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Journal ArticleDOI

Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations

01 Aug 2013-The Journal of Experimental Biology (The Company of Biologists Ltd)-Vol. 216, Iss: 15, pp 2771-2782
TL;DR: It is the intention of this paper to encourage transparency and accuracy in future studies that measure the aerobic metabolism of fishes, and to highlight the fundamental issues with assuming broad relevance of the OCLTT hypothesis.
Abstract: Measurements of aerobic scope [the difference between minimum and maximum oxygen consumption rate (![Graphic][1] and ![Graphic][2] , respectively)] are increasing in prevalence as a tool to address questions relating to fish ecology and the effects of climate change. However, there are underlying issues regarding the array of methods used to measure aerobic scope across studies and species. In an attempt to enhance quality control before the diversity of issues becomes too great to remedy, this paper outlines common techniques and pitfalls associated with measurements of ![Graphic][3] , ![Graphic][4] and aerobic scope across species and under different experimental conditions. Additionally, we provide a brief critique of the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis, a concept that is intricately dependent on aerobic scope measurements and is spreading wildly throughout the literature despite little evidence for its general applicability. It is the intention of this paper to encourage transparency and accuracy in future studies that measure the aerobic metabolism of fishes, and to highlight the fundamental issues with assuming broad relevance of the OCLTT hypothesis. [1]: /embed/inline-graphic-1.gif [2]: /embed/inline-graphic-2.gif [3]: /embed/inline-graphic-3.gif [4]: /embed/inline-graphic-4.gif

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Citations
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Journal ArticleDOI
31 Mar 2017-Science
TL;DR: The negative effects of climate change cannot be adequately anticipated or prepared for unless species responses are explicitly included in decision-making and global strategic frameworks, and feedbacks on climate itself are documented.
Abstract: Distributions of Earth’s species are changing at accelerating rates, increasingly driven by human-mediated climate change. Such changes are already altering the composition of ecological communities, but beyond conservation of natural systems, how and why does this matter? We review evidence that climate-driven species redistribution at regional to global scales affects ecosystem functioning, human well-being, and the dynamics of climate change itself. Production of natural resources required for food security, patterns of disease transmission, and processes of carbon sequestration are all altered by changes in species distribution. Consideration of these effects of biodiversity redistribution is critical yet lacking in most mitigation and adaptation strategies, including the United Nation’s Sustainable Development Goals.

1,917 citations


Cites background from "Aerobic scope measurements of fishe..."

  • ...For example, specific physiological mechanisms have been hypothesized to underlie the thermal ranges of ectothermic organisms (94), yet a lack of universality in the proposedmechanisms highlights a need for novel, multidisciplinary investigations (95)....

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Journal ArticleDOI
TL;DR: A view of why current theories provide an inadequate mechanistic account of the effects of temperature on aerobic metabolic processes across levels of organization from individual proteins to intact animals is presented.
Abstract: Because of its profound effects on the rates of biological processes such as aerobic metabolism, environmental temperature plays an important role in shaping the distribution and abundance of species. As temperature increases, the rate of metabolism increases and then rapidly declines at higher temperatures – a response that can be described using a thermal performance curve (TPC). Although the shape of the TPC for aerobic metabolism is often attributed to the competing effects of thermodynamics, which can be described using the Arrhenius equation, and the effects of temperature on protein stability, this account represents an over-simplification of the factors acting even at the level of single proteins. In addition, it cannot adequately account for the effects of temperature on complex multistep processes, such as aerobic metabolism, that rely on mechanisms acting across multiple levels of biological organization. The purpose of this review is to explore our current understanding of the factors that shape the TPC for aerobic metabolism in response to acute changes in temperature, and to highlight areas where this understanding is weak or insufficient. Developing a more strongly grounded mechanistic model to account for the shape of the TPC for aerobic metabolism is crucial because these TPCs are the foundation of several recent attempts to predict the responses of species to climate change, including the metabolic theory of ecology and the hypothesis of oxygen and capacity-limited thermal tolerance.

499 citations


Cites background from "Aerobic scope measurements of fishe..."

  • ...In addition, recent work in a variety of species of fishes has indicated that, at least in some species, aerobic scope can still be high at temperatures at which growth and reproduction are compromised, suggesting that thermal limitations on aerobic capacity cannot be the direct cause of fitness limitations in these species (Healy and Schulte, 2012; Clark et al., 2013a; Gräns et al., 2014; Norin et al., 2014)....

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  • ...As a result of these divergent observations, there is currently a very lively debate in the literature with respect to the relevance of the OCLTT for predicting the responses of species to climate change (Clark et al., 2013a,b; Pörtner and Giomi, 2013; Farrell, 2013)....

