Marine Biology

, 164:178 | Cite as

Maternal investment and nutrient utilization during early larval development of the sea cucumber Australostichopus mollis

  • Josefina Peters-Didier
  • Mary A. SewellEmail author
Original paper


Echinoderms are widely used to investigate the relationship between egg size, energy content and larval developmental strategies in marine invertebrates; although there have been few studies on ophiuroids and holothuroids. In this paper, we provide the first detailed biochemical information on egg composition and utilization in the planktotrophic holothuroid, Australostichopus mollis. The egg ultrastructure, protein content (85.1 ng egg−1) and lipid:protein ratio of 0.42 were consistent with those of other planktotrophic echinoderms of similar egg size. However, the lipid content (35.6 ng egg−1) was outside the 95% prediction band for the relationship between egg size and lipid content for echinoderms. Triacylglycerol (TAG) was the main energetic lipid present in the egg, with ca 50% of the TAG being utilized to construct the feeding auricularia; the remaining TAG was estimated to be consumed over 114.8 h (4.8 days) of development. Feeding a microalgal diet during early larval development did not affect the rate of TAG utilization, but increased protein content in the 90-h auricularia. Biochemical information from A. mollis eggs/larvae suggests that TAG might be the ancestral maternally derived energetic lipid in the Echinodermata, but also that there may be different patterns of lipid utilization between different classes.



We greatly appreciate the help with sea cucumber collections, lipid/protein analysis and microscopy from Adrian Turner, Erica Zarate, Angela Little and Emily Douglas. We gratefully acknowledge the comments of the three anonymous reviewers, which have greatly improved the manuscript, and the statistical advice of Dr. Katya Ruggiero during the manuscript revision. This research was also supported by a Chilean Government scholarship (Becas-Chile, National Commission for Scientific and Technological Research, CONICYT) awarded to JPD.

Compliance with ethical standards

Conflict of interest

The authors declare they have no conflict of interest.

Ethical approval

All applicable guidelines for the care and use of animals were followed.

Supplementary material

227_2017_3209_MOESM1_ESM.pdf (304 kb)
Supplementary material 1 (PDF 303 kb)


