Elevated stream temperature, origin, and individual size influence Chinook salmon prespawn mortality across the Columbia River Basin
Graphical abstract
Introduction
Each year, fisheries managers expend considerable effort to ensure that sufficient numbers of adult Pacific salmon Oncorhynchus spp. return to their natal habitats to reproduce. These efforts include limitations on the extent and duration of commercial and recreational fisheries (Mundy, 1997; Wang et al., 2018), trap and transport of adult salmon around impassable dams (Keefer et al., 2010; Lusardi and Moyle, 2017), and removal or non-lethal deterrence of marine mammals (Keefer et al., 2012; Schakner and Blumstein, 2013). However, the desired outcome of these actions—more reproducing fish—can be severely hampered by mortality along the migration route (termed en route mortality) and on the breeding grounds prior to completion of spawning (termed prespawn mortality; Gilhousen et al., 1990). Recent declines in several salmon populations have been attributed to high rates of adult mortality after their return to freshwater (Hinch et al., 2012). A combination of targeted studies and anecdotal evidence suggests that the phenomenon has increased in prevalence and scope in recent decades (Barnett et al., 2020; Hinch et al., 2012; Scholz et al., 2011), and reports of episodic salmon die-off events have become more common (Westley, 2020).
Anthropogenic and environmental factors can contribute to elevated premature mortality rates for adult salmon after they return to freshwater. En route mortality has been associated with exposure to pathogens (Hinch et al., 2012; Kocan et al., 2004) and environmental factors, such as elevated water temperatures (Farrell et al., 2008; Keefer et al., 2008; Martins et al., 2012) and high flow conditions (Martins et al., 2012; Minke-Martin et al., 2018). Environmental stressors and pathogens may in turn increase metabolic costs, leading to energetic depletion prior to reaching spawning grounds (Rand et al., 2006), since Pacific salmon cease feeding upon entering freshwater and energy stores steadily decrease until death (Brett, 1995).
In some cases, prespawn mortality may occur as a delayed result of the conditions encountered during migration (Minke-Martin et al., 2018). In other cases, salmon acquire diseases or encounter environmental conditions after arriving at the spawning grounds that may lead to physiological stress and reduced energy stores (Quinn et al., 2007). Depending on the salmon species and population, the period between arrival on spawning grounds and spawning can range from several days to many months (Quinn et al., 2016), so the effect of migration versus holding conditions varies. Understanding how environmental and anthropogenic factors contribute to premature death is important for fisheries forecasts and population recovery efforts. In many managed fisheries, escapement goals (the designated number of fish allowed to migrate up river to spawn) are established under the assumption that nearly all fish that escape the fishery go on to spawn (Cunningham et al., 2018). Mortality that occurs upstream of the fishery would therefore not be included in these estimates, potentially leading to lower recruitment than expected for escapement goals. Further, an understanding of factors that lead to prespawn mortality is an important component of salmon population models used to evaluate critical life stages for recovery planning (e.g., Honea et al., 2016; Jorgensen et al., 2009). Population projections indicate that even moderate prespawn mortality rates of 0.20 (i.e., 20 % of females that return to spawning grounds fail to lay eggs) can lead to a dramatic reduction in adult abundance in as few as 20 years and can thereby impede conservation, reintroduction, and restoration efforts (Spromberg and Scholz, 2011).
Prespawn mortality has been linked to a range of factors across Pacific salmon species, including elevated water temperatures (Barnett et al., 2020; Bowerman et al., 2018), infectious pathogens (Benda et al., 2015; Bradford et al., 2010), and pollutants in urban run-off (Scholz et al., 2011; Spromberg et al., 2015). In many cases, a combination of factors may interact to influence the likelihood of prespawn mortality. For example, high fish density coupled with warm temperatures can lead to anoxic conditions resulting in fish death near spawning grounds (Sergeant et al., 2017; Tillotson and Quinn, 2017). The effect of particular stressors can vary among species (Scholz et al., 2011) and even among individuals within a population. Certain individuals may be more susceptible to prespawn mortality due to the timing of migration or arrival on spawning grounds (Barnett et al., 2020; Hinch et al., 2012; Hruska et al., 2011), river conditions encountered during migration (Minke-Martin et al., 2018), or injuries related to infection, predation, or fisheries interactions (Baker and Schindler, 2009; Keefer et al., 2010). Miller et al. (2011) identified a genomic signature associated with premature mortality in sockeye salmon O. nerka, which the authors hypothesized occurred in response to a viral infection prior to freshwater entry.
