Thermal performance of the European flat oyster, Ostrea edulis (Linnaeus, 1758)—explaining ecological findings under climate change

Abstract

Climate change challenges marine organisms by constraining their temperature-dependent scope for performance, fitness, and survival. According to the concept of Oxygen and Capacity Limited Thermal Tolerance (OCLTT), the overall thermal performance curve relates to an organism's aerobic power budget, its overall aerobic scope for growth, exercise, reproduction, and other performances. We hypothesize that physiological principles shaping tolerance in extant ecosystems have also been operative during climatic changes in the distant past. To compare response patterns in extant fauna and their palaeo-relatives, we started here by studying the metabolic background of performance in the European flat oyster Ostrea edulis at organismic and cellular levels, focusing on the acute thermal window and the metabolic changes towards upper lethal temperatures. We investigated the response of the oysters (pre-acclimated at 12 °C) to a short-term warming protocol (by 2 °C every 48 h) from 14 to 36 °C which we identified as the lethal temperature. At the organismic level, heart and filtration rates were recorded. Gill metabolites were studied by 1 H NMR spectroscopy to address thermal responses at the cellular level. Feeding activity by O. edulis (assessed by the filtration rates) was highest between 18 and 24 °C when overall energy expenditure (indicated by heart rate as a proxy for routine metabolic rate) was moderate. We conclude that this range reflects the thermal optimum of this species. Beyond 26 °C, the gill tissue of O. edulis became partly anaerobic, and cardiac dysfunction (arrhythmia) developed at 28 °C followed by an Arrhenius break point (30 °C). This mirrors performance constraints and indicates a wide temperature range of passive tolerance which may be a long-standing characteristic of ostreids supporting survival in extreme environments as well as during past and present climate oscillations.

Temperature adaptations of the thermophilic snail Echinolittorina malaccana: insights from metabolomic analysis

“…To understand the relationship between thermotolerance and certain metabolites and metabolic pathways, we compared our results with literature data on critical temperature [the temperature that is lethal for one-half of the study population (LT 50 ) and FLT], induction temperature (the temperature that induces increases in metabolites) and content of amino acids of common molluscs, including Littorina littorea (Melatunan et al, 2011;Newell et al, 1971), Littorina saxatilis (Sokolova et al, 2000a,b), Theodoxus fluviatilis (Wiesenthal et al, 2019), Haliotis fulgens (Tripp-Valdez et al, 2019), Crassostrea gigas (Ghaffari et al, 2019;Haider et al, 2020;Moreira et al, 2017;Moullac et al, 2007;Pazos et al, 1996;Yang et al, 2016), Ostrea edulis (Eymann et al, 2020), Mytilus galloprovincialis (Digilio et al, 2016;Han and Dong, 2020;Yao and Somero, 2012), Mytilus californianus (Yao and Somero, 2012), Perna canaliculus (Dunphy et al, 2018) and Laternula elliptica (Clark et al, 2017;Peck et al, 2002).…”

“…Gray symbols depict normalized concentrations of individuals, the solid black line within the box is the median, the upper dashed black line within the box is the 75th centile and the lower dashed black line within the box is the 25th centile, N=18-19. (M-O) The induction temperature (the temperature that induces increase in a metabolite) of metabolites in Group 1, Group 2 and Group 3, the temperature that is lethal for one-half of the study population (LT 50 ) and the flatline temperature (FLT) of E. malaccana were compared with those of Littorina littorea, Littorina saxatilis (Sokolova et al, 2000a;Sokolova et al, 2000b), Haliotis fulgens (Tripp-Valdez et al, 2019), Crassostrea gigas (Pazos et al, 1996;Moullac et al, 2007;Yang et al, 2016;Moreira et al, 2017;Ghaffari et al, 2019), Ostrea edulis (Eymann et al, 2020), Mytilus galloprovincialis (Yao and Somero, 2012;Digilio et al, 2016;Han and Dong et al, 2020), Mytilus californianus (Yao and Somero, 2012), Perna canaliculus (Dunphy et al, 2018) and Laternula elliptica (Peck et al, 2002;Clark et al, 2017). The x-axis shows the induction temperature; the y-axes show LT 50 and FLT.…”

“…The shift in metabolic balance that occurs with entry into metabolic depression is revealed by changes in metabolic end-products that are produced. For example, in Ostrea edulis, levels of succinate, malate and fumarate (biomarkers of anaerobic metabolism) were significantly elevated under heat stress (Eymann et al, 2020).…”

Plate-Based Respirometry to Assess Thermal Sensitivity of Zebrafish Embryo Bioenergetics in situ

“…The effect of warming will depend on the thermal niche of the respective species. Species living below their thermal optimum will benefit from warm conditions, while others close to their thermal limit will suffer ( Shephard et al, 2010 ; Eymann et al, 2020 ).…”

“…To measure thermal viability in aquatic ectotherms, several methodological approaches and model organisms with various thermal tolerance have been used, such as annelids ( Arenicola marina ) sipunculids ( Sipunculus nudus ), bivalves ( Ostrea edulis ), cephalopods ( Lolliguncula brevis ), mollusks ( Laternula elliptica ), crustaceans ( Maja squinado ), and teleost fish ( Fundulus heteroclitus ; Zielinski and Po, 1996 ; Pörtner and Zielinski, 1998 ; Urban and Silva, 1998 ; Sommer and Pörtner, 1999 ; Frederich et al, 2000 ; Schulte, 2015 ; Eymann et al, 2020 ). The range of parameters to judge thermal plasticity includes gene expression, enzyme activities, motility (e.g., swimming speed), and heart and metabolic rates (e.g., indirectly via oxygen consumption; Lahnsteiner and Mansour, 2012 ; Little et al, 2013 ; Ferreira et al, 2014 ; Veilleux et al, 2015 ; Pichaud et al, 2019 ).…”