Trends in hepatic cadmium concentrations in marine bird species from the Canadian Arctic.

Cadmium (Cd) is a trace element of toxicological concern that has been monitored in marine birds inhabiting the Canadian Arctic since 1975. Despite nearly 50 years of monitoring, research to date has largely evaluated single species, locations, or time points, and there is as of yet no holistic overview that jointly considers all available Cd data. We addressed this information gap by combining and analyzing most of the existing data on hepatic Cd concentrations in marine birds from the Canadian Arctic. Using data collected between 1975 and 2018 from eight seabird species from 12 Arctic breeding colonies, we examined temporal, spatial, and interspecific variation in hepatic Cd levels, and we evaluated possible drivers of marine bird Cd loads. Hepatic Cd concentrations ranged from 1.6 to 124 µg/g dry weight across species, and were highest in thick-billed murres (Uria lomvia) and king eiders (Somateria spectabilis), and lowest in black guillemots (Cepphus grylle), black-legged kittiwakes (Rissa tridactyla), and long-tailed ducks (Clangula hyemalis). All sites with multiple years of data showed interannual fluctuations in Cd, which were correlated with the North Atlantic Oscillation (NAO) index and with the previous year's June sea ice coverage, where marine birds exhibited higher Cd concentrations in positive NAO years and following years with lower sea ice coverage. Climate change is likely to shift the NAO to being more negative and to reduce sea ice coverage, and our results thus identify various ways by which climate change could alter Cd concentrations in marine birds in the Canadian Arctic. Understanding variations in marine bird contaminant burdens, and how these may be alters by other stressors such as climate change, is important for long-term marine bird conservation efforts.

Polycyclic Aromatic Hydrocarbons Alter the Hepatic Expression of Genes Involved in Sanderling (Calidris alba) Pre-migratory Fueling.

Polycyclic aromatic hydrocarbons (PAHs) impaired pre-migratory fueling in 49 orally dosed Sanderling (Calidris alba). In the present study, 8 genes related to fat deposition and PAH exposure were measured in liver subsamples from these same shorebirds. At the highest dose (1260 µg total PAH [tPAH]/kg body wt/day), PAH exposure decreased liver basic fatty acid binding protein 1 (Lbfabp) and hepatic lipase (Lipc) expression. The present study reveals candidate molecular-level pathways for observed avian pre-migratory refueling impairment. Environ Toxicol Chem 2021;40:1983-1991. © 2021 SETAC.

Species traits predict the aryl hydrocarbon receptor 1 (AHR1) subtypes responsible for dioxin sensitivity in birds.

Differences in avian sensitivity to dioxin-like compounds (DLCs) are directly attributable to the identities of amino acids at two sites within the ligand binding domain (LBD) of the aryl hydrocarbon receptor 1 (AHR1). Recent work suggests that by influencing avian exposure to naturally occurring dioxins, differences in diet, habitat, and migration may have influenced the evolution of three AHR1 LBD genotypes in birds: type 1 (high sensitivity), type 2 (moderate sensitivity), and type 3 (low sensitivity). Using a boosted regression tree (BRT) analysis, we built on previous work by examining the relationship between a comprehensive set of 17 species traits, phylogeny, and the AHR1 LBD across 89 avian species. The 17 traits explained a combined 74% of the model deviance, while phylogenetic relatedness explained only 26%. The strongest predictors of AHR1 LBD were incubation period and habitat type. We found that type 3 birds tended to occupy aquatic habitats, and, uniquely, we also found that type 3 birds tended to have slower developmental rates. We speculate that this reflects higher evolutionary exposure to naturally occurring dioxins in waterbirds and species with K-selected life histories. This study highlights the value of trait-based approaches in helping to understand differing avian species sensitivities to environmental contaminants.

Drivers of declines in common loon (Gavia immer) productivity in Ontario, Canada.

Common loons (Gavia immer) are top predators that depend on lake food webs to successfully fledge chicks. Common loon reproductive success is consequently recognized as an important indicator of aquatic ecosystem health. Existing evidence points to long-term declines in productivity in portions of the common loon range; however, the reason for these declines is not well understood. Our objectives were to define underlying baseline patterns of loon reproductive success in Ontario, Canada, and to identify drivers of temporal changes in loon productivity. We analyzed 38 years of reproductive data from over 1500 lakes using data from the Canadian Lakes Loon Survey, a citizen science loon monitoring program managed by Birds Canada that has run annually in Ontario since 1981. Overall, we estimated a declining trend in common loon reproductive success of -0.10 six-week-old young per pair per year in Ontario between 1981 and 2018. We assessed the influence of 14 factors on loon reproductive success. We identified low pH and associated higher mercury as factors linked to loon productivity declines. We also demonstrated that lake area, longitude, and April temperatures can predict the number of six-week-old young per pair per year. We hypothesize that climate change-induced stress, acting through multiple interacting pathways involving mercury acidity, fish abundance, lake size, and geographic location, may account for declining loon productivity. These results will be important for focusing future research and conservation efforts to help understand and mitigate threats to common loon populations.

