Taken together, the total impact of the heatwave on common murre populations throughout all areas was likely between 0.53 and 1.2 million birds, or approximately 10–20% of total populations (~6 million). The fact that most birds killed in the die-off were probably breeding adults compounds the seriousness of the mortality for the population [ 60 ], and it will take longer for recovery of the population than if the die-off had affected mostly juveniles [ 60 , 61 ].

On the West Coast, we don’t have a comparable model to estimate total mortality. However, we know that beach survey coverage was more comprehensive on the West Coast, and so we used the conservative range of expansion factors from experimental studies (above, [ 57 ]) to estimate that 4x to 14x more birds than the ~14,500 murres counted were killed, i.e., between 58,000 and 203,000 birds. This would comprise about 4 to 14% of the CCS population (~1.5 million, estimated as above).

In this study, owing to logistic constraints and geographic expanse, we measured few or none of the factors needed to model total mortality in the areas most affected. However, we can draw upon a comparable study of carcass counts [ 45 ] conducted after the 1989 Exxon Valdez oil spill (EVOS) in which rates of carcass sinking, deposition, persistence, and search effort, were all measured in the core area of the oil spill zone [ 43 ], which also happens to overlap considerably with the area of highest murre mortality during the 2015–2016 heatwave. If we apply expansion factors determined from that study to bracket the lower (10x) and upper (22x) estimated limits of total mortality in the heatwave, we estimate that between 470,000 to 1,030,000 birds died in the Gulf of Alaska during the heatwave. This total probably included birds overwintering from Bering Sea colonies (see below), and it suggests that as much as one quarter of all murres breeding in the Gulf of Alaska and southeast Bering Sea (~4.5 million, U.S. Fish and Wildlife Service colony estimates and correction factor for birds at sea [ 46 ]) might have been killed.

Counts of dead seabirds on beaches following mass mortality incidents represent a minimum measure of total mortality. They do not include carcasses that sink at sea, or those washed ashore that are removed by scavengers or buried in sand and debris. Furthermore, the frequency and thoroughness of beach surveys ultimately determines how many carcasses will be discovered and counted [ 14 , 44 , 56 ]. Experimental studies (n = 19) conducted by releasing marked alcids (and/or decoys) at sea when systematic beach surveys were underway indicate that under a wide range of conditions at least 6.9x (95% CI 4.3x to 14.2x) more birds die at sea than are found on nearby beaches [ 57 ]. Recovery rates ranged between 0% and 61%, and much depends on the specifics of every experiment (e.g. wind direction, extent of search effort, etc.). Actual mass mortality events exhibit a range of expansion factors of similar magnitude (e.g., Tasman Sea 5x-10x [ 54 ]; Gulf of Biscay 5x-17x [ 57 ]; Gulf of Alaska in 1989 10x-22x [ 44 , 45 ]) or larger magnitudes (e.g., Gulf of Alaska in 1993 34x [ 20 ]; Gulf of Mexico 80x-950x [ 58 ]; Bering Sea 579x [ 59 ]). The largest multipliers were attached to studies of prolonged mortality (e.g. DeepWater Horizon oil spill, [ 58 ]) or those estimated by extrapolating from transects at sea (e.g. [ 59 ]).

A few exceptionally large die-offs have also occurred elsewhere in the world. During winter of 2013–2014, a total of 54,982 seabirds, mostly (54%) Atlantic puffins (Fratercula arctica) and common murres (29%), came ashore from Portugal north to the Shetland Islands, but mostly (80%) along the French coast [ 48 ]. This number “is likely to be a large underestimate of the final death toll.” Most mortality was attributed to starvation, perhaps precipitated by a powerful storm and difficulties foraging. There was no heatwave happening at the same time, but the die-off followed a nearly 30-year increase in SST in the North Atlantic from the 1980s through 2000s. This long-term increase in ocean temperature was implicated in the decline of several seabird populations during this period, as well as a reduction in abundance and quality of some forage fish species [ 39 , 49 – 52 ]. Elsewhere, following a major heatwave in the Tasman Sea [ 53 ] and after a severe winter storm off New Zealand in 2011, more than 53,840 dead prions (80% broad-billed prions Pachypatila vittata) were counted on long-term survey beaches during July and August [ 54 , 55 ]. Carcasses were found over the entire west coast of New Zealand and densities exceeded 1000 birds/km on several beaches. Total mortality was estimated conservatively at 250,000–500,000 individuals.

