Foraging in marine habitats increases mercury concentrations in a generalist seabird.

Methylmercury concentrations vary widely across geographic space and among habitat types, with marine and aquatic-feeding organisms typically exhibiting higher mercury concentrations than terrestrial-feeding organisms. However, there are few model organisms to directly compare mercury concentrations as a result of foraging in marine, estuarine, or terrestrial food webs. The ecological impacts of differential foraging may be especially important for generalist species that exhibit high plasticity in foraging habitats, locations, or diet. Here, we investigate whether foraging habitat, sex, or fidelity to a foraging area impact blood mercury concentrations in western gulls (Larus occidentalis) from three colonies on the US west coast. Cluster analyses showed that nearly 70% of western gulls foraged primarily in ocean or coastal habitats, whereas the remaining gulls foraged in terrestrial and freshwater habitats. Gulls that foraged in ocean or coastal habitats for half or more of their foraging locations had 55% higher mercury concentrations than gulls that forage in freshwater and terrestrial habitats. Ocean-foraging gulls also had lower fidelity to a specific foraging area than freshwater and terrestrial-foraging gulls, but fidelity and sex were unrelated to gull blood mercury concentrations in all models. These findings support existing research that has described elevated mercury levels in species using aquatic habitats. Our analyses also demonstrate that gulls can be used to detect differences in contaminant exposure over broad geographic scales and across coarse habitat types, a factor that may influence gull health and persistence of other populations that forage across the land-sea gradient.

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.

Heatwave-induced synchrony within forage fish portfolio disrupts energy flow to top pelagic predators.

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, changes in zooplankton communities may have driven bottom-up regulation as copepod community structure shifted toward 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.

Extreme mortality and reproductive failure of common murres resulting from the northeast Pacific marine heatwave of 2014-2016.

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.

Comparing imaging, acoustics, and radar to monitor Leach's storm-petrel colonies.

Seabirds are integral components of marine ecosystems and, with many populations globally threatened, there is a critical need for effective and scalable seabird monitoring strategies. Many seabird species nest in burrows, which can make traditional monitoring methods costly, infeasible, or damaging to nesting habitats. Traditional burrow occupancy surveys, where possible, can occur infrequently and therefore lead to an incomplete understanding of population trends. For example, in Oregon, during the last three decades there have been large changes in the abundance of Leach's storm-petrels (Hydrobates leucorhoa), which included drastic declines at some colonies. Unfortunately, traditional monitoring failed to capture the timing and magnitude of change, limiting managers' ability to determine causes of the decline and curtailing management options. New, easily repeatable methods of quantifying relative abundance are needed. For this study, we tested three methods of remote monitoring: passive acoustic monitoring, time-lapse cameras, and radar. Abundance indices derived from acoustics and imagery: call rates, acoustic energy, and counts were significantly related to traditional estimates of burrow occupancy of Leach's storm-petrels. Due to sampling limitations, we were unable to compare radar to burrow occupancy. Image counts were significantly correlated with all other indices, including radar, while indices derived from acoustics and radar were not correlated. Acoustic data likely reflect different aspects of the population and hold the potential for the further development of indices to disentangle phenology, attendance of breeding birds, and reproductive success. We found that image counts are comparable with standard methods (e.g., radar) in producing annual abundance indices. We recommend that managers consider a sampling scheme that incorporates both acoustics and imaging, but for sites inaccessible to humans, radar remains the sole option. Implementation of acoustic and camera based monitoring programs will provide much needed information for a vulnerable group of seabirds.

Microbial Ecology of the Western Gull (Larus occidentalis).

