Marine Biology

, Volume 155, Issue 5, pp 473–482 | Cite as

Maternal provisioning for larvae and larval provisioning for juveniles in the toxopneustid sea urchin Tripneustes gratilla

  • M. Byrne
  • T. A. A. Prowse
  • M. A. Sewell
  • S. Dworjanyn
  • J. E. Williamson
  • D. Vaïtilingon
Original Paper

Abstract

Lipid and protein biochemistry of eggs (84 μm in diameter), embryos and early larvae of the tropical echinoid Tripneustes gratilla (Linnaeus 1758) were quantified to determine how maternal provisions are used to fuel development of the echinopluteus. The eggs contained a mean of 30.82 ng lipid and 87.32 ng protein. Energetic lipids were the major lipid component (55.52% of total lipid) with the major class being triglyceride (TG: mean 15.9 ng, 51.58% of total). Structural lipid was dominated by phospholipid (PL: mean 11.18 ng, 36.26% of total). Early embryogenesis was not a major drain on egg energetic lipid and protein. Development of the functional feeding larva used ca. 50% of initial egg energetic lipid and most of this was TG. Maternal TG was still present in the 8-day echinoplutei and it was estimated that this energetic lipid would be depleted in unfed larvae by day 10. There was no change in PL. In a separate experiment lipid biochemistry of rudiment stage larvae and early developing juveniles were quantified to determine how lipids are used during metamorphosis. Fed larvae accumulated lipid (mean 275.49 ng) with TG and PL being the major energetic and structural lipids, respectively. Larval lipid stores were not appreciably depleted by metamorphosis and so were available for the early benthic stage juvenile. Juveniles started their benthic existence with 314 ng total lipid (TG: mean 46.84 ng, 14.9% of total, PL: mean 137.51 ng, 43.67% of total). Nile Red histochemistry and histology showed that the stomach serves as a nutrient storage organ and, that lipid stores accrued by larvae sustain developing juveniles for up to 4 days post settlement. Triglyceride supported both non-feeding stages of development and the prefeeding larval and perimetamorphic benthic stage. In this first study of lipid stores in settlement stage echinoderm larvae, we show that T. gratilla larvae sequester the same major energetic lipid (TG) to support the early juvenile that the female parent provided them to fuel early development.

References

  1. Allen JD, Zakas C, Podolsky RD (2006) Effects of egg size reduction and larval feeding on juvenile quality for a species with facultative-feeding development. J Exp Mar Biol Ecol 331:186–197CrossRefGoogle Scholar
  2. Bochenek EA, Klink JM, Powell EN, Hofmann EE (2001) A biochemically based model of the growth and development of Crassotrea gigas larvae. J Shellfish Res 20:243–265Google Scholar
  3. Byrne M, Cerra A (2000) Lipid dynamics in the embryos of Patiriella species with divergent modes of development. Dev Growth Differ 42:79–86PubMedCrossRefGoogle Scholar
  4. Byrne M, Villinski J, Popodi E, Cisternas P, Raff R (1999) Maternal factors and the evolution of developmental mode: Evolution of oogenesis in Heliocidaris erythrogramma. Dev Genes Evol 209:275–283PubMedCrossRefGoogle Scholar
  5. Byrne M, Cisternas P, Selvakumaraswamy P, Villinski JT, Raff RR (2003) Evolution of maternal provisioning in ophiuroids, asteroids and echinoids. In: Feral JP, David B (eds) Echinoderm research 2001. A.A. Balkema, Lisse, pp 171–175Google Scholar
  6. Byrne M, Sewell MA, Prowse TAA (2008) Nutritional ecology of sea urchin larvae: influence of endogenous and exogenous nutrition on echinopluteus growth and phenotypic plasticity in Tripneustes gratilla. Funct Ecol 22:643–648CrossRefGoogle Scholar