Few birds were recovered on beaches in British Columbia or southern southeast Alaska ( Fig 2 ), but this is a notable gap area in the distribution of murres during both summer and winter [ 46 ] ( S3 Fig ). In addition to a scarcity of murres, this area is sparsely populated and there was little search effort there ( Fig 2 ). Along the U.S. West Coast, murres are widely abundant ( S3 Fig ) and one of the more common species recorded on beach surveys, especially juvenile murres after they depart colonies in late summer [ 22 , 25 , 47 ]. However, there are few historical reports of natural die-offs involving more than hundreds or low thousands of birds, or of adults in particular. The recovery of ~8100 carcasses above the baseline is unprecedented for a “natural” die-off on the West Coast but has been surpassed in magnitude by the mortality of tens of thousands of murres in oil spills [ 46 ].

To put numbers into perspective with other mass mortalities in Alaska, biologists counted 22,800 emaciated (average 704 g) murre carcasses along an ~700 km stretch of coast on the southeast Bering Sea following a severe storm during April 1970 [ 42 ]. Aerial surveys averaged 80 carcasses/km (maximum 5440 carcasses/km) and total mortality was estimated conservatively to exceed 100,000 birds. Following the Exxon Valdez oil spill in March 1989, ~30,000 seabirds (74% murres) were recovered along a ~750 km stretch of coast in the northern GOA [ 43 ]. Based on a variety of in situ experiments to determine how many carcasses made it on shore and were likely to be counted (see below), models predicted that 300,000 to 645,000 birds actually died at sea [ 44 , 45 ]. In March 1993, about 3500 dead murres were recorded on beaches in the northern GOA; all were severely emaciated ( Fig 4 ). Deposition and persistence rates of murres on beaches were calculated from repetitive surveys [ 26 ] which indicated that a total of 10,900 murres were deposited cumulatively on the beaches surveyed. Assuming very conservatively that 90% of birds at sea came ashore, and that 10% of beaches in the die-off region had been surveyed, it was estimated that ~120,000 murres died in this wreck [ 20 ].

The 2015–2016 common murre die-off in the northeast Pacific is unprecedented globally in magnitude, spatial extent and duration. It occurred during a heatwave that was also severe (Category III) in magnitude, spatial extent and duration (711 days, [ 10 ]). The relative impact was greatest in Alaska, where ~47,000 carcasses reflected encounter rates that were up to a thousand times higher than usual. Peak encounter rates topped 4,600 carcasses/km in Prince William Sound. Many (~14,500) birds were also found on West Coast beaches, but part of this total resulted from much larger beach survey and rehabilitation efforts ( S1 and S2 Figs). About one-third of all birds counted on West Coast beach surveys (~11,800) can be accounted for by average background mortality in the region, and about three-quarters of the above-average (~5-10X) mortality was concentrated in the southern California Current System (CCS) ( Fig 3 ). Although strong heatwave anomalies occurred throughout the ~6000 km spatial range over which murres died, highest mortality rates occurred along an ~1,000 km arc of coastline in the northern Gulf of Alaska (GOA) and an ~500 km stretch of coastline in the southcentral and southern CCS, areas that overlapped spatially with the strongest SST anomalies and most rapid rates of warming ( Fig 1 ).

The frequency of total reproductive failures (n = 22), overall reduced breeding success and decline in numbers that occurred at multiple colonies in the northeast Pacific during 2015–2017 is a cause for astonishment and alarm. The common murre is probably the most widely studied seabird in the Northern Hemisphere and total reproductive failures at well-established colonies have been rare during some 70+ years of detailed observations ( Fig 5 )[ 17 , 39 , 40 , 46 , 63 ]. A smaller-scaled but similar die-off of murres in association with a collapse of forage stocks (capelin, sand lance, juvenile Atlantic cod Gadus morhua) occurred in the Barents Sea in 1986 [ 61 ]. Large common murre populations at many colonies in that region subsequently declined by 60–95% in a single winter [ 64 ]. Recovery of forage stocks and murre population growth started in the next year. However, two decades passed before murre populations recovered to pre-crash levels [ 61 ]. It remains to be seen when (or whether) murre populations in Alaska will recover from the heatwave in light of predicted global warming trends and the associated likelihood of more frequent heatwaves [ 5 ].

