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Increasing atmospheric carbon dioxide (CO2) has resulted in a change in seawater chemistry and lowering of pH, referred to as ocean acidification. Understanding how different organisms and processes respond to ocean acidification is vital to predict how marine ecosystems will be altered under future scenarios of continued environmental change. Regenerative processes involving biomineralization in marine calcifiers such as sea urchins are predicted to be especially vulnerable. In this study, the effect of ocean acidification on regeneration of external appendages (spines and tube feet) was investigated in the sea urchin Lytechinus variegatus exposed to ambient (546 µatm), intermediate (1027 µatm) and high (1841 µatm) partial pressure of CO2 (pCO2) for eight weeks. The rate of regeneration was maintained in spines and tube feet throughout two periods of amputation and regrowth under conditions of elevated pCO2. Increased expression of several biomineralization-related genes indicated molecular compensatory mechanisms; however, the structural integrity of both regenerating and homeostatic spines was compromised in high pCO2 conditions. Indicators of physiological fitness (righting response, growth rate, coelomocyte concentration and composition) were not affected by increasing pCO2, but compromised spine integrity is likely to have negative consequences for defence capabilities and therefore survival of these ecologically and economically important organisms.
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28573022
???displayArticle.pmcLink???PMC5451823 ???displayArticle.link???R Soc Open Sci ???displayArticle.grants???[+]
Figure 1. Sea urchin tube feet and spine regeneration assay. (a) Aboral view 1 day post-amputation showing tube feet and spines removed from along one of the ambulacral segments of the test from the oral to aboral surface. (b) Lateral view of the amputated region, 1 day post-amputation. (c) Lateral view of the amputated region, 8 days post-amputation.
Figure 2. Spine and tube feet regeneration in sea urchins exposed to elevated pCO2. Regeneration (% of full length) of amputated spines (a) and tube feet (b) in adult sea urchins exposed to ambient conditions (black bars), intermediate pCO2 (dark grey bars) and high pCO2 (light grey bars) over 59 days exposure. Arrows and vertical dashed lines indicate initial amputation and re-amputation, and dotted bars indicate first amputation of ambient captivity control treatment. Data are means ± s.e.m., n = 6 (except n = 4 for the ambient captivity control and n = 5 for tube feet intermediate treatment group after 29 days exposure); no overall treatment effect (GLM, p > 0.05) and (*) significantly different from ambient treatment, post hoc multiple range test.
Figure 3. Scanning electron micrographs of spines from ambient and high pCO2 conditions. (a,e) Homeostatic spine from ambient conditions. (b,f) Regenerating spine from ambient conditions. (c,g) Homeostatic spine from high pCO2 conditions. (d,h) Regenerating spine from high pCO2 conditions. (a–d) are about 1 mm from the tip of the spine (tip). (e–f) are about 5 mm from the tip of the spine (mid). Scale bar represents 50 µm. Images were selected as representatives of homeostatic and regenerating spines from n = 3 sea urchins for each of the ambient and high pCO2 conditions.
Figure 4. Sea urchin spine snap test after 59 days pCO2 treatment exposure period. The amount of weight required to break homeostatic and regenerating spines is shown for the three treatment groups: ambient (black bars), intermediate (grey bars) and high pCO2 (white bars). Regenerating spines were significantly weaker than homeostatic spines (GLM, p < 0.05), and animals from the high pCO2 treatment had significantly weaker spines (homeostatic and regenerated) compared with spines from animals kept under ambient control conditions (*one-way ANOVA, p < 0.05, post hoc multiple range test). Data are means ± s.e.m., n = 6 animals per treatment (technical replicates of 3–10 spines per individual).
Figure 5. Expression of biomineralization genes in regenerating spines from adult sea urchins exposed to elevated pCO2 for 29 days (light grey bars) and 59 days (dark grey bars). Data are means ± s.e.m., n = 6 in each treatment group, except n = 4 for intermediate treatment at 29-day exposure and n = 5 for high treatment at 59-day exposure. Relative fold change = (EtargetΔCt
(mean ambient − sample))/(EreferenceΔCt
(mean ambient − sample)), geometric mean from three reference genes (rpl8, profilin and cyclophilin7); *significantly higher than ambient (one-way ANOVA or Kruskal–Wallis, p < 0.05, post hoc multiple range test).
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