Effects of ocean acidification on trace element accumulation in the early-life stages of squid Loligo vulgaris

Abstract

The anthropogenic release of carbon dioxide (CO(2)) into the atmosphere leads to an increase in the CO(2) partial pressure (pCO(2)) in the ocean, which may reach 950 μatm by the end of the 21st century. The resulting hypercapnia (high pCO(2)) and decreasing pH ("ocean acidification") are expected to have appreciable effects on water-breathing organisms, especially on their early-life stages. For organisms like squid that lay their eggs in coastal areas where the embryo and then paralarva are also exposed to metal contamination, there is a need for information on how ocean acidification may influence trace element bioaccumulation during their development. In this study, we investigated the effects of enhanced levels of pCO(2) (380, 850 and 1500 μatm corresponding to pH(T) of 8.1, 7.85 and 7.60) on the accumulation of dissolved (110m)Ag, (109)Cd, (57)Co, (203)Hg, (54)Mn and (65)Zn radiotracers in the whole egg strand and in the different compartments of the egg of Loligo vulgaris during the embryonic development and also in hatchlings during their first days of paralarval life. Retention properties of the eggshell for (110m)Ag, (203)Hg and (65)Zn were affected by the pCO(2) treatments. In the embryo, increasing seawater pCO(2) enhanced the uptake of both (110m)Ag and (65)Zn while (203)Hg showed a minimum concentration factor (CF) at the intermediate pCO(2). (65)Zn incorporation in statoliths also increased with increasing pCO(2). Conversely, uptake of (109)Cd and (54)Mn in the embryo decreased as a function of increasing pCO(2). Only the accumulation of (57)Co in embryos was not affected by increasing pCO(2). In paralarvae, the CF of (110m)Ag increased with increasing pCO(2), whereas the (57)Co CF was reduced at the highest pCO(2) and (203)Hg showed a maximal uptake rate at the intermediate pCO(2). (54)Mn and (65)Zn accumulation in paralarvae were not significantly modified by hypercapnic conditions. Our results suggest a combined effect of pH on the adsorption and protective properties of the eggshell and of hypercapnia on the metabolism of embryo and paralarvae, both causing changes to the accumulation of metals in the tissues of L. vulgaris.

Environmental pH, O2 and Capsular Effects on the Geochemical Composition of Statoliths of Embryonic Squid Doryteuthis opalescens

“…Indirect maternal influence could be caused by a variation in the quality of the capsular and chorion membrane. Although this issue has not been explicitly studied, other investigators have found significant differences of Co uptake among capsules (one capsule of three capsules) of the squid, Loligo vulgaris [49]. Second, our findings show that the embryonic-statolith geochemistry is distinct for many elements among capsules, but not distinct for most elements among environmental treatments.…”

“…The only other known study that tested the effects of environmental pH on squid-embryo statolith geochemistry found that only 65 Zn significantly differed from an elemental suite that included 110m Ag, 109 Cd, 57 Co, 203 Hg and 54 Mn [49]. Evidence that environmental tracers in squid statoliths can track seawater pH and [O 2 ] is especially useful, because uranium has been shown to be promising for understanding squid life history, migrations and habitat use [88,90,91].…”

“…The mechanism behind the capsular effect on statolith elemental incorporation is presumably due to a process that similarly affects all embryos of the capsule. Mechanisms include maternal transfer [53,73,83,84] and capsular and chorion membrane structural differences [49,50] among capsules. Less likely mechanisms include processes within the embryos [17][18][19]45,46] that are expressed similarly among embryos.…”

“…These differences may be attributable to differences among capsular units. Each unit may have differences in: (1) elemental uptake in their capsular or chorion membranes [49,50]; (2) utilization of embryonic-epidermal ionocytes [17][18][19]; (3) embryonic metabolism [45,46] and the effect total embryo metabolism per capsule has on the diffusion of environmental [O 2 ] and pCO 2 [20,55,56]; and (4) the rate of active transport of the statocyst membrane [41]; or (5) any combination these factors. Although there are many reports that support environmental "recording" within statolith geochemistry [30,33,34,59], our data suggest that statolith geochemistry records both the environment and capsular effects within each embryo.…”

“…The pH/pCO 2 and [O 2 ] of the perivitelline fluid that surrounds the embryo are impacted additively by the environment and by the physiological processes of the embryo itself [17][18][19][42][43][44][45][46][47]. Elemental incorporation within statoliths can be influenced by the environment [30,33,34,48], but physiological process impacts on statolith geochemistry, including processes within the statocyst [41], embryo [18,19,45,46], as well as within outer-embryo structures [49,50], are not well understood. Further, the squid embryonic metabolic rate affects statolith formation [51,52].…”