Biological and environmental covariates of juvenile sockeye salmon distribution and abundance in the southeastern Bering Sea, 2002-2018.

Climate change is altering the distribution and abundance of marine species, especially in Arctic and sub-Arctic regions. In the eastern Bering Sea, home of the world's largest run of sockeye salmon (Oncorhynchus nerka), juvenile sockeye salmon abundance has increased and their migration path shifted north with warming, 2002-2018. The reasons for these changes are poorly understood. For these sockeye salmon, we quantify environmental and biological covariate effects within spatio-temporal species distribution models. Spatio-temporally, with respect to juvenile sockeye salmon densities: (1) sea surface temperature had a nonlinear effect, (2) large copepod, Calanus, a minor prey item, had no effect, (3) age-0 pollock (Gadus chalcogrammus), a major prey item during warm years, had a positive linear effect, and (4) juvenile pink salmon (O. gorbuscha) had a positive linear effect. Temporally, annual biomass of juvenile sockeye salmon was nonlinearly related to sea temperature and positively related to age-0 pollock and juvenile pink salmon abundance. Results indicate that sockeye salmon distributed with and increased in abundance with increases in prey, and reached a threshold for optimal temperatures in the eastern Bering Sea. Changes in population dynamics and distribution of sockeye salmon in response to environmental variability have potential implications for projecting specific future food securities and management of fisheries in Arctic waters.

Reliability of trans-generational genetic mark-recapture (tGMR) for enumerating Pacific salmon.

As Pacific salmon (Oncorhynchus spp.) decline across much of their range, it is imperative to further develop minimally invasive tools to quantify population abundance. One such advancement, trans-generational genetic mark-recapture (tGMR), uses parentage analysis to estimate the size of wild populations. Our study examined the precision and accuracy of tGMR through a comparison to a traditional mark-recapture estimate for Chilkat River Chinook salmon (O. tshawytscha) in Southeast Alaska. We examined how adult sampling location and timing impact tGMR by comparing estimates derived using samples collected in the lower river mainstem to those using samples obtained in upriver spawning tributaries. Results indicated that tGMR estimates using a representative sample of mainstem adults were most concordant with, and 3% more precise than, the traditional mark-recapture estimate for this stock. Importantly, the timing and location of adult sampling were found to impact abundance estimates, depending on what proportion of the population dies or moves to unsampled areas between downriver and upriver sampling events. Additionally, we identified potential sources of bias in tGMR arising from violations of key assumptions using a novel individual-based modeling framework, parameterized with empirical values from the Chilkat River. Simulations demonstrated that increased reproductive success and sampling selectivity of older, larger individuals, introduced negative bias into tGMR estimates. Our individual-based model offers a customizable and accessible method to identify and quantify these biases in tGMR applications (https://github.com/swrosenbaum/tGMR_simulations). We underscore the critical role of system-specific sampling design considerations in ensuring the precision and accuracy of tGMR projects. This study validates tGMR as a potentially useful tool for improved population enumeration in semelparous species.

Alternative life-history strategy contributions to effective population size in a naturally spawning salmon population.

Alternative life-history tactics are predicted to affect within-population genetic processes but have received little attention. For example, the impact of precocious males on effective population size (N e) has not been quantified directly in Pacific salmon Oncorhynchus spp., even though they can make up a large percentage of the total male spawners. We investigated the contribution of precocial males ("jacks") to N e in a naturally spawning population of Coho Salmon O. kisutch from the Auke Creek watershed in Juneau, Alaska. Mature adults that returned from 2009 to 2019 (~8000 individuals) were genotyped at 259 single-nucleotide polymorphism (SNP) loci for parentage analysis. We used demographic and genetic methods to estimate the effective number of breeders per year (N b). Jack contribution to N b was assessed by comparing values of N b calculated with and without jacks and their offspring. Over a range of N b values (108-406), the average jack contribution to N b from 2009 to 2015 was 12.9% (SE = 3.8%). Jacks consistently made up over 20% of the total male spawners. The presence of jacks did not seem to influence N b/N. The linkage disequilibrium N e estimate was lower than the demographic estimate, possibly due to immigration effects on population genetic processes: based on external marks and parentage data, we estimated that immigrant spawners produced 4.5% of all returning offspring. Our results demonstrate that jacks can influence N b and N e and can make a substantial contribution to population dynamics and conservation of threatened stocks.

Prior choice and data requirements of Bayesian multivariate hierarchical models fit to tag-recovery data: The need for power analyses.

