Red muscle recruitment during steady swimming correlates with rostral-caudal patterns of power production in trout

Rainbow trout (Oncorhynchus mykiss) and brook trout (or charr, Salvelinus fontinalis) display different rostral-caudal patterns of power production by the red or aerobic muscle during steady swimming. The anterior muscle of rainbow trout produces much less power for swimming than the posterior, while in brook trout there is no variation in power output. To determine if red muscle recruitment is associated with anterior-posterior patterns of power production, electromyography (EMG) was used to record red muscle activity at three body positions across a range of swimming speeds in fish of each species. The initial recruitment of the anterior red muscle in swimming rainbow trout was predicted to lag behind, i.e. occur at higher speeds, that of the posterior due to the variation in power production, but no variation in recruitment was expected for brook trout. Burst of red muscle EMG activity occurring with each tailbeat was analyzed for frequency (tailbeat frequency), duty cycle (DC) (duration of burst relative to the period of the tailbeat) and burst intensity (BI) (magnitude of the measured EMG activity). Brook trout swam with higher tailbeat frequencies and longer values of DC than rainbow trout. Both species showed a pattern of longitudinal variation in DC, with longer DC values in the anterior red muscle. BI also differed significantly along the length of rainbow trout but not brook trout. In the former, BI of anterior muscle was significantly less than the posterior at lower steady swimming speeds. The EMG data suggest that power production and muscle recruitment are related. In rainbow trout, where there is longitudinal variation in muscle power output, there are also significant rostral-caudal differences in red muscle recruitment.     

Red muscle function during steady swimming in brook trout, Salvelinus fontinalis.

Red muscle function during steady swimming in brook trout was studied through both in vivo swimming and in vitro muscle mechanics experiments. In the swimming experiments, red muscle activity was characterized through the use of electromyography and sonomicrometry, allowing the determination of several parameters such as tailbeat frequency, EMG burst duration, muscle length change patterns and relative phase of EMG activity and length change. Brook trout do show some shifts in these variables along their length during steady swimming, but the magnitude of these shifts is relatively small. In the muscle mechanics experiments, the in vivo muscle activity data were used to evaluate patterns of power production by red muscle during swimming. Unlike many fish species, the red muscle along the length of brook trout shows little change in isometric kinetic variables such as relaxation rate and twitch time. Furthermore, there is no rostral-caudal shift in red muscle mass-specific power output during steady swimming. This last result contrasts sharply with rainbow trout and with a variety of other fish species that power steady swimming primarily with the posterior red myotome.     

Central nervous system actions of growth hormone on brain monoamine levels and behavior of juvenile rainbow trout

Growth hormone (GH) has been demonstrated to alter the behavior of juvenile salmonids. However, the mechanisms behind this action are not yet understood. In mammals and birds, peripheral GH treatment has been shown to affect monoaminergic activity in the central nervous system, which may be a mechanism whereby GH alters behavior. To investigate if GH may influence behavior directly at the central nervous system, juvenile rainbow trout were injected with GH into the third ventricle of the brain, whereupon physical activity and food intake were observed during 2 h. Thereafter, brains were sampled and the content of serotonin, dopamine, and noradrenaline and their metabolites were measured in hypothalamus, telencephalon, optic tectum, and brainstem. The GH-treated fish increased their swimming activity relative to sham-injected controls, while appetite remained unchanged, compared with sham-injected controls. Analysis of brain content of monoamines revealed that the GH treatment caused a decrease in the dopamine metabolite homovanillic acid in the hypothalamus, indicating a lowered dopaminergic activity. It is concluded that GH may alter behavior by acting directly on the central nervous system in juvenile rainbow trout. Furthermore, GH seems to alter the dopaminergic activity in the hypothalamus. Whether this is a mechanism whereby GH affects swimming activity remains to be clarified.     

Comparative susceptibility of rainbow trout Oncorhynchus mykiss and brown trout Salmo trutta to Myxobolus cerebralis, the cause of salmonid whirling disease.

