Dissecting cause from consequence: a systematic approach to thermal limits

Abstract

Thermal limits mark the boundaries of ectotherm performance, and are increasingly appreciated as strong correlates and possible determinants of animal distribution patterns. The mechanisms setting the thermal limits of ectothermic animals are under active study and rigorous debate as we try to reconcile new observations in the lab and field with the knowledge gained from a long history of research on thermal adaptation. Here, I provide a perspective on our divided understanding of the mechanisms setting thermal limits of ectothermic animals. I focus primarily on the fundamental differences between high and low temperatures, and how animal form and environment can place different constraints on different taxa. Together, complexity and variation in animal form drive complexity in the interactions within and among levels of biological organization, creating a formidable barrier to determining mechanistic cause and effect at thermal limits. Progress in our understanding of thermal limits will require extensive collaboration and systematic approaches that embrace this complexity and allow us to separate the causes of failure from the physiological consequences that can quickly follow. I argue that by building integrative models that explain causal links among multiple organ systems, we can more quickly arrive at a holistic understanding of the varied challenges facing animals at extreme temperatures.

Physiological mechanisms linking cold acclimation and the poleward distribution limit of a range-extending marine fish

“…The OCLTT remains contentious; however, as for some species, temperatures that maximize aerobic scope have little relevance to real-world performance or temperature preference ( Fry, 1947 ; Clark et al , 2013 ; Norin et al , 2014 ; Jutfelt et al , 2018 ). The hypothesis predicts different mechanisms of oxygen limitation at low versus high temperatures ( Verberk et al , 2016 ; MacMillan, 2019 ) and thus could have predictive power at either temperature extreme even if not relevant at temperature optima or the other extreme. For example, energy allocation modelling of cod ( Gadus morhua ) based on the OCLTT predicts that fitness is optimized at a considerably lower temperature than aerobic scope, yet at temperature extremes, aerobic scope budgeting conflicts limit performance ( Holt and Jørgensen, 2015 ).…”

“…The OCLTT has scarcely been tested at long-term, sub-lethal temperatures ( Verberk , et al , 2016 ) or under naturally varying conditions ( Morash et al , 2018 ) relevant to range extensions. Thus, tests of this framework in the context of species’ range extensions are important because if the OCLTT has limited power to predict species’ cold range limits, research effort can be more fruitfully allocated towards other potential mechanisms ( Clark et al , 2013 ; Sinclair et al , 2016 ; MacMillan, 2019 ).…”

Hyperkalemia, not apoptosis, accurately predicts chilling injury in individual locusts

“…2) injury to the integrating neural centers, 3) loss of function in the neuromuscular excitationcontraction coupling (not investigated here), or 4) a combination of all three (1, 45).Cold-induced cell death in insect muscle is thought to be the consequence of a debilitating cascade, at the centre of which is a loss of ionoregulatory capacity that drives hemolymph hyperkalemia. This hyperkalemia, in turn, depolarizes muscle tissue and induces an excessive Ca 2+ influx, increasing the intracellular [Ca 2+ ], and this is thought to activate apoptotic/necrotic pathways and thereby drive injury phenotypes (1,18,[21][22][23]45). In our experiments we found that exposure to both prolonged cold and lethal heat (positive control) induced a marked increase in caspase-3-like activity in muscle tissue(Fig.…”

An impressive capacity for cold tolerance plasticity protects against ionoregulatory collapse in the disease vector,Aedes aegypti

“…1A), despite being more tolerant of chilling by every other measure. The CCO, CCRT, and chilling injury are all thought to be related to the capacity to maintain ion and water balance, but are mediated by different specific physiological mechanisms of failure occurring in different organs and across different time scales (MacMillan, 2019; Overgaard & MacMillan, 2017; Robertson et al, 2017). Our results in the present study thus suggest that acclimation alters mechanisms underlying CCRT and the development of chilling injury without impacting the temperature that causes paralysis.…”

“…While tolerance to extreme cold relies on a physiological capacity to avoid or survive ice formation inside the body, tolerance to chilling requires a physiological capacity to resist the effects of low temperature per se on organ, tissue, and cellular biochemistry (MacMillan, 2019; Overgaard & MacMillan, 2017; Teets & Denlinger, 2013). Consequently, measures of cold tolerance relevant to freeze avoidant and freeze tolerant insects, such as the supercooling point (the temperature of spontaneous ice formation within the body) or survival following freezing, are irrelevant to characterizing the thermal limits of chill susceptible insects (Overgaard & MacMillan, 2017).…”