Lacustrine sockeye salmon return straight to their natal area from open water using both visual and olfactory cues

Mechanisms of the amazing ability of salmon to migrate a long distance from open water to natal streams for spawning are still unknown. Lacustrine sockeye salmon (Oncorhynchus nerka) in Lake Toya offers an excellent model system for studying the orientation mechanism in open water, because mature fish return to the natal area with a high degree of accuracy. First we examined the percentage of fish returning to the natal area after they were released 7 km south of the natal area. Forty percent of control male mature fish and 25% of the fish blinded by injection of a mixture of carbon toner and corn oil into the eyeball were captured in the natal area within 5 days. Forty-four percent of fish with brass rings (control) and 31% of fish with NdFe magnetic rings which interfere with the magnetic cue were captured in the natal area within 3 days. These experiments suggested that, although the number of blinded fish captured in the natal area was less than that of the controls, the difference was not statistically significant. In the fish captured in the natal area within 3 or 5 days, fish which found the natal area using their olfactory cue after random swimming for a long time and returned to that area may be included. Hence we tracked fish telemetrically using an ultrasonic tracking system, and found that mature males released at a long distance (3.6 or 6.8 km) from the natal area swam straight to the vicinity of the natal area. Interference of the magnetic cue by the attachment of a magnetic ring did not affect their direct return. Blockage of the visual cue caused them to move randomly. These data suggest that lacustrine sockeye salmon return straight to the vicinity of the natal area using their visual cue and finally reach the exact homing point using their olfactory cue.      

Olfactory responses to natal stream water in sockeye salmon by BOLD fMRI

Many studies have shown that juvenile salmon imprint olfactory memory of natal stream odors during downstream migration, and adults recall this stream-specific odor information to discriminate their natal stream during upstream migration for spawning. The odor information processing of the natal stream in the salmon brain, however, has not been clarified. We applied blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging to investigate the odor information processing of the natal stream in the olfactory bulb and telencephalon of lacustrine sockeye salmon (Oncorhynchus nerka). The strong responses to the natal stream water were mainly observed in the lateral area of dorsal telencephalon (Dl), which are homologous to the medial pallium (hippocampus) in terrestrial vertebrates. Although the concentration of L-serine (1 mM) in the control water was 20,000-times higher than that of total amino acid in the natal stream water (47.5 nM), the BOLD signals resulting from the natal stream water were stronger than those by L-serine in the Dl. We concluded that sockeye salmon could process the odor information of the natal stream by integrating information in the Dl area of the telencephalon.     

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.     

Estimation of nitrogen stable isotope turnover rate of Oncorhynchus nerka

Estimation of the isotopic turnover rate in the tissues of organisms allows us to estimate the temporal relationship between the isotope ratio of an organism and its prey, and to analyze seasonal variations of food webs and migratory patterns of animals. We analyzed the isotopic turnover rate in the tissue of lacustrine sockeye salmon, Oncorhynchus nerka, of three age classes in a laboratory food alteration experiment to clarify the isotopic turnover rate. The contribution of growth to isotopic turnover was higher in young and fast-growing lacustrine sockeye salmon than in older and slow-growing fish. Maturation masks the relationship between the contributions of growth and metabolism to isotopic change. Our estimate of the isotopic time lag of lacustrine sockeye salmon can be used to research trophic relationships of anadromous sockeye salmon.     

Effects of river temperature and climate warming on stock‐specific survival of adult migrating Fraser River sockeye salmon (Oncorhynchus nerka)

