Ecology of the northern subpopulation of northern anchovy (Engraulis mordax) in the California Current large marine ecosystem

Northern anchovy (Engraulis mordax) are a dominant forage fish in the California Current large marine ecosystem (CCLME). However, little is known about northern anchovy abundance, distribution, age structure, or population fluctuations relative to ocean conditions in the eastern boundary upwelling system off the U.S. West Coast. This thesis includes three primary studies of northern anchovy in the CCLME off Oregon and Washington using data collected during four National Marine Fisheries Service (NMFS) surveys (1977-2006): inter- and intra-annual variation in anchovy distribution and its relationship to oceanography, growth rates of larval and juvenile anchovy that indicate the timing of major spawning events and changes in mortality rates, and analysis of whole lipids and fatty acid profiles to determine food sources in years of contrasting oceanographic conditions. First, I quantified the relationship between northern anchovy abundance with environmental variables at two spatial and temporal scales: 1) mesoscale, including sea surface temperature (SST), salinity (SSS), density (SSD), chlorophyll a, distance from shore, and depth; and 2) macroscale, including Pacific Decadal Oscillation Index, Multivariate El Niño Southern Oscillation Index, timing of the Spring Transition, and abundance of cold-water zooplankton. Anchovy densities increased significantly from 1999-2004, and decreased significantly from 2005-2006. SST and proximity to shore were the most consistent parameters explaining anchovy distribution. Year-class strength was highly correlated with, and presumably driven by, the abundance of cold-water copepods. Second, I characterized recruitment for northern anchovy by conducting microstructure analysis of saggital otoliths from late larval and juvenile life history phases collected in September 2006. I identified a protracted spawning period for northern anchovy ranging from June-August 2006. Juveniles that were spawned and hatched early in the summer 2006 had higher growth rates, but smaller back-calculated sizes-at-age during the larval phase, when compared to congeners spawned later that summer. Finally, I determined total lipid content and fatty acid signatures of northern anchovy and three other forage fish species during two contrasting periods of oceanographic conditions (summers of 2005 and 2006): Pacific sardine (Sardinops sagax), Pacific herring (Clupea harengus pallasii), and whitebait smelt (Allosmerus elongatus). Forage fish lipid levels were lowest in 2005 and increased in 2006. Fatty acid biomarkers in 2005 indicated that the food web was based mainly on dinoflagellates, corroborating observations of delayed coastal upwelling and low primary productivity in the CCLME. In 2006, fatty acids reflected higher levels of diatom feeding and zooplankton carnivory. The results of these studies confirm that in the CCLME, northern anchovy are sensitive to even small environmental perturbations, which is important because this work provides metrics for evaluating climate-mediated, bottom-up ecological processes affecting anchovy survival.Keywords: anchovy, fatty acids, otolith microstructure, ecology, forage fish, regime shif

Feeding Ecology and Growth of Juvenile Chinook Salmon (Oncorhynchus tshawytscha) During Early Marine Residence

The early marine phase following freshwater emigration has been identified as a critical period in salmonid (Oncorhynchus spp.) life history, characterized by high but variable mortality. Consistent with the “growth-mortality” and “bigger-is-better” hypotheses, at least some of the mortality during the critical period appears to be size-dependent – with smaller or slower growing individuals less likely to survive than larger, faster growing conspecifics. Size and growth are flexible morphological traits that vary with prey availability, yet there is incomplete information on the temporal and spatial match/mismatch between juvenile salmonids and their marine prey in the Northern California Current Ecosystem. This work addressed a gap in the understanding of seasonal variability in prey community composition, abundance, and quality during early marine residence. Three studies were conducted using a population of subyearling (age-0) Chinook salmon (O. tshawytscha) from the upper Columbia River in order to evaluate the effects of prey on salmon growth, biochemistry, and performance. The first was a laboratory study that tested for growth rate and swimming speed differences in salmon reared on three treatment diets followed by three fasting treatments to assess the effects of variability in summer diet quality and winter diet quantity. Significant differences in growth were detected among fasting treatments but not diet treatments. Also, larger salmon with more storage lipids swam faster than smaller leaner fish following fasting, indirectly supporting the notion that growth during the critical period provides a carryover benefit important for overwinter survival. Salmon fatty acids and bulk stable isotopes of carbon and nitrogen were measured throughout the experiment to provide estimates of turnover and incorporation rates. The next study was a longitudinal field study that measured variation in salmon size and prey field community throughout the early ocean period (May – September) over two years of high marine survival (2011 and 2012) to better understand the relationship between prey community composition and salmon growth. Maximum growth rates were associated with high biomass of northern anchovy (Engraulis mordax) which peaked in abundance at different times in each year. The final bioenergetics modeling study combined data from the laboratory and field studies to evaluate the relative importance of prey availability, prey energy density, and temperature on salmon growth. Variation in feeding rate was related most with growth rate variability and least with prey energy density. Throughout their range, subyearlings can grow at high rates in the ocean (>2% body weight per day) by consuming both invertebrate and marine fish prey. However, when marine fish prey are highly abundant they likely provide an energetic advantage over invertebrate prey by reducing overall foraging costs. Quantifying the abundance, size, diet, and distribution of juvenile salmonids relative to their prey field throughout early ocean residence will contribute to a better understanding of seasonal differences in trophic interactions that are associated with differences in annual growth and survival rates. Moreover, an integrated approach that combines sampling of prey with measurements of predator growth, diet, fatty acids, and stable isotopes provides a useful framework for assessing trophic dynamics and evaluating the effects of climate variability and change on predator and prey communities

