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. Threequarters 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 cooccurred 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 PLOS ONE | https://doi.org/10.1371/journal.pone.0226087 January 15, 2020 1 / 32 OPEN ACCESS Citation: Piatt JF, Parrish JK, Renner HM, Schoen SK, Jones TT, Arimitsu ML, et al. (2020) Extreme mortality and reproductive failure of common murres resulting from the northeast Pacific marine heatwave of 2014-2016. PLoS ONE 15(1):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.

a b s t r a c tCentral place foragers, such as breeding seabirds, need to commute between their nests and foraging grounds, thus close proximity of the breeding colony to productive oceanographic features might be beneficial for seabird reproduction. We tested this hypothesis by investigating the at-sea foraging and breeding behavior of thick-billed murres (Uria lomvia) nesting at three colonies (Bogoslof, St. Paul, and St. George Islands) in the Bering Sea located at different distances from the productive continental shelf-break. We found that distances to feeding areas differed only during night trips among colonies. St. Paul murres foraged entirely on the shelf, whereas St. George murres commuted to the continental shelf-break at night and foraged on the shelf during the day. Bogoslof murres foraged in oceanic waters in close proximity to the colony. Murres breeding at the both Pribilof colonies spent less time attending nests and had higher levels of stress hormone corticosterone compared to murres breeding at Bogoslof, although chick-provisioning rates and fledging success were similar among the three colonies. Lower nest attendance and higher corticosterone suggest lower food availability in the Pribilof domain compared to the Bogoslof region. Murres breeding at the Pribilofs used different foraging strategies to buffer effects of food shortages on their reproduction: flight costs associated with longer distance night trips at St. George were presumably balanced by benefits of higher density and/or more lipid rich prey in the continental shelf-break regions, whereas the additional distance of St. Paul from the continental shelf-break may have outweighed any energetic gain. Murres exhibited a remarkable degree of plasticity of foraging strategies in response to changes in their food availability, but the breeding success of murres did not reflect either food limitations or the colony proximity to productive oceanographic features.

As central-place foragers, seabirds from colonies located close to multiple and/or productive marine habitats might experience increased foraging opportunities and enhanced resilience to food shortages. We tested whether this hypothesis might explain divergent trends in 3 populations of black-legged kittiwakes Rissa tridactyla, a surface-feeding piscivore, in the eastern Bering Sea. We simultaneously studied the foraging behavior, diet, nutritional stress, and breeding performance of chick-rearing kittiwakes from 2 continental shelf colonies (St. Paul and St. George) and an oceanic colony (Bogoslof). Although shelf-based forage fishes were rare or absent in bird diets during the cold study year, not all kittiwakes from the 3 colonies concentrated foraging along the productive shelf break habitats. Compared to the oceanic colony, birds from both shelf-located colonies had lower chick provisioning rates, higher levels of nutritional stress, and lower breeding performance. Although birds from both shelf-based colonies foraged in nearby neritic habitats during daytime, birds from St. George, a stable population located closest to the continental shelf break, also conducted long overnight trips to the ocean basin to feed on lipid-rich myctophids. In contrast, birds from St. Paul, a declining population located farthest from shelf break/oceanic habitats, fed exclusively over the shelf and obtained less high-energy food. Birds from Bogoslof, an increasing population, foraged mainly on myctophids close to the colony in the oceanic basin and Aleutian coast habitats. Our study suggests that proximity to multiple foraging habitats may explain divergent population trends among colonies of kittiwakes in the southeastern Bering Sea.

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Long‐term studies of predator food habits (i.e., ‘predator‐based sampling’) are useful for identifying patterns of spatial and temporal variability of forage nekton in marine ecosystems. We investigated temporal changes in forage fish availability and relationships to ocean climate by analyzing diet composition of three puffin species (horned puffin Fratercula corniculata, tufted puffin Fratercula cirrhata, and rhinoceros auklet Cerorhinca monocerata) from five sites in the North Pacific from 1978–2012. Dominant forage species included squids and hexagrammids in the western Aleutians, gadids and Pacific sand lance (Ammodytes personatus) in the eastern Aleutians and western Gulf of Alaska (GoA), and sand lance and capelin (Mallotus villosus) in the northern and eastern GoA. Interannual fluctuations in forage availability dominated variability in the western Aleutians, whereas lower‐frequency shifts in forage fish availability dominated elsewhere. We produced regional multivariate indicators of sand lance, capelin, and age‐0 gadid availability by combining data across species and sites using Principal Component Analysis, and related these indices to environmental factors including sea level pressure (SPL), winds, and sea surface temperature (SST). There was coherence in the availability of sand lance and capelin across the study area. Sand lance availability increased linearly with environmental conditions leading to warmer ocean temperatures, whereas capelin availability increased in a non‐linear manner when environmental changes led to lower ocean temperatures. Long‐term studies of puffin diet composition appear to be a promising tool for understanding the availability of these difficult‐to‐survey forage nekton in remote regions of the North Pacific.

