Habitat modulates population-level responses of freshwater salmon growth to a century of change in climate and competition.

The impacts of climate change are widespread and threaten natural systems globally. Yet, within regions, heterogeneous physical landscapes can differentially filter climate, leading to local response diversity. For example, it is possible that while freshwater lakes are sensitive to climate change, they may exhibit a diversity of thermal responses owing to their unique morphology, which in turn can differentially affect the growth and survival of vulnerable biota such as fishes. In particular, salmonids are cold-water fishes with complex life histories shaped by diverse freshwater habitats that are sensitive to warming temperatures. Here we examine the influence of habitat on the growth of sockeye salmon (Oncorhynchus nerka) in nursery lakes of Canada's Skeena River watershed over a century of change in regional temperature and intraspecific competition. We found that freshwater growth has generally increased over the last century. While growth tended to be higher in years with relatively higher summer air temperatures (a proxy for lake temperature), long-term increases in growth appear largely influenced by reduced competition. However, habitat played an important role in modulating the effect of high temperature. Specifically, growth was positively associated with rising temperatures in relatively deep (>50 m) nursery lakes, whereas warmer temperatures were not associated with a change in growth for fish among shallow lakes. The influence of temperature on growth also was modulated by glacier extent whereby the growth of fish from lakes situated in watersheds with little (i.e., <5%) glacier cover increased with rising temperatures, but decreased with rising temperatures for fish in lakes within more glaciated watersheds. Maintaining the integrity of an array of freshwater habitats-and the processes that generate and maintain them-will help foster a diverse climate-response portfolio for important fish species, which in turn can ensure that salmon watersheds are resilient to future environmental change.

The role of spatial structure in at-risk metapopulation recoveries.

Metapopulations are often managed as a single contiguous population despite the spatial structure underlying their local and regional dynamics. Disturbances from human activities can also be spatially structured with mortality impacts concentrated to just a few local populations among the aggregate. Scale transitions between local and regional processes can generate emergent properties whereby the whole system can fail to recover as quickly as expected for an equivalent single population. Here, we draw on theory and empirical case studies to ask: what is the consequence of spatially structured ecological and disturbance processes on metapopulation recoveries? We suggest that exploring this question could help address knowledge gaps for managing metapopulations including: Why do some metapopulations recover quickly while others remain collapsed? And, what risks are unaccounted for when metapopulations are managed at aggregate scales? First, we used model simulations to examine how scale transitions among ecological and disturbance conditions interact to generate emergent metapopulation recovery outcomes. In general, we found that the spatial structure of disturbance was a strong determinant of recovery outcomes. Specifically, disturbances that unevenly impacted local populations consistently generated the slowest recoveries and highest conservation risks. Ecological conditions that dampened metapopulation recoveries included low dispersal, variable local demography, sparsely connected habitat networks, and spatially and temporally correlated stochastic processes. Second, we illustrate the unexpected challenges of managing metapopulations by examining the recoveries of three USA federally listed endangered species: Florida Everglade snail kites, California and Alaska sea otters, and Snake River Chinook salmon. Overall, our results show the pivotal role of spatial structure in metapopulation recoveries whereby the interplay between local and regional processes shapes the resilience of the whole system. With this understanding, we provide guidelines for resource managers tasked with conserving and managing metapopulations and identify opportunities for research to support the application of metapopulation theory to real-world challenges.

Marine and freshwater regime changes impact a community of migratory Pacific salmonids in decline.

