Climate and ecosystem linkages explain widespread declines in North American Atlantic salmon populations

North American Atlantic salmon (Salmo salar) populations experienced substantial declines in the early 1990s, and many populations have persisted at low abundances in recent years. Abundance and productivity declined in a coherent manner across major regions of North America, and this coherence points toward a potential shift in marine survivorship, rather than local, river‐specific factors. The major declines in Atlantic salmon populations occurred against a backdrop of physical and biological shifts in Northwest Atlantic ecosystems. Analyses of changes in climate, physical, and lower trophic level biological factors provide substantial evidence that climate conditions directly and indirectly influence the abundance and productivity of North American Atlantic salmon populations. A major decline in salmon abundance after 1990 was preceded by a series of changes across multiple levels of the ecosystem, and a subsequent population change in 1997, primarily related to salmon productivity, followed an unusually low NAO event. Pairwise correlations further demonstrate that climate and physical conditions are associated with changes in plankton communities and prey availability, which are ultimately linked to Atlantic salmon populations. Results suggest that poor trophic conditions, likely due to climate‐driven environmental factors, and warmer ocean temperatures throughout their marine habitat area are constraining the productivity and recovery of North American Atlantic salmon populations.     

Temporal variation in abundance, return rate and life histories of previously spawned Atlantic salmon in a large subarctic river

The 30 year time series analyses revealed large temporal variation in the return rates and a recent increase in abundance of previous spawning Atlantic salmon Salmo salar in the River Teno, northern Scandinavia. The mean proportion of repeat spawners was 7 and 4% in the total Atlantic salmon catch and 9 and 22% in multi‐sea‐winter (MSW) catch component for females and males, respectively. Previous spawners constituted on the average 7% of the catch in mass but up to 20%(31 t) and 30%(19 t) in 2003 and in 2004, respectively. In 1975–2000, the proportion of previous spawners varied between 1 and 6%(3–12% of MSW Atlantic salmon), whereas in 2001–2004, they accounted for 8–21%(16–35% of MSW Atlantic salmon) of the total Atlantic salmon catch. The number of previous spawners in the catch correlated significantly with the preceding numbers of respective 1–3 sea‐winter (SW) maiden Atlantic salmon 2 years earlier. The recent increase in the numbers of 1S1 and 2S1 (1 or 2 years at sea followed by first spawning and 1 year reconditioning period at sea) alternate spawning Atlantic salmon was a consequence of higher numbers of maiden 1SW and 2SW Atlantic salmon in the catches and increased sea temperatures. Similarly, the return rate of 1SW Atlantic salmon to second spawning has improved in recent years. Most previous spawners ascended and were captured early in the fishing season. The smolt and sea‐age combinations of repeat spawners comprised 68 age groups contributing with the annual mean of 15 age groups to the great diversity of the River Teno Atlantic salmon population complex.     

Reproduction of interspecific hybrids of Atlantic salmon and brown trout in a stream environment

1. Reproduction between Atlantic salmon males and interspecific hybrid Salmo salar × Salmo trutta females was monitored in a controlled flow channel diverted from a south European river located at the edge of Atlantic salmon natural geographic distribution in Europe. 2. Post‐F1 hybrids were viable and survived in the wild, at least until dispersal from redds. After transfer to hatchery conditions, 67% survived into the second year. 3. The hybrids possessed 98 chromosomes: two sets of Atlantic salmon(2n = 58) and one set of brown trout (n = 40) chromosomes. 4. The existence of a low proportion of allotriploid individuals can be expected in rivers where Atlantic salmon and brown trout populations coexist.     

Perspectives on wild and hatchery salmon interactions at sea,potential climate effects on Japanese chum salmon,and the need for sustainable salmon fishery management reform in Japan

Pacific salmon (Oncorhynchus spp.) play an important role as a keystone species and provider of ecosystem services in the North Pacific ecosystem. We review our studies on recent production trends, marine carrying capacity, climate effects and biological interactions between wild and hatchery origin populations of Pacific salmon in the open sea, with a particular focus on Japanese chum salmon (O. keta). Salmon catch data indicates that the abundance of Pacific salmon increased since the 1976/77 ocean regime shift. Chum and pink salmon (O. gorbuscha) maintained high abundances with a sharp increase in hatchery-released populations since the late 1980s. Since the 1990s, the biomass contribution of hatchery returns to the total catch amounts to 50% for chum salmon, more than 10% for pink salmon, and less than 10% for sockeye salmon (O. nerka). We show evidence of density-dependence of growth and survival at sea and how it might vary across spatial scales, and we provide some new information on foraging plasticity that may offer new insight into competitive interactions. The marine carrying capacity of these three species is synchronized with long-term patterns in climate change. At the present time, global warming has positively affected growth and survival of Hokkaido populations of chum salmon. In the future, however, global warming may decrease the marine carrying capacity and the area of suitable habitat for chum salmon in the North Pacific Ocean. We outline future challenges for salmon sustainable conservation management in Japan, and recommend fishery management reform to sustain the hatchery-supported salmon fishery while conserving natural spawning populations.     