Avian species host diverse communities of microorganisms which have important roles in the life of birds, including increased metabolism, protection from disease, and immune system development. Along with high human populations and a diversity of human uses of coastal zones, anthropogenic food sources are becoming increasingly available to some species, including gulls. Anthropogenic associations increase the likelihood of encountering foreign or pathogenic bacteria. Diseases in birds caused by bacteria are a substantial source of avian mortality; therefore, it is essential to characterize the microbiome of seabirds. Here, we determined both core and environmentally derived microbial communities of breeding western gulls (Larus occidentalis) from six colonies in California and Oregon. Using DNA extracted from bacterial swabs of the bill, cloaca, and feet of gulls, 16S rRNA gene sequencing was performed targeting the V4 region. We identified a total of 8542 operational taxonomic units (OTUs) from 75 gulls. Sixty-eight OTUs were identified in gulls from all six colonies with the greatest representation from phyla's of Firmicutes, Proteobacteria, Bacteroidetes, and Actinobacteria. Overall, microbial richness based on Chao's Abundance-based Coverage Estimator (ACE) index was similar for all colonies (mean = 2347 OTUs) with the smallest coastal colonies having the highest richness (mean = 2626 OTUs) and the largest colonies, located farther off-shore, having the lowest (mean = 2068 OTUs). This survey represents the most in-depth assessment to date of microbes associated with western gulls, and the first study to identify both species-specific and environmentally derived bacteria across multiple populations.

Lessons from seabird conservation in Alaskan longline fisheries.

Although bycatch of seabirds and other long-lived species is a critical conservation issue in world fisheries, case studies documenting significant reductions in the mortality of these low-productivity species in a fishery are rare. We studied progress toward seabird conservation in the Alaskan longline fisheries, one of the largest and most diverse demersal fisheries. We generated annual seabird bycatch rates in 4 target fisheries and all fisheries combined from 23 years of fisheries observer data. We used 0-inflated negative binomial models to evaluate variables influencing seabird bycatch per unit effort (BPUE) in 2 target fisheries. Following adoption of streamer lines, at first voluntarily and then mandatorily, seabird BPUE was reduced by 77-90%, preventing mortality of thousands of birds per year. Despite this, BPUE increased significantly in 2 of 4 target fisheries since streamer lines were adopted. Although night setting yielded significant reductions (74-97%) in seabird BPUE and significant increases (7-11%) in fish catch per unit effort over daytime setting, nighttime setting increased the BPUE of Northern Fulmar (Fulmarus glacialis) by 40% and nontarget fish species by 5-17%. Thus, best practices to prevent seabird mortalities in longline fisheries varied by species assemblage and fishery. Our results inform global efforts toward fisheries bycatch reduction by illustrating that successful conservation requires fishery-specific solutions, strong industry support, constant vigilance in analysis and reporting observer data, and ongoing outreach to fleets, especially to vessels with anomalously high BPUE.

Aprendizajes de la Conservación de Aves Marinas en las Pesquerías con Palangre de Alaska Melvin Resumen Aunque la captura accesoria de aves marinas y otras especies con ciclos de vida largos es un asunto de importancia para la conservación en las pesquerías a nivel global, son raros los estudios de caso que documentan las reducciones significativas de la mortalidad de estas especies de baja productividad en las pesquerías. Estudiamos el progreso hacia la conservación de aves marinas en las pesquerías con palangre en Alaska, una de las pesquerías demersales más grandes y con mayor diversidad. Generamos tasas anuales de capturas accesorias de aves marinas para cuatro pesquerías y todas las pesquerías combinadas a partir de 23 años de datos de observación de pesquerías. Usamos modelos binomiales negativos con inflación 0 para evaluar las variables que influyen sobre la captura accesoria de aves marinas por unidad de esfuerzo (BPUE, en inglés) en dos pesquerías. Después de la adopción de la caña de pescar, al principio voluntariamente y después de manera obligatoria, el BPUE de aves marinas se redujo entre un 77 y 90%, lo que previno la mortalidad de miles de aves por año. A pesar de esto, el BPUE incrementó significativamente en dos de las cuatro pesquerías diana desde que se adoptaron las cañas de pescar. Aunque las puestas nocturnas resultaron en reducciones significativas (74-97%) en el BPUE de aves marinas e incrementos significativos (7-11%) en la captura de peces por unidad de esfuerzo comparadas con las puestas diurnas, las puestas nocturnas incrementaron el BPUE del fulmar boreal (Fulmarus glacialis) en un 40% y entre un 5 y 17% el de las especies de peces cuya captura no es relevante para las pesquerías. Por lo tanto, las mejores prácticas para prevenir la mortalidad de las aves marinas en las pesquerías con palangre variaron dependiendo del grupo de especies y de la pesquería. Nuestros resultados informan a los esfuerzos globales hacia la reducción de la captura accesoria de las pesquerías al ilustrar que la conservación exitosa requiere de soluciones específicas por pesquería, un fuerte apoyo por parte de la industria, una vigilancia constante del análisis y el reporte de los datos de observación, y una participación continua de las flotas, especialmente en el caso de navíos con un BPUE anormalmente alto.

