Ocean acidification increases the sensitivity of and variability in physiological responses of an intertidal limpet to thermal stress

Abstract

Abstract. Understanding physiological responses of organisms to warming and ocean acidification is the first step towards predicting the potential population- and community-level ecological impacts of these stressors. Increasingly, physiological plasticity is being recognized as important for organisms to adapt to the changing microclimates. Here, we evaluate the importance of physiological plasticity for coping with ocean acidification and elevated temperature, and its variability among individuals, of the intertidal limpet Cellana toreuma from the same population in Xiamen. Limpets were collected from shaded mid-intertidal rock surfaces. They were acclimated under combinations of different pCO2 concentrations (400 and 1000 ppm, corresponding to a pH of 8.1 and 7.8) and temperatures (20 and 24 ∘C) in a short-term period (7 days), with the control conditions (20 ∘C and 400 ppm) representing the average annual temperature and present-day pCO2 level at the collection site. Heart rates (as a proxy for metabolic performance) and expression of genes encoding inducible and constitutive heat-shock proteins (hsp70 and hsc70) at different heat-shock temperatures (26, 30, 34, and 38 ∘C) were measured. Hsp70 and Hsc70 play important roles in protecting cells from heat stresses, but have different expression patterns, with Hsp70 significantly increased in expression during stress and Hsc70 constitutively expressed and only mildly induced during stress. Analysis of heart rate showed significantly higher temperature coefficients (Q10 rates) for limpets at 20 ∘C than at 24 ∘C and post-acclimation thermal sensitivity of limpets at 400 ppm was lower than at 1000 ppm. Expression of hsp70 linearly increased with the increasing heat-shock temperatures, with the largest slope occurring in limpets acclimated under a future scenario (24 ∘C and 1000 ppm pCO2). These results suggested that limpets showed increased sensitivity and stress response under future conditions. Furthermore, the increased variation in physiological response under the future scenario indicated that some individuals have higher physiological plasticity to cope with these conditions. While short-term acclimation to reduced pH seawater decreases the ability of partial individuals against thermal stress, physiological plasticity and variability seem to be crucial in allowing some intertidal animals to survive in a rapidly changing environment.

Can heat shock protein 70 (HSP70) serve as biomarkers in Antarctica for future ocean acidification, warming and salinity stress?

“…The effects of sudden changes in the sea surface has been reported in several studies such as the high mortality of krill near Carlini Station, King George Island (Fuentes et al 2016) and the loss of ability to adapt to sudden changes in water such as in scallops (Adamussium colbecki), clams (L. elliptica) and limpets (N. concinna) (Peck 2005;Peck et al 2010), marine invertebrates (Odontaster validus and Paraceradocus gibber) (Clark et al 2008a, b, c), and sea urchins (S. neumayeri) (González-Aravena et al 2018). Moreover, the intertidal limpet, Cellana toreuma, showed a significant increase in Hsp70 expression for coping with ocean acidification and elevated temperature (Wang et al 2018). Yusof et al (2021) reported that the Antarctic yeast, G. antarctica, showed increasing expression of Hsp70s upon thermal stress.…”

Increased Thermal Sensitivity of a Tropical Marine Gastropod Under Combined CO2 and Temperature Stress

“…Changes in body temperature are often among the most commonly studied responses for ectothermic marine invertebrates as temperature plays a large part in controlling cellular to physiological reactions, which in turn affects metabolism, growth and reproductive rates (Grigaltchik et al, 2012;Sinclair et al, 2016). Even small changes in the environment can cause a broad range of physiological responses due to variation among and within species (Harley et al, 2017;Wang et al, 2018). In particular, there has been an increasing focus on the physiological impacts of heatwaves, which are increasing in magnitude and frequency, increasing the likelihood that organisms are being subjected to thermal conditions beyond their optimal and lethal limits (Lannig et al, 2010;Sinclair et al, 2016).…”

“…Large variation in responses, even within a species, highlights that genetic variation and variability in physiological plasticity can affect the likelihood that populations survive short-term extremes (Wang et al, 2018). Should enough individuals be able to acclimate to novel conditions during extreme events, populations and communities may be able to handle future conditions better than currently predicted (Seebacher et al, 2014).…”

“…suffer far greater reduction in growth and higher metabolic activity when exposed simultaneously to elevated CO 2 (∼860-940 µatm) and temperature (ambient +2 to 3 • C) than when either is considered alone (Uthicke et al, 2014). Intertidal limpets not only have higher sensitivity to hotter environments under elevated CO 2 concentrations, but at a population level have greater variation in individual responses to temperature, signifying that some individuals have greater ability to alter their tolerance limits (Wang et al, 2018). Such variable responses ultimately determine the potential for acclimation and plasticity within populations, producing a selective advantage by extending the organism's physiological (fundamental) niche.…”

Physiological and Behavioral Plasticity of the Sea Cucumber Holothuria forskali (Echinodermata, Holothuroidea) to Acidified Seawater

“…Long-term studies are important in order to avoid inaccurate assessments of the chronic effects of ocean acidification ( Kurihara et al, 2013 ; Moulin et al, 2015 ; Queirós et al, 2015 ; Riebesell and Gattuso, 2015 ; Lucey et al, 2016 ). Organisms living in coastal or upwelling environments currently experience highly fluctuating p CO 2 /pH on diurnal, tidal and seasonal cycles ( Hofmann et al, 2011 ; Wang et al, 2018 ). Therefore, local adaptation plays a crucial role in population sensitivity ( Hofmann et al, 2014 ; Vargas et al, 2017 ), and understanding long term tolerance in these organisms is important to an assessment of their response.…”