Elevated stream temperature, origin, and individual size influence Chinook salmon prespawn mortality across the Columbia River Basin

https://doi.org/10.1016/j.fishres.2021.105874Get rights and content

Highlights

  • Warm stream temperatures increased female Chinook salmon prespawn mortality (i.e., mature salmon died prior to laying eggs).

  • Prespawn mortality was also higher for larger salmon and those of hatchery origin.

  • Higher stream temperatures by 2040 are likely to increase prespawn mortality.

  • However, some populations have low prespawn mortality under both current and future expected conditions.

Abstract

Conservation and restoration efforts for Pacific salmon Oncorhynchus spp. can be hampered by prespawn mortality, when adult fish reach reproductive sites but die before spawning. We examined annual estimates of female Chinook salmon O. tshawytscha prespawn mortality relative to individual fish traits (77,707 individual females) and reach-scale variables in 49 study reaches from 41 streams throughout the interior Columbia River Basin. Mean annual prespawn mortality estimates across 14 years ranged from 0 % to 65 %. For spring-run Chinook salmon, the probability of prespawn mortality decreased over the spawning period, was positively associated with mean August stream temperature and individual fish length, and was higher for hatchery-origin than natural-origin fish. Based on the basin-wide statistical model and future stream temperature predictions, average spring-run Chinook salmon prespawn mortality rates in 2040 were predicted to increase by 0–17 % for fish of natural origin and 1–17 % for fish of hatchery origin. Climate change is likely to exacerbate conditions that lead to prespawn mortality, particularly in low elevation stream reaches, for larger fish, and for those of hatchery origin.

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

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