  7. Carman KR, Thistle D, Ertman SC, Foy M (1991) Nile red as a probe for lipid-storage in benthic copepods. Mar Ecol Prog Ser 74:307–311CrossRefGoogle Scholar
  8. Chen C-P, Run J-Q (1988) Some aspects of rearing larvae and larval development of Tripneustes gratilla (L.) (Echinodermata: Echinoidea). Bull Inst Zool Acad Sin 27:151–157Google Scholar
  9. Chia FS, Burke RD (1978) Echinoderm metamorphosis: fate of larval structures. In: Chia FS, Rice ME (eds) Settlement and metamorphosis of marine invertebrate larvae. Elsevier North Holland Biomedical Press, New York, pp 219–234Google Scholar
  10. Dafni J (1992) Growth rate of the sea urchin Tripneustes gratilla elatensis. Isr J Zool 38:25–33Google Scholar
  11. Dworjanyn SA, Pirozzi I (2008) Induction of settlement in the sea urchin Tripneustes gratilla by macroalgae, diatom biofilms and conspecifics: a role for bacteria? Aquaculture 274:268–274Google Scholar
  12. Dworjanyn SA, Pirozzi I, Liu W (2007) The effect of the addition of algae feeding stimulants to artificial diets for the sea urchin Tripneustes gratilla. Aquaculture 273:624–633CrossRefGoogle Scholar
  13. Ebert TA (1982) Longevity, life history, and relative body wall size in sea urchins. Ecol Monogr 52:353–394CrossRefGoogle Scholar
  14. Emlet RB (1986) Facultative planktotrophy in the tropical echinoid Clypeaster rosaceus (Linnaeus) and a comparison with obligate planktotrophy in Clypeaster subdepressus (Gray) (Clypeasteroida: Echinoidea). J Exp Mar Biol Ecol 95:183–202CrossRefGoogle Scholar
  15. Emlet RB, Sadro SS (2006) Linking stages of life history: how larval quality translates into juvenile performance for an intertidal barnacle (Balanus glandula). Integr Comp Biol 46:334–346CrossRefGoogle Scholar
  16. Falkner I, Byrne M, Sewell MA (2006) Maternal provisioning in Ophionereis fasciata and O. schayeri: brittle stars with contrasting modes of development. Biol Bull 211:204–207PubMedCrossRefGoogle Scholar
  17. Fenaux L, Cellario C, Etienne M (1985) Variations in the ingestion rate of algal cells with morphological development of larvae of Paracentrotus lividus (Echinodermata: Echinoidae). Mar Ecol Prog Ser 24:161–165CrossRefGoogle Scholar
  18. Fenaux L, Strathmann MF, Strathmann RR (1994) 5 tests of food-limited growth of larvae in coastal waters by comparisons of rates of development and form of echinoplutei. Limnol Oceanogr 39:84–98Google Scholar
  19. Gallager SM, Mann R, Sasaki GC (1986) Lipid as an index of growth and viability in three species of bivalve larvae. Aquaculture 56:81–103CrossRefGoogle Scholar
  20. George SB, Cellario C, Fenaux L (1990) Population differences in egg quality of Arbacia lixula (Echinodermata: Echinoidea): Proximate composition of eggs and larval development. J Exp Mar Biol Ecol 141:107–118CrossRefGoogle Scholar
  21. George SB, Young CM, Fenaux L (1997) Proximate composition of eggs and larvae of the sand dollar Encope michelini (Agassiz): the advantage of higher investment in plankotrophic eggs. Invert Reprod Dev 32:11–19Google Scholar
  22. Gosselin P, Jangoux M (1998) From competent larva to exotrophic juvenile: a morphofunctional study of the perimetamorphic period of Paracentrotus lividus (Echinodermata, Echinoida). Zoomorphology 118:31–43CrossRefGoogle Scholar
  23. Hart MW (1995) What are the costs of small egg size for a marine invertebrate with a feeding planktonic larva? Amer Nat 146:415–426CrossRefGoogle Scholar
  24. Hart MW (1996) Evolutionary loss of larval feeding: development, form and function in a facultatively feeding larva, Brisaster latifrons. Evolution 50:174–187CrossRefGoogle Scholar
