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J Exp Biol
2024 Jan 15;2272:. doi: 10.1242/jeb.246707.
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Behavioural and physiological impacts of low salinity on the sea urchin Echinus esculentus.
Barrett NJ
,
Harper EM
,
Last KS
,
Reinardy HC
,
Peck LS
.
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Reduced seawater salinity as a result of freshwater input can exert a major influence on the ecophysiology of benthic marine invertebrates, such as echinoderms. While numerous experimental studies have explored the physiological and behavioural effects of short-term, acute exposure to low salinity in echinoids, surprisingly few have investigated the consequences of chronic exposure, or compared the two. In this study, the European sea urchin, Echinus esculentus, was exposed to low salinity over the short term (11‰, 16‰, 21‰, 26‰ and 31‰ for 24 h) and longer term (21, 26 and 31‰ for 25 days). Over the short term, oxygen consumption, activity coefficient and coelomic fluid osmolality were directly correlated with reduced salinity, with 100% survival at ≥21‰ and 0% at ≤16‰. Over the longer term at 21‰ (25 days), oxygen consumption was significantly higher, feeding was significantly reduced and activity coefficient values were significantly lower than at control salinity (31‰). At 26‰, all metrics were comparable to the control by the end of the experiment, suggesting acclimation. Furthermore, beneficial functional resistance (righting ability and metabolic capacity) to acute low salinity was observed at 26‰. Osmolality values were slightly hyperosmotic to the external seawater at all acclimation salinities, while coelomocyte composition and concentration were unaffected by chronic low salinity. Overall, E. esculentus demonstrate phenotypic plasticity that enables acclimation to reduced salinity around 26‰; however, 21‰ represents a lower acclimation threshold, potentially limiting its distribution in coastal areas prone to high freshwater input.
Fig. 1. Oxygen consumption of Echinus esculentus 2 h after transfer from ambient salinity (31‰). Results are shown for Kruskal–Wallis and post hoc Dunn’s test, with different letters indicating significant differences (P<0.05; n=10 biological replicates for each treatment) between treatments. Box plots show medians (black line), upper and lower quartiles, and maximum and minimum (whiskers). Means are represented by open circles and outliers by filled circles. AFDM, ash-free dry mass.
Fig. 2. Righting ability of adult E. esculentus 5 h after transfer from ambient salinity (31‰). Righting ability was converted to activity coefficient, calculated as AC=1000/righting time in seconds; a smaller AC value indicates a longer righting time. Results are shown for Kruskal–Wallis and post hoc Dunn’s test, with different letters indicating significant differences (P<0.05; n=10 biological replicates for each treatment) between treatments. Box plots show medians (black line), upper and lower quartiles, and maximum and minimum (whiskers). Means are represented by open circles and outliers by filled circles.
Fig. 3. Coelomic fluid osmolality of adult E. esculentus 24 h after transfer from ambient salinity (31‰) versus that of the corresponding tank water. All coelomic fluid values were significantly different from their corresponding tank water osmolality (one sample t-test: all P<0.05; n=5 biological replicates at each salinity; 31‰, 26‰, 21‰, 16‰ and 11‰ correspond to 951, 794, 640, 484 and 329 mOsm kg−1 tank water osmolality, respectively). A regression line (blue line) and the 95% confidence intervals (shaded grey area) were fitted to the data. The iso-osmotic line is represented by the dashed grey line. Linear regression coefficients and r2 value are included to the left of the regression line.
Fig. 4. Images of E. esculentus following exposure to ambient and low salinity treatment for 25 days. (A,B) Oral and aboral view after 25 days in 31‰ (control treatment). (C,D) Oral and aboral view after 25 days in 21‰ salinity (low salinity treatment). Note the high primary spine loss and the tube foot damage (arrows) in the low salinity treatment.
Fig. 5. Rate of oxygen consumption of E. esculentus at time points during the 25 day exposure to different salinity conditions. Results are shown for one-way ANOVA and post hoc Tukey test between salinity treatments at each time point (n.s., not significant; *P<0.05, **P<0.01, ***P<0.001; n=10 biological replicates at each time point and treatment). Box plots show medians (black line), upper and lower quartiles, and maximum and minimum (whiskers). Means are represented by open circles and outliers by filled circles.
Fig. 6. Righting ability of E. esculentus at time points during the 25 day exposure to different salinity conditions. Note: a smaller AC value indicates longer righting times. Results are shown for one-way ANOVA and post hoc Tukey test (days 5, 9 and 17) and Games–Howell test (days 1 and 25) between salinity treatments at each time point (n.s., not significant; *P<0.05, **P<0.01, ***P<0.001; n=7–9, 7–8, 7–10 biological replicates at each time point and treatment in control, medium and low salinity, respectively). Box plots show medians (black line), upper and lower quartiles, and maximum and minimum (whiskers). Means are represented by open circles and outliers by filled circles.
Fig. 7. Feeding rate of E. esculentus at time points during the 25 day exposure to different salinity conditions. Feeding rate was calculated as the amount of kelp eaten in 24 h (buoyant wet mass per wet mass of urchin). Results are shown for one-way ANOVA and post hoc Tukey test (day 13) and Games–Howell test (days 1, 5, 9, 17 and 25) between salinity treatments at each time point (n.s., not significant; *P<0.05, **P<0.01, ***P<0.001; n=10 biological replicates at each time point and treatment). Box plots show medians (black line), upper and lower quartiles, and maximum and minimum (whiskers). Means are represented by open circles and outliers by filled circles.
Fig. 8. Coelomic fluid osmolality of adult E. esculentus versus tank water osmolality. Data are mean±s.e.m. coelomic fluid (CF; n=5 biological replicates for each salinity and time point) and tank water (TW; n=3 technical replicates for each salinity and time point) osmolality at time points spanning 25 days of exposure to different salinity conditions. Asterisk indicates a significant difference (one-sample t-test: P<0.05; n=5) between corresponding coelomic fluid and tank water values.
Fig. 9. Oxygen consumption of E. esculentus before and after hypo-osmotic shock following acclimation to reduced salinity. Echinus esculentus were exposed to different salinity treatments for 25 days (red boxes: n=10 biological replicates) followed by an acute immersion in 18‰ salinity (hypo-osmotic shock; blue boxes: n=8 biological replicates). Asterisk indicates a significant difference (two-sample t-test: P<0.05) between mean oxygen consumption pre- and post-acute immersion for each salinity treatment (n.s., not significant). Box plots show medians (black line), upper and lower quartiles, and maximum and minimum (whiskers). Means are represented by open circles and outliers by filled circles.
