Partitioning the metabolic scope: the importance of anaerobic metabolism and implications for the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis

Ejbye-Ernst, Rasmus; Michaelsen, Thomas Yssing; Tirsgaard, Bjørn; Wilson, Jonathan M.; Jensen, Lasse Fast; Steffensen, John F.; Pertoldi, Cino; Aarestrup, Kim; Svendsen, Jon Christian

doi:10.1093/conphys/cow019

Cited by 22 publications

(14 citation statements)

References 111 publications

(192 reference statements)

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“…The models were constrained to swimming speeds less than or equal to U MAX,C and the swimming speed that produced Ṁ O2,MAX . Above these values, performance metrics are confounded by an increasing anaerobic contribution to swimming performance ( Rome, 1995 ; Rome, 2007 ; Marras , et al , 2013 ; Ejbye-Ernst et al , 2016 ). Swimming speed was modelled as second- and third-degree raw polynomials in the mass-specific Ṁ O2 and cost of swimming one body length models, respectively.…”

Section: Methodsmentioning

confidence: 99%

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

Wolfe

Fitzgibbon

Semmens

et al. 2020

Conservation Physiology

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Extensions of species’ geographical distributions, or range extensions, are among the primary ecological responses to climate change in the oceans. Considerable variation across the rates at which species’ ranges change with temperature hinders our ability to forecast range extensions based on climate data alone. To better manage the consequences of ongoing and future range extensions for global marine biodiversity, more information is needed on the biological mechanisms that link temperatures to range limits. This is especially important at understudied, low relative temperatures relevant to poleward range extensions, which appear to outpace warm range edge contractions four times over. Here, we capitalized on the ongoing range extension of a teleost predator, the Australasian snapper Chrysophrys auratus, to examine multiple measures of ecologically relevant physiological performance at the population’s poleward range extension front. Swim tunnel respirometry was used to determine how mid-range and poleward range edge winter acclimation temperatures affect metabolic rate, aerobic scope, swimming performance and efficiency and recovery from exercise. Relative to ‘optimal’ mid-range temperature acclimation, subsequent range edge minimum temperature acclimation resulted in absolute aerobic scope decreasing while factorial aerobic scope increased; efficiency of swimming increased while maximum sustainable swimming speed decreased; and recovery from exercise required a longer duration despite lower oxygen payback. Cold-acclimated swimming faster than 0.9 body lengths sec−1 required a greater proportion of aerobic scope despite decreased cost of transport. Reduced aerobic scope did not account for declines in recovery and lower maximum sustainable swimming speed. These results suggest that while performances decline at range edge minimum temperatures, cold-acclimated snapper are optimized for energy savings and range edge limitation may arise from suboptimal temperature exposure throughout the year rather than acute minimum temperature exposure. We propose incorporating performance data with in situ behaviour and environmental data in bioenergetic models to better understand how thermal tolerance determines range limits.

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Section: Methodsmentioning

confidence: 99%

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

Wolfe

Fitzgibbon

Semmens

et al. 2020

Conservation Physiology

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“…Outside the Antarctic literature progressively more reports have been published that question the validity of OCLTT as a universal overarching concept explaining thermal limits (e.g. Ejbye-Ernst et al 2016, Verberk et al 2016. This has been especially the case in insects, where studies investigating low-temperature limits do not support the paradigm, and investigations of uppertemperature limits show stronger support in water-respiring species than air-breathing taxa (e.g.…”

