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

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Abstract

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.

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References

  • Agudo N (1996) Sandfish hatchery techniques. Secretariat of the Pacific Community, Noumea

    Google Scholar 

  • 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 Zealand

  • Bertram DF, Strathmann RR (1998) Effects of maternal and larval nutrition on growth and form of planktotrophic larvae. Ecology 79:315–327

    Article  Google Scholar 

  • Byrne M (1989) Ultrastructure of the ovary and oogenesis in the ovoviviparous brittlestar Ophiolepis paucispina. (Echinodermata: Ophiuroidea). Biol Bull 176:79–95

    Article  Google Scholar 

  • Byrne M (1991) Reproduction, development and population biology of the Caribbean ophiuroid Ophionereis olivacea, a protandric hermaphrodite that broods its young. Mar Biol 111:387–399

    Article  Google Scholar 

  • Byrne M, Cerra A (2000) Lipid dynamics in the embryos of Patiriella species (Asteroidea) with divergent modes of development. Dev Growth Differ 42:79–86

    Article  CAS  Google Scholar 

  • Byrne M, Cerra A, Villinski JT (1999) Oogenic strategies in the evolution of development in Patiriella (Echinodermata: Asteroidea). Invert Reprod Develop 36:195–202

    Article  Google Scholar 

  • 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 171–175

    Google Scholar 

  • 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 155:473–482

    Article  Google Scholar 

  • 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 22:643–648

    Article  Google Scholar 

  • Christie WW (2014) AOCS lipid library http://lipidlibrary.aocs.org/index.html

  • 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 80:207–210

    Article  Google Scholar 

  • 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 56:1272–1277

    Article  CAS  Google Scholar 

  • 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 187:103–128

    Article  Google Scholar 

  • 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 95:183–202

    Article  Google Scholar 

  • 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 55–136

    Google Scholar 

  • Falkner I (2007) Evolution of maternal provisioning in ophiuroids: characterisation of egg nutrients and their roles in development. PhD dissertation, University of Sydney, Australia

  • Falkner I, Byrne M, Sewell MA (2006) Maternal provisioning in Ophionereis fasciata and O. schayeri: brittle stars with contrasting modes of development. Biol Bull 211:204–207

    Article  Google Scholar 

  • 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 57:189–199

    Article  Google Scholar 

  • 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 525:1–13

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • George SB (1999) Egg quality, larval growth and phenotypic plasticity in a forcipulate seastar. J Exp Mar Biol Ecol 237:203–224

    Article  Google Scholar 

  • 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 32:11–19

    Article  Google Scholar 

  • 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 278:141–155

    Article  Google Scholar 

  • Harwood JL (2012) Lipid metabolism. In: Gunstone FD, Harwood JL, Dijkstra AJ (eds) The lipid handbook with CD room. CRC Press, Boca Raton, pp 637–702

    Google Scholar 

  • Ito S, Kitamura H (1997) Induction of larval metamorphosis in the sea cucumber Stichopus japonicus by periphitic diatoms. Hydrobiologia 358:281–284

    Article  Google Scholar 

  • 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 49–77

    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 

  • 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 326:169–176

    Article  CAS  Google Scholar 

  • 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 16:305–319

    Article  CAS  Google Scholar 

  • Lacalli T (2003) Developmental biology: a larval revelation. Nature 421:120–121

    Article  CAS  Google Scholar 

  • 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 187–207

    Chapter  Google Scholar 

  • Lee RF, Hagen W, Kattner G (2006) Lipid storage in marine zooplankton. Mar Ecol Prog Ser 307:273–306

    Article  CAS  Google Scholar 

  • Leonet A, Rasolofonirina R, Wattiez R, Jangoux M, Eeckhaut I (2009) A new method to induce oocyte maturation in holothuroids (Echinodermata). Invert Reprod Dev 53:13–21

    Article  Google Scholar 

  • 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 156:175–192

    Article  CAS  Google Scholar 

  • Matsuura H, Yazaki I, Okino T (2009) Induction of larval metamorphosis in the sea cucumber Apostichopus japonicus by neurotransmitters. Fish Sci 75:777–783

    Article  CAS  Google Scholar 

  • McAlister JS, Moran AL (2012) Relationships among egg size, composition, and energy: a comparative study of geminate sea urchins. PLoS One 7:e41599

    Article  CAS  Google Scholar 

  • McEdward LR (1997) Reproductive strategies of marine benthic invertebrates revisited: facultative feeding by planktotrophic larvae. Am Nat 150:48–72. doi:10.1086/286056

