Development of a Piscirickettsia salmonis immersion challenge model to investigate the comparative susceptibility of three salmon species

BackgroundSalmon species vary in susceptibility to infections with the salmon louse (Lepeophtheirus salmonis). Comparing mechanisms underlying responses in susceptible and resistant species is important for estimating impacts of infections on wild salmon, selective breeding of farmed salmon, and expanding our knowledge of fish immune responses to ectoparasites. Herein we report three L. salmonis experimental infection trials of co-habited Atlantic Salmo salar, chum Oncorhynchus keta and pink salmon O. gorbuscha, profiling hematocrit, blood cortisol concentrations, and transcriptomic responses of the anterior kidney and skin to the infection.ResultsIn all trials, infection densities (lice per host weight (g)) were consistently highest on chum salmon, followed by Atlantic salmon, and lowest in pink salmon. At 43 days post-exposure, all lice had developed to motile stages, and infection density was uniformly low among species. Hematocrit was reduced in infected Atlantic and chum salmon, and cortisol was elevated in infected chum salmon. Systemic transcriptomic responses were profiled in all species and large differences in response functions were identified between Atlantic and Pacific (chum and pink) salmon. Pink and chum salmon up-regulated acute phase response genes, including complement and coagulation components, and down-regulated antiviral immune genes. The pink salmon response involved the largest and most diverse iron sequestration and homeostasis mechanisms. Pattern recognition receptors were up-regulated in all species but the active components were often species-specific. C-type lectin domain family 4 member M and acidic mammalian chitinase were specifically up-regulated in the resistant pink salmon.ConclusionsExperimental exposures consistently indicated increased susceptibility in chum and Atlantic salmon, and resistance in pink salmon, with differences in infection density occurring within the first three days of infection. Transcriptomic analysis suggested candidate resistance functions including local inflammation with cytokines, specific innate pattern recognition receptors, and iron homeostasis. Suppressed antiviral immunity in both susceptible and resistant species indicates the importance of future work investigating co-infections of viral pathogens and lice.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-200) contains supplementary material, which is available to authorized users.

Fraser River Pacific salmon have declined in recent decades, possibly from parasitism by sea lice (Caligus clemensi and Lepeophtheirus salmonis). We describe the abundance of both louse species infesting co-migrating juvenile pink (Oncorhynchus gorbuscha), chum (Oncorhynchus keta), and sockeye (Oncorhynchus nerka) salmon over 5 years in the Discovery Islands and Johnstone Strait, British Columbia. The generalist louse, C. clemensi, was 5, 7, and 39 times more abundant than the salmonid specialist, L. salmonis, on pink, chum, and sockeye salmon, respectively. Caligus clemensi abundance was higher on pink salmon (0.45, 95% CI: 0.38–0.55) and sockeye (0.39, 95% CI: 0.33–0.47) than on chum salmon. Lepeophtheirus salmonis abundance was highest on pink salmon (0.09, 95% CI = 0.06–0.15). Caligus clemensi had higher abundances in Johnstone Strait than in the Discovery Islands. These results suggest differences in host specialization and transmission dynamics between louse species. Because both lice infest farmed salmon, but only C. clemensi infests Pacific herring (Clupea pallasii), conservation science and management regarding lice and Fraser River salmon should further consider C. clemensi and transmission from farmed salmon and wild herring.