  25. Hentschel B, Emlet RB (2000) Metamorphosis of barnacle nauplii: effects of food variability and a comparison with amphibian models. Ecology 81:3495–3508Google Scholar
  26. Herrera JC, McWeeney SK, McEdward LR (1996) Diversity of energetic strategies among echinoid larvae and the transition from feeding to nonfeeding development. Oceanol Acta 19:313–321Google Scholar
  27. 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 Assoc UK 51:659–668CrossRefGoogle Scholar
  28. Imagawa S, Nakano Y, Watanabe T (2004) Molecular analysis of a major soluble egg protein in the scleractinian coral Favites chinensis. Comp Biochem Physiol B 137:11–19PubMedCrossRefGoogle Scholar
  29. Jaeckle WB (1995) Variation in the size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development. In: McEdward LR (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 49–77Google Scholar
  30. Juinio-Menez MA, Macawaris N, Bangi H (1998) Community-based sea urchin (Tripneustes gratilla) grow-out culture as a resource management tool. Can Spec Pub Fish Aquat Sci 125:393–399Google Scholar
  31. Koike I, Mukai H, Nojima S (1987) The role of the sea urchin Tripneustes gratilla (Linnaeus), in decomposition and nutrient cycling in a tropical sea grass bed. Ecol Res 2:19–29CrossRefGoogle Scholar
  32. Kozhina VP, Terekhova TA, Svetashev VI (1978) Lipid composition of gametes and embryos of the sea urchin Strongylocentrotus intermedius at early stages of development. Dev Biol 62:512–517PubMedCrossRefGoogle Scholar
  33. Lawrence JM, Agatsuma Y (2007) Ecology of Tripneustes. In: Lawrence JM (ed) The biology and ecology of edible urchins. Elsevier Science, Amsterdam, pp 499–520Google Scholar
  34. Lawrence JM, Bazhin A (1998) Life-history strategies and the potential of sea urchins for aquaculture. J Shellfish Res 17:1515–1522Google Scholar
  35. Lamare MD, Barker MF (1999) In situ estimates of larval development and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea). Mar Ecol Prog Ser 180:197–211CrossRefGoogle Scholar
  36. Lessios HA, Kane J, Robertson DR (2003) Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 57:2026–2036PubMedGoogle Scholar
  37. López S, Turon X, Montero E, Palacín C, Duarte CM, Tarjuelo I (1998) Larval abundance, recruitment and early mortality in Paracentrotus lividus (Echinoidea), interannual variability and plankton-benthos coupling. Mar Ecol Prog Ser 172:239–251CrossRefGoogle Scholar
  38. Liu H, Kelly MS, Cook EJ, Black K, Orr H, Zhu JX, Dong SL (2007) The effect of diet type on growth and fatty acid composition of the sea urchin larvae, II. Psamechinus miliaris (Gmelin). Aquaculture 264:263–278CrossRefGoogle Scholar
  39. Marshall DJ, Keough MJ (2006) Complex life cycles and offspring provisioning in marine invertebrates. Integr Comp Biol 46:643–651CrossRefGoogle Scholar
  40. McEdward LR, Miner BG (2006) Estimation and interpretation of egg provisioning in marine invertebrates. Integr Comp Biol 46:224–232CrossRefGoogle Scholar
  41. McClintock JB, Baker BJ (1997) Palatability and chemical defence of eggs, embryos and larvae of shallow-water Antarctic marine invertebrates. Mar Ecol Prog Ser 154:121–131CrossRefGoogle Scholar
  42. Metzman MS, Mastroianni A, Strauss JF (1978) Fatty acid composition of unfertilized and fertilized eggs of the sea urchin, Arbacia punctulata. Lipids 13:823–824PubMedCrossRefGoogle Scholar
  43. Meyer E, Green AJ, Moore M, Manahan DT (2007) Food availability and physiological state of sea urchin larvae (Strongylocentrotus purpuratus). Mar Biol 152:179–191CrossRefGoogle Scholar