Mean summer water temperatures in the Fraser River (British Columbia, Canada) have increased by ～1.5 °C since the 1950s. In recent years, record high river temperatures during spawning migrations of Fraser River sockeye salmon (Oncorhynchus nerka) have been associated with high mortality events, raising concerns about long‐term viability of the numerous natal stocks faced with climate warming. In this study, the effect of freshwater thermal experience on spawning migration survival was estimated by fitting capture–recapture models to telemetry data collected for 1474 adults (captured in either the ocean or river between 2002 and 2007) from four Fraser River sockeye salmon stock‐aggregates (Chilko, Quesnel, Stellako‐Late Stuart and Adams). Survival of Adams sockeye salmon was the most impacted by warm temperatures encountered in the lower river, followed by that of Stellako‐Late Stuart and Quesnel. In contrast, survival of Chilko fish was insensitive to the encountered river temperature. In all stocks, in‐river survival of ocean‐captured sockeye salmon was higher than that of river‐captured fish and, generally, the difference was more pronounced under warm temperatures. The survival–temperature relationships for ocean‐captured fish were used to predict historic (1961–1990) and future (2010–2099) survival under simulated lower river thermal experiences for the Quesnel, Stellako‐Late Stuart and Adams stocks. A decrease of 9–16% in survival of all these stocks was predicted by the end of the century if the Fraser River continues to warm as expected. However, the decrease in future survival of Adams sockeye salmon would occur only if fish continue to enter the river abnormally early, towards warmer periods of the summer, as they have done since 1995. The survival estimates and predictions presented here are likely optimistic and emphasize the need to consider stock‐specific responses to temperature and climate warming into fisheries management and conservation strategies.     

Olfactory gene expression in migrating adult sockeye salmon Oncorhynchus nerka

Expression of 12 olfactory genes was analysed in adult sockeye salmon Oncorhynchus nerka nearing spawning grounds and O. nerka that had strayed from their natal migration route. Variation was found in six of these genes, all of which were olfc olfactory receptors and had lower expression levels in salmon nearing spawning grounds. The results may reflect decreased sensitivity to natal water olfactory cues as these fish are no longer seeking the correct migratory route. The expression of olfactory genes during the olfactory‐mediated spawning migration of Pacific salmon Oncorhynchus spp. is largely unexplored and these findings demonstrate a link between migratory behaviours and olfactory plasticity that provides a basis for future molecular research on salmon homing.     

The impact of a brominated flame retardant on smoltification and olfactory function in Atlantic salmon (Salmo salar L.) smolts

Despite a reduction in exploitation of salmon stocks throughout the NE Atlantic, there continues to be a decline in many populations. The factors regulating these populations remain poorly understood, although there is evidence that environmental conditions experienced in freshwater can effect survival in the marine environment. The aim of this study was to investigate the impact of a brominated flame retardant (hexabromocyclododecane, HBCD) on the parr-smolt transformation in juvenile salmon. It is during this pre-adaptive period to marine life that olfactory imprinting to the natal river is considered to occur. Fish were exposed to low levels of HBCD for 30 days over the peak smoltification period in freshwater, and then transferred to clean seawater for 20 days. Fish were sampled weekly to assess changes in some of the physiological parameters associated with smoltification, and olfactory response to conspecific smolt urine was measured using an electro-olfactogram (EOG). Exposure to HBCD did not affect seawater adaptability, although there was some disruption of plasma thyroid hormone levels, as well as a reduction in olfactory function to conspecific smolt urine. The results are discussed in relation to the marine survival and successful homing of adult salmon.     

The impact of a brominated flame retardant on smoltification and olfactory function in Atlantic salmon (Salmo salar L.) smolts

Despite a reduction in exploitation of salmon stocks throughout the NE Atlantic, there continues to be a decline in many populations. The factors regulating these populations remain poorly understood, although there is evidence that environmental conditions experienced in freshwater can effect survival in the marine environment. The aim of this study was to investigate the impact of a brominated flame retardant (hexabromocyclododecane, HBCD) on the parr-smolt transformation in juvenile salmon. It is during this pre-adaptive period to marine life that olfactory imprinting to the natal river is considered to occur. Fish were exposed to low levels of HBCD for 30 days over the peak smoltification period in freshwater, and then transferred to clean seawater for 20 days. Fish were sampled weekly to assess changes in some of the physiological parameters associated with smoltification, and olfactory response to conspecific smolt urine was measured using an electro-olfactogram (EOG). Exposure to HBCD did not affect seawater adaptability, although there was some disruption of plasma thyroid hormone levels, as well as a reduction in olfactory function to conspecific smolt urine. The results are discussed in relation to the marine survival and successful homing of adult salmon.     

