Standardising multi-laboratory microsatellite data in Pacific salmon: an historical view of the future

Abstract –  For at least 15 years, multiple Pacific Rim Laboratories have cooperated to standardise the collection of Pacific salmon genetic data. For species such as Chinook salmon and chum salmon, allozyme electrophoretic data sets now include hundreds of populations sampled over multiple years throughout the north Pacific. More recently, microsatellite DNA markers have emerged as a new cornerstone of Pacific salmon genetic research. The allozyme experience provides at least two important lessons regarding shared, standardised databases. First, interlaboratory standardisation is sufficiently costly and time consuming that little progress is typically made in the absence of specific fishery management and conservation needs; thus immediate needs will direct future standardisation. Secondly, justified or not, there are significant concerns regarding intellectual propriety and other perceived privileges associated with unpublished genetic data that are shared among laboratories. This article describes challenges to genetic standardisation relative to new research goals, along with specific suggestions for meeting those challenges.     

Effects of the North Pacific Current on the productivity of 163 Pacific salmon stocks

Horizontal ocean transport can influence the dynamics of higher‐trophic‐level species in coastal ecosystems by altering either physical oceanographic conditions or the advection of food resources into coastal areas. In this study, we investigated whether variability in two North Pacific Current (NPC) indices was associated with changes in productivity of North American Pacific salmon stocks. Specifically, we used Bayesian hierarchical models to estimate the effects of the north‐south location of the NPC bifurcation (BI) and the NPC strength, indexed by the North Pacific Gyre Oscillation (NPGO), on the productivity of 163 pink, chum, and sockeye salmon stocks. We found that for salmon stocks located in Washington (WA) and British Columbia (BC), both the BI and NPGO had significant positive effects on productivity, indicating that a northward‐shifted bifurcation and a stronger NPC are associated with increased salmon productivity. For the WA and BC regions, the estimated NPGO effect was over two times larger than the BI effect for pink and chum salmon, whereas for sockeye salmon the BI effect was 2.4 times higher than the NPGO. In contrast to WA and BC stocks, we found weak effects of both horizontal ocean transport processes on the productivity of salmon stocks in Alaska. Our results indicated that horizontal transport pathways might strongly influence population dynamics of Pacific salmon in the southern part of their North American ranges, but not the northern part, suggesting that different environmental pathways may underlie changes in salmon productivity in northern and southern areas for the species under consideration.     

Distribution and feeding of juvenile Pacific salmon in freshwater tidal creeks of the lower Fraser River, British Columbia

Abstract This study examined juvenile salmonid use of a freshwater tidal creek system draining a wetland on the floodplain of the lower Fraser River, British Columbia, Canada. Chum, Oncorhynchus keta (Walbaum), chinook, O. tshawytscha (Walbaum), and sockeye, O. nerka (Walbaum), salmon fry were abundant in the tidal creeks in spring. The fry were found in non-natal habitat up to 1.5 km from the main channel of the river. The salmon fry ate dipteran adults, larvae and pupae, cyclopoid and harpacticoid copepods, and Collembola. Mysids Neomysis mercedis Holmes (Walbaum), and amphipods, Crangonyx richmondensis occidentalis (Hubricht and Harrison), were also consumed. The upper reaches of an undisturbed creek were the winter rearing habitat for presmolt coho salmon, O. kisutch (Walbaum), where this species ate dipteran pupae and larvae as well as a freshwater isopod, Asellus communis Say (Walbaum).     

The optimal stability `window': a mechanism underlying decadal fluctuations in North Pacific salmon stocks?

While recent evidence suggests that North Pacific salmon stocks are influenced by decadal variability in atmospheric forcing of the ocean, the actual combination of physical and biological processes that determines this linkage has not been identified. This paper describes a possible scenario in which water column stability is the primary factor by which the physical environment influences phytoplankton production, the basis for production at higher trophic levels. Variation in the strength of the wintertime Aleutian Low pressure area affects water column stabilities, hence primary production, along the entire eastern boundary of the North Pacific. The `optimal stability window' explains the qualitative relationship between fish stocks and the strength of the winter Aleutian Low, as well as the observed out-of-phase variation between northern and southern salmon stocks.     