  44. Miles CM, Hadfield MG, Wayne ML (2007) Heritability for egg size in the serpulid polychaete Hydroides elegans. Mar Ecol Prog Ser 340:155–162CrossRefGoogle Scholar
  45. Miller BA, Emlet RB (1999) Development of newly metamorphosed juvenile sea urchins (Strongylocentrotus franciscanus and S. purpuratus): morphology, the effects of temperature and larval food ration, and a method for determining age. J Exp Mar Biol Ecol 235:67–90CrossRefGoogle Scholar
  46. Miner BG, Vonesh JR (2004) Effects of fine grain environmental variability on morphological plasticity. Ecol Lett 7:794–801CrossRefGoogle Scholar
  47. Miner BG, McEdward LA, McEdward LR (2005) The relationship between egg size and the duration of the facultative feeding period in marine invertebrate larvae. J Exp Mar Biol Ecol 321:135–144CrossRefGoogle Scholar
  48. Moran A, Emlet RB (2001) Offspring size and performance in variable environments: field studies on a marine snail. Ecology 82:1597–1612Google Scholar
  49. Moran AL, Manahan DT (2003) Energy metabolism during larval development of green and white abalone, Haliotis fulgensi and H. sorenseni. Biol Bull 204:270–277PubMedCrossRefGoogle Scholar
  50. Olson RR, Olson MH (1989) Food limitation of planktotrophic marine invertebrate larvae: does it control recruitment success? Annu Rev Ecol Syst 20:225–247Google Scholar
  51. 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 44:722–731CrossRefGoogle Scholar
  52. Parrish CC (1999) Determination of total lipid, lipid classes, and fatty acids in aquatic samples. In: Arts MT (ed) Lipids in freshwater ecosystems. Springer, New York, pp 4–20Google Scholar
  53. Pechenik JA (2006) Larval experience and latent effects - metamorphosis is not a new beginning. Integr Comp Biol 46:323–333CrossRefGoogle Scholar
  54. Pechenik JA, Wendt DE, Jarrett JN (1998) Metamorphosis is not a new beginning. Bioscience 48:901–910CrossRefGoogle Scholar
  55. Pernet F, Tremblay R, Langdon C, Bourget E (2004) Effect of additions of dietary triacylglycerol microspheres on growth, survival, and settlement of mussel (Mytilus sp.) larvae. Mar Biol 144:693–703CrossRefGoogle Scholar
  56. Pernet F, Bricelj VM, Cartier S (2006) Lipid class dynamics during larval ontogeny of sea scallops, Placopecten magellanicus, in relation to metamorphic success and response to antibiotics. J Exp Mar Biol Ecol 329:265–280CrossRefGoogle Scholar
  57. Phillips NE (2002) Metamorphosis of barnacle nauplii: Effects of nutrition-mediated larval condition on juvenile performance. Ecology 83:2562–2574CrossRefGoogle Scholar
  58. Podolsky RD, Moran AL (2006) Integrating function across marine life cycles. Integr Comp Biol 46:577–586CrossRefGoogle Scholar
  59. Podolsky RD, Virtue P, Hamilton T, Vavra J, Manahan DT (1994) Energy metabolism during development of the antarctic sea urchin Sterechinus neumayeri. Antarct J US 29:157–158Google Scholar
  60. Powell EN, Bochenek EA, Klink JM, Hofmann EE (2004) Influence of short-term variations in food on survival of Crassostrea gigas larvae: a modelling study. J Mar Res 62:117–152CrossRefGoogle Scholar
  61. Prowse TAA, Sewell MA, Byrne M (2008) Fuels for development: evolution of maternal provisioning in asterinid sea stars. Mar Biol 153:337–349CrossRefGoogle Scholar
  62. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  63. Reitzel AM, Webb J, Arellano S (2004) Growth, development and condition of Dendraster excentricus (Eschscholtz) larvae reared on natural and laboratory diets. J Plankton Res 26:901–990CrossRefGoogle Scholar
  64. Scheibling RE, Mladenov PV (1987) The decline of the sea urchin, Tripneustes ventricosus fishery of Barbados: a survey of fisherman and consumers. Mar Fish Rev 49:62–69Google Scholar
