Article pubs.acs.org/est
Ocean Acidification Reduces Spine Mechanical Strength in Euechinoid but Not in Cidaroid Sea Urchins Aurélie Dery,* Marie Collard, and Philippe Dubois Université Libre de Bruxelles, Laboratoire de Biologie Marine, avenue F.D. Roosevelt 50 CP 160/15 1050, Bruxelles, France S Supporting Information *
ABSTRACT: Echinoderms are considered particularly sensitive to ocean acidification (OA) as their skeleton is made of high-magnesium calcite, one of the most soluble forms of calcium carbonate. Recent studies have investigated effects of OA on the skeleton of “classical” sea urchins (euechinoids), but the impact of etching on skeleton mechanical properties is almost unknown. Furthermore, the integrity of the skeleton of cidaroids has never been assessed, although their extracellular fluid is under-saturated with respect to their skeleton, and the skeleton of their primary spines is in direct contact with seawater. In this study, we compared the dissolution of test plates and spines as well as the spine mechanical properties (two-points bending tests) in a cidaroid (Eucidaris tribuloides) and a euechinoid (Tripneustes ventricosus) submitted to a 5 week acidification experiment (pHT of 8.1, 7.7, and 7.4). Test plates of both species were not affected by dissolution. The spines of E. tribuloides showed no mechanical effects at pHSW‑T 7.4 despite having traces of corrosion on secondary spines. On the contrary, spines of the T. ventricosus were significantly etched at both pHSW‑T 7.7 and 7.4 and their fracture force reduced by 16 to 35%, respectively. This increased brittleness is probably of little significance with regards to predation protection but has consequences in terms of energy allocation.
1. INTRODUCTION The increase of the atmospheric CO2 concentration due to anthropogenic emissions directly induces a parallel increase in oceanic seawater pCO2 and a shift in the carbonate equilibrium, a process known as ocean acidification (OA). This will result in a decrease of seawater pH of 0.13−0.42 units by 2100 and a decrease up to 0.7 units by 2300 (depending on the considered scenario of emissions) compared to current values. The calcium carbonate saturation horizons (the depth at which a given polymorph of calcium carbonate is at dissolution−precipitation equilibrium with seawater) will become shallower, especially at the poles.1 This is expected to have major effects on many marine organisms.2 The formation and maintenance of calcified skeletons have long been regarded as the processes most affected by OA.3 In particular, echinoderms have been considered to be particularly at risk from OA because of their low metabolism, limited regulation abilities, and extensive skeleton made of high-magnesium calcite, a form of calcium carbonate unstable in abiotic conditions.4−6 However, recent studies indicated that skeleton integrity would not be seriously threatened by OA in postmetamorphic (juvenile and adult) echinoderms at pH levels relevant to this century, and dissolution of the skeleton would be rather limited.7−11 However, very few studies addressed the impact of OA on the main functional characteristic of the echinoderm skeleton and its mechanical properties. These may be affected by different mechanisms. A change in the microarchitecture of the mineral due to changes in growth rates and morphogenesis will © XXXX American Chemical Society
affect the distribution of the material in the ossicle and, consequently, its mechanical strength. Modifications at the crystalline level (coherence length and angular dispersion) may modify the material properties themselves (hardness or stiffness) and, consequently, its mechanical strength. Finally, dissolution will affect the integrity of the material, affecting both the properties and the distribution of the material. The first two effects should be studied in long-term acidification experiments or in specimens collected along natural pH gradients (CO2 vents) so that all or most of the skeleton has been formed under reduced pH conditions. Dissolution may be studied in shorter-term experiments because it may occur rather fast after the organism is submitted to acidified conditions. In long-term experiments or specimens from CO2 vents, no effect of acidification was recorded either on the force at rupture (Fmax) or on the Young’s modulus (E, a measure of stiffness of the material) of test plates from adult sea urchins Paracentrotus lividus and Echinometra mathaei.10,11 In crushing tests, whole live Tripneustes gratilla urchins mostly ruptured along the collagenous sutures between the plates, indicating that skeletal plates were not weakened by OA.12 On the contrary, dissolution in sea urchin spines at pH ranging from pHT 7.8 to pHNBS 7.4 was documented in short-term Received: Revised: Accepted: Published: A
October 18, 2016 March 7, 2017 March 7, 2017 March 7, 2017 DOI: 10.1021/acs.est.6b05138 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
Article
Environmental Science & Technology
Table 1. Corrosion and Results of the Mechanical Tests (Mean ± s.d., n= 3) According to Species, Spine Type, and Seawater pHTa E. tribuloides primary spines E. tribuloides secondary spines
T. ventricosus primary spines
T. ventricosus secondary spines
Fmax E I2 (E-14) corrosion Fmax E I2 (E-17) corrosion Fmax E I2 (E-16) corrosion Fmax E I2 (E-18)
8.1
7.7
7.4
overall mean values
p (ANOVA)
15.8 ± 5.2 7.4 ± 3.5 5.2 ± 3.0 11% ± 11a 2.4 ± 0.3 7.5 ± 0.8 2.3 ± 1.2 20% ± 11.5a 0.77 ± 0.08a 35.6 ± 7.2 1.5 ± 0.3 33% ± 17a 0.26 ± 0.03a 44.2 ± 5.9 2.2 ± 0.5
12.7 ± 1.0 6.8 ± 3.9 7.8 ± 2.6 48% ± 6.3b 2.4 ± 0.4 11.9 ± 3.7 2.9 ± 2.0 50% ± 16.5b 0.62 ± 0.08a,b 32.7 ± 2.0 1.0 ± 0.4 27% ± 9.8a 0.21 ± 0.01a 48.6 ± 3.6 2.7 ± 0.8
14.3 ± 7.3 11.5 ± 4.0 3.0 ± 0.3 100% ± 0c 1.9 ± 0.3 7.5 ± 2.5 2.3 ± 0.3 100% ± 0c 0.53 ± 0.03b 29.2 ± 2.4 1.1 ± 0.1 100% ± 0b 0.16 ± 0.03b 44.7 ± 7.7 2.5 ± 0.5
14.2 ± 1.6 8.6 ± 2.5 5.3 ± 2.4 − 2.3 ± 0.2 8.9 ± 2.5 2.5 ± 0.35 − − 32.5 ± 3.2 1.2 ± 0.26 − − 45.8 ± 2.4 2.5 ± 0.25
0.8 0.3 0.1