Soybean meal-induced enteritis in Atlantic salmon (Salmo salar) and Chinook salmon (Oncorhynchus tshawytscha) but not in pink salmon (O. gorbuscha)

Sockeye salmon (Oncorhynchus nerka) populations from Southeast Alaska through British Columbia to Washington State have experienced similar declines in productivity over the past two decades, leading to economic and ecosystem concerns. Because the declines have spanned a wide geographic area, the primary mechanisms driving them likely operate at a large, multiregional scale at sea. However, identification of such mechanisms has remained elusive. Using hierarchical models of stock–recruitment dynamics, we tested the hypothesis that competition between pink (Oncorhynchus gorbuscha) and sockeye salmon for prey has led to reduced growth and productivity and delayed maturation of up to 36 sockeye populations spanning the region during the past 55 years. Our findings indicate the abundance of North Pacific pink salmon in the second year of sockeye life at sea is a key factor contributing to the decline of sockeye salmon productivity, including sockeye in the Fraser River where an increase from 200 to 400 million pink salmon is predicted to reduce sockeye recruitment by 39%. Additionally, length-at-age of Fraser River sockeye salmon declined with greater sockeye and pink salmon abundance, and age at maturity increased with greater pink salmon abundance. Our analyses provide evidence that interspecific competition for prey can affect growth, age, and survival of sockeye salmon at sea.

Some Pacific salmon populations have been experiencing increasingly warmer river temperatures during their once-in-a-lifetime spawning migration, which has been associated with en route and prespawn mortality. The mechanisms underlying such temperature-mediated mortality are poorly understood. Wild adult pink (Oncorhynchus gorbuscha) and sockeye (Oncorhynchus nerka) salmon were used in this study. The objectives were to investigate the effects of elevated water temperature on mortality, final maturation, and blood properties under controlled conditions that simulated a "cool" (13°C) and "warm" (19°C) freshwater spawning migration. After 10 d at 13°C, observed mortality was 50%-80% in all groups, which suggested that there was likely some mortality associated with handling and confinement. Observed mortality after 10 d at 19°C was higher, reaching ≥98% in male pink salmon and female pink and sockeye salmon. Thus, male sockeye salmon were the most thermally tolerant (54% observed mortality). Model selection supported the temperature- and sex-specific mortality patterns. The pink salmon were closer to reproductive maturation and farther along the senescence trajectory than sockeye salmon, which likely influenced their survival and physiological responses throughout the experiment. Females of both species held at 19°C had reduced plasma sex steroids compared with those held at 13°C, and female pink salmon were less likely to become fully mature at 19° than at 13°C. Male and female sockeye salmon held at 19°C had higher plasma chloride and osmolality than those held at 13°C, indicative of a thermally related stress response. These findings suggest that sex differences and proximity to reproductive maturity must be considered when predicting thermal tolerance and the magnitude of en route and prespawn mortality for Pacific salmon.

Size of salmon is of great importance to their value. In fisheries, body size affects the monetary and food value of the catch. On the spawning grounds, body size affects egg size, fecundity, and nutrient transport to natal locations from the ocean. Declines in body size have been reported for Chinook (Oncorhynchus tshawytscha), chum (O. keta), pink (O. gorbuscha) and sockeye (O. nerka) salmon in the eastern North Pacific Ocean (Losee et al. 2019; Oke et al. 2020) and have been linked to climate change and increased competition from pink and sockeye salmon (Connors et al. 2020; but see Neville and Beamish 2022). Over the same period of body size decline, salmon abundances in the North Pacific have been increasing (Ruggerone and Irvine 2018) while total biomass has remained stable since 1993, implying a carrying capacity limitation. Our goal was to show how body size in Fraser River sockeye and pink salmon has changed over time using data collected by the Pacific Salmon Commission (PSC), and to relate those changes in body size to estimates of salmon abundance in the North Pacific Ocean.