Salmonid olfactory system-specific protein (N24) exhibits glutathione S-transferase class pi-like structure

A salmonid olfactory system-specific protein (N24) that has been identified in lacustrine sockeye salmon (Oncorhynchus nerka) was characterized by biochemical and molecular biological techniques. N24 is a homodimer, and the intact molecular mass is estimated as approximately 43.3 kDa by gel filtration. Furthermore, N24 was located only in the cytosolic fraction of the olfactory tissues as determined by subcellular fractionation. cDNA encoding the lacustrine sockeye salmon N24 was isolated and sequenced. This cDNA contained a coding region encoding 216 amino acid residues and the molecular mass of this protein is calculated to be 242,224.77. The protein and nucleotide sequencing demonstrates the existence of a remarkable homology between N24 and glutathione S-transferase (GST; EC 2.5.1.18) class pi enzymes. Northern analysis showed that N24 mRNA with a length of 950 bases is expressed in lacustrine sockeye salmon olfactory epithelium. Olfactory receptor cells showed strong hybridization signals for N24 mRNA in the olfactory epithelium. N24 demonstrated glutathione binding activity in affinity-purified GST column experiments. The present study describes for the first time cDNA cloning of GST in fish olfactory epithelium.     

Individual variation in migration speed of upriver-migrating sockeye salmon in the Fraser River in relation to their physiological and energetic status at marine approach

Little research has examined individual variation in migration speeds of Pacific salmon (Oncorhynchus spp.) in natural river systems or attempted to link migratory behavior with physiological and energetic status on a large spatial scale in the wild. As a model, we used three stocks of summer-run sockeye salmon (Oncorhynchus nerka) from the Fraser River watershed, British Columbia, to test the hypothesis that individual variation in migration speed is determined by a combination of environmental factors (i.e., water temperature), intrinsic biological differences (sex and population), and physiological and energetic condition. Before the freshwater portion of the migration, sockeye salmon (Quesnel, Chilcotin, and Nechako stock complexes) were captured in Johnstone Strait ( approximately 215 km from river entry), gastrically implanted with radio transmitters, and sampled for blood, gill tissue, and energetic status before release. Analyses focused solely on individuals that successfully reached natal subwatersheds. Migration speeds were assessed by an extensive radiotelemetry array. Individuals from the stock complex that migrated the longest distance (Nechako) traveled at speeds slower than those of other stock complexes. Females traveled slower than males. An elevated energetic status of fish in the ocean was negatively correlated with migration speed in most river segments. During the transition from the ocean to the river, migration speed was negatively correlated with mean maximum water temperature; however, for the majority of river segments, it was positively correlated with migration speed. Physiological status measured in the ocean did not explain among-individual variability in river migration speeds. Collectively, these findings suggest that there could be extensive variation in migration behavior among individuals, sexes, and populations and that physiological condition in the ocean explained little of this variation relative to in-river environmental conditions and energetic status. Interestingly, individual fish generally retained their rank in swimming speed across different segments, except when transiting a challenging canyon midway during the migration.     

Going with the Flow: Spatial Distributions of Juvenile Coho Salmon Track an Annually Shifting Mosaic of Water Temperature

A critical challenge for ecologists is to understand the functional significance of habitat heterogeneity and connectivity for mobile animals. Here, we explore how a thermo-regulating fish responds to annual variation in the spatial patterning of thermal and trophic resources. In a third-order stream in coastal Alaska, juvenile coho salmon forage on sockeye salmon eggs at night in cold water and then move to warmer water to increase their digestive capacity. We mapped the spatial distributions of water temperature, juvenile coho salmon, and spawning sockeye salmon across a 5-year period during which summer discharge varied by greater than fivefold. In low flow years, warm water (9–12°C) was only available in thalweg (that is, main-channel) habitat at least approximately 400 m upstream of the cooler habitat (3–7°C) where sockeye salmon spawned. In high flow years, the entire stream thalweg was isothermal at 7–8°C, but inundated off-channel areas generated warm habitats (9–12°C) laterally adjacent to the downstream regions where sockeye salmon spawned. The daytime spatial distribution of juvenile coho salmon shifted from headwater thalweg habitats in low flow years, to downstream off-channel habitats in high flow years. In all years, the majority of juvenile coho salmon sampled during the daytime were found in warm habitat units without sockeye salmon present, yet they exhibited diet contents comprised virtually entirely of sockeye salmon eggs. Thus, thermoregulatory movements by coho salmon were able to track an annually shifting mosaic of water temperature. Our results demonstrate how the spatial habitat heterogeneity and connectivity of intact floodplains can in turn buffer aquatic organisms from high levels of temporal variation in habitat conditions and resource abundance.     

