Marine heatwaves disrupt ecosystem structure and function via altered food webs and energy flux.

The prevalence and intensity of marine heatwaves is increasing globally, disrupting local environmental conditions. The individual and population-level impacts of prolonged heatwaves on marine species have recently been demonstrated, yet whole-ecosystem consequences remain unexplored. We leveraged time series abundance data of 361 taxa, grouped into 86 functional groups, from six long-term surveys, diet information from a new diet database, and previous modeling efforts, to build two food web networks using an extension of the popular Ecopath ecosystem modeling framework, Ecotran. We compare ecosystem models parameterized before and after the onset of recent marine heatwaves to evaluate the cascading effects on ecosystem structure and function in the Northeast Pacific Ocean. While the ecosystem-level contribution (prey) and demand (predators) of most functional groups changed following the heatwaves, gelatinous taxa experienced the largest transformations, underscored by the arrival of northward-expanding pyrosomes. We show altered trophic relationships and energy flux have potentially profound consequences for ecosystem structure and function, and raise concerns for populations of threatened and harvested species.

An updated end-to-end ecosystem model of the Northern California Current reflecting ecosystem changes due to recent marine heatwaves.

The Northern California Current is a highly productive marine upwelling ecosystem that is economically and ecologically important. It is home to both commercially harvested species and those that are federally listed under the U.S. Endangered Species Act. Recently, there has been a global shift from single-species fisheries management to ecosystem-based fisheries management, which acknowledges that more complex dynamics can reverberate through a food web. Here, we have integrated new research into an end-to-end ecosystem model (i.e., physics to fisheries) using data from long-term ocean surveys, phytoplankton satellite imagery paired with a vertically generalized production model, a recently assembled diet database, fishery catch information, species distribution models, and existing literature. This spatially-explicit model includes 90 living and detrital functional groups ranging from phytoplankton, krill, and forage fish to salmon, seabirds, and marine mammals, and nine fisheries that occur off the coast of Washington, Oregon, and Northern California. This model was updated from previous regional models to account for more recent changes in the Northern California Current (e.g., increases in market squid and some gelatinous zooplankton such as pyrosomes and salps), to expand the previous domain to increase the spatial resolution, to include data from previously unincorporated surveys, and to add improved characterization of endangered species, such as Chinook salmon (Oncorhynchus tshawytscha) and southern resident killer whales (Orcinus orca). Our model is mass-balanced, ecologically plausible, without extinctions, and stable over 150-year simulations. Ammonium and nitrate availability, total primary production rates, and model-derived phytoplankton time series are within realistic ranges. As we move towards holistic ecosystem-based fisheries management, we must continue to openly and collaboratively integrate our disparate datasets and collective knowledge to solve the intricate problems we face. As a tool for future research, we provide the data and code to use our ecosystem model.

Spatiotemporal patterns of variability in the abundance and distribution of winter-spawned pelagic juvenile rockfish in the California Current.

Rockfish are an important component of West Coast fisheries and California Current food webs, and recruitment (cohort strength) for rockfish populations has long been characterized as highly variable for most studied populations. Research efforts and fisheries surveys have long sought to provide greater insights on both the environmental drivers, and the fisheries and ecosystem consequences, of this variability. Here, variability in the temporal and spatial abundance and distribution patterns of young-of-the-year (YOY) rockfishes are described based on midwater trawl surveys conducted throughout the coastal waters of California Current between 2001 and 2019. Results confirm that the abundance of winter-spawning rockfish taxa in particular is highly variable over space and time. Although there is considerable spatial coherence in these relative abundance patterns, there are many years in which abundance patterns are very heterogeneous over the scale of the California Current. Results also confirm that the high abundance levels of YOY rockfish observed during the 2014-2016 large marine heatwave were largely coastwide events. Species association patterns of pelagic YOY for over 20 rockfish taxa in space and time are also described. The overall results will help inform future fisheries-independent surveys, and will improve future indices of recruitment strength used to inform stock assessment models and marine ecosystem status reports.

Responses of ichthyoplankton assemblages to the recent marine heatwave and previous climate fluctuations in several Northeast Pacific marine ecosystems.

