Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings

Sandblom, Erik; Clark, Timothy D.; Gräns, Albin; Ekström, Andreas; Brijs, Jeroen; Sundström, L. Fredrik; Odelström, Anne; Adill, Anders; Aho, Teija; Jutfelt, Fredrik

doi:10.1038/ncomms11447

Cited by 213 publications

(260 citation statements)

References 38 publications

(47 reference statements)

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“…During acute warming in fish, whole-animal oxygen consumption rate generally increases with a temperature coefficient (Q 10 ) of 2-3 (Clark et al, 2008;Sandblom et al, 2016). When the warm exposure is prolonged, acclimation (i.e.…”

Section: Introductionmentioning

confidence: 99%

“…When the warm exposure is prolonged, acclimation (i.e. reversible phenotypic plasticity) may allow some species to fully or partially mitigate the direct thermodynamic effects on oxygen consumption rate and key cardiovascular variables such as heart rate (Ekström et al, 2016a;Sandblom et al, 2016). Such thermal responses at the whole-animal level can be linked to the need to redirect fuel reserves to power the metabolic pathways leading to the aerobic production of ATP by mitochondria (Iftikar and Hickey, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Dynamic changes in cardiac mitochondrial metabolism during warm acclimation in rainbow trout

Pichaud

Ekström

Hellgren

et al. 2017

Journal of Experimental Biology

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Although the mitochondrial metabolism responses to warm acclimation have been widely studied in fish, the time course of this process is less understood. Here, we characterized the changes of rainbow trout (Oncorhynchus mykiss) cardiac mitochondrial metabolism during acute warming from 10 to 16°C, and during the subsequent warm acclimation for 39 days. We repeatedly measured mitochondrial oxygen consumption in cardiac permeabilized fibers and the functional integrity of mitochondria (i.e. mitochondrial coupling and cytochrome c effect) at two assay temperatures (10 and 16°C), as well as the activities of citrate synthase (CS) and lactate dehydrogenase (LDH) at room temperature. LDH and CS activities significantly increased between day 0 (10°C acclimated fish) and day 1 (acute warming to 16°C) while mitochondrial oxygen consumption measured at respective in vivo temperatures did not change. Enzymatic activities and mitochondrial oxygen consumption rates significantly decreased by day 2, and remained stable during warm acclimation (days 2-39). The decrease in rates of oxygen between day 0 and day 1 coincided with an increased cytochrome c effect and a decreased mitochondrial coupling, suggesting a structural/ functional impairment of mitochondria during acute warming. We suggest that after 2 days of warm acclimation, a new homeostasis is reached, which may involve the removal of dysfunctional mitochondria. Interestingly, from day 2 onwards, there was a lack of differences in mitochondrial oxygen consumption rates between the assay temperatures, suggesting that warm acclimation reduces the acute thermal sensitivity of mitochondria. This study provides significant knowledge on the thermal sensitivity of cardiac mitochondria that is essential to delineate the contribution of cellular processes to warm acclimation.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Dynamic changes in cardiac mitochondrial metabolism during warm acclimation in rainbow trout

Pichaud

Ekström

Hellgren

et al. 2017

Journal of Experimental Biology

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“…The 'plastic floors and concrete ceilings' framework postulates ̇O 2STANDARD to be thermally plastic and ̇O 2MAX to be thermally fixed in fishes (Sandblom et al, 2016).…”

Section: Thermal Plasticity Of Aerobic Capacitymentioning

confidence: 99%

“…Moreover, assessing the sensitivity and flexibility of both resting and maximum cardiorespiratory functions is essential as disparities and trade-offs appear to be present and species specific (Sandblom et al, 2016). ̇O 2DIVE was the most thermally sensitive (Q10 = 7.4), followed by ̇O 2SURFACE (Q10 = 2.33) and ̇O 2STANDARD (Q10 = 2.28), and ̇O 2MAX was thermally insensitive (Q10 = 1.05).…”

Section: Relationship Between Diving Metabolism and Aerobic Capacitymentioning

confidence: 99%

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DIVING IN A WARMING WORLD: Thermal constraints on the diving capacity of estuarine crocodiles (Crocodylus porosus)

