Ecosystem response persists after a prolonged marine heatwave.

Some of the longest and most comprehensive marine ecosystem monitoring programs were established in the Gulf of Alaska following the environmental disaster of the Exxon Valdez oil spill over 30 years ago. These monitoring programs have been successful in assessing recovery from oil spill impacts, and their continuation decades later has now provided an unparalleled assessment of ecosystem responses to another newly emerging global threat, marine heatwaves. The 2014-2016 northeast Pacific marine heatwave (PMH) in the Gulf of Alaska was the longest lasting heatwave globally over the past decade, with some cooling, but also continued warm conditions through 2019. Our analysis of 187 time series from primary production to commercial fisheries and nearshore intertidal to offshore oceanic domains demonstrate abrupt changes across trophic levels, with many responses persisting up to at least 5 years after the onset of the heatwave. Furthermore, our suite of metrics showed novel community-level groupings relative to at least a decade prior to the heatwave. Given anticipated increases in marine heatwaves under current climate projections, it remains uncertain when or if the Gulf of Alaska ecosystem will return to a pre-PMH state.

Increased summer food supply decreases non-breeding movement in black-legged kittiwakes.

Individual condition at one stage of the annual cycle is expected to influence behaviour during subsequent stages, yet experimental evidence of food-mediated carry-over effects is scarce. We used a food supplementation experiment to test the effects of food supply during the breeding season on migration phenology and non-breeding behaviour. We provided an unlimited supply of fish to black-legged kittiwakes (Rissa tridactyla) during their breeding season on Middleton Island, Alaska, monitored reproductive phenology and breeding success, and used light-level geolocation to observe non-breeding behaviour. Among successful breeders, fed kittiwakes departed the colony earlier than unfed controls. Fed kittiwakes travelled less than controls during the breeding season, contracting their non-breeding range. Our results demonstrate that food supply during the breeding season affects non-breeding phenology, movement and distribution, providing a potential behavioural mechanism underlying observed survival costs of reproduction.

Diverging phenological responses of Arctic seabirds to an earlier spring.

The timing of annual events such as reproduction is a critical component of how free-living organisms respond to ongoing climate change. This may be especially true in the Arctic, which is disproportionally impacted by climate warming. Here, we show that Arctic seabirds responded to climate change by moving the start of their reproduction earlier, coincident with an advancing onset of spring and that their response is phylogenetically and spatially structured. The phylogenetic signal is likely driven by seabird foraging behavior. Surface-feeding species advanced their reproduction in the last 35 years while diving species showed remarkably stable breeding timing. The earlier reproduction for Arctic surface-feeding birds was significant in the Pacific only, where spring advancement was most pronounced. In both the Atlantic and Pacific, seabirds with a long breeding season showed a greater response to the advancement of spring than seabirds with a short breeding season. Our results emphasize that spatial variation, phylogeny, and life history are important considerations in seabird phenological response to climate change and highlight the key role played by the species' foraging behavior.

Circumpolar dynamics of a marine top-predator track ocean warming rates.

Global warming is a nonlinear process, and temperature may increase in a stepwise manner. Periods of abrupt warming can trigger persistent changes in the state of ecosystems, also called regime shifts. The responses of organisms to abrupt warming and associated regime shifts can be unlike responses to periods of slow or moderate change. Understanding of nonlinearity in the biological responses to climate warming is needed to assess the consequences of ongoing climate change. Here, we demonstrate that the population dynamics of a long-lived, wide-ranging marine predator are associated with changes in the rate of ocean warming. Data from 556 colonies of black-legged kittiwakes Rissa tridactyla distributed throughout its breeding range revealed that an abrupt warming of sea-surface temperature in the 1990s coincided with steep kittiwake population decline. Periods of moderate warming in sea temperatures did not seem to affect kittiwake dynamics. The rapid warming observed in the 1990s may have driven large-scale, circumpolar marine ecosystem shifts that strongly affected kittiwakes through bottom-up effects. Our study sheds light on the nonlinear response of a circumpolar seabird to large-scale changes in oceanographic conditions and indicates that marine top predators may be more sensitive to the rate of ocean warming rather than to warming itself.

Wintering North Pacific black-legged kittiwakes balance spatial flexibility and consistency.

