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.

Temperature, emergence phenology and consumption drive seasonal shifts in fish growth and production across riverscapes.

Changes in biophysical conditions through time generate spatial and temporal variability in habitat quality across landscapes. For river ecosystems, researchers are increasingly able to characterize spatial and temporal patterns in habitat conditions, referred to as shifting habitat mosaics, yet rarely demonstrate how this translates into corresponding biological processes such as organism growth and production. We assessed spatial patterns and processes determining seasonal changes in juvenile Chinook Salmon Oncorhynchus tshawytscha size, growth and production over 30-40 km in two NE Oregon subbasins. We quantified seasonal patterns of growth by combining estimated emergence dates and body size distributions in July and September. We then used analysis of bioenergetics, empirical fish diets and spatial models incorporating temperature, habitat and population density to evaluate mechanisms driving spatiotemporal patterns of growth. Lastly, we quantified seasonal contributions to individual fish growth and to total production as a function of position within the stream network. Spatial heterogeneity in incubation temperatures corresponded to later estimated emergence timing with distance upstream in both subbasins. During spring, estimated growth rates decreased with distance upstream, and coupled with emergence patterns, resulted in pronounced longitudinal gradients in body size by July. During summer, spatial patterns of growth reversed, with greater diet ration sizes and growth efficiencies upstream than downstream. These opposing spatiotemporal patterns of emergence timing and seasonal growth rates produced longitudinal gradients in the proportion of fish growth achieved in spring versus summer, with up to 80% of an individual's growth occurring in spring at downstream sites but as low as 10% at upstream sites. Coupling longitudinal patterns of fish density and growth revealed that in one subbasin the majority (65%) of total production occurred in spring, while in the other, in which fish were concentrated in headwaters, the majority (60%) of production occurred in summer. While recent work has emphasized inter-annual shifts in fish production across large spatial scales, this study demonstrates that longitudinal gradients of fish growth and production can reverse across seasons, and reveals important contributions of warmer, downstream habitats to overall production that occurred during cooler times of the year.

The importance of warm habitat to the growth regime of cold-water fishes.

A common goal of biological adaptation planning is to identify and prioritize locations that remain suitably cool during summer. This implicitly devalues areas that are ephemerally warm, even if they are suitable most of the year for mobile animals. Here we develop an alternative conceptual framework, the growth regime, which considers seasonal and landscape variation in physiological performance, focusing on riverine fish. Using temperature models for 14 river basins, we show that growth opportunities propagate up and down river networks on a seasonal basis, and that downstream habitats that are suboptimally warm in summer may actually provide the majority of growth potential expressed annually. We demonstrate with an agent-based simulation that shoulder-season use of warmer downstream habitats can fuel annual fish production. Our work reveals a synergy between cold and warm habitats that could be fundamental for supporting coldwater fisheries, highlighting the risk in conservation strategies that underappreciate warm habitats.

Emerging Perspectives on Resource Tracking and Animal Movement Ecology.

Resource tracking, where animals increase energy gain by moving to track phenological variation in resources across space, is emerging as a fundamental attribute of animal movement ecology. However, a theoretical framework to understand when and where resource tracking should occur, and how resource tracking should lead to emergent ecological patterns, is lacking. We present a framework that unites concepts from optimal foraging theory and landscape ecology, which can be used to generate and test predictions on how resource dynamics shape animal movement across taxa, systems, and scales. Consideration of the interplay between animal movement and resource dynamics not only advances ecological understanding but can also guide biodiversity conservation in an era of global change.

Aerial surveys cause large but ephemeral decreases in bear presence at salmon streams in Kodiak, Alaska.

