scholarly journals Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms

2002 ◽  
Vol 205 (15) ◽  
pp. 2217-2230 ◽  
Author(s):  
H. O. Pörtner

SUMMARYPolar, especially Antarctic, oceans host ectothermic fish and invertebrates characterized by low-to-moderate levels of motor activity; maximum performance is reduced compared with that in warmer habitats. The present review attempts to identify the trade-offs involved in adaptation to cold in the light of progress in the physiology of thermal tolerance. Recent evidence suggests that oxygen limitations and a decrease in aerobic scope are the first indications of tolerance limits at both low and high temperature extremes. The cold-induced reduction in aerobic capacity is compensated for at the cellular level by elevated mitochondrial densities, accompanied by molecular and membrane adjustments for the maintenance of muscle function. Particularly in the muscle of pelagic Antarctic fish, among notothenioids, the mitochondrial volume densities are among the highest known for vertebrates and are associated with cold compensation of aerobic metabolic pathways, a reduction in anaerobic scope, rapid recovery from exhaustive exercise and enhanced lipid stores as well as a preference for lipid catabolism characterized by high energy efficiency at high levels of ambient oxygen supply. Significant anaerobic capacity is still found at the very low end of the activity spectrum, e.g. among benthic eelpout (Zoarcideae).In contrast to the cold-adapted eurytherms of the Arctic, polar (especially Antarctic) stenotherms minimize standard metabolic rate and, as a precondition, the aerobic capacity per milligram of mitochondrial protein,thereby minimizing oxygen demand. Cost reductions are supported by the downregulation of the cost and flexibility of acid—base regulation. At maintained factorial scopes, the reduction in standard metabolic rate will cause net aerobic scope to be lower than in temperate species. Loss of contractile myofilaments and, thereby, force results from space constraints due to excessive mitochondrial proliferation. On a continuum between low and moderately high levels of muscular activity, polar fish have developed characteristics of aerobic metabolism equivalent to those of high-performance swimmers in warmer waters. However, they only reach low performance levels despite taking aerobic design to an extreme.

2016 ◽  
Vol 73 (10) ◽  
pp. 1493-1506 ◽  
Author(s):  
David Allen ◽  
Jordan Rosenfeld ◽  
Jeffrey Richards

Adaptive trade-offs define the trait combinations that differentiate taxa and allow coexistence along environmental gradients. To understand the physiological trade-offs associated with growth, we examined relationships among metabolic rate, digestive capacity, tissue energy content, and growth in juveniles of three strains of rainbow trout (Oncorhynchus mykiss) that differ in growth. Fish were reared under satiation, 1% of body mass per day, and complete food deprivation treatments to assess differences in performance and adaptive trade-offs along a gradient of resource availability. The fast-growing hatchery strain had higher standard metabolic rate (SMR), lower aerobic scope, and potentially lower maximum metabolic rates, suggesting that high growth trades off against a reduced capacity to do metabolic work. Trout with high growth rates also generally had larger gastrointestinal tracts, maximum food consumption, and growth efficiency. Results demonstrate (i) higher SMR of fast growers appears to be related to a greater investment in high-maintenance digestive tissue that supports rapid growth; (ii) growth appears to trade off against active metabolism; and (iii) selection on growth involves a suite of integrated physiological and anatomical traits that are affected by both genotype and environment (ration).


2015 ◽  
Vol 11 (2) ◽  
pp. 20141032 ◽  
Author(s):  
Rebecca E. Holt ◽  
Christian Jørgensen

The difference between maximum metabolic rate and standard metabolic rate is referred to as aerobic scope, and because it constrains performance it is suggested to constitute a key limiting process prescribing how fish may cope with or adapt to climate warming. We use an evolutionary bioenergetics model for Atlantic cod ( Gadus morhua ) to predict optimal life histories and behaviours at different temperatures. The model assumes common trade-offs and predicts that optimal temperatures for growth and fitness lie below that for aerobic scope; aerobic scope is thus a poor predictor of fitness at high temperatures. Initially, warming expands aerobic scope, allowing for faster growth and increased reproduction. Beyond the optimal temperature for fitness, increased metabolic requirements intensify foraging and reduce survival; oxygen budgeting conflicts thus constrain successful completion of the life cycle. The model illustrates how physiological adaptations are part of a suite of traits that have coevolved.