Marine and freshwater ecosystems are increasingly at risk of large and cascading changes from multiple human activities (termed "regime shifts"), which can impact population productivity, resilience, and ecosystem structure. Pacific salmon exhibit persistent and large fluctuations in their population dynamics driven by combinations of intrinsic (e.g., density dependence) and extrinsic factors (e.g., ecosystem changes, species interactions). In recent years, many Pacific salmon have declined due to regime shifts but clear understanding of the processes driving these changes remains elusive. Here, we unpacked the role of density dependence, ecosystem trends, and stochasticity on productivity regimes for a community of five anadromous Pacific salmonids (Steelhead, Coho Salmon, Pink Salmon, Dolly Varden, and Coastal Cutthroat Trout) across a rich 40-year time-series. We used a Bayesian multivariate state-space model to examine whether productivity shifts had similarly occurred across the community and explored marine or freshwater changes associated with those shifts. Overall, we identified three productivity regimes: an early regime (1976-1990), a compensatory regime (1991-2009), and a declining regime (since 2010) where large declines were observed for Steelhead, Dolly Varden, and Cutthroat Trout, intermediate declines in Coho and no change in Pink Salmon. These regime changes were associated with multiple cumulative effects across the salmon life cycle. For example, increased seal densities and ocean competition were associated with lower adult marine survival in Steelhead. Watershed logging also intensified over the past 40 years and was associated with (all else equal) ≥97% declines in freshwater productivity for Steelhead, Cutthroat, and Coho. For Steelhead, marine and freshwater dynamics played approximately equal roles in explaining trends in total productivity. Collectively, these changing environments limited juvenile production and lowered future adult returns. These results reveal how changes in freshwater and marine environments can jointly shape population dynamics among ecological communities, like Pacific salmon, with cascading consequences to their resilience.

Indigenous Systems of Management for Culturally and Ecologically Resilient Pacific Salmon (Oncorhynchus spp.) Fisheries.

Pacific salmon (Oncorhynchus spp.) are at the center of social-ecological systems that have supported Indigenous peoples around the North Pacific Rim since time immemorial. Through generations of interdependence with salmon, Indigenous Peoples developed sophisticated systems of management involving cultural and spiritual beliefs, and stewardship practices. Colonization radically altered these social-ecological systems, disrupting Indigenous management, consolidating authority within colonial governments, and moving most harvest into mixed-stock fisheries. We review Indigenous management of salmon, including selective fishing technologies, harvest practices, and governance grounded in multigenerational place-based knowledge. These systems and practices showcase pathways for sustained productivity and resilience in contemporary salmon fisheries. Contrasting Indigenous systems with contemporary management, we document vulnerabilities of colonial governance and harvest management that have contributed to declining salmon fisheries in many locations. We suggest that revitalizing traditional systems of salmon management can improve prospects for sustainable fisheries and healthy fishing communities and identify opportunities for their resurgence.

Changing estuaries and impacts on juvenile salmon: A systematic review.

Estuaries are productive ecosystems providing important habitat for a diversity of species, yet they also experience intense levels of anthropogenic development. To inform decision-making, it is essential to understand the pathways of impacts of particular human activities, especially those that affect species such as salmon, which have high ecological, social-cultural and economic values. Salmon systems provide an opportunity to build from the substantial body of research on responses to estuary developments and take stock of what is known. We conducted a systematic English-language literature review on the responses of juvenile salmon to anthropogenic activities in estuaries and nearshore areas asking: what has been studied, where are the major knowledge gaps and how do stressors affect salmon? We found a substantial body of research (n = 167 studies; 1,369 comparative tests) to help understand responses of juvenile salmon to 24 activities and their 14 stressors. Across studies, 82% of the research was conducted in the eastern Pacific (Oregon and Washington, USA and British Columbia, Canada) showing a limited geographical scope. Using a semiquantitative approach to summarize the literature, including a weight-of-evidence metric, we found a range of results from low to moderate-high confidence in the consequences of the stressors. For example, we found moderate-high confidence in the negative impacts of pollutants and sea lice and moderate confidence in negative impacts from connectivity loss and changes in flow. Our results suggest that overall, multiple anthropogenic activities cause negative impacts across ecological scales. However, our results also reveal knowledge gaps resulting from minimal research on particular species (e.g. sockeye salmon), regions (e.g. Atlantic) or stressors (e.g. entrainment) that would be expedient areas for future research. With estuaries acting as a nexus of biological and societal importance and hotspots of ongoing development, the insights gained here can contribute to informed decision-making.

Glacier Retreat and Pacific Salmon.

