Physiological mechanisms of imprinting and homing migration in Pacific salmon Oncorhynchus spp

After several years of feeding at sea, salmonids have an amazing ability to migrate long distances from the open ocean to their natal stream to spawn. Three different research approaches from behavioural to molecular biological studies have been used to elucidate the physiological mechanisms underpinning salmonid imprinting and homing migration. The study was based on four anadromous Pacific salmon Oncorhynchus spp., pink salmon Oncorhynchus gorbuscha, chum salmon Oncorhynchus keta, sockeye salmon Oncorhynchus nerka and masu salmon Oncorhynchus masou, migrating from the North Pacific Ocean to the coast of Hokkaido, Japan, as well as lacustrine O. nerka and O. masou in Lake Toya, Hokkaido, where the lake serves as the model oceanic system. Behavioural studies using biotelemetry techniques showed swimming profiles from the Bering Sea to the coast of Hokkaido in O. keta as well as homing behaviours of lacustrine O. nerka and O. masou in Lake Toya. Endocrinological studies on hormone profiles in the brain-pituitary-gonad axis of O. keta, and lacustrine O. nerka identified the hormonal changes during homing migration. Neurophysiological studies revealed crucial roles of olfactory functions on imprinting and homing during downstream and upstream migration, respectively. These findings are discussed in relation to the physiological mechanisms of imprinting and homing migration in anadromous and lacustrine salmonids.     

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Microalgae have been shown as a potential bioresource for food, biofuel, and pharmaceutical products. During the growth phases with corresponding environmental conditions, microalgae accumulate different amounts of various metabolites. We quantified the neutral lipids accumulation and analyzed the swimming signatures (speed and trajectories) of the motile green alga, Dunaliella primolecta, during the lag–exponential–stationary growth cycle at different nutrient concentrations. We discovered significant changes in the neutral lipid content and swimming signatures of microalgae across growth phases. The timing of the maximum swimming speed coincided with the maximum neutral lipid content and both maxima occurred under nutrient stress at the stationary growth phase. Furthermore, the swimming trajectories suggested statistically significant changes in swimming modes at the stationary growth phase when the maximum intracellular neutral lipid content was observed. Our results provide the potential exploitation of microalgal swimming signatures as possible indicators of the cultivation conditions and the timing of microalgal harvest to maximize the lipid yield for biofuel production. The findings can also be implemented to explore the production of food and antibiotics from other microalgal metabolites with low energy costs.     

Application of single nucleotide polymorphism markers to chum salmon Oncorhynchus keta: discovery, genotyping and linkage phase resolution

This study describes (1) the application of new methods to the discovery of informative single nucleotide polymorphism (SNP) markers in chum salmon Oncorhynchus keta, (2) a method to resolve the linkage phase of closely linked SNPs and (3) a method to inexpensively genotype them. Finally, it demonstrates that these SNPs provide information that discriminates among O. keta populations from different geographical regions of the northern Pacific Ocean. These informative markers can be used in conjunction with mixed-stock analysis to learn about the spatial and temporal marine distributions of O. keta and the factors that influence the distributions.     

Retinoid composition and retinal localization in the eggs of teleost fishes

Retinoids in the eggs of four teleosts, chum salmon (Oncorhynchus keta), black porgy (Acanthopagrus schlegeli), marbled flounder (Pleuronectes yokohamae), and stingfish (Inimicus japonicus), were analyzed by high performance liquid chromatography. Retinal (RAL1) or both RAL1 and 3,4-didehydroretinal (RAL2) were major or exclusive retinoids in the eggs of every species examined. In O. keta eggs, both RAL1 and RAL2 were present at the ratio of approximately 3:4, whereas RAL1 was the only retinal in the eggs of the other three marine species. RAL1 was the exclusive retinoid in the eggs of P. yokohamae and I. japonicus, whose eggs lack lipid bodies. In the eggs of O. keta and A. schlegeli, which have lipid bodies, retinylesters were also detected, and retinals composed 69% and 93%, respectively, of total retinoids. In O. keta eggs, retinals were present mostly in the aqueous part and were bound to a protein homologous to lipovitellin 1, an amphibian yolk protein, and retinylesters were located in lipids. These results indicate that retinals are the essential mode of retinoid storage in eggs of teleosts and they are the precursors of functional retinoids, such as retinoic acid and visual pigment chromophores. Retinylesters are additional retinoids that accompany lipid accumulation.     