  1. Agudo N (1996) Sandfish hatchery techniques. Secretariat of the Pacific Community, NoumeaGoogle Scholar
  2. Archer JE (1996) Aspects of the reproductive and larval biology and ecology of the temperate holothurian Stichopus mollis (Hutton). MSc dissertation, University of Auckland, New ZealandGoogle Scholar
  3. Bertram DF, Strathmann RR (1998) Effects of maternal and larval nutrition on growth and form of planktotrophic larvae. Ecology 79:315–327CrossRefGoogle Scholar
  4. Byrne M (1989) Ultrastructure of the ovary and oogenesis in the ovoviviparous brittlestar Ophiolepis paucispina. (Echinodermata: Ophiuroidea). Biol Bull 176:79–95CrossRefGoogle Scholar
  5. Byrne M (1991) Reproduction, development and population biology of the Caribbean ophiuroid Ophionereis olivacea, a protandric hermaphrodite that broods its young. Mar Biol 111:387–399CrossRefGoogle Scholar
  6. Byrne M, Cerra A (2000) Lipid dynamics in the embryos of Patiriella species (Asteroidea) with divergent modes of development. Dev Growth Differ 42:79–86CrossRefGoogle Scholar
  7. Byrne M, Cerra A, Villinski JT (1999) Oogenic strategies in the evolution of development in Patiriella (Echinodermata: Asteroidea). Invert Reprod Develop 36:195–202CrossRefGoogle Scholar
  8. Byrne M, Selvakumaraswamy P, Villinski JT, Raff RA (2003) Evolution of maternal provisioning in ophiuroids, asteroids and echinoids. In: David B (ed) Feral JP. Echinoderm Research AA Balkema, Lisse, pp 171–175Google Scholar
  9. Byrne M, Prowse TAA, Sewell MA, Dworjanyn S, Williamson JE, Vaïtilingon D (2008a) Maternal provisioning for larvae and larval provisioning for juveniles in the toxopneustid sea urchin Tripneustes gratilla. Mar Biol 155:473–482CrossRefGoogle Scholar
  10. Byrne M, Sewell MA, Prowse TAA (2008b) Nutritional ecology of sea urchin larvae: influence of endogenous and exogenous nutrition on echinopluteal growth and phenotypic plasticity in Tripneustes gratilla. Funct Ecol 22:643–648CrossRefGoogle Scholar
  11. Christie WW (2014) AOCS lipid library
  12. D’Amico F (2005) A polychromatic staining method for epoxy embedded tissue: a new combination of methylene blue and basic fuchsine for light microscopy. Biotech Histochem 80:207–210CrossRefGoogle Scholar
  13. Delmas RP, Parrish CC, Ackman RG (1984) Determination of lipid class concentrations in sea water by Thin-Layer Chromatography with Flame Ionization Detection. Anal Chem 56:1272–1277CrossRefGoogle Scholar
  14. Eckert GL (1995) A novel larval feeding strategy of the tropical sand dollar, Encope michelini (Agassiz): adaptation to food limitation and an evolutionary link between planktotrophy and lecithotrophy. J Exp Mar Biol Ecol 187:103–128CrossRefGoogle Scholar
  15. Emlet R (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
  16. Emlet R, McEdward L, Strathmann R (1987) Echinoderm larval ecology viewed from the egg. In: Jangoux M, Lawrence J (eds) Echinoderm studies 2. Balkema, Rotterdam, pp 55–136Google Scholar
  17. Falkner I (2007) Evolution of maternal provisioning in ophiuroids: characterisation of egg nutrients and their roles in development. PhD dissertation, University of Sydney, AustraliaGoogle Scholar
  18. Falkner I, Byrne M, Sewell MA (2006) Maternal provisioning in Ophionereis fasciata and O. schayeri: brittle stars with contrasting modes of development. Biol Bull 211:204–207CrossRefGoogle Scholar
  19. Falkner I, Barbosa S, Byrne M (2013) Reproductive biology of four ophiocomid ophiuroids in tropical and temperate Australia—reproductive cycle and oogenic strategies in species with different modes of development. Invert Reprod Develop 57:189–199CrossRefGoogle Scholar
  20. Falkner I, Sewell MA, Byrne M (2015) Evolution of maternal provisioning in ophiuroid echinoderms: characterisation of egg composition in planktotrophic and lecithotrophic developers. Mar Ecol Prog Ser 525:1–13CrossRefGoogle Scholar
  21. George SB (1990) Population and seasonal differences in egg quality of Arbacia lixula (Echinodermata: Echinoidea). Invert Reprod Dev 17:111–121. doi: 10.1080/07924259.1990.9672098 CrossRefGoogle Scholar
  22. George SB (1999) Egg quality, larval growth and phenotypic plasticity in a forcipulate seastar. J Exp Mar Biol Ecol 237:203–224CrossRefGoogle Scholar