Glaciers have shaped past and present habitats for Pacific salmon (Oncorhynchus spp.) in North America. During the last glacial maximum, approximately 45% of the current North American range of Pacific salmon was covered in ice. Currently, most salmon habitat occurs in watersheds in which glacier ice is present and retreating. This synthesis examines the multiple ways that glacier retreat can influence aquatic ecosystems through the lens of Pacific salmon life cycles. We predict that the coming decades will result in areas in which salmon populations will be challenged by diminished water flows and elevated water temperatures, areas in which salmon productivity will be enhanced as downstream habitat suitability increases, and areas in which new river and lake habitat will be formed that can be colonized by anadromous salmon. Effective conservation and management of salmon habitat and populations should consider the impacts of glacier retreat and other sources of ecosystem change.

Impacts of industrial atmospheric emissions on watershed export of dissolved ions in coastal streams: a Bayesian modeling approach.

Anthropogenic atmospheric emission and subsequent deposition of sulfur (S) has been linked to disrupted watershed biogeochemical processes through soil and surface water acidification. We investigated watershed-scale impacts of acidic deposition on tributary concentrations and watershed exports of major nutrients and ions for the Kitimat River Watershed, British Columbia. Since the 1950s, the Kitimat watershed had an aluminum smelting facility with substantial emissions at the river estuary. Emissions load the airshed overlying the watershed and potentially impact western tributaries leaving eastern tributaries available as reference. We assessed concentrations and export of key compounds in three reference and six potentially impacted tributaries and watersheds in 2015 and 2016. Sulfate (SO4), fluoride (F), nitrate (NO3), and chloride (Cl) were significantly higher in impacted tributaries. F concentrations exceeded the Canadian Council of Ministers of the Environment guideline for aquatic life in 83% of samples collected from impacted streams. Watershed export and associated uncertainty were determined by bootstrapped flow-stratified Beale's unbiased estimator. Impact of emissions on watershed export was modeled in a Bayesian approach to include variance in the export estimate to inform the uncertainty of model parameters. Export of SO4 and Ca increased significantly within 16 km and 8 km, respectively, toward the smelter emissions. The corresponding impacted area for SO4 and Ca was approximately 100 km2 and 45 km2, respectively. SO4 export is likely due to direct impacts of S deposition, with excess S being flushed from the watersheds. Ca export patterns likely result from indirect impacts of S deposition on soil chemistry and flushing of Ca. These impacts may contribute to effects within tributaries on benthic stream communities and regionally important juvenile Pacific salmon.

Risky business for a juvenile marine predator? Testing the influence of foraging strategies on size and growth rate under natural conditions.

Mechanisms driving selection of body size and growth rate in wild marine vertebrates are poorly understood, thus limiting knowledge of their fitness costs at ecological, physiological and genetic scales. Here, we indirectly tested whether selection for size-related traits of juvenile sharks that inhabit a nursery hosting two dichotomous habitats, protected mangroves (low predation risk) and exposed seagrass beds (high predation risk), is influenced by their foraging behaviour. Juvenile sharks displayed a continuum of foraging strategies between mangrove and seagrass areas, with some individuals preferentially feeding in one habitat over another. Foraging habitat was correlated with growth rate, whereby slower growing, smaller individuals fed predominantly in sheltered mangroves, whereas larger, faster growing animals fed over exposed seagrass. Concomitantly, tracked juveniles undertook variable movement behaviours across both the low and high predation risk habitat. These data provide supporting evidence for the hypothesis that directional selection favouring smaller size and slower growth rate, both heritable traits in this shark population, may be driven by variability in foraging behaviour and predation risk. Such evolutionary pathways may be critical to adaptation within predator-driven marine ecosystems.

Response diversity, nonnative species, and disassembly rules buffer freshwater ecosystem processes from anthropogenic change.