Little is known about the behaviour patterns and swimming speed strategies of anadromous upriver migrating fish. We used electromyogram telemetry to estimate instantaneous swimming speeds for individual sockeye (Oncorhynchus nerka) and pink salmon (O. gorbuscha) during their spawning migrations through reaches which spanned a gradient in river hydraulic features in the Fraser River, British Columbia. Our main objectives were to describe patterns of individual-specific swim speeds and behaviours, identify swimming speed strategies and contrast these between sexes, species and reaches. Although mean swimming speeds did not differ between pink salmon (2.21 BL s−1) and sockeye salmon (1.60 BL s−1), sockeye salmon were over twice as variable (mean CV; 54.78) in swimming speeds as pink salmon (mean CV; 22.54). Using laboratory-derived criteria, we classified swimming speeds as sustained ( 3.2 BL s−1). We found no differences between sexes or species in the proportion of total time swimming in these categories — sustained (0.76), prolonged (0.18), burst (0.06); numbers are based on species and sexes combined. Reaches with relatively complex hydraulics and fast surface currents had migrants with relatively high levels of swimming speed variation (e.g., high swimming speed CV, reduced proportions of sustained speeds, elevated proportions of burst speeds, and high rates of bursts) and high frequency of river crossings. We speculate that complex current patterns generated by river constrictions created confusing migration cues, which impeded a salmon’s ability to locate appropriate pathways.

In the warming Arctic, aquatic habitats are in flux and salmon are exploring their options. Adult Pacific salmon, including sockeye (Oncorhynchus nerka), coho (O. kisutch), Chinook (O. tshawytscha), pink (O. gorbuscha) and chum (O. keta) have been captured throughout the Arctic. Pink and chum salmon are the most common species found in the Arctic today. These species are less dependent on freshwater habitats as juveniles and grow quickly in marine habitats. Putative spawning populations are rare in the North American Arctic and limited to pink salmon in drainages north of Point Hope, Alaska, chum salmon spawning rivers draining to the northwestern Beaufort Sea, and small populations of chum and pink salmon in Canada’s Mackenzie River. Pacific salmon have colonized several large river basins draining to the Kara, Laptev and East Siberian seas in the Russian Arctic. These populations probably developed from hatchery supplementation efforts in the 1960’s. Hundreds of populations of Arctic Atlantic salmon (Salmo salar) are found in Russia, Norway and Finland. Atlantic salmon have extended their range eastward as far as the Kara Sea in central Russian. A small native population of Atlantic salmon is found in Canada’s Ungava Bay. The northern tip of Quebec seems to be an Atlantic salmon migration barrier for other North American stocks. Compatibility between life history requirements and ecological conditions are prerequisite for salmon colonizing Arctic habitats. Broad-scale predictive models of climate change in the Arctic give little information about feedback processes contributing to local conditions, especially in freshwater systems. This paper reviews the recent history of salmon in the Arctic and explores various patterns of climate change that may influence range expansions and future sustainability of salmon in Arctic habitats. A summary of the research needs that will allow informed expectation of further Arctic colonization by salmon is given.

The length and weight of Russian sockeye (Oncorhynchus nerka) returning to the Ozernaya River (Kamchatka) was substantially reduced in years when the ocean abundances of Kamchatkan pink (O. gorbuscha) and sockeye salmon were high. We found that the density‐dependent reduction in sockeye growth on a per‐capita basis was greater for sockeye than for pink salmon. However, the overall effect of pink salmon abundance on sockeye growth was greater because of the higher numerical abundance of pink salmon. The strongest statistical relationships were found for sockeye from separate age groups; pooled data combining all age classes were statistically insignificant. We estimate that, if pink salmon were absent, the most strongly affected age group of sockeye salmon (2.1 males) would weigh twice as much at maturity than if pink salmon populations from eastern and western Kamchatka were both simultaneously at peak observed abundances. Trophic competition in the ocean between pink and sockeye salmon can therefore have a significant influence on the productivity of sockeye populations for the most strongly affected age groups. These effects are large enough that they should be explicitly considered in the management of salmon populations.

