchronous between the two populations. In conjunction, there were distinct changes in gonad biochemistry. Differences in the fatty acid composition of the gonad reflected the changes in sexual maturation. Mature males and females had significant differences in the fatty acid composition of their gonads, whereas post-spawned individuals showed no gender differences. Male urchins had higher levels of polyunsaturated fatty acids (PUFAs) compared to females, and there was a dramatic reduction in the fatty acids 22:6(n−3) and 20:5(n−3) with increasing maturity stage. Using multivariate statistical techniques, these changes in the fatty acid composition of the sea urchin gonad were linked to habitat related diet differences combined with gender differences. These changes in the fatty acid signatures clearly reflect the dual function of the gonad as both a nutrient store and a reproductive organ.

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References

  • Allen WV (1968) Fatty-acid synthesis in the echinoderms:Asterias rubens and Echinus esculentus and Holothuria forskali. J Mar Biol Assoc of UK 48:521–533

    Article  CAS  Google Scholar 

  • Black KD, Hughes DJ, Provost PG, Pereira PMF (2000) Broad scale survey and mapping of seabed biota in Loch Creran, Argyll. Report no. F98AA408., Scottish Natural Heritage

  • Bonesi L, Chanin P, Macdonald DW (2004) Competition between Eurasian otter Lutra lutra and American mink Mustela vison probed by niche shift. Oikos 106:19–26

    Article  Google Scholar 

  • Brazao S, Morais S, Boaventura D, Re P, Narciso L, Hawkins SJ (2003) Spatial and temporal variation of the fatty acid composition of Patella spp. (Gastropoda: Prosobranchia) soft bodies and gonads. Comp Biochem Physiol B-Biochem Mol Biol 136:425–441

    Article  Google Scholar 

  • Byrne M, Andrew NL, Worthington DG, Brett PA (1998) Reproduction in the diadematoid sea urchin Centrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia. Mar Biol 132:305–318

    Article  Google Scholar 

  • Cook EJ, Bell MV, Black KD, Kelly MS (2000) Fatty acid compositions of gonadal material and diets of the sea urchin, Psammechinus miliaris: trophic and nutritional implications. J Exp Mar Biol Ecol 255:261–274

    Article  CAS  Google Scholar 

  • Cook PA, Gabbott PA (1972) Seasonal changes in the biochemical composition of the adult barnacles, Balanus balanoides, and the possible relationships between biochemical composition and cold-tolerance. J Mar Biol Assoc of UK 52:805–825

    Article  CAS  Google Scholar 

  • Cripps GC, Watkins JL, Hill HJ, Atkinson A (1999) Fatty acid content of Antarctic krill Euphausia superba at South Georgia related to regional populations and variations in diet. Mar Ecol Prog Ser 181:177–188

    Article  CAS  Google Scholar 

  • de la Moriniere EC, Pollux BJA, Nagelkerken I, Hemminga MA, Huiskes AHL, van der Velde G (2003) Ontogenetic dietary changes of coral reef fishes in the mangrove-seagrass-reef continuum: stable isotopes and gut- content analysis. Mar Ecol Prog Ser 246:279–289

    Article  Google Scholar 

  • Elton C (1927) Animal ecology. Sidgwick & Jackson Ltd., London

    Google Scholar 

  • Floreto EAT, Teshima S, Ishikawa M (1996) The effects of seaweed diets on the growth, lipid and fatty acids of juveniles of the white sea urchin Tripneustes gratilla. Fish Sci 62:589–593

    Article  CAS  Google Scholar 

  • Fraser AJ, Gamble JC, Sargent JR (1988) Changes in lipid-content, lipid class composition and fatty-acid composition of developing eggs and unfed larvae of Cod (Gadus-Morhua). Mar Biol 99:307–313

    Article  CAS  Google Scholar 

  • Fretwell SD (1987) Food-chain dynamics—the central theory of ecology. Oikos 50:291–301

    Article  Google Scholar 

  • Fry B, Sherr EB (1984) Delta-C-13 Measurements as indicators of carbon flow in marine and fresh-water ecosystems. Contrib in Mar Sci 27:13–47

    CAS  Google Scholar 

  • Go JV, Rezanka T, Srebnik M, Dembitsky VM (2002) Variability of fatty acid components of marine and freshwater gastropod species from the littoral zone of the Red Sea, Mediterranean Sea, and Sea of Galilee. Biochem Syst Ecol 30:819–835