Seasonal and interannual variation in juvenile salmonids and associated fish assemblage in open waters of the lower Columbia River estuary

The transition between freshwater and marine environments is associated with high mortality for juvenile anadromous salmonids, yet little is known about this critical period in many large rivers. To address this deficiency, we investigated the estuarine ecology of juvenile salmonids and their associated fish assemblage in open-water habitats of the lower Columbia River estuary during spring of 2007–10. For coho (Oncorhynchus kisutch), sockeye (O. nerka), chum (O. keta), and yearling (age 1.0) Chinook (O. tshawytscha) salmon, and steelhead (O. mykiss), we observed a consistent seasonal pattern characterized by extremely low abundances in mid-April, maximum abundances in May, and near absence by late June. Subyearling (age 0.0) Chinook salmon were most abundant in late June. Although we observed interannual variation in the presence, abundance, and size of juvenile salmonids, no single year was exceptional across all species-and-age classes. We estimated that >90% of juvenile Chinook and coho salmon and steelhead were of hatchery origin, a rate higher than previously reported. In contrast to juvenile salmonids, the abundance and composition of the greater estuarine fish assemblage, of which juvenile salmon were minor members, were extremely variable and likely responding to dynamic physical conditions in the estuary. Comparisons with studies conducted 3 decades earlier suggest striking changes in the estuarine fish assemblage—changes that have unknown but potentially important consequences for juvenile salmon in the Columbia River estuary.This is the publisher’s final pdf. The published article is copyrighted by National Marine Fisheries Service, NOAA, Scientific Publications Office and can be found at: http://fishbull.noaa.gov

Effects of Variable Oceanographic Conditions on Forage Fish Lipid Content and Fatty Acid Composition in the Northern California Current

Lipids and fatty acids (FA) were investigated in 4 species of forage fish: northern anchovy Engraulis mordax, Pacific sardine Sardinops sagax, Pacific herring Clupea pallasi, and whitebait smelt Allosmerus elongatus, for their ability to serve as biological indicators of ocean conditions in the California Current large marine ecosystem (CCLME). Samples were collected during the oceanographically contrasting years of 2005 and 2006. Upwelling was severely curtailed in the spring and early summer of 2005, leading to delayed biological productivity, whereas upwelling was relatively normal in spring 2006. Principal components analysis described 78% of the variance within the lipid and FA dataset using the first 2 principal components. We found significant intra- and interspecific, interannual, and seasonal differences in lipid and FA profiles using univariate and permutation- based multivariate analysis of variance. Indicator species analysis showed distinct lipid and FA properties associated with each fish species. Using the ratio of docosahexaenoic acid (C22:6n-3) to eicosapentaeonic acid (C20:5n-3), we detected a transition from a diet composed primarily of dinoflagellate origin in early 2005 to a diet resulting from diatom-based productivity by late summer 2006. This shift was due to interannual differences in primary production, which was confirmed through phytoplankton sampling. Our study demonstrates that lipid and FA biomarkers in the forage fish community can provide information on ocean conditions and productivity that affect food web structure in the CCLME

Biotic and abiotic factors influencing forage fish and pelagic nekton community in the Columbia River plume (USA) throughout the upwelling season 1999–2009

Large river plumes modify coastal environments and can impact production across multiple trophic levels. From 1999 to 2009, the assemblages of forage fish, predator fish, and other pelagic nekton were monitored in coastal waters associated with the Columbia River plume. Surveys were conducted at night to target vertically migrating species, and community structure evaluated to better understand ecological interactions. Distinct inshore and offshore communities were identified during spring and summer that were correlated with ocean temperature, salinity, plume volume, and upwelling intensity. Resident euryhaline forage fish species, such as smelts, anchovy, herring, market squid, juvenile salmon, and spiny dogfish, showed a high affinity for inshore habitat and the lower salinity plume during spring. Highly migratory species, such as sardine, piscivorous hake, sharks, and mackerels, were associated with warmer, saltier waters offshore, during strong upwelling periods in summer. Overall, our study of pelagic nekton revealed that temporal dynamics in abundance and community composition were associated with seasonal abiotic phenomenon, but not interannual, large-scale oceanographic processes. Forage fish assemblages differed seasonally and spatially from the assemblages of major piscivorous predators. This finding suggests a potential role of the plume as refuge for forage fish from predation by piscivorous fish in the northern California Current.Keywords: Predator fish, Columbia River plume, California current, Community analysis, Forage fishKeywords: Predator fish, Columbia River plume, California current, Community analysis, Forage fis

