Basin‐scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic salmon (Salmo salar)

Migrations between different habitats are key events in the lives of many organisms. Such movements involve annually recurring travel over long distances usually triggered by seasonal changes in the environment. Often, the migration is associated with travel to or from reproduction areas to regions of growth. Young anadromous Atlantic salmon (Salmo salar) emigrate from freshwater nursery areas during spring and early summer to feed and grow in the North Atlantic Ocean. The transition from the freshwater (‘parr’) stage to the migratory stage where they descend streams and enter salt water (‘smolt’) is characterized by morphological, physiological and behavioural changes where the timing of this parr‐smolt transition is cued by photoperiod and water temperature. Environmental conditions in the freshwater habitat control the downstream migration and contribute to within‐ and among‐river variation in migratory timing. Moreover, the timing of the freshwater emigration has likely evolved to meet environmental conditions in the ocean as these affect growth and survival of the post‐smolts. Using generalized additive mixed‐effects modelling, we analysed spatio‐temporal variations in the dates of downstream smolt migration in 67 rivers throughout the North Atlantic during the last five decades and found that migrations were earlier in populations in the east than the west. After accounting for this spatial effect, the initiation of the downstream migration among rivers was positively associated with freshwater temperatures, up to about 10 °C and levelling off at higher values, and with sea‐surface temperatures. Earlier migration occurred when river discharge levels were low but increasing. On average, the initiation of the smolt seaward migration has occurred 2.5 days earlier per decade throughout the basin of the North Atlantic. This shift in phenology matches changes in air, river, and ocean temperatures, suggesting that Atlantic salmon emigration is responding to the current global climate changes.     

Association between environmental factors, smolt size and the survival of wild and reared Atlantic salmon from the Simojoki River in the Baltic Sea

The survival of Atlantic salmon Salmo salar in the Baltic Sea was examined in relation to smolt traits (length and origin) and annual environmental factors [sea surface temperature (SST) and seasonal North Atlantic Oscillation (NAO) index], and prey fish abundance (herring Clupea harengus and sprat Sprattus sprattus) in the main basin and the southern Gulf of Bothnia. The study was based on recapture data for Carlin‐tagged hatchery‐reared and wild smolts from the Simojoki, a river flowing into the northern Gulf of Bothnia. The survival of the wild and reared groups was analysed using an ANOVA model and a stepwise regression model, with the arcsin‐transformed proportion of recaptured fish as the response variable. The results demonstrated a combined influence of smolt traits and environmental factors on survival. For the reared Atlantic salmon released in 1986–1998 (28 groups), the increasing annual mean SST in July in the southern Gulf of Bothnia and increasing mean smolt size improved survival. If the SST in July was excluded from the model, the NAO index in May to July also had a positive effect on survival (P < 0·10). The log₁₀‐transformed abundance of 0+ year herring in the southern Gulf of Bothnia entered the model (P < 0·15) if the SST and NAO index were excluded. For the wild Atlantic salmon released in 1972–1993 (21 groups), only the increasing SST in July showed a significant association with improved survival (P = 0·004). Prey fish abundance in the main basin of the Baltic Sea had no influence on the survival of reared or wild smolt groups. The interaction between smolt size and the SST in July was not significant. The origin was a better, but not a significant, predictor of marine survival compared to the smolt size or the SST in July. The mean recapture rate of the wild groups was twice that of the reared groups in the whole data. The results suggest that cold summers in the Gulf of Bothnia reduce the survival of young Atlantic salmon in both wild and reared groups. The larger smolt size of the reared groups compared with the wild groups to some extent compensated for their lower ability to live in the wild.     