    Article  CAS  Google Scholar 

  • Howell KL, Pond DW, Billett DSM, Tyler PA (2003) Feeding ecology of deep-sea seastars (Echinodermata: Asteroidea): a fatty-acid biomarker approach. Mar Ecol Prog Ser 255:193–206

    Article  CAS  Google Scholar 

  • Hudson IR, Wigham BD, Billett DSM, Tyler PA (2003) Seasonality and selectivity in the feeding ecology and reproductive biology of deep-sea bathyal holothurians. Prog Oceanogr 59:381–407

    Article  Google Scholar 

  • Hughes AD, Catarino AI, Kelly MS, Barnes DKA, Black KD (2005) Gonad fatty acids and trophic interactions of the echinoid Psammechinus miliaris. Mar Ecol Prog Ser (in press)

  • Iverson SJ, Frost KJ, Lowry LF (1997) Fatty acid signatures reveal fine scale structure of foraging distribution of harbor seals and their prey in Prince William Sound, Alaska. Mar Ecol Prog Ser 151:255–271

    Article  CAS  Google Scholar 

  • Kelly MS (2000) The reproductive cycle of the sea urchin Psammechinus miliaris (Echinodermata: Echinoidea) in a Scottish sea loch. J Mar Biol Assoc UK 80:909–919

    Article  Google Scholar 

  • Kelly MS (2001) Environmental parameters controlling gametogenesis in the echinoid Psammechinus miliaris. J Exp Mar Biol Ecol 266:67–80

    Article  Google Scholar 

  • Kelly MS, Cook EJ (2001) The ecology of Psammechinus miliaris. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 217–224

    Chapter  Google Scholar 

  • Linderman RL (1942) The trophic-dynamic aspect of ecology. Ecology 23:399–418

    Article  Google Scholar 

  • Lozano J, Galera J, Lopez S, Turon X, Palacin C, Morera G (1995) Biological cycles and recruitment of Paracentrotus-Lividus (Echinodermata, Echinoidea) in 2 contrasting habitats. Mar Ecol Prog Ser 122:179–191

    Article  Google Scholar 

  • McClanahan TR, Kurtis JD (1991) Population regulation of the rock-boring sea-urchin Echinometra-Mathaei (Deblainville). J Exp Mar Biol Ecol 147:121–146

    Article  Google Scholar 

  • McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393

    Article  Google Scholar 

  • Menge BA (2000) Top-down and bottom-up community regulation in marine rocky intertidal habitats. J Exp Mar Biol Ecol 250:257–289

    Article  CAS  Google Scholar 

  • Morais S, Boaventura D, Narciso L, Re P, Hawkins SJ (2003) Gonad development and fatty acid composition of Patella depressa Pennant (Gastropoda : Prosobranchia) populations with different patterns of spatial distribution, in exposed and sheltered sites. J Exp Mar Biol Ecol 294:61–80

    Article  CAS  Google Scholar 

  • Ojea J, Pazos AJ, Martinez D, Novoa S, Sanchez JL, Abad M (2004) Seasonal variation in weight and biochemical composition of the tissues of Ruditapes decussatus in relation to the gametogenic cycle. Aquaculture 238:451–468

    Article  CAS  Google Scholar 

  • Pazos AJ, Roman G, Acosta CP, Sanchez JL, Abad M (1997) Lipid classes and fatty acid composition in the female gonad of Pecten maximus in relation to reproductive cycle and environmental variables. Comp Biochem Physiol B-Biochem Mol Biol 117:393–402

    Article  Google Scholar 

  • Phillips KL, Jackson GD, Nichols PD (2003) Temporal variations in the diet of the squid Moroteuthis ingens at Macquarie Island: stomach contents and fatty acid analyses. Mar Ecol Prog Ser 256:135–149

    Article  CAS  Google Scholar 

  • Pond DW, Dixon DR, Bell MV, Fallick AE, Sargent JR (1997) Occurrence of 16:2(n−4) and 18:2(n−4) fatty acids in the lipids of the hydrothermal vent shrimps Rimicaris exoculata and Alvinocaris markensis: nutritional and trophic implications. Mar Ecol Prog Ser 156:167–174