We hypothesized that changes in southeastern Bering Sea foraging conditions for black-legged kittiwakes (Rissa tridactyla) have caused shifts in habitat use with direct implications for population trends. To test this, we compared at-sea distribution, breeding performance, and nutritional stress of kittiwakes in three years (2008–2010) at two sites in the Pribilof Islands, where the population has either declined (St. Paul) or remained stable (St. George). Foraging conditions were assessed from changes in (1) bird diets, (2) the biomass and distribution of juvenile pollock (Theragra chalcogramma) in 2008 and 2009, and (3) eddy kinetic energy (EKE; considered to be a proxy for oceanic prey availability). In years when biomass of juvenile pollock was low and patchily distributed in shelf regions, kittiwake diets included little or no neritic prey and a much higher occurrence of oceanic prey (e.g. myctophids). Birds from both islands foraged on the nearby shelves, or made substantially longer-distance trips overnight to the basin. Here, feeding was more nocturnal and crepuscular than on the shelf, and often occurred near anticyclonic, or inside cyclonic eddies. As expected from colony location, birds from St. Paul used neritic waters more frequently, whereas birds from St. George typically foraged in oceanic waters. Despite these distinctive foraging patterns, there were no significant differences between colonies in chick feeding rates or fledging success. High EKE in 2010 coincided with a 63% increase in use of the basin by birds from St. Paul compared with 2008 when EKE was low. Nonetheless, adult nutritional stress, which was relatively high across years at both colonies, peaked in birds from St. Paul in 2010. Diminishing food resources in nearby shelf habitats may have contributed to kittiwake population declines at St Paul, possibly driven by increased adult mortality or breeding desertion due to high foraging effort and nutritional stress.

The tufted puffin (Fratercula cirrhata) is a generalist seabird that breeds throughout the North Pacific and eats more than 75 different prey species. Using puffins as samplers, we characterized the geographic variability in pelagic food webs across the subarctic North Pacific from the composition of ~10,000 tufted puffin meals (~56,000 prey items) collected at 35 colonies in the Gulf of Alaska (GoA) and Aleutian Archipelago. Cluster analysis of diet species composition suggested three distinct forage fish communities: (i) in the northern GoA, multiple age‐classes of coastal and shelf residents such as capelin, sand lance and herring dominated the food web, (ii) in the western GoA to eastern Aleutians, the shelf community was dominated by transient age‐0 walleye pollock, and (iii) in the western Aleutians, shelf‐edge and mesopelagic forage species such as squid, lanternfish, and Atka mackerel were prevalent. Geographic patterns of abundance of capelin and sand lance in tufted puffin diets were corroborated by independent research fisheries and diets of piscivorous fish, indicating that puffin diets reflect the local abundance of forage species, not just selection of favored species. Generalized additive models showed that habitat characteristics predict, in a non‐linear fashion, forage species distribution and abundance across two large marine ecosystems. We conclude that major biogeographic patterns in forage fish distribution follow gradients in key habitat features, and puffin diets reflect those patterns.

Climate change and other human activities are causing profound effects on marine ecosystem productivity. We show that the breeding success of seabirds is tracking hemispheric differences in ocean warming and human impacts, with the strongest effects on fish-eating, surface-foraging species in the north. Hemispheric asymmetry suggests the need for ocean management at hemispheric scales. For the north, tactical, climate-based recovery plans for forage fish resources are needed to recover seabird breeding productivity. In the south, lower-magnitude change in seabird productivity presents opportunities for strategic management approaches such as large marine protected areas to sustain food webs and maintain predator productivity. Global monitoring of seabird productivity enables the detection of ecosystem change in remote regions and contributes to our understanding of marine climate impacts on ecosystems.