大麻哈鱼卵黄囊期仔鱼异速生长及其生态学意义

运用实验生态学的方法, 对大麻哈鱼(Oncorhynchus keta Walbaum)卵黄囊期仔鱼的异速生长及器官优先发育在早期生存和环境适应上的生态学意义进行了研究。结果表明, 大麻哈鱼卵黄囊期仔鱼的感觉、摄食, 呼吸和游泳等器官快速分化, 许多关键器官均存在异速生长现象。在身体各部分中, 头部和尾部为正异速生长, 躯干部为负异速生长, 体高有先增大后减小的趋势; 在头部器官中, 眼径、口宽、吻长和眼后头长均为正异速生长; 在游泳器官中, 胸鳍、腹鳍、背鳍、臀鳍、背鳍基、臀鳍基和尾鳍均为正异速生长, 脂鳍为负异速生长, 其中, 腹鳍在全长25.31 mm、12日龄出现生长拐点, 但拐点前后均为正异速生长。大麻哈鱼卵黄囊期仔鱼感觉、摄食, 呼吸和游泳等器官的快速发育, 使出膜后的仔鱼在最短的时间内获得了与早期生存密切相关的各种能力, 对适应复杂多变的外界环境具有重要的生态学意义。       

The effects of external ultrasonic tagging on the swimming performance of rainbow trout, Salmo gairdneri Richardson

The effects of externally mounted ultrasonic tags on the tail beat frequency (TBF) and opercular beat rate (OBR) of rainbow trout was measured at different swimming speeds. The increase in relative drag caused by the tags was also measured. Two tag types were used: one where both the circuitry and the battery were in a single package mounted on one side of the fish, the other where they were in two packages mounted symmetrically on either side of the fish. Both tag types raised both TBF and OBR. Of the two, the symmetrical tag effects behaviour less, especially at low swimming speeds, even though it causes a greater increase in relative drag.     

Anisakis simplex (s.s.) larvae in wild Alaska salmon: no indication of post-mortem migration from viscera into flesh

The prevalence, mean intensity and distribution of Anisakis nematode third-stage larvae (L3) in the muscle and viscera of wild-caught chum salmon Oncorhynchus keta, pink salmon O. gorbuscha and sockeye salmon O. nerka were compared immediately after catch. Salmon were collected during the fishing season in July 2007 in Bristol Bay and Prince William Sound close to Cordova, Alaska (USA). All fish were infected, and more than 90% of the nematode larvae were found in the edible muscle meat. The isolated anisakid L3 were genetically identified as A. simplex (s.s.). The distribution of nematodes in the muscle meat of fresh-caught salmon was examined in 49 O. keta, 50 O. nerka and 12 O. gorbuscha from Cordova. Most of the larvae were detected in the muscle parts around the body cavity, but nematodes were also found in the tail meat and epaxial muscle (loins). The mean intensity of Anisakis larvae in the edible part was 21 individuals for O. gorbuscha, 62 individuals for O. keta and 63 individuals for O. nerka. No difference in the intensity of Anisakis larvae in the hypaxial muscle was found between fresh-caught and immediately gutted salmon and individuals stored ungutted for 24 h either on ice or in refrigerated sea water.     

Feeding Behavior in the Ciliate Pseudomicrothorax dubius is a Series of Morphologically and Physiologically Distinct Events1

Based upon light and electron microscopical observations, the feeding behavior of the ciliate Pseudomicrothorax dubius, when fed the cyanobacterium Oscilatoria formosa, is resolved into two principal phases, contact swimming and phagocytosis, the latter being separable into two steps, attachment aad ingestion. Following collision with an O. formosa filament. cells swim along the filament with their ventral cilia in contact with it during the contact swimming phase. Phagocytosis commences with the attachment of the cytostome to the filament, which initiates lysosomal streaming in the cytostomal-cytopharyngeal region. The filament then enters the cytopharynx concomitant with food vacuole formation during the ingestion step. Treatment of cells with trypsin or modification of the extracellular ionic medium inhibits the attachment step of phagocytosis but does not affect contact swimming. Behavior of cells when fed different cyanobacterial species as well as artificial food substrates is also examined. Contact swimming is a form of contact guidance since the shape of the food substrate determines the direction of cell movement. Additionally, a chemical factor may be present in or on the cyanobacteria and play a role in contact swimming. Evidence is presented that suggests that during the attachment step, two phenomena are involved: direct adhesion between cell surfaces and adhesion due to material liberated by exocytosis.     

