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The Ecology Section examines how environmental variability, human activities and infrastructure influence food web interactions and species performance in freshwater and marine ecosystems. We have extensive experience in quantifying aquatic food web processes as they relate to growth, survival and production of key species of interest, especially resident and anadromous salmonids.
Our tactical food web modeling approach uses an analytical framework that accounts for the effects of changing environmental conditions, ecological processes, and human perturbations on: 1) the seasonal availability and access to food, 2) competition for shared food resources, 3) seasonal growth potential given the food supply and thermal regime, 4) predation risk or mortality associated with specific rearing and migratory habitats, and 5) the influence of size and growth performance on survival through subsequent life stages (e.g., survival to adulthood).
Expertise in the section includes prediction, assessment and evaluation of physical and biological responses to dam removal, dam operations, changing land-water use, species introductions or invasions; development and application of environmental DNA (eDNA) assays for detection, geographical distribution and potential quantification of species; age-growth and stage-specific habitat use of fishes via otolith micro-structure or micro-chemistry, scale analysis, and development of analogous non-lethal techniques using alternative body structures; stable isotope, diet analysis, image analysis (for growth measurement and invertebrate enumeration), bomb calorimetry and bioenergetics modeling for quantifying trophic interactions; and effective integration of sampling design, field sampling capability, and data analysis.
We can integrate an efficient, directed field sampling program to supply empirical inputs for bioenergetics and population modeling to quantify seasonal population-level consumption demand for major food resources, and relate demand to the temporal supply of food in a manner that accounts for variability in diet, growth, consumption, and metabolic demands associated with changing seasonal and size-specific habitat use, thermal regime, and other environmental and ecological processes. We have routinely used this approach to estimate the carrying capacity of lakes and reservoirs for both resident and anadromous salmonids, and for quantifying existing or potential predation mortality by resident predators on juvenile salmon or steelhead, kokanee, trout and other resident fishes. This tactical food web modeling approach has been successfully applied to numerous large lakes and reservoirs throughout western North America and in the southern hemisphere. The applications generally address the question of what factors limit production of a species or group of species of concern. The projects include estimating the seasonal carrying capacity for specific consumers, feasibility of species re-introductions (anadromous salmonids, Bull trout, Lahontan Cutthroat trout), impacts on non-native species on existing communities (trout in South America and New Zealand; smallmouth bass, walleye, American Shad, etc. in western waters), factors limiting growth during critical growth or survival periods for juvenile salmon in Puget Sound and Gulf of Alaska, and effects of environmental stressors on food web interactions.
We routinely design and execute directed field sampling, sample processing, analysis, modeling and synthesis. We have appropriately-scaled boats, nets, and other sampling gear for quantitative measurement of influential limnological features (turbidity, vertical profiles of temperature, DO, zooplankton prey, light intensity), and for sampling pelagic and benthic fishes (hydroacoustics, midwater trawls, gill nets, traps, etc.).
Dave Beauchamp’s research emphasizes bioenergetics and tactical food web ecology of salmonids. He has been the invited lead author for chapters in primary reference books solicited by the American Fisheries Society on “Standard Methods for Sampling North American Freshwater Fishes” (Chapter on “Large Coldwater Lakes”) and “Analysis and Interpretation of Freshwater Fisheries Data” (Chapter on “Predator-Prey Interactions”), and “Bioenergetic Ontogeny: Linking climate and mass-specific feeding to life-cycle growth and survival of salmon.”
Jeff Duda has been a leader in investigations related to feasibility and ecosystem effects of dam removals, having played a pivotal role in the Elwha dam removal program and co-lead on development and application the DRIP (Dam Removal Information Portal) database that assimilates data on former, current and pending dam removals in North America and beyond.
Carl Ostberg runs the genetics portion of our section with a focus on salmonid hybridization, and heavy involvement in development and application of eDNA assays and eDNA approaches for describing species ranges, recolonization, and invasion. His group is also developing innovative techniques for advancing beyond simple presence-absence to quantifying abundance of organisms, based on ontogenetic and environmental dynamics that influence production and shedding of the DNA products used in eDNA detections.
Kim Larsen’s age and growth group focuses on using the hard-part tissues of fish (scales, otoliths, fin rays, opercles, etc.) to estimate age and reconstruct growth histories of individuals based on microstructure patterns in ring formation. By combining stable isotope or elemental analysis with microstructure patterns, we can develop a sequence of habitat use through key periods in the life cycle of individuals (e.g., timing and size at saltwater entry for juvenile salmon, identifying natal streams of migrant species, shifts in trophic position across age/size).
Steve Rubin has focused on the role of sediment dynamics on eelgrass and kelp bed development, retention, and temporal-spatial estuarine habitat associations with juvenile salmon, forage fishes, and invertebrates.
Invasive species pose a severe threat to infrastructure and the integrity of aquatic ecosystems that support fish and invertebrates that provide recreational and commercial fisheries or pose conservation or health concerns. In order to confront threats from invasive species, effective strategies for prevention and early detection need to be melded with a mechanistic understanding for the roles of invasives in the food webs of host waterways. Invasive species can serve as new prey, predators, competitors, parasites, or pathogens to existing species. Some invasives can threaten infrastructure and alter the physical habitat of host communities (e.g., zebra and quagga mussels, or macrophytes like Eurasian milfoil,). As such, invasives could be relatively innocuous or impose profound impacts via direct or indirect pathways through the food web. Recognizing which invasives pose significant threats and understanding the conditions under which their impacts are exacerbated or can be minimized will be essential for effectively guiding attention and resources where they are most needed and not expending them on the more innocuous invaders.
The roles of these invasives change in response to different environmental conditions and the species composition and structure of host communities. Thus, developing a mechanistic framework for evaluating the context-specific threat and feasibility of potential remedies will facilitate our ability to identify and prioritize species of interest (both invasives and potentially impacted species) and waters of concern based on the potential magnitude of an invasive response and the vulnerability of the host systems. An additional benefit of this approach is that the same concepts apply to colonization or re-introductions of desirable species.
Detection: (eDNA, conventional sampling, spatially-explicit mapping of extent and magnitude of invasions)
Threat assessments (bioenergetically-based food web analysis, including mediating effects of changing environmental conditions): temporal food supply-demand for desirable species and competitors, predation mortality, effects of seasonal and altered environmental conditions on species interactions, growth and survival of species of concern. Focus on identifying important spatial-temporal patterns of emerging threats and understanding the underlying mechanisms that might be manipulated to ameliorate the threat.