A wide window of migration phenology captures inter‐annual variability of favourable conditions: Results of a whole‐lake experiment with juvenile Pacific salmon

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Variation in smoltification age and its determinants in sockeye salmon of Lake Azabach’e

In this paper, we analyze scale samples of sexually mature sockeye salmon from Lake Azabach'e collected over many years and data on the abundance of zooplankton in this lake. For native juvenile sockeye salmon, the major limiting factor of growth and smoltification is food availability. During the observation period from 1977 to 1993, two-year-olds were the most numerous group among the downstream-migrating sockeye salmon. Short-term fluctuations in the proportion of one-year-old smolts during downstream migration are attributed to outbreaks of plankton due to the natural fertilization of the lake.     

Philomena oncorhynchi: Effect of hormones on maturation in anadromous sockeye, Oncorhynchus nerka

Adult sockeye salmon, Oncorhynchus nerka (Walbaum), treated with salmon pituitary extract in July survived for up to 47 days and developed nuptial colours in both male and female fish during this period, whereas no such characteristics appeared in untreated control fish. Furthermore, results showed that 20 of 50 adult female Philomena oncorhynchi recovered from the 15 treated fish contained fully developed tailed larvae in the uterus as compared with only one of 44 female P. oncorhynchi from 31 untreated control fish. None of 51 worms from 13 stilboestrol treated adult sockeye showed development in utero beyond an elongated embryo, nor did the host fish develop nuptial colours. P. oncorhynchi and its immature sockeye host (approx. 1 year prior to spawning) remained unaffected by any of three separate hormone treatment experiments using injection of salmon pituitary extract, injection of 17-β-estradiol, and stilboestrol mixed in the food.     

Evidence for a carrier state of infectious hematopoietic necrosis virus in chinook salmon Oncorhynchus tshawytscha.

In British Columbia, Canada, infectious hematopoietic necrosis virus (IHNV) is prevalent in wild sockeye salmon Oncorhynchus nerka and has caused disease in seawater net-pen reared Atlantic salmon Salmo salar. In this study, chinook salmon Oncorhynchus tshawytscha experimentally exposed to an isolate of IHNV found in British Columbia became carriers of the virus. When Atlantic salmon were cohabited with these virus-exposed chinook salmon, IHNV was isolated from the Atlantic salmon. Identification of chinook salmon populations that have been exposed to IHNV may be difficult, as virus isolation was successful only in fish that were concurrently infected with either Renibacterium salmoninarum or Piscirickettisia salmonis. Also, IHNV-specific antibodies were detected in only 2 of the 70 fish experimentally exposed to the virus. Two samples collected from chinook salmon exposed to IHNV while at a salt water net-pen site had a seroprevalence of 19 and 22%; however, the inconsistencies between our laboratory and field data suggest that further research is required before we can rely on serological analysis for identifying potential carrier populations. Because of the difficulty in determining the exposure status of populations of chinook salmon, especially if there is no concurrent disease, it may be prudent not to cohabit Atlantic salmon with chinook salmon on a farm if there is any possibility that the latter have been exposed to the virus.     