Assessment of Shorebird Migratory Fueling Physiology and Departure Timing in Relation to Polycyclic Aromatic Hydrocarbon Contamination in the Gulf of Mexico.

Shorebirds depend on staging sites in the Gulf of Mexico that are frequently subject to pollution by oil and its toxic constituents, polycyclic aromatic hydrocarbons (PAHs). It was hypothesized that PAH contamination lowers staging site quality for migratory shorebirds, with consequences for fueling and departure timing. Sediment total PAH concentrations were measured at six staging sites along the Texas and Louisiana Gulf Coast. Sites in Louisiana were expected to have higher total PAH concentrations as they were more heavily impacted by the Deepwater Horizon oil spill. From 2015 to 2017, 165 Sanderling ( Calidris alba) and 55 Red knots ( C. canutus) were captured at these same sites during their northward migration (late April to mid May). Mass, body morphometrics, and plasma metabolite measurements were taken to determine fuel loads and fueling rates, and a subset of birds (120 Sanderling and 39 Red knots) received a coded radio tag to determine departure dates using the Motus telemetry array. Compared to Texas sites, sediment in Louisiana had higher total PAH concentrations, dominated by heavier 6 ring indeno[1,2,3- cd]pyrene (48%). Plasma metabolite profiles suggested that fueling rates for Sanderling, but not Red knots, tended to be lower in Louisiana, and both species departed later than the study average from Louisiana. However, multiple factors, including migration patterns, food supply, and other contaminants, also likely influenced fueling and departures. PAH contamination in the Gulf of Mexico remains an ongoing issue that may be impacting the staging site quality and migration timing of long-distance migratory birds.

Polycyclic aromatic hydrocarbon exposure impairs pre-migratory fuelling in captively-dosed Sanderling (Calidris alba).

Efficient fuelling is essential for migratory birds because fuel loads and fuelling rates affect individual fitness and survival during migration. Many migrant shorebirds are exposed to oil pollution and its toxic constituents, polycyclic aromatic hydrocarbons (PAHs), at migratory staging sites, which has the potential to interfere with avian refuelling physiology. In this study, we orally dosed shorebirds with environmentally-relevant PAH mixtures to simulate dietary exposure during staging. Forty-nine wild-caught Sanderling (Calidris alba) were exposed to 0 (control), 12.6 (low), 126 (medium), or 1260 (high) µg total PAH/kg body weight/day. Birds were dosed during a 21-day period of autumn pre-migratory fuelling to mimic the typical staging duration of Sanderling. We measured daily changes in mass and fat loads, as well as ethoxyresorufin-O-deethylase (EROD) activity, serum biochemical profiles, and liver mass and lipid content following dosing. All dose groups gained fat and increased in mass (size-corrected) during the study period, with females having a higher average body mass than males. However, mass gain was 3.9, 5.4, and 3.8 times lower in the low, medium, and high dose groups, respectively, relative to controls, and body mass in the medium and high dose groups significantly declined near the end of the experiment. EROD activity showed a dose-dependent increase and was significantly elevated in the high dose group relative to controls. Higher individual EROD activity was associated with reduced serum bile acid and elevated serum creatine kinase concentrations in both sexes, and with elevated serum lipase concentrations in females. These results suggest that PAH exposure in Sanderling can interfere with mechanisms of lipid transport and metabolism, can cause muscle damage, and can lead to reduced overall fat loads that are critical to staging duration, departure decisions, migratory speed, and flight range. Given that many shorebirds migrate thousands of kilometers between the breeding and wintering grounds and frequently aggregate at key staging sites that are subject to contamination, PAH exposure likely represents a significant threat to shorebird migratory success.

The amphibious fish Kryptolebias marmoratus uses different strategies to maintain oxygen delivery during aquatic hypoxia and air exposure.