The extreme reproductive failures of common murres that occurred during summer 2015 and in the two years after the main die-off were also focused in Alaska and occurred less frequently in the California Current System (CCS). Considering the low number of birds encountered on beaches in the Bering Sea, breeding failures at colonies there were surprisingly similar in magnitude to those in the Gulf of Alaska (GOA). This reduction in juvenile production will significantly delay recovery of populations in all affected colonies [ 60 ]. Also, the number of birds attending colonies in the Bering Sea (data from USFWS [ 40 ] and USGS averaged in 3-year windows before and after the 2015–2016 die-off, weighted by colony size) declined more in the Bering Sea (>80%) than in the GOA (>50%). Whether these declines were due to reduced attendance because of deferred breeding [ 62 ], or a crash in colony populations due to a crash in food supply [ 61 ] is still not clear. Either way, reproductive failures and reduced attendance in the Bering Sea suggest that prey deficits were also experienced by murres in the southeastern corner of the Bering Sea.

Causal factors

Several acute biological responses to this unprecedented heatwave were observed throughout the northeast Pacific. Phytoplankton biomass in the northeast Pacific transition zone waters was lower in winter 2014 than in any year measured since 1997 [11]. The largest and most wide-spread harmful algal bloom in recorded history—a bloom of Pseudonitzschia—extended from California to the Gulf of Alaska (GOA) in 2015 [12,13]. Fundamental shifts in coastal productivity indices [11] and micronekton assemblages [65] were also associated with this sustained warming event. Large predatory groundfish in Alaska, including trophically and commercially dominant species such as walleye pollock (Gadus chalcogrammus), Pacific cod (Gadus macrocephalus), arrowtooth flounder (Atheresthes stomias) and Pacific halibut (Hippoglossus stenolepis) all declined in body condition and some in abundance (e.g., cod, see below) during heatwave and post-heatwave years of 2015–2017 in the GOA and Bering Sea [66–69]. A large die-off of planktivorous Cassin’s auklets (Ptychoramphus aleuticus) occurred from central California to British Columbia (BC) in the winter of 2014–2015 [14] followed by a large die-off of rhinoceros auklets (Cerorhinca monocerata) in the same region during 2016 [70]. Hundreds-to-thousands of young-of-the-year California sea lions (Zalophus californianus) died in 2014 and 2015, and Guadalupe fur seals (Arctocephalus townsendi) died in large numbers and experienced reproductive failures during 2015 [15,71,72]. A record total of 79 humpback and fin whales stranded during 2015–2016 in Alaska and British Columbia waters, mostly for “unexplained” reasons, and mostly in the GOA [16]. This was accompanied by a >50% decline in summer populations of humpback whales, evidence of malnutrition (“skinny whales”), and near complete absence of calves in Glacier Bay between 2014–2017 [73].

A common thread to most of these events was that they involved either a loss in productivity or a mass mortality of higher trophic-level animals, both of which point to problems in food production or availability. All the vertebrate predators affected also share a common dietary dependence on a few key forage species (see below) and this points to a bottleneck in the forage base. These events all occurred within, and for some years after, the time-frame of the 2014–2016 heatwave, and over an enormous spatial range involving three large marine ecosystems (CCS, GOA and Bering Sea). This calls for an explanation that is plausible for all species and regions, and that involves water temperature as a driving force—either directly or indirectly. With respect to murres, we offer three non-exclusive hypotheses to explain the cause of these events: 1) temperature-mediated changes in the distribution and quality of the prey base available to murres; 2) harmful algal blooms associated with warm water anomalies; and, 3) temperature-enhanced competition from ectothermic predators.