Does catch and release affect the mating system and individual reproductive success of wild Atlantic salmon (Salmo salar L.)?

In this study, we documented the breeding system of a wild population of Atlantic salmon (Salmo salar L.) by genetically sampling every returning adult and assessed the determinants of individual fitness. We then quantified the impacts of catch and release (C&R) on mating and reproductive success. Both sexes showed high variance in individual reproductive success, and the estimated standardized variance was higher for males (2.86) than for females (0.73). We found a weak positive relationship between body size and fitness and observed that fitness was positively correlated with the number of mates, especially in males. Mature male parr sired 44% of the analysed offspring. The impact of C&R on the number of offspring was size dependent, as the reproductive success of larger fish was more impaired than smaller ones. Also, there was an interactive negative effect of water temperature and air exposure time on reproductive success of C&R salmon. This study improves our understanding of the complex reproductive biology of the Atlantic salmon and is the first to investigate the impact of C&R on reproductive success. Our study expands the management toolbox of appropriate C&R practices that promote conservation of salmon populations and limit negative impacts on mating and reproductive success.     

A global assessment of salmon aquaculture impacts on wild salmonids

Since the late 1980s, wild salmon catch and abundance have declined dramatically in the North Atlantic and in much of the northeastern Pacific south of Alaska. In these areas, there has been a concomitant increase in the production of farmed salmon. Previous studies have shown negative impacts on wild salmonids, but these results have been difficult to translate into predictions of change in wild population survival and abundance. We compared marine survival of salmonids in areas with salmon farming to adjacent areas without farms in Scotland, Ireland, Atlantic Canada, and Pacific Canada to estimate changes in marine survival concurrent with the growth of salmon aquaculture. Through a meta-analysis of existing data, we show a reduction in survival or abundance of Atlantic salmon; sea trout; and pink, chum, and coho salmon in association with increased production of farmed salmon. In many cases, these reductions in survival or abundance are greater than 50%. Meta-analytic estimates of the mean effect are significant and negative, suggesting that salmon farming has reduced survival of wild salmon and trout in many populations and countries.     

Carcass analogues provide marine subsidies for macroinvertebrates and juvenile Atlantic salmon in temperate oligotrophic streams

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MHC polymorphism and disease resistance in Atlantic salmon (<Emphasis Type="Italic">Salmo salar</Emphasis>); facing pathogens with single expressed major histocompatibility class I and class II loci

Few studies have yet addressed the functional aspects of MHC molecules in fish. To lay the foundation for this, we evaluated the association between disease resistance and MHC class I and class II polymorphism in Atlantic salmon. Standardized disease challenge trials were performed on a semi-wild Atlantic salmon population with subsequent MHC typing and statistical analysis. The pathogens employed were infectious salmon anaemia virus (ISAV) causing infectious salmon anaemia and the Aeromonas salmonicida bacteria causing furunculosis. The material consisted of 1,182 Atlantic salmon from 33 families challenged with A. salmonicida and 1,031 Atlantic salmon from 25 families challenged with ISAV. We found highly significant associations between resistance towards infectious diseases caused by both pathogens and MH class I and class II polymorphism in Atlantic salmon. The observed associations were detected due to independently segregating MH class I and class II single loci, and inclusion of a large number of fish allowing an extensive statistical analysis.     

Genomewide single nucleotide polymorphism discovery in Atlantic salmon (Salmo salar): validation in wild and farmed American and European populations

A considerable number of single nucleotide polymorphisms (SNPs) are required to elucidate genotype–phenotype associations and determine the molecular basis of important traits. In this work, we carried out de novo SNP discovery accounting for both genome duplication and genetic variation from American and European salmon populations. A total of 9 736 473 nonredundant SNPs were identified across a set of 20 fish by whole‐genome sequencing. After applying six bioinformatic filtering steps, 200 K SNPs were selected to develop an Affymetrix Axiom^® myDesign Custom Array. This array was used to genotype 480 fish representing wild and farmed salmon from Europe, North America and Chile. A total of 159 099 (79.6%) SNPs were validated as high quality based on clustering properties. A total of 151 509 validated SNPs showed a unique position in the genome. When comparing these SNPs against 238 572 markers currently available in two other Atlantic salmon arrays, only 4.6% of the SNP overlapped with the panel developed in this study. This novel high‐density SNP panel will be very useful for the dissection of economically and ecologically relevant traits, enhancing breeding programmes through genomic selection as well as supporting genetic studies in both wild and farmed populations of Atlantic salmon using high‐resolution genomewide information.     