Integrating knowledge of environmental degradation, biodiversity change, and ecosystem processes across large spatial scales remains a key challenge to illuminating the resilience of earth's systems. There is now a growing realization that the manner in which communities will respond to anthropogenic impacts will ultimately control the ecosystem consequences. Here, we examine the response of freshwater fishes and their nutrient excretion - a key ecosystem process that can control aquatic productivity - to human land development across the contiguous United States. By linking a continental-scale dataset of 533 fish species from 8100 stream locations with species functional traits, nutrient excretion, and land remote sensing, we present four key findings. First, we provide the first geographic footprint of nutrient excretion by freshwater fishes across the United States and reveal distinct local- and continental-scale heterogeneity in community excretion rates. Second, fish species exhibited substantial response diversity in their sensitivity to land development; for native species, the more tolerant species were also the species contributing greater ecosystem function in terms of nutrient excretion. Third, by modeling increased land-use change and resultant shifts in fish community composition, land development is estimated to decrease fish nutrient excretion in the majority (63%) of ecoregions. Fourth, the loss of nutrient excretion would be 28% greater if biodiversity loss was random or 84% greater if there were no nonnative species. Thus, ecosystem processes are sensitive to increased anthropogenic degradation but biotic communities provide multiple pathways for resistance and this resistance varies across space.

Shifting Thresholds: Rapid Evolution of Migratory Life Histories in Steelhead/Rainbow Trout, Oncorhynchus mykiss.

Expression of phenotypic plasticity depends on reaction norms adapted to historic selective regimes; anthropogenic changes in these selection regimes necessitate contemporary evolution or declines in productivity and possibly extinction. Adaptation of conditional strategies following a change in the selection regime requires evolution of either the environmentally influenced cue (e.g., size-at-age) or the state (e.g., size threshold) at which an individual switches between alternative tactics. Using a population of steelhead (Oncorhynchus mykiss) introduced above a barrier waterfall in 1910, we evaluate how the conditional strategy to migrate evolves in response to selection against migration. We created 9 families and 917 offspring from 14 parents collected from the above- and below-barrier populations. After 1 year of common garden-rearing above-barrier offspring were 11% smaller and 32% lighter than below-barrier offspring. Using a novel analytical approach, we estimate that the mean size at which above-barrier fish switch between the resident and migrant tactic is 43% larger than below-barrier fish. As a result, above-barrier fish were 26% less likely to express the migratory tactic. Our results demonstrate how rapid and opposing changes in size-at-age and threshold size contribute to the contemporary evolution of a conditional strategy and indicate that migratory barriers may elicit rapid evolution toward the resident life history on timescales relevant for conservation and management of conditionally migratory species.

Emergent stability in a large, free-flowing watershed.

While it is widely recognized that financial stock portfolios can be stabilized through diverse investments, it is also possible that certain habitats can function as natural portfolios that stabilize ecosystem processes. Here we propose and examine the hypothesis that free-flowing river networks act as such portfolios and confer stability through their integration of upstream geological, hydrological, and biological diversity. We compiled a spatially (142 sites) and temporally (1980-present) extensive data set on fisheries, water flows, and temperatures, from sites within one of the largest watersheds in the world that remains without dams on its mainstem, the Fraser River, British Columbia, Canada. We found that larger catchments had more stable fisheries catches, water flows, and water temperatures than smaller catchments. These data provide evidence that free-flowing river networks function as hierarchically nested portfolios with stability as an emergent property. Thus, free-flowing river networks can represent a natural system for buffering variation and extreme events.

Portfolio conservation of metapopulations under climate change.

Climate change is likely to lead to increasing population variability and extinction risk. Theoretically, greater population diversity should buffer against rising climate variability, and this theory is often invoked as a reason for greater conservation. However, this has rarely been quantified. Here we show how a portfolio approach to managing population diversity can inform metapopulation conservation priorities in a changing world. We develop a salmon metapopulation model in which productivity is driven by spatially distributed thermal tolerance and patterns of short- and long-term climate change. We then implement spatial conservation scenarios that control population carrying capacities and evaluate the metapopulation portfolios as a financial manager might: along axes of conservation risk and return. We show that preserving a diversity of thermal tolerances minimizes risk, given environmental stochasticity, and ensures persistence, given long-term environmental change. When the thermal tolerances of populations are unknown, doubling the number of populations conserved may nearly halve expected metapopulation variability. However, this reduction in variability can come at the expense of long-term persistence if climate change increasingly restricts available habitat, forcing ecological managers to balance society's desire for short-term stability and long-term viability. Our findings suggest the importance of conserving the processes that promote thermal-tolerance diversity, such as genetic diversity, habitat heterogeneity, and natural disturbance regimes, and demonstrate that diverse natural portfolios may be critical for metapopulation conservation in the face of increasing climate variability and change.

