The standard metabolic rate of dolphin fish

The standard metabolic rates (SMRs) of 11 (1.395–4.125 kg) dolphin fish (mahimahi or dorado, Coryphaena hippurus ) were measured at 25°± 0.5°C. Fish were prevented from swimming with neuromuscular blocking agents and force ventilated. Heart rates were determined simultaneously. SMRs (358–726 mg O₂ h ^–1) were several times those of other similarly sized active teleosts such as salmonids, but close to those of tunas. Heart rates (84–161 beats min ^–1) were also high, but alike those of tunas under similar circumstances. As in tunas, the high SMR of dolphin fish may result from high osmoregulatory costs engendered by their large gill surface areas and/or other adaptations necessary for achieving exceptionally high maximum metabolic rates.     

A high standard metabolic rate constrains juvenile growth

The allocation of energy to various components of an individual's energy budget is often viewed as a competitive process. As such, a tradeoff may exist between production (growth) and maintenance metabolism. One view of a potential tradeoff, termed “the principle of allocation”, suggests that individuals with lower maintenance metabolic expenditures may have higher growth rates. To determine whether such a tradeoff exists, I analyzed the relationship between growth rate and maintenance metabolism of 225 juvenile snapping turtles housed in the laboratory. I measured growth from hatching to 6 months of age, and then measured oxygen consumption and calculated standard metabolic rate. Mean growth rate was 0.19 g d⁻ and mean standard metabolic rate (SMR) was 1.41 kJ d⁻. Maintenance metabolism and growth were negatively correlated after both were adjusted for body mass. The results support the “principle of allocation” theory: individuals with higher standard metabolic rates tended to have low growth rates.     

Metabolic costs of growth in free-living Garter Snakes and the energy budgets of ectotherms

1. The metabolic or respiratory cost of growth ( R _G) is the increase in metabolic rate of a growing animal, and it represents chemical potential energy expended in support of net biosynthesis but not deposited as new tissue.
2. Two statistical methods (multiple non-linear regression and analysis of regression residuals) were used to calculate R _G from data ( n = 68) from a doubly labelled water study of free-ranging Garter Snakes ( Thamnophis sirtalis fitchi ) in northern California.
3. The sample-wise ('ecological') cost of growth was 2·07 kJ per gram of net growth (equivalent to 8·63 kJ g^–1 dry tissue); reanalysis of a subset of efficient growers yielded a more conservative 'physiological' estimate of 1·67 kJ g^–1.
4. Our empirical estimate of R _G, among the first reported for squamate reptiles and free-living animals of any kind, compares closely with published, laboratory-derived values for ectotherms.
5. The metabolic costs of growth accounted for an average of 30% of total field metabolic rates for these snakes, which were growing at a mean rate of 3% of body mass per day. However, our method probably underestimated the total ecological cost of growth for large animals, because potential growth costs that covary with body size were not included.
6. Distinction between conceptual and empirical energy budgets clarifies relationships among body size, metabolic rates, and the physiological and ecological costs of growth.     

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.     

Continuous growth through winter correlates with increased resting metabolic rate but does not affect daily energy budgets due to torpor use

Small mammals that are specialists in homeothermic thermoregulation reduce their self-maintenance costs of normothermy to survive the winter. By contrast, heterothermic ones that are considered generalists in thermoregulation can lower energy expenditure by entering torpor. It is well known that different species vary the use of their strategies to cope with harsh winters in temperate zones; however, little is still known about the intraspecific variation within populations and the associated external and internal factors. We hypothesized that yellow-necked mice Apodemus flavicollis decrease their resting metabolic rate (RMR) from autumn to winter, and then increase it during spring. However, since the alternative for seasonal reduction of RMR could be the development of heterothermy, we also considered the use of this strategy. We measured body mass (m_b), RMR, and body temperature (T_b) of mice during 2 consecutive years. In the 1st year, mice decreased whole animal RMR in winter, but did not do so in the 2nd year. All mice entered torpor during the 2nd winter, whereas only a few did so during the first one. Mice showed a continuous increase of m_b, which was steepest during the 2nd year. The relationship between RMR and m_b varied among seasons and years most likely due to different mouse development stages. The m_b gain at the individual level was correlated positively with RMR and heterothermy. This indicates that high metabolism in winter supports the growth of smaller animals, which use torpor as a compensatory mechanism. Isotope composition of mice hair suggests that in the 1st year they fed mainly on seeds, while in the 2nd, they likely consumed significant amounts of less digestible herbs. The study suggests that the use of specialist or generalist thermoregulatory strategies can differ with environmental variation and associated differences in developmental processes.     

