Physiological condition and migratory experience affect fitness‐related outcomes in adult female sockeye salmon

Relating fish physiology, behaviour and experience to fitness‐related outcomes at the individual scale is ecologically significant, but presents difficulties for free‐ranging fishes in natural systems. Physiological state (e.g. level of stress or maturity) and experience (e.g. habitat use or exposure to stressors) may alter the probability of survival or reproduction. This study examined the relative influence of physiology and migratory experience on survival, migration duration, reproductive longevity, and egg retention in adult female sockeye salmon (Oncorhynchus nerka) from a Fraser River population. One hundred and thirty‐five females were plasma sampled and tagged with radio transmitters and archival temperature loggers. Fish were tracked 55 km through two natal lakes to spawning grounds, following passage of a hydroelectric dam. For 39 females, we assessed the proportion of time within an optimal temperature (T_optAS) window (13.4–19.5°C), which provides ≥90% of maximum aerobic scope. Females with lower plasma glucose concentrations were more likely to reach spawning grounds. Early migrants spent longer in natal lakes. More time in the T_optAS window was associated with greater reproductive longevity and lower probability of egg retention. Later arriving females had reduced longevity on spawning grounds, as did females that retained eggs. Exposure to higher dam discharge was associated with reduced reproductive longevity and greater probability of egg retention, but not lower survival, indicating a delayed effect of dam passage. Our results underscore the complexity of factors governing fitness‐related outcomes for salmonids, particularly the importance of female experience in the days and weeks prior to spawning.     

Temperature-mediated en route migration mortality and travel rates of endangered Snake River sockeye salmon

Abstract  Conservation efforts for endangered Snake River sockeye salmon ( Oncorhynchus nerka ) have been hindered by high en route adult mortality during their ∼1450 km freshwater spawning migration. Identifying causal factors for this mortality has been difficult given very small (often <10 fish) annual returns in recent decades. However, several hundred hatchery-bred fish returned in 2000 and we intercepted and radio-tagged 31 in mid-migration to monitor behaviours and survival. All fish initially migrated at similar rates, but later-timed fish eventually slowed migration and were far more likely to be unsuccessful. Late-season mortality was strongly associated with water temperatures near tolerance thresholds (21–24 °C). The data also suggest increased risk for fish in poor initial condition (i.e., with injuries or parasites) and probable recent selection against late-timed salmon. Results parallel temperature- and condition-related adult mortality in Columbia and Fraser River sockeye salmon populations and demonstrate the potential vulnerability of marginal southern populations to regional climate warming.     

Site fidelity of spawning sockeye salmon (Oncorhynchus nerka W.) in the presence and absence of olfactory cues

Abstract –  We examined the site fidelity of spawning adult sockeye salmon ( Oncorhynchus nerka ) by tagging and releasing fish in the same stream reach (controls) and displacing them among different but nearby sites ( c . 50 m away). Three sites – two above a stream junction ('upper' reach and 'pond') and one below ('lower' reach) – allowed us to compare the behavior of salmon in the presence and absence of olfactory cues and habitat similarity. Most controls of both sexes (90%) remained in the immediate vicinity of the tagging and release site. When displaced downstream, where the odors of both the upper reach and the pond were detectable, most salmon returned to their former site (65%). Displaced sockeye were more likely to return to the pond from the lower reach than from the upper one ( P  = 0.05), consistent with olfactory orientation and the hypothesis that salmon prefer certain habitats. Salmon displaced from the upper to the lower reach were much more likely to return than those displaced to the pond ( P  < 0.01), consistent with the role of odors in orientation and inconsistent with the habitat choice hypothesis.     

