Temperature-dependent metabolic consequences of food deprivation in the European sardine

Abstract

Aquatic ecosystems can exhibit seasonal variation in resource availability and animals have evolved to cope with the associated caloric restriction. During winter in the NW Mediterranean Sea, the European sardine Sardina pilchardus naturally experiences caloric restriction due to a decrease in diversity and quantity of plankton. Ongoing global warming has, however, had deleterious effects on plankton communities such that food shortages may occur throughout the year, especially under warm conditions in the summer. We investigated the interactive effects of temperature and food availability on sardine metabolism, by continuously monitoring whole-animal respiration of groups of control (fed) and food-deprived sardines over a 60-day experiment in winter (12°C) or summer (20°C) conditions under natural photoperiod. In addition, we measured mitochondrial respiration of red muscle fibres, biometric variables and energy reserves, of individuals sampled at 30 and 60 days. This revealed that winter food deprivation elicits energy saving mechanisms at whole animal and cellular levels by maintaining a low metabolism to preserve energy reserves, allowing high survival. By contrast, despite energy saving mechanisms at the mitochondrial level, whole animal metabolic rate was high during food deprivation in summer, causing increased consumption of energy reserves at the muscular level and high mortality after 60 days. Furthermore, a 5-day refeeding did not improve survival and mortalities actually continued, suggesting that long-term food deprivation at high temperatures caused profound stress in sardines that potentially impaired nutrient absorption.

Environmental variation associated with overwintering elicits marked metabolic plasticity in a temperate salmonid, Salvelinus fontinalis

“…In combination with the processes we identified as helping reduce Ṁ O 2 standard , other studies have shown that increased mitochondrial efficiency (i.e. less proton leak) or reductions in mitochondrial abundance ( Guderley and St-Pierre, 2002 ; Salin et al, 2018 ; Secor and Carey, 2016 ; Thoral et al, 2023 ) can contribute greatly to reductions in Ṁ O 2 standard when food is limited.…”

Intergenerational plasticity aligns with temperature-dependent selection on offspring metabolic rates

“…(a) Parental condition and offspring temperature increased selection on offspring metabolism availability often selects for reduced metabolic rates [75], presumably to conserve energy reserves. Further, temperature and food availability can interact to affect metabolism in complex ways, with evidence for temperature mediating both an increase and decrease in metabolism with increases in food availability [76][77][78].…”

Interactive effects of intrinsic and extrinsic factors on metabolic rate

“…[24,[38][39][40][41][42]44,93,94]) life-history stage (e.g. [20,32,40,[47][48][49][50]66,91,123,126,[129][130][131][132][133][134][135][136][137][138][139][140][141][142][143][144][145][146][147]) interactive effects of intrinsic factors ecological life style pelagic versus benthic (e.g. [20,24,34,40,92,93]) food habits (e.g.…”

“…Higher temperature speeds up metabolism, whereas higher salinity reduces osmoregulatory metabolic demand in marine organisms. However, hypersaline conditions may increase metabolic costs in freshwater/estuarine organisms [120][121][122][123] temperature and pH (CO 2 ) variable (species-specific) combined effects of temperature and acidification (CO 2 levels) vary with species for unknown reasons [124,125] ( [84,121,126,127] temperature and food supply complex thermal sensitivity of metabolism varies with food supply in complex ways [128,129] temperature and toxicants complex thermal sensitivity of metabolic rate in a moth depended on an insecticide treatment when acclimated at 22°C, but not when acclimated at 28°C [130] temperature and microplastics complex in an aquatic amphipod, temperature effects are positive at low microplastic concentration, but negative at high microplastic concentration, for unknown reasons [131] temperature and latitude positive (low to high latitude) high-latitude populations in relatively cool habitats tend to show more thermal sensitivity of metabolic rate than that of low latitude populations in warmer habitats [132][133][134][135] temperature and altitude positive (low to high altitude) a high-altitude population of the tsetse fly Glossina pallidipes in a cool habitat showed higher temperature sensitivity of metabolic rate than did lowaltitude populations in warmer habitats [136] temperature and ecological life style complex invasive crayfish show higher metabolic rates at warm temperatures, but lower metabolic rates at cooler temperatures than do native crayfish [137] light and predator cues positive or negative metabolic rate of an aquatic amphipod changes in response to fish predator cues in light, but not in dark [138] interactive effects of intrinsic and extrinsic factors type direction of interactive effect a underlying mechanism selected sources body size and ecological life style pelagic versus benthic positive or negative (comparing pelagic species to benthic species) pelagic invertebrate/protist species (or life-stages) tend to show steeper metabolic scaling than do related benthic species (or life-stages), possibly because of age-and size-specific differences in locomotor costs, cellular mode of growth, or predation-caused rates of mortality, growth and reproduction. Opposite patterns are shown for teleost fishes, possibly owing, at least in part, to their lesser vulnerability to predation (associated with their larger body size and more rapid escape movements), and to thei...…”

“…However, hypersaline conditions may increase metabolic costs in freshwater/estuarine organisms[120–123]temperature and pH (CO 2 )variable (species-specific)combined effects of temperature and acidification (CO 2 levels) vary with species for unknown reasons[124,125]temperature and oxygen supplypositivethermal response of metabolic rate increases with increasing oxygen supply, perhaps because it can be expressed more freely when high-temperature causing hypoxia in water is prevented. However, temperature acclimation can mitigate effects of hypoxia on metabolic rate[84,121,126,127]temperature and food supplycomplexthermal sensitivity of metabolism varies with food supply in complex ways[128,129]temperature and toxicantscomplexthermal sensitivity of metabolic rate in a moth depended on an insecticide treatment when acclimated at 22°C, but not when acclimated at 28°C[130]temperature and microplasticscomplexin an aquatic amphipod, temperature effects are positive at low microplastic concentration, but negative at high microplastic concentration, for unknown reasons[131]temperature and latitudepositive (low to high latitude)high-latitude populations in relatively cool habitats tend to show more thermal sensitivity of metabolic rate than that of low latitude populations in warmer habitats[132–135]temperature and altitudepositive (low to high altitude)a high-altitude population of the tsetse fly Glossina pallidipes in a cool habitat showed higher temperature sensitivity of metabolic rate than did low-altitude populations in warmer habitats[136]temperature and ecological life stylecomplexinvasive crayfish show higher metabolic rates at warm temperatures, but lower metabolic rates at cooler temperatures than do native crayfish[137]light and predator cues…”