Sarah K. Schoen’s research while affiliated with United States Geological Survey and other places

The 2014–2016 Pacific marine heatwave caused unprecedented die-offs and multi-year reproductive failures for Common Murres Uria aalge along the west coast of North America. Lingering impacts, such as declines in colony attendance and productivity, have persisted at some colonies following the heatwave and are attributed largely to changes in prey availability and quality. Here, we present evidence of an additional, top-down mechanism contributing to Common Murre breeding failures on Gull Island (Alaska): disturbance of nesting birds by aerial predators and associated egg depredation. We collected time-lapse images over five murre breeding seasons (2016–2020) on Gull Island to document the frequency, duration, and intensity of disturbances caused by aerial predators, as well as to quantify disturbance-associated egg depredation. To identify seasonal and inter-annual variability of disturbances, we calculated a daily disturbance index and compared years using generalized additive models. In all years, Bald Eagles Haliaeetus leucocephalus were the primary cause of disturbance, which led to periods of prolonged colony abandonment by murres and facilitated high levels of murre egg depredation by Glaucous-winged Gulls Larus glaucescens and Herring Gulls L. argentatus. We found that the seasonality of disturbance was an important factor in determining egg depredation rates. In years when disturbance levels were high and persisted later in the season, the colony experienced complete breeding failures due to disturbance-associated egg depredation. Our study revealed that the response of nesting murres to a strong environmental perturbation, such as the Pacific marine heatwave, can be complex and involve multiple stressors from both bottom-up and top-down factors.

Introduction Seabirds are abundant, conspicuous members of marine ecosystems worldwide. Synthesis of distribution data compiled over time is required to address regional management issues and understand ecosystem change. Major challenges when estimating seabird densities at sea arise from variability in dispersion of the birds, sampling effort over time and space, and differences in bird detection rates associated with survey vessel type. Methods Using a novel approach for modeling seabirds at sea, we applied joint dynamic species distribution models (JDSDM) with a vector-autoregressive spatiotemporal framework to survey data collected over nearly five decades and archived in the North Pacific Pelagic Seabird Database. We produced monthly gridded density predictions and abundance estimates for 8 species groups (77% of all birds observed) within Cook Inlet, Alaska. JDSDMs included habitat covariates to inform density predictions in unsampled areas and accounted for changes in observed densities due to differing survey methods and decadal-scale variation in ocean conditions. Results The best fit model provided a high level of explanatory power (86% of deviance explained). Abundance estimates were reasonably precise, and consistent with limited historical studies. Modeled densities identified seasonal variability in abundance with peak numbers of all species groups in July or August. Seabirds were largely absent from the study region in either fall (e.g., murrelets) or spring (e.g., puffins) months, or both periods (shearwaters). Discussion Our results indicated that pelagic shearwaters (Ardenna spp.) and tufted puffin (Fratercula cirrhata) have declined over the past four decades and these taxa warrant further investigation into underlying mechanisms explaining these trends. JDSDMs provide a useful tool to estimate seabird distribution and seasonal trends that will facilitate risk assessments and planning in areas affected by human activities such as oil and gas development, shipping, and offshore wind and renewable energy.

A protracted period (2014-2016) of anomalously warm water in the northeast Pacific Ocean precipitated an extensive die-off of common murres Uria aalge (hereafter ‘murres’) during 2015-2016, accompanied by reduced colony attendance and reproductive success of murres and black-legged kittiwakes Rissa tridactyla (‘kittiwakes’) starting in 2015. Most murres died of starvation following a large-scale reduction in abundance and quality of forage fish. To assess murre and kittiwake recovery following the marine heatwave, we monitored their demographics at 2 colonies (Chisik and Gull Islands) in Cook Inlet, Alaska (USA), from 2016 to 2019. Compared to historic data (1995-1999), we observed declines and increased variability in colony attendance and productivity across species and colonies, and predation was widespread. At Chisik, where food limitations were common during historic studies, both species experienced substantial population declines and reproductive failures in all 4 years (2016-2019) following the heatwave. At Gull, a typically productive colony during historic studies, murres failed to fledge chicks for 3 years (2016-2018) following the heatwave. By 2019, murre productivity recovered to about half that observed during historic studies (0.28 vs. 0.54 chicks per pair), but populations had declined by half. Kittiwake population size at Gull declined a quarter from historic counts, and reproduction alternated between complete breeding failures (2016/2018) and high productivity (2017/2019). These multi-year demographic impacts indicate lingering effects of the heatwave on kittiwakes and murres through forage fish depletion and increased predator disturbance, and possibly other stressors. It remains unknown whether populations can rebound to historic levels. If so, recovery would likely take decades.