    Article  CAS  Google Scholar 

  • McEdward LR, Miner BG (2006) Estimation and interpretation of egg provisioning in marine invertebrates. Integr Comp Biol 46:224–232

    Article  Google Scholar 

  • Meyer E, Green A, Moore M, Manahan D (2007) Food availability and physiological state of sea urchin larvae Strongylocentrotus purpuratus. Mar Biol 152:179–191

    Article  Google Scholar 

  • 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 321:135–144

    Article  Google Scholar 

  • 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 463–469

    Google Scholar 

  • Moran AL, McAlister JS, Whitehill EAG (2013) Eggs as energy: revisiting the scaling of egg size and energetic content among echinoderms. Biol Bull 224:184–191

    Article  CAS  Google Scholar 

  • 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 363:89–95

    Article  Google Scholar 

  • Morgan AD (2009) Spawning of the temperate sea cucumber, Australostichopus mollis (Levin). J World Aquacult Soc 40:363–373

    Article  Google Scholar 

  • Nakano H, Hibino T, Oji T, Hara Y, Amemiya S (2003) Larval stages of a living sea lily (stalked crinoid echinoderm). Nature 421:158–160

    Article  CAS  Google Scholar 

  • Pace DA, Manahan DT (2007) Efficiencies and costs of larval growth in different food environments (Asteroidea: Asterina miniata). J Exp Mar Biol Ecol 353:89–106

    Article  Google Scholar 

  • 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 44:722–731

    Article  CAS  Google Scholar 

  • Pawson DL (1970) The marine fauna of New Zealand: sea cucumbers (Echinodermata: Holothuroidea). New Zealand Oceanographic Institute Memoir 52

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Prowse TAA, Sewell MA, Byrne M (2008) Fuels for development: evolution of maternal provisioning in asterinid sea stars. Mar Biol 153:337–349

    Article  Google Scholar 

  • Prowse TAA, Falkner I, Sewell MA, Byrne M (2009) Long-term storage lipids and developmental evolution in echinoderms. Evol Ecol Res 11:1069–1083

    Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Ramofafia C, Battaglene SC, Bell JD, Byrne M (2000) Reproductive biology of the commercial sea cucumber Holothuria fuscogilva in the Solomon Islands. Mar Biol 136:1045–1056

    Article  Google Scholar 

  • 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):e0119627

    Article  Google Scholar 

  • Sewell MA (1990) Aspects of the ecology of Stichopus mollis (Echinodermata: Holothuroidea) in north-eastern New Zealand. N Z J Mar Fresh 24:87–93

    Article  Google Scholar 

  • Sewell MA (1992) Reproduction of the temperate Aspidochirote Stichopus mollis (Echinodermata: Holothuroidea) in New Zealand. Ophelia 25:103–121

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sewell MA, Chia FS (1994) Reproduction of the intraovarian brooding apodid Leptosynapta clarki (Echinodermata: Holothuroidea) in British Columbia. Mar Biol 121:285–300

    Article  Google Scholar 

  • 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 55–58

    Google Scholar 

  • Sewell MA, Young CM (1997) Are echinoderm egg size distributions bimodal? Biol Bull 193:297–305

    Article  CAS  Google Scholar 

  • Sun X, Li Q (2012) Effects of temporary starvation on larval growth, survival and development of the sea cucumber Apostichopus japonicus. Mar Biol Res 8:771–777

    Article  Google Scholar 

  • 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 45:278–288

    Article  Google Scholar 

  • 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 281:20140479

    Article  Google Scholar 

  • 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 215–222

    Chapter  Google Scholar 

  • Villinski JT, Villinski JC, Byrne M, Raff RA (2002) Convergent maternal provisioning and life-history evolution in echinoderms. Evolution 56:1764–1775

    Article  Google Scholar 

  • Whitehill EAG, Moran AL (2012) Comparative larval energetics of an ophiuroid and an echinoid echinoderm. Invertebr Biol 131:345–354

    Article  Google Scholar 

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Acknowledgements

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.

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  1. School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand

    Josefina Peters-Didier & Mary A. Sewell

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  1. Josefina Peters-Didier
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  2. Mary A. Sewell
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Correspondence to Mary A. Sewell.

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Peters-Didier, J., Sewell, M.A. Maternal investment and nutrient utilization during early larval development of the sea cucumber Australostichopus mollis . Mar Biol 164, 178 (2017). https://doi.org/10.1007/s00227-017-3209-7

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