Change in chum salmon (Oncorhynchus keta) stomach contents associated with fluctuation of pink salmon (O. gorbuscha) abundance in the central subarctic Pacific and Bering Sea

The abundance and stomach contents of salmonids (Oncorhynchus spp.) and the biomass of prey organisms were examined in the central subarctic Pacific and Bering Sea in the summer of 1991 and 1992. Salmonids were caught by surface longline using the same level of fishing effort. Chum (O. keta) and pink (O. gorbuscha) salmon were the predominant species, representing 44% and 36% sof the total catch (n = 1275) in 1991. In 1992, chum salmon composed 85% of the total catch (n = 603), but the catch of pink salmon decreased to 1% of the total catch due to the odd/even year fluctuation of Asian pink salmon abundance in the study area. It was found that chum salmon changed their dominant diet from gelatinous zooplankton (pteropods, appendicular-ians, jellyfishes, chaetognaths, polychaetes and unidentified materials) in 1991, when pink salmon were abundant, to a diet of crustaceans (euphausiids, cope-pods, amphipods, ostracods, mysids and decapods) in 1992, when pink salmon were less abundant. Local crustacean biomass (wet weight; mg m^-3) had significant negative correlation with the CPUE (catch number per 30 hachi) of pink salmon in 1991 (r = -0.586; P = 0.026) and that of chum salmon in 1992 (r =–0.616; P = 0.014). There may be a limitation in the available prey resource for production of salmonids.     

Relative resistance of Pacific salmon to infectious salmon anaemia virus

Infectious salmon anaemia (ISA) is a major disease of Atlantic salmon, Salmo salar, caused by an orthomyxovirus (ISAV). Increases in global aquaculture and the international movement of fish made it important to determine if Pacific salmon are at risk. Steelhead trout, Oncorhynchus mykiss, and chum, O. keta, Chinook, O. tshawytscha, coho, O. kisutch, and Atlantic salmon were injected intraperitoneally with a high, medium, or low dose of a Norwegian strain of ISAV. In a second challenge, the same species, except chum salmon, were injected with a high dose of either a Canadian or the Norwegian strain. Average cumulative mortality of Atlantic salmon in trial 1 was 12% in the high dose group, 20% in the medium dose group and 16% in the low dose group. The average cumulative mortality of Atlantic salmon in trial 2 was 98%. No signs typical of ISA and no ISAV-related mortality occurred among any of the groups of Oncorhynchus spp. in either experiment, although ISAV was reisolated from some fish sampled at intervals post-challenge. The results indicate that while Oncorhynchus spp. are quite resistant to ISAV relative to Atlantic salmon, the potential for ISAV to adapt to Oncorhynchus spp. should not be ignored.     

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.     

Pacific hake (Merluccius productus Ayres, 1855) hydrolysates as feed attractants for juvenile Chinook salmon (Oncorhynchus tshawytscha Walbaum, 1792)

Soybean meal (SBM) inclusion in salmonid diets can lower feed cost, but dramatically reduces growth and feed utilization, and increases mortality in juvenile chinook salmon Oncorhynchus tshawytscha, due to diminished diet palatability and/or other adverse physiological effects exerted by antinutritional factors in SBM. The objective of this study was to investigate whether commercial Antarctic krill meal Euphausia superba or hydrolysates enzymatically produced from Pacific hake Merluccius productus could reverse the negative palatability effects of SBM inclusion in juvenile chinook salmon diets. Diets without SBM or with SBM and no added feed attractant were used as positive and negative control diets respectively. Incorporation of 2% krill meal or Alcalase^®‐produced hydrolysates into SBM‐containing diets (20% of dry matter by isonitrogenous replacement of fishmeal) significantly (P < 0.05) increased feed intake, feed utilization, fish weight gain and thermal growth coefficient during a 5‐week trial. Nevertheless, the negative effects on fish performance incurred by dietary inclusion of 20% SBM could not be fully reversed, indicating that most of those effects were likely unrelated to palatability. This study demonstrates the potential for using Pacific hake hydrolysates as a dietary feed attractant for salmonid diets, and supports the need for further research to optimize its application for ideal fish performance.     