The susceptibility of rainbow trout Oncorhynchus mykiss and brown trout Salmo trutta to Myxobolus cerebralis, the cause of salmonid whirling disease, was assessed following dosed exposures to the infectious stages (triactinomyxons). Parallel groups of age-matched brown trout and rainbow trout were exposed to 10, 100, 1000 or 10,000 triactinomyxons per fish for 2 h and then placed in aquaria receiving single pass 15 degrees C well water. Severity of infection was evaluated by presence of clinical signs (whirling and/or black tail), prevalence of infection, severity of microscopic lesions, and spore counts 5 mo after exposure. Clinical signs of whirling disease, including a darkened caudal region (black tail) and radical tail chasing swimming (whirling), occurred first among rainbow trout at the highest dose at 6 to 7 wk post exposure. Black tail and whirling occurred among rainbow trout receiving 1000 and 100 triactinomyxons per fish at 8 to 9 wk post exposure. Only 1 of 20 fish had a black tail among rainbow trout receiving 10 triactinomyxons per fish, although 30% of the fish were infected at 5 mo post exposure. Black tails were observed in brown trout at 1000 and 10,000 triactinomyxons per fish beginning at 11 and 7 wk post exposure, respectively. There was no evidence of the tail chasing swimming (whirling) in any group of brown trout. The prevalence of infection, spore numbers, and severity of microscopic lesions due to M. cerebralis among brown trout were less at each exposure dose when compared to rainbow trout. Infections were found among rainbow trout at all doses of exposure but only among brown trout exposed to doses of 100 triactinomyxons per fish or greater. Risk of infection analyses showed that rainbow trout were more apt to be infected at each exposure dose than brown trout. Spore counts reached 1.7 x 10(6) per head among rainbow trout at the highest dose of exposure compared to 1.7 x 10(4) at the same exposure dose among brown trout. Spore numbers increased with dose of exposure in rainbow trout but not in brown trout. As microscopic lesion scores increased from mild to moderate, spore numbers increased in rainbow trout but not brown trout. The mechanisms by which brown trout resist infections with M. cerebralis were not determined. Cellular immune functions, including those of eosinophilic granular leukocytes that were more prominent in brown trout than rainbow trout, may be involved.     

Exercise training and the stress response in rainbow trout, Salmo gairdneri Richardson

Plasma levels of catecholamines, cortisol, and glucose were monitored in rainbow trout during a 6-week forced swimming exercise programme. Compared to resting non-exercised controls, resting trained fish had lower levels of epinephrine, norephinephrine, cortisol, and glucose during the last 3 weeks of training. Initially, trained fish that were swimming had higher levels of epinephrine than resting trained fish. After 2 weeks of exercise, swimming did not significantly elevate epinephrine levels in trained fish. Glucose levels were consistently greater in swimming fish than in resting fish. At the end of the training period, exercised trout had lower (15–20%) oxygen consumption rates while resting or swimming than unexercised fish.
After a 5-month forced swimming exercise programme plasma levels of catecholamines and glucose were monitored in trained and untrained cannulated rainbow trout after 2 min of mild agitation. Trained fish showed an immediate (within 1 min) increase in the levels of epinephrine, but not norepinephrine and a delayed (within 15 min) increase in the levels of plasma glucose. Epinephrine levels returned to pre-stress levels within 15 min. Untrained fish had no significant increase in the plasma levels of norepinephrine, epinephrine, or glucose.     

Rainbow trout <Emphasis Type="Italic">Oncorhynchus mykiss</Emphasis> energetic responsesto pulsed flows in the American River,California, assessed by electromyogram telemetry

Although rainbow trout Oncorhynchus mykiss within the American River, California, apparently exhibit minimal upstream or downstream movements in response to hydroelectric-power-generation-related pulsed flows, the associated energetic costs are unknown. We implanted rainbow trout (n = 9, ≥30 cm SL) with electromyogram (EMG)-sensor-equipped radio transmitters to assess the swimming behavior and associated energetic costs associated with their responses to pulsed flows. Using laboratory calibrations in a Brett-type swimming respirometer, the trouts’ swimming speeds and oxygen consumption rates were estimated for their in-river EMG data, through a complete hydroelectric power-generation river pulsed-flow sequence (pre-pulse, increasing flow, peak, and decreasing flow stages), on several (mean: 3.2) sampling dates. Using a mixed-linear model, we found that fish swimming speed estimates increased during the increasing flow stage, while the associated mean oxygen consumption rates also increased at this stage. At river flows near the usual peak (>44 m³s⁻¹), swimming speeds and movement rates decreased, possibly due to the fish using the river’s habitat complexities as hydraulic cover. We conclude that rainbow trout incur increased swimming-related energetic costs during increasing flows and, potentially, decreased foraging opportunities at high flows.     

