Individual variation, population-specific behaviours and stochastic processes shape marine migration phenologies.

The phenology of long-distance migrations can influence individual fitness, moderate population dynamics and regulate the availability of ecosystem services to other trophic levels. Phenology varies within and among populations, and can be influenced by conditions individuals experience both prior to departure and encounter en route. Assessing how intrinsic and extrinsic factors (e.g., individual physical condition vs. environmental conditions) interact to influence variation in migratory phenologies across ecological scales is often limited due to logistical constraints associated with tracking large numbers of individuals from multiple populations simultaneously. We used two natural tags, DNA and otolith microstructure analysis, to estimate the relative influence of individual traits (life-history strategy, body size at departure and growth during migration), population-specific behaviours and interannual variability on the phenology of marine migrations in juvenile sockeye salmon Oncorhynchus nerka. We show that the timing and duration of juvenile sockeye salmon migrations were correlated with both life-history strategy and body size, while migration duration was also correlated with departure timing and growth rates during migration. Even after accounting for the effect of individual traits, several populations exhibited distinct migration phenologies. Finally, we observed substantial interannual and residual variation, suggesting stochastic environmental conditions moderate the influence of carry-over effects that develop prior to departure, as well as population-specific strategies. Migratory phenologies are shaped by complex interactions between drivers acting at multiple ecological and temporal scales. Given evidence that intraspecific diversity can stabilize ecological systems, conservation efforts should seek to maintain migratory variation among populations and preserve locally adapted phenotypes; however, variation within populations, which may buffer systems from environmental stochasticity, should also be regularly assessed and preserved.

Utilization of an endocrine growth index, insulin-like growth factor binding protein (IGFBP)-1b, for postsmolt coho salmon in the Strait of Georgia, British Columbia, Canada.

Monitoring the growth of salmon during their early marine phase provides insights into prey availability, and growth rates may be linked to risks of size-dependent mortality. However, the measurement of growth rate is challenging for free-living salmon in the ocean. Insulin-like growth factor (IGF)-I is a growth-promoting hormone that is emerging as a useful index of growth in salmon. In addition, laboratory-based studies using coho salmon have shown that one of circulating IGF-binding proteins (IGFBPs), IGFBP-1b, is induced by fasting and thus could be used as an inverse index of growth and/or catabolic state in salmon. However, few studies have measured plasma levels of IGFBP-1b in salmon in the wild. We measured plasma IGFBP-1b levels for postsmolt coho salmon collected in the Strait of Georgia and surrounding waters, British Columbia, Canada, and compared regional differences in IGFBP-1b to ecological information such as seawater temperature and stomach fullness. Plasma IGFBP-1b levels were the highest in fish from Eastern Johnstone Strait and relatively high in Queen Charlotte Strait and Western Johnstone Strait, which was in good agreement with the poor ocean conditions for salmon hypothesized to occur in that region. The molar ratio of plasma IGF-I to IGFBP-1b, a theoretical parameter of IGF-I availability to the receptor, discriminated differences among regions better than IGF-I or IGFBP-1b alone. Our data suggest that plasma IGFBP-1b reflects catabolic status in postsmolt coho salmon, as highlighted in fish in Eastern Johnston Strait, and is a useful tool to monitor negative aspects of salmon growth in the ocean.

Size- and condition-dependent predation: a seabird disproportionately targets substandard individual juvenile salmon.

Selection of prey that are small and in poor body condition is a widespread phenomenon in terrestrial predator-prey systems and may benefit prey populations by removing substandard individuals. Similar selection is widely assumed to operate in aquatic systems. Indeed, size-selective predation is a longstanding and central tenet of aquatic food web theory. However, it is not known if aquatic predators select prey based on their condition or state, compared to their size. Surprisingly, no comparable information is available for marine systems because it is exceedingly difficult to make direct observations in this realm. Thus the role of body condition in regulating susceptibility to predation remains a black box in the marine environment. Here we have exploited an ideal model system to evaluate selective predation on pelagic marine fish: comparing characteristics (fork length, mass corrected for fork length) of fresh, whole, intact juvenile Pacific salmon delivered by a seabird to its single nestling with salmon collected concurrently in coastal trawl surveys. Three species of juvenile salmon (Oncorhynchus spp.) are consumed by provisioning Rhinoceros Auklets (Cerorhinca nionocerata); an abundant, colonial, pursuit-diving seabird. Samples were collected from multiple colonies and fisheries surveys in coastal British Columbia in two years. As predicted, Auklets preyed on small individuals in poor condition and consistently selected them at levels higher than their relative availability. This is the first study to provide direct evidence for both size- and condition-selective predation on marine fish in the wild. We anticipate that our results will be a starting point in evaluating how selective predation may structure or influence marine fish populations and bridges a fundamental incongruity between ecological theory and application; although "bigger is better" is considered a fundamental tenet of marine food webs, marine predators are often assumed to consume indiscriminately.