Seasonal changes of hormones and muscle enzymes in adult lacustrine masu (Oncorhynchus masou) and sockeye salmon (O. nerka)

The upstream migration of adult anadromous fishes is characterized by physiological changes in responses to reproductive and energetic challenges. This study analyzed the physiological responses of lake-resident anadromous masu salmon (Oncorhynchus masou) and sockeye salmon (O. nerka) to migration in order to determine if these fish might serve as a suitable model for ocean-running populations and to differentiate between physiological responses to reproduction and to exercise-linked aspects of migration. Reproductive (estradiol, testosterone, 11-ketotestosterone, 17α,20β-dihydroxy-4-pregnen-3-one) and metabolically-linked (thyroxine, triiodothyronine) hormones showed similar patterns to ocean-running anadromous populations. White muscle pyruvate kinase, lactate dehydrogenase and malate dehydrogenase decreased with the onset of spawning season while white muscle citrate synthase, β-hydroxyacetyl CoA dehydrogenase, phosphofructokinase and glutamate oxaloacetate transaminase did not, suggesting that the former group of enzymes are responding to reproductive or food intake signals while the second group, which typically change during anadromous migration, may be responding to exercise-linked aspects of migration. This revised version was published online in August 2006 with corrections to the Cover Date.     

Epizootiology of Parvicapsulaminibicornis in Fraser River sockeye salmon, Oncorhynchusnerka (Walbaum)

Late-spawning Fraser River sockeye salmon, Oncorhynchus nerka , stocks have suffered significant prespawn mortality associated with an unusually early freshwater migration pattern and the myxosporean parasite Parvicapsula minibicornis . Surveys of migrating adult salmon from several spawning populations were conducted in 1999 and 2000 to determine the extent of infection with P. minibicornis , when and where the parasite first becomes detectable during migration, and whether early migrating stocks might be used as sentinels to assess risk of infection in late-spawning stocks. Posterior kidney, preserved in 95% ethanol, was examined for P. minibicornis in stained histological sections and using a polymerase chain reaction (PCR) test. The prevalence of this parasite in all Fraser River sockeye salmon stocks examined was high (range 47–100% infected). In contrast, P. minibicornis was not detected in the fish tested from the two sockeye salmon stocks outside the Fraser River drainage in either 1999 or 2000. The parasite was also not detected histologically or by PCR in the kidney tissue of the fish from the Fraser River that were sampled in salt water or early during their freshwater migration up the river. These findings and the progression in the prevalence and intensity of infection as the fish from three stocks (early Stuart, Weaver Creek and Cultus Lake) were monitored over time, suggest salmon acquired the parasite either in the lower Strait of Georgia or in the lower Fraser River before the confluence of the Harrison River. In both 1999 and 2000 the parasite was present in all Fraser River sockeye salmon stocks sampled, which suggests that early Stuart salmon may be valuable as a sentinel stock for the presence of the parasite in later-spawning stocks.     

Environmental conditions and physiological state influence estuarine movements of homing sockeye salmon

The reproductive migration of anadromous salmonids through estuarine waters is one of the most challenging stages of their life cycle, yet little is known about the environmental and physiological conditions that influence migratory behaviour. We captured, sampled tissues, tagged and released 365 sockeye salmon (Oncorhynchus nerka) homing through inner coastal waters towards the Fraser River, British Columbia, Canada. Biotelemetry was used to assess the behaviour of individual sockeye salmon approaching estuarine waters and at river entry, which were related to both fish physiological condition at release and to prevailing environmental conditions. Sockeye salmon tended to stay close to the shore, migrated during the day, and movements were related to tide. Sockeye salmon migration rate was linked to wind‐induced currents, salinity and an individual's physiological state, but these factors were specific to location and stock. We propose that wind‐induced currents exposed sockeye salmon entering the estuary to stronger olfactory cues associated with Fraser River water, which in turn resulted in faster migration rates presumably due to either an increased ability for olfactory navigation and/or advanced reproductive schedule through a neuroendocrine response to olfactory cues. However, once the migration had progressed further into more concentrated freshwater of the river plume, sockeye salmon presumably used wind‐induced currents to aid in movements towards the river, which may be associated with energy conservation. Results from this study improve our biological understanding of the movements of Fraser River sockeye salmon and are also broadly relevant to other anadromous salmonids homing in marine environments.     