Recent empirical studies have quantified correlation between survival and recovery by estimating these parameters as correlated random effects with hierarchical Bayesian multivariate models fit to tag-recovery data. In these applications, increasingly negative correlation between survival and recovery has been interpreted as evidence for increasingly additive harvest mortality. The power of these hierarchal models to detect nonzero correlations has rarely been evaluated, and these few studies have not focused on tag-recovery data, which is a common data type. We assessed the power of multivariate hierarchical models to detect negative correlation between annual survival and recovery. Using three priors for multivariate normal distributions, we fit hierarchical effects models to a mallard (Anas platyrhychos) tag-recovery data set and to simulated data with sample sizes corresponding to different levels of monitoring intensity. We also demonstrate more robust summary statistics for tag-recovery data sets than total individuals tagged. Different priors led to substantially different estimates of correlation from the mallard data. Our power analysis of simulated data indicated most prior distribution and sample size combinations could not estimate strongly negative correlation with useful precision or accuracy. Many correlation estimates spanned the available parameter space (-1,1) and underestimated the magnitude of negative correlation. Only one prior combined with our most intensive monitoring scenario provided reliable results. Underestimating the magnitude of correlation coincided with overestimating the variability of annual survival, but not annual recovery. The inadequacy of prior distributions and sample size combinations previously assumed adequate for obtaining robust inference from tag-recovery data represents a concern in the application of Bayesian hierarchical models to tag-recovery data. Our analysis approach provides a means for examining prior influence and sample size on hierarchical models fit to capture-recapture data while emphasizing transferability of results between empirical and simulation studies.

Can late stage marine mortality explain observed shifts in age structure of Chinook salmon?

Chinook salmon (Oncorhynchus tshawytscha) populations have experienced widespread declines in abundance and abrupt shifts toward younger and smaller adults returning to spawn in rivers. The causal agents underpinning these shifts are largely unknown. Here we investigate the potential role of late-stage marine mortality, defined as occurring after the first winter at sea, in driving this species' changing age structure. Simulations using a stage-based life cycle model that included additional mortality during after the first winter at sea better reflected observed changes in the age structure of a well-studied and representative population of Chinook salmon from the Yukon River drainage, compared with a model estimating environmentally-driven variation in age-specific survival alone. Although the specific agents of late-stage mortality are not known, our finding is consistent with work reporting predation by salmon sharks (Lamna ditropis) and marine mammals including killer whales (Orcinus orca). Taken as a whole, this work suggests that Pacific salmon mortality after the first winter at sea is likely to be higher than previously thought and highlights the need to investigate selective sources of mortality, such as predation, as major contributors to rapidly changing age structure of spawning adult Chinook salmon.

Watershed-scale climate influences productivity of Chinook salmon populations across southcentral Alaska.

The ecosystems supporting Pacific salmon (Oncorhynchus spp.) are changing rapidly as a result of climate change and habitat alteration. Understanding how-and how consistently-salmon populations respond to changes at regional and watershed scales has major implications for fisheries management and habitat conservation. Chinook salmon (O. tshawytscha) populations across Alaska have declined over the past decade, resulting in fisheries closures and prolonged impacts to local communities. These declines are associated with large-scale climate drivers, but uncertainty remains about the role of local conditions (e.g., precipitation, streamflow, and stream temperature) that vary among the watersheds where salmon spawn and rear. We estimated the effects of these and other environmental indicators on the productivity of 15 Chinook salmon populations in the Cook Inlet basin, southcentral Alaska, using a hierarchical Bayesian stock-recruitment model. Salmon spawning during 2003-2007 produced 57% fewer recruits than the previous long-term average, leading to declines in adult returns beginning in 2008. These declines were explained in part by density dependence, with reduced population productivity following years of high spawning abundance. Across all populations, productivity declined with increased precipitation during the fall spawning and early incubation period and increased with above-average precipitation during juvenile rearing. Above-average stream temperatures during spawning and rearing had variable effects, with negative relationships in many warmer streams and positive relationships in some colder streams. Productivity was also associated with regional indices of streamflow and ocean conditions, with high variability among populations. The cumulative effects of adverse conditions in freshwater, including high spawning abundance, heavy fall rains, and hot, dry summers may have contributed to the recent population declines across the region. Identifying both coherent and differential responses to environmental change underscores the importance of targeted, watershed-specific monitoring and conservation efforts for maintaining resilient salmon runs in a warming world.

The changing physical and ecological meanings of North Pacific Ocean climate indices.

Climate change is likely to change the relationships between commonly used climate indices and underlying patterns of climate variability, but this complexity is rarely considered in studies using climate indices. Here, we show that the physical and ecological conditions mapping onto the Pacific Decadal Oscillation (PDO) index and North Pacific Gyre Oscillation (NPGO) index have changed over multidecadal timescales. These changes apparently began around a 1988/1989 North Pacific climate shift that was marked by abrupt northeast Pacific warming, declining temporal variance in the Aleutian Low (a leading atmospheric driver of the PDO), and increasing correlation between the PDO and NPGO patterns. Sea level pressure and surface temperature patterns associated with each climate index changed after 1988/1989, indicating that identical index values reflect different states of basin-scale climate over time. The PDO and NPGO also show time-dependent skill as indices of regional northeast Pacific ecosystem variability. Since the late 1980s, both indices have become less relevant to physical-ecological variability in regional ecosystems from the Bering Sea to the southern California Current. Users of these climate indices should be aware of nonstationary relationships with underlying climate variability within the historical record, and the potential for further nonstationarity with ongoing climate change.