Aggression and growth depression in juvenile Atlantic salmon: the consequences of individual variation in standard metabolic rate

In aquaculture, competitive interactions for food are a major source of growth rate variation, since they result in aggressive individuals acquiring a disproportionate amount of food and growing faster. Consequently, such competition increases the variance and skew of the size distribution of fish. In Atlantic salmon Salmo salar acquaculture, rearing is often initiated with juveniles of uniform size. However, the initial factors allowing fish to out-compete others of the same size is unclear. This study shows that individual differences in standard metabolic rate (SMR) may contribute to differences in aggression between juvenile Atlantic salmon. Fish were segregated into three holding tanks on the basis of differences in relative SMR aggression was highest in the tank containing high SMR fish, and lowest in a low SMR group. However, there were no significant differences in mean growth between the three treatments, although the skew of the size distribution was much less in the low SMR group than in the high SMR group. Therefore, although mean growth was not improved in the low SMR group by excluding high SMR fish, their growth subsequently showed less variability, possibly as a consequence of fewer despotic individuals gaining disproportionate access to food.     

Relationship between standard metabolic rate and parasite-induced cataract of juveniles in three Atlantic salmon stocks

The connection between standard metabolic rate ( R _S) and parasite-induced cataract was investigated in this study. Oxygen consumption rate and cataract of 1 year-old fish in three Atlantic salmon Salmo salar stocks: Lake Saimaa, River Neva and River Teno reared at the same fish farm were examined. The measurements were carried out in winter, in spring before transporting the fish to the outside raceways and in autumn after the raceway period. Fish were exposed to natural Diplostomum spp. infection especially during the raceway period. The prevalence of cataract-bearing fish and cataract intensities ( I _C) differed between the populations. Most cataract-bearing individuals were found in the Saimaa stock and, in addition, the Saimaa stock had higher I _C than Neva and Teno stocks. These findings support the theory of a parasite being most infective to local population. The R _S, however, differed also between the stocks, the Teno stock had higher values compared to the Neva stock in winter. Furthermore, R _S and cataract intensity had a statistically significant positive correlation in autumn. Therefore, the results also reveal a possibility that parasite infection affects R _S of the fish.     

Valid oxygen uptake measurements: using high r2 values with good intentions can bias upward the determination of standard metabolic rate

This analysis shows good intentions in the selection of valid and precise oxygen uptake (O₂) measurements by retaining only slopes of declining dissolved oxygen level in a respirometer that have very high values of the coefficient of determination, r², are not always successful at excluding nonlinear slopes. Much worse, by potentially removing linear slopes that have low r² only because of a low signal-to-noise ratio, this procedure can overestimate the calculation of standard metabolic rate (SMR) of the fish. To remedy this possibility, a few simple diagnostic tools are demonstrated to assess the appropriateness of a given minimum acceptable r², such as calculating the proportion of rejected O₂ determinations, producing a histogram of the r² values and a plot of r² as a function of O₂. The authors offer solutions for cases when many linear slopes have low r². The least satisfactory but easiest to implement is lowering the minimum acceptable r². More satisfactory solutions involve processing (smoothing) the raw signal of dissolved oxygen as a function of time to improve the signal-to-noise ratio and the r²s.     

