Polycyclic aromatic compounds (PACs) were investigated in gull and tern eggs from breeding sites in receiving environments of the Athabasca Oil Sands Region (Alberta, Canada). Bitumen from natural outcrops and industry emissions of PACs are delivered downstream via the Athabasca River to the Peace-Athabasca Delta and Lake Athabasca. Parent and alkylated PACs were measured in eggs of Caspian Tern (n = 111), Common Tern (n = 53) and Ring-billed Gull (n = 40) from two downstream exposure sites and a reference lake. Total (sum of 47) PAC concentrations in eggs were 1-2 orders of magnitude higher for Caspian Tern (215.9 ± 263.3 ng/g wet weight [ww]) compared to Ring-billed Gull (32.6 ± 28.2 ng/g ww) and Common Tern (6.8 ± 5.8 ng/g ww). Concentrations were comparable in Ring-billed Gull eggs at an exposure and reference site. Eggs of all three species were dominated by alkylated low and high molecular weight compounds, and for Caspian Tern, alkylated dibenzothiophenes. Caspian Tern eggs showed large inter-year fluctuations in total PAC concentrations (2009 to 2022), with yearly means ranging from 2.0 to 661.3 ng/g ww. Carbon stable isotopes partially explained the inter-year variability, suggesting an influence of diet or habitat-specific feeding on Caspian Tern exposure to PACs. Egg PAC composition (particularly the detection of dibenzothiophenes) suggested petrogenic origins for Caspian Tern and pyrogenic or mixed sources for Ring-billed Gull and Common Tern. Future work is warranted to characterize the sources, drivers and toxicological risk of higher petrogenic PAC burdens in Caspian Tern eggs.
This study characterized the transport pathways and sources of mercury in downstream food webs of the Athabasca River Basin in northern Alberta, Canada. Flowing through a large boreal watershed in the Athabasca Oil Sands Region, the river drains into the ecologically-sensitive Peace-Athabasca Delta and western Lake Athabasca. Mercury stable isotope measurements on abiotic and biotic matrices were combined with spatial and temporal sampling to evaluate the importance of the Athabasca River as a conduit for mercury. Mixing model estimates derived from mercury isotopes indicated the Athabasca River was the source of 62–94% of the bioaccumulated mercury in otter, fish, and tern eggs collected from the delta or lake. A time series from 2009 to 2022 showed mercury loads from the Athabasca River enhanced bioaccumulation in western Lake Athabasca with the doubling of total mercury (THg) concentration in eggs of breeding terns following high flow years compared to low flow years. Mercury isotope data from potential abiotic sources (Athabasca River and Lake sediment, leaf litter, soil, air, rain) suggested a predominately terrestrial origin of mercury in fish of the Athabasca River. The similarity of terrestrial mercury isotope signatures with oil sands-related matrices (natural bitumen seeps, industry samples) precluded an estimation of contributions from oil sands operations to mercury bioaccumulation. Catchment processes or disturbances that increase mercury loads in the Athabasca River will increase mercury concentrations of aquatic biota in downstream receiving waters.
Rivers are major conduits that connect terrestrial carbon cycling with downstream receiving environments. In large lakes, the utilization of river-transported carbon in biological production remains poorly constrained. Lake Athabasca, the eighth largest lake in Canada, receives inflow from the Athabasca River and a large boreal wetland, the Peace-Athabasca Delta. Radiocarbon (14C) was measured to trace the transport of old carbon into western Lake Athabasca and its influence on a modern lake food web by distinguishing the ages of river and lake carbon pools. The fraction of modern carbon in surface sediments showed river inputs of old organic carbon extended at least 50 km into the lake. Old carbon was incorporated into the food web via surface water plankton, and it subsidized ~ 20–50% of carbon in vertebrate consumers, specifically fish and aquatic-feeding birds. These measurements of old carbon showed extensive river influence in western Lake Athabasca (likely > 1500 km2) and high connectivity of river loads with biological uptake.
Herring Gull (Larus argentatus) populations in Pukaskwa National Park have declined by 70% over the last 40 years. Populations of avian predators that prey on Herring Gulls have increased which could be a significant factor impacting gull populations. Here, we investigate Herring Gull daytime and nighttime nest attentiveness at locations with and without evidence of nocturnal predators. In 2017, Herring Gull nest attentiveness was examined at two sites using remote cameras. At one of those sites Great Horned Owl (Bubo virginianus) predation was observed, and gull nighttime nest attentiveness was lower there than at the site where owls were not observed. There were no inter-site differences in daytime nest attentiveness. In 2018, Herring Gull nest attentiveness was further investigated at the site where owls were present. At that site, Herring Gull nighttime nest attentiveness was significantly lower than during the day. Extended periods of absence of gulls from their nests during the night corresponded with the presence of owls. Predation of nest contents, in addition to the effects of other environmental stressors, are likely contributing to declines in Pukaskwa National Park's Herring Gull population.
