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.

Late-stage pregnancy reduces upper thermal tolerance in a live-bearing fish.

Upper thermal limits are considered a key determinant of a population's ability to persist in the face of extreme heat events. However, these limits differ considerably among individuals within a population, and the mechanisms underlying this differential sensitivity are not well understood. Upper thermal tolerance in aquatic ectotherms is thought to be determined by a mismatch between oxygen supply and the increased metabolic demands associated with warmer waters. As such, tolerance is expected to decline during reproduction given the heightened oxygen demand for gamete production and maintenance. Among live-bearing species, upper thermal tolerance of reproductive adults may decline even further after fertilization due to the cost of meeting the increasing oxygen demands of developing embryos. We examined the upper thermal tolerance of live-bearing female Trinidadian guppies at different stages of reproduction and found that critical thermal maximum was similar during the egg yolking and early embryos stage but then declined by almost 0.5 °C during late pregnancy when oxygen demands are the greatest. These results are consistent with the hypothesis that oxygen limitation sets thermal limits and show that reproduction is associated with a decline in upper thermal tolerance.

Metabolic Rate Interacts with Resource Availability to Determine Individual Variation in Microhabitat Use in the Wild.

Ecological pressures such as competition can lead individuals within a population to partition resources or habitats, but the underlying intrinsic mechanisms that determine an individual's resource use are not well understood. Here we show that an individual's own energy demand and associated competitive ability influence its resource use, but only when food is more limiting. We tested whether intraspecific variation in metabolic rate leads to microhabitat partitioning among juvenile Atlantic salmon (Salmo salar) in natural streams subjected to manipulated nutrient levels and subsequent per capita food availability. We found that individual salmon from families with a higher baseline (standard) metabolic rate (which is associated with greater competitive ability) tended to occupy faster-flowing water, but only in streams with lower per capita food availability. Faster-flowing microhabitats yield more food, but high metabolic rate fish only benefited from faster growth in streams with high food levels, presumably because in low-food environments the cost of a high metabolism offsets the benefits of acquiring a productive microhabitat. The benefits of a given metabolic rate were thus context dependent. These results demonstrate that intraspecific variation in metabolic rate can interact with resource availability to determine the spatial structuring of wild populations.

Energetic mechanisms for coping with changes in resource availability.

Given current anthropogenic alterations to many ecosystems and communities, it is becoming increasingly important to consider whether and how organisms can cope with changing resources. Metabolic rate, because it represents the rate of energy expenditure, may play a key role in mediating the link between resource conditions and performance and thereby how well organisms can persist in the face of environmental change. Here, we focus on the role that energy metabolism plays in determining organismal responses to changes in food availability over both short-term ecological and longer-term evolutionary timescales. Using a meta-analytical approach encompassing multiple species, we find that individuals with a higher metabolic rate grow faster under high food levels but slower once food levels decline, suggesting that the association between metabolism and life-history traits shifts along resource gradients. We also find that organisms can cope with changing resource availability through both phenotypic plasticity and genetically based evolutionary adaptation in their rates of energy metabolism. However, the metabolic rates of individuals within a population and of species within a lineage do not all respond in the same manner to changes in food availability. This diversity of responses suggests that there are benefits but also costs to changes in metabolic rate. It also underscores the need to examine not just the energy budgets of organisms within the context of metabolic rate but also how energy metabolism changes alongside other physiological and behavioural traits in variable environments.

Upper thermal limits are repeatable in Trinidadian guppies.

Measurements of thermal tolerance are critical for predicting species vulnerability to climate change. Critical thermal maximum (CTmax) is a measure of an animal's upper thermal tolerance, but there is limited evidence for how repeatable it is within individuals over time. We measured the CTmax of Trinidadian guppies (Poecilia reticulata) across six consecutive trials, each a week apart. The repeatability of CTmax over six trials was 0.43 (0.26-0.62). However, CTmax also changed over time, ranging from 39.0 to 39.6 °C and increasing by 0.6 °C across the first four trials before leveling off. This is most likely the effect of heat hardening, indicating that thermal tolerance can increase after repeated exposure to extreme heat events.