BACKGROUND: Marine environments are inherently dynamic, yet marine predators are often long-lived and employ strategies where consistency, individual specialization, routine migrations, and spatial memory are key components to their foraging and life-history strategies. Intrinsic determinates of animal movements are linked to physiological and life-history traits (e.g. sex, colony, experience), while extrinsic influences occur as the result of an animal's interactions with either other animals or the environment (e.g. prey availability, weather, competition). Knowledge of the factors affecting animal movements is critical to understand energetic bottlenecks and population dynamics. Here, we attempt to understand the interaction of some of these factors on the winter distributions of a surface-feeding seabird in the North Pacific. Between 2008 and 2011, we tracked 99 black-legged kittiwakes breeding at St. Paul and St. George in the Pribilof Islands, Alaska using geolocation loggers. We tested for colony and sex differences in winter distributions, and individual spatial fidelity over two consecutive winters of 17 individuals. Then we linked tracking data to associated environmental conditions as proxies of prey availability (e.g. sea surface temperature, mesoscale eddies, chlorophyll a, and wind) to understand their influence on kittiwake space use at an ocean basin scale. RESULTS: Black-legged kittiwakes from both Pribilof Islands primarily wintered in pelagic sub-arctic waters, however, distributions spanned seven ecoregions of the North Pacific. There was a high degree of similarity in area use of birds from the two closely situated colonies and between sexes. Birds tracked for two consecutive years showed higher fidelity to wintering areas than occurred at random. Annual changes were apparent, as distributions were further north in 2009/10 than 2008/09 or 2010/11. This occurred because 70 % of birds remained in the Bering Sea in the fall of 2009, which corresponded with lower October sea surface temperatures than the other two years. CONCLUSIONS: Although individuals returned to wintering areas in consecutive years, our results suggest that under current conditions individual black-legged kittiwakes have a high capacity to alter winter distributions.

Body size affects individual winter foraging strategies of thick-billed murres in the Bering Sea.

Foraging and migration often require different energetic and movement strategies. Though not readily apparent, constraints during one phase might influence the foraging strategies observed in another. For marine birds that fly and dive, body size constraints likely present a trade-off between foraging ability and migration as smaller bodies reduce flight costs, whereas larger bodies are advantageous for diving deeper. This study examines individual wintering strategies of deep diving thick-billed murres (Uria lomvia) breeding at three colonies in the south-eastern Bering Sea: St Paul, St George and Bogoslof. These colonies, arranged north to south, are located such that breeding birds forage in a gradient from shelf to deep-water habitats. We used geolocation time-depth recorders and stable isotopes from feathers to determine differences in foraging behaviour and diet of murres during three non-breeding periods, 2008-2011. Body size was quantified by a principal component analysis (wing, culmen, head+bill and tarsus length). A hierarchical cluster analysis identified winter foraging strategies based on individual movement, diving behaviour and diet (inferred from stable isotopes). Structural body size differed by breeding island. Larger birds from St Paul had higher wing loading than smaller birds from St George. Larger birds, mainly from St Paul, dove to deeper depths, spent more time in the Bering Sea, and likely consumed higher trophic-level prey in late winter. Three winter foraging strategies were identified. The main strategy, employed by small birds from all three breeding colonies in the first 2 years, was characterized by high residency areas in the North Pacific south of the Aleutians and nocturnal diving. In contrast, 31% of birds from St Paul remained in the Bering Sea and foraged mainly during the day, apparently feeding on higher trophic-level prey. Throat feather stable isotopes indicated that individuals exhibited flexibility in the use of this colony-specific foraging strategy. The third strategy only occurred in 2010/2011, when birds dove more and deeper, suggesting limited prey resources. Foraging strategies partitioned with respect to annual differences, presumably in response to shifts in distribution of prey, and were linked to body size. The presence of a colony-specific wintering strategy suggests the potential for overwinter survival differences between these populations.

Foraging responses of black-legged kittiwakes to prolonged food-shortages around colonies on the Bering Sea shelf.

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.

Transmission and reassortment of avian influenza viruses at the Asian-North American interface.

Twenty avian influenza viruses were isolated from seven wild migratory bird species sampled at St. Lawrence Island, Alaska. We tested predictions based on previous phylogenetic analyses of avian influenza viruses that support spatially dependent trans-hemispheric gene flow and frequent interspecies transmission at a location situated at the Asian-North American interface. Through the application of phylogenetic and genotypic approaches, our data support functional dilution by distance of trans-hemispheric reassortants and interspecific virus transmission. Our study confirms infection of divergent avian taxa with nearly identical avian influenza strains in the wild. Findings also suggest that H16N3 viruses may contain gene segments with unique phylogenetic positions and that further investigation of how host specificity may impact transmission of H13 and H16 viruses is warranted.