Somatic energy of sockeye salmon Oncorhynchus nerka at the onset of upriver migration: a comparison among ocean climate regimes

We examined somatic energy patterns in two stocks (Chilko and Early Stuart) of adult Fraser River (British Columbia, Canada) sockeye salmon (Oncorhynchus nerka), collected at the end of their ocean residency, spanning years across different climate regimes. Both stocks had high levels of somatic energy in years with high open ocean productivity (1956, 1957, 2001 and 2002), and relatively low levels in years with poor open ocean productivity (1999 and 2000). For Early Stuart sockeye, energy levels in 1999 and 2000 were approximately 15% lower (～1.5 MJ kg^?1) than that in the 1950s, an amount of energy equivalent to that necessary for migrating 600 km upriver. In recent years (2001 and 2002), energy levels have increased by about 9% for both stocks. Low energy levels at the onset of upriver migration, particularly in years of energetically demanding in‐river conditions, such as high flows or temperatures, are likely to contribute to prespawning and en route mortality in Fraser sockeye.     

Dynamic in-lake spawning migrations by female sockeye salmon

Abstract –  Precise homing by salmon to natal habitats is considered the primary mechanism in the evolution of population-specific traits, yet few studies have focused on this final phase of their spawning migration. We radio tagged 157 female sockeye salmon ( Oncorhynchus nerka ) as they entered Lake Clark, Alaska, and tracked them every 1–10 days to their spawning locations. Contrary to past research, no specific shoreline migration pattern was observed (e.g., clockwise) nor did fish enter a tributary unless they spawned in that tributary. Tributary spawning fish migrated faster (mean = 4.7 km·day⁻¹, SD = 2.7, vs. 1.6 km·day⁻¹, SD = 2.1) and more directly (mean linearity = 0.8, SD = 0.2, vs. 0.4, SD = 0.2) than Lake Clark beach spawning fish. Although radio-tagged salmon migrated to within 5 km of their final spawning location in an average of 21.2 days (SD = 13.2), some fish migrated five times the distance necessary and over 50 days to reach their spawning destination. These results demonstrate the dynamic nature of this final phase of migration and support studies indicating a higher degree of homing precision by tributary spawning fish.     

Protein degradation and protease activity of chum salmon (Oncorhynchus keta) muscle during spawning migration

Sarcoplasmic protein content decreased significantly and myosin heavy chain was degraded gradually during spawning migration of chum salmon (Oncorhynchus keta). Acid and neutral proteinase activities increased significantly during spawning migration. These proteinase activities were higher in females than in males. High levels of acid proteinase were not caused by the injury of lysosomal membranes. Considering the physiological states of chum salmon, neutral proteinase activity might be related to the degradation of muscle protein. As the changes in serum sex steroids were similar to those in the protease activities during spawning migration, it was considered that high levels of protease activity during spawning migration were closely related to the serum levels of androgens.     

Computer simulations of the effects of the Sitka eddy on the migration of sockeye salmon returning to British Columbia

The Sitka eddy is a mesoscale eddy, 300 km in diameter, that develops off SE Alaska in about one year in two. The eddy has surface currents exceeding 50 km day⁻¹ and it has been suggested that the eddy could deflect migrating salmon to the south, thereby reducing the proportion of British Columbia (BC) sockeye salmon accessible to Alaskan fishers. We modelled its effects on the migration of sockeye salmon ( Oncorhynchus nerka ) returning to northern BC, using an individual-based model to simulate migration paths, migration timing and metabolic costs of salmon with different migration behaviours. Except when their migration behaviour included positive rheotaxis, salmon that encountered the eddy had faster migration times and lower metabolic costs than those that did not. The least complex migration behaviour, compass orientation with no rheotaxis, was only slightly less efficient in metabolic terms than the optimal migration paths determined by dynamic programming. Our simulations show that the Sitka eddy itself does not deflect migrating salmon to the south or south-east regardless of migration behaviour, but that by interrupting the normal northward flow of the Alaskan Current, the eddy could influence latitude of landfall of migrating salmon.     

