Remnant salmon life history diversity rediscovered in a highly compressed habitat.

Chinook salmon (Oncorhynchus tshawytscha) display remarkable life history diversity, underpinning their ability to adapt to environmental change. Maintaining life history diversity is vital to the resilience and stability of Chinook salmon metapopulations, particularly under changing climates. However, the conditions that promote life history diversity are rapidly disappearing, as anthropogenic forces promote homogenization of habitats and genetic lineages. In this study, we use the highly modified Yuba River in California to understand if distinct genetic lineages and life histories still exist, despite reductions in spawning habitat and hatchery practices that have promoted introgression. There is currently a concerted effort to protect federally listed Central Valley spring-run Chinook salmon populations, given that few wild populations still exist. Despite this, we lack a comprehensive understanding of the genetic and life history diversity of Chinook salmon present in the Yuba River. To understand this diversity, we collected migration timing data and GREB1L genotypes from hook-and-line, acoustic tagging, and carcass surveys of Chinook salmon in the Yuba River between 2009 and 2011. Variation in the GREB1L region of the genome is tightly linked with run timing in Chinook salmon throughout their range, but the relationship between this variation and entry on spawning grounds is little explored in California's Central Valley. We found that the date Chinook salmon crossed the lowest barrier to Yuba River spawning habitat (Daguerre Point Dam) was tightly correlated with their GREB1L genotype. Importantly, our study confirms that ESA-listed spring-run Chinook salmon are spawning in the Yuba River, promoting a portfolio of life history and genetic diversity, despite the highly compressed habitat. This work highlights the need to identify and protect this life history diversity, especially in heavily impacted systems, to maintain healthy Chinook salmon metapopulations. Without protection, we run the risk of losing the last vestiges of important genetic variation.

Integrating otolith and genetic tools to reveal intraspecific biodiversity in a highly impacted salmon population.

Intraspecific biodiversity is vital for species persistence in an increasingly volatile world. By embracing methods that integrate information at different spatiotemporal scales, we can directly monitor and reconstruct changes in intraspecific biodiversity. Here we combined genetics and otolith biochronologies to describe the genotypic and phenotypic diversity of Chinook salmon (Oncorhynchus tshawytscha) in the Yuba River, California, comparing cohorts that experienced a range of hydroclimatic conditions. Yuba River salmon have been heavily impacted by habitat loss and degradation, and large influxes of unmarked hatchery fish each year have led to concern about introgression and uncertainty around the viability of its wild populations, particularly the rarer spring-run salmon. Otolith strontium isotopes showed that Yuba River origin fish represented, on average, 42% (range 7%-73%) of spawners across six return years (2009-2011, 2018-2020), with large interannual variability. The remainder of adult Chinook salmon in the river were primarily strays from the nearby Feather River hatchery, and since 2018 from the Mokelumne River hatchery. Among the Yuba-origin spawners, on average, 30% (range 14%-50%) exhibited the spring-run genotype. The Yuba-origin fish also displayed a variety of outmigration phenotypes that differed in the timing and size at which they left the Yuba river. Early-migrating fry dominated the returns (mean 59%, range 33%-89%), and their contribution rates were negatively correlated with freshwater flows. It is unlikely that fry survival rates are elevated during droughts, suggesting that this trend reflects disproportionately low survival of larger later migrating parr, smolts, and yearlings along the migratory corridor in drier years. Otolith daily increments indicated generally faster growth rates in non-natal habitats, emphasizing the importance of continuing upstream restoration efforts to improve in-river growing conditions. Together, these findings show that, despite a long history of habitat degradation and hatchery introgression, the Yuba River maintains intraspecific biodiversity that should be taken into account in future management, restoration, and reintroduction plans. The finding that genotypic spring-run are reproducing, surviving, and returning to the Yuba River every year suggests that re-establishment of an independent population is possible, although hatchery-wild interactions would need to be carefully considered. Integrating methods is critical to monitor changes in key genetic, physiological, and behavioral traits to assess population viability and resilience.

Biogeochemical processes create distinct isotopic fingerprints to track floodplain rearing of juvenile salmon.