Remedies: identify and exploit weak links in the life cycle of invasives or mediate conditions that alter the vulnerabilities of desirable species to invasive impacts.
Invasive species of concern in the Pacific Northwest:
| American shad | Northern pike |
| Brook trout | Other minnows |
|
Eurasian milfoil (and other aquatic macrophytes: Egeria, Hydrilla) |
Redside shiners |
| European Green Crab | Rusty Crayfish |
| Lake trout | Smallmouth bass |
| Mysid shrimp | Walleye |
| New Zealand mudsnails | Zebra and quagga mussels |
The marine survival of ESA-listed Chinook salmon and steelhead, as well as Coho salmon declined precipitously in the 1980s and have remained low in both US and Canadian stocks within the Salish Sea. Factors affecting survival and production of these species limits treaty tribal harvest and recreational fishing opportunities, diminishes the preferred food supply and health of ESA-listed resident Killer Whale populations, and fundamentally affects management of land, water, and energy usage in the region. This research is being conducted as part of the Salish Sea Marine Survival Project (a joint US-Canada program involving over federal, state, local and provincial agencies, universities, tribes and NGOs) in collaboration with scientists from NOAA and Washington Department of Fish and Wildlife with partial funding from Long Live the Kings.
Our work on the Salish Sea Marine Survival Project (SSMSP) continues to evolve. We've identified a critical growth period for juvenile Chinook salmon during the first month of feeding in epi-pelagic habitats within Puget Sound. After the juveniles transition to these "offshore" waters, they increase their body mass by a factor of 2-4x within that first month, and that resulting body mass in mid-late July is strongly correlated to overall marine survival (Smolt-to-adult returns, SARs). We've also determined that much of the variability in growth during that critical period can be attributed to the contribution of larval crab (mostly megalops) to the energy budget of Chinook during this period.
In Puget Sound, juvenile ESA-listed Chinook salmon and Steelhead are limited by predation mortality primarily from Harbor Seals and older Resident forms of Chinook salmon. Marine mortality is strongly size-selective for Chinook salmon, so the Ecology Section is investigating the dynamic role of seasonal food supply, energy allocation, and thermal conditions during critical early marine growth periods, and how these bottom-up processes influence the efficacy of their predators. Since most predators except Killer Whales rely on primarily on vision to locate and capture salmon, we are examining how changes in underwater light and turbidity affect predation, especially the effects of increasing artificial light at night (ALAN).
So we’re currently examining a number of related questions such as:
Most aquatic vertebrates rely primarily on vision as their primary sensory mechanism for movement, feeding and avoiding predation. Visual conditions underwater vary dramatically among water bodies, but also across day-twilight-night periods, seasons and among years within the same waters. Humans have significantly altered the visual environment, but the serious implications of these changes for survival and growth of aquatic species and the function of aquatic food webs has been largely ignored. Research to date on the visual capabilities of key aquatic species like salmon and trout have been opportunistic due to a lack of coherent programmatic funding. Despite the challenges of sporadic funding and lack of consistent access to adequate experimental facilities, we have developed visual foraging models and applied these to juvenile salmon and their predators in natural environments. These exercises reveal important patterns that relate directly to how human impacts on underwater light and transparency significantly affect the survival and production of ESA-listed and economically important species.
From experimental parameterization of the visual capabilities for several predatory salmonids on juvenile salmon and other forage fishes, some important patterns emerge related to the responses of both predators and prey to environmentally-relevant changes in underwater light intensity and turbidity. Both predators and prey can feed efficiently at low light levels common during daylight and twilight down to depths of 20-30 m in clear water. Over the past few decades in and around urbanized regions, increasing artificial light pollution has created periods of perpetual twilight, supplanting dark nocturnal periods that are critical for safe migration through shallow habitats and for refuge from predation in rearing habitats.
Land and water development has also altered the natural dynamics of water transparency/turbidity via changes in sediment transport from dams or erosion and algal blooms from altered nutrient fluxes. The predators’ ability to detect and consume prey diminishes rapidly over relatively small increases in turbidity, whereas the smaller invertebrate-feeding fish like juvenile salmon are minimally affected.
The interaction of changing light and turbidity over varying spatial and temporal scales survival and growth of economically-important and trust species. Therefore, a mechanistic understanding for how variability in the visual environment affects fitness of key species and their interactions with others in the food web offers considerable potential for improving their survival and production and restoring long term function of ecosystems in an economically and ecologically effective manner.
This program would contain several essential elements:
We’re also very much involved in food web interactions involving salmonids in lakes, reservoirs and streams. With a number of hydro-electric dams coming up for relicensing with FERC (Federal Energy Regulatory Commission), a rapidly emerging theme has been examining the ecological feasibility of re-introducing anadromous salmonids above previously impassable dams (e.g., do environmental conditions, seasonal food supply, competition, predation, and connectivity among critical habitats and life stages allow for sufficient production of salmon to warrant advancing through the process of considering costly re-introductions). We apply these same approaches to examine effects of non-native species on host food webs and salmonid production, all mediated by prevailing and projected environmental conditions.
Skagit River reservoirs - In preparation for FERC relicensing of mainstem dams on the Skagit River, we will conduct a quantitative analysis of species interactions, habitat and environmental conditions that affect production of native salmonids in reservoirs and major tributaries associated with Ross, Diablo, and Gorge dams on the Skagit River, Washington. The goal of this project will be to identify and quantify factors that limit recruitment and production of native adfluvial salmonids (Bull trout, Dolly Varden, Rainbow trout) and invasive species (e.g., Redside Shiners, Brook Trout, Brown Trout) that populate the reservoirs and associated tributaries above the mainstem dams on the Skagit River (Ross, Diablo, Gorge). We will initially focus on the food web structure of the reservoir-tributary complex, the presence and geographic extent of native and non-native fishes in the basin, and habitat suitability and production capacity of select tributaries. Food web interactions, distribution, and growth of native salmonids will ultimately be linked to environmental conditions, and these will be evaluated within the context of projected changes in climate or dam operations.