Due to their relatively high trophic position and importance as a food source for many communities in the circumpolar north, seabird eggs are an important matrix for monitoring contaminant levels. In fact, many countries, including Canada, have established long-term seabird egg contaminant monitoring programs, with oil related compounds a contaminant of emerging concern for seabirds in several regions. Current approaches to measuring many contaminant burdens in seabird eggs are time-consuming and often require large volumes of solvent. Here we propose an alternative approach, based on the principle of microbead beating tissue extraction using custom designed stainless-steel extraction tubes and lids, to measure a suite of 75 polycyclic aromatic compounds (polycyclic aromatic hydrocarbons (PAHs), alkyl-PAHs, halogenated-PAHs and some heterocyclic compounds) comprising a wide-range of chemical properties. Our method was conducted in strict accordance with ISO/IEC 17025 guidelines for method validation. Accuracies for our analytes generally ranged from 70 - 120%, and intra and inter-day repeatability for most analytes were < 30%. Limits of detection/quantitation for the 75 target analytes were < 0.2/0.6 ng g−1. The level of contamination in our method blanks was significantly smaller in our stainless-steel tubes/lids relative to commercially available high-density plastic alternatives. Overall, our method meets our data quality objectives and results in a notable reduction in sample processing times relative to current approaches.
Herring gulls (Larus argentatus) are generalist feeders; contaminant levels in their eggs reflect chemical exposure and uptake due to foraging in both aquatic and terrestrial environments. Hence, contaminant levels in their eggs provide insights into sources and relative importance of aquatic versus terrestrial pathways of chemical transfer. Here, perfluoroalkyl acids (PFAAs) known to be bioaccumulative were measured in individual herring gull eggs from one site on Lake Superior, Ontario, Canada. Thirteen perfluorinated carboxylates (PFCA, C4-C18) and four perfluorinated sulfonates (PFSA, C4-C10) were measured. Total PFCA and total PFSA concentrations varied 4- and 5-fold, respectively, among eggs. To understand these differences, stable carbon and nitrogen isotopes and fatty acid dietary tracers were measured in the same eggs. Stable isotopes were not useful in explaining inter-egg differences in PFAA concentrations. However, a variety of omega 3 (n-3) and omega 6 (n-6) fatty acid measures were correlated with C9-C13 PFCAs as well as the PFSAs: perfluoro-1-hexanesulfonic acid (PFHxS) and perfluoro-1-octanesulfonic acid (PFOS). In general, n-3 fatty acids were positively correlated with egg PFAA concentrations while only the n-6 fatty acids exhibited negative relationships with egg PFAA levels. Proportions of n-3 and n-6 fatty acids in eggs would be expected to increase and decrease, respectively, with increased aquatic food in the gull diet. Results indicate that increased use of aquatic food led to heightened PFAA exposure in these generalist consumers sampled in a relatively remote area. They also highlight the utility of employing a variety of dietary markers for understanding contaminant exposure and accumulation.
Leach’s storm-petrel Oceanodroma leucorhoa populations in the North Atlantic have declined in recent decades. The cause of those declines is not clear but one potential contributing factor could be reductions in the availability of essential nutrients due to changing marine ecology resulting from global warming. One group of particular concern is the omega-3 highly unsaturated fatty acids (n-3 HUFAs), in particular, eicosapentaenoic (EPA) and docosahexaenoic (DHA) acids. Dietary sources of EPA and DHA are required for normal growth and development in higher consumers, including birds. However, previous work has predicted increases in sea surface temperatures may cause declines in their availability. Here, we investigate this possibility by examining temporal trends (1992-2015) in EPA and DHA concentrations in Leach’s storm-petrel eggs from 5 Canadian colonies: 2 on the Atlantic coast (Gull, Kent Islands) and 3 on the Pacific coast (Hippa, Storm, Cleland Islands). Neither EPA nor DHA concentrations in eggs decreased with time on either coast; rather, on the Atlantic coast, both EPA and DHA increased over the period of study. Carbon stable isotopes in the same eggs indicated that storm-petrels foraging in offshore, pelagic waters may have had increased access to n-3 HUFA. The data generated here provide a baseline for future comparisons. Ongoing regular monitoring of fatty acids in seabird eggs would be prudent given the likelihood of further increases in ocean temperatures.