Harmful algal blooms produce biotoxins that can injure or kill fish, wildlife, and humans. These blooms occur naturally but have intensified in many locations globally due to recent climatic changes, including ocean warming. Such changes are especially pronounced in northern regions, where the effects of paralytic shellfish toxins (PSTs) on marine wildlife are of growing concern. In Alaska, seabird mortality events have increased in frequency, magnitude, and duration since 2015 alongside anomalously high ocean temperatures. Although starvation has been implicated as the apparent cause of death in many of these die-offs, saxitoxin (STX) and other PSTs have been identified as possible contributing factors. Here, we describe a mortality event at a nesting colony of Arctic Terns (Sterna paradisaea) near Juneau, Alaska in 2019 and report elevated concentrations of PSTs in bird, forage fish, and mussel samples. Concentrations of STX and other PSTs in tern tissues (2.5–51.2 µg 100g⁻¹ STX-equivalents [STX-eq]) were of similar magnitude to those reported from other PST-induced bird die-offs. We documented high PST concentrations in blue mussels (>11,000 µg 100g⁻¹ STX-eq; Mytilus edulis spp.) collected from nearby beaches, as well as in forage fish (up to 494 µg 100g⁻¹ STX-eq) retrieved from Arctic Tern nests, thereby providing direct evidence of PST exposure via the terns’ prey. At maximum concentrations measured in this study, a single 5 g Pacific Sand Lance (Ammodytes personatus) could exceed the median lethal STX dose (LD50) currently estimated for birds, offering strong support for PSTs as a likely source of tern mortality. In addition to describing this localized bird mortality event, we used existing energetics data from adult and nestling Arctic Terns to calculate estimated cumulative daily PST exposure based on ecologically relevant concentrations in forage fish. Our estimates revealed potentially lethal levels of PST exposure even at relatively low (≤30 ug 100g⁻¹ STX-eq) toxin concentrations in prey. These findings suggest that PSTs present a significant hazard to Arctic Terns and other northern seabirds and should be included in future investigations of avian mortality events as well as assessments of population health.

Kittlitz’s Murrelets (Brachyramphus brevirostris) nest during summer in glaciated or recently deglaciated (post-Wisconsin) landscapes. They forage in adjacent marine waters, especially those influenced by glacial meltwater. Little is known of their movements and distribution outside the breeding season. To identify post-breeding migrations of murrelets, we attached satellite transmitters to birds (n = 47) captured at sea in the Gulf of Alaska and Aleutian Islands during May – July 2009 – 15 and tracked 27 birds that migrated from capture areas. Post-breeding murrelets migrated toward the Bering Sea, with short periods of movement (median 2 d) separated by short stopovers (median 1 d). Travel speeds averaged 79.4 km d-1 (83.5 SD, 449.1 maximum). Five Kittlitz’s Murrelets tagged in Prince William Sound in May migrated to the Bering Sea by August and four continued north to the Arctic Ocean, logging 2500 – 4000 km of travel. Many birds spent 2‒3 weeks with little movement along coasts of the Alaska Peninsula or eastern Bering Sea during late August through September, also the pre-basic molt period. Ship-based surveys, many of which were conducted concurrently with our telemetry studies, confirmed that substantial numbers of Kittlitz’s Murrelets migrate into the Arctic Ocean during autumn. They also revealed that some birds spend winter and spring in the Bering Sea in association with ice-edge, polynya, or marginal ice zone habitats before returning to summer breeding grounds. We conclude that this species is best characterized as a sub-Arctic and Arctic species, which has implications for future risk assessments and threat mitigation.

