Spatial structuring of an evolving life-history strategy under altered environmental conditions.

Human disturbances to ecosystems have created challenges to populations worldwide, forcing them to respond phenotypically in ways that increase their fitness under current conditions. One approach to examining population responses to disturbance in species with complex life histories is to study species that exhibit spatial patterns in their phenotypic response across populations or demes. In this study, we investigate a threatened population of fall chinook salmon (Oncorhynchus tshawytscha) in the Snake River of Idaho, in which a significant fraction of the juvenile population have been shown to exhibit a yearling out-migration strategy which had not previously been thought to exist. It has been suggested that dam-related environmental changes may have altered the selective pressures experienced by out-migrating fall chinook, driving evolution of a later and more selectively advantageous migration strategy. Using isotopic analysis of otoliths from returning adult spawners, we reconstructed the locations of individual fish at three major juvenile life stages to determine if the representation of the yearling life history was geographically structured within the population. We reconstructed juvenile locations for natal, rearing and overwintering life stages in each of the major spawning areas in the basin. Our results indicate that the yearling life-history strategy is predominantly represented within one of the main spawning regions, the Clearwater River, rather than being distributed throughout the basin. Previous studies have shown the Clearwater River to have cooler temperatures, later hatch dates, and later outmigration of juveniles, indicating a link between environment and expression of the yearling life history. Our data suggest that this new yearling life history may be disproportionally represented in returning adult spawners, indicating selection for this life history within the population.

Effects of population density and environmental conditions on life-history prevalence in a migratory fish.

Individual variation in life-history traits can have important implications for the ability of populations to respond to environmental variability and change. In migratory animals, flexibility in the timing of life-history events, such as juvenile emigration from natal areas, can influence the effects of population density and environmental conditions on habitat use and population dynamics. We evaluated the functional relationships between population density and environmental covariates and the abundance of juveniles expressing different life-history pathways in a migratory fish, Chinook salmon (Oncorhynchus tshawytscha), in the Wenatchee River basin in Washington State, USA. We found that the abundance of younger emigrants from natal streams was best described by an accelerating or near-linear function of spawners, whereas the abundance of older emigrants was best described by a decelerating function of spawners. This supports the hypothesis that emigration timing varies in response to density in natal areas, with younger-emigrating life-history pathways comprising a larger proportion of emigrants when densities of conspecifics are high. We also observed positive relationships between winter stream discharge and abundance of younger emigrants, supporting the hypothesis that habitat conditions can also influence the prevalence of different life-history pathways. Our results suggest that early emigration, and a resultant increase in the use of downstream rearing habitats, may increase at higher population densities and with greater winter precipitation. Winter precipitation is projected to increase in this system due to climate warming. Characterizing relationships between life-history prevalence and environmental conditions may improve our understanding of species habitat requirements and is a first step in understanding the dynamics of species with diverse life-history strategies. As environmental conditions change-due to climate change, management, or other factors-resultant life-history changes are likely to have important demographic implications that will be challenging to predict when life-history diversity is not accounted for in population models.

Using time series analysis to characterize evolutionary and plastic responses to environmental change: a case study of a shift toward earlier migration date in sockeye salmon.

Environmental change can shift the phenotype of an organism through either evolutionary or nongenetic processes. Despite abundant evidence of phenotypic change in response to recent climate change, we typically lack sufficient genetic data to identify the role of evolution. We present a method of using phenotypic data to characterize the hypothesized role of natural selection and environmentally driven phenotypic shifts (plasticity). We modeled historical selection and environmental predictors of interannual variation in mean population phenotype using a multivariate state-space model framework. Through model comparisons, we assessed the extent to which an estimated selection differential explained observed variation better than environmental factors alone. We applied the method to a 60-year trend toward earlier migration in Columbia River sockeye salmon Oncorhynchus nerka, producing estimates of annual selection differentials, average realized heritability, and relative cumulative effects of selection and plasticity. We found that an evolutionary response to thermal selection was capable of explaining up to two-thirds of the phenotypic trend. Adaptive plastic responses to June river flow explain most of the remainder. This method is applicable to other populations with time series data if selection differentials are available or can be reconstructed. This method thus augments our toolbox for predicting responses to environmental change.