Thermal habitat of adult Atlantic salmon Salmo salar in a warming ocean

The year-round thermal habitat at sea for adult Atlantic salmon Salmo salar (n = 49) from northern Norway was investigated using archival tags over a 10 year study period. During their ocean feeding migration, the fish spent 90% of the time in waters with temperatures from 1.6–8.4°C. Daily mean temperatures ranged from −0.5 to 12.9°C, with daily temperature variation up to 9.6°C. Fish experienced the coldest water during winter (November–March) and the greatest thermal range during the first summer at sea (July–August). Trends in sea-surface temperatures influenced the thermal habitat of salmon during late summer and autumn (August–October), with fish experiencing warmer temperatures in warmer years. This pattern was absent during winter (November–March), when daily mean temperatures ranged from 3.4–5.0°C, in both colder and warmer years. The observations of a constant thermal habitat during winter in both warmer and colder years, may suggest that the ocean distribution of salmon is flexible and that individual migration routes could shift as a response to spatiotemporal alterations of favourable prey fields and ocean temperatures.     

Links between patterns of marine growth and survival of Atlantic salmon Salmo salar, L.

The hypothesis that marine survival of Atlantic salmon Salmo Salar is linked to marine growth was explored by using inter-circuli distances and total numbers of circuli existing on scales from a population monitored over nearly four decades. The results suggest that marine growth controls survival, particularly during the late summer and early winter of the first year at sea. Recruitment is strongly linked to growth, described as the total number of circuli, but not to inter-circuli distances. This highlights the potential of patterns of circuli number to be considered as proxies for growth. Indications that hatchery populations might be subject to other mortality events, in addition to those experienced by wild populations, are also presented.     

Residence time of the sea louse, Lepeophtheirus salmonis K., on Atlantic salmon, Salmo salar L., after immersion in fresh water

Returning adult salmon caught at the mouth of the River Dee, Aberdeenshire, were transferred to tanks in the laboratory. For fish placed in fresh water, sea lice remained attached for up to 6 days, though most lice were lost in the first 48 hours. Few lice were lost from salmon maintained in sea water. The experiments were conducted in water within a temperature range of 12·8 to 16° C, equivalent to summer river temperatures in the Aberdeenshire Dee.     

Amount and distribution of biochemical-genetic variation among wild populations and a hatchery stock of Atlantic salmon, Salmo salar L., from north-east Ireland

The effects of tributyltin (TBT) compounds on gill morphology were examined in the mummichog, Fundulus heteroclitus , in 96-h LC50 and 6-week sublethal exposures. Morphometry was used for the identification and quantification of effects with the light microscope. A 96-h LC50 of 17.2 μg 1 ¹ was determined. Morphometric analysis of gill tissues revealed hypertrophy of the lamellar epithelium in fish exposed to 17.2 μg 1–1. Relative diffusing capacity was significantly decreased (−41 %); ( P <0.05, ANOVA, Bonferroni t -test). At 35.6 μg 1⁻¹, TBT exposure resulted in a significant reduction (− 40%) in the volume of the lamellar blood channels. Both of these observations occurred in fish that showed signs of acute poisoning including loss of equilibrium. In fish exposed to sublethal concentrations of 0.105–2.000 μg TBT 1⁻¹ for 6 weeks, there were no pathological changes in the gill. There were no treatment-related changes in the surface morphology of the gills of fish from both experiments upon scanning electron microscopic examination. Although gill pathology was observed in acutely toxic exposures, it does not appear to be a major mechanism of TBT toxicity.     

Expression of olfactory receptors in different life stages and life histories of wild Atlantic salmon (Salmo salar)

It has been hypothesized that salmonids use olfactory cues to return to their natal rivers and streams. However, the key components of the molecular pathway involved in imprinting and homing are still unknown. If odorants are involved in salmon homing migration, then olfactory receptors should play a critical role in the dissipation of information from the environment to the fish. Therefore, we examined the expression profiles of a suite of genes encoding olfactory receptors and other olfactory-related genes in the olfactory rosettes of different life stages in two anadromous and one non-anadromous wild Atlantic salmon populations from Newfoundland, Canada. We identified seven differentially expressed OlfC genes in juvenile anadromous salmon compared to returning adults in both populations of anadromous Atlantic salmon. The salmon from the Campbellton River had an additional 10 genes that were differentially expressed in juveniles compared to returning adults. There was no statistically significant difference in gene expression of any of the genes in the non-anadromous population (P < 0.01). The function of the OlfC gene products is not clear, but they are predicted to be amino acid receptors. Other studies have suggested that salmon use amino acids for imprinting and homing. This study, the first to examine the expression of olfactory-related genes in wild North American Atlantic salmon, has identified seven OlfC genes that may be involved in the imprinting and homeward migration of anadromous Atlantic salmon.     

