Sexually unbalanced gonad development and nutrition of the newly range-extended sea urchin Heliocidaris crassispina in the northeastern Honshu, Japan

Ocean warming is increasingly recognized as a leading environmental risk to marine organisms. This phenomenon has led to poleward range extension of the sea urchin Heliocidaris crassispina to Toga Bay along the Oga Peninsula in Japan since 2014. Observations of H. crassispina gonads in maturation–spawning stages suggested delayed spermatogenesis in the new habitats. To determine the effects of ocean warming on H. crassispina, particularly to verify the delay in spermatogenesis and identify its specific cause, we investigated the seasonal changes in gonad development in relation to temperature and the associated carbon and nitrogen contents of the gonad and gut tissues and the gut contents to evaluate the nutritional status of the newly range-extended sea urchins by sex. Heliocidaris crassispina showed a defined gametogenic cycle with a single spawning per sex. The sex ratio was skewed to females (1.27:1). Males exhibited growing gonads during February–May, while females exhibited recovering gonads during February–April. Spermatogenesis was delayed one month compared to oogenesis. Spawning was partially synchronized between the sexes from August to September. A long-term warming trend in annual average and May–August in Toga Bay indicates that H. crassispina is subjected to the low temperature, particularly during winter in new habitat. The carbon/nitrogen (C/N) ratios were lower in the testes than in the ovaries regardless of no sexual differences in the gut from February to October. Although higher total protein content in testes than that of ovaries is required from the recovery to growing stages, N content of gonad showed no significantly sexual difference, suggesting that insufficient protein accumulation in testes suppress spermatogenesis that would be the possible factor of delayed spermatogenesis and partially synchronized spawning between sexes. Female-skewed sex ratio and delayed spermatogenesis suggest the lower possibility of self-reproduction in the newly extended population.