The Effect of Drag and Attachment Site of External Tags on Swimming Eels: Experimental Quantification and Evaluation Tool

Telemetry studies on aquatic animals often use external tags to monitor migration patterns and help to inform conservation effort. However, external tags are known to impair swimming energetics dramatically in a variety of species, including the endangered European eel. Due to their high swimming efficiency, anguilliform swimmers are very susceptibility for added drag. Using an integration of swimming physiology, behaviour and kinematics, we investigated the effect of additional drag and site of externally attached tags on swimming mode and costs. The results show a significant effect of a) attachment site and b) drag on multiple energetic parameters, such as Cost Of Transport (COT), critical swimming speed (U_crit) and optimal swimming speed (U_opt), possibly due to changes in swimming kinematics. Attachment at 0.125 bl from the tip of the snout is a better choice than at the Centre Of Mass (0.35 bl), as it is the case in current telemetry studies. Quantification of added drag effect on COT and U_crit show a (limited) correlation, suggesting that the U_crit test can be used for evaluating external tags for telemetry studies until a certain threshold value. U_opt is not affected by added drag, validating previous findings of telemetry studies. The integrative methodology and the evaluation tool presented here can be used for the design of new studies using external telemetry tags, and the (re-) evaluation of relevant studies on anguilliform swimmers.     

Relation of NADH/NAD to contraction in vascular smooth muscle

The relationship of NADH/NAD to O2 consumption with respect to the different phases of contraction in vascular smooth muscle in response to a maximal depolarizing concentration of KCl was investigated. The NADH bound to cellular proteins could be distinguished from free NADH in whole tissue homogenates. Evidence suggested that the NADH was bound to pyruvate dehydrogenase and perhaps to other dehydrogenases since binding paralleled the changes in the activity of pyruvate dehydrogenase with contraction. The measured changes in NADH were attributed to that within the mitochondrial compartment since the contribution of reducing equivalents within the cytoplasmic compartment was negligible. During the phase of contraction in which force was initially being generated and at which O2 consumption was the highest, there was a net increase in NADH/NAD. After stable isometric force was maintained, at which time O2 consumption had returned to slightly above the basal pre-contraction level, there was a net decrease in NADH/NAD. Previous evidence indicates the phosphorylation potential (ATP/ADP) may decrease during this phase of contraction. It is concluded that contraction of vascular smooth muscle is accompanied by a changing pool of reducing equivalents. Factors which govern O2 consumption may change during the different phases of muscle contraction.     

Analysis of growth phase regulated KatA and CatE and their physiological roles in determining hydrogen peroxide resistance in Agrobacterium tumefaciens

Agrobacterium tumefaciens possesses two catalases, a bifunctional catalase-peroxidase, KatA and a homologue of a growth phase regulated monofunctional catalase, CatE. In stationary phase cultures and in cultures entering stationary phase, total catalase activity increased 2-fold while peroxidase activity declined. katA and catE were found to be independently regulated in a growth phase dependent manner. KatA levels were highest during exponential phase and declined as cells entered stationary phase, while CatE was detectable at early exponential phase and increased during stationary phase. Only small increases in H2O2 resistance levels were detected as cells entering stationary phase. The katA mutant was more sensitive to H2O2 than the parental strain during both exponential and stationary phase. Inactivation of catE alone did not significantly change the level of H2O2 resistance. However, the katA catE double mutant was more sensitive to H2O2 during both exponential and stationary phase than either of the single catalase mutants. The data indicated that KatA plays the primary role and CatE acts synergistically in protecting A. tumefaciens from H2O2 toxicity during all phases of growth. Catalase-peroxidase activity (KatA) was required for full H2O2 resistance. The expression patterns of the two catalases in A. tumefaciens reflect their physiological roles in the protection against H2O2 toxicity, which are different from other bacteria.     