Characterization of transferrin‐linked microsatellites in brown trout (Salmo trutta) and Atlantic salmon (Salmo salar)

The transferrin (TF) gene has recently received increased interest in fish given its fitness relevance as a resistance gene against pathogenic bacteria. In this study, we characterized five TF‐linked microsatellites in brown trout (Salmo trutta) and Atlantic salmon (Salmo salar). Interestingly, each marker amplified duplicated loci and linkage analysis revealed that the TF gene has most likely experienced a tandem duplication during salmonid evolution. In addition, the amplification of all five markers across a wide range of salmonid species suggests that they may be of general interest for the genetic analysis of the TF gene(s) in this teleost family.     

Spawning-strategy-dependent diets in two North American populations of Atlantic salmon Salmo salar

The diet of repeat-spawner Atlantic salmon Salmo salar was investigated using carbon and nitrogen stable-isotope values from the outer growth band of scales, which reflect the fish's consumption and growth during their most recent marine phase. Isotope values for S. salar displaying different spawning strategies were compared between and within the Miramichi and Nashwaak Rivers, New Brunswick, Canada and a Bayesian mixing model was used to infer dietary contributions from potential prey items. Significant differences in the stable-isotope values were found among spawning strategies and between rivers, indicating differences in diet and feeding area, consistent with hypotheses. Bayesian mixing model results inferred the main prey items consumed during marine feeding by S. salar to consist of hyperiid amphipods and capelin Mallotus villosus for repeat alternate spawners from both rivers, sandlance Ammodytes sp. for repeat consecutive spawners from the Miramichi River and amphipods for repeat consecutive spawners from the Nashwaak River. These results demonstrate the diversity of feeding tactics among S. salar spawning strategies from the same river and between populations from different rivers. Accounting for differences in prey availability and the subsequent impact on S. salar diet and spawner return rates (i.e., marine survival) will facilitate the application of ecosystem-based management practices, such as ensuring that fisheries for forage species do not indirectly adversely affect S. salar return rates.     

Genetic differentiation among natural European populations of Atlantic salmon, Salmo salar L., from drainages of the Atlantic Ocean

Previously published allelic frequencies at four polymorphic protein coding loci were used as a basis for examining genetic relationships among 19 European populations of Atlantic salmon, Salmo salar L.--exclusive of Baltic drainages--from the Barents Sea to Spain. The data did not support a model of distinct ancestral (e.g. Boreal and Celtic) origins, but were consistent with all populations descending from a single ancestral group within this region with genetically diverged populations drawn together through limited local migrations.     

Migratory behaviour and survival rates of wild northern Atlantic salmon Salmo salar post‐smolts: effects of environmental factors