The stability of standard metabolic rate during a period of food deprivation in juvenile Atlantic salmon

Among juvenile Atlantic salmon Salmo salar either being fed ad libitum throughout a 3 month experiment or deprived of food in the middle month, food deprivation led to a decrease in SMR, which increased again once food was supplied ad libitum again. While the rank order of SMR among fish fed throughout remained relatively stable, that within the deprived group was inconsistent, suggesting that individual fish vary in their ability to reduce metabolic costs when food availability is low.     

Influence of sexual maturity on feeding, growth and energy stores of wild Atlantic salmon parr

Maturing Salmo salar parr had significantly lower short-term energy stores (indicated by hepato-somatic index) in August, and significantly lower energy stores and growth rate (indicated by RNA : DNA) in September than immature parr captured from the same stream sites on the same date. There were no significant differences in gut fullness or protein concentrations, suggesting that up to early September the main energetic consequences of maturation were a reduction in allocations to growth and short-term energy storage, but not a mobilization of long-term stored energy in the form of proteins. These are the first observations of relative food intake and energy storage for maturing parr under natural conditions, and also the first to assess growth effects on wild fish before completion of the maturation process.     

Gut morphology in growth hormone transgenic Atlantic salmon

Growth hormone transgenic Atlantic salmon Salmo salar reared at 12–13°C were F₂ generation derived, using eggs from a transgenic F₁ female and fertilized with milt from a non-transgenic male. At the time of tissue sampling the transgenic salmon were growing 1·6 times faster than control salmon. Transgenic salmon tended to have more intestinal folds that were longer than those of control salmon. Consequently, the transgenic salmon had a larger digestive surface area both in the anterior intestine (surface area 1·5 times control) and in the pyloric caeca (surface area 1·2 times control). Most morphological features of the intestine and of the pyloric caeca of transgenic salmon were larger than those of control salmon; in particular, the surface area of the anterior intestine was concordant with the growth rate difference.     

Warming up the system: higher predator feeding rates but lower energetic efficiencies

Predictions on the consequences of the rapidly increasing atmospheric CO₂ levels and associated climate warming for population dynamics, ecological community structure and ecosystem functioning depend on mechanistic energetic models of temperature effects on populations and their interactions. However, such mechanistic approaches combining warming effects on metabolic (energy loss of organisms) and feeding rates (energy gain by organisms) remain a key, yet elusive, goal. Aiming to fill this void, we studied the metabolic rates and functional responses of three differently sized, predatory ground beetles on one mobile and one more resident prey species across a temperature gradient (5, 10, 15, 20, 25 and 30 °C). Synthesizing metabolic and functional‐response theory, we develop novel mechanistic predictions how predator–prey interaction strengths (i.e., functional responses) should respond to warming. Corroborating prior theory, warming caused strong increases in metabolism and decreases in handling time. Consistent with our novel model, we found increases in predator attack rates on a mobile prey, whereas attack rates on a mostly resident prey remained constant across the temperature gradient. Together, these results provide critically important information that environmental warming generally increases the direct short‐term per capita interaction strengths between predators and their prey as described by functional‐response models. Nevertheless, the several fold stronger increase in metabolism with warming caused decreases in energetic efficiencies (ratio of per capita feeding rate to metabolic rate) for all predator–prey interactions. This implies that warming of natural ecosystems may dampen predator–prey oscillations thus stabilizing their dynamics. The severe long‐term implications; however, include predator starvation due to energetic inefficiency despite abundant resources.     