Life-history diversity and its importance to population stability and persistence of a migratory fish: steelhead in two large North American watersheds.

Life-history strategies can buffer individuals and populations from environmental variability. For instance, it is possible that asynchronous dynamics among different life histories can stabilize populations through portfolio effects. Here, we examine life-history diversity and its importance to stability for an iconic migratory fish species. In particular, we examined steelhead (Oncorhynchus mykiss), an anadromous and iteroparous salmonid, in two large, relatively pristine, watersheds, the Skeena and Nass, in north-western British Columbia, Canada. We synthesized life-history information derived from scales collected from adult steelhead (N = 7227) in these watersheds across a decade. These migratory fishes expressed 36 different manifestations of the anadromous life-history strategy, with 16 different combinations of freshwater and marine ages, 7·6% of fish performing multiple spawning migrations, and up to a maximum of four spawning migrations per lifetime. Furthermore, in the Nass watershed, various life histories were differently prevalent through time - three different life histories were the most prevalent in a given year, and no life history ever represented more than 45% of the population. These asynchronous dynamics among life histories decreased the variability of numerical abundance and biomass of the aggregated population so that it was > 20% more stable than the stability of the weighted average of specific life histories: evidence of a substantial portfolio effect. Year of ocean entry was a key driver of dynamics; the median correlation coefficient of abundance of life histories that entered the ocean the same year was 2·5 times higher than the median pairwise coefficient of life histories that entered the ocean at different times. Simulations illustrated how different elements of life-history diversity contribute to stability and persistence of populations. This study provides evidence that life-history diversity can dampen fluctuations in population abundances and biomass via portfolio effects. Conserving genetic integrity and habitat diversity in these and other large watersheds can enable a diversity of life histories that increases population and biomass stability in the face of environmental variability.

An interdisciplinary synthesis of floodplain ecosystem dynamics in a rapidly deglaciating watershed.

Glacier retreat is rapidly transforming some watersheds, with ramifications for water supply, ecological succession, important species such as Pacific salmon (Oncorhynchus spp.), and cultural uses of landscapes. To advance a more holistic understanding of the evolution of proglacial landscapes, we integrate multiple lines of knowledge starting in the early 1900s with contemporary data from the Taaltsux̱éi (Tulsequah) Watershed in British Columbia, Canada. Our objectives were to: 1) synthesize recent historical geography and Indigenous Knowledge, including glacier dynamics, and hydrology; 2) describe the limnology of a proglacial lake; 3) quantify decadal-scale downstream physical floodplain change; and 4) characterize riverine physical, chemical, and biological differences relative to distance from the proglacial lake. Since 1982, the Tulsequah Glacier has receded 0.07 km/yr, exposing a cold, deep, and growing proglacial lake. The downstream floodplain is rapidly changing; satellite imagery analysis revealed a 14 % increase in vegetation from 2003 to 2017 and Indigenous Knowledge described increases in vegetation and wildlife habitat over the last century. Contemporary measurements of physical-chemical water properties differed across sites representing the upper and lower watershed, and mainstem and off-channel habitats. Catches of juvenile salmonids in the upper watershed (closer to the glacier) were mostly limited to warmer, clearer groundwater-fed channels, whereas in the lower watershed there were salmonids in both groundwater-fed and mainstem habitats. There was limited zooplankton taxa diversity from the proglacial lake and benthic macroinvertebrates in the river. Collectively, our synthesis suggests that the transformation of proglacial landscapes experiencing rapid ice loss can be influenced by interlinked abiotic processes of glacier retreat, lake formation, and altered hydrology, as well as corresponding biological processes such as beaver repopulation, wetland formation, and riparian vegetation growth. These factors, along with expected increases to proglacial lake productivity and salmon habitat suitability, are an important consideration for forward-looking watershed management of glacier-fed rivers.

Physiological condition infers habitat choice in juvenile sockeye salmon.