Determining the relative importance of tributary and lake-rearing strategies for juvenile Spring Chinook Salmon in the Lake Wenatchee Basin - We are conducting an initial bioenergetics-based analysis of factors affecting growth and survival of juvenile Spring Chinook Salmon and the relative importance of rearing in tributary versus lake habitats in the Wenatchee Basin. We will conduct stable isotope analysis and scale-pattern analysis on archival samples, supplemented with targeted streamlined field sampling in tributary and lake habitats by collaborators from Washington Department of Fish and Wildlife and U.S. Forest Service to address questions related to the primary rearing distribution of juvenile spring Chinook salmon, their primary food sources, feeding habitats, associated growth performance, and their trophic relationships within the Wenatchee basin food web (i.e., their primary prey, competitors, and predators). The resulting information will be used to construct the initial bioenergetics modeling simulations of the temporal consumption demand by juvenile Chinook for key prey, the seasonal carrying capacity of the lake for Chinook, Sockeye, and other major planktivores, and the relative predation impact by different size classes of predators (i.e., Northern Pikeminnow and Bull Trout). The results of these simulations will quantify what we currently know about distribution, feeding, growth, and predation mortality associated with freshwater rearing phases of juvenile Chinook salmon, identify and prioritize the major uncertainties that should be targeted in subsequent research.
Feasibility of re-introducing anadromous salmonids in Lewis River Reservoirs (completed) and Lake Cushman (proposed) - Reintroductions of anadromous salmonids above formerly impassable dams are being proposed with increasing frequency in the Pacific Northwest. The suitability of reservoir habitat for rearing anadromous salmonids and interactions with resident fish affect the feasibility of reintroductions. To determine whether one or more of the Lewis River Reservoirs can support reintroduced populations of juvenile Spring Chinook and other salmonids, we evaluated prey supply and consumption demand of resident fishes to estimate the carrying capacity for planktivores. The primary resident planktivores, Kokanee and hatchery–reared Rainbow Trout were both highly dependent on Daphnia for food with a secondary reliance on insects based on stable isotope and stomach content analysis. Daphnia first bloomed in spring and remained at moderate levels with a smaller secondary peak in fall before declining to low levels in November. Zooplankton densities were highest in the epilimnion, but warm epilimnetic temperatures during peak stratification limited access by salmonids to foraging within the thermocline where densities of Daphnia were 50% lower than in the epilimnion. In all three reservoirs, consumption demand exceeded 50% of the most conservative estimate of prey resources during the growing season. However, more liberal estimates of prey supply, which included the production and standing stock biomass of the edible size-fraction of Daphnia, suggested that an additional 130,000–300,000 subyearling salmon could be supported during the most food-limited month of the growing season.
We also evaluated the predation risk from the two primary predators, Northern Pikeminnow and Tiger Muskellunge, to anadromous salmonids considered for reintroduction in Merwin Reservoir for both year–round rearing juveniles and migrating smolts. Seasonal and size-specific feeding for each predatory species was estimated using stable isotopes and stomach content analysis. We quantified seasonal per–capita predation using bioenergetics modeling, evaluated the size and age structures of the populations, and combined these inputs to estimate predation rates of size–structured populations of predators. Northern Pikeminnow ≥ 300 mm were highly cannibalistic with modest seasonal per–capita predation on salmonids, but were disproportionately much less abundant than smaller, less piscivorous conspecifics. The annual predation on Kokanee Oncorhynchus nerka (in biomass) by a size–structured unit of 1,000 Northern Pikeminnow of FL ≥ 300 mm was analogous to 16,000–40,000 age–0 spring Chinook Salmon rearing year–round in the reservoir, or 400–1,000 age–1 smolts migrating through the reservoir during April–June. The per–capita consumption of salmonids by Northern Pikeminnow of FL ≥ 200 mm was relatively low, due to spatial segregation during the summer and the skewed size distribution toward smaller, less predatory individuals in the population. Tiger muskellunge fed heavily on Northern Pikeminnow, other non–salmonids, and minimally on salmonids. Predation by tiger muskellunge, in addition to cannibalism, likely contributed to low recruitment of larger (more piscivorous) Northern Pikeminnow, effectively reducing predation risk to salmonids. This study highlights the importance of quantitatively evaluating trophic interactions within reservoirs slated for reintroduction, as they serve both as functional migration corridors and offer profitable juvenile–rearing habitats despite hosting abundant predator populations.
Below are other science projects associated with this project.
USGS scientist setting up underwater video cameras in an eelgrass meadow on the Skagit River Delta. Eelgrass grows in shallow marine and estuarine waters where it forms structurally complex habitats that support many other aquatic species by providing attachment substrate, food, refuge from predation, and nursery areas.
USGS scientist setting up underwater video cameras in an eelgrass meadow on the Skagit River Delta. Eelgrass grows in shallow marine and estuarine waters where it forms structurally complex habitats that support many other aquatic species by providing attachment substrate, food, refuge from predation, and nursery areas.
USGS scientist setting up underwater video cameras in an eelgrass meadow on the Skagit River Delta. Eelgrass grows in shallow marine and estuarine waters where it forms structurally complex habitats that support many other aquatic species by providing attachment substrate, food, refuge from predation, and nursery areas.
USGS scientist setting up underwater video cameras in an eelgrass meadow on the Skagit River Delta. Eelgrass grows in shallow marine and estuarine waters where it forms structurally complex habitats that support many other aquatic species by providing attachment substrate, food, refuge from predation, and nursery areas.
The sun setting behind the Olympic Mountains from a beach on Hood Canal, Washington. A beautiful ending of another day.
The sun setting behind the Olympic Mountains from a beach on Hood Canal, Washington. A beautiful ending of another day.
Coho salmon migrating on the Sol Duc River, Washington to spawning grounds upstream. Fish must leap through a series of small waterfalls called the Salmon Cascades in Olympic National Park to reach the waters where they were born to complete their life cycle by spawning the next generation.
Coho salmon migrating on the Sol Duc River, Washington to spawning grounds upstream. Fish must leap through a series of small waterfalls called the Salmon Cascades in Olympic National Park to reach the waters where they were born to complete their life cycle by spawning the next generation.
Coho salmon migrating on the Sol Duc River, Washington to spawning grounds upstream. Fish must leap through a series of small waterfalls called the Salmon Cascades in Olympic National Park to reach the waters where they were born to complete their life cycle by spawning the next generation.