Independent lineages in a common environment: the roles of determinism and contingency in shaping the migration timing of even- versus odd-year pink salmon over broad spatial and temporal scales.

Studies of parallel evolution are seldom able to disentangle the influence of cryptic environmental variation from that of evolutionary history; whereas the unique life history of pink salmon (Oncorhynchus gorbuscha) presents an opportunity to do so. All pink salmon mature at age two and die after breeding. Hence, pink salmon bred in even years are completely reproductively isolated from those bred in odd years, even if the two lineages bred in same location. We used time series (mean = 7 years, maximum = 74 years) of paired even- and odd-year populations from 36 rivers spanning over 2000 km to explore parallelism in migration timing, a trait with a strong genetic basis. Migration timing was highly parallel, being determined almost entirely by local environmental differences among rivers. Interestingly, interannual changes in migration timing different somewhat between lineages. Overall, our findings indicate very strong determinism, with only a minor contribution of contingency.

Alaskan brown bears (Ursus arctos) aggregate and display fidelity to foraging neighborhoods while preying on Pacific salmon along small streams.

The interaction between brown bears (Ursus arctos) and Pacific salmon (Oncorhynchus spp.) is important to the population dynamics of both species and a celebrated example of consumer-mediated nutrient transport. Yet, much of the site-specific information we have about the bears in this relationship comes from observations at a few highly visible but unrepresentative locations and a small number of radio-telemetry studies. Consequently, our understanding of brown bear abundance and behavior at more cryptic locations where they commonly feed on salmon, including small spawning streams, remains limited. We employed a noninvasive genetic approach (barbed wire hair snares) over four summers (2012-2015) to document patterns of brown bear abundance and movement among six spawning streams for sockeye salmon, O. nerka, in southwestern Alaska. The streams were grouped into two trios on opposite sides of Lake Aleknagik. Thus, we predicted that most bears would forage within only one trio during the spawning season because of the energetic costs associated with swimming between them or traveling around the lake and show fidelity to particular trios across years because of the benefits of familiarity with local salmon dynamics and stream characteristics. Huggins closed-capture models based on encounter histories from genotyped hair samples revealed that as many as 41 individuals visited single streams during the annual 6-week sampling season. Bears also moved freely among trios of streams but rarely moved between these putative foraging neighborhoods, either during or between years. By implication, even small salmon spawning streams can serve as important resources for brown bears, and consistent use of stream neighborhoods by certain bears may play an important role in spatially structuring coastal bear populations. Our findings also underscore the efficacy of noninvasive hair snagging and genetic analysis for examining bear abundance and movements at relatively fine spatial and temporal scales.

Signals of large scale climate drivers, hatchery enhancement, and marine factors in Yukon River Chinook salmon survival revealed with a Bayesian life history model.

Understanding how species might respond to climate change involves disentangling the influence of co-occurring environmental factors on population dynamics, and is especially problematic for migratory species like Pacific salmon that move between ecosystems. To date, debate surrounding the causes of recent declines in Yukon River Chinook salmon (Oncorhynchus tshawytscha) abundance has centered on whether factors in freshwater or marine environments control variation in survival, and how these populations at the northern extremity of the species range will respond to climate change. To estimate the effect of factors in marine and freshwater environments on Chinook salmon survival, we constructed a stage-structured assessment model that incorporates the best available data, estimates incidental marine bycatch mortality in trawl fisheries, and uses Bayesian model selection methods to quantify support for alternative hypotheses. Models fitted to two index populations of Yukon River Chinook salmon indicate that processes in the nearshore and marine environments are the most important determinants of survival. Specifically, survival declines when ice leaves the Yukon River later in the spring, increases with wintertime temperature in the Bering Sea, and declines with the abundance of globally enhanced salmon species consistent with competition at sea. In addition, we found support for density-dependent survival limitations in freshwater but not marine portions of the life cycle, increasing average survival with ocean age, and age-specific selectivity of bycatch mortality in the Bering Sea. This study underscores the utility of flexible estimation models capable of fitting multiple data types and evaluating mortality from both natural and anthropogenic sources in multiple habitats. Overall, these analyses suggest that mortality at sea is the primary driver of population dynamics, yet under warming climate Chinook salmon populations at the northern extent of the species' range may be expected to fare better than southern populations, but are influenced by foreign salmon production.

