Differential impacts of ocean acidification and warming on winter and summer progeny of a coastal squid (Loligo vulgaris)

Abstract

Little is known about the capacity of early life stages to undergo hypercapnic and thermal acclimation under the future scenarios of ocean acidification and warming. Here, we investigated a comprehensive set of biological responses to these climate changerelated variables (2°C above winter and summer average spawning temperatures and ΔpH=0.5 units) during the early ontogeny of the squid Loligo vulgaris. Embryo survival rates ranged from 92% to 96% under present-day temperature (13-17°C) and pH (8.0) scenarios. Yet, ocean acidification (pH 7.5) and summer warming (19°C) led to a significant drop in the survival rates of summer embryos (47%, P<0.05). The embryonic period was shortened by increasing temperature in both pH treatments (P<0.05). Embryo growth rates increased significantly with temperature under present-day scenarios, but there was a significant trend reversal under future summer warming conditions (P<0.05). Besides pronounced premature hatching, a higher percentage of abnormalities was found in summer embryos exposed to future warming and lower pH (P<0.05). Under the hypercapnic scenario, oxygen consumption rates decreased significantly in late embryos and newly hatched paralarvae, especially in the summer period (P<0.05). Concomitantly, there was a significant enhancement of the heat shock response (HSP70/HSC70) with warming in both pH treatments and developmental stages. Upper thermal tolerance limits were positively influenced by acclimation temperature, and such thresholds were significantly higher in late embryos than in hatchlings under present-day conditions (P<0.05). In contrast, the upper thermal tolerance limits under hypercapnia were higher in hatchlings than in embryos. Thus, we show that the stressful abiotic conditions inside the embryo's capsules will be exacerbated under near-future ocean acidification and summer warming scenarios. The occurrence of prolonged embryogenesis along with lowered thermal tolerance limits under such conditions is expected to negatively affect the survival success of squid early life stages during the summer spawning period, but not winter spawning.

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

“…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 capsular effects are the first evidence (statolith chemistry) of strong physiological differences among the same cohort, and the importance of these differences for the persistence of the D. opalescens population is not known.…”

“…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.…”

“…Curiously, when exposed to low [O 2 ] with low pH (low pHOx), statoliths were not enriched with Sr. Strontium incorporation into squid statoliths may be inversely related to metabolic rate. Low environmental pH/high pCO 2 and high temperatures can cause metabolic depression in squid embryos [45,46] and reduced growth [52].…”

“…The structures of the capsule can connect the external chemical environment to the embryo via the capsular membranes, interstitial jelly and the chorion membrane (hereafter, these effects are collectively referred to as "capsular effects"). 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]. The cephalopod-embryo metabolic rate greatly increases at the end of development [42,45,46] and is variable among embryos within the capsule [53]. The molluscan metabolic rate is highly influenced by temperature [45,46,54] and environmental oxygen [20,55,56]; cephalopods can be influenced by environmental pH/pCO 2 levels at the embryonic stages [45][46][47]52], but are tolerant at older stages [57,58].…”