Coho salmon migrating on the Sol Duc River, Washington to spawning grounds upstream. Fish must leap through a series of small waterfalls called the Salmon Cascades in Olympic National Park to reach the waters where they were born to complete their life cycle by spawning the next generation.
Sampling drifting invertebrates from a stream in the North Cascades of Washington State. We perform drift sampling to determine the invertebrate prey quality and quantity available for drift feeding fish. Data gathered from this sampling are used in bioenergetics modeling, a method of estimating fish growth potential.
Sampling drifting invertebrates from a stream in the North Cascades of Washington State. We perform drift sampling to determine the invertebrate prey quality and quantity available for drift feeding fish. Data gathered from this sampling are used in bioenergetics modeling, a method of estimating fish growth potential.
Photo taken from Magnuson boat launch before conducting water quality and light at depth measurements during Landsat-8 overpass windows on Lake Washington for the U.S. Geological Survey.
To learn more about this project and other related research you can visit the WFRC Ecology Section website.
Photo taken from Magnuson boat launch before conducting water quality and light at depth measurements during Landsat-8 overpass windows on Lake Washington for the U.S. Geological Survey.
To learn more about this project and other related research you can visit the WFRC Ecology Section website.
Photo taken from Magnuson boat launch before conducting a synoptic light survey of Lake Washington for the U.S. Geological Survey.
Photo taken from Magnuson boat launch before conducting a synoptic light survey of Lake Washington for the U.S. Geological Survey.
Lighting from the Kirkland waterfront viewed from the Seattle shoreline.
Photo taken from Magnuson boat launch before conducting a synoptic light survey of Lake Washington for the U.S. Geological Survey.
Lighting from the Kirkland waterfront viewed from the Seattle shoreline.
Photo taken from Magnuson boat launch before conducting a synoptic light survey of Lake Washington for the U.S. Geological Survey.
Researchers perform gastric lavage on a rainbow trout to sample its stomach contents. This fish was sampled as a part of a food web study on Ross and Diablo Lakes in Washington State to evaluate fish growth and limitations to production.
Researchers perform gastric lavage on a rainbow trout to sample its stomach contents. This fish was sampled as a part of a food web study on Ross and Diablo Lakes in Washington State to evaluate fish growth and limitations to production.
USGS boat tied to dock at Ross Lake during a week-long sampling trip for a food web study. Ross Lake is a large reservoir on the Upper Skagit River in the North Cascade mountains of northern Washington state.
USGS boat tied to dock at Ross Lake during a week-long sampling trip for a food web study. Ross Lake is a large reservoir on the Upper Skagit River in the North Cascade mountains of northern Washington state.
Researchers stage sampling equipment at the Ross Lake boat ramp and wait for boat to arrive to transport them to camping area. Food web sampling on large lakes requires a substantial amount of sampling gear. Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state.
Researchers stage sampling equipment at the Ross Lake boat ramp and wait for boat to arrive to transport them to camping area. Food web sampling on large lakes requires a substantial amount of sampling gear. Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state.
Marshal Hoy, a Biological Science Technician, angling on Ross Lake for Western Fisheries Research Center (WFRC) food web study in October 2021. As a part of this study, fish are sampled for stomach contents, scale samples to assess age and growth, and fin tissue for stable isotopes and genetic analysis.
Marshal Hoy, a Biological Science Technician, angling on Ross Lake for Western Fisheries Research Center (WFRC) food web study in October 2021. As a part of this study, fish are sampled for stomach contents, scale samples to assess age and growth, and fin tissue for stable isotopes and genetic analysis.
Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state. This photo was taken while conducting food web research to support the Skagit River Hydroelectric Dam FERC relicensing process. To learn more about this project and other related research you can visit the WFRC Ecology Section website.
Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state. This photo was taken while conducting food web research to support the Skagit River Hydroelectric Dam FERC relicensing process. To learn more about this project and other related research you can visit the WFRC Ecology Section website.
A native crayfish collected in Diablo Lake for an investigation into food availability for native fish and limitations to their growth. Crayfish are invertebrate prey for salmonids and provide useful representative stable isotope values for benthic members of the food web.
A native crayfish collected in Diablo Lake for an investigation into food availability for native fish and limitations to their growth. Crayfish are invertebrate prey for salmonids and provide useful representative stable isotope values for benthic members of the food web.
Evening shot of Ross Lake with boat wake. Heading back to camp after a day of research. Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state. This photo was taken while conducting food web research to support the Skagit River Hydroelectric Dam FERC relicensing process.
Evening shot of Ross Lake with boat wake. Heading back to camp after a day of research. Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state. This photo was taken while conducting food web research to support the Skagit River Hydroelectric Dam FERC relicensing process.
The Elwha River flows through the footprint of the former reservoir Lake Mills. The wide-angle image also shows revegetated uplands dominated by alder trees meeting coniferous forest along the former shoreline of the reservoir.
The Elwha River flows through the footprint of the former reservoir Lake Mills. The wide-angle image also shows revegetated uplands dominated by alder trees meeting coniferous forest along the former shoreline of the reservoir.
Researchers on their way to sampling site on Diablo Lake. Diablo Lake is a reservoir in the North Cascade mountains of northern Washington. Created by Diablo Dam, the lake is located between Ross Lake and Gorge Lake on the Skagit River.
Researchers on their way to sampling site on Diablo Lake. Diablo Lake is a reservoir in the North Cascade mountains of northern Washington. Created by Diablo Dam, the lake is located between Ross Lake and Gorge Lake on the Skagit River.
Aerial photograph of the mouth of the Elwha River showing sediment deposits from dam removal. Aerial assistance by LightHawk and plane piloted by Dr. Milton Bennett.
Aerial photograph of the mouth of the Elwha River showing sediment deposits from dam removal. Aerial assistance by LightHawk and plane piloted by Dr. Milton Bennett.
Biologists snorkel the Bogachiel River in Washington State to count resident and migratory fish as part of a riverscape survey.
Biologists snorkel the Bogachiel River in Washington State to count resident and migratory fish as part of a riverscape survey.
Re-vegetation in the river valley at the Elwha River restoration site. Image available at Olympic National Park flickr site.
Re-vegetation in the river valley at the Elwha River restoration site. Image available at Olympic National Park flickr site.