Prespawn mortality has been observed in Chinook salmon O. tshawytscha populations throughout their range (Bowerman et al., 2016), but information is limited regarding factors that influence the phenomenon. Chinook salmon, the largest of the Pacific salmon species, have tremendous cultural, economic, and ecological importance throughout the west coast of North America. Chinook salmon express considerable variability in many life-history characteristics, including age at juvenile seaward migration and the timing of adult migration to natal streams (run timing) (Bourret et al., 2016). Populations are distinguished by this latter characteristic, identified as the season in which adults enter freshwater (e.g., spring-, summer-, or fall-run). The freshwater prespawn holding period in most Chinook salmon populations ranges from days (fall-run) to months (spring-, summer-run), as spawning occurs in the fall of the year in which they leave the ocean. Chinook salmon have experienced widespread population declines, and numerous population groups, known as Evolutionarily Significant Units (ESUs), are listed as threatened or endangered under the U.S. Endangered Species Act (National Marine Fisheries Service, 2005). Understanding factors that contribute to prespawn mortality within and among ESUs is therefore an important component in developing recovery plans for at-risk populations.
For many salmon populations, managers estimate annual prespawn mortality rates based on carcasses gathered during routine spawning ground surveys. The purpose of this study was to analyze existing data on individual Chinook salmon carcasses to examine large-scale patterns in potential factors affecting prespawn mortality throughout the diverse Columbia River Basin. First, we standardized data provided by numerous management agencies to calculate annual prespawn mortality rates for Chinook salmon in 49 study reaches in 41 streams over 14 years. Next, we examined the relationship between prespawn mortality and the following factors hypothesized to affect the likelihood of mortality: 1) Work, a measure of migration difficulty which we expected might be positively correlated with mortality; 2) annual stream temperature in the spawning area with the expectation that mortality would increase at higher water temperatures (Bowerman et al., 2018; Gilhousen et al., 1990); 3) origin, whether a fish reared in a hatchery or natural setting, since previous research has shown higher rates of prespawn mortality in populations with more hatchery fish (Bowerman et al., 2018; Young and Blenden, 2011); 4) individual fish length because the likelihood of premature mortality has been associated with fish size (Westley, 2020); and 5) relative date of carcass recovery because mortality risk changes with residence time on spawning grounds (Bowerman et al., 2016; Hruska et al., 2011). Finally, because model results for spring-run ESUs showed clear water temperature effects, we used the statistical model to forecast prespawn mortality rates under predicted future climatic conditions in spring Chinook salmon spawning streams throughout the Columbia River Basin.
Section snippets
Study area and populations
Chinook salmon carcasses were assessed annually during routine spawning ground surveys in 2000 through 2013 by state, federal, and tribal fisheries biologists in tributaries to the Columbia River in Oregon, Idaho, and Washington (Fig. 1). The Columbia River Basin encompasses a 670,000 km2 area that supports numerous spatially and genetically distinct Chinook salmon populations with diverse life-history characteristics, including adult run timing (peak entry into freshwater), spawn timing (peak
Prespawn mortality estimates
The mean annual reach-specific prespawn mortality rate for natural- and hatchery-origin fish combined ranged from 0.00 to 0.82 (mean = 0.17, n = 247 estimates) in the Snake River ESU, 0.00–1.00 in the Mid-Columbia ESU (mean = 0.12, n = 126), 0.04–0.40 in the Upper Columbia spring ESU (mean = 0.06, n = 94), and 0.00 to 0.87 in the Upper Columbia summer ESU (mean = 0.09, n = 92) (Table 1). When averaged across years and study reaches, mean estimates were 0.13 higher for hatchery-origin compared
Patterns of prespawn mortality across the Columbia River Basin
Although there was considerable variability in prespawn mortality rates within and among study reaches in the large dataset collected by many different groups across a wide geographic range, associations between prespawn mortality and individual- and reach- scale factors were fairly consistent for all three spring-run Chinook ESUs. After accounting for variability in carcass sampling date, the probability of prespawn mortality increased with mean August stream temperature within each of the
CRediT authorship contribution statement
Tracy E. Bowerman: Data curation, Formal analysis, Methodology, Visualization, Writing - original draft, Writing - review & editing. Matthew L. Keefer: Conceptualization, Writing - review & editing. Christopher C. Caudill: Funding acquisition, Resources, Supervision, Conceptualization, Writing - review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank the many individuals who collected data used in this research, and specifically those who generously shared data with the University of Idaho and fielded questions along the way: Kim Apperson, William Bosch, Carrie Bretz, Craig Contor, Matt Corsi, Andrew Dittman, Joseph Feldhaus, Ryan Gerstenberger, Ryan Kinzer, Brian Mahoney, Jordan Messner, Andrew Murdoch, Craig Rabe, James Ruzycki, Robette Schmit, Steve Schonning, Ian Tattam, David Venditti, Bill Young, Joseph Zendt. The Fish
References (91)
- et al.
Increased prespawning mortality threatens an integrated natural-and hatchery-origin sockeye salmon population in the Lake Washington Basin
Fish. Res.
(2020) - et al.
Increasing water temperature and disease risks in aquatic systems: climate change increases the risk of some, but not all, diseases
Int. J. Parasitol.
(2010) - et al.
Temperature and depth profiles of Chinook salmon and the energetic costs of their long-distance homing migrations
J. Therm. Biol.
(2019) - et al.
Behavioral biology of marine mammal deterrents: a review and prospectus
Biol. Conserv.