  23. 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 32:11–19CrossRefGoogle Scholar
  24. Grange LT, Tyler PA, Peck LS, Cornelius N (2004) Longterm interannual cycles of the gametogenic ecology of the Antarctic brittle-star Ophionoctus victoriae. Mar Ecol Prog Ser 278:141–155CrossRefGoogle Scholar
  25. Harwood JL (2012) Lipid metabolism. In: Gunstone FD, Harwood JL, Dijkstra AJ (eds) The lipid handbook with CD room. CRC Press, Boca Raton, pp 637–702Google Scholar
  26. Ito S, Kitamura H (1997) Induction of larval metamorphosis in the sea cucumber Stichopus japonicus by periphitic diatoms. Hydrobiologia 358:281–284CrossRefGoogle Scholar
  27. Jaeckle WB (1995) Variation in size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development. In: McEdward LR (ed) Marine invertebrate larvae. CRC, Boca Raton, pp 49–77Google Scholar
  28. Jaeckle WB, Manahan DT (1989) Growth and energy imbalance during the development of a lecithotrophic molluscan larva (Haliotis rufescens). Biol Bull 177:237–246CrossRefGoogle Scholar
  29. Kato S, Tsurumaru S, Taga M, Yamane T, Shibata Y, Ohno K, Fujiwara A, Yamano K, Yoshikuni M (2009) Neuronal peptides induce oocyte maturation and gamete spawning of sea cucumber, Apostichopus japonicus. Dev Biol 326:169–176CrossRefGoogle Scholar
  30. Kessel RG (1966) Some observations on the ultrastructure of the oocyte of Thyone briareus with special reference to the relationship of the Golgi complex and endoplasmic reticulum in the formation of yolk. J Ultra R 16:305–319CrossRefGoogle Scholar
  31. Lacalli T (2003) Developmental biology: a larval revelation. Nature 421:120–121CrossRefGoogle Scholar
  32. Lee RF (1991) Lipoproteins from the hemolymph and ovaries of marine invertebrates. In: Gilles R (ed) Advances in comparative and environmental physiology, vol 7. Springer, Berlin, pp 187–207CrossRefGoogle Scholar
  33. Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306CrossRefGoogle Scholar
  34. Leonet A, Rasolofonirina R, Wattiez R, Jangoux M, Eeckhaut I (2009) A new method to induce oocyte maturation in holothuroids (Echinodermata). Invert Reprod Dev 53:13–21CrossRefGoogle Scholar
  35. Levitan DR (2000) Optimal egg size in marine invertebrates: theory and phylogenetic analysis of the critical relationship between egg size and development time in echinoids. Am Nat 156:175–192CrossRefGoogle Scholar
  36. Matsuura H, Yazaki I, Okino T (2009) Induction of larval metamorphosis in the sea cucumber Apostichopus japonicus by neurotransmitters. Fish Sci 75:777–783CrossRefGoogle Scholar
  37. McAlister JS, Moran AL (2012) Relationships among egg size, composition, and energy: a comparative study of geminate sea urchins. PLoS One 7:e41599CrossRefGoogle Scholar
  38. McEdward LR (1997) Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktotrophic larvae. Am Nat 150:48–72. doi: 10.1086/286056 CrossRefGoogle Scholar
  39. McEdward LR, Miner BG (2006) Estimation and interpretation of egg provisioning in marine invertebrates. Integr Comp Biol 46:224–232CrossRefGoogle Scholar
  40. Meyer E, Green A, Moore M, Manahan D (2007) Food availability and physiological state of sea urchin larvae Strongylocentrotus purpuratus. Mar Biol 152:179–191CrossRefGoogle Scholar
  41. 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
  42. Moloney P, Byrne M (1994) Histology and ultrastructure of the ovaries and oogenesis in the ophiuroid Ophionereis schayeri. In: David B, Guille A, Feral J-P, Roux M (eds) Echinoderms through time. AA Balkema, Rotterdam, pp 463–469Google Scholar
  43. Moran AL, McAlister JS, Whitehill EAG (2013) Eggs as energy: revisiting the scaling of egg size and energetic content among echinoderms. Biol Bull 224:184–191CrossRefGoogle Scholar
  44. Morgan AD (2008) The effect of food availability on phenotypic plasticity in larvae of the temperate sea cucumber Australostichopus mollis. J Exp Mar Biol Ecol 363:89–95CrossRefGoogle Scholar
  45. Morgan AD (2009) Spawning of the temperate sea cucumber, Australostichopus mollis (Levin). J World Aquacult Soc 40:363–373CrossRefGoogle Scholar
