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

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. In this study, 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 in turn affect the structure of wild populations in warming environments

Differential effects of food availability on minimum and maximum rates of metabolism

Metabolic rates reflect the energetic cost of living but exhibit remarkable variation among conspecifics, partly as a result of the constraints imposed by environmental conditions. Metabolic rates are sensitive to changes in temperature and oxygen availability, but effects of food availability, particularly on maximum metabolic rates, are not well understood. Here, we show in brown trout (Salmo trutta) that maximum metabolic rates are immutable but minimum metabolic rates increase as a positive function of food availability. As a result, aerobic scope (i.e. the capacity to elevate metabolism above baseline requirements) declines as food availability increases. These differential changes in metabolic rates likely have important consequences for how organisms partition available metabolic power to different functions under the constraints imposed by food availability

Metabolic rate evolves rapidly and in parallel with the pace of life history

Metabolic rates and life history strategies are both thought to set the "pace of life", but whether they evolve in tandem is not well understood. Here, using a common garden experiment that compares replicate paired populations, we show that Trinidadian guppy (Poecilia reticulata) populations that evolved a fast-paced life history in high-predation environments have consistently higher metabolic rates than guppies that evolved a slow-paced life history in low-predation environments. Furthermore, by transplanting guppies from high- to low-predation environments, we show that metabolic rate evolves in parallel with the pace of life history, at a rapid rate, and in the same direction as found for naturally occurring populations. Together, these multiple lines of inference provide evidence for a tight evolutionary coupling between metabolism and the pace of life history

The optimal combination of standard metabolic rate and aerobic scope for somatic growth depends on food availability

Metabolic rates can vary as much as threefold among individuals of the same size and age in a population, but why such variation persists is unclear given that they determine the energetic cost of living. Relationships between standard metabolic rate (SMR), growth and survival can vary with environmental conditions, suggesting that the fitness consequences of a given metabolic phenotype may be context-dependent. Less attention has focused on the link between absolute aerobic scope (AS, the difference between standard and maximum metabolic rate) and fitness under different environmental conditions, despite the importance of aerobic scope to an organism's total energetic capacity.<p></p> We examined the links between individual variation in both SMR and AS and somatic growth rates of brown trout (Salmo trutta) under different levels of food availability.<p></p> Standard metabolic rate and AS were uncorrelated across individuals. However, SMR and AS not only had interactive effects on growth, but these interactions depended on food level: at ad libitum food levels, AS had a positive effect on growth whose magnitude depended on SMR; at intermediate food levels, AS and SMR had interactive effects on growth, but at the low food level, there was no effect of either AS or SMR on growth. As a result, there was no metabolic phenotype that performed best or worst across all food levels.<p></p> These results demonstrate the importance of aerobic scope in explaining somatic growth rates and support the hypothesis that links between individual variation in metabolism and fitness are context-dependent.<p></p> The larger metabolic phenotype and the environmental context in which performance is evaluated both need to be considered in order to better understand the link between metabolic rates and fitness and thereby the persistence of individual variation in metabolic rates.<p></p&gt

Individuals with higher metabolic rates have lower levels of reactive oxygen species in vivo

There is increasing interest in the effect of energy metabolism on oxidative stress, but much ambiguity over the relationship between the rate of oxygen consumption and the generation of reactive oxygen species (ROS). Production of ROS (such as hydrogen peroxide, H2O2) in the mitochondria is primarily inferred indirectly from measurements in vitro, which may not reflect actual ROS production in living animals. Here, we measured in vivo H2O2 content using the recently developed MitoB probe that becomes concentrated in the mitochondria of living organisms, where it is converted by H2O2 into an alternative form termed MitoP; the ratio of MitoP/MitoB indicates the level of mitochondrial H2O2 in vivo. Using the brown trout Salmo trutta, we tested whether this measurement of in vivo H2O2 content over a 24 h-period was related to interindividual variation in standard metabolic rate (SMR). We showed that the H2O2 content varied up to 26-fold among fish of the same age and under identical environmental conditions and nutritional states. Interindividual variation in H2O2 content was unrelated to mitochondrial density but was significantly associated with SMR: fish with a higher mass-independent SMR had a lower level of H2O2. The mechanism underlying this observed relationship between SMR and in vivo H2O2 content requires further investigation, but may implicate mitochondrial uncoupling which can simultaneously increase SMR but reduce ROS production. To our knowledge, this is the first study in living organisms to show that individuals with higher oxygen consumption rates can actually have lower levels of H2O2