The Ecology Section examines how environmental variability, human activities and infrastructure influence food web interactions and species performance in freshwater and marine ecosystems. We have extensive experience in quantifying aquatic food web processes as they relate to growth, survival and production of key species of interest, especially resident and anadromous salmonids.
Our tactical food web modeling approach uses an analytical framework that accounts for the effects of changing environmental conditions, ecological processes, and human perturbations on: 1) the seasonal availability and access to food, 2) competition for shared food resources, 3) seasonal growth potential given the food supply and thermal regime, 4) predation risk or mortality associated with specific rearing and migratory habitats, and 5) the influence of size and growth performance on survival through subsequent life stages (e.g., survival to adulthood).
Expertise in the section includes prediction, assessment and evaluation of physical and biological responses to dam removal, dam operations, changing land-water use, species introductions or invasions; development and application of environmental DNA (eDNA) assays for detection, geographical distribution and potential quantification of species; age-growth and stage-specific habitat use of fishes via otolith micro-structure or micro-chemistry, scale analysis, and development of analogous non-lethal techniques using alternative body structures; stable isotope, diet analysis, image analysis (for growth measurement and invertebrate enumeration), bomb calorimetry and bioenergetics modeling for quantifying trophic interactions; and effective integration of sampling design, field sampling capability, and data analysis.
We can integrate an efficient, directed field sampling program to supply empirical inputs for bioenergetics and population modeling to quantify seasonal population-level consumption demand for major food resources, and relate demand to the temporal supply of food in a manner that accounts for variability in diet, growth, consumption, and metabolic demands associated with changing seasonal and size-specific habitat use, thermal regime, and other environmental and ecological processes. We have routinely used this approach to estimate the carrying capacity of lakes and reservoirs for both resident and anadromous salmonids, and for quantifying existing or potential predation mortality by resident predators on juvenile salmon or steelhead, kokanee, trout and other resident fishes. This tactical food web modeling approach has been successfully applied to numerous large lakes and reservoirs throughout western North America and in the southern hemisphere. The applications generally address the question of what factors limit production of a species or group of species of concern. The projects include estimating the seasonal carrying capacity for specific consumers, feasibility of species re-introductions (anadromous salmonids, Bull trout, Lahontan Cutthroat trout), impacts on non-native species on existing communities (trout in South America and New Zealand; smallmouth bass, walleye, American Shad, etc. in western waters), factors limiting growth during critical growth or survival periods for juvenile salmon in Puget Sound and Gulf of Alaska, and effects of environmental stressors on food web interactions.
We routinely design and execute directed field sampling, sample processing, analysis, modeling and synthesis. We have appropriately-scaled boats, nets, and other sampling gear for quantitative measurement of influential limnological features (turbidity, vertical profiles of temperature, DO, zooplankton prey, light intensity), and for sampling pelagic and benthic fishes (hydroacoustics, midwater trawls, gill nets, traps, etc.).
Dave Beauchamp’s research emphasizes bioenergetics and tactical food web ecology of salmonids. He has been the invited lead author for chapters in primary reference books solicited by the American Fisheries Society on “Standard Methods for Sampling North American Freshwater Fishes” (Chapter on “Large Coldwater Lakes”) and “Analysis and Interpretation of Freshwater Fisheries Data” (Chapter on “Predator-Prey Interactions”), and “Bioenergetic Ontogeny: Linking climate and mass-specific feeding to life-cycle growth and survival of salmon.”
Jeff Duda has been a leader in investigations related to feasibility and ecosystem effects of dam removals, having played a pivotal role in the Elwha dam removal program and co-lead on development and application the DRIP (Dam Removal Information Portal) database that assimilates data on former, current and pending dam removals in North America and beyond.
Carl Ostberg runs the genetics portion of our section with a focus on salmonid hybridization, and heavy involvement in development and application of eDNA assays and eDNA approaches for describing species ranges, recolonization, and invasion. His group is also developing innovative techniques for advancing beyond simple presence-absence to quantifying abundance of organisms, based on ontogenetic and environmental dynamics that influence production and shedding of the DNA products used in eDNA detections.
Kim Larsen’s age and growth group focuses on using the hard-part tissues of fish (scales, otoliths, fin rays, opercles, etc.) to estimate age and reconstruct growth histories of individuals based on microstructure patterns in ring formation. By combining stable isotope or elemental analysis with microstructure patterns, we can develop a sequence of habitat use through key periods in the life cycle of individuals (e.g., timing and size at saltwater entry for juvenile salmon, identifying natal streams of migrant species, shifts in trophic position across age/size).
Steve Rubin has focused on the role of sediment dynamics on eelgrass and kelp bed development, retention, and temporal-spatial estuarine habitat associations with juvenile salmon, forage fishes, and invertebrates.
Invasive species pose a severe threat to infrastructure and the integrity of aquatic ecosystems that support fish and invertebrates that provide recreational and commercial fisheries or pose conservation or health concerns. In order to confront threats from invasive species, effective strategies for prevention and early detection need to be melded with a mechanistic understanding for the roles of invasives in the food webs of host waterways. Invasive species can serve as new prey, predators, competitors, parasites, or pathogens to existing species. Some invasives can threaten infrastructure and alter the physical habitat of host communities (e.g., zebra and quagga mussels, or macrophytes like Eurasian milfoil,). As such, invasives could be relatively innocuous or impose profound impacts via direct or indirect pathways through the food web. Recognizing which invasives pose significant threats and understanding the conditions under which their impacts are exacerbated or can be minimized will be essential for effectively guiding attention and resources where they are most needed and not expending them on the more innocuous invaders.
The roles of these invasives change in response to different environmental conditions and the species composition and structure of host communities. Thus, developing a mechanistic framework for evaluating the context-specific threat and feasibility of potential remedies will facilitate our ability to identify and prioritize species of interest (both invasives and potentially impacted species) and waters of concern based on the potential magnitude of an invasive response and the vulnerability of the host systems. An additional benefit of this approach is that the same concepts apply to colonization or re-introductions of desirable species.
Detection: (eDNA, conventional sampling, spatially-explicit mapping of extent and magnitude of invasions)
Threat assessments (bioenergetically-based food web analysis, including mediating effects of changing environmental conditions): temporal food supply-demand for desirable species and competitors, predation mortality, effects of seasonal and altered environmental conditions on species interactions, growth and survival of species of concern. Focus on identifying important spatial-temporal patterns of emerging threats and understanding the underlying mechanisms that might be manipulated to ameliorate the threat.
