Inadequate food intake at high temperatures is related to depressed mitochondrial respiratory capacity

Abstract

Animals, especially ectotherms, are highly sensitive to the temperature of their surrounding environment. Extremely high temperature, for example, induces a decline of average performance of conspecifics within a population, but individual heterogeneity in the ability to cope with elevating temperatures has rarely been studied. Here, we examined inter-individual variation in feeding ability and consequent growth rate of juvenile brown trout Salmo trutta acclimated to a high temperature (19°C), and investigated the relationship between these metrics of whole-animal performances and among-individual variation in mitochondrial respiration capacity. Food was provided ad libitum, yet intake varied ten-fold amongst individuals, resulting in some fish losing weight whilst others continued to grow. Almost half of the variation in food intake was related to variability in mitochondrial capacity: low intake (and hence growth failure) was associated with high leak respiration rates within liver and muscle mitochondria, and a lower coupling of muscle mitochondria. These observations, combined with the inability of fish with low food consumption to increase their intake despite ad libitum food levels, suggest a possible insufficient capacity of the mitochondria for maintaining ATP homeostasis. Individual variation in thermal performance is likely to confer variation in the upper limit of an organism's thermal niche and might affect the structure of wild populations in warming environments.

Thermal acclimation and subspecies-specific effects on heart and brain mitochondrial performance in a eurythermal teleost (Fundulus heteroclitus)

“…1) following 33°C acclimation may be indicative of an energetic mismatch induced by insufficient food supply and high energetic demands (Chung and Schulte, 2015). These data provide support for a mismatch of organism-level energetic supply and demand with increasing temperature and potential sub-lethal costs associated with high-temperature acclimation; this may account for our observed mitochondrial suppression with potential consequences for the fitness of these animals (Salin et al, 2016;Lemoine and Burkepile, 2012;Iles, 2014).…”

Estimating thermal performance curves from repeated field observations

“…, Salin et al. ). Such variation in thermal performance parameters could be included in the model, particularly in relation to observable traits such as size, sex, or family membership.…”

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

“…A liver aliquot from each fish (mean ± SE across all treatments: 43.08 ± 2.02 mg) preserved in respirometry buffer (0.1 mM EGTA, 15 μM EDTA, 1 mM MgCl 2 , 20 mM Taurine, 10 mM KH 2 PO 4 , 20 mM HEPES, 110 mM D‐sucrose, 60 mM lactobionic acid, 1 g/L bovin serum albumin essentially free fatty acid, pH 7.2 with KOH) was shredded using microdissecting scissors, and the shredded solution then homogenized with a Potter‐Elvehjem homogenizer (three passages). Validations of the methods are described in (Salin, Auer, Anderson, et al., ; Salin, Auer, Rudolf, et al., ). The homogenate was then diluted further in respirometry buffer to obtain the desired final concentration (mean ± SE : 5.06 ± 0.03 mg/ml).…”

“…Specifically, we tested whether plasticity in mitochondrial respiratory capacities (state 3 and state 4) and density (estimated from cytochrome c oxidase (COX) activity) in response to food shortage causes a reduction in the liver's requirements for oxygen, and in turn energy substrates. Mass‐specific, COX‐normalized (to correct for variation in mitochondrial density, as in Salin, Auer, Anderson, Selman, and Metcalfe (); Salin, Auer, Rudolf, et al. ()) and whole‐tissue approaches were employed to determine the effects of fasting on mitochondrial oxidative capacities at different levels of biological organization.…”