Floodplains represent critical nursery habitats for a variety of fish species due to their highly productive food webs, yet few tools exist to quantify the extent to which these habitats contribute to ecosystem-level production. Here we conducted a large-scale field experiment to characterize differences in food web composition and stable isotopes (δ¹³C, δ¹5N, δ³4S) for salmon rearing on a large floodplain and adjacent river in the Central Valley, California, USA. The study covered variable hydrologic conditions including flooding (1999, 2017), average (2016), and drought (2012-2015). In addition, we determined incorporation rates and tissue fractionation between prey and muscle from fish held in enclosed locations (experimental fields, cages) at weekly intervals. Finally, we measured δ³4S in otoliths to test if these archival biominerals could be used to reconstruct floodplain use. Floodplain-reared salmon had a different diet composition and lower δ13C and δ³4S (δ¹³C = -33.02±2.66‰, δ³4S = -3.47±2.28‰; mean±1SD) compared to fish in the adjacent river (δ¹³C = -28.37±1.84‰, δ³4S = +2.23±2.25‰). These isotopic differences between habitats persisted across years of extreme droughts and floods. Despite the different diet composition, δ¹5N values from prey items on the floodplain (δ¹5N = 7.19±1.22‰) and river (δ¹5N = 7.25±1.46‰) were similar, suggesting similar trophic levels. The food web differences in δ13C and δ³4S between habitats were also reflected in salmon muscle tissue, reaching equilibrium between 24-30 days (2014, δ¹³C = -30.74±0.73‰, δ³4S = -4.6±0.68‰; 2016, δ¹³C = -34.74 ±0.49‰, δ³4S = -5.18±0.46‰). δ³4S measured in sequential growth bands in otoliths recorded a weekly time-series of shifting diet inputs, with the outermost layers recording time spent on the floodplain (δ³4S = -5.60±0.16‰) and river (δ³4S = 3.73±0.98‰). Our results suggest that δ¹³C and δ³4S can be used to differentiate floodplain and river rearing habitats used by native fishes, such as Chinook Salmon, across different hydrologic conditions and tissues. Together these stable isotope analyses provide a toolset to quantify the role of floodplains as fish habitats.

Coldwater fish in a warm water world: Implications for predation of salmon smolts during estuary transit.

Predator-prey systems face intensifying pressure from human exploitation and a warming climate with implications for where and how natural resource management can successfully intervene. We hypothesized young salmon migrating to the Pacific Ocean face a seasonally intensifying predator gauntlet when warming water temperature intensifies a multiple predator effect (MPE) from Striped Bass Morone saxatilis and Largemouth Bass Micropterus salmoides. We evaluated this hypothesis using data synthesis and simulation modeling.Contemporary studies based on acoustically tagged fish reaffirmed older observations that Chinook Salmon smolts must transit the Delta before water temperature reaches 20°C or mortality will be nearly 100%. Striped Bass attack rates on tethered smolts were insensitive to distance from shore and water temperature, whereas Largemouth Bass attack rates were highest near shorelines in warm water, supporting the temporal aspect of the hypothesis. Whether the combined effects of the two predators produce an MPE remains unconfirmed due to limitations on quantifying salmon behavior.We used multiple simulation models to try to reconstruct the empirical relationship between smolt survival and water temperature. Simulations reinforced attack rate results, but could not recreate the temperature dependence in smolt survival except at higher than observed temperatures. We propose three hypotheses for why and recommend discerning among them should be a focus of research.We found significant linear relationships between monthly mean inflow to the Delta from each of its two largest tributaries and monthly mean water temperatures along associated salmon migration routes, but these relationships can be nonlinear, with most of the correlation occurring at low inflows when water temperature is largely controlled by air temperature and day length. As the global climate warms, changed circumstances in predator-prey relationships may present important challenges when managing species vulnerable to extinction in addition to presently more abundant species.

Differential sensitivity to warming and hypoxia during development and long-term effects of developmental exposure in early life stage Chinook salmon.