Rodgers¹

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A central challenge in conserving biodiversity is predicting the consequences of anthropogenic climate change on species' distributions and persistence. Forced climate change has severely altered thermal regimes in marine and freshwater habitats. Rapid escalations in environmental temperatures may be particularly threatening to ectothermic species (almost all plants, invertebrates, fish, amphibians and reptiles), where body temperature and concomitant functional performance are strongly tied to the thermal environment. The threat of overheating is salient for air-breathing, ectothermic divers, such as the estuarine crocodile (Crocodylus porosus, Schneider, 1801), because submergence times are inversely related to water temperature. It is unknown how C. porosus will fare in warming waters but diving oxygen stores are hypothesised to be consumed more rapidly at elevated temperatures leading to a reduction of aerobic dive limits (i.e. maximum submergence time before lactate is accumulated). Shorter dive durations may force animals to spend more time at the water surface, leaving less time available for obligate underwater activities (e.g. predator avoidance and hunting for aquatic prey).This thesis assessed the effect of elevated water temperatures (emulating climate change scenarios) on the diving physiology and behaviour of C. porosus. The thermal sensitivity of predator avoidance dives (i.e. minutes submerged) was assessed in juveniles at three water temperatures reflecting climate change scenarios (Chapter 2). Diving performance was thermally sensitive with dive durations halving between the 'no warming' and 'moderate warming' scenarios. Ectotherms are however revered for their thermal acclimation/acclimatisation capacity following long term exposure to novel temperatures; whereby an animal's underlying physiology is responsively altered to maintain or optimise performance. For this reason, the acclimation capacity of C. porosus was assessed by exposing crocodiles to thermal acclimation treatments for a minimum of 30 days. Thermal acclimation treatments had no effect on dive durations -a result indicative of absent thermal acclimation capacity at elevated temperatures within 30 days.ii The physiological mechanisms underlying compromised diving performance at elevated temperatures were subsequently examined (Chapter 3). Reduced diving performance was hypothesised to be linked to increased oxygen demands and a reduced capacity for metabolic depression at elevated temperatures. Diving oxygen uptake, diving heart rate and post-dive plasma-lactate concentrations were assessed at two test temperatures (i.e. 28•C and 34•C). Diving metabolic rate increased threefold between 28•C and 34•C and the capacity to depress metabolic demands (from surface levels) was inhibited by 46%. Post-dive plasma-lactate accumulation was independent of water temperature. Collectively, these results show the aerobic dive limit of C. porosus was significantly reduced at elevated temperatures and animals behaviourally terminated dives...

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Developmental temperature, more than long‐term evolution, defines thermal tolerance in an estuarine copepod

Ashlock,

Darwin,

Crooker

et al. 2024

Ecology and Evolution

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Climate change is resulting in increasing ocean temperatures and salinity variability, particularly in estuarine environments. Tolerance of temperature and salinity change interact and thus may impact organismal resilience. Populations can respond to multiple stressors in the short‐term (i.e., plasticity) or over longer timescales (i.e., adaptation). However, little is known about the short‐ or long‐term effects of elevated temperature on the tolerance of acute temperature and salinity changes. Here, we characterized the response of the near‐shore and estuarine copepod, Acartia tonsa, to temperature and salinity stress. Copepods originated from one of two sets of replicated >40 generation‐old temperature‐adapted lines: ambient (AM, 18°C) and ocean warming (OW, 22°C). Copepods from these lines were subjected to one and three generations at the reciprocal temperature. Copepods from all treatments were then assessed for differences in acute temperature and salinity tolerance. Development (one generation), three generations, and >40 generations of warming increased thermal tolerance compared to Ambient conditions, with development in OW resulting in equal thermal tolerance to three and >40 generations of OW. Strikingly, developmental OW and >40 generations of OW had no effect on low salinity tolerance relative to ambient. By contrast, when environmental salinity was reduced first, copepods had lower thermal tolerances. These results highlight the critical role for plasticity in the copepod climate response and suggest that salinity variability may reduce copepod tolerance to subsequent warming.

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Physiological constraints to climate warming in fish follow principles of plastic floors and concrete ceilings

Cited by 213 publications

References 38 publications

Dynamic changes in cardiac mitochondrial metabolism during warm acclimation in rainbow trout

Dynamic changes in cardiac mitochondrial metabolism during warm acclimation in rainbow trout

DIVING IN A WARMING WORLD: Thermal constraints on the diving capacity of estuarine crocodiles (Crocodylus porosus)

Developmental temperature, more than long‐term evolution, defines thermal tolerance in an estuarine copepod

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