The relationships among sprint performance, voluntary swimming activity, and social dominance in juvenile rainbow trout

The specific objectives of this study were to determine whether sprint performance in juvenile rainbow trout is correlated with either voluntary swimming activity or aggressive behaviors and to determine the reciprocal: the effect of swimming activity and aggression on sprint performance. Sprint performance was assessed by rapidly accelerating trout (5-7-cm fork length) to a fixed velocity (40, 42, or 45 cm s(-1)) and then holding them at that velocity until fatigue. There was considerable interindividual variation in sprint performance not explained by variations in body size, but intraindividual performance was highly repeatable over at least 2 mo. Voluntary swimming was measured as the frequency of transits (voluntary transit activity, VTA) between two identical tanks via a connecting channel with two different flow regimes: zero or minimum velocity (0 or 2.5 cm s(-1)) and high velocity (84 cm s(-1)). There was a strong correlation between sprint performance and VTA in minimal current but no correlation in high current. Furthermore, sprint performance did not predict the outcome of dominance encounters. Experience with rapid acceleration, especially when voluntary, led to a pronounced improvement in sprint performance in proportion to the number of acceleration events. Social dominance encounters had a more complex effect: a significant reduction in sprint performance in previously high-performance sprinters and the reverse for low performers. We propose that there are four independent axes of interindividual variation in juvenile rainbow trout: spontaneous and rheotaxis-stimulated locomotor activity, aggressive activity, and the trainability of sprint performance. The independence of these axes has the potential to produce a much larger diversity in behavioral and ultimately physiological phenotypes than would be produced if the axes were linked.     

Heterochrony and the development of the escape response: prehatching movements in the rainbow trout Oncorhynchus mykiss

Teleost fishes produce coordinated escape responses (C-starts) at hatching. This implies that essential swimming morphologies and motor behaviors develop during the incubation interval while the embryo is in the chorion. We examined prehatching motor behaviors in rainbow trout Oncorhycus mykiss (considered morphologically mature at hatching) and compared this species with zebrafish Danio rerio (considered morphologically immature) and assessed two hypotheses concerning the development of escape behavior. (1) Escape behavior is associated with the formation of key elements of the musculoskeletal and nervous systems; thus, the escape response appears early in ontogeny, when these elements form. (2) Escape behavior is not directly associated with the formation of underlying morphological elements; instead, it appears at hatching (i.e. when needed). We find that rainbow trout, like zebrafish, respond to touch early in the incubation interval, but do not demonstrate a complete C-start (including the second, propulsive stage) until shortly before hatching. At hatching, rainbow trout and zebrafish are similar in the degree of development of the chondocranium, paired fins and visceral arches (which comprise the larval jaw and gill support); however, rainbow trout have incipient rays in their unpaired fins (dorsal, anal and caudal), whereas zebrafish retain the embryonic fin fold. Although rainbow trout are more mature in axial swimming morphology at hatching, the essential neural and musculoskeletal systems that produce a coordinated escape response are functional at hatching in both species. This finding supports the evolutionary hypothesis that an effective escape response is critical for the survival of newly hatched teleost fishes.     

A Flexible Fin with Bio-Inspired Stiffness Profile and Geometry

Biological evidence suggests that fish use mostly anterior muscles for steady swimming while the caudal part of the body is passive and,acting as a carrier of energy,transfers the momentum to the surrounding water.Inspired by those findings we hypothesize that certain swimming patterns can be achieved without copying the distributed actuation mechanism of fish but rather using a single actuator at the anterior part to create the travelling wave.To test the hypothesis a pitching flexible fin made of silicone rubber and silicone foam was designed by copying the stiffness distribution profile and geometry of a rainbow trout.The kinematics of the fin was compared to that of a steadily swimming trout.Fin's propulsive wave length and tail-beat amplitude were determined while it was actuated by a single servo motor.Results showed that the propulsive wave length and tail-beat amplitude of a steadily swimming 50 cm rainbow trout was achieved with our biomimetic fin while stimulated using certain actuation parameters (frequency 2.31 Hz and amplitude 6.6 degrees).The study concluded that fish-like swimming can be achieved by mimicking the stiffness and geometry of a rainbow trout and disregarding the details of the actuation mechanism.     