During the Pacific marine heatwave of 2014-2016, abundance and quality of several key forage fish species in the Gulf of Alaska were simultaneously reduced throughout the system. Capelin (Mallotus catervarius), sand lance (Ammodytes personatus), and herring (Clupea pallasii) populations were at historically low levels, and within this community abrupt declines in portfolio effects identify trophic instability at the onset of the heatwave. Although compensatory changes in age-structure, size, growth or energy content of forage fish were observed to varying degrees among all these forage fish, none were able to fully mitigate adverse impacts of the heatwave, which likely included both top-down and bottom-up forcing. Notably, changes to the demographic structure of forage fish suggested size-selective removals typical of top-down regulation. At the same time, zooplankton community structure may have driven bottom-up regulation as copepod community structure shifted towards smaller, warm-water species, and euphausiid biomass was reduced owing to the loss of cold-water species. Mediated by these impacts on the forage fish community, an unprecedented disruption of the normal pelagic food web was signaled by higher trophic level disruptions during 2015-2016, when seabirds, marine mammals, and groundfish experienced shifts in distribution, mass mortalities, and reproductive failures. Unlike decadal-scale variability underlying ecosystem regime shifts, the heatwave appeared to temporarily overwhelm the ability of the forage fish community to buffer against changes imposed by warm water anomalies, thereby eliminating any ecological advantages that may have accrued from having a suite of coexisting forage species with differing life history compensations.

About 62,000 dead or dying common murres (Uria aalge), the trophically dominant fish-eating seabird of the North Pacific, washed ashore between summer 2015 and spring 2016 on beaches from California to Alaska. Most birds were severely emaciated and, so far, no evidence for anything other than starvation was found to explain this mass mortality. Three-quarters of murres were found in the Gulf of Alaska and the remainder along the West Coast. Studies show that only a fraction of birds that die at sea typically wash ashore, and we estimate that total mortality approached 1 million birds. About two-thirds of murres killed were adults, a substantial blow to breeding populations. Additionally, 22 complete reproductive failures were observed at multiple colonies region-wide during (2015) and after (2016–2017) the mass mortality event. Die-offs and breeding failures occur sporadically in murres, but the magnitude, duration and spatial extent of this die-off, associated with multi-colony and multi-year reproductive failures, is unprecedented and astonishing. These events co-occurred with the most powerful marine heatwave on record that persisted through 2014–2016 and created an enormous volume of ocean water (the “Blob”) from California to Alaska with temperatures that exceeded average by 2–3 standard deviations. Other studies indicate that this prolonged heatwave reduced phytoplankton biomass and restructured zooplankton communities in favor of lower-calorie species, while it simultaneously increased metabolically driven food demands of ectothermic forage fish. In response, forage fish quality and quantity diminished. Similarly, large ectothermic groundfish were thought to have increased their demand for forage fish, resulting in greater top-predator demands for diminished forage fish resources. We hypothesize that these bottom-up and top-down forces created an “ectothermic vise” on forage species leading to their system-wide scarcity and resulting in mass mortality of murres and many other fish, bird and mammal species in the region during 2014–2017.