Habitat restoration weakens negative environmental effects on telomere dynamics

Habitat quality can have far-reaching effects on organismal fitness, an issue of concern given the current scale of habitat degradation. Many temperate upland streams have reduced nutrient levels due to human activity. Nutrient restoration confers benefits in terms of invertebrate food availability and subsequent fish growth rates. Here we test whether these mitigation measures also affect the rate of cellular ageing of the fish, measured in terms of the telomeres that cap the ends of eukaryotic chromosomes. We equally distributed Atlantic salmon eggs from the same 30 focal families into 10 human-impacted oligotrophic streams in northern Scotland. Nutrient levels in five of the streams were restored by simulating the deposition of a small number of adult Atlantic salmon Salmo salar carcasses at the end of the spawning period, while five reference streams were left as controls. Telomere lengths and expression of the telomerase reverse transcriptase (TERT) gene that may act to lengthen telomeres were then measured in the young fish when 15 months old. While TERT expression was unrelated to any of the measured variables, telomere lengths were shorter in salmon living at higher densities and in areas with a lower availability of the preferred substrate (cobbles and boulders). However, the adverse effects of these habitat features were much reduced in the streams receiving nutrients. These results suggest that adverse environmental pressures are weakened when nutrients are restored, presumably because the resulting increase in food supply reduces levels of both competition and stress

Simulating nutrient release from parental carcasses increases the growth, biomass and genetic diversity of juvenile Atlantic salmon

The net transport of nutrients by migratory fish from oceans to inland spawning areas has decreased due to population declines and migration barriers. Restoration of nutrients to increasingly oligotrophic upland streams (that were historically salmon spawning areas) have shown short‐term benefits for juvenile salmon, but the longer term consequences are little known. Here we simulated the deposition of a small number of adult Atlantic salmon Salmo salar carcasses at the end of the spawning period in five Scottish upland streams (‘high parental nutrient’ treatment), while leaving five reference streams without carcasses (‘low parental nutrient’ treatment). All streams received exactly the same number of salmon eggs (n = 3,000) drawn in equal number from the same 30 wild‐origin families, thereby controlling for initial egg density and genetic composition. We then monitored the resulting juvenile salmon and their macroinvertebrate prey, repeating the carcass addition treatment in the next spawning season. Macroinvertebrate biomass and abundance were five times higher in the high parental nutrient streams, even 1 year after the carcass addition, and led to faster growth of juvenile salmon over the next 2 years (but with no change in population density). This faster growth led to more fish exceeding the size threshold that would trigger emigration to sea at 2 rather than 3 years of age. There was also higher genetic diversity among surviving salmon in high parental nutrient streams; genotyping showed that these effects were not due to immigration but to differential survival. Synthesis and applications. This 2‐year field experiment shows that adding nutrients that simulate the presence of small numbers of adult salmon carcasses can have long‐term effects on the growth rate of juvenile salmon, likely increasing the number that will migrate to sea early and also increasing their genetic diversity. However, the feasibility of adding nutrients to spawning streams as a management tool to boost salmon populations will depend on whether the benefits at this stage are maintained over the entire life cycle

Simulating nutrient release from parental carcasses increases the growth, biomass and genetic diversity of juvenile Atlantic salmon

The net transport of nutrients by migratory fish from oceans to inland spawning areas has decreased due to population declines and migration barriers. Restoration of nutrients to increasingly oligotrophic upland streams (that were historically salmon spawning areas) have shown short‐term benefits for juvenile salmon, but the longer term consequences are little known. Here we simulated the deposition of a small number of adult Atlantic salmon Salmo salar carcasses at the end of the spawning period in five Scottish upland streams (‘high parental nutrient’ treatment), while leaving five reference streams without carcasses (‘low parental nutrient’ treatment). All streams received exactly the same number of salmon eggs (n = 3,000) drawn in equal number from the same 30 wild‐origin families, thereby controlling for initial egg density and genetic composition. We then monitored the resulting juvenile salmon and their macroinvertebrate prey, repeating the carcass addition treatment in the next spawning season. Macroinvertebrate biomass and abundance were five times higher in the high parental nutrient streams, even 1 year after the carcass addition, and led to faster growth of juvenile salmon over the next 2 years (but with no change in population density). This faster growth led to more fish exceeding the size threshold that would trigger emigration to sea at 2 rather than 3 years of age. There was also higher genetic diversity among surviving salmon in high parental nutrient streams; genotyping showed that these effects were not due to immigration but to differential survival. Synthesis and applications. This 2‐year field experiment shows that adding nutrients that simulate the presence of small numbers of adult salmon carcasses can have long‐term effects on the growth rate of juvenile salmon, likely increasing the number that will migrate to sea early and also increasing their genetic diversity. However, the feasibility of adding nutrients to spawning streams as a management tool to boost salmon populations will depend on whether the benefits at this stage are maintained over the entire life cycle