Hypoxia vulnerability in the salmon watersheds of Southeast Alaska.

The frequency of dissolved oxygen depletion events (hypoxia) in coastal aquatic ecosystems has risen dramatically since the late 20th century, yet the causes and consequences of hypoxia for some culturally and economically important species remain poorly understood. In rivers, oxygen depletion can be caused by high densities of spawning Pacific salmon (Oncorhynchus spp.) consuming oxygen faster than can be replaced by reaeration. This process may be exacerbated when salmon densities are artificially inflated, such as when hatchery-origin salmon stray into rivers instead of returning to hatcheries. In Southeast Alaska, hatchery salmon production has increased rapidly since the 1970s, with over 553 million chum salmon (O. keta) and 64 million pink salmon (O. gorbuscha) released in 2021 alone. Straying is pervasive in streams with outlets <25 km from nearshore marine hatchery release sites. Using a previously ground-truthed mechanistic model of dissolved oxygen dynamics, we examined how water temperature and low-flow channel hydraulics contribute to hypoxia vulnerability. We then applied the model to predict hypoxia vulnerability for watersheds within 25 km of hatchery salmon release points, where straying salmon spawner densities are expected to be higher and promote dissolved oxygen depletion. Our model predicted that low-gradient stream reaches, regardless of water temperature, are the most prone to hypoxia due to low reaeration rates. Our spatial analysis determined that nearly 17,000 km of anadromous-accessible stream reaches are vulnerable to high densities of hatchery-origin salmon based on 2021 release sites. To our knowledge, this study is the first to map the spatial variation of hypoxia vulnerability in anadromous watersheds, identify habitat conditions most likely to promote hypoxia, and provide a repeatable analytical approach to identify hypoxia-prone stream reaches that can be updated as empirical data sets improve.

Pan-Arctic marine biodiversity and species co-occurrence patterns under recent climate.

The Arctic region is experiencing drastic climatic changes bringing about potential ecological shifts. Here, we explored marine biodiversity and potential species associations across eight Arctic marine areas between 2000 and 2019. We compiled species occurrences for a subset of 69 marine taxa (i.e., 26 apex predators and 43 mesopredators) and environmental factors to predict taxon-specific distributions using a multi-model ensemble approach. Arctic-wide temporal trends of species richness increased in the last 20 years and highlighted potential emerging areas of species accrual due to climate-driven species redistribution. Further, regional species associations were dominated by positive co-occurrences among species pairs with high frequencies in the Pacific and Atlantic Arctic areas. Comparative analyses of species richness, community composition, and co-occurrence between high and low summer sea ice concentrations revealed contrasting impacts of and detected areas vulnerable to sea ice changes. In particular, low (high) summer sea ice generally resulted in species gains (loss) in the inflow and loss (gains) in the outflow shelves, accompanied by substantial changes in community composition and therefore potential species associations. Overall, the recent changes in biodiversity and species co-occurrences in the Arctic were driven by pervasive poleward range shifts, especially for wide-ranging apex predators. Our findings highlight the varying regional impacts of warming and sea ice loss on Arctic marine communities and provide important insights into the vulnerability of Arctic marine areas to climate change.

Marine biodiversity refugia in a climate-sensitive subarctic shelf.

The subarctic shelf of the Eastern Bering Sea (EBS) is one of the world's most productive marine environments, exposed to drastic climate changes characterized by extreme fluctuations in temperature, sea ice concentration, timing, and duration. These climatic changes elicit profound responses in species distribution, abundance, and community composition. Here, we examined the patterns of alpha and temporal beta diversity of 159 marine taxa (66 vertebrates and 93 invertebrate species) from 29 years (1990-2018) of species observations from the NOAA bottom trawl surveys in the EBS. Based on these data, we identified geographically distinct refugial zones in the northern and southern regions of the middle shelf, defined by high species richness and similarity in community species composition over time. These refugial zones harbor higher frequencies of occurrence for representative taxa relative to the regions outside of refugia. We also explored the primary environmental factors structuring marine biodiversity distributions, which underpinned the importance of the winter sea ice concentration to alpha and temporal beta diversity. The spatial biodiversity distributions between high and low winter sea ice regimes highlighted contrasting signals. In particular, the latter showed elevated species richness compared to the former. Further, the temporal beta diversity between the high and low winter sea ice periods underpinned an overall increase in the compositional similarity of marine communities in the EBS. Despite these spatiotemporal differences in biodiversity distributions, the identified refugia represent safe havens of marine biodiversity in the EBS. Distinguishing these areas can help facilitate conservation and management efforts under accelerated and ongoing climatic changes.