Pop up satellite tags impair swimming performance and energetics of the European eel (Anguilla anguilla)

Pop-up satellite archival tags (PSATs) have recently been applied in attempts to follow the oceanic spawning migration of the European eel. PSATs are quite large, and in all likelihood their hydraulic drag constitutes an additional cost during swimming, which remains to be quantified, as does the potential implication for successful migration. Silver eels (L_T = 598.6±29 mm SD, N = 9) were subjected to swimming trials in a Steffensen-type swim tunnel at increasing speeds of 0.3–0.9 body lengths s⁻¹, first without and subsequently with, a scaled down PSAT dummy attached. The tag significantly increased oxygen consumption (MO₂) during swimming and elevated minimum cost of transport (COT_min) by 26%. Standard (SMR) and active metabolic rate (AMR) as well as metabolic scope remained unaffected, suggesting that the observed effects were caused by increased drag. Optimal swimming speed (U _opt) was unchanged, whereas critical swimming speed (U _crit) decreased significantly. Swimming with a PSAT altered swimming kinematics as verified by significant changes to tail beat frequency (f), body wave speed (v) and Strouhal number (St). The results demonstrate that energy expenditure, swimming performance and efficiency all are significantly affected in migrating eels with external tags.     

Phase-dependence of elbow muscle coactivation in front crawl swimming

Propulsion in swimming is achieved by complex sculling movements with elbow quasi-fixed on the antero-posterior axis to transmit forces from the hand and the forearm to the body. The purpose of this study was to investigate how elbow muscle coactivation was influenced by the front crawl stroke phases. Ten international level male swimmers performed a 200-m front crawl race-pace bout. Sagittal views were digitized frame by frame to determine the stroke phases (aquatic elbow flexion and extension, aerial elbow flexion and extension). Surface electromyograms (EMG) of the right biceps brachii and triceps brachii were recorded and processed using the integrated EMG to calculate a coactivation index (CI) for each phase. A significant effect of the phases on the CI was revealed with highest levels of coactivation during the aquatic elbow flexion and the aerial elbow extension. Swimmers stabilize the elbow joint to overcome drag during the aquatic phase, and act as a brake at the end of the recovery to replace the arm for the next stroke. The CI can provide insight into the magnitude of mechanical constraints supported by a given joint, in particular during a complex movement.     

Schwimmverhalten und Schwimmgeschwindigkeit bei den Larven des HeringsClupea harengus

The present study is based on two year experiments; it analyses swimming behaviour and swimming speed at different developmental stages of the herring. Yolk sac larvae tend to sink rather rapidly during resting phases. At the end of the yolk sac stage the sinking rate is at its minimum; it increases again with increasing larva size. During the phase of yolk sac resorption, vertical movements become gradually transformed into horizontal ones. Generally, three types of swimming can be distinguished: (1) “Abrupt swimming” consisting of very short periods of fast swimming; normally each dart is connected with a change in swimming direction. (2) “Normal swimming” characterized by steady movements for several seconds; it results in a winding path. (3) “Slow meandering” representing search swimming, a slowly winding locomotion with a large amplitude of each winding but with very little net progression of the larva. Swimming speed varies considerably in all size groups. The 8 to 11 mm (total length) larvae reach a mean swimming velocity (undulation) of 1.0 to 1.2 cm per second. Swimming speed, measured as the straight line distance between start and end points of a single swimming phase, attains mean values of 7 to 8 mm/sec in 8 to 11 mm larvae, 10 to 11 mm/sec in 11 to 15 mm larvae, 21 to 25 mm/sec in 19 to 24 mm larvae, and 40 to 50 mm/sec in 32 to 40 mm larvae. Swimming activity changes during larval development and seems to be influenced by food supply. The total distance travelled in 5 minutes by the head of a yolk sac larva is 1 to 3 m. About 8 days after hatching, sinking rate is low and “search swimming” (slow meandering movements) prevails. The path covered by the head within 5 minutes is 0.8 to 1.5 m.     