Aerial surveys are often used to monitor wildlife and fish populations, but rarely are the effects on animal behavior documented. For over 30 years, the Kodiak National Wildlife Refuge has conducted low-altitude aerial surveys to assess Kodiak brown bear (Ursus arctos middendorffi) space use and demographic composition when bears are seasonally congregated near salmon spawning streams in southwestern Kodiak Island, Alaska. Salmon (Oncorhynchus spp.) are an important bear food and salmon runs are brief, so decreases in time spent fishing for salmon may reduce salmon consumption by bears. The goal of this study was to apply different and complementary field methods to evaluate the response of bears to these aerial surveys. Ground-based counts at one stream indicated 62% of bears departed the 200m-wide survey zone in response to aerial surveys, but bear counts returned to pre-survey abundance after only three hours. Although this effect was brief, survey flights occurred during the hours of peak daily bear activity (morning and evening), so the three-hour disruption appeared to result in a 25% decline in cumulative daily detections by 38 time-lapse cameras deployed along 10 salmon streams. Bear responses varied by sex-male bears were much more likely than female bears (with or without cubs) to depart streams and female bears with GPS collars did not move from streams following surveys. Although bears displaced by aerial surveys may consume fewer salmon, the actual effect on their fitness depends on whether they compensate by foraging at other times or by switching to other nutritious resources. Data from complementary sources allows managers to more robustly understand the impacts of surveys and whether their benefits are justified. Similar assessments should be made on alternative techniques such as Unmanned Aerial Vehicles and non-invasive sampling to determine whether they supply equivalent data while limiting bear disturbance.

Migratory coupling between predators and prey.

Animal migrations act to couple ecosystems and are undertaken by some of the world's most endangered taxa. Predators often exploit migrant prey, but the movements taken by these consumers are rarely studied or understood. We define such movements, where migrant prey induce large-scale movements of predators, as migratory coupling. Migratory coupling can have ecological consequences for the participating prey, predators and the communities they traverse across the landscape. We review examples of migratory coupling in the literature and provide hypotheses regarding conditions favourable for their occurrence. We also provide a framework for interactions induced by migratory coupling and demonstrate their potential community-level impacts by examining other forms of spatial shifts in predators. Migratory coupling integrates the fields of landscape, movement, food web and community ecologies, and represents an understudied frontier in ecology.

Phenological tracking associated with increased salmon consumption by brown bears.

There is growing interest in the ecological significance of phenological diversity, particularly in how spatially variable resource phenologies (i.e. resource waves) prolong foraging opportunities for mobile consumers. While there is accumulating evidence of consumers moving across landscapes to surf resource waves, there is little data quantifying how phenological tracking influences resource consumption due to the challenge of documenting all the components of this ecological phenomenon (i.e., phenological variation, consumer movement, resource consumption, and consumer fitness). We examined the space use of GPS collared female brown bears to quantify the exploitation of a salmon resource wave by individual bears. We then estimated salmon consumption levels in the same individuals using stable isotope and mercury analyses of hair. We found strong positive relationships between time spent on salmon streams and percent salmon in assimilated diets (R2 = 0.70) and salmon mass consumed (R2 = 0.49). Salmon abundance varied 2.5-fold between study years, yet accounting for salmon abundance did not improve salmon consumption models. Resource abundance generally is viewed as the key variable controlling consumption levels and food web dynamics. However, our results suggest that in intact watersheds of coastal Alaska with abundant salmon runs, interannual variation in salmon abundance likely has less effect on salmon consumption than individual variation in bear foraging behavior. The results complement previous work to demonstrate the importance of phenological variation on bear foraging behavior and fitness.

Phenological synchronization disrupts trophic interactions between Kodiak brown bears and salmon.

