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The environmental control of reproductive processes is central to both fundamental and applied aspects of animal ecology. The present study experimentally assessed how environmental factors modulate gametogenesis and spawning and impact embryo development and survival in the holothuroid Cucumaria frondosa, a cold-water echinoderm with lecithotrophic development. Adults were exposed to three seawater temperatures, four photoperiod regimes, and two food concentrations during 120 days overlapping the natural gametogenic and spawning periods. Among all the treatments tested, exposure to ambient conditions of water temperature (−1 to 3 °C), photoperiod (8 to 13 h of light) and food concentration (3 × 103 ± 896 rotifers g−1 of sea cucumbers d−1) yielded the greatest reproductive output and embryo survival. At pre-spawning, males and females had the highest gonad index (~33%) and where filled with mature gametes. At spawning, females in ambient conditions released the highest number of oocytes (1.2 × 103 oocytes female−1) and yielded the highest embryo survival rates (21% at 20 days post fertilization). Individuals exposed to warmer water temperatures (6 and 12 °C) experienced delayed gametogenesis and did not spawn. Individuals under 24-h light, 24-h dark, and advanced (4 months) photoperiods showed delayed gametogenesis and low numbers of oocytes released; moreover, embryos died within 10 days post fertilization. Individuals fed with high food concentration (6 × 103 ± 982 rotifers g−1 of sea cucumbers d−1) showed similar results to ambient conditions, suggesting that increased food supply neither decreased nor enhanced reproductive output over the experimental period. This study sheds new light on the environmental drivers of reproductive success in C. frondosa, which is of value for developing conservation strategies and mariculture protocols in cold-water holothuroids with lecithotrophic development.

The present study investigated methods to trigger spawning and artificially induce oocyte maturation in the commercial cold-water suspension-feeding sea cucumber Cucumaria frondosa. Spawning occurred after exposure to live phytoplankton, commercial phytoplankton paste, and conspecific sperm. Live phytoplankton at 1 × 105 cells ml−1 induced the highest proportion of females to spawn (mean of 56%); promoted the greatest oocyte release (mean of 19,200 oocytes female−1), best quality of eggs and highest survival of embryos (65%; 20 d post fertilization). More concentrated live phytoplankton (1 × 106 cells ml−1) triggered 43% of the females to release ~16,100 oocytes female−1 and survival rates 20 d post fertilization were lower (50%). Both phytoplankton paste treatments (1 × 105 and 1 × 106 cells ml−1) yielded intermediate results in terms of percent spawning females (26%), abundance of oocytes released (11,000 and 7300 oocytes female−1, respectively), quality of eggs, and survival of embryos (44 and 50%, respectively). Sperm from conspecific (2 and 10 × 106 spermatozoa ml−1) induced the lowest proportion of females to spawn (16%) with release of 3000 and 1700 oocytes female−1, respectively; furthermore, all embryos died within 10 d post fertilization. Results for males were slightly different: spawning was more frequent (63%) in the sperm treatment at 2 × 106 spermatozoa ml−1 followed by live phytoplankton at 1 × 106 and 1 × 105 cells ml−1 (43%), and phytoplankton paste at 1 × 105 cells ml−1 (46%); the lowest spawning success was observed for phytoplankton paste at 1 × 106 cells ml−1 and conspecific sperm at 10 × 106 spermatozoa ml−1 (26%). Thermal shock, desiccation, potassium chloride (injection or bath), and serotonin (injection) did not induce spawning in C. frondosa. When oocytes isolated from mature ovaries were exposed to three different concentrations of 1-Methyladenine (1-MA), Dithiothreitol (DTT), 2,3-Dimercapto-1-propanol (BAL), and L-cysteine (L-cyst), DTT at 10−1 M induced the highest proportion of oocytes (48%) to shed follicle cells (i.e. ovulate); whereas other treatments induced only 2–6% of ovulation, similar to the control (seawater). All oocytes that shed follicle cells remained unfertilizable. Overall, live phytoplankton emerged as the most suitable spawning trigger for C. frondosa, a Dendrochirotida that produces maternally-provisioned oocytes. In the context of expanding sea cucumber aquaculture, this finding provides a tool to maximize the availability of gametes in this cold-water species, with possible applicability to similar commercial dendrochitotids.

The present study examined morphological and behavioural development in post-settled juveniles of the commercial sea cucumber Cucumaria frondosa, in an effort to assist captive breeding and conservation initiatives. Juveniles developed all 10 tentacles within 16 months; they had 9 podia and measured 4.6 mm in length after 21 months. Scaling between body length and number of podia was isometric, whereas dorsal tentacle metrics showed negative allometric scaling, indicating that growth was accompanied by a decreasing tentacle to body size ratio. Dorsally-oriented tentacles developed and ramified faster, showing 6 ramifications after 21 months, when ventrally-oriented tentacles only displayed one. This asynchrony underlines the distinctive roles of dorsal vs. ventral tentacles during the early months. The former were strictly used to capture plankton from the water column; whereas the latter were used for anchorage and feeding on deposited material. Ossicles of the body wall increased in length and thickness, and became slightly curved and rounded in older juveniles. Light intensity and water flow tolerance increased with age; from 25 lx and 5 cm s−1 in 1-month-old individuals, to >50 lx and 10 cm s−1 in 6, 12, and 21-month-old individuals, consistent with migration from sheltered to more exposed locations. Moreover, 1 and 6-month-old juveniles preferred rock substrates and black or red background colours; whereas 12 and 21-monthd-old individuals favoured substrates of coralline algae and a red background, also indicative of increasing affinity with sunlit environments and a shift from benthic to planktonic feeding. Juveniles of all age classes were feeding (i.e. had deployed tentacles) 24 h a day and commonly sought vertical surfaces. Together, the findings shed light on the early juvenile ecology of this cold-water suspension-feeding sea cucumber. Considering the expansion of sea cucumber fisheries and growing interest in the aquaculture of C. frondosa, this work also provides a framework for improved stock management and culture protocols.

While the suspension-feeding sea cucumber Cucumaria frondosa is commercially exploited in the North Atlantic and is considered to have potential for integrated aquaculture, the impact of environmental conditions on its behaviour and population structure remains incompletely understood. The present study showed that adults are not photosensitive; they do not exhibit any preference for either illuminated or shaded areas. Within each photoperiod treatment, analyses of the daily activity cycle revealed that the proportion of individuals with feeding tentacles deployed did not change over time; however, the proportion of moving individuals increased in the dark phase under the 12 h light/12 dark regime, but remained constant under continuous light or darkness. Hence, from an aquaculture perspective, long days (i.e. summer photoperiod) might decrease the time spent moving in favour of feeding, potentially shifting the energy budget toward faster growth. Variations in phytoplankton concentration modulated the deployment of tentacles but did not trigger any displacement toward the food source, indicating that feeding responds directly to the presence of food. Moreover, C. frondosa exhibited a clear preference for substrates composed of bare rocks and rocks with coralline algae and displayed a weak preference for darker substrate backgrounds. Together, these findings highlight how some key environmental factors can govern the feeding, locomotor activities, and eventual distribution of cold-water suspension-feeding sea cucumbers.