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.

Prey patch patterns predict habitat use by top marine predators with diverse foraging strategies.

Spatial coherence between predators and prey has rarely been observed in pelagic marine ecosystems. We used measures of the environment, prey abundance, prey quality, and prey distribution to explain the observed distributions of three co-occurring predator species breeding on islands in the southeastern Bering Sea: black-legged kittiwakes (Rissa tridactyla), thick-billed murres (Uria lomvia), and northern fur seals (Callorhinus ursinus). Predictions of statistical models were tested using movement patterns obtained from satellite-tracked individual animals. With the most commonly used measures to quantify prey distributions--areal biomass, density, and numerical abundance--we were unable to find a spatial relationship between predators and their prey. We instead found that habitat use by all three predators was predicted most strongly by prey patch characteristics such as depth and local density within spatial aggregations. Additional prey patch characteristics and physical habitat also contributed significantly to characterizing predator patterns. Our results indicate that the small-scale prey patch characteristics are critical to how predators perceive the quality of their food supply and the mechanisms they use to exploit it, regardless of time of day, sampling year, or source colony. The three focal predator species had different constraints and employed different foraging strategies--a shallow diver that makes trips of moderate distance (kittiwakes), a deep diver that makes trip of short distances (murres), and a deep diver that makes extensive trips (fur seals). However, all three were similarly linked by patchiness of prey rather than by the distribution of overall biomass. This supports the hypothesis that patchiness may be critical for understanding predator-prey relationships in pelagic marine systems more generally.

Wind, waves, and wing loading: morphological specialization may limit range expansion of endangered albatrosses.

Among the varied adaptations for avian flight, the morphological traits allowing large-bodied albatrosses to capitalize on wind and wave energy for efficient long-distance flight are unparalleled. Consequently, the biogeographic distribution of most albatrosses is limited to the windiest oceanic regions on earth; however, exceptions exist. Species breeding in the North and Central Pacific Ocean (Phoebastria spp.) inhabit regions of lower wind speed and wave height than southern hemisphere genera, and have large intrageneric variation in body size and aerodynamic performance. Here, we test the hypothesis that regional wind and wave regimes explain observed differences in Phoebastria albatross morphology and we compare their aerodynamic performance to representatives from the other three genera of this globally distributed avian family. In the North and Central Pacific, two species (short-tailed P. albatrus and waved P. irrorata) are markedly larger, yet have the smallest breeding ranges near highly productive coastal upwelling systems. Short-tailed albatrosses, however, have 60% higher wing loading (weight per area of lift) compared to waved albatrosses. Indeed, calculated aerodynamic performance of waved albatrosses, the only tropical albatross species, is more similar to those of their smaller congeners (black-footed P. nigripes and Laysan P. immutabilis), which have relatively low wing loading and much larger foraging ranges that include central oceanic gyres of relatively low productivity. Globally, the aerodynamic performance of short-tailed and waved albatrosses are most anomalous for their body sizes, yet consistent with wind regimes within their breeding season foraging ranges. Our results are the first to integrate global wind and wave patterns with albatross aerodynamics, thereby identifying morphological specialization that may explain limited breeding ranges of two endangered albatross species. These results are further relevant to understanding past and potentially predicting future distributional limits of albatrosses globally, particularly with respect to climate change effects on basin-scale and regional wind fields.