Climate change is altering the seasonal timing of life cycle events in organisms across the planet, but the magnitude of change often varies among taxa [Thackeray SJ, et al. (2016) Nature 535:241-245]. This can cause the temporal relationships among species to change, altering the strength of interaction. A large body of work has explored what happens when coevolved species shift out of sync, but virtually no studies have documented the effects of climate-induced synchronization, which could remove temporal barriers between species and create novel interactions. We explored how a predator, the Kodiak brown bear (Ursus arctos middendorffi), responded to asymmetric phenological shifts between its primary trophic resources, sockeye salmon (Oncorhynchus nerka) and red elderberry (Sambucus racemosa). In years with anomalously high spring air temperatures, elderberry fruited several weeks earlier and became available during the period when salmon spawned in tributary streams. Bears departed salmon spawning streams, where they typically kill 25-75% of the salmon [Quinn TP, Cunningham CJ, Wirsing AJ (2016) Oecologia 183:415-429], to forage on berries on adjacent hillsides. This prey switching behavior attenuated an iconic predator-prey interaction and likely altered the many ecological functions that result from bears foraging on salmon [Helfield JM, Naiman RJ (2006) Ecosystems 9:167-180]. We document how climate-induced shifts in resource phenology can alter food webs through a mechanism other than trophic mismatch. The current emphasis on singular consumer-resource interactions fails to capture how climate-altered phenologies reschedule resource availability and alter how energy flows through ecosystems.

Adaptive capacity at the northern front: sockeye salmon behaviourally thermoregulate during novel exposure to warm temperatures.

As climate change increases maximal water temperatures, behavioural thermoregulation may be crucial for the persistence of coldwater fishes, such as salmonids. Although myriad studies have documented behavioural thermoregulation in southern populations of salmonids, few if any have explored this phenomenon in northern populations, which are less likely to have an evolutionary history of heat stress, yet are predicted to experience substantial warming. Here, we treated a rare heat wave as a natural experiment to test whether wild sockeye salmon (Oncorhynchus nerka) at the northern extent of their primary range (60° latitude) can thermoregulate in response to abnormally high thermal conditions. We tagged adult sockeye salmon with temperature loggers as they staged in a lake epilimnion prior to spawning in small cold streams (n = 40 recovered loggers). As lake surface temperatures warmed to physiologically suboptimal levels (15-20°C), sockeye salmon thermoregulated by moving to tributary plumes or the lake metalimnion. A regression of fish body temperature against lake surface temperature indicated that fish moved to cooler waters when the epilimnion temperature exceeded ~12°C. A bioenergetics model suggested that the observed behaviour reduced daily metabolic costs by as much as ~50% during the warmest conditions (18-20°C). These results provide rare evidence of cool-seeking thermoregulation at the poleward extent of a species range, emphasizing the potential ubiquity of maximal temperature constraints and the functional significance of thermal heterogeneity for buffering poikilotherms from climate change.

Kodiak brown bears surf the salmon red wave: direct evidence from GPS collared individuals.

A key constraint faced by consumers is achieving a positive energy balance in the face of temporal variation in foraging opportunities. Recent work has shown that spatial heterogeneity in resource phenology can buffer mobile consumers from this constraint by allowing them to track changes in resource availability across space. For example, salmon populations spawn asynchronously across watersheds, causing high-quality foraging opportunities to propagate across the landscape, prolonging the availability of salmon at the regional scale. However, we know little about how individual consumers integrate across phenological variation or the benefits they receive by doing so. Here, we present direct evidence that individual brown bears track spatial variation in salmon phenology. Data from 40 GPS collared brown bears show that bears visited multiple spawning sites in synchrony with the order of spawning phenology. The number of sites used was correlated with the number of days a bear exploited salmon, suggesting the phenological variation in the study area influenced bear access to salmon, a resource which strongly influences bear fitness. Fisheries managers attempting to maximize harvest while maintaining ecosystem function should strive to protect the population diversity that underlies the phenological variation used by wildlife consumers.

Resource waves: phenological diversity enhances foraging opportunities for mobile consumers.

Time can be a limiting constraint for consumers, particularly when resource phenology mediates foraging opportunity. Though a large body of research has explored how resource phenology influences trophic interactions, this work has focused on the topics of trophic mismatch or predator swamping, which typically occur over short periods, at small spatial extents or coarse resolutions. In contrast many consumers integrate across landscape heterogeneity in resource phenology, moving to track ephemeral food sources that propagate across space as resource waves. Here we provide a conceptual framework to advance the study of phenological diversity and resource waves. We define resource waves, review evidence of their importance in recent case studies, and demonstrate their broader ecological significance with a simulation model. We found that consumers ranging from fig wasps (Chalcidoidea) to grizzly bears (Ursus arctos) exploit resource waves, integrating across phenological diversity to make resource aggregates available for much longer than their component parts. In model simulations, phenological diversity was often more important to consumer energy gain than resource abundance per se. Current ecosystem-based management assumes that species abundance mediates the strength of trophic interactions. Our results challenge this assumption and highlight new opportunities for conservation and management. Resource waves are an emergent property of consumer-resource interactions and are broadly significant in ecology and conservation.