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  • ...…can still be high at temperatures at which growth and reproduction are compromised, suggesting that thermal limitations on aerobic capacity cannot be the direct cause of fitness limitations in these species (Healy and Schulte, 2012; Clark et al., 2013a; Gräns et al., 2014; Norin et al., 2014)....

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  • ...In fact, different conceptions of what is meant by the term aerobic scope may underlie some of the debate about the concept (Clark et al., 2013a,b; Pörtner and Giomi, 2013; Farrell, 2013)....

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Journal ArticleDOI
TL;DR: The main objective was to compare eight methods to estimate SMR and show that 12 h is insufficient but 24 h is adequate, and a list of basic recommendations for practitioners who use respirometry to measure SMR in fishes is provided.
Abstract: This review and data analysis outline how fish biologists should most reliably estimate the minimal amount of oxygen needed by a fish to support its aerobic metabolic rate (termed standard metabolic rate; SMR). By reviewing key literature, it explains the theory, terminology and challenges underlying SMR measurements in fishes, which are almost always made using respirometry (which measures oxygen uptake, ṀO2 ). Then, the practical difficulties of measuring SMR when activity of the fish is not quantitatively evaluated are comprehensively explored using 85 examples of ṀO2 data from different fishes and one crustacean, an analysis that goes well beyond any previous attempt. The main objective was to compare eight methods to estimate SMR. The methods were: average of the lowest 10 values (low10) and average of the 10% lowest ṀO2 values, after removing the five lowest ones as outliers (low10%), mean of the lowest normal distribution (MLND) and quantiles that assign from 10 to 30% of the data below SMR (q0·1 , q0·15 , q0·2 , q0·25 and q0·3 ). The eight methods yielded significantly different SMR estimates, as expected. While the differences were small when the variability was low amongst the ṀO2 values, they were important (>20%) for several cases. The degree of agreement between the methods was related to the c.v. of the observations that were classified into the lowest normal distribution, the c.v. MLND (C.V.MLND ). When this indicator was low (≤5·4), it was advantageous to use the MLND, otherwise, one of the q0·2 or q0·25 should be used. The second objective was to assess if the data recorded during the initial recovery period in the respirometer should be included or excluded, and the recommendation is to exclude them. The final objective was to determine the minimal duration of experiments aiming to estimate SMR. The results show that 12 h is insufficient but 24 h is adequate. A list of basic recommendations for practitioners who use respirometry to measure SMR in fishes is provided.

398 citations


Cites background from "Aerobic scope measurements of fishe..."

  • ...Similarly, some gregarious species such as Atlantic menhaden Brevoortia tyrannus (Latrobe 1802) may become hyperactive, stressed and even die when tested alone (Hettler, 1976) such that testing in groups is necessary....

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  • ...Minimally, fishes are typically placed in respirometers for 10–48 h before starting to measure ṀO2 to minimize handling stress (Clausen, 1936; Fry & Hart, 1948; Clark et al., 2013)....

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  • ...When considering adaptability or susceptibility to a slow temperature change, such as global warming, aerobic scope needs © 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, 88, 81–121 to be measured in thermally acclimated fishes (Clark et al., 2013)....

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  • ...…water’, or water that previously contained fishes (Winberg, 1960) or water from the tank where the fish was previously held (Fry, 1971), but it has never been shown that these measures lower ṀO2 when respirometer design is appropriate and fishes are properly acclimated to experimental conditions....

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Journal ArticleDOI
TL;DR: The present review presents a clear message that ocean acidification may cause significant effects on fish across multiple physiological systems, suggesting that pH compensation does not necessarily confer tolerance as downstream consequences and tradeoffs occur.
Abstract: Most fish studied to date efficiently compensate for a hypercapnic acid-base disturbance; however, many recent studies examining the effects of ocean acidification on fish have documented impacts a...

359 citations

Journal ArticleDOI
TL;DR: Various techniques used to elicit and measure maximum (aerobic) metabolic rate in different fish species with contrasting lifestyles are outlined and the relevance of MMR to the ecology, fitness and climate change resilience of fishes is discussed.
Abstract: Maximum (aerobic) metabolic rate (MMR) is defined here as the maximum rate of oxygen consumption (M˙O2max ) that a fish can achieve at a given temperature under any ecologically relevant circumstance. Different techniques exist for eliciting MMR of fishes, of which swim-flume respirometry (critical swimming speed tests and burst-swimming protocols) and exhaustive chases are the most common. Available data suggest that the most suitable method for eliciting MMR varies with species and ecotype, and depends on the propensity of the fish to sustain swimming for extended durations as well as its capacity to simultaneously exercise and digest food. MMR varies substantially (>10 fold) between species with different lifestyles (i.e. interspecific variation), and to a lesser extent (

284 citations


Cites background or methods from "Aerobic scope measurements of fishe..."

  • ...Having said that, it is fundamental that metabolic measurements are performed accurately and with proven reproducibility, such that the understanding of the topic is not confounded by experimental artefacts (Clark et al., 2013a)....