Bottom-up effects: Murres as marine predators. Reduction in primary production, and ultimately zooplankton or forage fish biomass, has been implicated in past seabird die-offs and reproductive failures (e.g., [14,27,46,61,74–78], often in association with anomalous oceanographic conditions (too warm, too cold, loss of upwelling, etc.). In order to understand how murres are affected by climate-mediated bottom-up changes in their forage base, we need to first consider their foraging ecology and the types of prey they eat. Throughout their Pacific range, common murres feed on a wide variety of prey, but around any particular colony they select among just a few species that may be found nearby such as sand lance (Ammodytes personatus), capelin (Mallotus catervarius) and other smelt, Pacific herring (Clupea pallasii), Pacific sardine (Sardinops sagax), northern anchovy (Engraulis mordax) and euphausiids (e.g., large Thysanoessa species), as well as juvenile age classes of salmon, gadids, hexagrammids, rockfish and squid [79–83]. (Note, we lump euphausiids and squid with “forage fish” here because a few invertebrates are also consumed in abundance by “piscivorous” groundfish, seabirds and marine mammals, especially in winter). Common murres are extremely well adapted for foraging on continental shelves; they fly faster than any other northern seabird [84], are capable of traversing any shelf in the CCS or GOA within hours, and, they are deep divers, making the entire shelf habitat accessible [85]. This is probably why breeding failures and die-offs have been historically rare (see above). On the other hand, as endotherms living in hostile, cold environments, murres maintain high metabolic rates (2.14 kJ/g/d [86]) and assuming an average body mass of 1054 g in the GOA (Fig 4) and a base energy value for “high quality” prey (5.0 kJ/g wet, [87]), murres need to eat 56% of their body mass every day to meet daily metabolic demands. Murres in Alaska generally eat age-0 or age-1 forage fish that weigh approximately 5–10 g ([88–90], J.F. Piatt and M. Arimitsu, unpubl. data), so to maintain body mass, murres would have to catch and eat about 60–120 high-lipid forage fish every day. If only smaller or leaner prey (e.g., juvenile pollock) were available, then the number needed could double [87,91]. By comparison, an ectothermic cod of similar size to a murre would only need to eat about 0.4–1.5% of its own body mass (BM) in food per day [92], i.e., as little as 1–3 high-quality forage fish a day. This is the ultimate “Achilles heel” for murres, and one that sets it far apart from competing ectothermic groundfish (eating typically 0.1–1% of BM/d) and endothermic marine mammals [93] including large cetaceans (1–2% BM/d) or small cetaceans and pinnipeds (5–15% BM/d). If murres can’t fully meet this food demand every day, they lose body condition quickly and jeopardize survival. If they can’t find any food for 3–5 days, they will die of starvation [36]. The fact that common murres are the most successful and abundant piscivorous seabirds breeding in the Northern Hemisphere speaks to their remarkable ability to meet this demand day-after-day. However, shifts in taxonomic composition of prey fields in response to changing environmental conditions have been shown to dramatically reduce murre foraging success, reproductive success and survival occasionally [61,83,94], demonstrating that even these superlative marine predators have limits [38,95]. Still, examples of such limitations in murres are rare and the magnitude of the events reported on here are beyond extraordinary.