Inter-Tributary Movements by Resident Salmonids across a Boreal Riverscape.

Stream-dwelling fishes inhabit river networks where resources are distributed heterogeneously across space and time. Current theory emphasizes that fishes often perform large-scale movements among habitat patches for reproduction and seeking refugia, but assumes that fish are relatively sedentary during growth phases of their life cycle. Using stationary passive integrated transponder (PIT)-tag antennas and snorkel surveys, we assessed the individual and population level movement patterns of two species of fish across a network of tributaries within the Wood River basin in southwestern Alaska where summer foraging opportunities vary substantially among streams, seasons, and years. Across two years, Arctic grayling (Thymallus arcticus) and rainbow trout (Oncorhynchus mykiss) exhibited kilometer-scale movements among streams during the summer growing season. Although we monitored movements at a small fraction of all tributaries used by grayling and rainbow trout, approximately 50% of individuals moved among two or more streams separated by at least 7 km within a single summer. Movements were concentrated in June and July, and subsided by early August. The decline in movements coincided with spawning by anadromous sockeye salmon, which offer a high-quality resource pulse of food to resident species. Inter-stream movements may represent prospecting behavior as individuals seek out the most profitable foraging opportunities that are patchily distributed across space and time. Our results highlight that large-scale movements may not only be necessary for individuals to fulfill their life-cycle, but also to exploit heterogeneously spaced trophic resources. Therefore, habitat fragmentation and homogenization may have strong, but currently undescribed, ecological effects on the access to critical food resources in stream-dwelling fish populations.

Predator avoidance during reproduction: diel movements by spawning sockeye salmon between stream and lake habitats.

Daily movements of mobile organisms between habitats in response to changing trade-offs between predation risk and foraging gains are well established; however, less in known about whether similar tactics are used during reproduction, a time period when many organisms are particularly vulnerable to predators. We investigated the reproductive behaviour of adult sockeye salmon (Oncorhynchus nerka) and the activity of their principal predator, brown bears (Ursus arctos), on streams in south-western Alaska. Specifically, we continuously monitored movements of salmon between lake habitat, where salmon are invulnerable to bears, and three small streams, where salmon spawn and are highly vulnerable to bears. We conducted our study across 2 years that offered a distinct contrast in bear activity and predation rates. Diel movements by adult sockeye salmon between stream and lake habitat were observed in 51.3% ± 17.7% (mean ± SD) of individuals among years and sites. Fish that moved tended to hold in the lake for most of the day and then migrated into spawning streams during the night, coincident with when bear activity on streams tended to be lowest. Additionally, cyclic movements between lakes and spawning streams were concentrated earlier in the spawning season. Individuals that exhibited diel movements had longer average reproductive life spans than those who made only one directed movement into a stream. However, the relative effect was dependent on the timing of bear predation, which varied between years. When predation pressure primarily occurred early in the spawning run (i.e., during the height of the diel movements), movers lived 120-310% longer than non-movers. If predation pressure was concentrated later in the spawning run (i.e. when most movements had ceased), movers only lived 10-60% longer. Our results suggest a dynamic trade-off in reproductive strategies of sockeye salmon; adults must be in the stream to reproduce, but must also avoid predation long enough to spawn. Given the interannual variation in the timing and intensity of predation pressure, the advantages of a particular movement strategy will likely vary among years. Regardless, movements by salmon allowed individuals to exploit fine-scale habitat heterogeneity during reproduction, which appears to be a strategy to reduce predation risk on the spawning grounds.

Performance of salmon fishery portfolios across western North America.