Hierarchical analysis of wild Atlantic salmon (Salmo salar) fecundity in relation to body size and developmental traits.

Using data from wild Atlantic salmon Salmo salar returning to spawn in seven Scottish rivers, we developed a model of fecundity based on individual body size and key developmental traits. We used a novel approach to model selection which maximises predictive accuracy for application to target river stocks to select the best from a suite of Bayesian hierarchical models. This approach aims to ensure the optimal model within the candidate set includes covariates that best predict out-of-sample data to estimate fecundity in areas where no direct observations are available. In addition to body size, the final model included the developmental characteristics of age at smolting and years spent at sea. Using two independent long-term monitoring datasets, the consequences of ignoring these characteristics was revealed by comparing predictions from the best model with models that omitted them.

Nutrients from salmon parents alter selection pressures on their offspring.

Organisms can modify their surrounding environment, but whether these changes are large enough to feed back and alter their evolutionary trajectories is not well understood, particularly in wild populations. Here we show that nutrient pulses from decomposing Atlantic salmon (Salmo salar) parents alter selection pressures on their offspring with important consequences for their phenotypic and genetic diversity. We found a strong survival advantage to larger eggs and faster juvenile metabolic rates in streams lacking carcasses but not in streams containing this parental nutrient input. Differences in selection intensities led to significant phenotypic divergence in these two traits among stream types. Stronger selection in streams with low parental nutrient input also decreased the number of surviving families compared to streams with high parental nutrient levels. Observed effects of parent-derived nutrients on selection pressures provide experimental evidence for key components of eco-evolutionary feedbacks in wild populations.

Individuals exhibit consistent differences in their metabolic rates across changing thermal conditions.

Metabolic rate has been linked to growth, reproduction, and survival at the individual level and is thought to have far reaching consequences for the ecology and evolution of organisms. However, metabolic rates must be consistent (i.e. repeatable) over at least some portion of the lifetime in order to predict their longer-term effects on population dynamics and how they will respond to selection. Previous studies demonstrate that metabolic rates are repeatable under constant conditions but potentially less so in more variable environments. We measured the standard (=minimum) metabolic rate, maximum metabolic rate, and aerobic scope (=interval between standard and maximum rates) in juvenile brown trout (Salmo trutta) after 5weeks acclimation to each of three consecutive test temperatures (10, 13, and then 16°C) that simulated the warming conditions experienced throughout their first summer of growth. We found that metabolic rates are repeatable over a period of months under changing thermal conditions: individual trout exhibited consistent differences in all three metabolic traits across increasing temperatures. Initial among-individual differences in metabolism are thus likely to have significant consequences for fitness-related traits over key periods of their life history.

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. 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.

Repeatability of metabolic rate is lower for animals living under field versus laboratory conditions.

Metabolic rate has been linked to several components of fitness and is both heritable and repeatable to a certain extent. However, its repeatability can differ among studies, even after controlling for the time interval between measurements. Some of this variation in repeatability might be due to the relative stability of the environmental conditions in which the animals are living between measurements. We compared published repeatability estimates for basal, resting and maximum metabolic rate from studies of endotherms living in the laboratory with those living in the wild during the interval between measurements. We found that repeatability declines over time, as demonstrated previously, but show for the first time that estimates from free-living animals are also considerably lower than those from animals living under more stable laboratory conditions.

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.

Flexibility in metabolic rate and activity level determines individual variation in overwinter performance.