The effects of climate warming on ecosystem dynamics are widespread throughout the world's oceans. In the Northeast Pacific, large-scale climate patterns such as the El Niño/Southern Oscillation and Pacific Decadal Oscillation, and recently unprecedented warm ocean conditions from 2014 to 2016, referred to as a marine heatwave (MHW), resulted in large-scale ecosystem changes. Larval fishes quickly respond to environmental variability and are sensitive indicators of ecosystem change. Categorizing ichthyoplankton dynamics across marine ecosystem in the Northeast Pacific can help elucidate the magnitude of assemblage shifts, and whether responses are synchronous or alternatively governed by local responses to regional oceanographic conditions. We analyzed time-series data of ichthyoplankton abundances from four ecoregions in the Northeast Pacific ranging from subarctic to subtropical: the Gulf of Alaska (1981-2017), British Columbia (2001-2017), Oregon (1998-2017), and the southern California Current (1981-2017). We assessed the impact of the recent (2014-2016) MHW and how ichthyoplankton assemblages responded to past major climate perturbations since 1981 in these ecosystems. Our results indicate that the MHW caused widespread changes in the ichthyoplankton fauna along the coast of the Northeast Pacific Ocean, but impacts differed between marine ecosystems. For example, abundances for most dominant taxa were at all-time lows since the beginning of sampling in the Gulf of Alaska and British Columbia, while in Oregon and the southern California Current species richness increased as did abundances of species associated with warmer waters. Lastly, species associated with cold waters also increased in abundances close to shore in southern California during the MHW, a pattern that was distinctly different from previous El Niño events. We also found several large-scale, synchronized ichthyoplankton assemblage composition shifts during past major climate events. Current climate projections suggest that MHWs will become more intense and thus our findings can help project future changes in larval dynamics, allowing for improved ecosystem management decisions.

Percent ash-free dry weight as a robust method to estimate energy density across taxa.

Determining how energy flows through ecosystems reveals underlying ecological patterns that drive processes such as growth and food web dynamics. Models that assess the transfer of energy from producers to consumers require information on the energy content or energy density (ED) of prey species. ED is most accurately measured through bomb calorimetry, but this method suffers from limitations of cost, time, and sample requirements that often make it unrealistic for many studies. Percent dry weight (DW) is typically used as a proxy for ED, but this measure includes an indigestible portion (e.g., bones, shell, salt) that can vary widely among organisms. Further, several distinct models exist for various taxonomic groups, yet none can accurately estimate invertebrate, vertebrate and plant ED with a single equation. Here, we present a novel method to estimate the ED of organisms using percent ash-free dry weight (AFDW). Using data obtained from 11 studies diverse in geographic, temporal and taxonomic scope, AFDW, DW as well as percent protein and percent lipid were compared as predictors of ED. Linear models were produced on a logarithmic scale, including dummy variables for broad taxonomic groups. AFDW was the superior predictor of ED compared to DW, percent protein content and percent lipid content. Model selection revealed that using correction factors (dummy variables) for aquatic animals (AA) and terrestrial invertebrates (TI) produced the best-supported model-log10(ED) = 1.07*log10(AFDW) - 0.80 (R 2 = 0.978, p < .00001)-with an intercept adjustment of 0.09 and 0.04 for AA and TI, respectively. All models including AFDW as a predictor had high predictive power (R 2 > 0.97), suggesting that AFDW can be used with high degrees of certainty to predict the ED of taxonomically diverse organisms. Our AFDW model will allow ED to be determined with minimal cost and time requirements and excludes ash-weight from estimates of digestible mass. Its ease of use will allow for ED to be more readily and accurately determined for diverse taxa across different ecosystems.

Unclear associations between small pelagic fish and jellyfish in several major marine ecosystems.

During the last 20 years, a series of studies has suggested trends of increasing jellyfish (Cnidaria and Ctenophora) biomass in several major ecosystems worldwide. Some of these systems have been heavily fished, causing a decline among their historically dominant small pelagic fish stocks, or have experienced environmental shifts favouring jellyfish proliferation. Apparent reduction in fish abundance alongside increasing jellyfish abundance has led to hypotheses suggesting that jellyfish in these areas could be replacing small planktivorous fish through resource competition and/or through predation on early life stages of fish. In this study, we test these hypotheses using extended and published data of jellyfish, small pelagic fish and crustacean zooplankton biomass from four major ecosystems within the period of 1960 to 2014: the Southeastern Bering Sea, the Black Sea, the Northern California Current and the Northern Benguela. Except for a negative association between jellyfish and crustacean zooplankton in the Black Sea, we found no evidence of jellyfish biomass being related to the biomass of small pelagic fish nor to a common crustacean zooplankton resource. Calculations of the energy requirements of small pelagic fish and jellyfish stocks in the most recent years suggest that fish predation on crustacean zooplankton is 2-30 times higher than jellyfish predation, depending on ecosystem. However, compared with available historical data in the Southeastern Bering Sea and the Black Sea, it is evident that jellyfish have increased their share of the common resource, and that jellyfish can account for up to 30% of the combined fish-jellyfish energy consumption. We conclude that the best available time-series data do not suggest that jellyfish are outcompeting, or have replaced, small pelagic fish on a regional scale in any of the four investigated ecosystems. However, further clarification of the role of jellyfish requires higher-resolution spatial, temporal and taxonomic sampling of the pelagic community.

