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.

Contribution of warm habitat to cold-water fisheries.

A central tenet of landscape ecology is that mobile species depend on complementary habitats, which are insufficient in isolation, but combine to support animals through the full annual cycle. However, incorporating the dynamic needs of mobile species into conservation strategies remains a challenge, particularly in the context of climate adaptation planning. For cold-water fishes, it is widely assumed that maximum temperatures are limiting and that summer data alone can predict refugia and population persistence. We tested these assumptions in populations of redband rainbow trout (Oncorhynchus mykiss newberrii) in an arid basin, where the dominance of hot, hyperproductive water in summer emulates threats of climate change predicted for cold-water fish in other basins. We used telemetry to reveal seasonal patterns of movement and habitat use. Then, we compared contributions of hot and cool water to growth with empirical indicators of diet and condition (gut contents, weight-length ratios, electric phase angle, and stable isotope signatures) and a bioenergetics model. During summer, trout occurred only in cool tributaries or springs (<20 °C) and avoided Upper Klamath Lake (>25 °C). During spring and fall, ≥65% of trout migrated to the lake (5-50 km) to forage. Spring and fall growth (mean [SD] 0.58% per day [0.80%] and 0.34 per day [0.55%], respectively) compensated for a net loss of energy in cool summer refuges (-0.56% per day [0.55%]). In winter, ≥90% of trout returned to tributaries (25-150 km) to spawn. Thus, although perennially cool tributaries supported thermal refuge and spawning, foraging opportunities in the seasonally hot lake ultimately fueled these behaviors. Current approaches to climate adaptation would prioritize the tributaries for conservation but would devalue critical foraging habitat because the lake is unsuitable and unoccupied during summer. Our results empirically demonstrate that warm water can fuel cold-water fisheries and challenge the common practice of identifying refugia based only on summer conditions.

RESUMEN: Un principio central de la ecología de paisaje es que las especies ambulantes dependen de hábitats complementarios, los cuales son insuficientes en aislamiento, pero al combinarse mantienen a los animales durante el ciclo anual completo. Sin embargo, la incorporación de las necesidades dinámicas de las especies ambulantes dentro de las estrategias de conservación todavía es un reto, particularmente en el contexto de la planeación de la adaptación climática. Para los peces de agua fría, generalmente se asume que las temperaturas máximas son limitantes y que los datos estivales son suficientes para predecir refugios y la persistencia poblacional. Pusimos a prueba estas suposiciones en poblaciones de trucha arcoíris (Oncorhynchus mykiss newberrii) de una cuenca árida, en donde el dominio de aguas cálidas e hiperproductivas durante el verano emula las amenazas del cambio climático pronosticadas para los peces de agua fría en otras cuencas. Usamos telemetría para descubrir los patrones estacionales de movimiento y uso de hábitat. Después, comparamos las contribuciones que tienen las aguas cálidas y frías al crecimiento con indicadores empíricos de dieta y condición (contenidos intestinales, proporciones peso-longitud, ángulo de fase eléctrica y huellas de isotopos estables) y un modelo bioenergético. Durante el verano, las truchas sólo estuvieron presentes en manantiales o afluentes fríos (<20°C) y evitaron el Lago Klamath Superior (>25°C). Durante la primavera y el otoño, ≥65% de las truchas migraron al lago (5-50 km) para procurar alimento. El crecimiento durante la primavera y el otoño (media [SD] 0.58% día-1 [0.80%] y 0.34 día-1 [0.55%], respectivamente) compensaron la pérdida neta de energía en los refugios fríos durante el verano (-0.56% día-1 [0.55%]). En el invierno, ≥90% de las truchas regresaron a los afluentes (25-150 km) para desovar. Entonces, mientras que los afluentes perennemente fríos fomentaron los refugios termales y el desove, fueron las oportunidades de alimentación en el lago cálido estacional las que finalmente alentaron estos comportamientos. Las estrategias actuales de adaptación climática pondrían como prioridad de conservación a los afluentes, pero devaluarían el hábitat crítico de alimentación porque el lago está desocupado y no es apto durante el verano. Nuestros resultados demuestran empíricamente que las aguas cálidas pueden promover las pesquerías de aguas frías y desafiar la práctica común de identificar refugios basándose solamente en las condiciones estivales.

Anthropogenic habitat alteration leads to rapid loss of adaptive variation and restoration potential in wild salmon populations.

