Winter diet of brown trout <i>Salmo trutta</i> in groundwater‐dominated streams: influence of environmental factors on spatial and temporal variation

French, William E.; Vondracek, Bruce; Ferrington, Leonard C.; Finlay, Jacques C.; Dieterman, Douglas J.

doi:10.1111/jfb.13128

Cited by 5 publications

(3 citation statements)

References 49 publications

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“…Like many other organisms, Brown trout experience periods of limited food availability in their natural environment (Bayir et al, 2011;French, Vondracek, Ferrington, Finlay, & Dieterman, 2016;Huusko et al, 2007). The first winter is a critical period for the survival of young salmonid fishes: food is often limiting, and their survival is dependent on metabolic adjustments (Finstad, Ugedal, Forseth, & Naesje, 2004;Huusko et al, 2007).…”

Section: Discussionmentioning

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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Section: Discussionmentioning

confidence: 99%

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

et al. 2018

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“…In the present study we examined the effects of food availability on mitochondrial properties, focusing in particular on the consequences for these alternative measures of mitochondrial efficiency. We determined the mitochondrial responses of brown trout (Salmo trutta) to a period of food shortage that simulated the situation periodically faced by these fish in their natural environment (Huusko et al, 2007;French et al, 2016). We chose liver as our tissue to analyse mitochondrial flexibility because liver mitochondria have been shown to be particularly sensitive to fluctuations in food availability (Frick et al, 2008;Trzcionka et al, 2008;Rui, 2014;Chausse et al, 2015).…”

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confidence: 99%

The RCR and ATP/O Indices Can Give Contradictory Messages about Mitochondrial Efficiency

Salin

Villasevil

Anderson

et al. 2018

Integrative and Comparative Biology

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Mitochondrial efficiency is typically taken to represent an animal's capacity to convert its resources into ATP. However, the term mitochondrial efficiency, as currently used in the literature, can be calculated as either the respiratory control ratio, RCR (ratio of mitochondrial respiration supporting ATP synthesis to that required to offset the proton leak) or as the amount of ATP generated per unit of oxygen consumed, ATP/O ratio. The question of how flexibility in mitochondrial energy properties (i.e., in rates of respiration to support ATP synthesis and offset proton leak, and in the rate of ATP synthesis) affects these indices of mitochondrial efficiency has tended to be overlooked. Furthermore, little is known of whether the RCR and ATP/O ratio vary in parallel, either among individuals or in response to environmental conditions. Using data from brown trout Salmo trutta we show that experimental conditions affect mitochondrial efficiency, but the apparent direction of change depends on the index chosen: a reduction in food availability was associated with an increased RCR (i.e., increased efficiency) but a decreased ATP/O ratio (decreased efficiency) in liver mitochondria. Moreover, there was a negative correlation across individuals held in identical conditions between their RCR and their ATP/O ratio. These results show that the choice of index of mitochondrial efficiency can produce different, even opposing, conclusions about the capacity of the mitochondria to produce ATP. Neither ratio is necessarily a complete measure of efficiency of ATP production in the living animal (RCR because it contains no assessment of ATP production, and ATP/O because it contains no assessment of respiration to offset the proton leak). Consequently, we suggest that a measure of mitochondrial efficiency obtained nearer to conditions where respiration simultaneously offsets the proton leak and produce ATP would be sensitive to changes in both proton leakage and ATP production, and is thus likely to be more representative of the state of the mitochondria in vivo.

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“…However, Brown Trout diets contained high numbers of rarely observed drifting prey taxa (e.g., Gammurus, Lirceus, Gastropoda) (Rader 1997) suggesting some epibenthic foraging has occurred. Several diet studies conducted in Minnesota streams found benthic feeding by Brown Trout occurred in the winter due to the selection for large-bodied taxa (Gammarus, Isopoda, Limnephilidae, Tipulidae, Physella) (French et al 2014(French et al , 2016b and prey in the benthos rather than in the drift (Anderson et al 2016). Brown Trout diets in the Arkansas tailwaters also suggest that consuming benthic macroinvertebrates (e.g., Gammarus, Lirceus) wase more important than selecting for drifting macroinvetebrates (e.g., Chironomidae).…”

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Spatial and Temporal Consumption Dynamics of Trout in Catch‐and‐Release Areas in Arkansas Tailwaters

Flinders¹,

Magoulick

2017

Trans Am Fish Soc

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Restrictive angling regulations in tailwater trout fisheries may be unsuccessful if food availability limits energy for fish to grow. We examined spatial and temporal variation in energy intake and growth in populations of Brown Trout Salmo trutta and Rainbow Trout Oncorhynchus mykiss within three catch-and-release (C-R) areas in Arkansas tailwaters to evaluate food availability compared with consumption. Based on bioenergetic simulations, Rainbow Trout fed at submaintenance levels in both size-classes (≤400 mm TL, >400 mm TL) throughout most seasons. A particular bottleneck in food availability occurred in the winter for Rainbow Trout when the daily ration was substantially below the minimum required for maintenance, despite reduced metabolic costs associated with lower water temperatures. Rainbow Trout growth rates followed a similar pattern to consumption with negative growth rates during the winter periods. All three size-classes (<250 mm TL, 250-400 mm TL, >400 mm TL) of Brown Trout experienced high growth rates and limited temporal bottlenecks in food availability. We observed higher mean densities for Rainbow Trout (47-342 fish/ha) than for Brown Trout (3-84 fish/ha) in all C-R areas. Lower densities of Brown Trout coupled with an ontogenetic shift towards piscivory may have allowed for higher growth rates and sufficient consumption rates to meet energetic demands. Brown Trout at current densities were more effective in maintaining adequate growth rates and larger sizes in C-R areas than were Rainbow Trout. Bioenergetic simulations suggest that reducing stocking levels of Rainbow Trout in the tailwaters may be necessary in order to achieve increased catch rates of larger trout in the C-R areas.

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Winter diet of brown trout Salmo trutta in groundwater‐dominated streams: influence of environmental factors on spatial and temporal variation

Cited by 5 publications

References 49 publications

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

The RCR and ATP/O Indices Can Give Contradictory Messages about Mitochondrial Efficiency

Spatial and Temporal Consumption Dynamics of Trout in Catch‐and‐Release Areas in Arkansas Tailwaters

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