Bottom-up effects: Shifts in the prey base. Warming of subarctic shelf waters may lead to both vertical (deepening) [96,97] and northward migrations of these forage species, or entire communities, according to thermal gradients and tolerances [98–100], a phenomena widely observed during the 2014–2016 heatwave [14,101–103]. In the California Current System (CCS), shifts in zooplankton [101] and forage fish diversity [65,103] signaled a persistent northward expansion of southern species. Zooplankton shifts may have also resulted in a depleted food chain in terms of relative energy transfer [101], although larval forage fish species were actually more abundant in samples off central California and central Oregon [65,103]. In contrast, anchovies and sardines in the CCS both declined by 2–3 orders of magnitude from the mid-2000s to 2014 [104,105]. Although these declines preceded the heatwave, fish and plankton net sampling in Oregon and Washington indicate that catches of these forage fish, as well as of euphausiids were further depressed in 2015 and 2016 [9,12,70,71]. In the Gulf of Alaska (GOA), a similar introgression of smaller zooplankton was observed, along with a breakdown in established SST-phytoplankton-zooplankton dynamics after 2013 [102]. Shifts to earlier peak biomass of smaller copepods associated with warmer temperatures [102] were cited as potential factors in concomitant declines in forage fish quality in Prince William Sound in the winter of 2015–2016 [106,107]. Shifts in forage fish availability in the GOA were apparent in marine bird diet starting in 2014 [108], with a sharp decline in capelin and an increase in sablefish (Anoplopoma fimbria), combined with a slow rebound of sand lance. In GOA waters, sand lance began a long steady decline in the early 2000s, to a low in 2011, and remained low to 2015 [67,109]. Capelin stocks were depressed after the 1976 regime shift [110], rebounded dramatically in 2007 as the GOA entered a new cold phase [67,109], and collapsed again during the heatwave in 2014–2016 [67,100]. In 2015 and 2016, age-0 pollock larvae in the GOA were 2–3 orders of magnitude less abundant than average; indicating complete recruitment failures for pollock [67,68]. In sum, latitudinal shifts in zooplankton and forage fish prey, combined with overall depression of major prey taxa, apparently created marginal foraging conditions for murres for several years. In addition to shifts in latitudinal abundance of specific taxa, warm water conditions diminished body condition and somatic growth of ectothermic forage fish. Body condition of capelin and sand lance in the GOA and CCS was reduced during the heatwave, resulting in smaller, less energy-dense prey for murres [107,111–113]. Whole-body energy content of age-1 sand lance declined by 44% in 2015 and 89% in 2016 in Alaska [114], and body condition of sand lance in the northern CCS declined markedly in 2014–2015 [113]. Presumably, consumed food was re-directed to fuel metabolism rather than somatic growth or fat storage [69,115]. Similarly, others [116] have shown marked reduction in growth of several CCS forage species during warming events, including the 2015–2016 heatwave. These included northern anchovy, Pacific herring, Pacific sardine, surf smelt (Hypomesus pretiosus), and whitebait smelt (Allosmerus elongatus), all common prey for murres in the CCS. They also demonstrated a marked change in forage fish diets in 2015–2016, from energy-rich plankton species to energy-poor gelatinous species; a change they ascribe to a restructuring of nektonic communities that occurred in response to the heatwave [116]. Thus, the heatwave increased metabolic demand of forage fish while at the same time it reduced the quality of some prey eaten by forage fish, creating a bottleneck for mass/energy flow to higher trophic levels, including seabirds (Fig 6). As all fish and invertebrates are ectothermic, this effect could potentially have far-reaching impacts on food webs in the GOA and CCS [69,117]. PPT PowerPoint slide

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larger image TIFF original image Download: Fig 6. Illustration of the “ectothermic vise” hypothesis to explain the dramatic decline of forage fish and starvation of murres across three large marine ecosystems during the 2014–2016 marine heatwave. We propose that an unusually warm layer of water in the NE Pacific, persisting for more than 2 years, had a powerful cumulative effect on ectothermic groundfish (stimulating food intake rate) and ectothermic forage fish (reducing their quality) leading to a strong top-down and bottom up (vise-like) impact on murre survival and reproductive success. https://doi.org/10.1371/journal.pone.0226087.g006

