Dose-dependence and small-scale variability in responses to ocean acidification during squid, Doryteuthis pealeii, development

Abstract

Coastal squids lay their eggs on the benthos, leaving them to develop in a dynamic system that is undergoing rapid acidification due to human influence. Prior studies have broadly investigated the impacts of ocean acidification on embryonic squid, but have not addressed the thresholds at which these responses occur or their potential variability. We raised squid, Doryteuthis pealeii (captured in Vineyard Sound, Massachusetts, USA: 41° 23.370N 70° 46.418´W), eggs in three trials across the breeding season (May-September, 2013) in a total of six chronic pCO 2 exposures (400, 550, 850, 1300, 1900, and 2200 ppm). Hatchlings were counted and subsampled for mantle length, yolk volume, hatching time, hatching success, and statolith morphology. New methods for analysis of statolith shape, rugosity, and surface degradation were developed and are presented (with code). Responses to acidification (e.g., reduced mantle lengths, delayed hatching, and smaller, more degraded statoliths) were evident at ~ 1300 ppm CO 2. However, patterns of physiological response and energy management, based on comparisons of yolk consumption and growth, varied among trials. Interactions between pCO 2 and hatching day indicated a potential influence of exposure time on responses, while interactions with culture vessel highlighted the substantive natural variability within a clutch of eggs. While this study is consistent with, and expands upon, previous findings of sensitivity of the early life stages to acidification, it also highlights the plasticity and potential for resilience in this population of squid.

Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and Paralarvae

“…Experiments were performed between May and October of 2016 at the Environmental Systems Laboratory (ESL) of the Woods Hole Oceanographic Institution, Woods Hole, MA, United States during peak breeding season of Doryteuthis pealeii for this region (Arnold et al, 1974;Jacobson, 2005). Methods presented throughout are similar to those reported in detail in Zakroff et al (2019) so will be reiterated in brief, but with differences noted.…”

“…Observers have recorded eggs laid at depths of up to 50 m, in temperatures of 10-23 • C, and salinities of 30-32, which contextualizes a presumed preferred laying habitat for this species (McMahon and Summers, 1971;Jacobson, 2005). Less is known about the preferences for pH of egg laying habitat for this species, but pH t calculated from shelf carbonate system profiles throughout their habitat range indicate a typical exposure range of 7.88-8.2 (600-250 ppm pCO 2 ) during the breeding season (Wang et al, 2013;Zakroff et al, 2019). Navarro et al (2018) reported preferred egg laying habitat for the California market squid, Doryteuthis opalescens, as requiring pH t greater than 7.8 and O 2 concentrations greater than 160 µmol with no apparent temperature limitation within the region.…”

“…Kaplan et al (2013); experiments ran in 2011 reared D. pealeii egg capsules under a low, facility ambient (550 ppm), and high acidification (2200 ppm), observing development delays of about 1 day, a decrease in DML of the hatchling paralarvae, and decreased size and quality of the statoliths. Subsequently, Zakroff et al (2019; experiments ran in 2013) expanded upon this preliminary work, exposing D. pealeii egg capsules to a range of pCO 2 levels (from 400 to 2200 ppm), noting delays in development time, decreases in DML, and smaller, rougher statoliths that indicated a potential dose response threshold of 1300 ppm. In addition, this study highlighted notable variability in response intensity across the breeding season, demonstrating potentially different physiological strategies or responses to acidification stress within the egg capsules that expressed as different levels of sensitivity or resistance across the season (Zakroff et al, 2019).…”

“…Subsequently, Zakroff et al (2019; experiments ran in 2013) expanded upon this preliminary work, exposing D. pealeii egg capsules to a range of pCO 2 levels (from 400 to 2200 ppm), noting delays in development time, decreases in DML, and smaller, rougher statoliths that indicated a potential dose response threshold of 1300 ppm. In addition, this study highlighted notable variability in response intensity across the breeding season, demonstrating potentially different physiological strategies or responses to acidification stress within the egg capsules that expressed as different levels of sensitivity or resistance across the season (Zakroff et al, 2019). Behavioral experiments run in parallel to and following Zakroff et al (2019) showed full years where paralarvae showed little to no response to acidification even up to the original 2200 ppm level, suggesting greater levels of resilience than had been expected (Zakroff et al, 2018; experiments ran from 2013 to 2015).…”

“…In this study, we examined the extent of stress resistance and response variability in developing D. pealeii embryos by both increasing the acidification exposure (2200 ppm was considered a variable response, while 3500 ppm was used as a positive control) and by adding warming (+2 • C above peak breeding season temperature for Vineyard Sound, MA, United States) as a potentially compounding stressor. Metrics analyzed are the same as those in Zakroff et al (2019) except that proportions of malformation in the paralarvae were added based on their prevalence in work by Rosa et al (2012Rosa et al ( , 2014 and statolith data are not included to maintain concision in this manuscript. Further, unlike most of the previously cited work, which used wild collected or lab produced egg capsules most likely sourced from multiple parents, egg capsule maternity was monitored, allowing for an examination of both between and within clutch variability of stress responses.…”