Prospects for the future of pink salmon in three oceans: From the native Pacific to the novel Arctic and Atlantic

While populations of other migratory salmonids suffer in the Anthropocene, pink salmon (Oncorhynchus gorbusca Salmonidae) are thriving, and their distribution is expanding both within their natural range and in the Atlantic and Arctic following introduction of the species to the White Sea in the 1950s. Pink salmon are now rapidly spreading in Europe and even across the ocean to North America. Large numbers of pink salmon breed in Norwegian rivers and small numbers of individuals have been captured throughout the North Atlantic since 2017. Although little is known about the biology and ecology of the pink salmon in its novel distribution, the impacts of the species' introduction are potentially highly significant for native species and watershed productivity. Contrasts between pink salmon in the native and extended ranges will be key to navigating management strategies for Atlantic nations where the pink salmon is entrenching itself among the fish fauna, posing potential threats to native fish communities. One key conclusion of this paper is that the species' heritable traits are rapidly selected and drive local adaptation and evolution. Within the Atlantic region, this may facilitate further establishment and spread. The invasion of pink salmon in the Atlantic basin is ultimately a massive ecological experiment and one of the first examples of a major faunal change in the North Atlantic Ocean that is already undergoing rapid changes due to other anthropogenic stressors. New research is urgently needed to understand the role and potential future impacts of pink salmon in Atlantic ecosystems.     

Fecundity trends of Chinook salmon in the Pacific Northwest

Fecundity is an important demographic parameter that contributes to the productivity of anadromous fish stock dynamics. Yet, studies on fecundity patterns in Pacific salmon (Oncorhynchus spp.) often only include a few years of data, limiting our ability to understand spatio-temporal trends. Here, we used data on 43 hatchery Chinook salmon (O. tshawytscha, Salmonidae) populations in Washington State to evaluate whether average fecundity changed over the past three decades. We then used data from a subset of stocks (18) to evaluate the relationship between fecundity and body length. Our results revealed significant changes in fecundity across the 25-year study period with most stocks showing declines in fecundity over the past decade. Results further showed that Chinook salmon have decreased in length over this same period and that annual variation in mean length explains a majority (62%) of annual variation in mean fecundity. Specifically, we estimated that a 1-mm reduction in length results in 7.8 fewer eggs (95% CI = 6.6–8.9). Given that the majority of Pacific Northwest Chinook salmon in the environment and harvested in fisheries originate from hatchery releases and that nearby hatchery and wild populations generally have similar ocean distributions, these results likely reflect patterns for many populations not included. Combined, our results highlight the need to consider changes in body size and egg production when assessing the dynamics of anadromous fish populations and designing management or conservation plans, particularly for depressed populations.     

Competition between Asian pink salmon (Oncorhynchus gorbuscha) and Alaskan sockeye salmon (O. nerka) in the North Pacific Ocean

The importance of interspecific competition as a mechanism regulating population abundance in offshore marine communities is largely unknown. We evaluated offshore competition between Asian pink salmon and Bristol Bay (Alaska) sockeye salmon, which intermingle in the North Pacific Ocean and Bering Sea, using the unique biennial abundance cycle of Asian pink salmon from 1955 to 2000. Sockeye salmon growth during the second and third growing seasons at sea, as determined by scale measurements, declined significantly in odd‐numbered years, corresponding to years when Asian pink salmon are most abundant. Bristol Bay sockeye salmon do not interact with Asian pink salmon during their first summer and fall seasons and no difference in first year scale growth was detected. The interaction with odd‐year pink salmon led to significantly smaller size at age of adult sockeye salmon, especially among younger female salmon. Examination of sockeye salmon smolt to adult survival rates during 1977–97 indicated that smolts entering the ocean during even‐numbered years and interacting with abundant odd‐year pink salmon during the following year experienced 26% (age‐2 smolt) to 45% (age‐1 smolt) lower survival compared with smolts migrating during odd‐numbered years. Adult sockeye salmon returning to Bristol Bay from even‐year smolt migrations were 22% less abundant (reduced by 5.9 million fish per year) compared with returns from odd‐year migrations. The greatest reduction in adult returns occurred among adults spending 2 compared with 3 years at sea. Our new evidence for interspecific competition highlights the need for multispecies, international management of salmon production, including salmon released from hatcheries into the ocean.     