Hitting the moving target: modelling ontogenetic shifts with stable isotopes reveals the importance of isotopic turnover.

Ontogenetic niche shifts are widely prevalent in nature and are important in shaping the structure and dynamics of ecosystems. Stable isotope analysis is a powerful tool to assess these shifts, with δ(15) N providing a measure of trophic level and δ(13) C a measure of energy source. Previous applications of stable isotopes to study ontogenetic niche shifts have not considered the appreciable time lag between diet and consumer tissue associated with isotopic turnover. These time lags introduce significant complexity into field studies of ontogenetic niche shifts. Juvenile Chinook salmon (Oncorhynchus tshawytscha) migrate from freshwater to marine ecosystems and shift their diet from feeding primarily on invertebrates to feeding primarily on fish. This dual ontogenetic habitat and diet shift, in addition to the long time lag associated with isotopic turnover, suggests that there is potential for a disconnect between the prey sources that juvenile salmon are consuming, and the inferred prey sources from stable isotopes. We developed a model that considered ontogenetic niche shifts and time lags associated with isotopic turnover, and compared this 'ontogeny' model to one that considered only isotopic turnover. We used a Bayesian framework to explicitly account for parameter uncertainty. Data showed overwhelming support for the ontogeny model relative to the isotopic turnover model. Estimated variables from best model fits indicate that the ontogeny model predicts a much greater reliance on fish prey than does the stomach content data. Overall, we found that this method of quantifying ontogenetic niche shifts effectively accounted for both isotopic turnover and ontogenetic diet shifts; a finding that could be widely applicable to a variety of systems.

Interpreting dual ELISA and qPCR data for bacterial kidney disease of salmonids.

Although there are a variety of methods available for the detection of Renibacterium salmoninarum, the causative agent of bacterial kidney disease in salmon and trout, the enzyme-linked immunosorbent assay (ELISA) is probably the most widely used method. However, ELISA measures bacterial antigen, which does not necessarily reflect the number of cells present. We hypothesized that dual analysis of kidney tissue by ELISA and a quantitative real-time polymerase chain reaction assay (qPCR) would provide complementary information about antigen level and the number of bacterial genomes. We found that DNA extracted from the insoluble fraction of the ELISA tissue preparation produced the same qPCR result as DNA extracted directly from frozen tissue, permitting true dual analysis of the same tissue sample. We examined kidney tissue in this manner from individual free-ranging juvenile Chinook salmon and antibiotic-treated captive subadult Chinook salmon and observed 3 different patterns of results. Among the majority of fish, there was a strong correlation between the ELISA value and the qPCR value. However, subsets of fish exhibited either low ELISA values with elevated qPCR values or higher ELISA values with very low qPCR values. These observations suggest a conceptual model that allows inferences about the state of infection of individual fish based on dual ELISA/qPCR results. Although this model requires further assessment through experimental infections and treatments, it may have utility in broodstock selection programs that currently apply egg-culling practices based on ELISA alone.

Percent ash-free dry weight as a robust method to estimate energy density across taxa.

