Cardiovascular responses of three salmonid species affected with amoebic gill disease (AGD)

The cardiovascular effects of amoebic gill disease (AGD) were investigated immediately following surgery in three salmonid species; Atlantic salmon (Salmo salar L.), brown trout (Salmo trutta L.) and rainbow trout (Oncorhynchus mykiss Walbaum). Fish, both naïve (control) and infected (AGD-affected) of each species, were fitted with dorsal aorta catheters and cardiac flow probes. Cardiac output and dorsal aortic pressures were then continuously measured over a 6-h period following surgery. Results showed that Atlantic salmon, brown trout and rainbow trout displayed similar dorsal aortic pressure, cardiac output, and systemic vascular resistance (mean dorsal aotic pressure divided by cardiac output) values. However, the only significant differences relating to disease status i.e. infected or control, were found in Atlantic salmon. Although no significant differences were seen in dorsal aortic pressure values, AGD-affected salmon displayed significantly elevated systemic vascular resistance at 4 and 6 h post surgery. Cardiac output was also approximately 35% lower in AGD-affected salmon compared to the non-affected control counterparts. These results comparatively examine cardiac function in response to AGD across three salmonid species and highlight species-specific cardiovascular responses that occur in association with disease. It is suggested that the apparent cardiac dysfunction seen in AGD-affected Atlantic salmon could, under stressful conditions, become exacerbated. Cardiac failure is therefore suggested to be a possible physiological mechanism by which AGD causes or contributes to mortality in Atlantic salmon.     

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.     

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.     

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.     

Energy metabolism of swimming trout (Salmo gairdneri)

Summary The oxidation of 1-¹⁴C palmitate, 2-¹⁴C glucose, 1-¹⁴C lactate, 1-¹⁴C alanine, 1-¹⁴C leucine and 1-¹⁴C glutamate, injected via a cannula into the dorsal aorta, was determined in trout, either at rest, or during swimming at 80% of the maximum sustained speed. The oxygen consumption and the excretion rates of¹⁴CO₂ as well as CO₂ were measured.While the oxygen consumption of swimming trout was about twice as high as of resting trout, the oxidation rates of the injected tracers increased by up to 9 time. Despite the increased importance of blood borne substrates, the estimated contribution to total CO₂ production is about 6% for the resting and 17% for the active trout. The majority of the oxidisable substrates must therefore be endogenous.The mobilization and oxidation rates of lactate, palmitate and leucine were particularly increased during swimming. During rest, palmitate and leucine oxidation rates are low. While oxidation rates of alanine and glutamate are intermediate, those of glucose were found to be extremely low, both at rest and during swimming. The measured RQ values for resting and swimming trout were 0.91 and 0.96 respectively, indicating that protein is the major fuel, since glucose oxidation seems of minor importance.Abbreviations and symbols SA specific activity - tt transit time - decay (time) constant - flux (in % of injected dose per hour) - U_crit critical velocity of sustained swimming - TCO₂ total CO₂     

Cardiorespiratory status of triploid brown trout during swimming at two acclimation temperatures

At 14° C, standard metabolic rate (75·1 mg O₂ h⁻¹ kg⁻¹), routine metabolic rate (108.8 mg O₂ h⁻¹ kg⁻¹), active metabolic rate ( c . 380 mg O₂ h⁻¹ kg⁻¹), critical swimming speed (U_crit 1·7 BL s⁻¹), heart rate 47 min⁻¹), dorsal aortic pressure (3·2 kPa) and ventilation frequency (63 min⁻¹) for triploid brown trout Salmo trutta were within the ranges reported for diploid brown trout and other salmonids at the same temperature. During prolonged swimming ( c . 80% U _crit), cardiac output increased by 2·3-fold due to increases in heart rate (1·8-fold) and stroke volume (1·2-fold). At 18° C, although standard and routine metabolic rates, as well as resting heart rate and ventilation frequency increased significantly, active metabolic rate and certain cardiorespiratory variables during exercise did not differ from those values for fish acclimated to 14° C. As a result, factorial metabolic scope was reduced (2·93-fold at 18° C v . 5·13-fold at 14° C). Therefore, it is concluded that cardiorespiratory performance in triploid brown trout was not unusual at 18° C, but that reduced factorial metabolic scope may be a contributing factor to the mortality observed in triploid brown trout at temperatures near 18° C.     