Primers for sequence characterization and polymorphism detection in the Atlantic salmon (Salmo salar) growth hormone 1 (GH1) gene

We report the identification of intraspecific sequence variation in the Atlantic salmon (Salmo salar) growth hormone 1 gene. Rapid and inexpensive assays for polymorphism detection were developed for 10 sites. Five of the assays detected single nucleotide polymorphisms (SNPs) using polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP) analyses, and five were indel polymorphisms, detected using fragment length analyses. The average within population frequency of the most common allele varied from 0.52 to 0.90, and the average within population heterozygosity varied from 0.02 to 0.37 in seven European salmon populations.     

Spatial synchrony in the response of a long range migratory species (Salmo salar) to climate change in the North Atlantic Ocean

A major challenge in understanding the response of populations to climate change is to separate the effects of local drivers acting independently on specific populations, from the effects of global drivers that impact multiple populations simultaneously and thereby synchronize their dynamics. We investigated the environmental drivers and the demographic mechanisms of the widespread decline in marine survival rates of Atlantic salmon (Salmo salar) over the last four decades. We developed a hierarchical Bayesian life cycle model to quantify the spatial synchrony in the marine survival of 13 large groups of populations (called stock units, SU) from two continental stock groups (CSG) in North America (NA) and Southern Europe (SE) over the period 1971–2014. We found strong coherence in the temporal variation in postsmolt marine survival among the 13 SU of NA and SE. A common North Atlantic trend explains 37% of the temporal variability of the survivals for the 13 SU and declines by a factor of 1.8 over the 1971–2014 time series. Synchrony in survival trends is stronger between SU within each CSG. The common trends at the scale of NA and SE capture 60% and 42% of the total variance of temporal variations, respectively. Temporal variations of the postsmolt survival are best explained by the temporal variations of sea surface temperature (SST, negative correlation) and net primary production indices (PP, positive correlation) encountered by salmon in common domains during their marine migration. Specifically, in the Labrador Sea/Grand Banks for populations from NA, 26% and 24% of variance is captured by SST and PP, respectively and in the Norwegian Sea for populations from SE, 21% and 12% of variance is captured by SST and PP, respectively. The findings support the hypothesis of a response of salmon populations to large climate‐induced changes in the North Atlantic simultaneously impacting populations from distant continental habitats.     

Population and size-specific distribution of Atlantic salmon Salmo salar in the Baltic Sea over five decades

Population-specific assessment and management of anadromous fish at sea requires detailed information about the distribution at sea over ontogeny for each population. However, despite a long history of mixed-stock sea fisheries on Atlantic salmon, Salmo salar, migration studies showing that some salmon populations feed in different regions of the Baltic Sea and variation in dynamics occurs among populations feeding in the Baltic Sea, such information is often lacking. Also, current assessment of Baltic salmon assumes equal distribution at sea and therefore equal responses to changes in off-shore sea fisheries. Here, we test for differences in distribution at sea among and within ten Atlantic salmon Salmo salar populations originating from ten river-specific hatcheries along the Swedish Baltic Sea coast, using individual data from >125,000 tagged salmon, recaptured over five decades. We show strong population and size-specific differences in distribution at sea, varying between year classes and between individuals within year classes. This suggests that Atlantic salmon in the Baltic Sea experience great variation in environmental conditions and exploitation rates over ontogeny depending on origin and that current assessment assumptions about equal exploitation rates in the offshore fisheries and a shared environment at sea are not valid. Thus, our results provide additional arguments and necessary information for implementing population-specific management of salmon, also when targeting life stages at sea.     

Reproductive Strategies Explain Genetic Diversity in Atlantic Salmon, Salmo salar

Synopsis We investigated the relationship between conservation status and genetic variability in European and North American Atlantic salmon, Salmo salar, populations, many of which have suffered severe bottlenecks. A negative north--south cline exists for the status of population conservation in this species. A literature review of genetic variability and demographic parameters of wild Atlantic salmon populations resulted in no statistical associations between population conservation status and genetic variation at enzyme or VNTR loci. We found however, a negative relationship between male parr maturation rates and geographical latitude for both American and European populations. The increase in effective population size due to participation by mature male parr and the increased proportions of these males in smaller (southern) populations could explain the lack of expected relationship between genetic variation and conservation status.     

