Tough places and safe spaces: Can refuges save salmon from a warming climate?

The importance of thermal refuges in a rapidly warming world is particularly evident for migratory species, where individuals encounter a wide range of conditions throughout their lives. In this study, we used a spatially explicit, individual-based simulation model to evaluate the buffering potential of cold-water thermal refuges for anadromous salmon and trout (Oncorhynchus spp.) migrating upstream through a warm river corridor that can expose individuals to physiologically stressful temperatures. We considered upstream migration in relation to migratory phenotypes that were defined in terms of migration timing, spawn timing, swim speed, and use of cold-water thermal refuges. Individuals with different migratory phenotypes migrated upstream through riverine corridors with variable availability of cold-water thermal refuges and mainstem temperatures. Use of cold-water refuges (CWRs) decreased accumulated sublethal exposures to physiologically stressful temperatures when measured in degree-days above 20, 21, and 22°C. The availability of CWRs was an order of magnitude more effective in lowering accumulated sublethal exposures under current and future mainstem temperatures for summer steelhead than fall Chinook Salmon. We considered two emergent model outcomes, survival and percent of available energy used, in relation to thermal heterogeneity and migratory phenotype. Mean percent energy loss attributed to future warmer mainstem temperatures was at least two times larger than the difference in energy used in simulations without CWRs for steelhead and salmon. We also found that loss of CWRs reduced the diversity of energy-conserving migratory phenotypes when we examined the variability in entry timing and travel time outside of CWRs in relation to energy loss. Energy-conserving phenotypic space contracted by 7%-23% when CWRs were unavailable under the current thermal regime. Our simulations suggest that, while CWRs do not entirely mitigate for stressful thermal exposures in mainstem rivers, these features are important for maintaining a diversity of migration phenotypes. Our study suggests that the maintenance of diverse portfolios of migratory phenotypes and cool- and cold-water refuges might be added to the suite of policies and management actions presently being deployed to improve the likelihood of Pacific salmonid persistence into a future characterized by climate change.

Technical fishway passage structures provide high passage efficiency and effective passage for adult Pacific salmonids at eight large dams.

Fishways have been widely used for upstream passage around human-built structures, but 'success' has varied dramatically. Evaluation of fishway success has typically been conducted at local scales using metrics such as fish passage efficiency and passage time, but evaluations are increasingly used in broader assessments of whether passage facilities meet population-specific conservation and management objectives. Over 15 years, we monitored passage effectiveness at eight dams on the Columbia and Snake rivers for 26,886 radio-tagged spring-summer and fall Chinook Salmon O. tshwaytscha, Sockeye Salmon O. nerka, and summer steelhead O. mykiss during their migrations to spawning sites. Almost all fish that entered dam tailraces eventually approached and entered fishways. Tailrace-to-forebay passage efficiency estimates at individual dams were consistently high, averaging 0.966 (SD = 0.035) across 245 run×year×dam combinations. These estimates are among the highest recorded for any migratory species, which we attribute to the scale of evaluation, salmonid life history traits (e.g., philopatry), and a sustained adaptive management approach to fishway design, maintenance, and improvement. Full-dam fish passage times were considerably more variable, with run×year×dam medians ranging from 5-65 h. Evaluation at larger scales provided evidence that fishways were biologically effective, e.g., we observed rapid migration rates (medians = 28-40 km/d) through river reaches with multiple dams and estimated fisheries-adjusted upstream migration survival of 67-69%. However, there were substantive uncertainties regarding effectiveness. Uncertainty about natal origins confounded estimation of population-specific survival and interpretation of apparent dam passage 'failure', while lack of post-migration reproductive data precluded analyses of delayed or cumulative effects of passing the impounded system on fish fitness. Although the technical fishways are effective for salmonids in the Columbia-Snake River system, other co-migrating species have lower passage rates, highlighting the need for species-specific design and evaluation wherever passage facilities impact fish management and conservation goals.

Collective navigation can facilitate passage through human-made barriers by homeward migrating Pacific salmon.