Section: Mechanisms Of Resistance To Warmingmentioning

confidence: 99%

Oceanography and Marine Biology

Hawkins¹,

Evans²,

Dale³

et al. 2018

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Animals living in the Southern Ocean have evolved in a singular environment. It shares many of its attributes with the high Arctic, namely low, stable temperatures, the pervading effect of ice in its many forms and extreme seasonality of light and phytobiont productivity. Antarctica is, however, the most isolated continent on Earth and is the only one that lacks a continental shelf connection with another continent. This isolation, along with the many millions of years that these conditions have existed, has produced a fauna that is both diverse, with around 17,000 marine invertebrate species living there, and has the highest proportions of endemic species of any continent. The reasons for this are discussed. The isolation, history and unusual environmental conditions have resulted in the fauna producing a range and scale of adaptations to low temperature and seasonality that are unique. The best known such adaptations include channichthyid icefish that lack haemoglobin and transport oxygen around their bodies only in solution, or the absence, in some species, of what was only 20 years ago termed the universal heat shock response. Other adaptations include large size in some groups, a tendency to produce larger eggs than species at lower latitudes and very long gametogenic cycles, with egg development (vitellogenesis) taking 18-24 months in some species. The rates at which some cellular and physiological processes are conducted appear adapted to, or at least partially compensated for, low temperature such as microtubule assembly in cells, whereas other processes such as locomotion and metabolic rate are not compensated, and whole-animal growth, embryonic development, and limb regeneration in echinoderms proceed at rates even slower than would be predicted by the normal rules governing the effect of temperature on biological processes. This review describes the current state of knowledge on the biodiversity of the Southern Ocean fauna and on the majority of known ecophysiological adaptations of coldblooded marine species to Antarctic conditions. It further evaluates the impacts these adaptations have on capacities to resist, or respond to change in the environment, where resistance to raised temperatures seems poor, whereas exposure to acidified conditions to end-century levels has comparatively little impact. Zone Description Area (km 2) Length (km) Southern Ocean Total area (km 2)

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“…To date, sampling windows have varied considerably for the two most common testing protocols used with fishes: from 5 to 60 min for U crit tests (e.g. Fry and Hart, 1948;Brett, 1964;Bushnell et al, 1994;Nelson et al, 1996;McKenzie et al, 2001;Gallaugher et al, 2001;Lee et al, 2003a,b;Claireaux et al, 2005Claireaux et al, , 2006Marras et al, 2010;Svendsen et al, 2010;Ejbye-Ernst et al, 2016;Di Santo et al, 2017) and from 0.5 to 60 min for chase-to-exhaustion tests (Lucas and Priede, 1992;Reidy et al, 1995;Norin and Malte, 2011;Clark et al, 2012Clark et al, , 2013Norin and Clark, 2016;Norin et al, 2014;Gräns et al, 2014;Auer et al, 2016;. Fortunately, fibre optic oxygen sensors greatly facilitate exploration of the dynamic nature of _ M O2active in fishes by having a fast response time (<15 s; pyroscience.com/ index.html), unlike early swim tunnel respirometry that had to use the Winkler method (Winkler, 1888) to follow the decline in dissolved oxygen (DO) over lengthy periods (30-60 min) to estimate _ M O2active .…”

Section: Introductionmentioning

confidence: 99%

Finding the peak of dynamic oxygen uptake during fatiguing exercise in fish

Zhang

Gilbert

Farrell

2019

Journal of Experimental Biology

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As fish approach fatigue at high water velocities in a critical swimming speed (U crit) test, their swimming mode and oxygen cascade typically move to an unsteady state because they adopt an unsteady, burst-andglide swimming mode despite a constant, imposed workload. However, conventional rate of oxygen uptake (_ M O2) sampling intervals (5-20 min) tend to smooth any dynamic fluctuations in active _ M O2 (_ M O2active) and thus likely underestimate the peak _ M O2active. Here, we used rainbow trout (Oncorhynchus mykiss) to explore the dynamic nature of _ M O2active near U crit using various sampling windows and an iterative algorithm. Compared with a conventional interval regression analysis of _ M O2active over a 10-min period, our new analytical approach generated a 23% higher peak _ M O2active. Therefore, we suggest that accounting for such dynamics in _ M O2active with this new analytical approach may lead to more accurate estimates of maximum _ M O2 in fishes.

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Partitioning the metabolic scope: the importance of anaerobic metabolism and implications for the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis

Cited by 22 publications

References 111 publications

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

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

Oceanography and Marine Biology

Finding the peak of dynamic oxygen uptake during fatiguing exercise in fish

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