Spatial correlation patterns in coastal environmental variables and survival rates of salmon in the north-east Pacific Ocean

We examined spatial correlations for three coastal variables [upwelling index, sea surface temperature (SST), and sea surface salinity (SSS)] that might affect juvenile salmon ( Oncorhynchus spp.) during their early marine life. Observed correlation patterns in environmental variables were compared with those in survival rates of pink ( O. gorbuscha ), chum ( O. keta ), and sockeye ( O. nerka ) salmon stocks to help identify appropriate variables to include in models of salmon productivity. Both the upwelling index and coastal SST were characterized by strong positive correlations at short distances, which declined slowly with distance in the winter months, but much more rapidly in the summer. The SSS had much weaker and more variable correlations at all distances throughout the year. The distance at which stations were no longer correlated (spatial decorrelation scale) was largest for the upwelling index (> 1000 km), intermediate for SST (400–800 km in summer), and shortest for SSS (< 400 km). Survival rate indices of salmon showed moderate positive correlations among adjacent stocks that decreased to zero at larger distances. Spatial decorrelation scales ranged from approximately 500 km for sockeye salmon to approximately 1000 km for chum salmon. We conclude that variability in the coastal marine environment during summer, as well as variability in salmon survival rates, are dominated by regional scale variability of several hundred to 1000 km. The correlation scale for SST in the summer most closely matched the observed correlation scales for survival rates of salmon, suggesting that regional-scale variations in coastal SST can help explain the observed regional-scale covariation in survival rates among salmon stocks.     

Marine and freshwater climatic factors affecting interannual variation in the timing of return migration to fresh water of sockeye salmon (Oncorhynchus nerka)

Interannual variation in the timing of the return migration to fresh water of adult sockeye salmon, Oncorhynchus nerka, from 46 populations throughout the species North American range was examined in a broad analysis of how timing patterns are affected by marine and freshwater conditions. Migration timing data (measured at various points along the migration, including just prior to freshwater entry, just after freshwater entry, and near the spawning grounds) were examined for correlations with sea‐surface temperatures (SST) prior to migration and to freshwater temperatures and flows during migration. Following a spring–summer period with warm SST, populations from southwestern Alaska tended to return early, Fraser River populations returned late, and populations from other regions showed no consistent patterns. Similarities between interannual timing of both nearby and distant populations indicated the presence of common or coincidental influences on timing. When riverine conditions related to timing, high flows and low temperatures were associated with late migrations, low flows and high temperatures were associated with early migrations. However, even counting stations at upriver locations showed correlations with SST. Notwithstanding some inconsistencies among the many populations examined and the indirect nature of the inferences, the results supported the hypotheses that (i) interannual variations in salmon distributions at sea reflect temperature conditions, and (ii) the date when salmon initiate homeward migration is a population‐specific trait, largely unaffected by the fish's location at sea.     

Prey partitioning and use of insects by juvenile sockeye salmon and a potential competitor,threespine stickleback,in Afognak Lake,Alaska

Freshwater growth of juvenile sockeye salmon (Oncorhynchus nerka) depends upon the quality and quantity of prey and interactions with potential competitors in the foraging environment. To a large extent, knowledge about the ecology of lake‐rearing juvenile sockeye salmon has emerged from studies of commercially important runs returning to deep nursery lakes, yet information from shallow nursery lakes (mean depth ≤ 10 m) is limited. We examined seasonal and ontogenetic variation in diets of juvenile sockeye salmon (N = 219, 30–85 mm) and an abundant potential competitor, threespine stickleback (Gasterosteus aculeatus; N = 198, 42–67 mm), to understand their foraging ecology and potential trophic interactions in a shallow Alaska lake. This study revealed that adult insects made up 74% of all sockeye salmon diets by weight and were present in 98% of all stomachs in Afognak Lake during the summer of 2013. Diets varied temporally for all fishes, but small sockeye salmon (<60 mm) showed a distinct shift in consumption from zooplankton in early summer to adult insects in late summer. We found significant differences in diet composition between sockeye salmon and threespine stickleback and the origin of their prey indicated that they also separated their use of habitat on a fine scale; however, the two species showed overlap in size selectivity of zooplankton prey. Considering that aquatic insects can be a primary resource for juvenile sockeye salmon in Afognak Lake, we encourage the development of nursery lake carrying capacity models that include aquatic insects as a prey source for sockeye salmon.     