Metabolites ◽  
2021 ◽  
Vol 11 (7) ◽  
pp. 447
Author(s):  
Yangfan Zhang ◽  
Bog E. So ◽  
Anthony P. Farrell

The utility of measuring whole-animal performance to frame the metabolic response to environmental hypoxia is well established. Progressively reducing ambient oxygen (O2) will initially limit maximum metabolic rate as a result of a hypoxemic state and ultimately lead to a time-limited, tolerance state supported by substrate-level phosphorylation when the O2 supply can no longer meet basic needs (standard metabolic rate, SMR). The metabolic consequences of declining ambient O2 were conceptually framed for fishes initially by Fry’s hypoxic performance curve, which characterizes the hypoxemic state and its consequences to absolute aerobic scope (AAS), and Hochachka’s concept of scope for hypoxic survival, which characterizes time-limited life when SMR cannot be supported by O2 supply. Yet, despite these two conceptual frameworks, the toolbox to assess whole-animal metabolic performance remains rather limited. Here, we briefly review the ongoing debate concerning the need to standardize the most commonly used assessments of respiratory performance in hypoxic fishes, namely critical O2 (the ambient O2 level below which maintenance metabolism cannot be sustained) and the incipient lethal O2 (the ambient O2 level at which a fish loses the ability to maintain upright equilibrium), and then we advance the idea that the most useful addition to the toolbox will be the limiting-O2 concentration (LOC) performance curve. Using Fry & Hart’s (1948) hypoxia performance curve concept, an LOC curve was subsequently developed as an eco-physiological framework by Neil et al. and derived for a group of fish during a progressive hypoxia trial by Claireaux and Lagardère (1999). In the present review, we show how only minor modifications to available respirometry tools and techniques are needed to generate an LOC curve for individual fish. This individual approach to the LOC curve determination then increases its statistical robustness and importantly opens up the possibility of examining individual variability. Moreover, if peak aerobic performance at a given ambient O2 level of each individual is expressed as a percentage of its AAS, the water dissolved O2 that supports 50% of the individual’s AAS (DOAAS-50) can be interpolated much like the P50 for an O2 hemoglobin dissociation curve (when hemoglobin is 50% saturated with O2). Thus, critical O2, incipient lethal O2, DOAAS-50 and P50 and can be directly compared within and across species. While an LOC curve for individual fish represents a start to an ongoing need to seamlessly integrate aerobic to anaerobic capacity assessments in a single, multiplexed respirometry trial, we close with a comparative exploration of some of the known whole-organism anaerobic and aerobic capacity traits to examine for correlations among them and guide the next steps.


1976 ◽  
Vol 231 (3) ◽  
pp. 903-912 ◽  
Author(s):  
B Pinshow ◽  
MA Fedak ◽  
DR Battles ◽  
K Schmidt-Nielsen

During the antarctic winter emperor penguins (Aptenodytes forsteri) spend up to four mo fasting while they breed at rookeries 80 km or more from the sea, huddling close together in the cold. This breeding cycle makes exceptional demands on their energy reserves, and we therefore studied their thermoregulation and locomotion. Rates of metabolism were measured in five birds (mean body mass, 23.37 kg) at ambient temperatures ranging from 25 to -47 degrees C. Between 20 and -10 degrees C the metabolic rate (standard metabolic rate (SMR)) remained neraly constant, about 42.9 W. Below -10 degrees C metabolic rate increased lineraly with decreasing ambient temperature and at -47 degrees C it was 70% above the SMR. Mean thermal conductance below -10 degrees C was 1.57 W m-2 degrees C-1. Metabolic rate during treadmill walking increased linearly with increasing speed. Our data suggest that walking 200 km (from the sea to the rookery and back) requires less than 15% of the energy reserves of a breeding male emperor penguin initially weighing 35 kg. The high energy requirement for thermoregulation (about 85%) would, in the absence of huddling, probably exceed the total energy reserves.