Metals in the stomach contents and brain, gonad, kidney, and liver tissues of subsistence-harvested northern sea otters (Enhydra lutris kenyoni) from Icy Strait, Alaska.

Southeast Alaska sea otters (Enhydra lutris) have had a rapid rise in their population. As they feed primarily on sessile prey, they are excellent sentinels for examining metals contamination. Objectives of this study on sea otters were to determine: (1) concentrations of metals in different tissues; (2) whether metals biomagnify from stomach contents (i.e., the prey) to other tissues; (3) whether selenium and mercury concentrations indicate an overall health benefit or risk; and (4) if metals concentrations in tissues vary with body size. Brain, kidney, gonad, liver, and stomach contents were collected from freshly harvested sea otters in Icy Strait, Alaska, and analyzed for arsenic (As), cadmium (Cd), copper (Cu), lead (Pb), total mercury (THg), and selenium (Se). Metals concentrations varied significantly, and some were biomagnified, with livers and kidneys harboring the highest concentrations. Lead and arsenic appeared to be readily excreted. This study represents baseline metals concentrations to assist in monitoring the health of sea otters.

Multiple facets of marine biodiversity in the Pacific Arctic under future climate.

Climate change is triggering a global reorganization of marine life. Biogeographical transition zones, diversity-rich regions straddling biogeographical units where many species live at, or close to, their physiological tolerance limits (i.e., range distribution edges), are redistribution hotspots that offer a unique opportunity to understand the mechanisms and consequences of climate-driven thermophilization processes in natural communities. In this context, we examined the impacts of climate change projections in the 21st century (2026-2100) on marine biodiversity in the Eastern Bering and Chukchi seas within the Pacific Arctic, a climatically exposed and sensitive boreal-to-Arctic transition zone. Overall, projected changes in species distributions, modeled using species distribution models, resulted in poleward increases in species richness and functional redundancy, along with pronounced reductions in phylogenetic distances by century's end (2076-2100). Future poleward shifts of boreal species in response to warming and sea ice changes are projected to alter the taxonomic and functional biogeography of contemporary Arctic communities as larger, longer-lived and more predatory taxa expand their leading distributional margins. Drawing from the existing evidence from other Arctic regions, these changes are anticipated to increase the susceptibility and vulnerability of the Arctic ecosystems, as trophic connectance between biological components increases, thus decreasing the modularity of Arctic food webs. Our results demonstrate how integrating multiple diversity facets can provide key insights into the relationships between climate change, species composition and ecosystem functioning across marine biogeographic regions.

Development of a predation index to assess trophic stability in the Gulf of Alaska.

Predation can have substantial and long-term effects on the population dynamics of ecologically important prey. Diverse predator assemblages, however, may produce stabilizing (i.e., portfolio) effects on prey mortality when consumption varies asynchronously among predators. We calculated spatiotemporal variation in predation on a dominant forage species to quantify synchrony and portfolio effects in a food web context and better understand diversity-stability relationships in a large marine ecosystem that has undergone considerable changes in community composition. We selected Walleye Pollock (Gadus chalcogrammus) as our case study because they support some of the largest, most valuable commercial fisheries in the world and serve as essential prey for an array of economically and culturally important species. Thus, there are sufficient data for Pollock with which to test ecological theories in an empirical setting. Spatially explicit predation indices accounted for annual variation in predator biomass, bioenergetics-based rations, and age-specific proportions of Pollock consumed by a suite of groundfishes in the Gulf of Alaska (1990-2015). We found that Arrowtooth Flounder (Atheresthes stomias) was, by far, the dominant Pollock predator (proportional consumption: 0.74 ± 0.14). We also found synchronous trends in consumption among predator species, indicating a lack of portfolio effects at the basin scale. This combination of a single dominant predator and synchronous consumption dynamics suggests strong top-down control over Pollock in the Gulf of Alaska, though the degree of synchrony was highly variable at all spatial scales. Whereas synchrony generally increased in the western subregion, consumption in the central Gulf of Alaska became less synchronous through time. This suggests diminished trophic stability in one area and increased stability in another, thereby emphasizing the importance of spatiotemporal heterogeneity in maintaining food web structure and function. Finally, total Pollock consumption was highly variable (ranging from 1.87 to 7.63 Tg) and often exceeded assessment-based estimates of productivity. We assert that using our holistic and empirically derived predation index as a modifier of assumed constant natural mortality would provide a practical method for incorporating ecological information into single-species stock assessments.