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  • ...…and the thermal dependence of aerobic scope (Pörtner & Knust, 2007; Pörtner & Farrell, 2008; Clark et al., 2013a, b; Jutfelt et al., 2014) and the perceived simplicity of measuring aerobic metabolism using respirometry (Steffensen, 1989; Clark et al., 2013a; Nelson, 2016; Svendsen et al., 2016)....

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  • ...This design was later modified by Steffensen [see design in Clark et al. (2013a); Roche et al. (2014); www.loligosystems.com] to consist of an oval (racetrack) shaped plexiglass chamber with a partitioning in the centre that allowed a water flow over the swimming fish on one side created by a…...

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  • ...E X H AU S T I V E C H A S E P ROT O C O L An exhaustive chase protocol, where the experimenter manually chases the fish to exhaustion, is the next most common method for eliciting MMR in fishes (Soofiani & Priede, 1985; Reidy et al., 1995; Clark et al., 2013a; Roche et al., 2013)....

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  • ...…owing largely to the proposed link between fitness and the thermal dependence of aerobic scope (Pörtner & Knust, 2007; Pörtner & Farrell, 2008; Clark et al., 2013a, b; Jutfelt et al., 2014) and the perceived simplicity of measuring aerobic metabolism using respirometry (Steffensen, 1989;…...

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References
More filters
Journal ArticleDOI
01 Jul 2004-Ecology
TL;DR: This work has developed a quantitative theory for how metabolic rate varies with body size and temperature, and predicts how metabolic theory predicts how this rate controls ecological processes at all levels of organization from individuals to the biosphere.
Abstract: Metabolism provides a basis for using first principles of physics, chemistry, and biology to link the biology of individual organisms to the ecology of populations, communities, and ecosystems. Metabolic rate, the rate at which organisms take up, transform, and expend energy and materials, is the most fundamental biological rate. We have developed a quantitative theory for how metabolic rate varies with body size and temperature. Metabolic theory predicts how metabolic rate, by setting the rates of resource uptake from the environment and resource allocation to survival, growth, and reproduction, controls ecological processes at all levels of organization from individuals to the biosphere. Examples include: (1) life history attributes, including devel- opment rate, mortality rate, age at maturity, life span, and population growth rate; (2) population interactions, including carrying capacity, rates of competition and predation, and patterns of species diversity; and (3) ecosystem processes, including rates of biomass production and respiration and patterns of trophic dynamics. Data compiled from the ecological literature strongly support the theoretical predictions. Even- tually, metabolic theory may provide a conceptual foundation for much of ecology, just as genetic theory provides a foundation for much of evolutionary biology.

6,017 citations


"Aerobic scope measurements of fishe..." refers background in this paper

  • ...2771 Introduction Measurements of aerobic metabolic rate (≈oxygen consumption rate, MO2) are becoming increasingly popular to address questions relating to animal ecology owing to hypotheses like the metabolic theory of ecology (Brown et al., 2004; Whitfield, 2004; Price et al., 2012)....

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Book
01 Jan 1962
TL;DR: In this article, the authors present an overview of the physiological properties of the human body, including Oxygen, Respiration, Food and Energy, Water and osmotic regulation, control and integration, and Hormone control.
Abstract: Preface Part I. Oxygen: 1. Respiration 2. Blood 3. Circulation Part II. Food and Energy: 4. Food and fuel 5. Energy metabolism Part III. Temperature: 6. Temperature effects 7. Temperature regulation Part IV. Water: 8. Water and osmotic regulation 9. Excretion Part V. Movement, Information, Integration: 10. Movement, muscle, biomechanics 11. Control and integration 12. Hormonal control 13. Information and senses Appendices Index.

2,520 citations

Journal ArticleDOI
31 Oct 2008-Science
TL;DR: Studies of physiological mechanisms are needed to predict climate effects on ecosystems at species and community levels and to help scientists understand the drivers of climate change.
Abstract: Studies of physiological mechanisms are needed to predict climate effects on ecosystems at species and community levels.

2,055 citations


"Aerobic scope measurements of fishe..." refers background or result in this paper

  • ...This idea has guided the interpretations of many researchers (e.g. Pörtner and Knust, 2007; Pörtner and Farrell, 2008; Nilsson et al., 2009; Gardiner et al., 2010; Donelson et al., 2011; Neuheimer et al., 2011; Miller et al., 2012; Comte and Grenouillet, 2013), as it promises an elegant,…...

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  • ...Hypothetical curves depicting changes in aerobic performance (aerobic scope) of fishes with temperature, where A is redrawn from Pörtner and Farrell (Pörtner and Farrell, 2008) and B is an alternative explanation of how aerobic performance responds to temperature and interacts with animal performance [based on Clark et al. (Clark et al., 2011)]....

