An investigation of physiological effects of the Deepwater Horizon oil spill on a long-distance migratory seabird, the northern gannet.

Exposure to oil can have long-term impacts on migratory birds. Following the 2010 Deepwater Horizon blowout in the Gulf of Mexico (GOM), we investigated potential impacts of oil exposure on a population of northern gannets (Morus bassanus) that breed on Bonaventure Island (Québec, Canada) and winter in GOM and along the U.S. Atlantic coast (AC). Blood and feather samples were collected from adults previously equipped with geolocators to determine wintering locations. Parent and alkylated polycyclic aromatic hydrocarbons (PAHs); trace metals; stable isotopes of carbon, nitrogen, and hydrogen; and immune, thyroid, steroid, retinoid, and genetic endpoints were measured. PAH and trace metal concentrations did not differ between gannets using different wintering sites. Feather stable isotope values varied significantly between birds from different wintering locations. Gannets wintering in GOM showed higher feather corticosterone and plasma thyroid hormone levels, which may indicate increased energetic demands and/or greater exposure to environmental stressors.

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.

Feather corticosterone during non-breeding correlates with multiple measures of physiology during subsequent breeding in a migratory seabird.

Carry-over effects in migratory birds are likely mediated by physiological processes that are activated in response to environmental variation. Such processes affect body condition and/or reproductive success, and can include corticosterone (CORT) because this hormone responds to environmental stressors and influences energy balance. Few studies have considered how CORT levels during non-breeding relate to a broader physiological profile during subsequent breeding, and fewer still have considered measures other than body condition. To explore CORT's potential role in carry-over effects, we investigated the relationship between CORT and foraging ecology of northern gannets (Morus bassanus) during the non-breeding period, and tested for associations between these factors and variation in a suite of physiological and biochemical metrics during subsequent breeding. Northern gannets are the largest seabird top predator in the North Atlantic and were among the hardest hit by the Deepwater Horizon oil blowout in the Gulf of Mexico in 2010. We used light-level geolocators to confirm winter origins of individuals in our study. No interrelationships were found among levels of CORT from feathers grown during non-breeding (CORTf) and variation in foraging ecology, measured by stable isotopes of carbon (δ13C) and nitrogen (δ15N) from the same feathers. CORTf was correlated negatively with hematocrit and positively with triglyceride measured during subsequent incubation, and explained more variation in these variables than did body mass during incubation. These findings provide support for the hypothesis that energy management, measured using CORTf, during non-breeding carries over to influence physiological measures other than body condition. Gannets that previously wintered within the Gulf of Mexico in the years following the Deepwater Horizon oil blowout had higher levels of CORTf compared to birds that wintered along the Atlantic coast, suggesting an increased energetic cost associated with visiting the Gulf of Mexico. Our results indicate that CORT during non-breeding is associated with a broader physiological profile during subsequent breeding than previously reported in birds.

Polychlorinated dibenzo-p-dioxins, dibenzofurans, and flame retardants in northern gannet (Morus bassanus) eggs from Bonaventure Island, Gulf of St. Lawrence, 1994-2014.

Northern gannet (Morus bassanus) eggs from Bonaventure Island, Québec, Canada, were collected to monitor concentrations of contaminants. Polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDDs/Fs) and non-ortho polychlorinated biphenyls (PCBs) were measured in eggs from 2004 and 2009, and several brominated and nonbrominated flame retardants (FRs) were measured every 2-5 years in eggs from 1994 to 2014. The sum (Σ) concentrations of PCDDs/Fs were significantly lower in 2009 relative to 2004, but the total toxic equivalent concentrations for PCDDs, PCDFs, and PCBs showed no significant differences (196 ng/kg wet weight (ww) in 2004 and 220 ng/kg ww in 2009). The mean ΣFR concentrations decreased significantly between 1994 and 2014, from 58 ng/g ww to 19 ng/g ww. Hexabromocyclododecane (HBCDD) was the principal nonbrominated FR detected in gannet eggs and ranged from <1.0 ng/g ww to 6.9 ng/g ww. The PCDD/F and nonortho PCB profiles were dominated by 2,3,7,8- tetrachloro-dibenzofuran (2,3,7,8-TCDF; from 26.2 ng/g ww to 34.8 ng/kg ww) and PCB-77 (from 1580 ng/g ww to 2650 ng/kg ww), respectively. Although the values of both ecological tracer stable isotopes of carbon (δ13C) and nitrogen (δ15N) showed differences among the years, no temporal trends were observed, which indicates relatively stable adults' diet and foraging area over this time period. The trends over time in concentrations of the studied contaminants likely reflect a decrease in environmental contamination. The mean 2012 eggshell thickness was 10% lower than the pre-DDT value and corresponded to a year of poor reproductive success.