Bottom-up effects: Toxigenic algae. Increased ocean temperatures during and following the heatwave have been associated with harmful algal blooms (HABs) [13,118], which are known to cause marine bird mortality, primarily through plankton-derived toxicants entering the food chain and occasionally resulting in die-offs of thousands of birds [119]. Saxitoxin and domoic acid have been widely detected in top marine predators [31,120] but we know little about toxicity levels or effects of chronic exposure in most cases. During the common murre mass mortality event, an extensive HAB of a toxigenic diatom (Pseudo nitzschia sp.) that commonly produces domoic acid was documented in coastal California from March through June 2015 [13] resulting in bioaccumulation of domoic acid in northern anchovies (Engraulis mordax), one of the main prey species of common murres [121]. Investigators [120] detected low levels of domoic acid in tissues of beach cast common murres during and after the 2015 bloom (July—November). Nonetheless, they concluded that starvation “was likely the ultimate cause of death” and that any harmful algal bloom effects were secondary. In Alaska, it remains unclear whether HABs played any role in the elevated mortality rates of common murres during the 2015–2016 heatwave. Immediate testing for domoic acid in murres was minimal (n = 9 birds) and none was detected, but Pseudo nitzschia were 2-3X more abundant than average on the GOA shelf during 2014 and 2015 (S. Batten, pers. comm.). Saxitoxin, which can cause paralytic shellfish poisoning, has been linked to mortality of seabirds in Alaska [122] and concentrations of saxitoxin in some areas peaked during the summers of 2014–2016 [118]. Trace levels of saxitoxin (1.4–3.9 ppb) were detected in eight of 39 murre samples (stomach or cloacal content) obtained by the National Wildlife Health Center and tested immediately in 2015–2016 (see Methods). Later analyses of an additional 56 murres at the USGS Alaska Science Center, including die-off and healthy specimens, as well as samples of forage fish and invertebrate prey collected in 2015–2017, revealed a low to moderate frequency (20%-54%) of saxitoxin occurrence among taxa groups; but all at low concentrations [123]. Domoic acid was found in a single bird, and in some prey taxa (4%-33%). Authors noted that all biotoxin values were below levels reported in other seabird die-offs where causal links were established between toxin concentration and bird mortality, and as such, do not support a hypothesis that algal bloom biotoxins were a primary cause of murre mortality in Alaska [123]. Furthermore, the likelihood that HAB toxins were a primary and acute causal factor in the die-off appears small given that the center of the murre mass mortality event was the GOA, and the extended duration of the die-off (9 months of 100x baseline) both preceded and extended well past peak HAB bloom windows [118]. Also, we should have seen behavioral changes in affected birds as well as a larger number of species affected if HABs were a primary source of mortality [120,124]. Nonetheless, we are still lacking in basic information (e.g., what is a lethal dose?) about HAB effects on marine birds, and it cannot be ruled out as a contributing factor to the die-off [123]. We need more information on the depuration rates of HAB toxins, acute toxic levels (e.g., LD 50 ) and the effects of chronic toxin exposure in order to fully assess their potential contribution to the die-off [120,123].