Remedies: identify and exploit weak links in the life cycle of invasives or mediate conditions that alter the vulnerabilities of desirable species to invasive impacts.
Invasive species of concern in the Pacific Northwest:
| American shad | Northern pike |
| Brook trout | Other minnows |
|
Eurasian milfoil (and other aquatic macrophytes: Egeria, Hydrilla) |
Redside shiners |
| European Green Crab | Rusty Crayfish |
| Lake trout | Smallmouth bass |
| Mysid shrimp | Walleye |
| New Zealand mudsnails | Zebra and quagga mussels |
The marine survival of ESA-listed Chinook salmon and steelhead, as well as Coho salmon declined precipitously in the 1980s and have remained low in both US and Canadian stocks within the Salish Sea. Factors affecting survival and production of these species limits treaty tribal harvest and recreational fishing opportunities, diminishes the preferred food supply and health of ESA-listed resident Killer Whale populations, and fundamentally affects management of land, water, and energy usage in the region. This research is being conducted as part of the Salish Sea Marine Survival Project (a joint US-Canada program involving over federal, state, local and provincial agencies, universities, tribes and NGOs) in collaboration with scientists from NOAA and Washington Department of Fish and Wildlife with partial funding from Long Live the Kings.
Our work on the Salish Sea Marine Survival Project (SSMSP) continues to evolve. We've identified a critical growth period for juvenile Chinook salmon during the first month of feeding in epi-pelagic habitats within Puget Sound. After the juveniles transition to these "offshore" waters, they increase their body mass by a factor of 2-4x within that first month, and that resulting body mass in mid-late July is strongly correlated to overall marine survival (Smolt-to-adult returns, SARs). We've also determined that much of the variability in growth during that critical period can be attributed to the contribution of larval crab (mostly megalops) to the energy budget of Chinook during this period.
In Puget Sound, juvenile ESA-listed Chinook salmon and Steelhead are limited by predation mortality primarily from Harbor Seals and older Resident forms of Chinook salmon. Marine mortality is strongly size-selective for Chinook salmon, so the Ecology Section is investigating the dynamic role of seasonal food supply, energy allocation, and thermal conditions during critical early marine growth periods, and how these bottom-up processes influence the efficacy of their predators. Since most predators except Killer Whales rely on primarily on vision to locate and capture salmon, we are examining how changes in underwater light and turbidity affect predation, especially the effects of increasing artificial light at night (ALAN).
So we’re currently examining a number of related questions such as:
Most aquatic vertebrates rely primarily on vision as their primary sensory mechanism for movement, feeding and avoiding predation. Visual conditions underwater vary dramatically among water bodies, but also across day-twilight-night periods, seasons and among years within the same waters. Humans have significantly altered the visual environment, but the serious implications of these changes for survival and growth of aquatic species and the function of aquatic food webs has been largely ignored. Research to date on the visual capabilities of key aquatic species like salmon and trout have been opportunistic due to a lack of coherent programmatic funding. Despite the challenges of sporadic funding and lack of consistent access to adequate experimental facilities, we have developed visual foraging models and applied these to juvenile salmon and their predators in natural environments. These exercises reveal important patterns that relate directly to how human impacts on underwater light and transparency significantly affect the survival and production of ESA-listed and economically important species.
From experimental parameterization of the visual capabilities for several predatory salmonids on juvenile salmon and other forage fishes, some important patterns emerge related to the responses of both predators and prey to environmentally-relevant changes in underwater light intensity and turbidity. Both predators and prey can feed efficiently at low light levels common during daylight and twilight down to depths of 20-30 m in clear water. Over the past few decades in and around urbanized regions, increasing artificial light pollution has created periods of perpetual twilight, supplanting dark nocturnal periods that are critical for safe migration through shallow habitats and for refuge from predation in rearing habitats.
Land and water development has also altered the natural dynamics of water transparency/turbidity via changes in sediment transport from dams or erosion and algal blooms from altered nutrient fluxes. The predators’ ability to detect and consume prey diminishes rapidly over relatively small increases in turbidity, whereas the smaller invertebrate-feeding fish like juvenile salmon are minimally affected.
The interaction of changing light and turbidity over varying spatial and temporal scales survival and growth of economically-important and trust species. Therefore, a mechanistic understanding for how variability in the visual environment affects fitness of key species and their interactions with others in the food web offers considerable potential for improving their survival and production and restoring long term function of ecosystems in an economically and ecologically effective manner.
This program would contain several essential elements:
We’re also very much involved in food web interactions involving salmonids in lakes, reservoirs and streams. With a number of hydro-electric dams coming up for relicensing with FERC (Federal Energy Regulatory Commission), a rapidly emerging theme has been examining the ecological feasibility of re-introducing anadromous salmonids above previously impassable dams (e.g., do environmental conditions, seasonal food supply, competition, predation, and connectivity among critical habitats and life stages allow for sufficient production of salmon to warrant advancing through the process of considering costly re-introductions). We apply these same approaches to examine effects of non-native species on host food webs and salmonid production, all mediated by prevailing and projected environmental conditions.
Skagit River reservoirs - In preparation for FERC relicensing of mainstem dams on the Skagit River, we will conduct a quantitative analysis of species interactions, habitat and environmental conditions that affect production of native salmonids in reservoirs and major tributaries associated with Ross, Diablo, and Gorge dams on the Skagit River, Washington. The goal of this project will be to identify and quantify factors that limit recruitment and production of native adfluvial salmonids (Bull trout, Dolly Varden, Rainbow trout) and invasive species (e.g., Redside Shiners, Brook Trout, Brown Trout) that populate the reservoirs and associated tributaries above the mainstem dams on the Skagit River (Ross, Diablo, Gorge). We will initially focus on the food web structure of the reservoir-tributary complex, the presence and geographic extent of native and non-native fishes in the basin, and habitat suitability and production capacity of select tributaries. Food web interactions, distribution, and growth of native salmonids will ultimately be linked to environmental conditions, and these will be evaluated within the context of projected changes in climate or dam operations.