The amount of time that juvenile salmon remain in an estuary varies among and within populations, with some individuals passing through their estuary in hours while others remain in the estuary for several months. Underlying differences in individual physiological condition, such as body size, stored energy and osmoregulatory function, could drive individual variation in the selection of estuary habitat. Here we investigated the role of variation in physiological condition on the selection of estuarine and ocean habitat by sockeye salmon (Oncorhynchus nerka) smolts intercepted at the initiation of their 650-km downstream migration from Chilko Lake, Fraser River, British Columbia (BC). Behavioural salinity preference experiments were conducted on unfed smolts held in fresh water at three time intervals during their downstream migration period, representing the stage of migration at lake-exit, and the expected timing for estuary-entry and ocean-entry (0, 1 and 3 weeks after lake-exit, respectively). In general, salinity preference behaviour varied across the three time periods consistent with expected transition from river to estuary to ocean. Further, individual physiological condition did influence habitat choice. Smolt condition factor (K) and energy density were positively correlated with salinity preference behaviour in the estuary and ocean outmigration stages, but not at lake-exit. Our results suggest that smolt physiological condition upon reaching the estuary could influence migratory behaviour and habitat selection. This provides evidence on the temporally dependent interplay of physiology, behaviour and migration in wild juvenile Pacific salmon, with juvenile rearing conditions influencing smolt energetic status, which in turn influences habitat choice during downstream migration. The implication for the conservation of migratory species is that the relative importance of stopover habitats may vary as a function of initial condition.

Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout.

Stable isotopes can illuminate resource usage by organisms, but effective interpretation is predicated on laboratory validation. Here we develop stable isotope clocks to track resource shifts in anadromous rainbow trout (Oncorhynchus mykiss). We used a diet-switch experiment and model fitting to quantify N stable isotope (δ(15)N) turnover rates and discrimination factors for seven tissues: plasma, liver, fin, mucus, red blood cells, muscle, and scales. Among tissues, diet-tissue δ(15)N discrimination factors ranged from 1.3 to 3.4 ‰. Model-supported tissue turnover half-lives ranged from 9.0 (fin) to 27.7 (scale) days. We evaluated six tissue turnover models using Akaike's information criterion corrected for small sample sizes. The use of equilibrium tissue values was supported in all tissues and two-compartment models were supported in plasma, liver, and mucus. Using parameter estimates and their uncertainty we developed stable isotope clocks to estimate the time since resource shifts. Longer turnover tissues provided accurate estimates of time since resource switch for durations approximately twice their half-life. Faster turnover tissues provided even higher precision estimates, but only within their half-life post-switch. Averaging estimates of time since resource shift from multiple tissues provided the highest precision estimates of time since resource shift for the longest duration (up to 64 days). This study therefore provides insight into physiological processes that underpin stable isotope patterns, explicitly tests alternative models, and quantifies key parameters that are the foundation of field-based stable isotope analysis.

Mining stakes claim on salmon futures as glaciers retreat.

Future ecological value of emerging habitats must be considered as climate change transforms the planet.

Phenological shifts and mismatch with marine productivity vary among Pacific salmon species and populations.

Global climate change is shifting the timing of life-cycle events, sometimes resulting in phenological mismatches between predators and prey. Phenological shifts and subsequent mismatches may be consistent across populations, or they could vary unpredictably across populations within the same species. For anadromous Pacific salmon (Oncorhynchus spp.), juveniles from thousands of locally adapted populations migrate from diverse freshwater habitats to the Pacific Ocean every year. Both the timing of freshwater migration and ocean arrival, relative to nearshore prey (phenological match/mismatch), can control marine survival and population dynamics. Here we examined phenological change of 66 populations across six anadromous Pacific salmon species throughout their range in western North America with the longest time series spanning 1951-2019. We show that different salmon species have different rates of phenological change but that there was substantial within-species variation that was not correlated with changing environmental conditions or geographic patterns. Moreover, outmigration phenologies have not tracked shifts in the timing of marine primary productivity, potentially increasing the frequency of future phenological mismatches. Understanding population responses to mismatches with prey are an important part of characterizing overall population-specific climate vulnerability.