Climate change threatens Chinook salmon throughout their life cycle.

Widespread declines in Atlantic and Pacific salmon (Salmo salar and Oncorhynchus spp.) have tracked recent climate changes, but managers still lack quantitative projections of the viability of any individual population in response to future climate change. To address this gap, we assembled a vast database of survival and other data for eight wild populations of threatened Chinook salmon (O. tshawytscha). For each population, we evaluated climate impacts at all life stages and modeled future trajectories forced by global climate model projections. Populations rapidly declined in response to increasing sea surface temperatures and other factors across diverse model assumptions and climate scenarios. Strong density dependence limited the number of salmon that survived early life stages, suggesting a potentially efficacious target for conservation effort. Other solutions require a better understanding of the factors that limit survival at sea. We conclude that dramatic increases in smolt survival are needed to overcome the negative impacts of climate change for this threatened species.

Interacting effects of density and temperature on body size in multiple populations of Chinook salmon.

1. The size individuals attain reflects complex interactions between food availability and quality, environmental conditions and ecological interactions. A statistical interaction between temperature and the density of conspecifics is expected to arise from various ecological dynamics, including bioenergetic constraints, if population density affects mean consumption rate or activity level. Density effects on behaviour or size-selective predation could also generate this pattern. This interaction plays an important role in bioenergetic models, in particular, and yet has not been documented in natural populations. 2. The lengths of 131 286 juvenile wild Chinook salmon (Oncorhynchus tshawytscha) across 13 populations spread throughout the Salmon River Basin, Idaho, USA over 15 years were compared to test whether juvenile density alters the relationship between body size and temperature. 3. Strong evidence for a negative interaction between mean summer temperature and density emerged, despite the relatively cool temperatures in this high elevation habitat. Growth correlated positively with temperature at lower densities, but the correlation was negative at the highest densities. 4. This is the first study to document this interaction at such a large spatial and temporal scale, and suggests that warmer temperatures might intensify some density-dependent processes. How climate change will affect individual growth rates in these populations will depend intimately on ecological conditions, particularly food availability and population dynamics. More broadly, the conditions that led to the interactions observed in our study - limited food availability and temperatures that ranged above those optimal for growth - likely exist for many other natural populations, and warrant broader exploration.

Continuous models of population-level heterogeneity inform analysis of animal dispersal and migration.

Behavioral heterogeneity among individuals is a universal feature of natural populations. Most diffusion-based models of animal dispersal, however, implicitly assume homogeneous movement parameters within a population. Recent attempts to consider the effect of heterogeneous populations on dispersal distributions have been somewhat limited by the high number of parameters required to subdivide a population into several groups. A solution to this problem is to characterize the value of a movement parameter as continuously distributed within a population. We present several cases in which this method is useful and tractable, applying the framework both to spatial distribution data and closely related first passage times. The resulting models allow ecologists to identify the extent to which the variability in dispersal distributions can be attributed to population-level heterogeneity as opposed to intrinsic randomness. We apply the formulation to two very different cases of dispersal: resident organisms in a stream (freshwater chub Nocomis leptocephalus) and migrating organisms (juvenile salmonids Oncorhynchus spp.). In both cases, the application of heterogeneity-explicit models provides insights into the behavioral mechanisms of movement.

Legacy habitat contamination as a limiting factor for Chinook salmon recovery in the Willamette Basin, Oregon, USA.

In the western United States, the long-term recovery of many Pacific salmon populations is inextricably linked to freshwater habitat quality. Industrial activities from the past century have left a legacy of pollutants that persist, particularly near working waterfronts. The adverse impacts of these contaminants on salmon health have been studied for decades, but the population-scale consequences of chemical exposure for salmonids are still poorly understood. We estimated acute and delayed mortality rates for seaward migrating juvenile Chinook salmon that feed and grow in a Superfund-designated area in the Lower Willamette River in Portland, Oregon. We combined previous, field-collected exposure data for juvenile Chinook salmon together with reduced growth and disease resistance data from earlier field and laboratory studies. Estimates of mortality were then incorporated into a life cycle model to explore chemical habitat-related fish loss. We found that 54% improved juvenile survival-potentially as a result of future remediation activities-could increase adult Chinook salmon population abundance by more than 20%. This study provides a framework for evaluating pollution remediation as a positive driver for species recovery.