An automated ultrasonic telemetry system for the assessment of locomotor activity in free-ranging rainbow trout, Salmo gairdneri, Richardson

A new automated ultrasonic telemetry system for monitoring the swimming activity of adult rainbow trout, Salmo gairdneri , at liberty in the wild is described. The transmitter detects bioelectric potentials (i.e. electromyograms) associated with the contraction of the epaxial myomeres during swimming. Transmitter output is relayed to the signal processing system via submerged hydrophones. The incoming signals represent averaged electromyograms which have been shown in earlier studies to correlate well with swimming activity and concurrent oxygen consumption of rainbow trout in the laboratory.
Electromyogram records obtained from rainbow trout released into a small lake and monitored for up to 4 weeks, indicate a fairly regular pattern of elevated midday activity contrasting with periods of relative quiescence during the evening and morning. This midday peak in locomotory activity is the result of an increased feeding activity which is evidently a response to a concomitant increase in the activity of the fish's prey.     

Locomotion of Gymnarchus Niloticus： Experiment and Kinematics

In addition to forward undulatory swimming, Gymnarchus niloticus can swim via undulations of the dorsal fin while the body axis remains straight; furthermore, it swims forward and backward in a similar way, which indicates that the undulation of the dorsal fin can simultaneously provide bidirectional propulsive and maneuvering forces with the help of the tail fin. A high-resolution Charge-Coupled Device （CCD） imaging camera system is used to record kinematics of steady swimming as well as maneuvering in G. niloticus. Based on experimental data, this paper discusses the kinematics （cruising speed, wave speed, cycle frequency, amplitude, lateral displacement） of forward as well as backward swimming and maneuvering. During forward swimming, the propulsive force is generated mainly by undulations of the dorsal fin while the body axis remains straight. The kinematic parameters （wave speed, wavelength, cycle frequency, amplitude） have statistically significant correlations with cruising speed. In addition, the yaw at the head is minimal during steady swimming. From experimental data, the maximal lateral displacement of head is not more than 1% of the body length, while the maximal lateral displacement of the whole body is not more than 5% of the body length. Another important feature is that G. niloticus swims backwards using an undulatory mechanism that resembles the forward undulatory swimming mechanism. In backward swimming, the increase of lateral displacement of the head is comparatively significant; the amplitude profiles of the propulsive wave along the dorsal fin are significantly different from those in forward swimming. When G. niloticus does fast maneuvering, its body is first bent into either a C shape or an S shape, then it is rapidly unwound in a travelling wave fashion. It rarely maneuvers without the help of the tail fin and body bending.     

Adrenergic control of venous capacitance during moderate hypoxia in the rainbow trout (Oncorhynchus mykiss): role of neural and circulating catecholamines

Central venous blood pressure (P(ven)) increases in response to hypoxia in rainbow trout (Oncorhynchus mykiss), but details on the control mechanisms of the venous vasculature during hypoxia have not been studied in fish. Basic cardiovascular variables including P(ven), dorsal aortic blood pressure, cardiac output, and heart rate were monitored in vivo during normoxia and moderate hypoxia (P(W)O(2) = approximately 9 kPa), where P(W)O(2) is water oxygen partial pressure. Venous capacitance curves for normoxia and hypoxia were constructed at 80-100, 90-110, and 100-120% of total blood volume by transiently (8 s) occluding the ventral aorta and measure P(ven) during circulatory arrest to estimate the mean circulatory filling pressure (MCFP). This allowed for estimates of hypoxia-induced changes in unstressed blood volume (USBV) and venous compliance. MCFP increased due to a decreased USBV at all blood volumes during hypoxia. These venous responses were blocked by alpha-adrenoceptor blockade with prazosin (1 mg/kg body mass). MCFP still increased during hypoxia after pretreatment with the adrenergic nerve-blocking agent bretylium (10 mg/kg body mass), but the decrease in USBV only persisted at 80-100% blood volume, whereas vascular capacitance decreased significantly at 90-110% blood volume. In all treatments, hypoxia typically reduced heart rate while cardiac output was maintained through a compensatory increase in stroke volume. Despite the markedly reduced response in venous capacitance after adrenergic blockade, P(ven) always increased in response to hypoxia. This study reveals that venous capacitance in rainbow trout is actively modulated in response to hypoxia by an alpha-adrenergic mechanism with both humoral and neural components.     