Comparison of techniques for correlating survival and gene expression data from wild salmon

Abstract – In laboratory and field studies of survival, one of two alternative analytical techniques is often used to estimate survival rates and identify covariates, namely parametric survival analysis or Cormack–Jolly–Seber models. These techniques differ in algorithms and assumptions of the data. They also tend to be used under different circumstances depending on whether the intention is to demonstrate group‐specific differences or to predict survival variables. Here, we apply and compare both analytical techniques in a study that couples functional genomics with biotelemetry to ascertain the role of physiological condition on survival of adult sockeye salmon (Oncorhynchus nerka) migrating in the Fraser River, British Columbia, which builds on the growing concern over the decline in numbers of spawning fish. Herein, we show a high level of quantitative and qualitative agreement between the two analytical methods, with both showing a strong relationship exists between the genomic signature that accounts for the largest source of variance in gene expression among individuals and survival in one of the three populations assessed. This high level of agreement suggests the data and the approaches are generating reliable results. The novel approach used in our study to identify physiological processes associated with reduced fitness in wild populations should be of broad interest to conservation biologists and resource managers as it may help reduce the uncertainty associated with predicting population sizes.     

Lake trout growth is sensitive to spring temperature in southwest Alaska lakes

In high‐latitude lakes, air temperature is an important driver of ice cover thickness and duration, which in turn influence water temperature and primary production supporting lake consumers and predators. In lieu of multidecadal observational records necessary to assess the response of lakes to long‐term warming, we used otolith‐based growth records from a long‐lived resident lake fish, lake trout (Salvelinus namaycush), as a proxy for production. Lake trout were collected from seven deep, oligotrophic lakes in Lake Clark National Park and Preserve on in southwest Alaska that varied in the presence of marine‐derived nutrients (MDN) from anadromous sockeye salmon (Oncorhynchus nerka). Linear mixed‐effects models were used to partition variation in lake trout growth by age and calendar‐year and model comparisons tested for a mean increase in lake trout growth with sockeye salmon presence. Year effects from the best mixed‐effects model were subsequently compared to indices of temperature, lake ice, and regional indices of sockeye salmon escapement. A strong positive correlation between annual lake trout growth and temperature suggested that warmer springs, earlier lake ice break‐up, and a longer ice‐free growing season increase lake trout growth via previously identified bottom‐up increases in production with warming. Accounting for differences in the presence or annual escapement of sockeye salmon with available data did not improve model fit. Collectively with other studies, the results suggest that productivity of subarctic lakes has benefitted from warming spring temperatures and that temperature can synchronise otolith growth across lakes with and without sockeye salmon MDN.     

Changes in GnRH levels in the brain and pituitary gland during migrations of sockeye salmon and chum salmon

Levels of two moleculer types of gonadotropin-releasing hormone (GnRH), salmon GnRH (sGnRH) and chicken GnRH–II (cGnRH–II) in the various brain regions and pituitary gland of sockeye salmon (Oncorhynchus nerka) and chum salmon (O. keta) during smoltification and spawning migration, respectively, were measured using specific time-resolved fluoroimmunoassay (TR-FIA) systems. Changes in sGnRH levels in different brain regions tended to be specifically synchronized with serum thyroid hormone or pituitary gonadotropin (GTH) levels during smoltification and spawning migration, respectively. In contrast, cGnRH–II levels did not show such synchronized changes. SGnRH and cGnRH–II in various brain regions might have different roles during smoltification and spawning migration of salmonid fishes.     