Evidence for dietary time series in layers of cetacean skin using stable carbon and nitrogen isotope ratios.

RATIONALE: Stable isotope analysis integrates diet information over a time period specific to the type of tissue sampled. For metabolically active skin of free-ranging cetaceans, cells are generated at the basal layer of the skin and migrate outward until they eventually slough off, suggesting potential for a dietary time series. METHODS: Skin samples from cetaceans were analyzed using continuous-flow elemental analyzer isotope ratio mass spectrometry. We used ANOVAs to compare the variability of δ13 C and δ15 N values within and among layers and columns ("cores") of the skin of a fin, humpback, and sperm whale. We then used mixed-effects models to analyze isotopic variability among layers of 28 sperm whale skin samples, over the course of a season and among years. RESULTS: We found layer to be a significant predictor of δ13 C values in the sperm whale's skin, and δ15 N values in the humpback whale's skin. There was no evidence for significant differences in δ15 N or δ13 C values among cores for any species. Mixed-effects models selected layer and day of the year as significant predictors of δ13 C and δ15 N values in sperm whale skin across individuals sampled during the summer months in the Gulf of Alaska. CONCLUSIONS: These results suggest that skin samples from cetaceans may be subsampled to reflect diet during a narrower time period; specifically different layers of skin may contain a dietary time series. This underscores the importance of selecting an appropriate portion of skin to analyze based on the species and objectives of the study.

Reassessing regime shifts in the North Pacific: incremental climate change and commercial fishing are necessary for explaining decadal-scale biological variability.

In areas of the North Pacific that are largely free of overfishing, climate regime shifts - abrupt changes in modes of low-frequency climate variability - are seen as the dominant drivers of decadal-scale ecological variability. We assessed the ability of leading modes of climate variability [Pacific Decadal Oscillation (PDO), North Pacific Gyre Oscillation (NPGO), Arctic Oscillation (AO), Pacific-North American Pattern (PNA), North Pacific Index (NPI), El Niño-Southern Oscillation (ENSO)] to explain decadal-scale (1965-2008) patterns of climatic and biological variability across two North Pacific ecosystems (Gulf of Alaska and Bering Sea). Our response variables were the first principle component (PC1) of four regional climate parameters [sea surface temperature (SST), sea level pressure (SLP), freshwater input, ice cover], and PCs 1-2 of 36 biological time series [production or abundance for populations of salmon (Oncorhynchus spp.), groundfish, herring (Clupea pallasii), shrimp, and jellyfish]. We found that the climate modes alone could not explain ecological variability in the study region. Both linear models (for climate PC1) and generalized additive models (for biology PC1-2) invoking only the climate modes produced residuals with significant temporal trends, indicating that the models failed to capture coherent patterns of ecological variability. However, when the residual climate trend and a time series of commercial fishery catches were used as additional candidate variables, resulting models of biology PC1-2 satisfied assumptions of independent residuals and out-performed models constructed from the climate modes alone in terms of predictive power. As measured by effect size and Akaike weights, the residual climate trend was the most important variable for explaining biology PC1 variability, and commercial catch the most important variable for biology PC2. Patterns of climate sensitivity and exploitation history for taxa strongly associated with biology PC1-2 suggest plausible mechanistic explanations for these modeling results. Our findings suggest that, even in the absence of overfishing and in areas strongly influenced by internal climate variability, climate regime shift effects can only be understood in the context of other ecosystem perturbations.

Rising catch variability preceded historical fisheries collapses in Alaska.