Dynamic synchronization analysis of venous pressure-driven cardiac output in rainbow trout

Measurement of venous function in vivo is inherently difficult. In this study, we used the Hilbert transform to examine the dynamic relationships between venous pressure and cardiac output (CO) in rainbow trout whose blood volume was continuously increased and decreased by ramp infusion and withdrawal (I/W). The dorsal aorta and ductus Cuvier were cannulated percutaneously and connected to pressure transducers; a flow probe was placed around the ventral aorta. Whole blood from a donor was then I/W via the dorsal aortic cannula at a rate of 10% of the estimated blood volume per minute, and the duration of I/W was varied from 40, 60, 80, 90, 120, 230, 240, 260, 300, and 340 s. Compliance [change in (delta) blood vol/deltavenous pressure] was 2.8 +/- 0.2 ml x mmHg-1x g-1 (N = 25 measurements; 6 fish with closed pericardium) and 2.8 +/- 0.3 ml. mmHg-1x kg-1 (N = 19 measurements, 4 fish with open pericardium). Compliance was positively correlated with the duration of I/W, indicative of cardiovascular reflex responses at longer I/W durations. In trout with closed pericardium, CO followed venous pressure oscillations with an average time lag of 4.2 +/- 1.0 s (N = 9); heart rate (HR) was inversely correlated with CO. These studies show that CO is entrained by modulation of venous pressure, not by HR. Thus, although trout have a rigid pericardium, venous pressure (vis-a-tergo), not cardiac suction (vis-a-fronte), appears to be the primary determinant of CO. Estimation of venous compliance by ramp-modulation of venous pressure is faster and less traumatic than classical capacitance measurements and appears applicable to a variety of vertebrate species, as does the Hilbert transform, which permits analysis of signals with disparate frequencies.     

Ventilatory Responses of Teleost Fish to Exercise and Thermal Stress

Exercise and thermal stress both markedly raise the oxygen demandof fish. The control of ventilation under these two conditionsis apparently quite different and contrasts between speciesare noteworthy. Under both exercise and thermal stress, changes in respiratorypumping amplitude tend to be greater than changes in ventilatoryfrequency in most species. Respiratory pump uncoupling duringthermal stress is frequently seen in trout but much less soin bullhead catfish or bluegills. In fish that actively ventilate the gills while swimming, thecontrol for this probably depends on swimming muscle reflexesrather than blood humoral factors. This control mechanism mayoperate in a reverse fashion in fish that use ram-jet ventilation.During recovery from severe exercise and during thermal stressthe control of gill ventilation is apparently humoral. Of thepossible factors, blood oxygen and possibly also pH are consideredto be the most important. Evidence is summarized that suggeststhe error detector is on the arterial side of the gas exchanger.     

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.     

In-vitro investigation of a potential wave pumping effect in human aorta

An impedance pump – also known as Liebau pump – is a simple valveless pump that operates based on the principles of wave propagation and reflection. It has been shown in embryonic zebrafish that a similar mechanism is responsible for the pumping action in the embryonic heart during the early stages before valve formation. Recent studies suggest that the cardiovascular system is designed to take advantage of wave propagation and reflection phenomena in the arterial network. In this study we report the results of an in-vitro study that examines the hypothesis that the adult human aorta acts as a passive pump based on Liebau effect. A hydraulic model with different compliant models of an artificial aorta was used for a series of in-vitro experiments. Our result indicates that wave propagation and reflection can result in a pumping mechanism in a compliant aorta.     

The use of telemetry to study light synchronization with feeding and gill ventilation rates in Salmo trutta

A technique is described whereby the electromyogram of the m. adductor mandibulae of brown trout is detected by implanted extracellular electrodes and used as the input signal for an ultrasonic transmitter attached externally to the fish. The periodic electrical activity of the muscle during ventilation is relayed by the transmitter using an analogue pulse system.
As the ventilatory electromyogram occurs in discrete rhythmic trains, it follows that alterations to this rhythm can be used to telemeter, instantaneously, single feeding events from a free swimming fish. Laboratory tests have shown that the feeding act is unequivocally distinct electromyographically from other manoeuvres such as 'coughing'.
Four adult brown trout have been equipped with this transmitter system and released in Airthrey Loch, Stirling. Using a tracking facility, feeding activity and ventilatory rhythms have been recorded for extended periods.
The results indicate the presence of three daily peaks of feeding activity, which is discussed in relation to changes in light levels. The telemetry records indicate that night feeding is a common occurrence in brown trout. In addition, ventilatory rates were found to be at or near resting levels.     