Multivariate Models of Adult Pacific Salmon Returns

Most modeling and statistical approaches encourage simplicity, yet ecological processes are often complex, as they are influenced by numerous dynamic environmental and biological factors. Pacific salmon abundance has been highly variable over the last few decades and most forecasting models have proven inadequate, primarily because of a lack of understanding of the processes affecting variability in survival. Better methods and data for predicting the abundance of returning adults are therefore required to effectively manage the species. We combined 31 distinct indicators of the marine environment collected over an 11-year period into a multivariate analysis to summarize and predict adult spring Chinook salmon returns to the Columbia River in 2012. In addition to forecasts, this tool quantifies the strength of the relationship between various ecological indicators and salmon returns, allowing interpretation of ecosystem processes. The relative importance of indicators varied, but a few trends emerged. Adult returns of spring Chinook salmon were best described using indicators of bottom-up ecological processes such as composition and abundance of zooplankton and fish prey as well as measures of individual fish, such as growth and condition. Local indicators of temperature or coastal upwelling did not contribute as much as large-scale indicators of temperature variability, matching the spatial scale over which salmon spend the majority of their ocean residence. Results suggest that effective management of Pacific salmon requires multiple types of data and that no single indicator can represent the complex early-ocean ecology of salmon

Responses in growth rate of larval northern anchovy (Engraulis mordax) to anomalous upwelling in the northern California Current

We examined variability in growth rate during the larval stage of northern anchovy (Engraulis mordax) in response to physical and biological environmental factors in 2005 and 2006. The onset of spring upwelling was anomalously delayed by 2–3 months until mid-July in 2005; in contrast, spring upwelling in 2006 began as a normal year in the northern California Current. Larval and early juvenile E. mordax were collected in August, September, and October off the coast of Oregon and Washington. Hatch dates ranged from May to September, with peaks in June and August in 2005 and a peak in July in 2006, based on the number of otolith daily increments. Back-calculated body length-at-age in the June 2005 hatch cohort was significantly smaller than in the August 2005 cohort, which had comparable growth to the July 2006 cohort. Standardized otolith daily increment widths as a proxy for seasonal variability in somatic growth rates in 2005 were negative until late July and then changed to positive with intensification of upwelling. The standardized increment width was a positive function of biomass of chlorophyll a concentration, and neritic cold-water and oceanic subarctic copepod species sampled biweekly off Newport, Oregon. Our results suggest that delayed upwelling in 2005 resulted in low food availability and, consequently, reduced E. mordax larval growth rate in early summer, but once upwelling began in July, high food availability enhanced larval growth rate to that typical of a normal upwelling year (e.g., 2006) in the northern California Current.Keywords: otolith, growth rate, northern anchovy, delayed upwelling, increment width, California CurrentKeywords: otolith, growth rate, northern anchovy, delayed upwelling, increment width, California Curren

Multivariate models of adult Pacific salmon returns.

Most modeling and statistical approaches encourage simplicity, yet ecological processes are often complex, as they are influenced by numerous dynamic environmental and biological factors. Pacific salmon abundance has been highly variable over the last few decades and most forecasting models have proven inadequate, primarily because of a lack of understanding of the processes affecting variability in survival. Better methods and data for predicting the abundance of returning adults are therefore required to effectively manage the species. We combined 31 distinct indicators of the marine environment collected over an 11-year period into a multivariate analysis to summarize and predict adult spring Chinook salmon returns to the Columbia River in 2012. In addition to forecasts, this tool quantifies the strength of the relationship between various ecological indicators and salmon returns, allowing interpretation of ecosystem processes. The relative importance of indicators varied, but a few trends emerged. Adult returns of spring Chinook salmon were best described using indicators of bottom-up ecological processes such as composition and abundance of zooplankton and fish prey as well as measures of individual fish, such as growth and condition. Local indicators of temperature or coastal upwelling did not contribute as much as large-scale indicators of temperature variability, matching the spatial scale over which salmon spend the majority of their ocean residence. Results suggest that effective management of Pacific salmon requires multiple types of data and that no single indicator can represent the complex early-ocean ecology of salmon

Observed and predicted spring Chinook adult returns.

<p>Observed spring Chinook adult returns (solid circles) and leave-one-out predictions (open diamonds) with 95% prediction intervals obtained from MCA. Predicted returns in 2011 and 2012 (2009 and 2010 juvenile migration year) are shown with 95% prediction intervals (grey diamonds).</p

Indicator importance values.

<p>Percent of variance in salmon returns explained in the MCA analysis that can be attributed to each indicator (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0054134#pone-0054134-t001" target="_blank">Table 1</a>).</p