Herring gulls (Larus argentatus) are used as ecological indicators of the coastal Lake Superior ecosystem in Pukaskwa National Park, Ontario, Canada. Their populations have declined by 70 % over the last 40 years, suggesting changes in the park ecosystem. Previous studies highlighted declining prey abundance as a possible contributing factor to population declines. Here, we assess herring gull diets via stable isotope (nitrogen, carbon) and fatty acid indicators to investigate how diet may influence population trends through effects on physiology (stress-related hormones), reproduction (egg size) and behavior (nest attentiveness). Diets were variable among individual herring gulls. Gulls utilizing anthropogenic food sources exhibited reduced levels of stress-associated hormones, increased egg size, and increased nest attentiveness. Anthropogenic food sources are likely buffering the impacts of declines in aquatic food availability; however, populations are still declining. Understanding factors contributing to population trends in ecological indicator species is critical for species management and for identifying stressors that are likely affecting the broader ecosystem. Herring gulls are archetypal examples of the "canary in a coalmine" indicator but in an ecosystem context. Changes in their diets and in variables associated with their physiology, reproduction, and behavior point to very significant changes occurring in the Lake Superior ecosystem. Integrated research across the Great Lakes is required to understand the extent of this change and its implications for the sustainability of wildlife populations. Crown Copyright (c) 2022 Published by Elsevier B.V. on behalf of International Association for Great Lakes Research. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/ 4.0/).
Lead (Pb) is a toxic element which is released as a result of anthropogenic activities, and Pb stable isotope ratios provide a means to distinguish sources and transport pathways in receiving environments. In this study, isotopes of bioaccumulated Pb (204Pb, 206Pb, 207Pb, 208Pb) were examined for diverse terrestrial and aquatic biota from three areas in western Canada: (a) otter, marten, gulls, terns, and wood frogs in the Alberta Oil Sands Region (AOSR), (b) fish, plankton, and gulls of Great Slave Lake (Yellowknife, Northwest Territories), and (c) wolverine from the Yukon. Aquatic and terrestrial biota from different habitats and a broad geographic area showed a remarkable similarity in their Pb isotope composition (grand mean ± 1 standard deviation: 206Pb/207Pb = 1.189 ± 0.007, 208Pb/207Pb = 2.435 ± 0.009, n = 116). Comparisons with Pb isotope ratios of local sources and environmental receptors showed that values in biota were most similar to those of atmospheric Pb, either measured in local aerosols influenced by industrial activities in the AOSR or in lichens (an aerosol proxy) near Yellowknife and in the Yukon. Biotic Pb isotope ratios were different from those of local geogenic Pb. Although the Pb isotope measurements could not unambiguously identify the specific anthropogenic sources of atmospheric Pb in biota, initial evidence points to the importance of fossil fuels currently used in transportation and power generation. Further research should characterize bioavailable chemical species of Pb in aerosols and important emission sources in western Canada.
Colonies of Herring (Larus argentatus) and/or Ring-billed Gulls (L. delawarensis) on Lake Ontario and the upper St. Lawrence River were searched annually, 1981-2018, for nesting Great Black-backed Gulls (L. marinus). Great Black-backed Gulls nested at nine sites where both Herring and Ring-billed Gulls nested, at seven sites with only Herring Gulls, and at one site where they nested solitarily. Nests per site ranged from 1-21 on Lake Ontario and 1-5 on the St. Lawrence River. On Lake Ontario, nest numbers increased from six nests in 1981 to 51 nests in 2001 (+ 11.3%/yr), then declined to zero nests in 2008, where they have remained ever since. The decline in nesting Great Black-backed Gulls was due primarily to mortality from Type E botulism that affected that species to a greater degree than other gull species, probably because of their superior ability to dominate and scavenge toxin-laden carrion. Temporal changes in routes and efficiency of botulinum toxin transfer likely explain why Great Black-back Gulls were initially able to colonize Lake Ontario, but have undergone extirpation in recent times. Our results illustrate how changes in disease prevalence in the Great Lakes can degrade environmental quality to the extent that some species simply cannot persist. Received 18 Nov 2020, accepted 14 Feb 2021.