Warming and hypoxia are two stressors commonly found within natural salmon redds that are likely to co-occur. Warming and hypoxia can interact physiologically, but their combined effects during fish development remain poorly studied, particularly stage-specific effects and potential carry-over effects. To test the impacts of warm water temperature and hypoxia as individual and combined developmental stressors, late fall-run Chinook salmon embryos were reared in 10 treatments from fertilization through hatching with two temperatures [10°C (ambient) and 14°C (warm)], two dissolved oxygen saturation levels [normoxia (100% air saturation, 10.4-11.4 mg O2/l) and hypoxia (50% saturation, 5.5 mg O2/l)] and three exposure times (early [eyed stage], late [silver-eyed stage] and chronic [fertilization through hatching]). After hatching, all treatments were transferred to control conditions (10°C and 100% air saturation) through the fry stage. To study stage-specific effects of stressor exposure we measured routine metabolic rate (RMR) at two embryonic stages, hatching success and growth. To evaluate carry-over effects, where conditions during one life stage influence performance in a later stage, RMR of all treatments was measured in control conditions at two post-hatch stages and acute stress tolerance was measured at the fry stage. We found evidence of stage-specific effects of both stressors during exposure and carry-over effects on physiological performance. Both individual stressors affected RMR, growth and developmental rate while multiple stressors late in development reduced hatching success. RMR post-hatch showed persistent effects of embryonic stressor exposure that may underlie differences observed in developmental timing and acute stress tolerance. The responses to stressors that varied by stage during development suggest that stage-specific management efforts could support salmon embryo survival. The persistent carry-over effects also indicate that considering sub-lethal effects of developmental stressor exposure may be important to understanding how climate change influences the performance of salmon across life stages.

Resolving selenium exposure risk: Spatial, temporal, and tissue-specific variability of an endemic fish in a large, dynamic estuary.

Estuaries provide critical habitat for a vast array of fish and wildlife but are also a nexus for core economic activities that mobilize and concentrate contaminants that can threaten aquatic species. Selenium (Se), an essential element and potent reproductive toxin, is enriched in parts of the San Francisco Estuary (SFE) to levels known to cause toxicity, yet the risk of Se to species that inhabit the SFE is not well understood. We quantified Se concentrations in muscle, liver and ovary of the demersal cyprinid Sacramento Splittail from six regions in the SFE at three time points to evaluate Se exposure risk. Selenium levels exceeded proposed EPA criteria in ovary and thresholds of concern for liver in 15% and 20%, respectively, of fish collected in the fall of 2010, preceding the discovery of juvenile Splittail displaying a high incidence (>40%) of spinal deformities characteristic of Se toxicity, and again in 2011. No exceedances were detected in muscle tissue. Selenium concentrations varied significantly among regions for muscle (F5,113 = 20.49, p < 0.0001), liver (F5,113 = 28.4, p < 0.0001) and ovary (F5,112 = 19.3, p < 0.0001) but did not vary between the wet and dry years, nor were they influenced by foraging trophic level or prey selection. Foraging location along the salinity gradient, defined by δ34S values, explained regional Se exposures in Splittail. Relationships between tissues varied among regions for muscle and liver and muscle and ovary, but a single global relationship could be defined for ovary and liver Se concentrations. Our results suggest that the proposed EPA Se criteria for muscle tissue in Splittail may be under-protective as it would not have predicted exceedances in liver or ovary tissue and that the relationship between muscle tissue and ovary and liver may be Se concentration and seasonal dependent.

Unnatural selection of salmon life histories in a modified riverscape.