Sub-lethal plasma ammonia accumulation and the exercise performance of salmonids

The proposal that plasma ammonia accumulation might impair the swimming performance of fish was first made over a decade ago, and has now proven to be the case for a number of salmonid species. The first experimental evidence was indirect, when a negative linear relationship between plasma ammonia concentrations and maximum sustainable swimming speed (U(crit)) was found following the exposure of brown trout (Salmo trutta) to sub-lethal concentrations of copper in soft acidic water. Since then, negative linear relationships between plasma ammonia concentration and U(crit) have been demonstrated following exposure of brown trout, rainbow trout (Oncorhynchus mykiss) and coho salmon (Oncorhynchus kisutch) to elevated water ammonia. For brown trout, the relationships between plasma ammonia and U(crit) were remarkably similar following either exposure to elevated water ammonia or to sub-lethal copper. This indicates that the impairment of swimming performance resulting from exposure to sub-lethal concentrations of heavy metals may be attributable in large part to an accumulation of endogenous ammonia. The negative relationship between plasma ammonia concentration and U(crit) was similar in size-matched rainbow and brown trout but, under similar regimes of ammonia exposure, rainbow trout were able to maintain a significantly lower plasma ammonia concentration, revealing inter-specific differences in ammonia permeability and/or transport. One primary mechanism by which ammonia accumulation may impair exercise performance is a partial depolarisation of membrane potential in tissues such as the brain and white muscle. This may prejudice the co-ordination of swimming movements and reduce or abolish the development of muscle tension, thus, compromising swimming efficiency and performance at the top end of the range.     

Observations of poor swimming performance among hatchery-reared rainbow trout,Salmo gairdneri

Synopsis The swimming performance, as judged by maximum sustained swimming speed, of rainbow trout from a fish farm in S.W. England, is low when compared to previously published values for this species. This may be a localised peculiarity resulting from hatchery selection and rearing procedures.     

Effects of temperature, salinity, and feeding on aminotransferase activity in the liver and white muscle of rainbow trout (Salmo gairdneri Richardson).

1. The liver-somatic index of rainbow trout is governed by temperature and salinity, and by the interaction of these two factors. 2. The overall liver-alanine aminotransferase activity (in units/100 g body weight) increases slightly with increasing salinity of the surroundings in the case of rainbow trout. 3. The overall liver-aspartate aminotransferase activity (in units/100 g body weight) in rainbow trout depends on their food and the temperature at which they are kept. 4. Salinity adaptation leads to reductions in the specific alanine and aspartate aminotransferase activity in the liver of rainbow trout. 5. The specific alanine aminotransferase activity in the muscle of starving rainbow trout kept in diluted seawater (580 mOsm/l, 18 degrees C) is clearly higher than in control animals kept in tapwater.     

Exhaustive exercise does not affect the preferred temperature for recovery in juvenile rainbow trout (Oncorhynchus mykiss)

We tested the hypothesis that juvenile rainbow trout (Oncorhynchus mykiss) would select a temperature colder than their acclimation temperature (16 deg +/-1 deg C) to minimize postexhaustive exercise metabolic demands and enhance oxygen availability. After an initial 3-h exploratory period in a thermal gradient (6 degrees -25 degrees C), fish selected a temperature of approximately 14 degrees C and had a baseline exploratory swimming activity of approximately 60 cm min(-1). Subsequently, experimental (chased) fish were individually removed, exhaustively exercised for 1.5 min, and replaced. Both control (unchased) and experimental fish were allowed to explore the thermal gradient for another 2 h. Immediately after being chased, trout had a metabolic profile that was consistent with being exhausted; levels of plasma and muscle lactate were 4.38+/-0.25 mmol L(-1) and 28.0+/-2.0 mmol kg(-1), respectively, and levels of muscle glycogen, adenosine triphosphate, and phosphocreatine were 3.89+/-0.95, 4.23+/-0.62, and 3.07+/-0.73 mmol kg(-1), respectively. Although exploratory swimming activity of the chased fish was significantly lower (by 81%) as compared with control fish during the first 5 min postchase, differences in the mean, median, and mode values for selected temperatures during the next 2 h were neither large (<1 degrees C) nor significant (P>0.05). Contrary to our initial hypothesis, these findings suggest that juvenile rainbow trout do not select a colder temperature to decrease metabolic rate following exhaustive exercise. Instead, rainbow trout selected a temperature marginally cooler than their acclimation temperature (16 degrees C) regardless of whether they had been previously exhausted.     