Pelagic marine refugia and climatically sensitive areas in an eastern boundary current upwelling system.

Refugia are areas relatively buffered from contemporary climate change that enable the persistence of valued physical, ecological, or sociocultural resources. Spatially identifying refugia is important for conservation and applied management. Yet the concept of refugia has not been broadly extended to marine ecosystems. Here, we analyze data from a unique and long-term (1999-2015) standardized survey of pelagic marine and anadromous species off Oregon and Washington in the northern California Current to identify such refugia. We use quantitative approaches to assess locations with high species richness and community persistence relative to local and basin-scale environmental fluctuations. We have identified a potential climate change refugial zone along the continental shelf of Washington State in the Northeastern Pacific Ocean, characterized by a species-rich community with low interannual temporal community change. This region contrasts with adjacent areas to the south and offshore that have lower species richness, and higher temporal species community change. Also, using spatially variant generalized additive mixed models, we identify areas with species compositions that are more influenced by basin-scale climatic fluctuations than others. We propose that upwelling regions with retentive topographic features, such as wide continental shelves, can function as marine refugia for pelagic fauna, whereas offshore locations are potentially more climatically sensitive and experience high temporal change in species composition. Further identification of these marine refugia using in situ data for pelagic biodiversity and climatically sensitive areas can help guide management in the face of inevitable climatically driven change.

Phenological and distributional shifts in ichthyoplankton associated with recent warming in the northeast Pacific Ocean.

Understanding changes in the migratory and reproductive phenology of fish stocks in relation to climate change is critical for accurate ecosystem-based fisheries management. Relocation and changes in timing of reproduction can have dramatic effects upon the success of fish populations and throughout the food web. During anomalously warm conditions (1-4°C above normal) in the northeast Pacific Ocean during 2015-2016, we documented shifts in timing and spawning location of several pelagic fish stocks based on larval fish samples. Total larval concentrations in the northern California Current (NCC) during winter (January-March) 2015 and 2016 were the highest observed since annual collections first occurred in 1998, primarily due to increased abundances of Engraulis mordax (northern anchovy) and Sardinops sagax (Pacific sardine) larvae, which are normally summer spawning species in this region. Sardinops sagax and Merluccius productus (Pacific hake) exhibited an unprecedented early and northward spawning expansion during 2015-16. In addition, spawning duration was greatly increased for E. mordax, as the presence of larvae was observed throughout the majority of 2015-16, indicating prolonged and nearly continuous spawning of adults throughout the warm period. Larvae from all three of these species have never before been collected in the NCC as early in the year. In addition, other southern species were collected in the NCC during this period. This suggests that the spawning phenology and distribution of several ecologically and commercially important fish species dramatically and rapidly changed in response to the warming conditions occurring in 2014-2016, and could be an indication of future conditions under projected climate change. Changes in spawning timing and poleward migration of fish populations due to warmer ocean conditions or global climate change will negatively impact areas that were historically dependent on these fish, and change the food web structure of the areas that the fish move into with unforeseen consequences.

Warming Ocean Conditions Relate to Increased Trophic Requirements of Threatened and Endangered Salmon.