Top-down effects: Resource competition from ectotherms. In addition to affecting spatial distribution of large predatory groundfish [125], increasing water temperature has the immediate and predictable effect of increasing metabolic rate, and usually food demand, of these marine ectotherms when they are operating within preferred temperature regimes [92,126]. The influence of this ecological “master factor” [127] on groundfish must have been substantial during the extreme 2014–2016 heatwave, but this pathway of upper trophic impact has been largely overlooked as a factor in regulating populations of groundfish, or other marine predators that compete with groundfish for food [92,117,128,129]. Recent modeling [92] of the effect of temperature on metabolic rate and food consumption in the GOA of three dominant groundfish predators including walleye pollock (Gadus chalcogrammus), Pacific cod (Gadus macrocephalus) and arrowtooth flounder (Atheresthes stomias) showed that an increase of 2°C in the GOA from pre-heatwave (1981–2011) temperatures would have increased food consumption of these species by 70%, 34% and 65% respectively. If we weight each species consumption estimate by its population size (stock biomass [130]), then the increase in prey demand by all species combined would be 63% higher than it was before the temperature increase. Pacific halibut (Hippoglossus stenolepis) show a similar response to increasing temperature in the GOA and Bering Sea [69]. The micronekton most commonly eaten by these groundfish include several species also favored by murres and other avian piscivores, especially capelin, sand lance, juvenile pollock, herring and euphausiids (especially in winter) [131]. Given the size of these three groundfish stocks in 2015 (4.48 M mt, [130]) and calculated consumption rates [92], these groundfish would have consumed ~10 M mt/yr of prey in 2015 if temperatures remained average. By comparison, total annual forage consumption by the ~2.5 million common murres in the GOA (calculations following [46,132,133]) total only ~0.45 M mt/yr. Thus in 2015, without a temperature increase, predatory groundfish would have consumed approximately ~20 times more total prey biomass, and ~6 times more forage fish biomass than murres (since fish comprise about a quarter of these groundfish diets; [134]). The 2ºC increase in water temperature would have pushed ectothermic groundfish prey consumption to ~15 M mt/yr, and thereby substantially increase forage fish grazing rates. Given that groundfish typically out-consume seabirds by 10:1 or even 100:1 ratios in northern shelf ecosystems [135,136], a 60% increase in consumption rates by groundfish should have some consequences for seabirds. No comparable modelling of temperature impact on metabolism of fish in the CCS has been undertaken, but the CCS shelf sustains at least 3.1 M mt of large predatory fishes (mostly hake Merluccius productus, rockfish, flatfish] [137,138], comparable to biomass density in the GOA and likely to also have provided significant increases in competition with murres during warming events. If the GOA marine ecosystem was operating at “relative equilibrium” [139,140] prior to the heatwave, then we hypothesize that this massive increase in foraging rate would have eventually led to prey deficits [69,136] for the groundfish themselves (creating intra-specific competition) and for other competitors such as seabirds and marine mammals (creating inter-specific competition) [136,141]. In this scenario, murres would be more sensitive to reductions in key forage fish species than competing groundfish, which typically have much broader diets and less sensitivity to fluctuations in any one prey type [136,142]. Also, it would presumably require a passage of some time for elevated grazing to deplete prey stocks below critical levels needed by murres. In fact, it was almost a full year from start of the “official” heatwave (August 2014, [10]) and more than 3 years after the rate of warming turned positive in 2012 (Fig 1) before a few murre colonies experienced reproductive failure and elevated murre mortality appeared in the GOA and northern CCS (Figs 3 and 5). Murre mortalities increased and persisted through fall in the GOA and southern CCS, and then peaked in the GOA during December 2015 and January 2016, a full 18 months after initiation of the heatwave. Murre die-offs diminished to background levels by April-June of 2016, as water temperatures returned to normal [10]. In contrast, reproductive failures peaked at 13 colonies during the summer of 2016 (23–24 months from heatwave initiation), continued at 9 colonies in 2017, and declined to only 4 colonies in 2018 (USGS, USFWS unpubl. data), although it is bracing to remember that a synchronized failure of even 4 murre colonies would have once been considered an extreme event. Overall, these findings suggest that prey stocks were replenished slowly during the 2 years after the heatwave ended in summer 2016, or that some sort of relative equilibrium among ectothermic and endothermic predators was being re-established following a large cull of bird, fish and mammal populations, or both. While murres were visibly dying en masse and failing to reproduce in 2015–2017, adult Pacific cod populations in the GOA were silently crashing underwater. Following three years in which commercial catches were well below quotas in the GOA (2015–24%, 2016–35%, 2017–45%), and a severe reduction in abundance of some older age cohorts occurred, the allowable catch quota for 2018 was reduced by 80% from the 2017 level [129]. The decline in the cod stock was attributed to reduced adult survival from starvation owing to a major reduction of forage in diets (especially capelin), coupled with a large increase in metabolic rates and food demands [129]. The same changes appeared in arrowtooth flounder, to a lesser degree [69,143]. In addition, the authors concluded that “other ectothermic fish species would be expected to have similarly elevated metabolic demands during the warm conditions, increasing the potential for broad scale prey limitations”, a conclusion that would seem to fit Pacific halibut in the Bering Sea and GOA as well [69]. Indeed, we might expect elevated consumption from some more of the other 30 commercial groundfish species [130], five species of salmon, and non-commercial fish species, alongside the usual competition from other common endothermic piscivores in the GOA, including at least thirty other species of seabirds, ten cetaceans, and five pinnipeds [144,145]. Finally, we find independent supporting evidence for potential basin-scale resource competition between large predatory fish and seabirds in the Bering Sea, where biennial high-low cycles in pink salmon (Oncorhynchus gorbuscha) abundance result in high rates of forage consumption in high salmon years, and create synchronized biennial cycles in seabird body condition and reproductive success (both low in high salmon years [141,146,147]).