Despite the abundance of oxygen in atmospheric air relative to water, the initial loss of respiratory surface area and accumulation of carbon dioxide in the blood of amphibious fishes during emersion may result in hypoxemia. Given that the ability to respond to low oxygen conditions predates the vertebrate invasion of land, we hypothesized that amphibious fishes maintain O2 uptake and transport while emersed by mounting a co-opted hypoxia response. We acclimated the amphibious fish Kryptolebias marmoratus, which are able to remain active for weeks in both air and water, for 7 days to normoxic brackish water (15‰, ~21kPa O2; control), aquatic hypoxia (~3.6kPa), normoxic air (~21 kPa) or aerial hypoxia (~13.6kPa). Angiogenesis in the skin and bucco-opercular chamber was pronounced in air- versus water-acclimated fish, but not in response to hypoxia. Aquatic hypoxia increased the O2-carrying capacity of blood via a large (40%) increase in red blood cell density and a small increase in the affinity of hemoglobin for O2 (P50 decreased 11%). In contrast, air exposure increased the hemoglobin O2 affinity (decreased P50) by 25% without affecting the number of red blood cells. Acclimation to aerial hypoxia both increased the O2-carrying capacity and decreased the hemoglobin O2 affinity. These results suggest that O2 transport is regulated both by O2 availability and also, independently, by air exposure. The ability of the hematological system to respond to air exposure independent of O2 availability may allow extant amphibious fishes, and may also have allowed primitive tetrapods to cope with the complex challenges of aerial respiration during the invasion of land.

Hypoxia delays hematopoiesis: retention of embryonic hemoglobin and erythrocytes in larval rainbow trout, Oncorhynchus mykiss, during chronic hypoxia exposure.

In rainbow trout development, a switch occurs from high-affinity embryonic hemoglobin (Hb) and round, embryonic erythrocytes to lower-affinity adult Hb and oval, adult erythrocytes. Our study investigated the early ontogeny of rainbow trout blood properties and the hypoxia response. We hypothesized that hypoxia exposure would delay the ontogenetic turnover of Hb and erythrocytes because retention of high-affinity embryonic Hb would facilitate oxygen loading. To test this hypothesis we developed a method of efficiently extracting blood from individual embryos and larvae and optimized several techniques for measuring hematological parameters on microliter (0.5-2.0 µl) blood samples. In chronic hypoxia (30% of oxygen saturation), stage-matched embryos and larvae possessed half the Hb concentration, erythrocyte counts and hematocrit observed in normoxia. Hypoxia-reared larvae also had threefold to sixfold higher mRNA expression of the embryonic Hb α-1, ß-1 and ß-2 subunits relative to stage-matched normoxia-reared larvae. Furthermore, in hypoxia, the round embryonic erythrocytic shape persisted into later developmental stages. Despite these differences, Hb-oxygen affinity (P50), cooperativity and the Root effect were unaltered in hypoxia-reared O. mykiss. The data support our hypothesis that chronic hypoxia delays the ontogenetic turnover of Hb and erythrocytes, but without the predicted functional consequences (i.e. higher than expected P50). These results also suggest that the Hb-oxygen affinity is protected during development in chronic hypoxia to favor oxygen unloading at the tissues. We conclude that in early trout development, the blood-oxygen transport system responds very differently to chronic hypoxia relative to adults, possibly because respiration depends relatively more on oxygen diffusion than convection.

Acid water interferes with salamander-green algae symbiosis during early embryonic development.

The inner egg capsule of embryos of the yellow-spotted salamander (Ambystoma maculatum) are routinely colonized by green algae, such as Oophila amblystomatis, that supply O(2) in the presence of light and may consume nitrogenous wastes, forming what has been proposed to be a mutualistic relationship. Given that A. maculatum have been reported to breed in acidic (pH <5.0) and neutral lakes, we hypothesized that low water pH would negatively affect these symbiotic organisms and alter the gradients within the jelly mass. Oxygen gradients were detected within jelly masses measured directly in a natural breeding pond (pH 4.5-4.8) at midday in full sunlight. In the lab, embryo jelly masses reared continuously at pH 4.5 had lower P(O)2and higher ammonia levels relative to jelly masses held at pH 8.0 (control). Ammonia and lactate concentrations in embryonic tissues were approximately 37%-93% higher, respectively, in embryos reared at water pH 4.5 compared with pH 8.0. Mass was also reduced in embryos reared at pH 4.5 versus pH 8.0. In addition, light conditions (24 h light, 12L : 12D, or 24 h dark) and embryonic position (periphery vs. center) in the jelly mass affected P(O)2but not ammonia gradients, suggesting that algal symbionts generate O(2) but do not significantly impact local ammonia concentrations, regardless of the pH of the water. We conclude that chronic exposure to acidic breeding ponds had a profound effect on the microenvironment of developing A. maculatum embryos, which in turn resulted in an elevation of potentially harmful metabolic end products and inhibited growth. Under acidic conditions, the expected benefit provided by the algae to the salamander embryo (i.e., high O(2) and low ammonia microenvironment) is compromised, suggesting that the A. maculatum-algal mutualism is beneficial to salamanders only at higher water pH values.