The mass migration of animals is one of the great wonders of the natural world. Although there are multiple benefits for individuals migrating in groups, an increasingly recognized benefit is collective navigation, whereby social interactions improve animals' ability to find their way. Despite substantial evidence from theory and laboratory-based experiments, empirical evidence of collective navigation in nature remains sparse. Here we used a unique large-scale radiotelemetry dataset to analyse the movements of adult Pacific salmon (Oncorhynchus sp.) in the Columbia River Basin, USA. These salmon face substantial migratory challenges approaching, entering and transiting fishways at multiple large-scale hydroelectric mainstem dams. We assess the potential role of collective navigation in overcoming these challenges and show that Chinook salmon (O. tshawytscha), but not sockeye salmon (O. nerka) locate fishways faster and pass in fewer attempts at higher densities, consistent with collective navigation. The magnitude of the density effects were comparable to major established drivers such as water temperature, and model simulations predicted that major fluctuations in population density can have substantial impacts on key quantities including mean passage time and fraction of fish with very long passage times. The magnitude of these effects indicates the importance of incorporating conspecific density and social dynamics into models of the migration process. Density effects on both ability to locate fishways and number of passage attempts have the potential to enrich our understanding of migratory energetics and success of migrating anadromous salmonids. More broadly, our work reveals a potential role of collective navigation, in at least one species, to mitigate the effects of anthropogenic barriers to animals on the move.

Genomic islands of divergence infer a phenotypic landscape in Pacific lamprey.

High rates of dispersal can breakdown coadapted gene complexes. However, concentrated genomic architecture (i.e., genomic islands of divergence) can suppress recombination to allow evolution of local adaptations despite high gene flow. Pacific lamprey (Entosphenus tridentatus) is a highly dispersive anadromous fish. Observed trait diversity and evidence for genetic basis of traits suggests it may be locally adapted. We addressed whether concentrated genomic architecture could influence local adaptation for Pacific lamprey. Using two new whole genome assemblies and genotypes from 7,716 single nucleotide polymorphism (SNP) loci in 518 individuals from across the species range, we identified four genomic islands of divergence (on chromosomes 01, 02, 04, and 22). We determined robust phenotype-by-genotype relationships by testing multiple traits across geographic sites. These trait associations probably explain genomic divergence across the species' range. We genotyped a subset of 302 broadly distributed SNPs in 2,145 individuals for association testing for adult body size, sexual maturity, migration distance and timing, adult swimming ability, and larval growth. Body size traits were strongly associated with SNPs on chromosomes 02 and 04. Moderate associations also implicated SNPs on chromosome 01 as being associated with variation in female maturity. Finally, we used candidate SNPs to extrapolate a heterogeneous spatiotemporal distribution of these predicted phenotypes based on independent data sets of larval and adult collections. These maturity and body size results guide future elucidation of factors driving regional optimization of these traits for fitness. Pacific lamprey is culturally important and imperiled. This research addresses biological uncertainties that challenge restoration efforts.

Assessing contributions of cold-water refuges to reproductive migration corridor conditions for adult Chinook Salmon and steelhead trout in the Columbia River, USA.

Diadromous fish populations face multiple challenges along their migratory routes. These challenges include suboptimal water quality, harvest, and barriers to longitudinal and lateral connectivity. Interactions among factors influencing migration success make it challenging to assess management options for improving migratory fish conditions along riverine migration corridors. We describe a spatially explicit simulation model that integrates complex individual behaviors of fall-run Chinook Salmon (Oncorhynchus tshawytscha) and summer-run steelhead trout (O. mykiss) during migration, responds to variable habitat conditions over a large extent of the Columbia River, and links migration corridor conditions to fish condition outcomes. The model is built around a mechanistic behavioral decision tree that drives individual interactions of fish within their simulated environments. By simulating several thermalscapes with alternative scenarios of thermal refuge availability, we examined how behavioral thermoregulation in cold-water refuges influenced migrating fish conditions. Outcomes of the migration corridor simulation model show that cold-water refuges can provide relief from exposure to high water temperatures, but do not substantially contribute to energy conservation by migrating adults. Simulated cooling of the Columbia River decreased reliance on cold-water refuges and there were slight reductions in migratory energy expenditure. This modeling of simulated thermalscapes provides a framework for assessing the contribution of cold-water refuges to the success of migrating fishes, but any final determination will depend on analyzing fish survival and health for their entire migration, water temperature management goals and species recovery targets.

Temperature and depth profiles of Chinook salmon and the energetic costs of their long-distance homing migrations.