Phenotypic variation is critical for the long-term persistence of species and populations. Anthropogenic activities have caused substantial shifts and reductions in phenotypic variation across diverse taxa, but the underlying mechanism(s) (i.e., phenotypic plasticity and/or genetic evolution) and long-term consequences (e.g., ability to recover phenotypic variation) are unclear. Here we investigate the widespread and dramatic changes in adult migration characteristics of wild Chinook salmon caused by dam construction and other anthropogenic activities. Strikingly, we find an extremely robust association between migration phenotype (i.e., spring-run or fall-run) and a single locus, and that the rapid phenotypic shift observed after a recent dam construction is explained by dramatic allele frequency change at this locus. Furthermore, modeling demonstrates that continued selection against the spring-run phenotype could rapidly lead to complete loss of the spring-run allele, and an empirical analysis of populations that have already lost the spring-run phenotype reveals they are not acting as sustainable reservoirs of the allele. Finally, ancient DNA analysis suggests the spring-run allele was abundant in historical habitat that will soon become accessible through a large-scale restoration (i.e., dam removal) project, but our findings suggest that widespread declines and extirpation of the spring-run phenotype and allele will challenge reestablishment of the spring-run phenotype in this and future restoration projects. These results reveal the mechanisms and consequences of human-induced phenotypic change and highlight the need to conserve and restore critical adaptive variation before the potential for recovery is lost.

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.

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.

Stream network geomorphology mediates predicted vulnerability of anadromous fish habitat to hydrologic change in southeast Alaska.

In rivers supporting Pacific salmon in southeast Alaska, USA, regional trends toward a warmer, wetter climate are predicted to increase mid- and late-21st-century mean annual flood size by 17% and 28%, respectively. Increased flood size could alter stream habitats used by Pacific salmon for reproduction, with negative consequences for the substantial economic, cultural, and ecosystem services these fish provide. We combined field measurements and model simulations to estimate the potential influence of future flood disturbance on geomorphic processes controlling the quality and extent of coho, chum, and pink salmon spawning habitat in over 800 southeast Alaska watersheds. Spawning habitat responses varied widely across watersheds and among salmon species. Little variation among watersheds in potential spawning habitat change was explained by predicted increases in mean annual flood size. Watershed response diversity was mediated primarily by topographic controls on stream channel confinement, reach-scale geomorphic associations with spawning habitat preferences, and complexity in the pace and mode of geomorphic channel responses to altered flood size. Potential spawning habitat loss was highest for coho salmon, which spawn over a wide range of geomorphic settings, including steeper, confined stream reaches that are more susceptible to streambed scour during high flows. We estimated that 9-10% and 13-16% of the spawning habitat for coho salmon could be lost by the 2040s and 2080s, respectively, with losses occurring primarily in confined, higher-gradient streams that provide only moderate-quality habitat. Estimated effects were lower for pink and chum salmon, which primarily spawn in unconfined floodplain streams. Our results illustrate the importance of accounting for valley and reach-scale geomorphic features in watershed assessments of climate vulnerability, especially in topographically complex regions. Failure to consider the geomorphic context of stream networks will hamper efforts to understand and mitigate the vulnerability of anadromous fish habitat to climate-induced hydrologic change.

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.

Hierarchical genetic structure and implications for conservation of the world's largest salmonid, Hucho taimen.

Population genetic analyses can evaluate how evolutionary processes shape diversity and inform conservation and management of imperiled species. Taimen (Hucho taimen), the world's largest freshwater salmonid, is threatened, endangered, or extirpated across much of its range due to anthropogenic activity including overfishing and habitat degradation. We generated genetic data using high throughput sequencing of reduced representation libraries for taimen from multiple drainages in Mongolia and Russia. Nucleotide diversity estimates were within the range documented in other salmonids, suggesting moderate diversity despite widespread population declines. Similar to other recent studies, our analyses revealed pronounced differentiation among the Arctic (Selenge) and Pacific (Amur and Tugur) drainages, suggesting historical isolation among these systems. However, we found evidence for finer-scale structure within the Pacific drainages, including unexpected differentiation between tributaries and the mainstem of the Tugur River. Differentiation across the Amur and Tugur basins together with coalescent-based demographic modeling suggests the ancestors of Tugur tributary taimen likely diverged in the eastern Amur basin, prior to eventual colonization of the Tugur basin. Our results suggest the potential for differentiation of taimen at different geographic scales, and suggest more thorough geographic and genomic sampling may be needed to inform conservation and management of this iconic salmonid.

Glacier retreat creating new Pacific salmon habitat in western North America.

Glacier retreat poses risks and benefits for species of cultural and economic importance. One example is Pacific salmon (Oncorhynchus spp.), supporting subsistence harvests, and commercial and recreational fisheries worth billions of dollars annually. Although decreases in summer streamflow and warming freshwater is reducing salmon habitat quality in parts of their range, glacier retreat is creating new streams and lakes that salmon can colonize. However, potential gains in future salmon habitat associated with glacier loss have yet to be quantified across the range of Pacific salmon. Here we project future gains in Pacific salmon freshwater habitat by linking a model of glacier mass change for 315 glaciers, forced by five different Global Climate Models, with a simple model of salmon stream habitat potential throughout the Pacific Mountain ranges of western North America. We project that by the year 2100 glacier retreat will create 6,146 (±1,619) km of new streams accessible for colonization by Pacific salmon, of which 1,930 (±569) km have the potential to be used for spawning and juvenile rearing, representing 0 to 27% gains within the 18 sub-regions we studied. These findings can inform proactive management and conservation of Pacific salmon in this era of rapid climate change.