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  • ...The OCLTT hypothesis states that at a species’ upper pejus temperature (where the aerobic scope starts to drop), the performance decreases because of reduced aerobic scope, which in turn leads to reduced tissue oxygen levels (tissue hypoxia) (Pörtner and Farrell, 2008)....

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  • ...Clark, T. D., Jeffries, K. M., Hinch, S. G. and Farrell, A. P. (2011)....

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  • ...…of temperatures and subsequently determine the temperature at which aerobic scope is maximal (ToptAS), as it has been proposed that processes such as growth and reproductive output are maximised at this temperature (Brett, 1971; Pörtner and Knust, 2007; Pörtner and Farrell, 2008; Pörtner, 2010)....

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Journal ArticleDOI
TL;DR: Rate of replacement of oxygen debt following fatigue was determined by tracing the return to a resting state of metabolism, and confirmed by re-tests at fatigue velocities, and in most instances the rate declined logarithmically with time.
Abstract: The rate of oxygen consumption in young sockeye salmon (Oncorhynchus nerka) was determined for various swimming speeds, including fatigue levels, at temperatures of 5, 10, 15, 20, and 24 °C. A loga...

1,952 citations


"Aerobic scope measurements of fishe..." refers background in this paper

  • ...…respirometers are usually rounded-rectangular in shape and contain a propeller (or impeller) that circulates water in one direction, while the fish is restricted to one of the long compartments called the ‘working section’, where a laminar flow profile is desired (Fig.3A) (Brett, 1964; Fry, 1971)....

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Journal ArticleDOI
05 Jan 2007-Science
TL;DR: It is shown in the eelpout, Zoarces viviparus, a bioindicator fish species for environmental monitoring from North and Baltic Seas, that thermally limited oxygen delivery closely matches environmental temperatures beyond which growth performance and abundance decrease, which will be the first process to cause extinction or relocation to cooler waters.
Abstract: A cause-and-effect understanding of climate influences on ecosystems requires evaluation of thermal limits of member species and of their ability to cope with changing temperatures. Laboratory data available for marine fish and invertebrates from various climatic regions led to the hypothesis that, as a unifying principle, a mismatch between the demand for oxygen and the capacity of oxygen supply to tissues is the first mechanism to restrict whole-animal tolerance to thermal extremes. We show in the eelpout, Zoarces viviparus, a bioindicator fish species for environmental monitoring from North and Baltic Seas (Helcom), that thermally limited oxygen delivery closely matches environmental temperatures beyond which growth performance and abundance decrease. Decrements in aerobic performance in warming seas will thus be the first process to cause extinction or relocation to cooler waters.

1,798 citations


"Aerobic scope measurements of fishe..." refers background or result in this paper

  • ...…of temperatures and subsequently determine the temperature at which aerobic scope is maximal (ToptAS), as it has been proposed that processes such as growth and reproductive output are maximised at this temperature (Brett, 1971; Pörtner and Knust, 2007; Pörtner and Farrell, 2008; Pörtner, 2010)....

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  • ...While processes such as growth and reproductive output are suggested, as a unifying principle, to be directly determined by the available aerobic scope (Pörtner and Knust, 2007; Pörtner and Farrell, 2008), studies linking such fundamental processes with aerobic scope under chronic thermal exposures remain scarce....

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  • ...In particular, measurements of MO2 are proliferating in the context of fish biology and climate change, largely because of renewed interest and further developments in the hypothesis relating aerobic scope (the difference between minimum and maximum MO2; MO2,min and MO2,max, respectively) to whole-animal performance and fitness (Fry, 1947; Brett, 1971; Claireaux and Lefrançois, 2007; Pörtner and Knust, 2007; Farrell et al., 2008; Pörtner et al., 2008; Pörtner and Farrell, 2008; Munday et al., 2009; Nilsson et al., 2009; Pörtner, 2010; Pörtner and Peck, 2010; Clark et al., 2011; Eliason et al., 2011; Donelson et al., 2012; Munday et al., 2012; Pörtner, 2012)....

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  • ...…and maximum MO2; MO2,min and MO2,max, respectively) to whole-animal performance and fitness (Fry, 1947; Brett, 1971; Claireaux and Lefrançois, 2007; Pörtner and Knust, 2007; Farrell et al., 2008; Pörtner et al., 2008; Pörtner and Farrell, 2008; Munday et al., 2009; Nilsson et al., 2009; Pörtner,…...

    [...]

  • ...This idea has guided the interpretations of many researchers (e.g. Pörtner and Knust, 2007; Pörtner and Farrell, 2008; Nilsson et al., 2009; Gardiner et al., 2010; Donelson et al., 2011; Neuheimer et al., 2011; Miller et al., 2012; Comte and Grenouillet, 2013), as it promises an elegant,…...

    [...]