The trophic habits, size and condition of yearling Chinook salmon (Oncorhynchus tshawytscha) caught early in their marine residence were examined during 19 survey years (1981-1985; 1998-2011). Juvenile salmon consumed distinct highly piscivorous diets in cold and warm ocean regimes with major differences between ocean regimes driven by changes in consumption of juvenile rockfishes, followed by several other fish prey, adult euphausiids and decapod larvae. Notable, Chinook salmon consumed 30% more food in the warm versus cold ocean regime in both May and June. Additionally, there were about 30% fewer empty stomachs in the warm ocean regime in May, and 10% fewer in warm June periods. The total prey energy density consumed during the warmer ocean regime was also significantly higher than in cold. Chinook salmon had lower condition factor and were smaller in fork length during the warm ocean regime, and were longer and heavier for their size during the cold ocean regime. The significant increase in foraging during the warm ocean regime occurred concurrently with lower available prey biomass. Adult return rates of juvenile Chinook salmon that entered the ocean during a warm ocean regime were lower. Notably, our long term data set contradicts the long held assertion that juvenile salmon eat less in a warm ocean regime when low growth and survival is observed, and when available prey are reduced. Comparing diet changes between decades under variable ocean conditions may assist us in understanding the effects of projected warming ocean regimes on juvenile Chinook salmon and their survival in the ocean environment. Bioenergetically, the salmon appear to require more food resources during warm ocean regimes.

Trace levels of Fukushima disaster radionuclides in East Pacific albacore.

The Fukushima Daiichi power station released several radionuclides into the Pacific following the March 2011 earthquake and tsunami. A total of 26 Pacific albacore (Thunnus alalunga) caught off the Pacific Northwest U.S. coast between 2008 and 2012 were analyzed for (137)Cs and Fukushima-attributed (134)Cs. Both 2011 (2 of 2) and several 2012 (10 of 17) edible tissue samples exhibited increased activity concentrations of (137)Cs (234-824 mBq/kg of wet weight) and (134)Cs (18.2-356 mBq/kg of wet weight). The remaining 2012 samples and all pre-Fukushima (2008-2009) samples possessed lower (137)Cs activity concentrations (103-272 mBq/kg of wet weight) with no detectable (134)Cs activity. Age, as indicated by fork length, was a strong predictor for both the presence and concentration of (134)Cs (p < 0.001). Notably, many migration-aged fish did not exhibit any (134)Cs, suggesting that they had not recently migrated near Japan. None of the tested samples would represent a significant change in annual radiation dose if consumed by humans.

Recurrent jellyfish blooms are a consequence of global oscillations.

A perceived recent increase in global jellyfish abundance has been portrayed as a symptom of degraded oceans. This perception is based primarily on a few case studies and anecdotal evidence, but a formal analysis of global temporal trends in jellyfish populations has been missing. Here, we analyze all available long-term datasets on changes in jellyfish abundance across multiple coastal stations, using linear and logistic mixed models and effect-size analysis to show that there is no robust evidence for a global increase in jellyfish. Although there has been a small linear increase in jellyfish since the 1970s, this trend was unsubstantiated by effect-size analysis that showed no difference in the proportion of increasing vs. decreasing jellyfish populations over all time periods examined. Rather, the strongest nonrandom trend indicated jellyfish populations undergo larger, worldwide oscillations with an approximate 20-y periodicity, including a rising phase during the 1990s that contributed to the perception of a global increase in jellyfish abundance. Sustained monitoring is required over the next decade to elucidate with statistical confidence whether the weak increasing linear trend in jellyfish after 1970 is an actual shift in the baseline or part of an oscillation. Irrespective of the nature of increase, given the potential damage posed by jellyfish blooms to fisheries, tourism, and other human industries, our findings foretell recurrent phases of rise and fall in jellyfish populations that society should be prepared to face.

Functional responses and scaling in predator-prey interactions of marine fishes: contemporary issues and emerging concepts.

Predator-prey interactions are a primary structuring force vital to the resilience of marine communities and sustainability of the world's oceans. Human influences on marine ecosystems mediate changes in species interactions. This generality is evinced by the cascading effects of overharvesting top predators on the structure and function of marine ecosystems. It follows that ecological forecasting, ecosystem management, and marine spatial planning require a better understanding of food web relationships. Characterising and scaling predator-prey interactions for use in tactical and strategic tools (i.e. multi-species management and ecosystem models) are paramount in this effort. Here, we explore what issues are involved and must be considered to advance the use of predator-prey theory in the context of marine fisheries science. We address pertinent contemporary ecological issues including (1) the approaches and complexities of evaluating predator responses in marine systems; (2) the 'scaling up' of predator-prey interactions to the population, community, and ecosystem level; (3) the role of predator-prey theory in contemporary fisheries and ecosystem modelling approaches; and (4) directions for the future. Our intent is to point out needed research directions that will improve our understanding of predator-prey interactions in the context of the sustainable marine fisheries and ecosystem management.