River warming poses an existential threat to many Pacific salmon (Oncorhynchus spp) populations. However, temperature-mediated risks to salmon are often complex and addressing them requires species- and population-specific data collected over large spatial and temporal scales. In this study, we combined radiotelemetry with archival depth and temperature sensors to collect continuous thermal exposure histories of 21 adult spring- and summer-run Chinook salmon (O. tshawytscha) as they migrated hundreds of kilometers upstream in the Columbia River basin. Salmon thermal histories in impounded reaches of the Columbia and Snake rivers were characterized by low daily temperature variation but frequent and extensive vertical movements. Dives were associated with slightly cooler salmon body temperatures (~ 0.01 to 0.02 °C/m), but there was no evidence for use of cool-water thermal refuges deep in reservoirs or at tributary confluences along the migration route. In tributaries, salmon were constrained to relatively shallow water, and they experienced ~ 2-5 °C diel temperature fluctuations. Differences in migration timing and among route-specific thermal regimes resulted in substantial among-individual variation in migration temperature exposure. Bioenergetics models using the collected thermal histories and swim speeds ranging from 1.0 to 1.5 body-lengths/s predicted median energetic costs of ~ 24-40% (spring-run) and ~ 37-60% (summer-run) of initial reserves. Median declines in total mass were ~ 16-24% for spring-run salmon and ~ 19-29% for summer-run salmon. A simulated + 2 °C increase in water temperatures resulted in 4.0% (spring-run) and 6.3% (summer-run) more energy used per fish, on average. The biotelemetry data provided remarkable spatial and temporal resolution on thermal exposure. Nonetheless, substantial information gaps remain for the development of robust bioenergetics and climate effects models for adult Chinook salmon.

Thermal exposure of adult Chinook salmon and steelhead: Diverse behavioral strategies in a large and warming river system.

Rising river temperatures in western North America have increased the energetic costs of migration and the risk of premature mortality in many Pacific salmon (Oncorhynchus spp.) populations. Predicting and managing risks for these populations requires data on acute and cumulative thermal exposure, the spatio-temporal distribution of adverse conditions, and the potentially mitigating effects of cool-water refuges. In this study, we paired radiotelemetry with archival temperature loggers to construct continuous, spatially-explicit thermal histories for 212 adult Chinook salmon (O. tshawytscha) and 200 adult steelhead (O. mykiss). The fish amassed ~500,000 temperature records (30-min intervals) while migrating through 470 kilometers of the Columbia and Snake rivers en route to spawning sites in Idaho, Oregon, and Washington. Spring- and most summer-run Chinook salmon migrated before river temperatures reached annual highs; their body temperatures closely matched ambient temperatures and most had thermal maxima in the lower Snake River. In contrast, many individual fall-run Chinook salmon and most steelhead had maxima near thermal tolerance limits (20-22 °C) in the lower Columbia River. High temperatures elicited extensive use of thermal refuges near tributary confluences, where body temperatures were ~2-10 °C cooler than the adjacent migration corridor. Many steelhead used refuges for weeks or more whereas salmon use was typically hours to days, reflecting differences in spawn timing. Almost no refuge use was detected in a ~260-km reach where a thermal migration barrier may more frequently develop in future warmer years. Within population, cumulative thermal exposure was strongly positively correlated (0.88 ≤ r ≤ 0.98) with migration duration and inconsistently associated (-0.28 ≤ r ≤ 0.09) with migration date. All four populations have likely experienced historically high mean and maximum temperatures in recent years. Expected responses include population-specific shifts in migration phenology, increased reliance on patchily-distributed thermal refuges, and natural selection favoring temperature-tolerant phenotypes.

Thermal exposure of adult Chinook salmon in the Willamette River basin.

Radiotelemetry and archival temperature loggers were used to reconstruct the thermal experience of adult spring Chinook salmon (Oncorhynchus tshawytscha) in the highly regulated Willamette River system in Oregon. The study population is threatened and recovery efforts have been hampered by episodically high prespawn mortality that is likely temperature mediated. Over three years, 310 salmon were released with thermal loggers and 68 were recovered in spawning tributaries, primarily at hatchery trapping facilities downstream from high-head dams. More than 190,000 internal body temperature records were collected (mean ~2800 per fish) and associated with 14 main stem and tributary reaches. Most salmon experienced a wide temperature range (minima ~8-10 °C; maxima ~13-22 °C) and 65% encountered potentially stressful conditions (≥18 °C). The warmest salmon temperatures were in lower Willamette River reaches, where some fish exhibited short-duration behavioral thermoregulation. Cumulative temperature exposure, measured by degree days (DD) above 0 °C, varied more than seven-fold among individuals (range=208-1498 DDs) and more than two-fold among sub-basin populations, on average. Overall, ~72% of DDs accrued in tributaries and ~28% were in the Willamette River main stem. DD differences among individuals and populations were related to migration distance, migration duration, and salmon trapping protocols (i.e., extended pre-collection holding in tributaries versus hatchery collection shortly after tributary entry). The combined data provide spatially- and temporally-referenced information on both short-duration stressful temperature exposure and the biologically important total exposure. Thermal exposure in this population complex proximately influences adult salmon physiology, maturation, and disease processes and ultimately affects prespawn mortality and fitness. The results should help managers develop more effective salmon recovery plans in basins with marginal thermal conditions.