Understanding changes in environmental mercury concentrations is important for assessing the risk to human and wildlife populations from this potent toxicant. Here, we use herring gull (Larus argentatus) eggs to evaluate temporal changes in total mercury (THg) availability from two locations on Great Slave Lake (GSL), Northwest Territories, Canada. Egg THg concentrations increased through time, but this change was due to shifts in gull diets. Stable nitrogen isotopes allowed adjustment of egg THg concentrations for dietary changes. Diet-adjusted egg THg concentrations showed no long-term trend. Consistent with that result, new statistical analysis of THg concentrations in three species of GSL fish showed minor or no temporal changes. Although a long-term trend was absent, inter-year differences in adjusted egg THg concentrations persisted. Contributions of environmental variables (i.e., river flow, lake level, air temperature, precipitation, and wildfire) to these differences were investigated. Egg THg concentrations were greater following years of lower lake levels and greater wildfire extent. Lake level could have affected mercury methylation. Increased wildfire could have enhanced terrestrial Hg releases to the atmosphere where it was transported long distances to GSL. Climate change may increase wildfire extent with impacts on Hg bioaccumulation in northern ecosystems. Egg Hg levels reported here are unlikely to pose health risks to gulls, but in light of ongoing environmental change, monitoring should continue. Our study emphasizes the importance of ancillary datasets in elucidating Hg trends; such information will be critical for evaluating the effectiveness of Hg mitigation strategies implemented as part of the Minamata Convention.
The diet of Peregrine Falcons (Falco peregrinus) largely consists of live avian prey (Cade et al. 1982, White et al. 2020). Scavenging of carcasses has been documented but usually on land adjacent to marine ecosystems (Beebe 1960, Holland 1989, Buchanan 1991, Henny and Pagel 2003, Varland et al. 2018). This could possibly reflect the relatively high availability of carcasses associated with productive marine systems and their preservation in low temperature waters (Varland et al. 2018). Scavenging has only rarely been reported from non-marine ecosystems (see Holland 1989, Dekker 1999) and is absent from the literature for eastern North America. Here, we report one such example from Lake Superior, the largest of the five Laurentian Great Lakes. In 2018, there were 52 occupied Peregrine Falcon territories (46 territorial pairs, 6 single adults on territory) on the Ontario side of Lake Superior (Thunder Bay Field Naturalists 2018). Included in this total were six occupied peregrine territories in Pukaskwa National Park, three of which produced eggs, nestlings, or fledglings (Adair 2018). As part of research examining factors regulating Herring Gull (Larus argentatus) populations on Lake Superior (Laurich et al. 2019), we monitored Herring Gull nest attentiveness using infrared remote cameras (Reconyx PC900 professional). Cameras were programmed to take one photograph per minute, 24 hr/d, at each nest. All necessary permits for this work were obtained from Environment and Climate Change Canada (CA 0304 Amend 2) and the Parks Canada Agency (PUK-201827697). Here, we focus on results from a camera installed adjacent to a Herring Gull nest on Gull Rock, Lake Superior (48836.54N, 86820.64W), within Pukaskwa National Park, on 17 May 2018. The female occupying that nest had finished laying, as she had produced a 3-egg clutch, the usual maximum clutch size for this species (Nisbet et al. 2020). Male and female Herring Gulls share incubation duties and, at this nest, they incubated continuously until 21 May 2018. On that date, as the day progressed, the incubating female became increasingly lethargic but remained on the nest (Fig. 1A). She showed no sign of physical trauma. Problems associated with egg production were unlikely as the female had finished laying. At approximately 2025 H (EDT), the female died on the nest while incubating (Fig. 1B). Her body remained there (Fig. 1C) until 1658 H on 25 May 2018 when an adult Peregrine Falcon landed on the carcass. None of the preceding photographs showed the falcon, hence we could not gain insights into the falcon’s behavior prior to landing. The sex of the falcon was unknown but it may have been a female as their larger size allows them to take larger prey (White et al. 2020). Local (Marathon, ON) female Herring Gulls have a mean mass of 937 6 63 (SD) g (C. Hebert unpubl. data), which is near the maximum size of prey usually taken by female falcons and is much greater than that taken by males (White et al. 2020). The falcon decapitated and de-feathered the pectoral area of the gull and proceeded to feed on the gull in the nest (Fig. 1D). Over an 86-min period, the falcon fed continuously, then departed at 1824 H. The eggs in the nest were not disturbed. At 1825 H, the male gull returned and at 1833 H he removed the carcass from the nest, revealing the complete consumption of the pectoralis muscle and extensive consumption of internal organs. Afterward, the 1 Email address: craig.hebert@canada.ca
Egg quality (size, energy density) is important in determining early survival of birds. Here, we examine temporal (1981–2019) trends in herring gull (Larus argentatus) egg volume and energy density at breeding colonies on all five Laurentian Great Lakes. Temporal declines in egg volume were observed at 4/6 colonies on the upper Great Lakes (Lakes Superior, Michigan, Huron). On the lower Great Lakes (Lakes Erie, Ontario, and connecting channels) egg volume declined at 3/8 colonies and increased at one site. Egg energy density (kJ/g of egg contents) declined at 4/6 upper Great Lakes colonies and at 2/8 lower Great Lakes colonies. All of the upper Great Lakes colonies showed declines in either egg volume or energy density, or both, and these declines were related to dietary markers in eggs (fatty acids, stable nitrogen and carbon isotopes). On the lower Great Lakes and connecting channels, declines in egg volume or energy density were related to dietary endpoints in 3/5 instances. An information-theoretic approach indicated that trends in egg volume were best explained at the colony level while egg energy density trends were best explained by lake of origin. Diet-related declines in herring gull egg quality are likely a reflection of broad-scale ecosystem changes limiting aquatic food availability for gulls, particularly on the upper Great Lakes. These changes may be contributing to population declines in herring gulls and other surface-feeding aquatic birds. This study highlights the value of long-term monitoring of wildlife for identifying ecosystem change.
