Intestinal lesions and parasites associated with senescence and prespawn mortality in Chinook Salmon (Oncorhynchus tshawytscha).

Prespawn mortality (PSM) presents a major problem for the recovery of spring Chinook Salmon (Oncorhynchus tshawytscha) populations. In the Willamette River, Oregon, PSM exceeds 90% in some years but factors explaining it are not well understood. We examined intestinal tissue samples using histological slides from over 783 spring Chinook Salmon collected between 2009 and 2021, which included tissues from PSM fish, artificially spawned captive broodstock (BS) and normal river run fish, comprised of trapped (Live) and naturally post-spawned river (RPS) fish collected from the river. We observed degeneration of the intestinal epithelium and loss of villous structure, with concurrent severe enteritis. A natural progression of decline in epithelial integrity (EI) through the summer and fall until spawning and subsequent death was also observed. Live fish exhibited high EI scores (mean = 68%), BS exhibited variable EI scores (35%) and RPS exhibited severe loss of EI (14%). PSM fish exhibited prominent loss of intestinal epithelium with EI scores (13%), very similar to RPS fish, despite having been collected earlier in the year. Hence, we argue that low EI scores are strongly linked with PSM. Ceratonova shasta and Enterocytozoon schreckii were common in all groups, but neither were linked to either PSM or a decline in EI.

Ceratonova shasta: a cnidarian parasite of annelids and salmonids.

The myxozoan Ceratonova shasta was described from hatchery rainbow trout over 70 years ago. The parasite continues to cause severe disease in salmon and trout, and is recognized as a barrier to salmon recovery in some rivers. This review incorporates changes in our knowledge of the parasite's life cycle, taxonomy and biology and examines how this information has expanded our understanding of the interactions between C. shasta and its salmonid and annelid hosts, and how overarching environmental factors affect this host­parasite system. Development of molecular diagnostic techniques has allowed discrimination of differences in parasite genotypes, which have differing host affinities, and enabled the measurement of the spatio-temporal abundance of these different genotypes. Establishment of the C. shasta life cycle in the laboratory has enabled studies on host­parasite interactions and the availability of transcriptomic data has informed our understanding of parasite virulence factors and host defences. Together, these advances have informed the development of models and management actions to mitigate disease.

Spatiotemporal distribution of Ceratonova shasta in the lower Columbia River Basin and effects of exposure on survival of juvenile chum salmon Oncorhynchus keta.

In the Columbia River Basin (CRB), USA, anthropogenic factors ranging from dam construction to land use changes have modified riverine flow and temperature regimes and degraded salmon habitat. These factors are directly implicated in native salmon and steelhead (Oncorhynchus species) population declines and also indirectly cause mortality by altering outcomes of ecological interactions. For example, attenuated flows and warmer water temperatures drive increased parasite densities and in turn, overwhelm salmonid resistance thresholds, resulting in high disease and mortality. Outcomes of interactions between the freshwater myxozoan parasite, Ceratonova shasta, and its salmonid hosts (e.g., coho O. kisutch and Chinook salmon O. tshawytscha) are well-described, but less is known about effects on chum salmon O. keta, which have a comparatively brief freshwater residency. The goal of this study was to describe the distribution of C. shasta relative to chum salmon habitat in the CRB and assess its potential to cause mortality in juvenile chum salmon (listed as threatened in the CRB under the U.S. Endangered Species Act). We measured C. shasta densities in water samples collected from chum salmon habitat throughout the lower CRB during the period of juvenile chum salmon outmigration, 2018-2020. In 2019, we exposed caged chum salmon fry from two hatchery stocks at three C. shasta-positive sites to assess infection prevalence and survival. Results demonstrated: (1) C. shasta was detected in spawning streams from which chum salmon have been extirpated but was not detected in contemporary spawning habitat while juvenile chum salmon were present, (2) spatiotemporal overlap occurs between C. shasta and juvenile chum salmon in the Columbia River mainstem, and (3) low densities of C. shasta caused lethal infection in chum salmon fry from both hatchery stocks. Collectively, our results suggest C. shasta may limit recovery of chum salmon now and in the future.

Using a mechanistic framework to model the density of an aquatic parasite Ceratonova shasta.