The effect of antioxidants on the quality of cryopreserved semen in two salmonid fish, the brook trout (Salvelinus fontinalis) and the rainbow trout (Oncorhynchus mykiss)

Until now the supplementation of cryopreservation extenders with antioxidants has not been examined in teleost fish. Therefore, the present study investigated whether addition of antioxidants (catalase, superoxide dismutase, peroxidase, reduced glutathione, reduced methione, mixtures of reduced and oxidized glutathione or methionine) to the cryopreservation extenders could increase the quality of frozen-thawed semen of brook trout, Salvelinus fontinalis, and rainbow trout, Oncorhynchus mykiss. In brook trout and rainbow trout semen post-thaw fertility and motility were evaluated and in brook trout additionally the membrane integrity, DNA integrity, and sperm lipid peroxidation were evaluated. The tested antioxidants affected the motility parameters, DNA integrity, and fertility of cryopreserved semen, but not the membrane integrity. Most of the observed effects were negative and only minor positive effects were found. In brook trout 1.5 mmol/l reduced methionine and a mixture of 1.5 mmol/l oxidized and reduced glutathione increased the swimming velocity of frozen-thawed semen. One hundred U/l catalase, 1.5 mmol/l reduced glutathione, and 1.5 mmol/l reduced methionine slightly, but not statistically significantly increased the semen post-thaw fertility. However, these effects were not detectable in rainbow trout. Antioxidative stress or damage seems to play no role during cryopreservation, as also in the lipid peroxidation test no differences were obtained between fresh and cryopreserved semen. Therefore, for routine cryopreservation extender supplementation with antioxidants is not recommended in brook trout and rainbow trout.     

A biotelemetry system recording fish activity

A biotelemetry system is described for obtaining, transmitting and recording the electromyograms (EMGs) produced in muscle activity of free-swimming fish as quantitative indicators of overall fish activity. The radiotransmitters used come in the form of cylindrical packages having two sensing electrodes, all fully implantable in the fish body cavity. EMGs are transmitted as radio pulses with the intensity of muscular activity determining the intervals between pulses. The packages also contain temperature sensors and fish temperatures are transmitted with every 32nd pulse. Transmitted EMG pulses are detected, 'measured' and stored by a single portable receiver (Model SRX_400, Lotek). Data can be subsequently transferred to a computer (which can also be portable) for storage, processing and statistical analysis. Transmitter battery life can be in excess of 7 months, permitting laboratory or field studies of long duration. Transmitter package implantation surgery requires a mid-ventral incision and internal securing of transmitter and sensing electrodes. Surgical silk, cyanoacrylate tissue adhesives, and polydioxanone (PD), a synthetic absorbable suture, were all tried as means of incision closure. The most effective was PD alone. Trials of the system consisted of forced swims by transmitter-equipped rainbow trout Oncorhynchus mykiss Walbaum. The data obtained provided an inverse linear relation between forced swim speed and EMG pulse interval. Trials were conducted at intervals over periods up to 2 months. Fish showed neither distress, nor difficulty in swimming up to maximum speeds of 60 cm s ⁻¹ (fish lengths 41.0, 44.4 cm).     