Nutritional stress in Northern gannets during an unprecedented low reproductive success year: can extreme sea surface temperature event and dietary change be the cause?

Reproductive success of seabirds is tightly associated with availability of their prey for which the spatiotemporal distribution may be influenced by sea surface temperature (SST) fluctuations. The objective of this study was to investigate whether Northern gannets (Morus bassanus) from the largest colony in North America (Bonaventure Island, Quebec, Canada) were in negative nutritional state during the unprecedented low reproductive success year of 2012, and whether this was associated with changes in SST anomalies and diet. The incubation period of gannets in 2012 was characterized by a significant decline, from early to late incubation, in plasma triglyceride levels that was associated with an increase in plasma corticosterone levels. However, no changes in plasma glycerol and ß-hydroxybutyrate levels were noted. SST anomalies recorded in this area (south of the Gulf of St. Lawrence) during the breeding period were consistently higher in 2012 compared to the previous year (a better reproductive success year). Based on signatures of stable carbon (δ(13)C) and nitrogen (δ(15)N) isotopes in gannet red blood cells and in whole fish homogenates of three major preys (mackerel, herring, and capelin), a minor dietary shift was noted between those years and incubation periods. In light of these findings, it is suggested that the extreme warm-water perturbation event that prevailed in the Gulf of St. Lawrence during summer 2012 was associated with a rapid deterioration of nutritional condition of Bonaventure Island gannets during the incubation. These suboptimal physiological changes likely contributed to the dramatic decline in reproductive success reported in this colony.

Temporal trends of mercury, organochlorines and PCBs in northern gannet (Morus bassanus) eggs from Bonaventure Island, Gulf of St. Lawrence, 1969-2009.

Since 1969, northern gannet (Morus bassanus) eggs from Bonaventure Island, Québec, have been collected to monitor concentrations of contaminants. Levels of p,p'-DDE, which caused low breeding success of Bonaventure gannets in the 1960s, decreased by 99.4% from 1969 to 2009 (17.1-0.1 mg/kg ww), with concomitant improvement of hatching success. PCBs, most organochlorines and mercury also showed decreasing trends. Stable isotopes of carbon (δ(13)C) and nitrogen (δ(15)N) were measured to track the possible influence of diet changes on concentrations of contaminants over time. The confounding effect of the combustion of fossil fuels on baseline values of δ(13)C (the Suess effect) was taken into account. No temporal trends were observed in δ(13)C and δ(15)N values in gannet eggs. Hence trophic level or foraging area had a negligible influence on temporal trends of contaminants.

Prevalence and composition of fishing gear debris in the nests of northern gannets (Morus bassanus) are related to fishing effort.

Bycatch and indirect mortality associated with global fishing operations affect non-target species. Northern gannets (Morus bassanus) and other seabirds incorporate marine debris, much of it originating in fisheries, into their nests, at times resulting in entanglement. We compared the prevalence and composition of marine debris in nests at two gannet colonies in Newfoundland before and after a basin-wide ground fish closure in 1992, and at the species' largest colony in the Gulf of St. Lawrence, where fishing effort is low. The proportion of nests with marine debris decreased following the fishery closure, and the proportion of nests with fishing gear was related exponentially to the number of gillnets set around breeding colonies. Assessing the composition of gannet nests could provide a useful index of the prevalence of fishing debris and could be used to assess entanglement risk of other animals in the marine environment over decadal scales.