Determining the relative importance of tributary and lake-rearing strategies for juvenile Spring Chinook Salmon in the Lake Wenatchee Basin - We are conducting an initial bioenergetics-based analysis of factors affecting growth and survival of juvenile Spring Chinook Salmon and the relative importance of rearing in tributary versus lake habitats in the Wenatchee Basin. We will conduct stable isotope analysis and scale-pattern analysis on archival samples, supplemented with targeted streamlined field sampling in tributary and lake habitats by collaborators from Washington Department of Fish and Wildlife and U.S. Forest Service to address questions related to the primary rearing distribution of juvenile spring Chinook salmon, their primary food sources, feeding habitats, associated growth performance, and their trophic relationships within the Wenatchee basin food web (i.e., their primary prey, competitors, and predators). The resulting information will be used to construct the initial bioenergetics modeling simulations of the temporal consumption demand by juvenile Chinook for key prey, the seasonal carrying capacity of the lake for Chinook, Sockeye, and other major planktivores, and the relative predation impact by different size classes of predators (i.e., Northern Pikeminnow and Bull Trout). The results of these simulations will quantify what we currently know about distribution, feeding, growth, and predation mortality associated with freshwater rearing phases of juvenile Chinook salmon, identify and prioritize the major uncertainties that should be targeted in subsequent research.
Feasibility of re-introducing anadromous salmonids in Lewis River Reservoirs (completed) and Lake Cushman (proposed) - Reintroductions of anadromous salmonids above formerly impassable dams are being proposed with increasing frequency in the Pacific Northwest. The suitability of reservoir habitat for rearing anadromous salmonids and interactions with resident fish affect the feasibility of reintroductions. To determine whether one or more of the Lewis River Reservoirs can support reintroduced populations of juvenile Spring Chinook and other salmonids, we evaluated prey supply and consumption demand of resident fishes to estimate the carrying capacity for planktivores. The primary resident planktivores, Kokanee and hatchery–reared Rainbow Trout were both highly dependent on Daphnia for food with a secondary reliance on insects based on stable isotope and stomach content analysis. Daphnia first bloomed in spring and remained at moderate levels with a smaller secondary peak in fall before declining to low levels in November. Zooplankton densities were highest in the epilimnion, but warm epilimnetic temperatures during peak stratification limited access by salmonids to foraging within the thermocline where densities of Daphnia were 50% lower than in the epilimnion. In all three reservoirs, consumption demand exceeded 50% of the most conservative estimate of prey resources during the growing season. However, more liberal estimates of prey supply, which included the production and standing stock biomass of the edible size-fraction of Daphnia, suggested that an additional 130,000–300,000 subyearling salmon could be supported during the most food-limited month of the growing season.
We also evaluated the predation risk from the two primary predators, Northern Pikeminnow and Tiger Muskellunge, to anadromous salmonids considered for reintroduction in Merwin Reservoir for both year–round rearing juveniles and migrating smolts. Seasonal and size-specific feeding for each predatory species was estimated using stable isotopes and stomach content analysis. We quantified seasonal per–capita predation using bioenergetics modeling, evaluated the size and age structures of the populations, and combined these inputs to estimate predation rates of size–structured populations of predators. Northern Pikeminnow ≥ 300 mm were highly cannibalistic with modest seasonal per–capita predation on salmonids, but were disproportionately much less abundant than smaller, less piscivorous conspecifics. The annual predation on Kokanee Oncorhynchus nerka (in biomass) by a size–structured unit of 1,000 Northern Pikeminnow of FL ≥ 300 mm was analogous to 16,000–40,000 age–0 spring Chinook Salmon rearing year–round in the reservoir, or 400–1,000 age–1 smolts migrating through the reservoir during April–June. The per–capita consumption of salmonids by Northern Pikeminnow of FL ≥ 200 mm was relatively low, due to spatial segregation during the summer and the skewed size distribution toward smaller, less predatory individuals in the population. Tiger muskellunge fed heavily on Northern Pikeminnow, other non–salmonids, and minimally on salmonids. Predation by tiger muskellunge, in addition to cannibalism, likely contributed to low recruitment of larger (more piscivorous) Northern Pikeminnow, effectively reducing predation risk to salmonids. This study highlights the importance of quantitatively evaluating trophic interactions within reservoirs slated for reintroduction, as they serve both as functional migration corridors and offer profitable juvenile–rearing habitats despite hosting abundant predator populations.
Below are other science projects associated with this project.
USGS scientist setting up underwater video cameras in an eelgrass meadow on the Skagit River Delta. Eelgrass grows in shallow marine and estuarine waters where it forms structurally complex habitats that support many other aquatic species by providing attachment substrate, food, refuge from predation, and nursery areas.
USGS scientist setting up underwater video cameras in an eelgrass meadow on the Skagit River Delta. Eelgrass grows in shallow marine and estuarine waters where it forms structurally complex habitats that support many other aquatic species by providing attachment substrate, food, refuge from predation, and nursery areas.
USGS scientist setting up underwater video cameras in an eelgrass meadow on the Skagit River Delta. Eelgrass grows in shallow marine and estuarine waters where it forms structurally complex habitats that support many other aquatic species by providing attachment substrate, food, refuge from predation, and nursery areas.
USGS scientist setting up underwater video cameras in an eelgrass meadow on the Skagit River Delta. Eelgrass grows in shallow marine and estuarine waters where it forms structurally complex habitats that support many other aquatic species by providing attachment substrate, food, refuge from predation, and nursery areas.
The sun setting behind the Olympic Mountains from a beach on Hood Canal, Washington. A beautiful ending of another day.
The sun setting behind the Olympic Mountains from a beach on Hood Canal, Washington. A beautiful ending of another day.
Coho salmon migrating on the Sol Duc River, Washington to spawning grounds upstream. Fish must leap through a series of small waterfalls called the Salmon Cascades in Olympic National Park to reach the waters where they were born to complete their life cycle by spawning the next generation.
Coho salmon migrating on the Sol Duc River, Washington to spawning grounds upstream. Fish must leap through a series of small waterfalls called the Salmon Cascades in Olympic National Park to reach the waters where they were born to complete their life cycle by spawning the next generation.
Coho salmon migrating on the Sol Duc River, Washington to spawning grounds upstream. Fish must leap through a series of small waterfalls called the Salmon Cascades in Olympic National Park to reach the waters where they were born to complete their life cycle by spawning the next generation.
