Background For echinoderms with feeding larvae, metamorphic and post-settlement success may be highly dependent on larval nutrition and the accumulation of energetic lipids from the diet. In contrast to the sea urchins, starfish and brittle stars within the Phylum Echinodermata, sea cucumber metamorphosis does not involve formation of a juvenile rudiment, but instead there is a rearrangement of the entire larval body. Successful metamorphosis in sea cucumbers is often associated with the presence in the late auricularia stage of an evolutionary novelty, the hyaline spheres (HS), which form in the base of the larval arms. Known since the 1850s the function of these HS has remained enigmatic—suggestions include assistance with flotation, as an organizer for ciliary band formation during metamorphosis and as a nutrient store for metamorphosis. Results Here using multiple methodologies (lipid mapping, resin-section light microscopy, lipid and fatty acid analyses) we show definitively that the HS are used to store neutral lipids that fuel the process of metamorphosis in Australostichopus mollis . Neutral lipids derived from the phytoplankton diet are transported by secondary mesenchyme cells (“lipid transporting cells”, LTC), likely as free fatty acids or lipoproteins, from the walls of the stomach and intestine through the blastocoel to the HS; here, they are converted to triacylglycerol with a higher saturated fatty acid content. During metamorphosis the HS decreased in size as the triacylglycerol was consumed and LTC again transported neutral lipids within the blastocoel. Conclusion The HS in A. mollis functions as a nutrient storage structure that separates lipid stores from the major morphogenic events that occur during the metamorphic transition from auricularia–doliolaria–pentactula (settled juvenile). The discovery of LTC within the blastocoel of sea cucumbers has implications for other invertebrate larvae with a gel-filled blastocoel and for our understanding of lipid use during metamorphosis in marine invertebrates.
In marine invertebrates with planktotrophic larvae, modelling studies predict that water temperature and food availability are the primary factors influencing oocyte size, with large oocyte sizes being favoured by cold water and low food availability. We examined intraspecific variation in oocyte size in the polychaete Spirobranchus cariniferus in populations from the East and West Coasts of New Zealand's North Island, which differ in temperature and food availability during the reproductive season: the East Coast has consistently warmer seawater temperatures throughout the summer and higher phytoplankton abundance in late summer than the West Coast. A cross-fertilization experiment and DNA sequencing confirmed that Spirobranchus populations on both coasts belong to the same species. Then, analyses of S. cariniferus oocytes from 5 sites per coast revealed that the West Coast population produces oocytes that are on average 14% larger and contain up to 41% more triacylglycerols (TAGs) than the East Coast population. West Coast S. cariniferus oocytes also developed into larger larvae that reached competence 22% sooner than East Coast oocytes and larvae. These intraspecific comparisons of East and West Coast S. cariniferus populations reveal oocyte size to differ substantially even among populations that are probably not fully isolated, consistent with predictions of life history models. We estimate that genetic divergence may be responsible for up to 58% of the difference in oocyte size between East and West Coast populations, and that oocyte size may be subject to local adaptation to temperature and, to a lesser extent, food availability differences between coasts.
Reproductive aspects of the sea cucumber Athyonidium chilensis were studied over a year in Valdivia, Chile, through gonad index (GI) analysis, macro- and microscopic analysis of the gonads, fecundity and size at first sexual maturity estimations. We also explored the reliability of live size estimators for their use in fisheries. Athyonidium chilensis showed continuous gametogenesis and spawning individuals could be found throughout the year. However, spring was the main reproductive time, where an important GI decrease coincided with enhanced spawning activity evidenced through histology. GIs recovered in summer, and new signs of enhanced spawning activity were observed towards autumn (April 2008). GI peaks were observed in August 2007 and March 2008 for females (22.8 and 24.4% respectively) and September 2007 and March 2008 for males (31.9 and 25.9% respectively). Low mean GIs occurred in May and December 2007 for females (15.2 and 11.6% respectively) and May and October 2007 for males (12.7 and 14.1% respectively). Males reached sexual maturity at a smaller size than females (males: 21.2 g, females: 43.7 g eviscerated weight), and mature females showed a high mean absolute fecundity for a species with lecithotrophic larval development (6.31 × 105 ± 1.97 × 105 SD). For fisheries, we recommend a minimum catch size over 237.89 g drained weight to ensure that caught individuals are sexually mature. This study provides relevant information for the conservation and fishery management of A. chilensis. Continuous gametogenesis and high fecundity make this species particularly suitable for aquaculture in southern Chile.
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