Quantifying the variability in the delivery of ecosystem services across the landscape can be used to set appropriate management targets, evaluate resilience and target conservation efforts. Ecosystem functions and services may exhibit portfolio-type dynamics, whereby diversity within lower levels promotes stability at more aggregated levels. Portfolio theory provides a framework to characterize the relative performance among ecosystems and the processes that drive differences in performance. We assessed Pacific salmon Oncorhynchus spp. portfolio performance across their native latitudinal range focusing on the reliability of salmon returns as a metric with which to assess the function of salmon ecosystems and their services to humans. We used the Sharpe ratio (e.g. the size of the total salmon return to the portfolio relative to its variability (risk)) to evaluate the performance of Chinook and sockeye salmon portfolios across the west coast of North America. We evaluated the effects on portfolio performance from the variance of and covariance among salmon returns within each portfolio, and the association between portfolio performance and watershed attributes. We found a positive latitudinal trend in the risk-adjusted performance of Chinook and sockeye salmon portfolios that also correlated negatively with anthropogenic impact on watersheds (e.g. dams and land-use change). High-latitude Chinook salmon portfolios were on average 2·5 times more reliable, and their portfolio risk was mainly due to low variance in the individual assets. Sockeye salmon portfolios were also more reliable at higher latitudes, but sources of risk varied among the highest performing portfolios. Synthesis and applications. Portfolio theory provides a straightforward method for characterizing the resilience of salmon ecosystems and their services. Natural variability in portfolio performance among undeveloped watersheds provides a benchmark for restoration efforts. Locally and regionally, assessing the sources of portfolio risk can guide actions to maintain existing resilience (protect habitat and disturbance regimes that maintain response diversity; employ harvest strategies sensitive to different portfolio components) or improve restoration activities. Improving our understanding of portfolio reliability may allow for management of natural resources that is robust to ongoing environmental change. Portfolio theory provides a straightforward method for characterizing the resilience of salmon ecosystems and their services. Natural variability in portfolio performance among undeveloped watersheds provides a benchmark for restoration efforts. Locally and regionally, assessing the sources of portfolio risk can guide actions to maintain existing resilience (protect habitat and disturbance regimes that maintain response diversity; employ harvest strategies sensitive to different portfolio components) or improve restoration activities. Improving our understanding of portfolio reliability may allow for management of natural resources that is robust to ongoing environmental change.

Diel horizontal migration in streams: juvenile fish exploit spatial heterogeneity in thermal and trophic resources.

Vertical heterogeneity in the physical characteristics of lakes and oceans is ecologically salient and exploited by a wide range of taxa through diel vertical migration to enhance their growth and survival. Whether analogous behaviors exploit horizontal habitat heterogeneity in streams is largely unknown. We investigated fish movement behavior at daily timescales to explore how individuals integrated across spatial variation in food abundance and water temperature. Juvenile coho salmon made feeding forays into cold habitats with abundant food, and then moved long distances (350-1300 m) to warmer habitats that accelerated their metabolism and increased their assimilative capacity. This behavioral thermoregulation enabled fish to mitigate trade-offs between trophic and thermal resources by exploiting thermal heterogeneity. Fish that exploited thermal heterogeneity grew at substantially faster rates than did individuals that assumed other behaviors. Our results provide empirical support for the importance of thermal diversity in lotic systems, and emphasize the importance of considering interactions between animal behavior and habitat heterogeneity when managing and restoring ecosystems.

Riding the crimson tide: mobile terrestrial consumers track phenological variation in spawning of an anadromous fish.

