Enhancing thermal tolerance by eliminating the pejus range: a comparative study with three decapod crustaceans

Abstract

Marine invertebrates in the intertidal and subtidal zones are often exposed to highly variable environmental conditions, especially rapid changes in temperature. The ability to survive at different temperatures has previously been described using an extended version of Shelford's law of tolerance, with optimum, pejus (Latin: 'turning worse'), and pessimum ranges, and the respective thresholds, critical (T c ) and pejus (T p ) temperatures, that mark the transition from one range into the next. The width of the pejus range, in which the scope for activity gradually declines, varies among species. We tested the hypothesis that the width of the pejus range is correlated to the temperature stability of the species' respective habitats. We used locomotor activity, heart rate, lactate accumulation, heat shock protein 70 (HSP70) levels, and the activation of AMPactivated protein kinase (AMPK) to identify T c and T p in 3 decapod crustaceans: green crab Carcinus maenas, rock crab Cancer irroratus, and lobster Homarus americanus. We found speciesspecific patterns of temperature-induced changes in all parameters, especially in HSP70 protein and AMPK activity. The width of the pejus range (between T p and T c ) was 8 to 12°C for rock crabs and 12 to 16°C for lobsters. Most importantly, green crab, the most temperature-tolerant of our 3 species and which lives in a highly variable habitat, switched directly from optimum to pessimum range, meaning that the pejus range was eliminated completely. Additionally, even lethal temperatures did not activate AMPK in green crabs, pointing to a different cellular tolerance strategy than in rock crabs and lobsters. This modified tolerance pattern might represent a broader strategy to enhance physiological tolerance in a highly variable habitat. KEY WORDS: AMP-activated protein kinase · AMPK · Heat shock protein 70 · HSP70 · Temperature stress · Critical temperatures Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 444: 263-274, 2012 264 ranges at both extremes. T c characterizes the transition into the pessimum range. However, in its natural environment an animal is frequently exposed to suboptimal conditions, often well before T c is attained. Consequently, Frederich & Pörtner (2000) added 'pejus temperature' (T p ) and 'pejus range' (from the Latin for 'turning worse') to this concept. In the pejus range, which is between the optimum and pessimum ranges, animals can still survive, but with a reduced scope for aerobic activity. Subsequent studies have identified T p and pejus ranges in various species of marine invertebrates and fish (reviewed by Pört-ner 2010). T p and T c differ by several degrees, thus in dicating a well-defined and broad pejus range. However, the width of the pejus range appears to vary among species, and the outstanding question of whether this is associated with habitat stability needs to be addressed.In a previous study on the rock crab Cancer irroratus, we showed that T p can be identified on the cell...

Oxygen-dependence of upper thermal limits in fishes

“…Although the two species were acclimated to different temperatures, as befitted the species, these data indicate that the lumpfish retained a lower oxygen supply capacity at CT max in normoxia when compared with red drum. It has been suggested that species occupying a wide thermal range (niche) have been evolutionarily selected for a more thermally resistant cardiorespiratory system (Ern et al, 2014;Jost et al, 2012). The differences in oxygen supply capacity at CT max , observed here for lumpfish and red drum, may therefore be related to the ecology of the two species.…”

“…It has also been suggested that oxygen-dependent upper thermal limits identified in the laboratory represent those in the field (Giomi et al, 2014;Pörtner and Knust, 2007). However, the link between oxygen supply capacity and upper thermal limits has recently been questioned, as other studies have reported that aerobic scope (AS, the difference between the maximum metabolic rate, MMR, and the standard metabolic rate, SMR) and cardiorespiratory performance are maintained in a number of fish and crustacean species experiencing ecologically relevant thermal extremes (Brijs et al, 2015;Clark et al, 2013;Ern et al, 2015Ern et al, , 2014Gräns et al, 2014;Healy and Schulte, 2012;Jost et al, 2012;Norin et al, 2014). It has, therefore, been suggested that some species possess a more thermally resistant cardiorespiratory system (Ern et al, 2014;Jost et al, 2012), and that insufficient tissue oxygen supply is not the primary determinant of upper thermal limits in all water-breathing ectotherms (Brijs et al, 2015;Wang et al, 2014).…”

Oxygen delivery does not limit thermal tolerance in a tropical eurythermal crustacean

“…In crustaceans, several studies over the past decade have reported such limitations in the oxygen supply capacity at high temperatures, revealed as a decline in cardiac and ventilatory performance as well as reductions in oxygen levels in the hemolymph with increasing temperature (Frederich and Pörtner, 2000;Frederich et al, 2009;Marshall et al, 2011;Jost et al, 2012). As further support for the OCLTT model, several marine invertebrates, including crustaceans, resort to anaerobic metabolism when approaching their upper thermal limit (Taylor et al, 1973;Taylor et al, 1977;Sommer et al, 1997;Frederich and Pörtner, 2000;Peck et al, 2002;Sokolova and Pörtner, 2003).…”

Physiological Performances of Temperate Vegetables with Response to Chronic and Acute Heat Stress

“…Arguably, while organismal mortality, pessimum (least favourable conditions, usually the switch from aerobic to anaerobic respiration) and pejus (=getting worse; compromise of physiological performances) may be difficult to pinpoint in the study of plant stress response (c.f. [47] [48]), it is proposed in this study here that for photosynthetic parameters, F v /F m ratio approaches the pessimum (CT max : critical thermal maxima, see [49] [50]) if not the upper lethal limit of organismal survival while LT 50 values of photosynthetic O 2 evolution could represent the onset of photosynthetic compromises (pejus) due to the increasing heat stress.…”