Determining how energy flows through ecosystems reveals underlying ecological patterns that drive processes such as growth and food web dynamics. Models that assess the transfer of energy from producers to consumers require information on the energy content or energy density (ED) of prey species. ED is most accurately measured through bomb calorimetry, but this method suffers from limitations of cost, time, and sample requirements that often make it unrealistic for many studies. Percent dry weight (DW) is typically used as a proxy for ED, but this measure includes an indigestible portion (e.g., bones, shell, salt) that can vary widely among organisms. Further, several distinct models exist for various taxonomic groups, yet none can accurately estimate invertebrate, vertebrate and plant ED with a single equation. Here, we present a novel method to estimate the ED of organisms using percent ash-free dry weight (AFDW). Using data obtained from 11 studies diverse in geographic, temporal and taxonomic scope, AFDW, DW as well as percent protein and percent lipid were compared as predictors of ED. Linear models were produced on a logarithmic scale, including dummy variables for broad taxonomic groups. AFDW was the superior predictor of ED compared to DW, percent protein content and percent lipid content. Model selection revealed that using correction factors (dummy variables) for aquatic animals (AA) and terrestrial invertebrates (TI) produced the best-supported model-log10(ED) = 1.07*log10(AFDW) - 0.80 (R 2 = 0.978, p < .00001)-with an intercept adjustment of 0.09 and 0.04 for AA and TI, respectively. All models including AFDW as a predictor had high predictive power (R 2 > 0.97), suggesting that AFDW can be used with high degrees of certainty to predict the ED of taxonomically diverse organisms. Our AFDW model will allow ED to be determined with minimal cost and time requirements and excludes ash-weight from estimates of digestible mass. Its ease of use will allow for ED to be more readily and accurately determined for diverse taxa across different ecosystems.

Comparison of infectious agents detected from hatchery and wild juvenile Coho salmon in British Columbia, 2008-2018.

Infectious diseases are potential contributors to decline in Coho salmon (Oncorhynchus kisutch) populations. Although pathogens are theoretically considered to pose higher risk in high-density rearing environments like hatcheries, there is no direct evidence that hatchery-origin Coho salmon increase the transmission of infectious agents to sympatric wild populations. This study was undertaken to compare prevalence, burden, and diversity of infectious agents between hatchery-reared and wild juvenile Coho salmon in British Columbia (BC), Canada. In total, 2,655 juvenile Coho salmon were collected between 2008 and 2018 from four regions of freshwater and saltwater in BC. High-throughput microfluidics qPCR was employed for simultaneous detection of 36 infectious agents from mixed-tissue samples (gill, brain, heart, liver, and kidney). Thirty-one agents were detected at least once, including ten with prevalence >5%. Candidatus Brachiomonas cysticola, Paraneuclospora theridion, and Parvicapsula pseudobranchiocola were the most prevalent agents. Diversity and burden of infectious agents were substantially higher in marine environment than in freshwater. In Mainland BC, infectious burden and diversity were significantly lower in hatchery smolts than in wild counterparts, whereas in other regions, there were no significant differences. Observed differences in freshwater were predominantly driven by three parasites, Loma salmonae, Myxobolus arcticus, and Parvicapsula kabatai. In saltwater, there were no consistent differences in agent prevalence between hatchery and wild fish shared among the west and east coasts of Vancouver Island. Although some agents showed differential infectious patterns between regions, annual variations likely contributed to this signal. Our findings do not support the hypothesis that hatchery smolts carry higher burdens of infectious agents than conspecific wild fish, reducing the potential risk of transfer to wild smolts at this life stage. Moreover, we provide a baseline of infectious agents in juvenile Coho salmon that will be used in future research and modeling potential correlations between infectious profiles and marine survival.

Validity of inferring size-selective mortality and a critical size limit in Pacific salmon from scale circulus spacing.

Size-selective mortality owing to lack of energy reserves during the first marine winter has been suggested to be a result of juvenile salmon failing to reach a critical size or condition by the end of their first marine summer and not surviving the following winter due to this presumed energy deficit. This hypothesis implies strong size dependency of mortality, and is subject to empirical data support for acceptance. Scale circulus spacing has been interpreted as an index for body size, and we reviewed the effect of size-selective mortality with a knife-edge mortality function on descriptive statistics for a scale circulus spacing index (SCSI). In order to invoke size selection as an important driver of mortality during the first year of ocean rearing, it is necessary to demonstrate not only that size-selective mortality is directed towards the smaller members of the population, but that the selective nature of the mortality can account for a substantial portion of the observed mortality. If the assumption is made that a random sample of a single juvenile population has been obtained, then studies that employ a SCSI to infer size-selective mortality coupled with a critical size limit must demonstrate a shift toward larger values of the SCSI, but also a concomitant reduction in the variance and range of the SCSI and an increase in the skewness and kurtosis of the SCSI values. Through simulation we found that the percentage of adults that displayed a SCSI value greater than the maximum observed in the juvenile sample was highly dependent on the initial juvenile sample size and size-selective mortality rate. Geographical distributions of juvenile Pacific salmon can be stratified by size, with larger individuals migrating earlier from local ocean entry locations than smaller individuals, and thus differential timing migration of juveniles based upon body size prior to the collection of the marine juvenile sample may be a more plausible explanation of published trends in the SCSI, rather than invoking substantial size-selective mortality and a critical size limit.

