Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes

Abstract

SUMMARYEffects of latitudinal cold adaptation and cold acclimation on metabolic rates and aerobic scope were studied in the eurythermal marine gastropod Littorina saxatilis from temperate North Sea and sub-arctic White Sea areas. Animals were acclimated for 6-8 weeks at control temperature (13°C) or at 4°C, and their respiration rates were measured during acute temperature change (1-1.5°C h-1) in a range between 0°C and 32°C. In parallel, the accumulation of anaerobic end products and changes in energy status were monitored. Starting from 0°C, aerobic metabolic rates of L. saxatilis rose quickly with increasing temperatures up to a point at or slightly above the respective acclimation temperature. Beyond this value, thermal sensitivity of oxygen consumption rate (V̇O2) greatly decreased in a wide, 15°C range of experimental temperatures. This change in metabolic regulation was also reflected in the activation energy of aerobic metabolism (Ea), which was approximately seven times lower at temperatures above Arrhenius breakpoint temperatures (ABTs) than at temperatures below ABTs. Warming progressively led to a discrepancy between energy demand and energy production, as demonstrated by a decrease in the levels of high-energy phosphates [phosho-L-arginine (PLA) and ATP], and resulted in the onset of anaerobiosis at critically high temperatures, indicating a limitation of aerobic scope. The comparison of aerobic and anaerobic metabolic rates in L. saxatilis in air and water suggests that the heat-induced onset of anaerobiosis is due to the insufficient oxygen supply to tissues at high temperatures. Cold acclimation led to an increase in aerobic metabolic rates and a considerable downward shift of the upper critical temperature in North Sea L. saxatilis but not in White Sea L. saxatilis. Limited metabolic plasticity in response to cold acclimation in sub-arctic White Sea snails as compared with their temperate North Sea counterparts suggests that metabolic depression occurs during overwintering under the more extreme winter conditions at the White Sea.

Oxygen limited thermal tolerance in fish?

“…As the interdependence of thermal tolerance and aerobic scope have only recently been discussed as a unifying principle among animals (Pörtner, 2001) these relationships have not been systematically investigated. However, invertebrate examples from the intertidal zone where they may be exposed to midday sunshine and heat, would most adequately illustrate that extreme heat goes hand in hand with anaerobic metabolism and passive survival (Sokolova and Pörtner, 2003) and thus very likely involves a metabolic depression scenario which contributes to energy savings and thereby extends the period during which heat beyond the critical temperature can be tolerated.…”

“…Early evidence collected in marine invertebrates (annelids and sipunculids) demonstrated a transition to anaerobic metabolism (including mitochondrial anaerobiosis) at both cold and warm temperature extremes (Zielinski and Pörtner, 1996;Sommer et al, 1997), later on confirmed in crustaceans (Frederich and Pörtner, 2000) and molluscs, i.e. bivalves, gastropods and cephalopods (Pörtner and Zielinski, 1998;Pörtner et al, 1999;Peck et al, 2002;Sokolova and Pörtner, 2003). Studies in a sipunculid (Sipunculus nudus, Zielinski and Pörtner, 1996) and the spider crab (Maja squinado, Frederich and Pörtner, 2000) investigated the pattern of coelomic fluid/haemolymph oxygen tensions in relation to warming and/or cooling and demonstrated development of hypoxia which preceded the onset of anaerobic metabolism towards both cold and warm temperature extremes.…”

Exploring key issues of aerobic scope interpretation in ectotherms: absolute versus factorial

“…The concept has since been applied to a great range of aquatic and terrestrial species (e.g. Auer et al 2015;Bishop 1999;Moberly 1968;Overgaard et al 2012;Schippers et al 2014;Sokolova and Pörtner 2003). On the surface, aerobic scope seems to be a relatively straightforward variable.…”

Linking Post-Translational Modifications and Variation of Phenotypic Traits

“…Among them, metabolic networks involve series of interconnected chemical reactions catalyzed by enzymes, allowing the transformation of input substrates into intermediate or final metabolites. These networks play an essential role in an organism's growth, reproduction, and ability to maintain cell integrity and to respond to environmental changes (1,2). The metabolic fluxes, as well as the metabolite concentrations, are governed by the activity of the enzymes, which depends on three types of factors: kinetic parameters, enzyme abundance, and activation state of the enzyme.…”