Field metabolic rates of rainbow trout estimated using electromyogram telemetry

Field metabolic rates (FMR) of five rainbow trout were estimated using electromyogram (EMG) telemetry of the axial muscle. A series of laboratory experiments indicated that the EMG transmitter output was related strongly to total oxygen consumption of the fish over a wide range of swimming speeds and temperatures. No differences were evident when the oxygen consumption v . EMG relationship for routine swimming was compared with that for forced swimming. FMR was assessed on two time scales, revealing diel patterns and seasonal patterns. On the diel scale, the FMR pattern could be classified as crepuscular. At the upper and lower limits of temperature tolerance, the diel pattern was less distinct. On the seasonal scale, mean daily FMR was strongly dependent on mean environmental temperature. Comparisons between FMR and laboratory derived estimates of standard and maximally active metabolism indicate that the rainbow trout in the field utilize <20% of the available scope for activity.     

Experiments on the central pattern generator for swimming in amphibian embryos

The central nervous system of paralysed Xenopus laevis embryos can generate a motor output pattern suitable for swimming locomotion. By recording motor root activity in paralysed embryos with transected nervous systems we have shown that: (a) the spinal cord is capable of swimming pattern generation; (b) swimming pattern generator capability in the hindbrain and spinal cord is distributed; (c) caudal hindbrain is necessary for sustained swimming output after discrete stimulation. By recording similarly from embryos whose central nervous system was divided longitudinally into left and right sides, we have shown that: (a) each side can generate rhythmic motor output with cycle periods like those in swimming; (b) during this activity cycle period increases within an episode, and there is the usual rostrocaudal delay found in swimming; (c) this activity is influenced by sensory stimuli in the same way as swimming activity; (d) normal phase coupling of the left and right sides can be established by the ventral commissure in the spinal cord. We conclude that interactions between the antagonistic (left and right) motor systems are not necessary for swimming rhythm generation and present a model for swimming pattern generation where autonomous rhythm generators on each side of the nervous system drive the motoneurons. Alternation is achieved by reciprocal inhibition, and activity is initiated and maintained by tonic excitation from the hindbrain.     

A technique for repeated sampling of the blood of individual resting fish.

A dorsal cannulation technique is described. It has been employed for repeated blood sampling in unanaesthetized rainbow trout (Salmo gairdneri) kept singly in special receptacles described in the paper. The level of the studied haematological parameters (Haematocrit, Hb, glucose, lactate, K+, Na+, Ca2+) differed between fish kept in receptacles for 1 week and free-swimming fish, most probably owing to differences in the motility of the fish. The receptacle seems to minimize visual and handling disturbances, and permits both the standardization of experimental conditions and quick and easy sampling via the dorsal aorta cannula. The general variation in the blood parameter values was very small compared with the previously reported variation in such values for rainbow trout.     

Notochordal and elastic components of the axial skeleton of fishes and their functions in locomotion

Structural details of the notochord and elastic longitudinal ligaments (dorsal and ventral) of fish are presented with discussions on their possible contribution to the speed, power and modes of swimming by conferring an automatic spring-like resilience to the vertebral axis as a whole. The notochord is also believed to function as a series of ring-like hinges placed intervertebrally which dictates that the centra must be biconcave (amphicoelous) to support and house them. Examination of about 100 species shows that, whilst the dorsal ligament is always present, the ventral is found in primitive teleosts only. The phylogenetic significance of this in relation to the different efferent branchial systems will be submitted (with diagrammatic recording of dissections) for publication in the near future. The dorsal and ventral ligaments are suitably situated to assist the circulation of lymph and blood respectively in the small lateral vessels associated with the main longitudinal one of the appropriate system. Experimental work is required to test the hypotheses presented.     

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.     

Migration speeds and orientation of Atlantic salmon and sea trout post-smolts in a Norwegian fjord system

We recorded the observed and actual swimming speeds of Atlantic salmon and sea trout post-smolts in a Norwegian fjord system, and initiated studies on the orientation mechanisms of the post-smolts. We tracked Atlantic salmon and sea trout with acoustic transmitters for up to 14 h after release. The actual swimming speed and direction of a fish relative to the ground is the vector sum of the observed movements of the fish and the movements of the water. We determined actual swimming speeds and directions of the post-smolts, which reflect their real swimming capacities and orientation, by corrections for the speed and direction of the water current. The post-smolts were actively swimming. The observed direction of movement was dependent on the actual movement of the fish and not the water current. Water currents were not systematically used as an orientation cue either in Atlantic salmon or sea trout, as the actual movements were random compared to the direction of the water current. The actual movement of sea trout were in all compass directions, with no systematic pattern. The Atlantic salmon also moved in all compass directions, but with the lowest frequency of actual movement towards the fjord.