(2013) - et al.
Climate and conspecific density trigger pre-spawning mortality in sockeye salmon (Oncorhynchus nerka)
Fish. Res.
(2017) - et al.
Unaccounted mortality in salmon fisheries: non-retention in gillnets and effects on estimates of spawners
J. Appl. Ecol.
(2009) MuMIn: Multi-Model Inference. R Package Version 1.42.1
(2018)- et al.
Fitting linear mixed-effects models using lme4
J. Stat. Softw.
(2015) - et al.
Cool, pathogen-free refuge lowers pathogen-associated prespawn mortality of Willamette River Chinook Salmon
Trans. Am. Fish. Soc.
(2015) - et al.
Diversity of juvenile Chinook salmon life history pathways
Rev. Fish Biol. Fish.
(2016)
Pacific salmon prespawn mortality: patterns, methods, and study design considerations
Fisheries
Prespawn mortality of female Chinook Salmon increases with water temperature and percent hatchery origin
Trans. Am. Fish. Soc.
Parvicapsula minibicornis infections in gill and kidney and the premature mortality of adult sockeye salmon (Oncorhynchus nerka) from Cultus Lake, British Columbia
Can. J. Fish. Aquat. Sci.
Energetics
Model Selection and Multimodel Inference
Identifying optimal hauling densities for adult Chinook salmon trap and haul operations
River Res. Appl.
Umatilla Basin natural production monitoring and evaluation, 2011 annual progress report
Abnormal migration timing and high en route mortality of sockeye salmon in the Fraser River, British Columbia
Fisheries
Physiology of individual late-run Fraser River sockeye salmon (Oncorhynchus nerka) sampled in the ocean correlates with fate during spawning migration
Can. J. Fish. Aquat. Sci.
Experimental evaluation of adult spring Chinook Salmon radio-tagged during the late stages of spawning migration
N. Am. J. Fish. Manag.
Somatic energy of sockeye salmon Oncorhynchus nerka at the onset of upriver migration: a comparison among ocean climate regimes
Fish. Oceanogr.
Exposure to high temperature influences the behaviour, physiology, and survival of sockeye salmon during spawning migration
Can. J. Zool.
Potential responses to climate change in organisms with complex life histories: evolution and plasticity in Pacific salmon
Evol. Appl.
Refining Our Understanding of Early and Late Migration of Adult Upper Columbia spring and Snake River Spring/Summer Chinook Salmon: Passage Timing, Travel Time, Fallback, and Survival
Climate vulnerability assessment for Pacific salmon and steelhead in the California Current Large Marine Ecosystem
PLoS One
Selecting for the phenotypic optimum: size-related trade-offs between mortality risk and reproductive output in female sockeye salmon
Funct. Ecol.
A hidden-process model for estimating prespawn mortality using carcass survey data
N. Am. J. Fish. Manag.
Homing and spawning site selection by supplemented hatchery- and natural-origin Yakima River spring Chinook salmon
Trans. Am. Fish. Soc.
Selection against late emergence and small offspring in atlantic salmon (Salmo salar)
Evolution
Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations
Physiol. Biochem. Zool.
Prespawning mortalities of sockeye salmon in the Fraser River system and possible causal factors
Effects of size and temperature on metabolic rate
Science
Behavioral thermoregulation and slowed migration by adult fall Chinook salmon in response to high Columbia River water temperatures
Trans. Am. Fish. Soc.
A brief introduction to mixed effects modelling and multi-model inference in ecology
PeerJ
Dharma: Residual Diagnostics for Hierarchical (Multi-Level/ Mixed) Regression Models. R Package Version 0.2.4
Monitoring stock-specific abundance, run timing, and straying of Chinook salmon in the Columbia River using genetic stock identification (GSI)
N. Am. J. Fish. Manag.
Dead fish swimming: a review of research on the early migration and high premature mortality in adult Fraser River sockeye salmon Oncorhynchus nerka
J. Fish Biol.
Run timing, spawn timing, and spawning distribution of hatchery- and natural-origin spring Chinook Salmon in the Imnaha River, Oregon
N. Am. J. Fish. Manag.
Assessing freshwater life-stage vulnerability of an endangered Chinook salmon population to climate change influences on stream habitat
Clim. Res.
Egg retention in relation to arrival timing and reproductive longevity in female sockeye salmon (Oncorhynchus nerka)
Can. J. Fish. Aquat. Sci.
Spawning habitat of hatchery spring Chinook Salmon and possible mechanisms contributing to lower reproductive success
Trans. Am. Fish. Soc.
Impact and adaptation responses of Okanagan River sockeye salmon (Oncorhynchus nerka) to climate variation and change efects during freshwater migration: stock restoration and fisheries management implications
Can. Water Resour. J.
Emissions Scenarios Summary for Policymakers
The NorWeST summer stream temperature model and scenarios for the western U.S.: a crowd-sourced database and new geospatial tools foster a user community and predict broad climate warming of rivers and streams
Water Resour. Res.
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