    Article  CAS  Google Scholar 

  • Rosa R, Costa PR, Nunes ML (2004a) Effect of sexual maturation on the tissue biochemical composition of Octopus vulgaris and O. defflippi (Mollusca : Cephalopoda). Mar Biol 145:563–574

    Article  CAS  Google Scholar 

  • Rosa R, Costa PR, Pereira J, Nunes ML (2004b) Biochemical dynamics of spermatogenesis and oogenesis in Eledone cirrhosa and Eledone moschata (Cephalopoda: Octopoda). Comp Biochem Physiol B-Biochem Mol Biol 139:299–310

    Article  CAS  Google Scholar 

  • Rosa R, Nunes ML (2002) Biochemical changes during the reproductive cycle of the deep-sea decapod Nephrops norvegicus on the south coast of Portugal. Mar Biol 141:1001–1009

    Article  CAS  Google Scholar 

  • Rosa R, Nunes ML (2003) Tissue biochemical composition in relation to the reproductive cycle of deep-sea decapod Aristeus antennatus in the Portuguese south coast. J Mar Biol Assoc UK 83:963–970

    Article  CAS  Google Scholar 

  • Russell MP (1998) Resource allocation plasticity in sea urchins: rapid, diet induced, phenotypic changes in the green sea urchin, Strongylocentrotus droebachiensis (Muller). J Exp Mar Biol Ecol 220:1–14

    Article  Google Scholar 

  • Serrazanetti GP, Pagnucco C, Conte LS, Cattani O (1995) Hydrocarbons, Sterols and fatty-acids in Sea-Urchin (Paracentrotus-Lividus) of the Adriatic Sea. Chemosphere 30:1453–1461

    Article  Google Scholar 

  • Soudant P, Van Ryckeghem K, Marty Y, Moal J, Samain JF, Sorgeloos P (1999) Comparison of the lipid class and fatty acid composition between a reproductive cycle in nature and a standard hatchery conditioning of the Pacific Oyster Crassostrea gigas. Comp Biochem Physiol B-Biochem Mol Biol 123:209–222

    Article  Google Scholar 

  • Xu XL, Ji WJ, Castell JD, Odor RK (1994) Influence of dietary-lipid sources on fecundity, egg hatchability and fatty-acid composition of Chinese Prawn (Penaeus-Chinensis) Broodstock. Aquaculture 119:359–370

    Article  CAS  Google Scholar 

  • Yatsuya K, Nakahara H (2004) Density, growth and reproduction of the sea urchin Anthocidaris crassispina (A. Agassiz) in two different adjacent habitats, the Sargassum area and Corallina area. Fish Sci 70:233–240

    Article  CAS  Google Scholar 

  • Zamon JE (2001) Seal predation on salmon and forage fish schools as a function of tidal currents in the San Juan Islands, Washington, USA. Fish Oceanogr 10:353–366

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank Dr. E. Cook for her help and Miss H. Muir for her technical support with the fatty acid analysis. They would also like to thank M.V. Bell for his helpful comments on an earlier draft of this manuscript. We would also like to acknowledge the Leonardo da Vinci scholarship for facilitating the visit of AIC to SAMS. This research was funded through the NERC Ph.D. studentship NER/S/A/2002/1055.

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Authors and Affiliations

  1. Scottish Association for Marine Science, Dunbeg, Oban, Argyll, PA37 1QA, Scotland

    Adam D. Hughes, Maeve S. Kelly, Ana I. Catarino & Kenneth D. Black

  2. Biological Sciences Division, British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge, CB3 0ET, UK

    David K. A. Barnes

  3. Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1149-016, Lisboa, Portugal

    Ana I. Catarino

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  1. Adam D. Hughes
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  2. Maeve S. Kelly
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  3. David K. A. Barnes
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  4. Ana I. Catarino
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  5. Kenneth D. Black
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Correspondence to Adam D. Hughes.

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Communicated by J. P. Thorpe

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Hughes, A.D., Kelly, M.S., Barnes, D.K.A. et al. The dual functions of sea urchin gonads are reflected in the temporal variations of their biochemistry. Marine Biology 148, 789–798 (2006). https://doi.org/10.1007/s00227-005-0124-0

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  • DOI: https://doi.org/10.1007/s00227-005-0124-0

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