Prevalence of Influenza A viruses in wild migratory birds in Alaska: patterns of variation in detection at a crossroads of intercontinental flyways.

BACKGROUND: The global spread of the highly pathogenic avian influenza H5N1 virus has stimulated interest in a better understanding of the mechanisms of H5N1 dispersal, including the potential role of migratory birds as carriers. Although wild birds have been found dead during H5N1 outbreaks, evidence suggests that others have survived natural infections, and recent studies have shown several species of ducks capable of surviving experimental inoculations of H5N1 and shedding virus. To investigate the possibility of migratory birds as a means of H5N1 dispersal into North America, we monitored for the virus in a surveillance program based on the risk that wild birds may carry the virus from Asia. RESULTS: Of 16,797 birds sampled in Alaska between May 2006 and March 2007, low pathogenic avian influenza viruses were detected in 1.7% by rRT-PCR but no highly pathogenic viruses were found. Our data suggest that prevalence varied among sampling locations, species (highest in waterfowl, lowest in passerines), ages (juveniles higher than adults), sexes (males higher than females), date (highest in autumn), and analytical technique (rRT-PCR prevalence = 1.7%; virus isolation prevalence = 1.5%). CONCLUSION: The prevalence of low pathogenic avian influenza viruses isolated from wild birds depends on biological, temporal, and geographical factors, as well as testing methods. Future studies should control for, or sample across, these sources of variation to allow direct comparison of prevalence rates.

Long-term ecosystem response to the Exxon Valdez oil spill.

The ecosystem response to the 1989 spill of oil from the Exxon Valdez into Prince William Sound, Alaska, shows that current practices for assessing ecological risks of oil in the oceans and, by extension, other toxic sources should be changed. Previously, it was assumed that impacts to populations derive almost exclusively from acute mortality. However, in the Alaskan coastal ecosystem, unexpected persistence of toxic subsurface oil and chronic exposures, even at sublethal levels, have continued to affect wildlife. Delayed population reductions and cascades of indirect effects postponed recovery. Development of ecosystem-based toxicology is required to understand and ultimately predict chronic, delayed, and indirect long-term risks and impacts.

Raising young reduces body condition and fat stores in black-legged kittiwakes.

We conducted a manipulative experiment to investigate how raising chicks affects the body condition (body mass scaled by body size) and body composition (percent fat vs. lean mass) of black-legged kittiwakes (Rissa tridactyla). For 4 consecutive years (1991-1994) we removed eggs from randomly selected nests and then compared adults raising chicks with adults that had their eggs removed. At the end of the chick-rearing period, adults raising chicks were significantly lighter for their size than adults that had their eggs removed. Adults raising chicks also had a significantly lower percent body fat (by 28%) than adults from manipulated nests. The difference in percent body fat between the two groups was apparent at all levels of condition, suggesting that adults that are raising chicks apportion their reserves differently than adults that are working only to meet their own metabolic needs. End-of-season body condition of adults from manipulated and unmanipulated nests varied significantly among 5 years of study, and appeared to reflect differences in local foraging conditions. In all years, females were in worse condition than males at the end of the breeding season. This sex-specific condition difference did not, however, appear to indicate a greater short-term reproductive cost among females. Females were lighter for their size than males in both the manipulated and unmanipulated groups. Our results suggest that adult kittiwakes compromise their body condition and body composition during chick rearing to increase the likelihood of successfully fledging young, even though such adjustments may decrease their own post-reproductive survival probabilities. Prior to estimating the body composition of the experimental birds, we evaluated the usefulness of several noninvasive techniques for predicting fat mass in kittiwakes. We used cross-validation techniques to compare multiple regression models that included total body electrical conductivity (TOBEC), total body water (TBW), and morphometric measurements as independent variables. The most parsimonious model for predicting fat mass was based on TOBEC and mass measurements. TBW and morphometrics were of little utility in predicting fat mass in kittiwakes. Previous studies that have evaluated the usefulness of TOBEC as a predictor of fat mass have shown mixed results. We suggest that the size of the experimental subject relative to the size of the TOBEC measurement chamber may affect the accuracy of this technique.