Conservation planning for freshwater-marine carryover effects on Chinook salmon survival.

Experiences of migratory species in one habitat may affect their survival in the next habitat, in what is known as carryover effects. These effects are especially relevant for understanding how freshwater experience affects survival in anadromous fishes. Here, we study the carryover effects of juvenile salmon passage through a hydropower system (Snake and Columbia rivers, northwestern United States). To reduce the direct effect of hydrosystem passage on juveniles, some fishes are transported through the hydrosystem in barges, while the others are allowed to migrate in-river. Although hydrosystem survival of transported fishes is greater than that of their run-of-river counterparts, their relative juvenile-to-adult survival (hereafter survival) can be less. We tested for carryover effects using generalized linear mixed effects models of survival with over 1 million tagged Chinook salmon, Oncorhynchus tshawytscha (Walbaum) (Salmonidae), migrating in 1999-2013. Carryover effects were identified with rear-type (wild vs. hatchery), passage-type (run-of-river vs. transported), and freshwater and marine covariates. Importantly, the Pacific Decadal Oscillation (PDO) index characterizing cool/warm (i.e., productive/nonproductive) ocean phases had a strong influence on the relative survival of rear- and passage-types. Specifically, transportation benefited wild Chinook salmon more in cool PDO years, while hatchery counterparts benefited more in warm PDO years. Transportation was detrimental for wild Chinook salmon migrating early in the season, but beneficial for later season migrants. Hatchery counterparts benefited from transportation throughout the season. Altogether, wild fish could benefit from transportation approximately 2 weeks earlier during cool PDO years, with still a benefit to hatchery counterparts. Furthermore, we found some support for hypotheses related to higher survival with increased river flow, high predation in the estuary and plume areas, and faster migration and development-related increased survival with temperature. Thus, pre- and within-season information on local- and broad-scale conditions across habitats can be useful for planning and implementing real-time conservation programs.

Assessing spatial covariance among time series of abundance.

For species of conservation concern, an essential part of the recovery planning process is identifying discrete population units and their location with respect to one another. A common feature among geographically proximate populations is that the number of organisms tends to covary through time as a consequence of similar responses to exogenous influences. In turn, high covariation among populations can threaten the persistence of the larger metapopulation. Historically, explorations of the covariance in population size of species with many (>10) time series have been computationally difficult. Here, we illustrate how dynamic factor analysis (DFA) can be used to characterize diversity among time series of population abundances and the degree to which all populations can be represented by a few common signals. Our application focuses on anadromous Chinook salmon (Oncorhynchus tshawytscha), a species listed under the US Endangered Species Act, that is impacted by a variety of natural and anthropogenic factors. Specifically, we fit DFA models to 24 time series of population abundance and used model selection to identify the minimum number of latent variables that explained the most temporal variation after accounting for the effects of environmental covariates. We found support for grouping the time series according to 5 common latent variables. The top model included two covariates: the Pacific Decadal Oscillation in spring and summer. The assignment of populations to the latent variables matched the currently established population structure at a broad spatial scale. At a finer scale, there was more population grouping complexity. Some relatively distant populations were grouped together, and some relatively close populations - considered to be more aligned with each other - were more associated with populations further away. These coarse- and fine-grained examinations of spatial structure are important because they reveal different structural patterns not evident in other analyses.

Using "travel time" data to characterize the behavior of migrating animals.