When resources are spatially and temporally variable, consumers can increase their foraging success by moving to track ephemeral feeding opportunities as these shift across the landscape; the best examples derive from herbivore-plant systems, where grazers migrate to capitalize on the seasonal waves of vegetation growth. We evaluated whether analogous processes occur in watersheds supporting spawning sockeye salmon (Oncorhynchus nerka), asking whether seasonal activities of predators and scavengers shift spatial distributions to capitalize on asynchronous spawning among populations of salmon. Both glaucous-winged gulls and coastal brown bears showed distinct shifts in their spatial distributions over the course of the summer, reflecting the shifting distribution of spawning sockeye salmon, which was associated with variation in water temperature among spawning sites. By tracking the spatial and temporal variation in the phenology of their principal prey, consumers substantially extended their foraging opportunity on a superabundant, yet locally ephemeral, resource. Ecosystem-based fishery management efforts that seek to balance trade-offs between fisheries and ecosystem processes supported by salmon should, therefore, assess the importance of life-history variation, particularly in phenological traits, for maintaining important ecosystem functions, such as providing marine-derived resources for terrestrial predators and scavengers.

Phenotype flexibility in wild fish: Dolly Varden regulate assimilative capacity to capitalize on annual pulsed subsidies.

1. Large digestive organs increase rates of energy gain when food is plentiful but are costly to maintain and increase rates of energy loss when food is scarce. The physiological adaptations to this trade-off differ depending on the scale and predictability of variation in food abundance. 2. Currently, there is little understanding of how animals balance trade-offs between the cost and capacity of the digestive system in response to resource pulses: rare, ephemeral periods of resource superabundance. We investigated the physiological and behavioural tactics of the fish Dolly Varden (Salvelinus malma) that rear in watersheds with low in situ productivity, but experience annual resource pulses from the spawning migrations of Pacific salmon. The eggs of Pacific salmon provide high-energy food for Dolly Varden. 3. Dolly Varden sampled 6 weeks prior to the resource pulse exhibited atrophy of the stomach, pyloric caeca, intestine and liver. Throughout the portion of the growing season prior to the resource pulse, fish exhibited empty stomachs, low indices of energy condition and muscle isotope signatures reflecting the previous resource pulse. 4. During the resource pulse, Dolly Varden exhibited large digestive machinery, gorged on salmon eggs and rapidly stored energy in fat reserves, somatic growth and gonad development. Dolly Varden appeared to achieve nearly their entire annual energy surplus during the ∼ 5-week period when sockeye salmon spawn. 5. Digestive flexibility provides Dolly Varden the energy efficiency required to survive and reproduce when resource abundance is concentrated into an annual pulse that is predictable, yet highly ephemeral. Although fish are known to incur extremely variable energy budgets, our study is one of the first to document digestive flexibility in wild fish. Our study emphasizes that fish can rely heavily on rare, high-magnitude foraging opportunities. Human actions that attenuate spikes in food abundance may have stronger than anticipated effects on consumer energy budgets.

Temperature-associated population diversity in salmon confers benefits to mobile consumers.

Habitat heterogeneity can generate intraspecific diversity through local adaptation of populations. While it is becoming increasingly clear that population diversity can increase stability in species abundance, less is known about how population diversity can benefit consumers that can integrate across population diversity in their prey. Here we demonstrate cascading effects of thermal heterogeneity on trout-salmon interactions in streams where rainbow trout rely heavily on the seasonal availability of anadromous salmon eggs. Water temperature in an Alaskan stream varied spatially from 5 degrees C to 17.5 degrees C, and spawning sockeye salmon showed population differentiation associated with this thermal heterogeneity. Individuals that spawned early in cool regions of the 5 km long stream were genetically differentiated from those spawning in warmer regions later in the season. Sockeye salmon spawning generates a pulsed resource subsidy that supports the majority of seasonal growth in stream-dwelling rainbow trout. The spatial and temporal structuring of sockeye salmon spawn timing in our focal stream extended the duration of the pulsed subsidy compared to a thermally homogeneous stream with a single population of salmon. Further, rainbow trout adopted movement strategies that exploited the multiple pulses of egg subsidies in the thermally heterogeneous stream. Fish that moved to track the resource pulse grew at rates about 2.5 times higher than those that remained stationary or trout in the reference stream with a single seasonal pulse of eggs. Our results demonstrate that habitat heterogeneity can have important effects on the population diversity of dominant species, and in turn, influence their value to species that prey upon them. Therefore, habitat homogenization may have farther-reaching ecological effects than previously considered.