Genes predict long distance migration and large body size in a migratory fish, Pacific lamprey.

Elucidation of genetic mechanisms underpinning migratory behavior could help predict how changes in genetic diversity may affect future spatiotemporal distribution of a migratory species. This ability would benefit conservation of one such declining species, anadromous Pacific lamprey (Entosphenus tridentatus). Nonphilopatric migration of adult Pacific lamprey has homogenized population-level neutral variation but has maintained adaptive variation that differentiates groups based on geography, run-timing and adult body form. To investigate causes for this adaptive divergence, we examined 647 adult lamprey sampled at a fixed location on the Columbia River and radiotracked during their subsequent upstream migration. We tested whether genetic variation [94 neutral and adaptive single nucleotide polymorphisms (SNPs) previously identified from a genomewide association study] was associated with phenotypes of migration distance, migration timing, or morphology. Three adaptive markers were strongly associated with morphology, and one marker also correlated with upstream migration distance and timing. Genes physically linked with these markers plausibly influence differences in body size, which is also consistently associated with migration distance in Pacific lamprey. Pacific lamprey conservation implications include the potential to predict an individual's upstream destination based on its genotype. More broadly, the results suggest a genetic basis for intrapopulation variation in migration distance in migratory species.

Indirect effects of impoundment on migrating fish: temperature gradients in fish ladders slow dam passage by adult Chinook salmon and steelhead.

Thermal layering in reservoirs upstream from hydroelectric dams can create temperature gradients in fishways used by upstream migrating adults. In the Snake River, Washington, federally-protected adult salmonids (Oncorhynchus spp.) often encounter relatively cool water in dam tailraces and lower ladder sections and warmer water in the upstream portions of ladders. Using radiotelemetry, we examined relationships between fish passage behavior and the temperature difference between the top and bottom of ladders (∆T) at four dams over four years. Some spring Chinook salmon (O. tshawytscha) experienced ∆T ≥ 0.5 °C. Many summer and fall Chinook salmon and summer steelhead (O. mykiss) experienced ∆T ≥ 1.0 °C, and some individuals encountered ΔT > 4.0°C. As ΔT increased, migrants were consistently more likely to move down fish ladders and exit into dam tailraces, resulting in upstream passage delays that ranged from hours to days. Fish body temperatures equilibrated to ladder temperatures and often exceeded 20°C, indicating potential negative physiological and fitness effects. Collectively, the results suggest that gradients in fishway water temperatures present a migration obstacle to many anadromous migrants. Unfavorable temperature gradients may be common at reservoir-fed fish passage facilities, especially those with seasonal thermal layering or stratification. Understanding and managing thermal heterogeneity at such sites may be important for ensuring efficient upstream passage and minimizing stress for migratory, temperature-sensitive species.

Transporting juvenile salmonids around dams impairs adult migration.

Mitigation and ecosystem-restoration efforts may have unintended consequences on both target and nontarget populations. Important effects can be displaced in space and time, making them difficult to detect without monitoring at appropriate scales. Here, we examined the effects of a mitigation program for juvenile salmonids on subsequent adult migration behaviors and survival. Juvenile chinook salmon (Oncorhynchus tshawytscha) and steelhead (O. mykiss) were collected and uniquely tagged with passive integrated transponder (PIT) tags at Lower Granite Dam (Washington State, USA) on the Snake River and were then either transported downstream in barges in an effort to reduce out-migration mortality or returned to the river as a control group. Returning adults were collected and radio-tagged at Bonneville Dam (Washington-Oregon, USA) on the Columbia River 1-3 years later and then monitored during approximately 460 km of their homing migrations. The proportion of adults successfully homing was significantly lower, and unaccounted loss and permanent straying into non-natal rivers was higher, for barged fish of both species. On average, barged fish homed to Lower Granite Dam at rates about 10% lower than for in-river migrants. Barged fish were also 1.7-3.4 times more likely than in-river fish to fall back downstream past dams as adults, a behavior strongly associated with lower survival. These results suggest that juvenile transport impaired adult orientation or homing abilities, perhaps by disrupting sequential imprinting processes during juvenile out-migration. While juvenile transportation has clear short-term juvenile-survival benefits, the delayed effects that manifest in adult stages illustrate the need to assess mitigation success throughout the life cycle of target organisms, i.e., the use of fitness-based measures. In the case of Snake River salmonids listed under the Endangered Species Act, the increased straying and potential associated genetic and demographic effects may represent significant risks to successful recovery for both target and nontarget populations.