  65. Schiopu D, George SB, Castell J (2006) Ingestion rates and dietary lipids affect growth and fatty acid composition of Dendraster excentricus larvae. J Exp Mar Biol Ecol 328:47–75CrossRefGoogle Scholar
  66. Sewell MA (2005) Utilization of lipids during early development of the sea urchin Evechinus chloroticus. Mar Ecol Prog Ser 304:133–142CrossRefGoogle Scholar
  67. Sewell MA, Manahan DT (2001) Echinoderm eggs: biochemistry and larval biology. In: Barker M (ed) Echinoderms 2000. Swets & Zeitlinger, Lisse, pp 55–58Google Scholar
  68. Sewell MA, Young CM (1997) Are echinoderm egg size distributions bimodal? Biol Bull 193:297–305CrossRefGoogle Scholar
  69. 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 309:219–237CrossRefGoogle Scholar
  70. Shimabukuro S (1991) Tripneustes gratilla. In: Shokita S, Yamaguchi M, Masashi M (eds) Aquaculture in tropical areas. Midori Shobo, Tokyo, pp 313–328Google Scholar
  71. 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 106:119–127CrossRefGoogle Scholar
  72. Strathmann RR, Fenaux L, Strathmann MF (1992) Heterochronic developmental plasticity in larval sea-urchins and its implications for evolution of nonfeeding larvae. Evolution 46:972–986CrossRefGoogle Scholar
  73. Vaïtilingon D (2004) The biology and ecology of the echinoid Tripneustes gratilla (Linnaeus, 1758) off Toliara (Madagascar): feeding, reproduction, larval development, population dynamics and parasitism. Ph.D. hesis, Université libre de BruxellesGoogle Scholar
  74. Vaïtilingon D, Morgan R, Grosjean P, Gosselin P, Jangoux M (2001) Effects of delayed metamorphosis and food rations on the perimetamorphic events in the echinoid Paracentrotus lividus (Lamarck, 1816) (Echinodermata). J Exp Mar Biol Ecol 262:41–60CrossRefGoogle Scholar
  75. Vaïtilingon D, Rasolofonirina R, Jangoux M (2003) Feeding preferences, seasonal gut repletion indices, and diel feeding patterns of the sea urchin Tripneustes gratilla (Echinodermata: Echinoidea) on a coastal habitat off Toliara (Madagascar). Mar Biol 143:45–458CrossRefGoogle Scholar
  76. Vaïtilingon D, Rasolofonirina R, Jangoux M (2005) Reproductive cycle of edible echinoderms from the Southwestern Indian Ocean I. Tripneustes gratilla L. (Echinodermata: Echinoidea). Western Indian Ocean J Mar Sci 4:47–60Google Scholar
  77. Vance RR (1973) On reproductive strategies in marine benthic invertebrates. Am Nat 107:339–352CrossRefGoogle Scholar
  78. Villinski JT, Villinski JC, Byrne M, Raff RA (2002) Convergent maternal provisioning and life-history evolution in echinoderms. Evolution 56:1764–1775PubMedGoogle Scholar
  79. Yasumasu I, Hino A, Suzuki A, Mita M (1984) Change in the triglyceride level in sea urchin eggs and embryos during early development. Dev Growth Differ 26:525–532CrossRefGoogle Scholar
  80. Yokota Y, Kato KH, Mita M (1993) Morphological and biochemical studies on yolk degradation in the sea urchin, Hemicentrotus pulcherrimus. Zool Sci 10:661–670Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • M. Byrne
    • 1
  • T. A. A. Prowse
    • 1
  • M. A. Sewell
    • 2
  • S. Dworjanyn
    • 3
  • J. E. Williamson
    • 4
  • D. Vaïtilingon
    • 4
    • 5
  1. 1.Anatomy and Histology, Bosch Institute, F13University of SydneySydneyAustralia
  2. 2.School of Biological SciencesUniversity of AucklandAucklandNew Zealand
  3. 3.National Marine Science CentreUniversity of New England and Southern Cross UniversityCoffs HarbourAustralia
  4. 4.Marine Ecology GroupMacquarie UniversitySydneyAustralia
  5. 5.Laboratoire de Biologie MarineUniversité Libre de BruxellesBrusselsBelgium

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