CO2-induced fertilization impairment in Strongylocentrotus droebachiensis collected in the Arctic

Abstract

Fertilization depends on distribution and aggregation patterns of sea urchins which influence gamete contact time and may potentially enhance their vulnerability to ocean acidification. In this study, we conducted fertilization experiments to assess the effects of selected pH scenarios on fertilization success of Strongylocentrotus droebachiensis, from Spitsbergen, Arctic. Acidification was achieved by aerating seawater with different CO 2 partial pressures to represent preindustrial and present conditions (measured *180-425 latm) and future acidification scenarios (*550-800, *1,300, *2,000 latm). Fertilization success was defined as the proportion of successful/unsuccessful fertilizations per treatment; eggs were classified according to features of their fertilization envelope (FE), hyaline layer (HL) and achievement of cellular division. The diagnostic findings of specific pathological aberrations were described in detail. We additionally measured intracellular pH changes in unfertilized eggs exposed for 1 h to selected acidification treatments using BCECF/AM. We conclude that (a) acidified conditions increase the proportion of eggs that failed fertilization, (b) acidification may increase the risk of polyspermy due to failures in the FE formation supported by the occasional observation of multiple sperms in the perivitelline space and (c) irregular formation of the embryo may arise due to impaired formation of the HL. The decrease in fertilization success could be also related to the observed changes in intracellular pH at pCO 2 * 1,000 latm or higher.

Ocean acidification does not overlook sex: Review of understudied effects and implications of low pH on marine invertebrate sexual reproduction

“…These impacts are likely species-and population-specific, with some urchins exhibiting no impact of low pH on egg jelly coat area, and populations exhibiting varied impacts depending on prior pH exposure (Foo et al, 2018). Egg intracellular pH adjusts according to the external chemical environment (Ciapa and Philippe, 2013;Bögner et al, 2014), which may also hamper egg activation by interfering with calcium signaling and actin dynamics (Limatola et al, 2020). Indeed, Shi et al (2017b) observed that low pH disrupts the intracellular calcium ion (Ca 2+ ) activity in T. granosa eggs, which was associated with reduced fertilization rates.…”

An updated synthesis of the observed and projected impacts of climate change on the chemical, physical and biological processes in the oceans

“…More evidence of the negative effects of decreasing pH on fertilization success of invertebrates has been found (Sewell et al, 2013;Bögner et al, 2014;Frieder, 2014;Scanes et al, 2014;Sung et al, 2014) and RCP8.5 acidification has been shown to have negative effects on clam larval dispersal (Clements and Hunt, 2014).…”

Life under Climate Change Scenarios: Sea Urchins’ Cellular Mechanisms for Reproductive Success

“…Interestingly, Ciapa and Philippe [112] found eggs showing cellular constrictions and nuclear envelope breakdown, probably related to alterations in the Ca i 2+ regulation under cytosolic acidosis caused by the Na + deprivation outside the cell, followed by compensation throughout additional removal of HCO 3f rom the media. Constricted eggs which failed to progress into the cell cycle were also observed by Bögner, et al [22]. For the accomplishment of cytokinesis a highly-regulated sequence of events concerning the nucleus and the cytosol must occur and the communication between these compartments is essential.…”

“…Fertilization rate óó Proportion of fertilized eggs [22,23] ó Fecundity (reversible effect) [24] ó Fertilization success at longer exposure periods before fertilization [25] ò Polyspermy rates [26] Depending on species origin and methods used, there are inconsistent results indicating the need of a standard protocol.…”

“…ó pH i due to exposure to acidified seawater matrices before and after fertilization [22] (with still unstudied impact on Ca i 2+ sequestration and cytosolic buffer affinity for Ca 2+ ) ó Proportion of perfect FE and HL formation [22] ó Actin polymerization in the cortex region [38] -Cleavage retardation/inhibition at low pH leading to delayed larval formation [38,39] ò Alterations of the division plane [40,41] ò Embryo radialization [42][43][44] There are few studies dealing with T and oxygen depletion impacts on eggs before and immediately after fertilization. The strong dependence of all stages after fertilization on the redox state of the zygote, the pH i and Ca i 2+ levels and the sensitivity of the molecular machinery to pH (and probably T and H/A too), make of these stages a great-unexplored field requiring further attention.…”