To study smolt behaviour and survival of a northern Atlantic salmon Salmo salar population during river descent, sea entry and fjord migration, 120 wild S. salar were tagged with acoustic tags and registered at four automatic listening station arrays in the mouth of the north Norwegian River Alta and throughout the Alta Fjord. An estimated 75% of the post‐smolts survived from the river mouth, through the estuary and the first 17 km of the fjord. Survival rates in the fjord varied with fork length (L_F), and ranged from 97·0 to 99·5% km^?1. On average, the post‐smolts spent 1·5 days (36 h, range 11–365 h) travelling from the river mouth to the last fjord array, 31 km from the river mouth. The migratory speed was slower (1·8 L_F s^?1) in the first 4 km after sea entry compared with the next 27 km (3·0 L_F s^?1). Post‐smolts entered the fjord more often during the high or ebbing tide (70%). There was no clear diurnal migration pattern within the river and fjord, but most of the post‐smolts entered the fjord at night (66%, 2000–0800 hours), despite the 24 h daylight at this latitude. The tidal cycle, wind‐induced currents and the smolts' own movements seemed to influence migratory speeds and routes in different parts of the fjord. A large variation in migration patterns, both in the river and fjord, might indicate that individuals in stochastic estuarine and marine environments are exposed to highly variable selection regimes, resulting in different responses to environmental factors on both temporal and spatial scales. Post‐smolts in the northern Alta Fjord had similar early marine survival rates to those observed previously in southern fjords; however, fjord residency in the north was shorter.     

Microsatellite loci reveal highly significant genetic differentiation among Atlantic salmon (Salmo salar L.) stocks from the east coast of Canada

Allele frequency data from eight microsatellite loci provide evidence of highly significant genetic differentiation among stocks of Atlantic salmon Salmo salar L. from the Bay of Fundy, eastern and north-western Nova Scotia and Newfoundland. Estimates of genetic structure ( R _ST and θ) were significant both among all samples taken from the different geographical locations and among samples from geographical regions for which more than one stock was sampled. Samples from the Bay of Fundy taken from stocks which are phenotypically and behaviourally diverse showed particularly high levels of genetic structure. Rogers', allele sharing and (δμ)² distances also revealed significant differences among stock samples and were significantly correlated [Rogers' and (δμ)²] with sea distance between rivers. Results suggest that stocks of Atlantic salmon in eastern Canada are highly diverse genetically and that this should be an important consideration in any management programme for stocks in the area.     

Territory size and distribution of newly-emerged Atlantic salmon (Salmo salar)

Newly emerged Atlantic salmon (Salmo salar) were observed from May to August 1981 at six isolated redds in Washington County, Maine, USA. Territorial size and distribution were measured. At the end of the emergence period (12 to 28 May), fish maintained positions (stations) at redds where water velocity did not exceed 52 cm s^–1 By 12 June, most salmon (80–96%) had moved off the redds of origin and had established territories 1 to 5 m from the redd. The area defended increased substantially after mid-June, but territorial aggression diminished by 15 July, and the fry dispersed downstream. All fish observed were territorial, and the percentage of time during which stations were held decreased from 89 in mid-May to as low as 40% in mid-June.Cooperators are the Maine Department of Inland Fisheries and Wildlife, University of Maine, U.S. Fish and Wildlife Service, and the Wildlife Management Institute     

Hierarchical analysis of wild Atlantic salmon (Salmo salar) fecundity in relation to body size and developmental traits

Using data from wild Atlantic salmon Salmo salar returning to spawn in seven Scottish rivers, we developed a model of fecundity based on individual body size and key developmental traits. We used a novel approach to model selection which maximises predictive accuracy for application to target river stocks to select the best from a suite of Bayesian hierarchical models. This approach aims to ensure the optimal model within the candidate set includes covariates that best predict out-of-sample data to estimate fecundity in areas where no direct observations are available. In addition to body size, the final model included the developmental characteristics of age at smolting and years spent at sea. Using two independent long-term monitoring datasets, the consequences of ignoring these characteristics was revealed by comparing predictions from the best model with models that omitted them.     

Does increased abundance of sea lice influence survival of wild Atlantic salmon post‐smolt?