Diverse foraging opportunities drive the functional response of local and landscape-scale bear predation on Pacific salmon.

The relationship between prey abundance and predation is often examined in single habitat units or populations, but predators may occupy landscapes with diverse habitats and foraging opportunities. The vulnerability of prey within populations may depend on habitat features that hinder predation, and increased density of conspecifics in both the immediate vicinity and the broader landscape. We evaluated the relative effects of physical habitat, local, and neighborhood prey density on predation by brown bears on sockeye salmon in a suite of 27 streams using hierarchical Bayesian functional response models. Stream depth and width were inversely related to the maximum proportion of salmon killed, but not the asymptotic limit on total number killed. Interannual variation in predation was density dependent; the number of salmon killed increased with fish density in each stream towards an asymptote. Seven streams in two geographical groups with ≥23 years of data in common were then analyzed for neighborhood density effects. In most (12 of 18) cases predation in a stream was reduced by increasing salmon abundance in neighboring streams. The uncertainty in the estimates for these neighborhood effects may have resulted from interactions between salmon abundance and habitat that influenced foraging by bears, and from bear behavior (e.g., competitive exclusion) and abundance. Taken together, the results indicated that predator-prey interactions depend on density at multiple spatial scales, and on habitat features of the surrounding landscape. Explicit consideration of this context dependency should lead to improved understanding of the ecological impacts of predation across ecosystems and taxa.

Can intense predation by bears exert a depensatory effect on recruitment in a Pacific salmon population?

It has long been recognized that, as populations increase in density, ecological processes affecting growth and survival reduce per capita recruitment in the next generation. In contrast to the evidence for such "compensatory" density dependence, the alternative "depensatory" process (reduced per capita recruitment at low density) has proven more difficult to demonstrate in the field. To test for such depensation, we measured the spawner-recruit relationship over five decades for a sockeye salmon (Oncorhynchus nerka) population in Alaska breeding in high-quality, unaltered habitat. Twenty-five years of detailed estimates of predation by brown bears, Ursus arctos, revealed strong density dependence in predation rate; the bears killed ca. 80% of the salmon in years of low salmon spawning abundance. Nevertheless, the reconstructed spawner-recruit relationship, adjusted to include salmon intercepted in the commercial fishery, provided no evidence of demographic depensation. That is, in years when few salmon returned and the great majority were killed by bears, the few that spawned were successful enough that the population remained highly productive, even when those killed by bears were included as potential spawners. We conclude that the high quality of breeding habitat at this site and the productive nature of semelparous Pacific salmon allowed this population to avoid the hypothesized depressed recruitment from depensatory processes expected at low density. The observed lack of demographic depensation is encouraging from a conservation standpoint because it implies that depleted populations may have the potential to rebound successfully given suitable spawning and rearing habitat, even in the presence of strong predation pressure.

Evolutionary rescue in a changing world.

Evolutionary rescue occurs when adaptive evolutionary change restores positive growth to declining populations and prevents extinction. Here we outline the diagnostic features of evolutionary rescue and distinguish this phenomenon from demographic and genetic rescue. We then synthesize the rapidly accumulating theoretical and experimental studies of evolutionary rescue, highlighting the demographic, genetic, and extrinsic factors that affect the probability of rescue. By doing so, we clarify the factors to target through management and conservation. Additionally, we identify several putative cases of evolutionary rescue in nature, but conclude that compelling evidence remains elusive. We conclude with a horizon scan of where the field might develop, highlighting areas of potential application, and suggest areas where experimental evaluation will help to evaluate theoretical predictions.

Size selectivity of predation by brown bears depends on the density of their sockeye salmon prey.

Can variation in prey density drive changes in the intensity or direction of selective predation in natural systems? Despite ample evidence of density-dependent selection, the influence of prey density on predatory selection patterns has seldom been investigated empirically. We used 20 years of field data on brown bears (Ursus arctos) foraging on sockeye salmon (Oncorhynchus nerka) in Alaska, to test the hypothesis that salmon density affects the strength of size-selective predation. Measurements from 41,240 individual salmon were used to calculate variance-standardized selection differentials describing the direction and magnitude of selection. Across the time series, the intensity of predatory selection was inversely correlated with salmon density; greater selection for smaller salmon occurred at low salmon densities as bears' tendency to kill larger-than-average salmon was magnified. This novel connection between density dependence and selective predation runs contrary to some aspects of optimal foraging theory and differs from many observations of density-dependent selection because (1) the direction of selection remains constant while its magnitude changes as a function of density and (2) stronger selection is observed at low abundance. These findings indicate that sockeye salmon may be subject to fishery-induced size selection from both direct mechanisms and latent effects of altered predatory selection patterns on the spawning grounds, resulting from reduced salmon abundance.