Altered river flows and fragmented habitats often simplify riverine communities and favor non-native fishes, but their influence on life-history expression and survival is less clear. Here, we quantified the expression and ultimate success of diverse salmon emigration behaviors in an anthropogenically altered California river system. We analyzed two decades of Chinook salmon monitoring data to explore the influence of regulated flows on juvenile emigration phenology, abundance, and recruitment. We then followed seven cohorts into adulthood using otolith (ear stone) chemical archives to identify patterns in time- and size-selective mortality along the migratory corridor. Suppressed winter flow cues were associated with delayed emigration timing, particularly in warm, dry years, which was also when selection against late migrants was the most extreme. Lower, less variable flows were also associated with reduced juvenile and adult production, highlighting the importance of streamflow for cohort success in these southernmost populations. While most juveniles emigrated from the natal stream as fry or smolts, the survivors were dominated by the rare few that left at intermediate sizes and times, coinciding with managed flows released before extreme summer temperatures. The consistent selection against early (small) and late (large) migrants counters prevailing ecological theory that predicts different traits to be favored under varying environmental conditions. Yet, even with this weakened portfolio, maintaining a broad distribution in migration traits still increased adult production and reduced variance. In years exhibiting large fry pulses, even marginal increases in their survival would have significantly boosted recruitment. However, management actions favoring any single phenotype could have negative evolutionary and demographic consequences, potentially reducing adaptability and population stability. To recover fish populations and support viable fisheries in a warming and increasingly unpredictable climate, coordinating flow and habitat management within and among watersheds will be critical to balance trait optimization versus diversification.

Climate vulnerability assessment for Pacific salmon and steelhead in the California Current Large Marine Ecosystem.

Major ecological realignments are already occurring in response to climate change. To be successful, conservation strategies now need to account for geographical patterns in traits sensitive to climate change, as well as climate threats to species-level diversity. As part of an effort to provide such information, we conducted a climate vulnerability assessment that included all anadromous Pacific salmon and steelhead (Oncorhynchus spp.) population units listed under the U.S. Endangered Species Act. Using an expert-based scoring system, we ranked 20 attributes for the 28 listed units and 5 additional units. Attributes captured biological sensitivity, or the strength of linkages between each listing unit and the present climate; climate exposure, or the magnitude of projected change in local environmental conditions; and adaptive capacity, or the ability to modify phenotypes to cope with new climatic conditions. Each listing unit was then assigned one of four vulnerability categories. Units ranked most vulnerable overall were Chinook (O. tshawytscha) in the California Central Valley, coho (O. kisutch) in California and southern Oregon, sockeye (O. nerka) in the Snake River Basin, and spring-run Chinook in the interior Columbia and Willamette River Basins. We identified units with similar vulnerability profiles using a hierarchical cluster analysis. Life history characteristics, especially freshwater and estuary residence times, interplayed with gradations in exposure from south to north and from coastal to interior regions to generate landscape-level patterns within each species. Nearly all listing units faced high exposures to projected increases in stream temperature, sea surface temperature, and ocean acidification, but other aspects of exposure peaked in particular regions. Anthropogenic factors, especially migration barriers, habitat degradation, and hatchery influence, have reduced the adaptive capacity of most steelhead and salmon populations. Enhancing adaptive capacity is essential to mitigate for the increasing threat of climate change. Collectively, these results provide a framework to support recovery planning that considers climate impacts on the majority of West Coast anadromous salmonids.

Warm, dry winters truncate timing and size distribution of seaward-migrating salmon across a large, regulated watershed.

Ecologists are pressed to understand how climate constrains the timings of annual biological events (phenology). Climate influences on phenology are likely significant in estuarine watersheds because many watersheds provide seasonal fish nurseries where juvenile presence is synched with favorable conditions. While ecologists have long recognized that estuaries are generally important to juvenile fish, we incompletely understand the specific ecosystem dynamics that contribute to their nursery habitat value, limiting our ability to identify and protect vital habitat components. Here we examined the annual timing of juvenile coldwater fish migrating through a seasonally warm, hydrologically managed watershed. Our goal was to (1) understand how climate constrained the seasonal timing of water conditions necessary for juvenile fish to use nursery habitats and (2) inform management decisions about (a) mitigating climate-mediated stress on nursery habitat function and (b) conserving heat-constrained species in warming environments. Cool, wet winters deposited snow and cold water into mountains and reservoirs, which kept the lower watershed adequately cool for juveniles through the spring despite the region approaching its hot, dry summers. For every 1°C waters in April were colder, the juvenile fish population (1) inhabited the watershed 4-7 d longer and (2) entered marine waters, where survival is size selective, at maximum sizes 2.1 mm larger. Climate therefore appeared to constrain the nursery functions of this system by determining seasonal windows of tolerable rearing conditions, and cold water appeared to be a vital ecosystem component that promoted juvenile rearing. Fish in this system inhabit the southernmost extent of their range and already rear during the coolest part of the year, suggesting that a warming climate will truncate rather than shift their annual presence. Our findings are concerning for coldwater diadromous species in general because warming climates may constrain watershed use and diminish viability of life histories (e.g., late springtime rearing) and associated portfolio benefits over the long term. Lower watershed nurseries for coldwater fish in warming climates may be enhanced through allocating coldwater reservoir releases to prolong juvenile rearing periods downstream or restorations that facilitate colder conditions.