Multi‐timescale interactions between pink and chum salmon catch per unit effort in the Bering Sea

Based on generalized linear models, interspecific interactions were identified between chum and pink salmon. In addition, the effects of sea surface temperature and location on the variability of catch per unit effort (CPUE) of chum salmon from gill‐net surveys carried out between 1972 and 2010 were investigated. In the optimal model, interspecific interactions between CPUEs of chum and pink salmon on a year scale were positive for approximately half of all years in the central Bering Sea. In addition, interspecific interactions on a multi‐year scale were positive in even‐numbered years. The effects of location on the CPUE of chum salmon were significant variables in the optimal model. The CPUEs of chum salmon located near the continental shelf in the Bering Sea were higher than those of other locations. This study provides new evidence of positive interspecific interactions between the CPUEs of chum and pink salmon. The results also suggest that the standardized CPUE of chum salmon from the gill‐net surveys reflects relative chum salmon abundance in the North Pacific Ocean in the following year.     

Steroidogenic capacity of coho salmon ovarian follicles throughout the periovulatory period

Coho salmon follicles obtained at various times throughout the periovulatory period were incubatedin vitro with graded amounts of partially purified salmon gonadotropin (SG-G100) for 24 h and the amounts of 17β-estradiol, testosterone and 17α20β dihydroxy-4-pregnen-3-one (17α20βP) released into the media determined by radioimmunoassay. By this approach, the pattern of steroid secretion by ovarian follicles was shown to change in relation to the developmental status of the oocyte. Full-grown immature follicles produced large amounts of 17β-estradiol but negligible amounts of testosterone and 17α20βP. Both basal and gonadotropin-stimulated 17β-estradiol production was subsequently reduced with advancing oocyte development. In contrast, the production of testosterone and 17α20βP increased during the course of ovarian development with testosterone production highest in follicles with a peripheral germinal vesicle and 17α20βP production highest in matured and postovulatory follicles. These data are discussed in relation to information on the preovulatory changes in circulating levels of steriod hormones in salmonids.     

δ13C-δ15N values as indicators of trophic position and competitive overlap for Pacific salmon (Oncorhynchus spp.)

Analysis of δ¹³C and δ¹⁵N isotope values for five species of Pacific salmon indicate that they form a trophic hierarchy on the high seas. On the basis of an analysis of these stable isotope ratios, chinook salmon feed at the upper end of the food chain and pink salmon at the lower end, in the sequence pink → sockeye → coho → chinook, with chinook and pink salmon separated by ca. 0.8 of a trophic level. Chum salmon occupy a peculiar position, with low δ¹³C values and high δ¹⁵N values, possibly reflecting an unusual diet that includes large amounts of gelatinous zooplankton (salps, ctenophoi;s, and medusae). Chum appear to occupy a unique trophic position, at a trophic level nearly as high as that of chinook but at the end of a different branch of the food chain. If true, the potential for trophodynamic competition with other salmon species is small. Our results suggest that the greatest potential for trophodynamic competition occurs within the pink-sockeye-coho grouping. A similar analysis, restricted to five stocks of North American sockeye, shows that four widely separated stocks have similar heavy isotope compositions but that the separation between these stocks is still statistically significant. The Chilko stock is strikingly different, however, suggesting that it is located in the central Gulf of Alaska, a region of intense upwelling. Circumstantial evidence supporting the possibility that the Chilko and other sockeye stocks are geographically separated within the Gulf of Alaska is reviewed.     

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.     

