Stress and food deprivation: linking physiological state to migration success in a teleost fish

Midwood, Jonathan D.; Larsen, Mette Voldby; Aarestrup, Kim; Cooke, Steven J.

doi:10.1242/jeb.140665

Cited by 31 publications

(24 citation statements)

References 75 publications

(89 reference statements)

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“…The validation study used the same population and the same products (cortisol and vehicle) as we used here, and similar methods for elevating cortisol have been used in several other studies of the same trout population (Midwood et al, 2014(Midwood et al, , 2016. We therefore did not measure individual cortisol levels in the current study as the objective was to investigate average treatment effects.…”

Section: Materials and Methods Study Locationmentioning

confidence: 99%

Short-term and long-term effects of transient exogenous cortisol manipulation on oxidative stress in juvenile brown trout

Birnie‐Gauvin

Peiman

Larsen

et al. 2017

Journal of Experimental Biology

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In the wild, animals are exposed to a growing number of stressors with increasing frequency and intensity, as a result of human activities and human-induced environmental change. To fully understand how wild organisms are affected by stressors, it is crucial to understand the physiology that underlies an organism's response to a stressor. Prolonged levels of elevated glucocorticoids are associated with a state of chronic stress and decreased fitness. Exogenous glucocorticoid manipulation reduces an individual's ability to forage, avoid predators and grow, thereby limiting the resources available for physiological functions like defence against oxidative stress. Using brown trout (Salmo trutta), we evaluated the short-term (2 weeks) and long-term (4 months over winter) effects of exogenous cortisol manipulations (versus relevant shams and controls) on the oxidative status of wild juveniles. Cortisol caused an increase in glutathione over a 2 week period and appeared to reduce glutathione over winter. Cortisol treatment did not affect oxidative stress levels or low molecular weight antioxidants. Cortisol caused a significant decrease in growth rates but did not affect predation risk. Over-winter survival in the stream was associated with low levels of oxidative stress and glutathione. Thus, oxidative stress may be a mechanism by which elevated cortisol causes negative physiological effects.

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Section: Materials and Methods Study Locationmentioning

confidence: 99%

Short-term and long-term effects of transient exogenous cortisol manipulation on oxidative stress in juvenile brown trout

Birnie‐Gauvin

Peiman

Larsen

et al. 2017

Journal of Experimental Biology

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“…However, mitochondria are also a major source of reactive oxygen species (ROS) that have the potential to cause oxidative damage (Brand, ). Temporary reductions in mitochondrial energy requirements, while providing short‐term energetic benefits, could potentially lead to associated increases in ROS levels, resulting in the long‐term costs of oxidative stress (Schull et al., ; Sorensen et al., ), potentially faster organismal senescence and hence constraints on future life history (Dowling & Simmons, ; Midwood, Larsen, Aarestrup, & Cooke, ; Monaghan, Metcalfe, & Torres, ; Selman, Blount, Nussey, & Speakman, ; Speakman et al., ). However, surprisingly little is known about these interactions as studies of mitochondrial energetics are generally conducted separately from those of ROS production (Sorensen et al., ; Zhang, Wu, & Klaassen, ; but see Brown & Staples, ; Chausse et al., ).…”

Section: Introductionmentioning

confidence: 99%

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

et al. 2018

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Summary Many animals experience periods of food shortage in their natural environment. It has been hypothesised that the metabolic responses of animals to naturally‐occurring periods of food deprivation may have long‐term negative impacts on their subsequent life‐history.In particular, reductions in energy requirements in response to fasting may help preserve limited resources but potentially come at a cost of increased oxidative stress. However, little is known about this trade‐off since studies of energy metabolism are generally conducted separately from those of oxidative stress.Using a novel approach that combines measurements of mitochondrial function with in vivo levels of hydrogen peroxide (H2O2) in brown trout (Salmo trutta), we show here that fasting induces energy savings in a highly metabolically active organ (the liver) but at the cost of a significant increase in H2O2, an important form of reactive oxygen species (ROS).After a 2‐week period of fasting, brown trout reduced their whole‐liver mitochondrial respiratory capacities (state 3, state 4 and cytochrome c oxidase activity), mainly due to reductions in liver size (and hence the total mitochondrial content). This was compensated for at the level of the mitochondrion, with an increase in state 3 respiration combined with a decrease in state 4 respiration, suggesting a selective increase in the capacity to produce ATP without a concomitant increase in energy dissipated through proton leakage. However, the reduction in total hepatic metabolic capacity in fasted fish was associated with an almost two‐fold increase in in vivo mitochondrial H2O2 levels (as measured by the MitoB probe).The resulting increase in mitochondrial ROS, and hence potential risk of oxidative damage, provides mechanistic insight into the trade‐off between the short‐term energetic benefits of reducing metabolism in response to fasting and the potential long‐term costs to subsequent life‐history traits.

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“…However, the effect of resource availability on migration is not clear. For example, a reduction in food availability can result in lower body condition and fat content and increased smoltification (Jones, Bergman, & Greenberg, ) but has also been shown to reduce migration (Midwood, Larsen, Aarestrup, & Cooke, ) or delay smoltification (Näslund, Sundström, & Johnsson, ). Females are more likely to migrate, mature later, and at a larger body size (Klemetsen et al, ) than males, and the difference in fecundity between large and small female fish can result in differences in trout population dynamics (via egg and juvenile density; Elliot, ), even at small geographic scales.…”

Section: Introductionmentioning

confidence: 99%

Landscape features determine brown trout population structure and recruitment dynamics

Jones

Akbaripasand

Nakagawa

et al. 2019

Ecology of Freshwater Fish

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Variation in brown trout (Salmo trutta L.) population recruitment and structure is related to migratory patterns, which should depend on ease of access to habitats providing increased opportunity for growth. We quantified the number of young of year (YOY) as a proportion of the total number of brown trout at 24 locations on 11 streams within the Taieri catchment, New Zealand, including back calculated growth rates and emergence dates from otoliths. Locations with high absolute and relative abundance of YOY fish were related to elevation and distance from the river mainstem (habitat used by migratory fish), fish density, and the interaction between invertebrate food biomass, distance and elevation. Hatch date and growth were not related to the proportion of YOY fish, though growth was negatively correlated to total fish density. We suggest landscape features play a large role in determining recruitment and population structure. Locations at lower elevations have a high YOY density, high competition and lower growth, likely prompting out‐migration. These conditions could be created by successful return migration and spawning of large fecund fish resulting in YOY densities exceeding the habitat carrying capacity. Environmental factors, such as food availability, also played a role in determining population structure. These results provide an example of how population structure and recruitment might be controlled by local conditions and access to high growth environments in wild populations of introduced brown trout across a catchment.

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Stress and food deprivation: linking physiological state to migration success in a teleost fish

Cited by 31 publications

References 75 publications

Short-term and long-term effects of transient exogenous cortisol manipulation on oxidative stress in juvenile brown trout

Short-term and long-term effects of transient exogenous cortisol manipulation on oxidative stress in juvenile brown trout

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

Landscape features determine brown trout population structure and recruitment dynamics

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