Coho salmon migrating on the Sol Duc River, Washington to spawning grounds upstream. Fish must leap through a series of small waterfalls called the Salmon Cascades in Olympic National Park to reach the waters where they were born to complete their life cycle by spawning the next generation.
Sampling drifting invertebrates from a stream in the North Cascades of Washington State. We perform drift sampling to determine the invertebrate prey quality and quantity available for drift feeding fish. Data gathered from this sampling are used in bioenergetics modeling, a method of estimating fish growth potential.
Sampling drifting invertebrates from a stream in the North Cascades of Washington State. We perform drift sampling to determine the invertebrate prey quality and quantity available for drift feeding fish. Data gathered from this sampling are used in bioenergetics modeling, a method of estimating fish growth potential.
Photo taken from Magnuson boat launch before conducting water quality and light at depth measurements during Landsat-8 overpass windows on Lake Washington for the U.S. Geological Survey.
To learn more about this project and other related research you can visit the WFRC Ecology Section website.
Photo taken from Magnuson boat launch before conducting water quality and light at depth measurements during Landsat-8 overpass windows on Lake Washington for the U.S. Geological Survey.
To learn more about this project and other related research you can visit the WFRC Ecology Section website.
Photo taken from Magnuson boat launch before conducting a synoptic light survey of Lake Washington for the U.S. Geological Survey.
Photo taken from Magnuson boat launch before conducting a synoptic light survey of Lake Washington for the U.S. Geological Survey.
Lighting from the Kirkland waterfront viewed from the Seattle shoreline.
Photo taken from Magnuson boat launch before conducting a synoptic light survey of Lake Washington for the U.S. Geological Survey.
Lighting from the Kirkland waterfront viewed from the Seattle shoreline.
Photo taken from Magnuson boat launch before conducting a synoptic light survey of Lake Washington for the U.S. Geological Survey.
Researchers perform gastric lavage on a rainbow trout to sample its stomach contents. This fish was sampled as a part of a food web study on Ross and Diablo Lakes in Washington State to evaluate fish growth and limitations to production.
Researchers perform gastric lavage on a rainbow trout to sample its stomach contents. This fish was sampled as a part of a food web study on Ross and Diablo Lakes in Washington State to evaluate fish growth and limitations to production.
USGS boat tied to dock at Ross Lake during a week-long sampling trip for a food web study. Ross Lake is a large reservoir on the Upper Skagit River in the North Cascade mountains of northern Washington state.
USGS boat tied to dock at Ross Lake during a week-long sampling trip for a food web study. Ross Lake is a large reservoir on the Upper Skagit River in the North Cascade mountains of northern Washington state.
Researchers stage sampling equipment at the Ross Lake boat ramp and wait for boat to arrive to transport them to camping area. Food web sampling on large lakes requires a substantial amount of sampling gear. Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state.
Researchers stage sampling equipment at the Ross Lake boat ramp and wait for boat to arrive to transport them to camping area. Food web sampling on large lakes requires a substantial amount of sampling gear. Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state.
Marshal Hoy, a Biological Science Technician, angling on Ross Lake for Western Fisheries Research Center (WFRC) food web study in October 2021. As a part of this study, fish are sampled for stomach contents, scale samples to assess age and growth, and fin tissue for stable isotopes and genetic analysis.
Marshal Hoy, a Biological Science Technician, angling on Ross Lake for Western Fisheries Research Center (WFRC) food web study in October 2021. As a part of this study, fish are sampled for stomach contents, scale samples to assess age and growth, and fin tissue for stable isotopes and genetic analysis.
Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state. This photo was taken while conducting food web research to support the Skagit River Hydroelectric Dam FERC relicensing process. To learn more about this project and other related research you can visit the WFRC Ecology Section website.
Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state. This photo was taken while conducting food web research to support the Skagit River Hydroelectric Dam FERC relicensing process. To learn more about this project and other related research you can visit the WFRC Ecology Section website.
A native crayfish collected in Diablo Lake for an investigation into food availability for native fish and limitations to their growth. Crayfish are invertebrate prey for salmonids and provide useful representative stable isotope values for benthic members of the food web.
A native crayfish collected in Diablo Lake for an investigation into food availability for native fish and limitations to their growth. Crayfish are invertebrate prey for salmonids and provide useful representative stable isotope values for benthic members of the food web.
Evening shot of Ross Lake with boat wake. Heading back to camp after a day of research. Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state. This photo was taken while conducting food web research to support the Skagit River Hydroelectric Dam FERC relicensing process.
Evening shot of Ross Lake with boat wake. Heading back to camp after a day of research. Ross Lake is a large reservoir in the North Cascade mountains of northern Washington state. This photo was taken while conducting food web research to support the Skagit River Hydroelectric Dam FERC relicensing process.
The Elwha River flows through the footprint of the former reservoir Lake Mills. The wide-angle image also shows revegetated uplands dominated by alder trees meeting coniferous forest along the former shoreline of the reservoir.
The Elwha River flows through the footprint of the former reservoir Lake Mills. The wide-angle image also shows revegetated uplands dominated by alder trees meeting coniferous forest along the former shoreline of the reservoir.
Researchers on their way to sampling site on Diablo Lake. Diablo Lake is a reservoir in the North Cascade mountains of northern Washington. Created by Diablo Dam, the lake is located between Ross Lake and Gorge Lake on the Skagit River.
Researchers on their way to sampling site on Diablo Lake. Diablo Lake is a reservoir in the North Cascade mountains of northern Washington. Created by Diablo Dam, the lake is located between Ross Lake and Gorge Lake on the Skagit River.
Aerial photograph of the mouth of the Elwha River showing sediment deposits from dam removal. Aerial assistance by LightHawk and plane piloted by Dr. Milton Bennett.
Aerial photograph of the mouth of the Elwha River showing sediment deposits from dam removal. Aerial assistance by LightHawk and plane piloted by Dr. Milton Bennett.
Biologists snorkel the Bogachiel River in Washington State to count resident and migratory fish as part of a riverscape survey.
Biologists snorkel the Bogachiel River in Washington State to count resident and migratory fish as part of a riverscape survey.
Re-vegetation in the river valley at the Elwha River restoration site. Image available at Olympic National Park flickr site.
Re-vegetation in the river valley at the Elwha River restoration site. Image available at Olympic National Park flickr site.