Tracking long-distance migration to assess marine pollution impact.

Animal tracking provides new means to assess far-reaching environmental impacts. In the aftermath of the Deepwater Horizon explosion in the Gulf of Mexico, a long-distance migrant, the northern gannet (Morus bassanus) suffered the highest oiling among beach-wrecked birds recovered. Analysis of bird-borne tracking data indicated that 25 per cent of their North American population from multiple colonies in eastern Canada migrated to the pollution zone. Findings contrasted sharply with available mark-recapture (band recovery) data. The timing of movement into and out of the Gulf indicates that immature birds would have absorbed most oil-induced mortality. Consequently, one of two outcomes is likely: either a lagged (likely difficult to assess) population decrease, or an undetectable population response buffered by age-related life-history adaptations. Tracking research is especially useful when little information on animal distributions in pollution zones is available, as is the case in the Gulf of Mexico. Ongoing research highlights current risks and conservation concerns.

Trophic structure and mercury distribution in a Gulf of St. Lawrence (Canada) food web using stable isotope analysis.

Even at low concentrations in the environment, mercury has the potential to biomagnify in food chains and reaches levels of concern in apex predators. The aim of this study was to relate the transfer of total mercury (THg) and methylmercury (MeHg) in a Gulf of St. Lawrence food web to the trophic structure, from primary consumers to seabirds, using stable nitrogen (δ(15)N) and carbon (δ(13)C) isotope analysis and physical environmental parameters. The energy reaching upper trophic level species was principally derived from pelagic primary production, with particulate organic matter (POM) at the base of the food chain. We developed a biomagnification factor (BMF) taking into account the various prey items consumed by a given predator using stable isotope mixing models. This BMF provides a more realistic estimation than when using a single prey. Lipid content, body weight, trophic level and benthic connection explained 77.4 and 80.7% of the variation in THg and MeHg concentrations, respectively in this food web. When other values were held constant, relationships with lipid and benthic connection were negative whereas relationships with trophic level and body weight were positive. Total Hg and MeHg biomagnified in this food web with biomagnification power values (slope of the relationship with δ(15)N) of 0.170 and 0.235, respectively on wet weight and 0.134 and 0.201, respectively on dry weight. Values of biomagnification power were greater for pelagic and benthopelagic species compared to benthic species whereas the opposite trend was observed for levels at the base of the food chain. This suggests that Hg would be readily bioavailable to organisms at the base of the benthic food chain, but trophic transfer would be more efficient in each trophic level of pelagic and benthopelagic food chains.

Organochlorines, brominated flame retardants and mercury levels in six seabird species from the Gulf of St. Lawrence (Canada): relationships with feeding ecology, migration and molt.

Concentrations of organochlorines (OCs), brominated flame retardants (BFRs) and mercury (Hg) were measured in eggs of six seabird species breeding in the Gulf of St. Lawrence, Canada. Stable nitrogen (delta15N) and carbon (delta13C) isotopes were used as ecological tracers to measure trophic level and connectivity with benthos, respectively. Concentrations, patterns as well as ecological tracers varied significantly between species. The sum of polychlorinated biphenyls (SigmaPCBs) was the most important group measured in all seabird species based on concentration followed generally by the sum of chlorinated pesticides (SigmaCPs), the sum of brominated flame retardants (SigmaBFRs) and finally total Hg (THg). SigmaPCBs, SigmaCPs and SigmaBFRs increased with trophic level, whereas THg did not. Only SigmaBFRs increased with a higher connectivity with the benthos. Seabird species resident to the Great Lakes-St. Lawrence ecosystem showed higher Hg and BFR levels than migratory species. Molt patterns were used to explain variations of contaminant levels.