  46. Nakano H, Hibino T, Oji T, Hara Y, Amemiya S (2003) Larval stages of a living sea lily (stalked crinoid echinoderm). Nature 421:158–160CrossRefGoogle Scholar
  47. Pace DA, Manahan DT (2007) Efficiencies and costs of larval growth in different food environments (Asteroidea: Asterina miniata). J Exp Mar Biol Ecol 353:89–106CrossRefGoogle Scholar
  48. Parrish CC (1987) Separation of aquatic lipid classes by chromarod thin-layer chromatography with measurement by Iatroscan flame ionization detection. Can J Fish Aquat Sci 44:722–731CrossRefGoogle Scholar
  49. Pawson DL (1970) The marine fauna of New Zealand: sea cucumbers (Echinodermata: Holothuroidea). New Zealand Oceanographic Institute Memoir 52Google Scholar
  50. Podolsky RD, Strathmann RR (1996) Evolution of egg size in free-spawners: consequences of the fertilization-fecundity trade-off. Am Nat 148:160–173. doi: 10.2307/2463076 CrossRefGoogle Scholar
  51. 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 29:157Google Scholar
  52. Prowse TAA, Sewell MA, Byrne M (2008) Fuels for development: evolution of maternal provisioning in asterinid sea stars. Mar Biol 153:337–349CrossRefGoogle Scholar
  53. Prowse TAA, Falkner I, Sewell MA, Byrne M (2009) Long-term storage lipids and developmental evolution in echinoderms. Evol Ecol Res 11:1069–1083Google Scholar
  54. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  55. Ramofafia C, Battaglene SC, Bell JD, Byrne M (2000) Reproductive biology of the commercial sea cucumber Holothuria fuscogilva in the Solomon Islands. Mar Biol 136:1045–1056CrossRefGoogle Scholar
  56. Reich A, Dunn C, Akasaka K, Wessel G (2015) Phylogenomic analyses of Echinodermata support the sister groups of Asterozoa and Echinozoa. PLoS One 10(3):e0119627CrossRefGoogle Scholar
  57. Sewell MA (1990) Aspects of the ecology of Stichopus mollis (Echinodermata: Holothuroidea) in north-eastern New Zealand. N Z J Mar Fresh 24:87–93CrossRefGoogle Scholar
  58. Sewell MA (1992) Reproduction of the temperate Aspidochirote Stichopus mollis (Echinodermata: Holothuroidea) in New Zealand. Ophelia 25:103–121CrossRefGoogle Scholar
  59. Sewell MA (2005) Utilization of lipids during early development of the sea urchin Evechinus chloroticus. Mar Ecol Prog Ser 304:133–142CrossRefGoogle Scholar
  60. Sewell MA, Chia FS (1994) Reproduction of the intraovarian brooding apodid Leptosynapta clarki (Echinodermata: Holothuroidea) in British Columbia. Mar Biol 121:285–300CrossRefGoogle Scholar
  61. Sewell MA, Manahan DT (2001) Echinoderm eggs: biochemistry and larval biology. In: Barker M (ed) Echinoderms 2000: proceedings of the 10th international conference, Dunedin, New Zealand. Swets and Zeitlinger, Lisse, pp 55–58Google Scholar
  62. Sewell MA, Young CM (1997) Are echinoderm egg size distributions bimodal? Biol Bull 193:297–305CrossRefGoogle Scholar
  63. Sun X, Li Q (2012) Effects of temporary starvation on larval growth, survival and development of the sea cucumber Apostichopus japonicus. Mar Biol Res 8:771–777CrossRefGoogle Scholar
  64. Sun X, Li Q (2014) Effects of delayed first feeding on larval growth, survival and development of the sea cucumber Apostichopus japonicus (Holothuroidea). Aquacult Res 45:278–288CrossRefGoogle Scholar
  65. Telford MJ, Lowe CJ, Cameron CB, Ortega-Martinez O, Aronowicz J, Oliveri P, Copley RR (2014) Phylogenomic analysis of echinoderm class relationships supports Asterozoa. Proc R Soc B 281:20140479CrossRefGoogle Scholar
  66. Tyler PA, Gage JD (1979) Reproductive ecology of deep-sea ophiuroids from the Rockall Trough. In: Naylor E, Hartnoll RG (eds) Cyclic phenomena in marine plants and animals: proceedings of the 13th European marine biology symposium. Pergamon Press, Oxford, pp 215–222CrossRefGoogle Scholar
  67. Villinski JT, Villinski JC, Byrne M, Raff RA (2002) Convergent maternal provisioning and life-history evolution in echinoderms. Evolution 56:1764–1775CrossRefGoogle Scholar
  68. Whitehill EAG, Moran AL (2012) Comparative larval energetics of an ophiuroid and an echinoid echinoderm. Invertebr Biol 131:345–354CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of AucklandAucklandNew Zealand

Personalised recommendations