The metabolic rates associated with resting, and with the performance of agonistic, submissive and digging behaviours in the cichlid fish Neolamprologus pulcher (Pisces: Cichlidae)

We measured the metabolic rates as a direct estimate of energy expenditure of individual Neolamprologus pulcher, a cooperatively breeding cichlid fish, when resting and when performing agonistic, submissive or digging behaviours in a respirometer. Standard and routine metabolic rates increased linearly with body mass (range 0.9–8.4 g) when plotted on a doubly logarithmic scale (linear regression equations: standard metabolic rate: log individual oxygen consumption rate = 0.65 + 0.86 log body mass; routine metabolic rate: log individual oxygen consumption rate = 0.75 + 0.86 log body mass). Routine metabolic rates were, on average, 30% higher than standard metabolic rates. Submissive and agonistic behaviours raised routine metabolic rates by factors of 3.3 and 3.9, respectively. Digging resulted in a 6.1-fold increase of routine metabolic rates. Differences in metabolic rates between active and resting rates were statistically significant. However, those between the three behaviours were not. Mean opercular beat frequencies correlated significantly with routine metabolic rates and with metabolic rates when performing specific behaviours, which offers methodological prospects for field measurements. In N. pulcher, the high energy expenditure for submissive behaviour may indicate that this is a reliable signal. The considerable energy expenditure involved in territory defence suggests that these costs should be considered in addition to risk in cost-benefit analyses. This is the first study in which the energy expenditures of specific social and territory maintenance behaviours of individual fish were measured directly by respirometry and within the usual social setting of the fish. Accepted: 20 February 1998     

Intestinal morphology in growth hormone transgenic coho salmon

In two GH transgenic coho salmon Oncorhynchus kisutch , the surface area of the intestine was 2·2 times that of control salmon and the growth rate was about twice that of controls. It seems likely that the enhanced intestinal surface area is a compensatory feature that is manifested in fast growing salmonids.     

Basal metabolic rate is positively correlated with parental investment in laboratory mice

The assimilation capacity (AC) hypothesis for the evolution of endothermy predicts that the maternal basal metabolic rate (BMR) should be positively correlated with the capacity for parental investment. In this study, we provide a unique test of the AC model based on mice from a long-term selection experiment designed to produce divergent levels of BMR. By constructing experimental families with cross-fostered litters, we were able to control for the effect of the mother as well as the type of pup based on the selected lines. We found that mothers with genetically determined high levels of BMR were characterized by higher parental investment capacity, measured as the offspring growth rate. We also found higher food consumption and heavier visceral organs in the females with high BMR. These findings suggested that the high-BMR females have higher energy acquisition abilities. When the effect of the line type of a foster mother was controlled, the pup line type significantly affected the growth rate only in the first week of life, with young from the high-BMR line type growing more rapidly. Our results support the predictions of the AC model.     

Offspring viability benefits but no apparent costs of mating with high quality males

Traditional models of sexual selection posit that male courtship signals evolve as indicators of underlying male genetic quality. An alternative hypothesis is that sexual conflict over mating generates antagonistic coevolution between male courtship persistence and female resistance. In the scarabaeine dung beetle Onthophagus taurus, females are more likely to mate with males that have high courtship rates. Here, we examine the effects of exposing females to males with either high or low courtship rates on female lifetime productivity and offspring viability. Females exposed to males with high courtship rates mated more often and produced offspring with greater egg-adult viability. Female productivity and lifespan were unaffected by exposure to males with high courtship rates. The data are consistent with models of sexual selection based on indirect genetic benefits, and provide little evidence for sexual conflict in this system.     

Hypoxia impairs the digestive advantage of individual southern catfish (Silurus meridionalis) with high resting metabolic rates and postprandial metabolic responses

Empirical studies suggest that individuals with a high resting metabolic rate (RMR) are at an advantage under favourable conditions because they digest food rapidly and exhibit a greater growth potential. However, we hypothesised that high-RMR individuals have less energy available for digestion under hypoxia than they do under normoxia due to their relatively high maintenance cost. To test this hypothesis, we measured the RMR and postprandial metabolic responses of juvenile southern catfish, Silurus meridionalis, under normoxia and moderate hypoxia. The results provided the first evidence that (1) both the RMR and postprandial metabolic rate showed repeatability across different water [O₂] conditions and (2) the correlation between the RMR and postprandial metabolic traits differs with changes in environmental factors (water [O₂]). These findings suggested that the digestive advantage of individual southern catfish with a high RMR is impaired under hypoxia.