Energy stores are essential for the overwinter survival of many temperate and polar animals, but individuals within a species often differ in how quickly they deplete their reserves. These disparities in overwinter performance may be explained by differences in their physiological and behavioral flexibility in response to food scarcity. However, little is known about whether individuals exhibit correlated or independent changes in these traits, and how these phenotypic changes collectively affect their winter energy use. We examined individual flexibility in both standard metabolic rate and activity level in response to food scarcity and their combined consequences for depletion of lipid stores among overwintering brown trout (Salmo trutta). Metabolism and activity tended to decrease, yet individuals exhibited striking differences in their physiological and behavioral flexibility. The rate of lipid depletion was negatively related to decreases in both metabolic and activity rates, with the smallest lipid loss over the simulated winter period occurring in individuals that had the greatest reductions in metabolism and/or activity. However, changes in metabolism and activity were negatively correlated; those individuals that decreased their SMR to a greater extent tended to increase their activity rates, and vice versa, suggesting among-individual variation in strategies for coping with food scarcity.

Variation in the link between oxygen consumption and ATP production, and its relevance for animal performance.

It is often assumed that an animal's metabolic rate can be estimated through measuring the whole-organism oxygen consumption rate. However, oxygen consumption alone is unlikely to be a sufficient marker of energy metabolism in many situations. This is due to the inherent variability in the link between oxidation and phosphorylation; that is, the amount of adenosine triphosphate (ATP) generated per molecule of oxygen consumed by mitochondria (P/O ratio). In this article, we describe how the P/O ratio can vary within and among individuals, and in response to a number of environmental parameters, including diet and temperature. As the P/O ratio affects the efficiency of cellular energy production, its variability may have significant consequences for animal performance, such as growth rate and reproductive output. We explore the adaptive significance of such variability and hypothesize that while a reduction in the P/O ratio is energetically costly, it may be associated with advantages in terms of somatic maintenance through reduced production of reactive oxygen species. Finally, we discuss how considering variation in mitochondrial efficiency, together with whole-organism oxygen consumption, can permit a better understanding of the relationship between energy metabolism and life history for studies in evolutionary ecology.

Flexibility in metabolic rate confers a growth advantage under changing food availability.

1. Phenotypic flexibility in physiological, morphological and behavioural traits can allow organisms to cope with environmental challenges. Given recent climate change and the degree of habitat modification currently experienced by many organisms, it is therefore critical to quantify the degree of phenotypic variation present within populations, individual capacities to change and what their consequences are for fitness. 2. Flexibility in standard metabolic rate (SMR) may be particularly important since SMR reflects the minimal energetic cost of living and is one of the primary traits underlying organismal performance. SMR can increase or decrease in response to food availability, but the consequences of these changes for growth rates and other fitness components are not well known. 3. We examined individual variation in metabolic flexibility in response to changing food levels and its consequences for somatic growth in juvenile brown trout (Salmo trutta). 4. SMR increased when individuals were switched to a high food ration and decreased when they were switched to a low food regime. These shifts in SMR, in turn, were linked with individual differences in somatic growth; those individuals that increased their SMR more in response to elevated food levels grew fastest, while growth at the low food level was fastest in those individuals that depressed their SMR most. 5. Flexibility in energy metabolism is therefore a key mechanism to maximize growth rates under the challenges imposed by variability in food availability and is likely to be an important determinant of species' resilience in the face of global change.

Aerobic scope explains individual variation in feeding capacity.

Links between metabolism and components of fitness such as growth, reproduction and survival can depend on food availability. A high standard metabolic rate (SMR; baseline energy expenditure) or aerobic scope (AS; the difference between an individual's maximum and SMR) is often beneficial when food is abundant or easily accessible but can be less important or even disadvantageous when food levels decline. While the mechanisms underlying these context-dependent associations are not well understood, they suggest that individuals with a higher SMR or AS are better able to take advantage of high food abundance. Here we show that juvenile brown trout (Salmo trutta) with a higher AS were able to consume more food per day relative to individuals with a lower AS. These results help explain why a high aerobic capacity can improve performance measures such as growth rate at high but not low levels of food availability.

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.