Early ocean distribution of juvenile Chinook salmon in an upwelling ecosystem

Extreme variability in abundance of California salmon populations is often ascribed to ocean conditions, yet relatively little is known about their marine life history. To investigate which ocean conditions influence their distribution and abundance, we surveyed juvenile Chinook salmon (Oncorhynchus tshawytscha) within the California Current (central California [37°30′N) to Newport, Oregon (44°00′N]) for a 2‐week period over three summers (2010–2012). At each station, we measured chlorophyll‐a as an indicator of primary productivity, acoustic‐based metrics of zooplankton density as an indicator of potential prey availability and physical characteristics such as bottom depth, temperature and salinity. We also measured fork lengths and collected genetic samples from each salmon that was caught. Genetic stock identification revealed that the majority of juvenile salmon were from the Central Valley and the Klamath Basin (91–98%). We constructed generalized logistic‐linear negative binomial hurdle models and chose the best model(s) using Akaike's Information Criterion (AIC) to determine which covariates influenced the salmon presence and, at locations where salmon were present, determined the variables that influenced their abundance. The probability of salmon presence was highest in shallower waters with a high chlorophyll‐a concentration and close to an individual's natal river. Catch abundance was primarily influenced by year, mean fork length and proximity to natal rivers. At the scale of sampling stations, presence and abundance were not related to acoustic indices of zooplankton density. In the weeks to months after ocean entry, California's juvenile Chinook salmon population appears to be primarily constrained to coastal waters near natal river outlets.     

From Atlantic to Pacific: Price links in the US wild and farmed salmon market

Abstract

In 1990, the US International Trade Commission stated that Atlantic and Pacific salmon species did not share a substitute relationship in any of the product forms. This result is contrary to economic demand studies that show a substitute relationship for Atlantic and Pacific salmon species. Time‐series results reported in this paper are consistent with the earlier demand studies and show evidence of an equilibrium price system that includes Atlantic, chinook and coho salmon species for the US market. For these three salmon species a substitute relationship cannot be rejected. However, we observe only weak price links across the three different species in the different US regional markets.     

Spatial variations in feeding and condition of juvenile pink and chum salmon off Vancouver Island, British Columbia

Spatial variations in feeding and condition of juvenile pink (Oncorhynchus gorbuscha) and chum (Oncorhynchus keta) salmon, and their implications for growth, were examined on the Vancouver Island continental shelf in early summer 1992. Juvenile pink salmon off northern Vancouver Island had more material in their stomachs, were in better condition, and had higher potential growth rates (from a bioenergetics model) than pink salmon off southern Vancouver Island. These variations were consistent with spatial differences in zoo-plankton biomass, there being more plankton in the northern region. There was a significant positive relationship between condition of pinks and the amount of material in their stomachs, suggesting a positive feedback on feeding success. Juvenile chum in the north also had more material in their stomachs than chum to the south. However, condition factor was not significantly different between southern and northern regions nor was there a significant relationship between condition factor and the weight of stomach contents for chum on the southern shelf. A bioenergetics model suggests that chum in the south were food limited. Stable carbon isotope data also indicated different feeding histories for some chum in the southern region, which may have been recent migrants onto the continental shelf from near-shore areas, or possibly a nearby hatchery. Estimation of the energy required by juvenile salmon to migrate north in a continental shelf area with low zooplankton biomass and a weak northerly current (inner shelf), compared with an area with higher zooplankton biomass but a strong southerly current (outer shelf), indicated sufficient surplus energy only in the inner shelf, consistent with observations of northward migrations predominantly through this area. Spatial variations in current velocity and zooplankton biomass can affect feeding, condition, and potential growth of juvenile pink and chum salmon off Vancouver Island.     

Body size trends along vertical and thermal gradients of chum salmon in the Bering Sea during summer

Relationships between the vertical distribution and thermal habitat, and body size of chum salmon Oncorhynchus keta were studied in the Bering Sea in summer using trawl surveys at various depths. Chum salmon abundance decreased with increasing depth, but the patterns of decrease differed between size groups. The abundance of small salmon fell rapidly with depth, whereas that of large salmon decreased gradually to 40 m depth, and abruptly below that. The average fork length of chum salmon collected from each trawl correlated positively with trawl net depth and negatively with water temperature. Since the optimal temperature for growth decreases with body size in this species, the observed body size‐related vertical habitat use by chum salmon may indicate size‐dependent thermal preferences.