Oral contraceptive cycle phase does not affect 200-m swim time trial performance

The purpose of this study was to examine whether swimming performance was affected by acute hormonal fluctuation within a monophasic oral contraceptive (OC) cycle. Six competitive swimmers and water polo players completed a 200-m time trial at 3 time points of a single OC cycle: during the consumption phase (CONS), early (WITH1), and late in the withdrawal phase (WITH2). Split times and stroke rate were recorded during the time trial, and heart rate, blood lactate, glucose, and pH were measured after each performance test. Resting endogenous serum estradiol and progesterone concentrations were also assessed. No significant differences were observed between phases for body composition, 200-m swim time, mean stroke rate, peak heart rate, or blood glucose (p > 0.05). The mean peak blood lactate was significantly lower during WITH2 (9.9 ± 3.0 mmol·L(-1)) compared with that of CONS (12.5 ± 3.0 mmol·L(-1)) and mean pH higher during WITH2 (7.183 ± 0.111) compared with that of CONS (7.144 ± 0.092). Serum estradiol levels were significantly greater during WITH2 compared with that during WITH1 and CONS, but there was no difference in serum progesterone levels. These results demonstrate that for monophasic OC users, cycle phase does not impact the 200-m swimming performance. There was a reduction in blood lactate and an increase in pH during the withdrawal phase, possibly because of an increase in fluid retention, plasma volume, and cellular alkalosis. Therefore, female 200-m swimmers taking a monophasic OC need not be concerned by the phase of their cycle with regard to competition and optimizing performance. However, coaches and scientists should exercise caution when interpreting blood lactate results obtained from swimming tests and consider controlling for cycle phase for athletes taking an OC.     

Mechanics of branchial ventilation in the valviferan isopod Idotea wosnesenskii (Crustacea)

Idotea wosnesenskii Brandt, a valviferan isopod, has five pairs of pleopods within a branchial chamber enclosed by modified uropods (operculae). The pumping mechanism of resting isopods was videotaped to observe ventilation, and particularly to determine whether or not the swimming pleopods (first three pairs) and the gas exchange pleopods (last two pairs) have ventilatory roles. Observations on intact animals (to observe water flow into and out of the branchial chamber) and on animals with operculae propped open or with parts of their abdominal wall removed (to study the actual pumping movements of the pleopods) revealed that all five pairs of pleopods function in ventilation. The ventilatory stroke has two phases: an opening phase in which the pleopods move medially and ventrally, opening spaces between pleopods (analogous to the swimming recovery stroke), and a closing phase, wherein the pleopods move laterally and dorsally, reducing the gaps between succeeding pleopods (analogous to the swimming power stroke). Ventilatory strokes may be continuous or they may be separated by resting phases. Both the frequency and amplitude are variable: the frequency changes greatly due to the wide variation in resting phase duration. By opening the operculae the amplitude can increase so that ventilatory strokes grade into swimming strokes. The ventilatory stroke pattern at rest is generally similar to the swimming stroke pattern but differs in its slower and nearly simultaneous dorsoventral movements and its lower frequencies. Dye and particle movements around intact animals and those with exposed pleopods show that water typically takes about three strokes to pass through the branchial chamber.     

Diel activity pattern and food search behaviour in cod, Gadus morhua

Food search behaviour in cod, Gadus morhua, was studied by means of a stationary positioning system. Six fish in a fjord in northern Norway were tagged in situ by allowing them to shallow bait-wrapped acoustic tags, and their swimming behaviour was continuously recorded. The fish exhibited a diel activity rhythm, with higher swimming speeds and a larger range during the day than at night. Chemically mediated food search was studied in periods of both high and low activity by setting a string of baits in the morning and at night. During the period of high activity, more fish localized the baits (70 versus 45% of the observations) and the time to localization was 50% shorter, indicating that high swimming activity increased the probability of encountering the odour plume and the odour source. No diel variations in the response threshold to olfactory stimuli were found, as the proportion of fish in the odour plume that responded rheotactically, and their response distances were similar in the two periods (240 and 227 m respectively). Cod performed area-restricted searches on encountering the string of baits during the day. The probability of cod detecting prey by taste receptors, encountering the odour plume of prey or localizing a stationary food source after olfactory stimulation should be relatively independent of light, and this could explain why cod were active throughout the 24 h cycle. On the other hand, the visual detection distance and the ability to capture active prey are influenced by the light level, resulting in higher activity during the day.     