Movements of Atlantic salmon migrating upstream through a fish-pass complex in Scotland

Abstract  – Movements of adult Atlantic salmon were tracked through a series of four fish passes and an impoundment on the River Conon system, Northern Scotland. Proportions of fish passing individual obstructions ranged from 63 to 100%. The cumulative effect was that only 4 of the 54 tagged fish reached the spawning areas. The fish were delayed for 1–41 days at a pool-and-overfall ladder and 1–52 days at a Borland fish lift. The fish swam through a 10 km long reservoir at 0.21–1.16 km·h⁻¹. A total of 13 fish negotiated a 2.5 km long, 3 m diameter diversion tunnel through a mountain to their home river. High levels of electromyogram (EMG) activity were recorded during ascent of a pool-and-overfall fish ladder, indicating that high energy demanding burst swimming was required.     

Reproductive strategies in small populations: using Atlantic salmon as a case study

Abstract –  Wild salmonid populations with only a few breeding adults may not exhibit a significant reduction in genetic variability compared with larger populations. Such an observation suggests that effective population sizes are larger than population size estimates based on direct adult counts and/or the mating strategy maximises outbreeding, contributing to increased heterozygosity. In the case of wild Atlantic salmon Salmo salar populations, stratification by age classes and sexes on the spawning grounds avoids inbreeding and increases genetic variability. We studied the breeding composition of four Spanish salmon populations. Over a 7-year period we concluded that the probability of within-cohort mating is very low: females generally reproduce after two sea-winters whereas males reproduce mostly as one sea-winter ( grilse ) and/or mature parr. Considering different levels of contribution of mature parr to spawning derived from field surveys, we developed a simple model for estimating effective population sizes and found that they doubled with 65% parr contribution expected for rivers at this latitude (43°N), and ranged from 100–800 individuals. The effect of between-cohort mating was modelled considering different ranges of differences in allele frequencies between cohorts and resulted in 28–50% increases in heterozygosity when considering a 65% parr contribution. The complex mating strategy of Atlantic salmon contributes to explain the high levels of genetic variability found for small populations of this species. This model can probably be extended to other animal species with mating strategies involving different cohorts.     

Detection of infectious haematopoietic necrosis virus in river water and demonstration of waterborne transmission

Abstract. In a study of the possible role of waterborne infectious haematopoietic necrosis virus in transmission of the disease among spawning sockeye salmon, Oncorhynchus nerka (Walbaum), both infection rates and virus titres were higher in fish held at high density in a side channel than in fish in the adjacent river. Virus was never isolated from river water, but was found in water from the side channel at levels ranging from 32.5 to 1600 plaque-forming units (p.f.u.)/ml. Uninfected yearling sockeye salmon held in a box in the side channel developed localized gill infections with IHN virus. The disease did not progress to the viscera until a threshold titre of about 10⁵ p.f.u./g was reached in the gill. The effectiveness of the gill as a barrier limiting development of systemic infections means that waterborne IHN virus probably does not greatly increase the infection rate in a sockeye salmon population during spawning.     

Effects of low pH on the reproductive behavior of salmonid fishes

In northern Europe and America, the acidification of lakes and rivers induced by acid precipitation has damaged fish populations. At present, rapidly expanding industrial activities in East Asia have led to continuous increases in the quantity of emission of acidic pollutants, and rain of acidic levels of pH4 has precipitated throughout Japan. In this way, the effects of acid rain on fish populations have also been manifested in Japan. In order to examine the effects of low pH on the reproductive behavior of salmonids which are known to be acid-sensitive species, changes in the frequency of upstream behavior and spawning-related female nest-digging behavior in response to changes in pH were observed in mature hime salmon (land-locked sockeye salmon) Oncorhynchus nerka, brown trout Salmo trutta and Japanese char Salvelinus leucomaenis. Digging and upstream behavior were significantly inhibited in weakly acidic water of pH 5.8–6.4 formulated using sulfuric acid. Land-locked sockeye salmon was the most sensitive to changes in pH among the three species.