BackgroundInfection with the myxozoan parasite Parvicapsula pseudobranchicola causes disease in wild and farmed salmonids in Norway. In the northeast Pacific Ocean, the parasite has been reported in Pacific salmon Oncorhynchus spp. without evidence of disease. The objectives of the present study were to confirm the identity of P. pseudobranchicola in the Pacific, document its host and geographic ranges, and describe associated pathological changes.MethodsOcean-entry year wild pink salmon Oncorhynchus gorbuscha, chum salmon O. keta, Chinook salmon O. tshawytscha, coho salmon O. kisutch and sockeye salmon O. nerka were collected in summer and autumn surveys near Vancouver Island (VI) and from a winter survey in the Gulf of Alaska. Samples were also obtained from farmed Atlantic salmon Salmo salar and Chinook salmon near VI. Samples were analysed by qPCR and histology using conventional staining or in situ hybridisation. Parasite sequence was obtained from small subunit ribosomal RNA gene (SSU rDNA).ResultsIdentical 1525 base-pair SSU rDNA sequences from infected pink salmon, chum salmon and Chinook salmon shared 99.93% identity with a P. pseudobranchicola sequence from Norwegian Atlantic salmon. In autumn surveys, the prevalence was greatest in chum salmon (91.8%) and pink salmon (85.9%) and less so in Chinook salmon (68.8%) and sockeye salmon (8.3%). In farmed salmon, the prevalence was zero in Atlantic salmon (n = 967) and 41% in Chinook salmon (n = 118). Infections were preferentially sited in pseudobranch and visualised by in situ hybridisation. Heavy parasite burdens in all species of Pacific salmon were inconsistently associated with focal granulomatous pseudobranchitis.ConclusionsIn the northeast Pacific, widespread occurrence of P. pseudobranchicola in Pacific salmon together with its absence or sporadic occurrence in farmed Atlantic salmon differs from its epidemiology in Norway, despite similar pathological development in the pseudobranch. Consequences of the infections to the health of wild Pacific salmon, identity of the invertebrate host and the distribution and abundance of infective actinospores are unknown and remain high priorities for research.Graphical

Spatiotemporal distributions and microhabitat use of pink salmon Oncorhynchus gorbuscha and sockeye salmon O. nerka were studied in Lake Creek, southeast Alaska, during three spawning seasons. Sockeye salmon migrated approximately 1 week earlier than pink salmon and spawned 250–350 m upstream from pink salmon. Habitat overlap measured with proportional similarity index monotonically increased with increasing spawner densities. Multidimensional niche spaces measured with water depth, current velocity, and channel gradient at redds were significantly different between pink and sockeye salmon (P < 0.005, Hotelling's T 2-test). However, classification of the redds into individual species was subjected to large error rates; 33% of 70 pink salmon redds and 34% of 125 sockeye salmon redds were misclassified. Competitive interaction between pink and sockeye salmon was not demonstrated.

Complex nature of long-term dynamics is revealed for thermal parameters of the pacific salmon habitat that includes a trend to warming and cyclic changes. Changes in annual landing of pink, chum and sockeye salmon have generally positive relationship to variations of the temperature background. Period of a full cycle in the dynamics of pink, chum, sockeye, coho, and chinook salmon abundance is about 80 years, with the cycles for pink, chum and sockeye salmon synchronous to those of temperature, the cycles for chinook salmon counter-phase them, and the variations in coho salmon abundance ahead those for pink, chum and sockeye salmon in 20–25 years and ahead those for chinook salmon in ~15 years. In the current cycle, the highest catches of mass species, as pink, chum and sockeye salmon, have been supposedly passed in the early 2020s, so the total annual catch of pacific salmon in Russia is expected to decline to the minimum in 2050s that would be higher than the previous minimum and provide a level of ~250 . 103 t. The individual weight of pacific salmon has a tendency to decrease in the modern times of warming climate. The loss of weight in the last 70–100 years is estimated in 60 % for chinook salmon and 30–35 % for chum, sockeye and coho salmon. Dynamics of the average individual weight for pink salmon is not determined by changes in environments, but depends on abundance of feeding individuals, especially for super-strong year-classes.