The use of opercular muscle electromyograms as an indicator of the metabolic costs of fish activity in rainbow trout, Salmo gairdneri Richardson, as determined by radiotelemetry

Averages of electromyogram (EMG) signals emanating from the levator arcus palatini , a small muscle involved in the operation of the operculum in rainbow trout, Salmo gairdneri , were analysed in terms of their relationship to the fish's oxygen consumption rates under various activity levels. The EMG signals were detected and transmitted with a radio-telemetry system. The EMG values showed a good correlation with corresponding oxygen consumption rates for fish under forced-swimming conditions but not when the fish was swimming spontaneously; this is attributed to an ability to regulate oxygen uptake at the gill surfaces by other means than increasing the ventilation volume, including alterations in the gill blood flow dynamics (e.g. secondary lamellar recruitment), and changes in the cardiac output. Under forced-swim conditions, where the oxygen demands by the respiring muscles were higher, increased ventilation volume, as indicated by increased opercular muscle activity, was directly related to swimming speed and oxygen uptake.     

Peripherally administered growth hormone increases brain dopaminergic activity and swimming in rainbow trout

There is increasing evidence that growth hormone (GH) has important behavioral effects in fish, but the underlying mechanisms are not well understood. To investigate if peripherally administered GH influences the monoaminergic activity of the brain, and how this is correlated to behavior, juvenile rainbow trout were implanted intraperitoneally with ovine GH. Fish were either kept isolated or in groups of five. The physical activity and food intake of the isolated fish were observed after 1 and 7 days, when brains were also sampled. The content of serotonin, dopamine, and noradrenaline and their metabolites in hypothalamus, telencephalon, optic tectum, and brain stem was then analyzed. For fish kept isolated for 7 days following implant, GH increased swimming activity and the levels of the dopamine metabolite 3, 4-hydroxy-phenylacetic acid (DOPAC) were higher in all brain parts examined. In the optic tectum, the levels of the dopamine metabolite homovanillic acid (HVA) were lowered by the GH treatment. One-day GH implant did not affect behavior or monoamine levels of isolated fish. In the fish kept in groups, a 7-day GH implant increased the hypothalamic levels of DOPAC, but not in the other brain parts examined, which may indicate an effect on the brain dopaminergic system from social interactions. It can be concluded that peripherally administered GH may function as a neuromodulator, affecting the dopaminergic activity of the rainbow trout brain, and this is associated with increased swimming activity.     

Magnetic field perception in the Rainbow Trout, <Emphasis Type="Italic">Oncorhynchus</Emphasis> <Emphasis Type="Italic">mykiss</Emphasis>

In this study, we present evidence for the perception of different magnetic field parameters in a facultative anadromous fish species of the family Salmonidae. Magnetic field perception of the rainbow trout, Oncorhynchus mykiss, was demonstrated with a heartbeat conditioning test. The electrocardiogram was measured with subcutaneously inserted silver wire electrodes in freely swimming fish. We demonstrate a conditioned response (i.e. a significant longer interval between two heartbeats) to an intensity/inclination shift for three adult and two juvenile rainbow trouts. Moreover, a conditioned response to a 90° direction shift was demonstrated for three adult and two juvenile trouts. These findings support the hypothesis that the rainbow trout is able to perceive different magnetic field parameters. Furthermore, the study demonstrates magnetosensation in different developmental stages in the rainbow trout, i.e. juvenile and adult fish.     

Non-invasive recording of heart rate and ventilation rate in rainbow trout during rest and swimming. Fish go wireless!

Resting heart rates and ventilation rates in rainbow trout Oncorhynchus mykiss at 15°C are 31·8±1·8 beat min⁻¹ and 53·1±3·7 breaths min⁻¹, respectively. The non-invasive recording system picked up the bioelectric potentials generated by the fish in the water and was based on an array of six silver-silver chloride electrodes covered with agar-gel, which provided a better signal-to-noise ratio than in previously described systems, and allowed the determination of heart rate and ventilation rates at different swimming speeds up to 21 s⁻¹. In concert with the lower rates, the scope for changes in heart rate and ventilation rate during swimming was also considerably larger than in earlier studies (2·4- and 2·0-fold, respectively). Two main conclusions result from this work: (i) short recovery times under 48 h after anaesthesia and surgery are unlikely to provide truly resting heart rates and ventilation rates in trout at 15°C; (ii) heart rate regulation during exercise is more important than previously thought and might account for a larger proportion of the increase in cardiac output observed in swimming trout.