This study examined factors contributing to temporal variability (2009-2017) in total mercury (THg) concentrations in aquatic bird eggs collected in the Peace-Athabasca Delta and Lake Athabasca in northern Alberta. Factors examined included annual changes in oil sands production, bird diets, forest fires, and flow of the Athabasca River. Surface mining activities associated with Alberta’s Athabasca oil sands are centered north of Fort McMurray, Alberta, adjacent to the northward-flowing Athabasca River. Previous studies have found that oil sands industrial operations release mercury into the local (within ~50 km) environment. However, temporal trends in egg THg levels did not track trends in synthetic oil production from the oil sands. Intraspecific fluctuations in bird diet also could not explain annual variability in egg THg levels. Annual extent of forest fires in Alberta was only related to egg THg concentrations in California Gulls from Lake Athabasca; annual levels in other species showed no relationship with fire extent. The inclusion of more terrestrial foods in gull diets may have contributed to this difference. For the majority of species, annual fluctuations in maximal flow of the Athabasca River were important in influencing annual egg THg levels. Eggs collected following years of high flow had higher THg concentrations with distinct stable Hg isotope compositions. Riverine processes associated with suspended sediment were likely critical in regulating Hg availability to nesting birds. This study highlights the importance of the Athabasca River as a conduit for Hg transport to ecologically-sensitive downstream ecosystems such as the Peace-Athabasca Delta and Wood Buffalo National Park (a UNESCO World Heritage Site). Human activities that increase atmospheric Hg deposition to the Athabasca River watershed, or that enhance Hg releases to the river through erosion of Hg-bearing soils, will likely increase the availability of Hg to organisms inhabiting downstream areas.
The occurrence of tetrabromobisphenol-A-bis(2,3,-dibromopropyl ether) (TBBPA-BDBPE) flame retardant is generally unknown in wildlife. A highly sensitive, gas chromatography-mass spectrometry-based method was developed for TBBPA-BDBPE with optimized parameters for large volume injection. We report on TBBPA-BDBPE and temporal and spatial trends in herring gull egg pools and individuals from 14 colony sites across the Laurentian Great Lakes of North America. TBBPA-BDBPE identification was confirmed using liquid chromatography time-of-flight mass spectrometry and quantification with liquid chromatography tandem mass spectrometry analysis. TBBPA-BDBPE was quantifiable in 95% of egg pools from all colonies sampled in 2013-2017, and retrospective analysis of archived eggs (2001-2017) at 3 of the 14 colonies indicated that TBBPA-BDBPE concentrations were greater in pools from eggs collected in more recent years (<MLOD to 42.8 ng/g wet weight (ww)). For individual eggs, the concentration range was <MLOD to 497 ng/g ww. Individual eggs from 2 other herring gull colonies, north and south Pukaskwa National Park, Lake Superior, were analyzed for TBBPA-BDBPE, and dietary markers (fatty acids) revealed possible exposure pathways. Selected colonies with known dietary differences (i.e., terrestrial versus aquatic) indicated that TBBPA-BDBPE exposure was associated with terrestrial origin. Herring gull regurgitates and feces were collected from several colonies with TBBPA-BDBPE ranging from <MLOD to 21.7 ng/g dry weight (dw) and <MLOD to 16.3 ng/g ww, respectively. Typical of many alternate flame retardants in wildlife, TBBPA-BDBPE levels in the gull samples were low with a few high values and increasing prevalence through time.