Effects of fasting and nutritional restriction on the isotopic ratios of nitrogen and carbon: a meta-analysis.

Many organisms experience fasting in their life time, and this physiological process has the potential to alter stable isotope values of organisms, and confound interpretation of food web studies. However, previous studies on the effects of fasting and starvation on stable isotopes show disparate results, and have never been quantitatively synthesized. We performed a laboratory experiment and meta-analysis to determine how stable isotopes of δ (15)N and δ (13)C change with fasting, and we tested whether moderators such as taxa and tissue explain residual variation. We collected literature data from a wide variety of taxa and tissues. We surveyed over 2000 papers, and of these, 26 met our selection criteria, resulting in 51 data points for δ (15)N, and 43 data points for δ (13)C. We determine that fasting causes an average increase in the isotopic value of organisms of 0.5‰ for δ (15)N and that the only significant moderator is tissue type. We find that the overall effect size for δ (13)C is not significant, but when the significant moderator of tissue is considered, significant increases in blood and whole organisms are seen with fasting. Our results show that across tissues and taxa, the nutritional status of an organism must be considered when interpreting stable isotope data, as fasting can cause large differences in stable isotope values that would be otherwise attributed to other factors.

A report on radioactivity measurements of fish samples from the west coast of Canada.

Even though many studies have shown that radioactive caesium levels in fish caught outside of Japan were below experimental detection limits of a few Bq kg(-1), significant public concern has been expressed about the safety of consuming seafood from the Pacific Ocean following the Fukushima-Daiichi nuclear accident. To address the public concerns, samples of commonly consumed salmon and groundfish harvested from the Canadian west coast in 2013 were analysed for radioactive caesium. None of the fish samples analysed in this study contained any detectable levels of (134)Cs and (137)Cs under given experimental setting with the average detection limit of ∼2 Bq kg(-1). Using a conservative worst-case scenario where all fish samples would contain (137)Cs exactly at the detection limit level and (134)Cs at half of the detection limit level (to account for much shorter half-life of (134)Cs), the resulting radiation dose for people from consumption of this fish would be a very small fraction of the annual dose from exposure to natural background radiation in Canada. Therefore, fish, such as salmon and groundfish, from the Canadian west coast are of no radiological health concern.

Infectious disease, shifting climates, and opportunistic predators: cumulative factors potentially impacting wild salmon declines.

Emerging diseases are impacting animals under high-density culture, yet few studies assess their importance to wild populations. Microparasites selected for enhanced virulence in culture settings should be less successful maintaining infectivity in wild populations, as once the host dies, there are limited opportunities to infect new individuals. Instead, moderately virulent microparasites persisting for long periods across multiple environments are of greatest concern. Evolved resistance to endemic microparasites may reduce susceptibilities, but as barriers to microparasite distributions are weakened, and environments become more stressful, unexposed populations may be impacted and pathogenicity enhanced. We provide an overview of the evolutionary and ecological impacts of infectious diseases in wild salmon and suggest ways in which modern technologies can elucidate the microparasites of greatest potential import. We present four case studies that resolve microparasite impacts on adult salmon migration success, impact of river warming on microparasite replication, and infection status on susceptibility to predation. Future health of wild salmon must be considered in a holistic context that includes the cumulative or synergistic impacts of multiple stressors. These approaches will identify populations at greatest risk, critically needed to manage and potentially ameliorate the shifts in current or future trajectories of wild populations.

Ecosystemic effects of salmon farming increase mercury contamination in wild fish.

Net-pen salmon aquaculture has well-known effects on coastal ecosystems: farm waste increases sediment organic content and the incidence of sediment anoxia, supports increased production of deposit-feeding invertebrates, and attracts higher densities of demersal fish and other mobile carnivores. These impacts are widely considered to be localized and transitory, and are commonly managed by imposing a period of fallowing between cycles of production. The implications of these ecosystemic effects for contaminant cycling, however, have not previously been considered. We found elevated levels of mercury in demersal rockfishes near salmon farms in coastal British Columbia, Canada, attributable to a combination of higher rockfish trophic position and higher mercury levels in prey near farms. Mercury concentrations in long-lived species such as rockfishes change over a longer time scale than cycles of production and fallowing, and thus at least some important effects of fish farms may not be considered transitory.