Sensory modification of leech swimming: interactions between ventral stretch receptors and swim-related neurons

The neuronal circuits that generate the leech swimming rhythm comprise oscillatory interneurons that provide appropriately phased output to drive swim-related motoneurons. Within ganglia, these interneurons express three phases; between ganglia there exists a phase delay between homologs. Our earlier experiments revealed that stretch receptors embedded in the body wall participate in intersegmental coordination and setting intersegmental phases. To identify the basis for these sensory effects, we mapped interactions between a ventral stretch receptor and swim-related neurons. Connections between this receptor and motoneurons are weak and variable in quiescent preparations, but during fictive swimming stretch receptor activation modulates motoneuron oscillations, hence, these effects are polysynaptic, mediated by interneurons. We identified a strong, nonrectifying, and apparently direct electrical connection between the stretch receptor and oscillator neuron 33. The ventral stretch receptor also interacts with most of the other oscillatory interneurons, including inhibitory inputs to cells 28 and 208, excitatory input to the contralateral cell 115, and mixed input to the ipsilateral cell 115. These direct and indirect interactions can account for previously described effects of body-wall stretch on motoneuron activity. They also could mediate the previously described modification of intersegmental phase relationships by appropriately phased stretch receptor activation.     

Factors affecting the circatidal rhythm in vertical swimming of ovigerous blue crabs, Callinectes sapidus, involved in the spawning migration

Ovigerous blue crabs, Callinectes sapidus, are observed to undergo nocturnal ebb-tide transport (ETT) during their seaward spawning migration. A previous study found that females undergoing the spawning migration have a circatidal rhythm in vertical swimming, which serves as the biological basis for ETT. The present study asked three questions about this endogenous rhythm. First, does the rhythm occur in females with mature embryos regardless of whether they are undergoing ETT? Second, when exposed to a light/dark cycle in the laboratory, do ovigerous females only swim vertically at the time of ebb tide during the dark phase? Third, do attachments to the backs of ovigerous crabs affect the circatidal rhythm? The circatidal rhythm occurred in all crabs with mid-stage embryos that were prevented from undergoing ETT. The rhythm was unaffected by the light/dark cycle, which implies that migration can occur at lower light levels at depth during the day. Finally, attachments did not affect the rhythm, which suggests that tags and transmitters will not affect the spawning migration.     

Exercise VE and physical performance at altitude are not affected by menstrual cycle phase.

We hypothesized that progesterone-mediated ventilatory stimulation during the midluteal phase of the menstrual cycle would increase exercise minute ventilation (VE; l/min) at sea level (SL) and with acute altitude (AA) exposure but would only increase arterial O2 saturation (SaO2, %) with AA exposure. We further hypothesized that an increased exercise SaO2 with AA exposure would enhance O2 transport and improve both peak O2 uptake (VO2 peak; ml x kg-1 x min-1) and submaximal exercise time to exhaustion (Exh; min) in the midluteal phase. Eight female lowlanders [33 +/- 3 (mean +/- SD) yr, 58 +/- 6 kg] completed a VO2 peak and Exh test at 70% of their altitude-specific VO2 peak at SL and with AA exposure to 4,300 m in a hypobaric chamber (446 mmHg) in their early follicular and midluteal phases. Progesterone levels increased (P < 0.05) approximately 20-fold from the early follicular to midluteal phase at SL and AA. Peak VE (101 +/- 17) and submaximal VE (55 +/- 9) were not affected by cycle phase or altitude. Submaximal SaO2 did not differ between cycle phases at SL, but it was 3% higher during the midluteal phase with AA exposure. Neither VO2 peak nor Exh time was affected by cycle phase at SL or AA. We conclude that, despite significantly increased progesterone levels in the midluteal phase, exercise VE is not increased at SL or AA. Moreover, neither maximal nor submaximal exercise performance is affected by menstrual cycle phase at SL or AA.