Metabolic recovery and compensatory shell growth of juvenile Pacific geoduck Panopea generosa following short-term exposure to acidified seawater

Abstract

While acute stressors can be detrimental, environmental stress conditioning can improve performance. To test the hypothesis that physiological status is altered by stress conditioning, we subjected juvenile Pacific geoduck, Panopea generosa, to repeated exposures of elevated pCO2 in a commercial hatchery setting followed by a period in ambient common garden. Respiration rate and shell length were measured for juvenile geoduck periodically throughout short-term repeated reciprocal exposure periods in ambient (~550 μatm) or elevated (~2400 μatm) pCO2 treatments and in common, ambient conditions, 5 months after exposure. Short-term exposure periods comprised an initial 10-day exposure followed by 14 days in ambient before a secondary 6-day reciprocal exposure. The initial exposure to elevated pCO2 significantly reduced respiration rate by 25% relative to ambient conditions, but no effect on shell growth was detected. Following 14 days in common garden, ambient conditions, reciprocal exposure to elevated or ambient pCO2 did not alter juvenile respiration rates, indicating ability for metabolic recovery under subsequent conditions. Shell growth was negatively affected during the reciprocal treatment in both exposure histories; however, clams exposed to the initial elevated pCO2 showed compensatory growth with 5.8% greater shell length (on average between the two secondary exposures) after 5 months in ambient conditions. Additionally, clams exposed to the secondary elevated pCO2 showed 52.4% increase in respiration rate after 5 months in ambient conditions. Early exposure to low pH appears to trigger carryover effects suggesting bioenergetic re-allocation facilitates growth compensation. Life stage-specific exposures to stress can determine when it may be especially detrimental, or advantageous, to apply stress conditioning for commercial production of this long-lived burrowing clam.

Repeat exposure to hypercapnic seawater modifies growth and oxidative status in a tolerant burrowing clam

“…A growing body of research posits an adaptive role of early life as a 'programming window' owing to the importance of environmental information in setting the stage for subsequent phenotypic outcomes (Fawcett and Frankenhuis, 2015). Beneficial carryover effects in the present study are also corroborated by compensatory physiology and differential DNA methylation of juvenile P. generosa in other studies (Putnam et al, 2017;Gurr et al, 2020). In contrast, OA can have deleterious effects on growth/development, settlement and proteomic composition of larval P. generosa (Timmins-Schiffman et al, 2019), further emphasizing the life-stage dependence of P CO2 stress exposure.…”

“…Oxygen concentration (µg O 2 l −1 ) was recorded every 15 s until concentrations declined to ∼50-70% saturation (∼20 min). Vial seawater volume was measured and clams from each vial were photographed with a size standard (1 mm stage micrometer) to measure shell length ( parallel to hinge; mm) using Image J. Respiration rates were calculated using the R package LoLinR (https://github.com/colin-olito/LoLinR) with suggested parameters by the package authors (Olito et al, 2017) and following Gurr et al (2020) with minor adjustments: fixed constants for weighting method (L % ) and observations (alpha=0.4) over the full 20 min record. Final respiration rates of juvenile geoduck were corrected for blank vial rates and vial seawater volume (µg O 2 h −1 individual −1 ).…”

“…Previous studies describe metabolic compensation and regulation of CSR during hypercapnia as attributes of a well-adapted stress response to control acid-base status and normal development/metamorphosis (Walsh and Milligan, 1989;Dineshram et al, 2015). Indeed, prior work on juvenile P. generosa also demonstrates positive acclimatory carryover effects, with increased shell length and metabolic rate after repeat exposures to hypercapnic and undersaturated conditions with respect to aragonite (Gurr et al, 2020). Contrary to our findings, similar P CO2 and Ω arg levels decrease metabolic rate and scope for growth in the mussel Mytilus chilensis (Navarro et al, 2013), cause a three-fold increase in mortality rate in juvenile hard clam Mercenaria mercenaria (Green et al, 2009), and alter metamorphosis and juvenile burrowing behavior in Panopea japonica (Huo et al, 2019).…”

“…Pacific geoduck (Panopea generosa Gould 1850) is a burrowing clam of ecological (Goodwin and Pease, 1987) and economic importance (Shamshak and King, 2015) and is a great candidate for investigating hormetic priming for generation of stress-acclimated phenotypes. Juvenile geoduck have shown positive carryover effects after exposure to high P CO2 /low Ω arg conditions, including compensatory respiration rates and shell growth (Gurr et al, 2020). In contrast, larval performance is negatively impacted under OA exposure (Timmins-Schiffman et al, 2019).…”

Dynamic DNA methylation contributes to carryover effects and beneficial acclimatization in geoduck clams

“…The Geoduck clam, Panopea sp., is an ideal species for studying environmental tolerance because in addition to being the basis of a high-value commercial fishery, it is among the longest lived animals on earth despite being a sessile marine invertebrate that needs to acclimate and adapt to dynamic local conditions. While the Pacific geoduck, Panopea generosa, has shown delayed development under low pH stress (Timmins-Schiffman et al 2020), interestingly it has also shown compensatory growth when re-exposed to low pH stress to which it was previously conditioned (Gurr et al 2020). This beneficial acclimation suggests conditioning or 'priming' could enhance environmental tolerance and there is a growing body of evidence supporting this concept in a variety of biomineralizaing marine invertebrate species (Eirin-Lopez and Putnam 2019), including the Sydney rock oyster (Parker et al 2015), the Manilla clam (Zhao et al 2018), and the purple sea urchin (Strader et al 2019).…”