Metabolic depression in animals: physiological perspectives and biochemical generalizations

Abstract

Depression of metabolic rate has been recorded for virtually all major animal phyla in response to environmental stress. The extent of depression is usually measured as the ratio of the depressed metabolic rate to the normal resting metabolic rate. Metabolic rate is sometimes only depressed to approx. 80% of the resting value (i.e. a depression of approx. 20% of resting); it is more commonly 5-40% of resting (i.e. a depression of approx. 60-95% of resting); extreme depression is to 1% or less of resting, or even to an unmeasurably low metabolic rate (i.e. a depression of approx. 99-100% of resting). We have examined the resting and depressed metabolic rate of animals as a function of their body mass, corrected to a common temperature. This allometric approach allows ready comparison of the absolute level of both resting and depressed metabolic rate for various animals, and suggests three general patterns of metabolic depression. Firstly, metabolic depression to approx. 0.05-0.4 of rest is a common and remarkably consistent pattern for various non-cryptobiotic animals (e.g. molluscs, earthworms, crustaceans, fishes, amphibians, reptiles). This extent of metabolic depression is typical for dormant animals with 'intrinsic' depression, i.e. reduction of metabolic rate in anticipation of adverse environmental conditions but without substantial changes to their ionic or osmotic status, or state of body water. Some of these types of animal are able to survive anoxia for limited periods, and their anaerobic metabolic depression is also to approx. 0.05-0.4 of resting. Metabolic depression to much less than 0.2 of resting is apparent for some 'resting', 'over-wintering' or diapaused eggs of these animals, but this can be due to early developmental arrest so that the egg has a low 'metabolic mass' of developed tissue (compared to the overall mass of the egg) with no metabolic depression, rather than having metabolic depression of the entire cell mass. A profound decrease in metabolic rate occurs in hibernating (or aestivating) mammals and birds during torpor, e.g. to less than 0.01 of pre-torpor metabolic rate, but there is often no intrinsic metabolic depression in addition to that reduction in metabolic rate due to readjustment of thermoregulatory control and a decrease in body temperature with a concommitant Q10 effect. There may be a modest intrinsic metabolic depression for some species in shallow torpor (to approx. 0.86) and a more substantial metabolic depression for deep torpor (approx. 0.6), but any energy saving accruing from this intrinsic depression is small compared to the substantial savings accrued from the readjustment of thermoregulation and the Q10 effect. Secondly, a more extreme pattern of metabolic depression (to < 0.05 of rest) is evident for cryptobiotic animals. For these animals there is a profound change in their internal environment--for anoxybiotic animals there is an absence of oxygen and for osmobiotic, anhydrobiotic or cryobiotic animals there is an alteration of the ionic/osmotic balance or s...

Effect of winter cold duration on spring phenology of the orange tip butterfly, Anthocharis cardamines

“…As most cycles returned very little CO 2 , but once or twice during a night a significant CO 2 amount was measured, respiration in A. cardamines likely is through discontinuous gas exchange cycles (DGC) while in diapause. DGCs are commonly seen in diapausing insects and are suggested to carry benefits in terms of water retention, protection against oxidative stress, and pathogen avoidance (Guppy and Withers 1999; Lehmann et al. 2015).…”

“…2015). After diapause is broken, respiration increases gradually, with DGCs increasing in frequency, approaching a state of continuous gas exchange where spiracles are continuously kept open (Guppy and Withers 1999). In the later part of the post‐diapause development, there is only continuous breathing, at an accelerating rate (Fig.…”

Adaptation and acclimatization to ocean acidification in marine ectotherms: anin situtransplant experiment with polychaetes at a shallow CO2vent system

“…It has been proposed that metabolic depression evolved to enable organisms to maintain a balance between energy supply and demand when their physiological machinery may be impaired as a result of environmental challenges [25,26]. Consequently, metabolic depression is considered to be primarily a shortterm strategy [27] as, over the long term, it may have high costs in terms of growth, performances, reproductive output and may ultimately affect fitness. Thus, chronic metabolic depression has the potential to limit or prevent colonization of elevated pCO 2 environments, and in a future, more acidic ocean to increase the risk of local and global taxa extinction.…”

Diurnal Fluctuations in Acidification and Hypoxia Reduce Growth and Survival of Larval and Juvenile Bay Scallops (Argopecten irradians) and Hard Clams (Mercenaria mercenaria)

“…Here, by examining multiple levels of pH and DO, the quantitative extent of impairment due to diurnal changes in acidification and hypoxia was identified and affirmed that large diurnal changes in pH and DO have strong negative effects on early-life stage bivalves. While bivalves have a series of physiological adaptions to acclimate to low pH and low DO including acid-base regulation, anaerobic metabolism, and metabolic depression (Grieshaber et al, 1994;Guppy and Withers, 1999;Hochachka and Lutz, 2001;Wu, 2002;Michaelidis et al, 2005), it would seem these processes are ineffective against the combined level and variation of acidification and hypoxia at least for larval bivalves which may have more poorly developed physiological systems for resisting physiological stress. While it is probable that juvenile-stage bivalves with more well-developed physiological systems may be better able to adapt to diurnal changes on pH and DO, this has yet to be explored.…”