For migratory species, duration of migration, or "travel time," is often a critical variable in determining the cost of migration. Observed travel times are the result of both environmental factors such as air or water currents and the behavior of individuals. In an effort to distinguish among these components, I developed a migration model based on an advection-diffusion equation that characterizes population movements in terms of two biologically meaningful parameters: migration rate and rate of population spread. I applied the model to travel time data from juvenile chinook salmon (Onchorhynchus tshawytscha), which were tagged during their seaward migration. The tagged fish originated from three separate evolutionarily significant units (ESUs) as classified by the U. S. National Marine Fisheries Service. The model was expanded by allowing migration and diffusion rates to vary with fish length and river flow. Variability in travel times explained by these factors was strikingly similar from year to year within ESUs, and the migratory behavior revealed by the analysis was consistent with the life-history patterns that distinguish the ESUs. The approach presented here is easily adaptable to a wide range of migratory species and may be particularly useful for predicting how at-risk populations respond to variable conditions in regulated or otherwise disturbed migration habitats.

Non-indigenous brook trout and the demise of Pacific salmon: a forgotten threat?

Non-indigenous species may be the most severe environmental threat the world now faces. Fishes, in particular, have been intentionally introduced worldwide and have commonly caused the local extinction of native fish. Despite their importance, the impact of introduced fishes on threatened populations of Pacific salmon has never been systemically examined. Here, we take advantage of several unique datasets from the Columbia River Basin to address the impact of non-indigenous brook trout, Salvelinus fontinalis, on threatened spring/summer-run chinook salmon, Oncorhynchus tshawytscha. More than 41 000 juvenile chinook were individually marked, and their survival in streams without brook trout was nearly double the survival in streams with brook trout. Furthermore, when brook trout were absent, habitat quality was positively associated with chinook survival, but when brook trout were present no relationship between chinook survival and habitat quality was evident. The difference in juvenile chinook survival between sites with, and without, brook trout would increase population growth rate (lambda) by ca. 2.5%. This increase in lambda would be sufficient to reverse the negative population growth observed in many chinook populations. Because many of the populations we investigated occur in wilderness areas, their habitat has been considered pristine; however, our results emphasize that non-indigenous species are present and may have a dramatic impact, even in remote regions that otherwise appear pristine.

Simple assumptions on age composition lead to erroneous conclusions on the nature of density dependence in age-structured populations.

Ecologists have debated the nature of density dependence in natural populations for decades, and efforts to detect density dependence from time series of abundance data have paralleled these debates. Yet due to the correlative nature of time series data, these undertakings have been statistically problematic. Most analyses of density dependence have focused on simple population models (i.e., non-overlapping generations), but in reality most vertebrates exhibit more complex life histories, and this complexity has been incorporated into population models in a variety of ways. Unfortunately, adding complexity to population models can further exacerbate efforts to detect density dependence. We examined the effect of adding age structure when inadequate data exist in support; to demonstrate this effect, we adopted Pacific salmon (Oncorhynchus spp.) as our study organism. Most salmon populations are semelparous and have variable age at maturity. Salmon populations (and many other fish species populations) are typically modeled in terms of numbers of recruits arising from spawners in a given brood year. Recruits are enumerated as they return as adults to spawn, and proper assignment of recruits to brood year requires age information. Unfortunately, while adult counts are common, detailed age information is not. A common practice is to apply long-term averages of age composition to returning adults to "reconstruct" time series of recruits. Here, by conducting simulations and analyzing data from natural populations, we demonstrated that this practice leads to a biased portrayal of density dependence by overestimating recruits from small spawning classes and underestimating recruits from large spawning classes. Also, productivity was overestimated and variance was underestimated, which could lead to overly optimistic predictions of extinction risk or overharvesting.

Evolutionary responses by native species to major anthropogenic changes to their ecosystems: Pacific salmon in the Columbia River hydropower system.

The human footprint is now large in all the Earth's ecosystems, and construction of large dams in major river basins is among the anthropogenic changes that have had the most profound ecological consequences, particularly for migratory fishes. In the Columbia River basin of the western USA, considerable effort has been directed toward evaluating demographic effects of dams, yet little attention has been paid to evolutionary responses of migratory salmon to altered selective regimes. Here we make a first attempt to address this information gap. Transformation of the free-flowing Columbia River into a series of slack-water reservoirs has relaxed selection for adults capable of migrating long distances upstream against strong flows; conditions now favour fish capable of migrating through lakes and finding and navigating fish ladders. Juveniles must now be capable of surviving passage through multiple dams or collection and transportation around the dams. River flow patterns deliver some groups of juvenile salmon to the estuary later than is optimal for ocean survival, but countervailing selective pressures might constrain an evolutionary response toward earlier migration timing. Dams have increased the cost of migration, which reduces energy available for sexual selection and favours a nonmigratory life history. Reservoirs are a benign environment for many non-native species that are competitors with or predators on salmon, and evolutionary responses are likely (but undocumented). More research is needed to tease apart the relative importance of evolutionary vs. plastic responses of salmon to these environmental changes; this research is logistically challenging for species with life histories like Pacific salmon, but results should substantially improve our understanding of key processes. If the Columbia River is ever returned to a quasinatural, free-flowing state, remaining populations might face a Darwinian debt (and temporarily reduced fitness) as they struggle to re-evolve historical adaptations.