Local adaptation in Trinidadian guppies alters ecosystem processes.

Theory suggests evolutionary change can significantly influence and act in tandem with ecological forces via ecological-evolutionary feedbacks. This theory assumes that significant evolutionary change occurs over ecologically relevant timescales and that phenotypes have differential effects on the environment. Here we test the hypothesis that local adaptation causes ecosystem structure and function to diverge. We demonstrate that populations of Trinidadian guppies (Poecilia reticulata), characterized by differences in phenotypic and population-level traits, differ in their impact on ecosystem properties. We report results from a replicated, common garden mesocosm experiment and show that differences between guppy phenotypes result in the divergence of ecosystem structure (algal, invertebrate, and detrital standing stocks) and function (gross primary productivity, leaf decomposition rates, and nutrient flux). These phenotypic effects are further modified by effects of guppy density. We evaluated the generality of these effects by replicating the experiment using guppies derived from two independent origins of the phenotype. Finally, we tested the ability of multiple guppy traits to explain observed differences in the mesocosms. Our findings demonstrate that evolution can significantly affect both ecosystem structure and function. The ecosystem differences reported here are consistent with patterns observed across natural streams and argue that guppies play a significant role in shaping these ecosystems.

Life histories have a history: effects of past and present conditions on adult somatic growth rates in wild Trinidadian guppies.

1. Environmental conditions in the present, more recent past and during the juvenile stage can have significant effects on adult performance and population dynamics, but their relative importance and potential interactions remain unexplored. 2. We examined the influence of food availability at the time of sampling, 2 months prior and during the juvenile stage on adult somatic growth rates in wild Trinidadian guppies (Poecilia reticulata). 3. We found that food availability during both the early and later parts of an individual's ontogeny had important consequences for adult growth strategies, but the direction of these effects differed among life stages and their magnitude, in some cases, depended on food levels experienced during other life stages. Current food levels and those 2 months prior to growth measurements had positive effects on adult growth rate; though, food levels 2 months prior had a greater effect on growth than current food levels. In contrast, the effects of food availability during the juvenile stage were higher in magnitude but opposite in direction to current food levels and those 2 months prior to growth rate measurements. Individuals recruiting under low food levels grew faster as adults than individuals recruiting during periods of high food availability. There was also a positive interaction between food levels experienced during the juvenile stage and 2 months prior such that the effects of juvenile food level diminished as the food level experienced 2 months prior increased. 4. These results suggest that the similar conditions occurring at different life stages can have different effects on short- and long-term growth strategies of individuals within a population. They also demonstrate that, while juvenile conditions can have lasting effects on adult performance, the strength of that effect can be dampened by environmental conditions experienced as an adult. 5. A simultaneous consideration of past events in both the adult and juvenile stage may therefore improve predictions for individual- and population-level responses to environmental change.

A model for optimal offspring size in fish, including live-bearing and parental effects.

Since Smith and Fretwell's seminal article in 1974 on the optimal offspring size, most theory has assumed a trade-off between offspring number and offspring fitness, where larger offspring have better survival or fitness, but with diminishing returns. In this article, we use two ubiquitous biological mechanisms to derive the shape of this trade-off: the offspring's growth rate combined with its size-dependent mortality (predation). For a large parameter region, we obtain the same sigmoid relationship between offspring size and offspring survival as Smith and Fretwell, but we also identify parameter regions where the optimal offspring size is as small or as large as possible. With increasing growth rate, the optimal offspring size is smaller. We then integrate our model with strategies of parental care. Egg guarding that reduces egg mortality favors smaller or larger offspring, depending on how mortality scales with size. For live-bearers, the survival of offspring to birth is a function of maternal survival; if the mother's survival increases with her size, then the model predicts that larger mothers should produce larger offspring. When using parameters for Trinidadian guppies Poecilia reticulata, differences in both growth and size-dependent predation are required to predict observed differences in offspring size between wild populations from high- and low-predation environments.