Ceratonova shasta is a myxozoan parasite endemic to the Pacific Northwest of North America that is linked to low survival rates of juvenile salmonids in some watersheds such as the Klamath River basin. The density of C. shasta actinospores in the water column is typically highest in the spring (March-June), and directly influences infection rates for outmigrating juvenile salmonids. Current management approaches require quantities of C. shasta density to assess disease risk and estimate survival of juvenile salmonids. Therefore, we developed a model to simulate the density of waterborne C. shasta actinospores using a mechanistic framework based on abiotic drivers and informed by empirical data. The model quantified factors that describe the key features of parasite abundance during the period of juvenile salmon outmigration, including the week of initial detection (onset), seasonal pattern of spore density, and peak density of C. shasta. Spore onset was simulated by a bio-physical degree-day model using the timing of adult salmon spawning and accumulation of thermal units for parasite development. Normalized spore density was simulated by a quadratic regression model based on a parabolic thermal response with river water temperature. Peak spore density was simulated based on retained explanatory variables in a generalized linear model that included the prevalence of infection in hatchery-origin Chinook juveniles the previous year and the occurrence of flushing flows (≥171 m3/s). The final model performed well, closely matched the initial detections (onset) of spores, and explained inter-annual variations for most water years. Our C. shasta model has direct applications as a management tool to assess the impact of proposed flow regimes on the parasite, and it can be used for projecting the effects of alternative water management scenarios on disease-induced mortality of juvenile salmonids such as with an altered water temperature regime or with dam removal.

Effect of Nanophyetus salmincola and Bacterial Co-Infection on Mortality of Juvenile Chinook Salmon.

The freshwater trematode Nanophyetus salmincola has been demonstrated to impair salmonid immune function and resistance to the marine pathogen Vibrio anguillarum, potentially resulting in ocean mortality. We examined whether infection by the parasite N. salmincola similarly increases mortality of juvenile Chinook Salmon Oncorhynchus tshawytscha when they are exposed to the freshwater pathogens Flavobacterium columnare or Aeromonas salmonicida, two bacteria that juvenile salmonids might encounter during their migration to the marine environment. We used a two-part experimental design where juvenile Chinook Salmon were first infected with N. salmincola through cohabitation with infected freshwater snails, Juga spp., and then challenged with either F. columnare or A. salmonicida. Cumulative percent mortality from F. columnare infection was higher in N. salmincola-parasitized fish than in nonparasitized fish. In contrast, cumulative percent mortality from A. salmonicida infection did not differ between N. salmincola-parasitized and nonparasitized groups. No mortalities were observed in the N. salmincola-parasitized-only and control groups from either challenge. Our study demonstrates that a relatively high mean intensity (>200 metacercariae per posterior kidney) of encysted N. salmincola metacercariae can alter the outcomes of bacterial infection in juvenile Chinook Salmon, which might have implications for disease in wild fish populations.

Defenses of susceptible and resistant Chinook salmon (Oncorhynchus tshawytscha) against the myxozoan parasite Ceratomyxa shasta.

We investigated intra-specific variation in the response of salmon to infection with the myxozoan Ceratomyxa shasta by comparing the progress of parasite infection and measures of host immune response in susceptible and resistant Chinook salmon Oncorhynchus tshawytscha at days 12, 25 and 90 post exposure. There were no differences in invasion of the gills indicating that resistance does not occur at the site of entry. In the intestine on day 12, infection intensity and Ig(+) cell numbers were higher in susceptible than resistant fish, but histological examination at that timepoint showed more severe inflammation in resistant fish. This suggests a role for the immune response in resistant fish that eliminates some parasites prior to or soon after reaching the intestine. Susceptible fish had a higher IFNγ, IL-6 and IL-10 response at day 12, but all died of fatal enteronecrosis by day 25. The greatest fold change in IFNγ expression was detected at day 25 in resistant Chinook. In addition, the number of Ig(+) cells in resistant Chinook also increased by day 25. By day 90, resistant Chinook had resolved the inflammation, cytokine expression had decreased and Ig(+) cell numbers were similar to uninfected controls. Thus, it appears that the susceptible strain was incapable of containing or eliminating C. shasta but resistant fish: 1) reduced infection intensity during early intestinal infection, 2) elicited an effective inflammatory response in the intestine that eliminated C. shasta, 3) resolved the inflammation and recovered from infection.