Statistical indicators such as rising variance and rising skewness in key system parameters may provide early warning of "regime shifts" in communities and populations. However, the utility of these indicators has rarely been tested in the large, complex ecosystems that are of most interest to managers. Crustacean fisheries in the Gulf of Alaska and Bering Sea experienced a series of collapses beginning in the 1970s, and we used spatially resolved catch data from these fisheries to test the predictions that increasing variability and skewness would precede stock collapse. Our data set consisted of catch data from 14 fisheries (12 collapsing and two non-collapsing), spanning 278 cumulative years. Our sampling unit for analysis was the Alaska Department of Fish and Game statistical reporting area (mean n for individual fisheries = 42 areas, range 7-81). We found that spatial variability in catches increased prior to stock collapse: a random-effects model estimating trend in variability across all 12 collapsing fisheries showed strong evidence of increasing variability prior to collapse. Individual trends in variability were statistically significant for only four of the 12 collapsing fisheries, suggesting that rising variability might be most effective as an indicator when information from multiple populations is available. Analyzing data across multiple fisheries allowed us to detect increasing variability 1-4 years prior to collapse, and trends in variability were significantly different for collapsing and non-collapsing fisheries. In spite of theoretical expectations, we found no evidence of pre-collapse increases in catch skewness. Further, while models generally predict that rising variability should be a transient phenomenon around collapse points, increased variability was a persistent feature of collapsed fisheries in our study. We conclude that this result is more consistent with fishing effects as the cause of increased catch variability, rather than the critical slowing down that is the driver of increased variability in regime shift models. While our results support the use of rising spatial variability as a leading indicator of regime shifts, the failure of our data to support other model-derived predictions underscores the need for empirical validation before these indicators can be used with confidence by ecosystem managers.

Spatial match-mismatch between juvenile fish and prey provides a mechanism for recruitment variability across contrasting climate conditions in the eastern Bering Sea.

Understanding mechanisms behind variability in early life survival of marine fishes through modeling efforts can improve predictive capabilities for recruitment success under changing climate conditions. Walleye pollock (Theragra chalcogramma) support the largest single-species commercial fishery in the United States and represent an ecologically important component of the Bering Sea ecosystem. Variability in walleye pollock growth and survival is structured in part by climate-driven bottom-up control of zooplankton composition. We used two modeling approaches, informed by observations, to understand the roles of prey quality, prey composition, and water temperature on juvenile walleye pollock growth: (1) a bioenergetics model that included local predator and prey energy densities, and (2) an individual-based model that included a mechanistic feeding component dependent on larval development and behavior, local prey densities and size, and physical oceanographic conditions. Prey composition in late-summer shifted from predominantly smaller copepod species in the warmer 2005 season to larger species in the cooler 2010 season, reflecting differences in zooplankton composition between years. In 2010, the main prey of juvenile walleye pollock were more abundant, had greater biomass, and higher mean energy density, resulting in better growth conditions. Moreover, spatial patterns in prey composition and water temperature lead to areas of enhanced growth, or growth 'hot spots', for juvenile walleye pollock and survival may be enhanced when fish overlap with these areas. This study provides evidence that a spatial mismatch between juvenile walleye pollock and growth 'hot spots' in 2005 contributed to poor recruitment while a higher degree of overlap in 2010 resulted in improved recruitment. Our results indicate that climate-driven changes in prey quality and composition can impact growth of juvenile walleye pollock, potentially severely affecting recruitment variability.

Sea ice retreat alters the biogeography of the Bering Sea continental shelf.

Seasonal ice cover creates a pool of cold bottom water on the eastern Bering Sea continental shelf each winter. The southern edge of this cold pool, which defines the ecotone between arctic and subarctic communities, has retreated approximately 230 km northward since the early 1980s. Bottom trawl surveys of fish and invertebrates in the southeastern Bering Sea (1982-2006) show a coincident reorganization in community composition by latitude. Survey catches show community-wide northward distribution shifts, and the area formerly covered by the cold pool has seen increases in total biomass, species richness, and average trophic level as subarctic fauna have colonized newly favorable habitats. Warming climate has immediate management implications, as 57% of variability in commercial snow crab (Chionoecetes opilio) catch is explained by winter sea ice extent. Several measures of community distribution and structure show linear relationships with bottom temperature, suggesting warming climate as the primary cause of changing biogeography. However, residual variability in distribution not explained by climate shows a strong temporal trend, suggesting that internal community dynamics also contribute to changing biogeography. Variability among taxa in their response to temperature was not explained by commercial status or life history traits, suggesting that species-specific responses to future warming will be difficult to predict.