Ontogenetic shifts in olfactory rosette morphology of the sockeye salmon,Oncorhynchus nerka

Sockeye salmon, Oncorhynchus nerka, are anadromous, semelparous fish that breed in freshwater—typically in streams, and juveniles in most populations feed in lakes for 1 or 2 years, then migrate to sea to feed for 2 or 3 additional years, before returning to their natal sites to spawn and die. This species undergoes important changes in behavior, habitat, and morphology through these multiple life history stages. However, the sensory systems that mediate these migratory patterns are not fully understood, and few studies have explored changes in sensory function and specialization throughout ontogeny. This study investigates changes in the olfactory rosette of sockeye salmon across four different life stages (fry, parr, smolt, and adult). Development of the olfactory rosette was assessed by comparing total rosette size (RS), lamellae number, and lamellae complexity from scanning electron microscopy images across life stages, as a proxy for olfactory capacity. Olfactory RS increased linearly with lamellae number and body size (p < .001). The complexity of the rosette, including the distribution of sensory and nonsensory epithelia and the appearance of secondary lamellar folding, varied between fry and adult life stages. These differences in epithelial structure may indicate variation in odor-processing capacity between juveniles imprinting on their natal stream and adults using those odor memories in the final stages of homing to natal breeding sites. These findings improve our understanding of the development of the olfactory system throughout life in this species, highlighting that ontogenetic shifts in behavior and habitat may coincide with shifts in nervous system development.     

Amino acid cues emanating from Pacific salmon eggs and ovarian fluid

The eggs of salmonid fishes are an important food source for many aquatic predators that detect eggs using olfaction. Moreover, chemicals from eggs and ovarian fluid aid sperm cells in detecting and locating eggs for fertilization, and ovarian fluid is attractive to conspecific males. Thus chemicals from eggs and ovarian fluid may facilitate reproduction but may also attract egg predators. The authors sampled mature females of three Pacific salmon species – Chinook (Oncorhynchus tshawytscha), coho (Oncorhynchus kisutch) and sockeye (Oncorhynchus nerka) – and determined the proportional representation of amino acids, potent fish odorants, from their eggs and ovarian fluid (Chinook and coho salmon only). They then tested juvenile coho salmon, an egg predator, for responses to ovarian fluid and egg odours using the electro-olfactogram (EOG) recording technique. The amino acid compositions of the salmon species were significantly and positively correlated with each other, and the interspecific differences were comparable to those between individuals of the same species. The egg water samples were, on average, dominated by lysine, alanine and glutamine (12.6%, 12.4% and 10.9%, respectively). The ovarian fluid samples were dominated by lysine (20.5%), followed by threonine (9.7%), glycine (9.2%) and arginine (8.8%). EOG recordings demonstrated the ability of juvenile coho salmon to detect the chemical traces of eggs and ovarian fluid. It is concluded that salmon eggs are a potent source of odours for potential predators but likely not highly differentiated among salmon species.     

Sea louse infection of juvenile sockeye salmon in relation to marine salmon farms on Canada's west coast

Background

Pathogens are growing threats to wildlife. The rapid growth of marine salmon farms over the past two decades has increased host abundance for pathogenic sea lice in coastal waters, and wild juvenile salmon swimming past farms are frequently infected with lice. Here we report the first investigation of the potential role of salmon farms in transmitting sea lice to juvenile sockeye salmon (Oncorhynchus nerka).

Methodology/Principal Findings

We used genetic analyses to determine the origin of sockeye from Canada''s two most important salmon rivers, the Fraser and Skeena; Fraser sockeye migrate through a region with salmon farms, and Skeena sockeye do not. We compared lice levels between Fraser and Skeena juvenile sockeye, and within the salmon farm region we compared lice levels on wild fish either before or after migration past farms. We matched the latter data on wild juveniles with sea lice data concurrently gathered on farms. Fraser River sockeye migrating through a region with salmon farms hosted an order of magnitude more sea lice than Skeena River populations, where there are no farms. Lice abundances on juvenile sockeye in the salmon farm region were substantially higher downstream of farms than upstream of farms for the two common species of lice: Caligus clemensi and Lepeophtheirus salmonis, and changes in their proportions between two years matched changes on the fish farms. Mixed-effects models show that position relative to salmon farms best explained C. clemensi abundance on sockeye, while migration year combined with position relative to salmon farms and temperature was one of two top models to explain L. salmonis abundance.

Conclusions/Significance

This is the first study to demonstrate a potential role of salmon farms in sea lice transmission to juvenile sockeye salmon during their critical early marine migration. Moreover, it demonstrates a major migration corridor past farms for sockeye that originated in the Fraser River, a complex of populations that are the subject of conservation concern.