Reconstructing the Migratory Behavior and Long-Term Survivorship of Juvenile Chinook Salmon under Contrasting Hydrologic Regimes.

The loss of genetic and life history diversity has been documented across many taxonomic groups, and is considered a leading cause of increased extinction risk. Juvenile salmon leave their natal rivers at different sizes, ages and times of the year, and it is thought that this life history variation contributes to their population sustainability, and is thus central to many recovery efforts. However, in order to preserve and restore diversity in life history traits, it is necessary to first understand how environmental factors affect their expression and success. We used otolith (87)Sr/(86)Sr in adult Chinook salmon (Oncorhynchus tshawytcha) returning to the Stanislaus River in the California Central Valley (USA) to reconstruct the sizes at which they outmigrated as juveniles in a wetter (2000) and drier (2003) year. We compared rotary screw trap-derived estimates of outmigrant timing, abundance and size with those reconstructed in the adults from the same cohort. This allowed us to estimate the relative survival and contribution of migratory phenotypes (fry, parr, smolts) to the adult spawning population under different flow regimes. Juvenile abundance and outmigration behavior varied with hydroclimatic regime, while downstream survival appeared to be driven by size- and time-selective mortality. Although fry survival is generally assumed to be negligible in this system, >20% of the adult spawners from outmigration year 2000 had outmigrated as fry. In both years, all three phenotypes contributed to the spawning population, however their relative proportions differed, reflecting greater fry contributions in the wetter year (23% vs. 10%) and greater smolt contributions in the drier year (13% vs. 44%). These data demonstrate that the expression and success of migratory phenotypes vary with hydrologic regime, emphasizing the importance of maintaining diversity in a changing climate.

Managed metapopulations: do salmon hatchery 'sources' lead to in-river 'sinks' in conservation?

Maintaining viable populations of salmon in the wild is a primary goal for many conservation and recovery programs. The frequency and extent of connectivity among natal sources defines the demographic and genetic boundaries of a population. Yet, the role that immigration of hatchery-produced adults may play in altering population dynamics and fitness of natural populations remains largely unquantified. Quantifying, whether natural populations are self-sustaining, functions as sources (population growth rate in the absence of dispersal, λ>1), or as sinks (λ<1) can be obscured by an inability to identify immigrants. In this study we use a new isotopic approach to demonstrate that a natural spawning population of Chinook salmon, (Oncorhynchus tshawytscha) considered relatively healthy, represents a sink population when the contribution of hatchery immigrants is taken into consideration. We retrieved sulfur isotopes ((34)S/(32)S, referred to as δ(34)S) in adult Chinook salmon otoliths (ear bones) that were deposited during their early life history as juveniles to determine whether individuals were produced in hatcheries or naturally in rivers. Our results show that only 10.3% (CI = 5.5 to 18.1%) of adults spawning in the river had otolith δ(34)S values less than 8.5‰, which is characteristic of naturally produced salmon. When considering the total return to the watershed (total fish in river and hatchery), we estimate that 90.7 to 99.3% (CI) of returning adults were produced in a hatchery (best estimate = 95.9%). When population growth rate of the natural population was modeled to account for the contribution of previously unidentified hatchery immigrants, we found that hatchery-produced fish caused the false appearance of positive population growth. These findings highlight the potential dangers in ignoring source-sink dynamics in recovering natural populations, and question the extent to which declines in natural salmon populations are undetected by monitoring programs.