Analysis of Correlation between Body Length and Genetic Polymorphism for Loci ESTD-1 and IDHP-3 in the Atlantic Salmon Salmo salar

Correlation between body length and characteristics of genetic polymorphism for loci Me-2, IDHP-3, ESTD-1, and AAT-2 were studied in the Atlantic salmon Salmo salar. The study was based on data on genetic variation in more than 4000 fish grown at the Kandalaksha Hatchery. Of four loci studied, loci ESTD-1 and IDHP-3 were distinguished by the fact that they can be confidently considered body-length markers in the Atlantic salmon. Analysis of mean locus heterozygosity indicates a disturbance of the mechanism of negative heterosis that is characteristic of natural populations. This presumably reflects a change in the genetic diversity of the Atlantic salmon under the influence of breeding.     

Divergent trends in anadromous salmonid populations in Norwegian and Scottish rivers

The Atlantic salmon (Salmo salar) is a charismatic anadromous fish of high conservation and economic value. Concerns have been expressed regarding the long-term viability of fisheries throughout the species''s distributional range because of abundance variations that cannot currently be explained or predicted. Here, we analyse long-term catch data obtained over a wide geographical range and across a range of spatial subscales to understand more fully the factors that drive population abundance. We use rod catch data from 84 Norwegian rivers over 125 years (1876–2000) and 48 Scottish rivers over 51 years (1952–2002). The temporal correlation in catches is very long-term, with trends persisting over several decades. The spatial correlation is relatively short-range, indicating strong local-scale effects on catch. Furthermore, Scottish salmon populations exhibit recent negative trends in contrast to some more positive trends in Norway—especially in the north.     

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.     

Adaptive and Neutral Genetic Variation and Colonization History of Atlantic Salmon, Salmo salar

Synopsis I combined neutral microsatellite markers with the major histocompatibility complex (MHC) class IIB to study genetic differentiation and colonization history in Atlantic salmon, Salmo salar, in the Baltic Sea and in the north-eastern Atlantic. Baltic salmon populations have lower levels of microsatellite genetic variation, in terms of heterozygosity and allelic richness than Atlantic populations, confirming earlier findings with other genetic markers, suggesting that the Baltic Sea populations have been exposed to genetic bottlenecks, most likely at a founding event. On the other hand, the level of MHC variation was similar in the Baltic and in the north-eastern Atlantic, indicating that positive balancing selection has increased the level of MHC-variation. Both microsatellite and MHC class IIB genetic variation give strong support to the hypothesis that the Baltic salmon are of a biphyletic origin, the southern population in this study is strongly differentiated from both the northern Baltic salmon populations and from the north-eastern Atlantic populations. Salmon may have colonized the northern Baltic Sea either from the south, via the so called “N?rke strait” or from the north, via a proposed historical connection between the White Sea and the northern Baltic. At microsatellites, no significant isolation-by distance was found at either colonization route. At the MHC, populations were significantly isolated by distance when assuming that colonization occurred via the “N?rke strait”.     

Stable isotope analyses of otoliths in identification of hatchery origin of Atlantic salmon (Salmo salar) in Maine

We conducted stable oxygen and carbon isotope analyses for otoliths of Atlantic salmon (Salmo salar), in an attempt to develop a reference database on isotopic variability among private and federal hatcheries in Maine which currently support the salmon aquaculture industry and recovery of endangered populations. During the first phase of our study, we collected 40–50 sagittal otoliths of juvenile Atlantic salmon from each of the five hatcheries and analyzed for stable oxygen and carbon isotope ratios (¹⁸O/¹⁶O or δ¹⁸O, and ¹³C/¹²C or δ¹³C). Combination of δ¹⁸O and δ¹³C signatures in otoliths showed that the five hatcheries can be clearly separated and chemically distinguished. By identifying stable isotopic variations of otoliths from different hatchery settings, we were able to establish some isotopic criteria or standards to assign a likelihood that an individual Atlantic salmon came from a specific hatchery within the reference database. If successful, a diagnostic tool that can provide definitive information on identification of the hatchery origin could serve as a novel marking technique, and the chemical method may provide a more effective alternative to DNA analysis for mixed stocks. Overall our isotopic data from otoliths support the hypothesis that there are detectable differences between the five hatcheries, and multiple statistical analyses indicated that we can correctly distinguish individual Atlantic salmon into a hatchery with high confidence.