Embryo and alevin survival, time to hatching and emergence, and alevin and fry size of five species of Pacific salmon (Oncorhynchus) were observed at five incubation temperatures (2, 5, 8, 11, and 14 °C). No pink (Oncorhynchus gorbuscha) or chum (O. keta) salmon embryos survived to hatching at 2 °C. Coho (O. kisutch) and sockeye (O. nerka) salmon had higher embryo survival at 2 °C than chinook (O. tschawytscha) salmon. At 14 °C, chum, pink, and chinook salmon had higher embryo survival than coho or sockeye salmon. In all species, peaks of embryo mortality occurred at specific developmental stages (completion of epiboly, eye pigmentation, and hatching). Alevin survival to emergence was high for all species, except for coho and pink salmon at 14 °C. Hatching and emergence time varied inversely with incubation temperature, but coho salmon hatched and emerged sooner at all temperatures than the other species. Coho and sockeye salmon alevins were larger at 2 °C, pink, chum, and chinook salmon alevins were larger at 5 and 8 °C. Coho salmon fry were larger at 2 °C, chinook and chum salmon fry were larger at 5 °C, and sockeye and pink salmon fry were larger at 8 °C. High incubation temperatures reduced fry size in all species. Each species of Pacific salmon appears to be adapted to different spawning times and temperatures, and thus indirectly to specific incubation temperatures, to ensure maximum survival and size and to maintain emergence at the most favorable time each year.

Animals navigate using a variety of sensory cues, but how each is weighted during different phases of movement (e.g. dispersal, foraging, homing) is controversial. Here, we examine the geomagnetic and olfactory imprinting hypotheses of natal homing with datasets that recorded variation in the migratory routes of sockeye (Oncorhynchus nerka) and pink (Oncorhynchus gorbuscha) salmon returning from the Pacific Ocean to the Fraser River, British Columbia. Drift of the magnetic field (i.e. geomagnetic imprinting) uniquely accounted for 23.2% and 44.0% of the variation in migration routes for sockeye and pink salmon, respectively. Ocean circulation (i.e. olfactory imprinting) predicted 6.1% and 0.1% of the variation in sockeye and pink migration routes, respectively. Sea surface temperature (a variable influencing salmon distribution but not navigation, directly) accounted for 13.0% of the variation in sockeye migration but was unrelated to pink migration. These findings suggest that geomagnetic navigation plays an important role in long-distance homing in salmon and that consideration of navigation mechanisms can aid in the management of migratory fishes by better predicting movement patterns. Finally, given the diversity of animals that use the Earth's magnetic field for navigation, geomagnetic drift may provide a unifying explanation for spatio-temporal variation in the movement patterns of many species.

The growth rates of naturally sympatric juvenile pink Oncorhynchus gorbuscha and sockeye Oncorhynchus nerka salmon were compared in a common lacustrine environment in south‐west Alsaka, an unusual opportunity given the normal disparity in freshwater residence time of these two species. Fork length (LF) frequency distributions of juvenile pink salmon caught in the lake during the summer in 1991 and 1999–2003 indicated a growth rate of 0·54 mm day−1, 54% greater than the estimated growth rate of juvenile sockeye salmon sampled from 1958 to 2003 (0·35 mm day−1). Examination of daily growth rings on otoliths indicated that pink salmon in Lake Aleknagik grew an average of 1·34 mm day−1 in 2003 but sockeye salmon grew only 0·63 mm day−1(average specific growth rates were 3·0 and 1·8% day−1, respectively). Pink salmon increased from c. 32 mm LF and 0·2 g at emergence to 78 mm LF and 3·0 g within 3–4 weeks. After experiencing these rapid growth rates, the pink salmon appeared to leave the lake by late July in most years. The diets of pink and sockeye salmon in the littoral zone of the lake were very similar; &gt;80% of the stomach contents consisted of adult and pupal insects and the remainder was zooplankton. This high degree of diet overlap suggested that the observed differences in growth rate were not attributable to variation in prey composition.