A synthesis of results from two projects was assessed to analyse possible influence of sea lice Lepeophtheirus salmonis on marine Atlantic salmon Salmo salar survival. During the years 1992–2004, trawling for wild migrating post-smolts was performed in Trondheimsfjord, a fjord in which no Atlantic salmon aquaculture activity is permitted. Prevalence and intensity of sea lice infections on migrating wild post-smolts differed between years. A correlation analysis between 1 sea-winter (SW) Atlantic salmon catch statistics from the River Orkla (a Trondheimsfjord river) and sea lice infections on the migrating smolts in the Trondheimsfjord was not significant. Up to 2% reduction in adult returns due to sea-lice infection was expected. In addition, experimental releases from 1996 to 1998 with individually tagged groups of hatchery-reared Atlantic salmon smolts given protection against sea-lice infection was performed. Higher recaptures of adult Atlantic salmon from 1998 treated smolts compared to the control group may correspond to high abundance of sea lice found on the wild smolt, and may indicate influence on post-smolt mortality. These studies indicate that post-smolt mortality in Trondheimsfjord is marginally influenced by sea lice infection; however, the methods for assessing wild smolt mortality might be insufficient. Higher infections of sea lice farther out in the fjord may indicate more loss in Atlantic salmon returns in some years.     

Overwintering and migration behaviour of post-spawned Atlantic salmon Salmo salar in a large hydropower-regulated river and reservoir

Tracking 47 post-spawned adult Atlantic salmon Salmo salar L. in a hydropower-regulated river through autumn, winter and spring revealed that winter survival was 56% and 75% in two study years, respectively, with higher mortality of males than females (50% vs. 33% and 100% vs. 13%, respectively). Some kelts (n = 7) displayed nondirected movements that were interpreted as a reconditioning period for an average of 9–17 days prior to directed downstream movements indicating the initiation of migration. Survival after the initiation of migration in spring was 83% and 94% to the hydropower dam in the first and second study years, and decreased to 60 and 63%, respectively, after dam passage. There were no further losses in the downriver reach in the second year, with the first year having a cumulative survival estimate of 53% to the river mouth. Kelts approached the dam when the spillway gates were available as a passage option most of the time (64%–75%), but some kelts arrived at the dam or had not yet passed when spillways were closed (n = 6) and the only remaining passage option was restricted to the turbines. However, all but one kelt that must have passed via turbine were successful in reaching the river mouth. Migratory delay presumably due to searching behaviour caused by low water flow was estimated at approximately 6 days as migration rates were significantly slower in the reservoir (median ± s.e. 8.5 ± 2.5 km day⁻¹) than up- (29.7 ± 5.0 km day⁻¹) or downriver (22.1 ± 3.1 km day⁻¹). The proportion of time (median 30%) that kelts spent swimming upstream (searching behaviour) in the reservoir was a significant variable for migration success.     

Date of marine annulus formation in Atlantic salmon (Salmo salar) and implications for retrospective growth analyses using scales

Fish scales have increasingly been used to quantify annual and seasonal growth trends and in efforts to relate growth to environmental conditions. Understanding the timing of formation of an annulus (a group of narrowly spaced circuli) is critical when assessing the influence of marine ecosystem conditions on seasonal growth patterns of Atlantic salmon, yet the literature does not provide consistent answers regarding the timing or drivers of marine annulus formation. This study demonstrates a novel method for estimating stock-specific annulus formation timing based on marked individuals with known emigration and return/recovery dates. An equation was applied to estimate the date of annulus completion for Atlantic salmon (Salmo salar) using known dates, number of circuli after the most recent annulus and marine circulus deposition rate. Five marine circulus deposition rate scenarios were tested, some of which accounted for individual, seasonal and age-related variability and others which use previously published marine circulus deposition rates. Based on these results, an argument is presented to reconsider the practice of assigning annulus formation dates to winter solstice in favour of dates estimated by a scenario that accounts for individual, seasonal and age-related variation in circulus deposition. This scenario suggests that annulus formation occurs between mid-February and late March. In this case, the annulus would be formed during the coldest part of the year in the primary overwintering area for North American Atlantic salmon.     

The effect of intragastric transmitters on feeding behaviour of Atlantic salmon, Salmo salar; parr during autumn

The proportion of Atlantic salmon parr (146 265 mm total length) that fed in laboratory tanks during autumn was 0% in fish filled with intragastric transmitters compared with 78 100% in controls.