Elevated seawater temperatures are linked to the development of harmful algal blooms (HABs), which pose a growing threat to marine birds and other wildlife. During late 2015 and early 2016, a massive die-off of Common Murres (Uria aalge; hereafter, murres) was observed in the Gulf of Alaska coincident with a strong marine heat wave. Previous studies have documented illness and death among seabirds resulting from exposure to the HAB neurotoxins saxitoxin (STX) and domoic acid (DA). Given the unusual mortality event, corresponding warm water anomalies, and recent detection of STX and DA throughout coastal Alaskan waters, HABs were identified as a possible factor of concern. To evaluate whether algal toxins may have contributed to murre deaths, we tested for STX and DA in a suite of tissues obtained from beach-cast murre carcasses associated with the die-off as well as from apparently healthy murres and Black-legged Kittiwakes (Rissa tridactyla; hereafter, kittiwakes) sampled in the preceding and following summers. We also tested forage fish and marine invertebrates collected in the Gulf of Alaska in 2015-2017 to evaluate potential sources of HAB toxin exposure for seabirds. Saxitoxin was present in multiple tissue types of both die-off (36.4 %) and healthy (41.7 %) murres and healthy kittiwakes (54.2 %). Among birds, we detected the highest concentrations of STX in liver tissues (range 1.4-10.8 μg 100 g −1) of die-off murres. Saxitoxin was relatively common in forage fish (20.3 %) and invertebrates (53.8 %). No established toxicity limits currently exist for seabirds, but concentrations of STX in birds and forage fish in our study were lower than values reported from most other bird die-offs in which STX intoxication was causally linked. We detected low concentrations of DA in a single bird sample and in 33.3 % of invertebrates and 4.0 % of forage fish samples. Although these results do not support the hypothesis that acute exposure to STX or DA was a primary factor in the 2015-2016 mortality event, additional information about the sensitivity of murres to these toxins is needed before we can discount their potential role in the die-off. The widespread occurrence of STX in seabirds, forage fish, and invertebrates in the Gulf of Alaska indicates that algal toxins should be considered in future assessments of seabird health, especially given the potential for greater occurrence of HABs in the future.

Pacific sand lance Ammodytes personatus are a key forage fish in the North Pacific for many species of salmon, groundfish, seabirds, and marine mammals and have historically been important to predators in relatively warm years. However, extreme declines in the nutritional value of sand lance in Prince William Sound, Alaska, USA, during 2012-2016 indicate that energy transfer from lower trophic levels to predators via sand lance may have been disrupted during the North Pacific marine heatwave in 2015 and 2016. Nutritional value (length, energy density, and whole-body energy) was measured in age-0 and age-1 sand lance collected during July in cool (2012-2013) and increasingly warm (2014-2016) years. The value of age-0 fish was relatively stable, with only minor differences among years for length and whole-body energy. By contrast, the value of age-1 fish significantly declined in 2015, and by 2016 they were 38% shorter and 13% lower in energy density compared to cooler years. This contributed to significant declines in whole-body energy of 44% in 2015 and 89% in 2016 compared to cooler years (2012-2014). The 2015 sand lance cohort experienced little growth or lipid accumulation from July 2015 at age-0 to July 2016 at age-1. This effective disruption of energy flow through pelagic food webs probably contributed to population declines and/or breeding failures observed among several predators in the Gulf of Alaska and suggests that tipping points were reached during the heatwave.

How well seabirds compensate for variability in prey abundance and composition near their breeding colonies influences their distribution and reproductive success. We used tufted puffins (Fratercula cirrhata) as forage fish samplers to study marine food webs from the western Aleutian Islands (53°N, 173°E) to Kodiak Island (57°N, 153°W), Alaska, during August 2012–2014. Around each colony we obtained data on: environmental characteristics (sea surface temperature and salinity, seafloor depth and slope, tidal range, and chlorophyll-a), relative forage fish biomass (hydroacoustic backscatter), and seabird community composition and density at-sea. On colonies, we collected puffin chick-meals to characterize forage communities and determine meal energy density, and measured chicks to obtain a body condition index. There were distinct environmental gradients from west to east, and environmental variables differed by ecoregions: the (1) Western-Central Aleutians, (2) Eastern Aleutians, and, (3) Alaska Peninsula. Forage fish biomass, species richness, and community composition all differed markedly between ecoregions. Forage biomass was strongly correlated with environmental gradients, and environmental gradients and forage biomass accounted for ~ 50% of the variability in at-sea density of tufted puffins and all seabird taxa combined. Despite the local and regional variability in marine environments and forage, the mean biomass of prey delivered to puffin chicks did not differ significantly between ecoregions, nor did chick condition or puffin density at-sea. We conclude that puffins can adjust their foraging behavior to produce healthy chicks across a wide range of environmental conditions. This extraordinary flexibility enables their overall success and wide distribution across the North Pacific Ocean. © 2018, This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign