Jonathan B. Armstrong

Excess digestive capacity in predators reflects a life of feast and famine

A central challenge for predators is achieving positive energy balance when prey are spatially and temporally heterogeneous. Ecological heterogeneity produces evolutionary trade-offs in the physiological design of predators; this is because the ability to capitalize on pulses of food abundance requires high capacity for food-processing, yet maintaining such capacity imposes energetic costs that are taxing during periods of food scarcity. Recent advances in physiology show that when variation in foraging opportunities is predictable, animals may adjust energetic trade-offs by rapidly modulating their digestive system to track variation in foraging opportunities. However, it is increasingly recognized that foraging opportunities for animals are unpredictable, which should favour animals that maintain a capacity for food-processing that exceeds average levels of consumption (loads). Despite this basic principle of quantitative evolutionary design, estimates of digestive load:capacity ratios in wild animals are virtually non-existent. Here we provide an extensive assessment of load:capacity ratios for the digestive systems of predators in the wild, compiling 639 estimates across 38 species of fish. We found that piscine predators typically maintain the physiological capacity to feed at daily rates 2–3 times higher than what they experience on average. A numerical simulation of the trade-off between food-processing capacity and metabolic cost suggests that the observed level of physiological opportunism is profitable only if predator–prey encounters, and thus predator energy budgets, are far more variable in nature than currently assumed.

The portfolio concept in ecology and evolution

Biological systems have similarities to efficient financial portfolios; the emergent properties of aggregate systems are often less volatile than their components. These portfolio effects derive from statistical averaging across the dynamics of system components, which often correlate weakly or negatively with each other through time and space. The “portfolio” concept when applied to ecological research provides important insights into how ecosystems are organized, how species interact, and how evolutionary strategies develop. It also helps identify appropriate scales for developing robust management and conservation schemes, and offers an approach that does not rely on prescriptive predictions about threats in an uncertain future. Rather, it presents a framework for managing risk from inevitable perturbations, many of which we will not be able to understand or anticipate.

Scientific Evidence Supports a Ban on Microbeads

Chelsea M. Rochman,*,†,‡ Sara M. Kross,†,§ Jonathan B. Armstrong,†,∥,@ Michael T. Bogan,†,⊥,@ Emily S. Darling,†,#,@ Stephanie J. Green,†,¶,@ Ashley R. Smyth,†,▲,@ and Diogo Verissimo†,▼,@ †David H. Smith Conservation Research Program, Society for Conservation Biology, Washington, DC 20001, United States ‡School of Veterinary Medicine, Aquatic Health Program, University of California Davis, Davis, California 95616, United States Department of Wildlife, Fish and Conservation Biology, University of California Davis, Davis, California 95616-8627, United States USGS Cooperative Fish and Wildlife Research Unit, University of Wyoming, Laramie, Wyoming 82071, United States Department of Environmental Science, Management and Policy, University of California Berkeley, Berkeley, California 94720-3114, United States Marine Program, Wildlife Conservation Society, New York 10460-1099, United States Department of Integrative Biology, Oregon State University, Corvallis, Oregon 97331, United States Virginia Institute of Marine Science, College of William and Mary, Gloucester Point, Virginia 23062, United States Andrew Young School of Policy Studies, Department of Economics, Georgia State University, 33 Gilmer Street SE, Atlanta, Georgia 30303, United States

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.

Thermal heterogeneity mediates the effects of pulsed subsidies across a landscape

Spatial and temporal heterogeneity interact to make the foraging rates of individuals more variable than expected from models assuming that spatial and temporal dimensions of habitat conditions operate independently. For example, trophic resource pulses produce temporal patches of prey superabundance, yet little is known about how spatial heterogeneity in habitat conditions mediates the ability of consumers to exploit these high-quality foraging opportunities. We studied how spatial variation in water temperature regulates the potential for juvenile coho salmon to exploit a seasonal pulsed subsidy of eggs produced by anadromous sockeye salmon. Streams within the Wood River watershed, southwestern Alaska, USA, ranged in mean summer temperature from 3.6 degrees to 14.5 degrees C. Growth of juvenile coho prior to the arrival of the seasonal egg subsidy was positively related to water temperature among streams. An in situ experiment combined with field samples of diets revealed a size threshold for egg consumption; only individuals longer than approximately 70 mm could consume eggs due to gape limitation of smaller individuals. A bioenergetics simulation demonstrated that water temperature regulated whether age-0 coho salmon could grow large enough to exceed the size threshold for egg consumption. Coho salmon that consumed eggs had energy rations that were five times higher than fish that did not consume eggs, resulting in a positive feedback of water temperature on their integrated seasonal growth. Across this landscape, heterogeneity in water temperature mediates individual- and population-level responses to seasonally available resource pulses. Our study illustrates that ecological mechanisms, such as size-based foraging asymmetries, can magnify the effects of climate change compared to predictions based on physiology alone.

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.

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.

Performance of salmon fishery portfolios across western North America

Summary 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.

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.