2011 ◽  
Vol 279 (1727) ◽  
pp. 357-364 ◽  
Author(s):  
Shaun S. Killen ◽  
Stefano Marras ◽  
John F. Steffensen ◽  
David J. McKenzie

The schooling behaviour of fish is of great biological importance, playing a crucial role in the foraging and predator avoidance of numerous species. The extent to which physiological performance traits affect the spatial positioning of individual fish within schools is completely unknown. Schools of juvenile mullet Liza aurata were filmed at three swim speeds in a swim tunnel, with one focal fish from each school then also measured for standard metabolic rate (SMR), maximal metabolic rate (MMR), aerobic scope (AS) and maximum aerobic swim speed. At faster speeds, fish with lower MMR and AS swam near the rear of schools. These trailing fish required fewer tail beats to swim at the same speed as individuals at the front of schools, indicating that posterior positions provide hydrodynamic benefits that reduce swimming costs. Conversely, fish with high aerobic capacity can withstand increased drag at the leading edge of schools, where they could maximize food intake while possibly retaining sufficient AS for other physiological functions. SMR was never related to position, suggesting that high maintenance costs do not necessarily motivate individuals to occupy frontal positions. In the wild, shifting of individuals to optimal spatial positions during changing conditions could influence structure or movement of entire schools.


2015 ◽  
Vol 29 (4) ◽  
pp. 479-486 ◽  
Author(s):  
Sonya K. Auer ◽  
Karine Salin ◽  
Agata M. Rudolf ◽  
Graeme J. Anderson ◽  
Neil B. Metcalfe

Author(s):  
Emily A. Hardison ◽  
Krista Kraskura ◽  
Jacey Van Wert ◽  
Tina Nguyen ◽  
Erika J. Eliason

Thermal acclimation is a key process enabling ectotherms to cope with temperature change. To undergo a successful acclimation response, ectotherms require energy and nutritional building blocks obtained from their diet. However, diet is often overlooked as a factor that can alter acclimation responses. Using a temperate omnivorous fish, opaleye (Girella nigricans), as a model system, we tested the hypotheses that 1) diet can impact the magnitude of thermal acclimation responses and 2) traits vary in their sensitivity to both temperature acclimation and diet. We fed opaleye a simple omnivorous diet (ad libitum Artemia sp. and Ulva sp.) or a carnivorous diet (ad libitum Artemia sp.) at two ecologically relevant temperatures (12 and 20°C) and measured a suite of whole animal (growth, sprint speed, metabolism), organ (cardiac thermal tolerance), and cellular-level traits (oxidative stress, glycolytic capacity). When opaleye were offered two diet options compared to one, they had reduced cardiovascular thermal performance and higher standard metabolic rate under conditions representative of the maximal seasonal temperature the population experiences (20°C). Further, sprint speed and absolute aerobic scope were insensitive to diet and temperature, while growth was highly sensitive to temperature but not diet, and standard metabolic rate and maximum heart rate were sensitive to both diet and temperature. Our results reveal that diet influences thermal performance in trait-specific ways, which could create diet trade-offs for generalist ectotherms living in thermally variable environments. Ectotherms that alter their diet may be able to regulate their performance at different environmental temperatures.


2014 ◽  
Vol 281 (1794) ◽  
pp. 20141490 ◽  
Author(s):  
Erik Sandblom ◽  
Albin Gräns ◽  
Michael Axelsson ◽  
Henrik Seth

Temperature acclimation may offset the increased energy expenditure (standard metabolic rate, SMR) and reduced scope for activity (aerobic scope, AS) predicted to occur with local and global warming in fishes and other ectotherms. Yet, the time course and mechanisms of this process is little understood. Acclimation dynamics of SMR, maximum metabolic rate, AS and the specific dynamic action of feeding (SDA) were determined in shorthorn sculpin ( Myoxocephalus scorpius ) after transfer from 10°C to 16°C. SMR increased in the first week by 82% reducing AS to 55% of initial values, while peak postprandial metabolism was initially greater. This meant that the estimated AS during peak SDA approached zero, constraining digestion and leaving little room for additional aerobic processes. After eight weeks at 16°C, SMR was restored, while AS and the estimated AS during peak SDA recovered partly. Collectively, this demonstrated a considerable capacity for metabolic thermal compensation, which should be better incorporated into future models on organismal responses to climate change. A mathematical model based on the empirical data suggested that phenotypes with fast acclimation rates may be favoured by natural selection as the accumulated energetic cost of a slow acclimation rate increases in a warmer future with exacerbated thermal variations.


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