Potential for anthropogenic disturbances to influence evolutionary change in the life history of a threatened salmonid.

Although evolutionary change within most species is thought to occur slowly, recent studies have identified cases where evolutionary change has apparently occurred over a few generations. Anthropogenically altered environments appear particularly open to rapid evolutionary change over comparatively short time scales. Here, we consider a Pacific salmon population that may have experienced life-history evolution, in response to habitat alteration, within a few generations. Historically, juvenile fall Chinook salmon (Oncorhynchus tshawytscha) from the Snake River migrated as subyearlings to the ocean. With changed riverine conditions that resulted from hydropower dam construction, some juveniles now migrate as yearlings, but more interestingly, the yearling migration tactic has made a large contribution to adult returns over the last decade. Optimal life-history models suggest that yearling juvenile migrants currently have a higher fitness than subyearling migrants. Although phenotypic plasticity likely accounts for some of the change in migration tactics, we suggest that evolution also plays a significant role. Evolutionary change prompted by anthropogenic alterations to the environment has general implications for the recovery of endangered species. The case study we present herein illustrates the importance of integrating evolutionary considerations into conservation planning for species at risk.

Climate impacts at multiple scales: evidence for differential population responses in juvenile Chinook salmon.

1. We explored differential population responses to climate in 18 populations of threatened spring-summer Chinook salmon Onchorynchus tshawytscha in the Salmon River basin, Idaho. 2. Using data from a long-term mark-release-recapture study of juvenile survival, we found that fall stream flow is the best predictor of average survival across all populations. 3. To determine whether all populations responded similarly to climate, we used a cluster analysis to group populations that had similar annual fluctuations in survival. The populations grouped into four clusters, and different environmental factors were important for different clusters. 4. Survival in two of the clusters was negatively correlated with summer temperature, and survival in the other two clusters was positively correlated with minimum fall stream flow, which in turn depends on snow pack from the previous winter. 5. Using classification and regression tree analysis, we identified stream width and stream temperature as key habitat factors that shape the responses of individual populations to climate. 6. Climate change will likely have different impacts on different populations within this metapopulation, and recognizing this diversity is important for accurately assessing risks.

The interplay between climate variability and density dependence in the population viability of Chinook salmon.

The viability of populations is influenced by driving forces such as density dependence and climate variability, but most population viability analyses (PVAs) ignore these factors because of data limitations. Additionally, simplified PVAs produce limited measures of population viability such as annual population growth rate (lamda) or extinction risk. Here we developed a "mechanistic" PVA of threatened Chinook salmon (Oncorhynchus tshawytscha) in which, based on 40 years of detailed data, we related freshwater recruitment of juveniles to density of spawners, and third-year survival in the ocean to monthly indices of broad-scale ocean and climate conditions. Including climate variability in the model produced important effects: estimated population viability was very sensitive to assumptions of future climate conditions and the autocorrelation contained in the climate signal increased mean population abundance while increasing probability of quasi extinction. Because of the presence of density dependence in the model, however we could not distinguish among alternative climate scenarios through mean lamda values, emphasizing the importance of considering multiple measures to elucidate population viability. Our sensitivity analyses demonstrated that the importance of particular parameters varied across models and depended on which viability measure was the response variable. The density-dependent parameter associated with freshwater recruitment was consistently the most important, regardless of viability measure, suggesting that increasing juvenile carrying capacity is important for recovery.