Do songbirds in wetlands show higher mercury bioaccumulation relative to conspecifics in non-wetland habitats?

Environmental conditions in wetlands facilitate favorable biogeochemical conditions for the conversion of inorganic mercury into methylmercury. For this reason, wetlands are increasingly classified as mercury hotspots, places where biota exhibit elevated mercury concentrations. While it is clear that wetlands play an important role in methylmercury production, factors such as geographic variation in mercury deposition, wetland type, and trophic dynamics can cause variation in mercury dynamics and bioaccumulation in biota occupying wetlands or connected to wetland trophic systems. Here, we use songbirds as bioindicators in a two-pronged approach aimed at evaluating the state of our understanding of mercury bioaccumulation by songbirds in wetland ecosystems. First, we use a case study in southeast Missouri to compare blood mercury concentrations in tree swallows (Tachycineta bicolor) and eastern bluebirds (Sialia sialis) occupying wetland and non-wetland habitats to test the hypothesis that songbirds in wetlands will have higher mercury bioaccumulation than those in non-wetlands. Adult tree swallows in wetlands had significantly higher blood mercury concentrations than those in non-wetlands; however, no difference between ecosystems was detected in eastern bluebirds. Second, we present a review of the current literature on mercury in songbirds in wetland ecosystems across North America. Mercury concentrations in songbirds varied among wetland types and with geographic location, often in an unpredictable manner. Mercury concentrations in songbird blood varied 3-10 fold at locations separated only by ~10 to several hundred kilometers. This magnitude of difference in blood mercury concentrations among wetlands exceeds documented differences between wetland and non-wetland ecosystems. Therefore, we caution against the automatic assumption that songbirds occupying wetlands will have higher mercury bioaccumulation than conspecifics living in other habitats.

Wetland water-management may influence mercury bioaccumulation in songbirds and ducks at a mercury hotspot.

Mercury is a persistent, biomagnifying contaminant that can cause negative behavioral, immunological, and reproductive effects in wildlife and human populations. We examined the role of wetland water-management on mercury bioaccumulation in songbirds and ducks at Kellys Slough National Wildlife Refuge Complex, near Grand Forks, North Dakota USA. We assessed mercury concentrations in blood of wetland-foraging songbirds (80 common yellowthroats [Geothlypis trichas] and 14 Nelson's sparrows [Ammospiza nelsoni]) and eggs of upland-nesting ducks (28 gadwall [Mareca strepera], 19 blue-winged teal [Spatula discors], and 13 northern shoveler [S. clypeta]) across four wetland water-management classifications. Nelson's sparrow blood mercury concentrations were elevated (mean: 1.00 µg/g ww; 95% CL: 0.76-1.31) and similar to those reported 6 years previously. Mercury in songbird blood and duck eggs varied among wetland water-management classifications. Songbirds and ducks had 67% and 49% lower mercury concentrations, respectively, when occupying wetlands that were drawn down with water flow compared to individuals occupying isolated-depressional wetlands with no outflow. Additionally, songbirds within impounded and partially drawn-down wetland units with water flow had mercury concentrations that were 26-28% lower, respectively, than individuals within isolated-depressional wetlands with no outflow. Our results confirm that mercury concentrations in songbirds at Kellys Slough continue to be elevated and suggest that water-management could be an important tool for wetland managers to reduce bioaccumulation of mercury in birds.

Genomics of rapid ecological divergence and parallel adaptation in four tidal marsh sparrows.

Theory suggests that different taxa having colonized a similar, challenging environment will show parallel or lineage-specific adaptations to shared selection pressures, but empirical examples of parallel evolution in independent taxa are exceedingly rare. We employed comparative genomics to identify parallel and lineage-specific responses to selection within and among four species of North American sparrows that represent four independent, post-Pleistocene colonization events by an ancestral, upland subspecies and a derived salt marsh specialist. We identified multiple cases of parallel adaptation in these independent comparisons following salt marsh colonization, including selection of 12 candidate genes linked to osmoregulation. In addition to detecting shared genetic targets of selection across multiple comparisons, we found many novel, species-specific signatures of selection, including evidence of selection of loci associated with both physiological and behavioral mechanisms of osmoregulation. Demographic reconstructions of all four species highlighted their recent divergence and small effective population sizes, as expected given their rapid radiation into saline environments. Our results highlight the interplay of both shared and lineage-specific selection pressures in the colonization of a biotically and abiotically challenging habitat and confirm theoretical expectations that steep environmental clines can drive repeated and rapid evolutionary diversification in birds.

Subspecies delineation amid phenotypic, geographic and genetic discordance in a songbird.

Understanding the processes that drive divergence within and among species is a long-standing goal in evolutionary biology. Traditional approaches to assessing differentiation rely on phenotypes to identify intra- and interspecific variation, but many species express subtle morphological gradients in which boundaries among forms are unclear. This intraspecific variation may be driven by differential adaptation to local conditions and may thereby reflect the evolutionary potential within a species. Here, we combine genetic and morphological data to evaluate intraspecific variation within the Nelson's (Ammodramus nelsoni) and salt marsh (Ammodramus caudacutus) sparrow complex, a group with populations that span considerable geographic distributions and a habitat gradient. We evaluated genetic structure among and within five putative subspecies of A. nelsoni and A. caudacutus using a reduced-representation sequencing approach to generate a panel of 1929 SNPs among 69 individuals. Although we detected morphological differences among some groups, individuals sorted along a continuous phenotypic gradient. In contrast, the genetic data identified three distinct clusters corresponding to populations that inhabit coastal salt marsh, interior freshwater marsh and coastal brackish-water marsh habitats. These patterns support the current species-level recognition but do not match the subspecies-level taxonomy within each species-a finding which may have important conservation implications. We identified loci exhibiting patterns of elevated divergence among and within these species, indicating a role for local selective pressures in driving patterns of differentiation across the complex. We conclude that this evidence for adaptive variation among subspecies warrants the consideration of evolutionary potential and genetic novelty when identifying conservation units for this group.

Characterization of mercury and its risk in Nelson's, Saltmarsh, and Seaside Sparrows.

BACKGROUND: Nelson's, Saltmarsh, and Seaside Sparrows (Ammodramus nelsoni, A. caudacutus, and A. maritimus, respectively) depend on marsh and wetland habitats--ecosystems in which mercury (Hg) bioavailability is notoriously high. The purpose of the present study was to address the potential impact of Hg on these species using first primary and breast feathers as non-destructive biomonitoring tools. METHODS AND PRINCIPAL FINDINGS: Feathers were sampled from wintering sparrows in North Carolina salt marshes (2006-2010). Feather Hg data were used in three risk analysis components (1) Threshold Component--examined feather Hg with regard to published negative effects thresholds; (2) Hg Dynamics Component--examined Hg in sparrows captured multiple times; and (3) Capture Frequency and Survival Component--tested for links between Hg and return frequency and survival. Threshold Component analyses indicated that Hg concentrations in 42-77% of sampled individuals (breast feather n = 879; first primary feather n = 663) were within the range associated with decreased reproduction in other avian species. Hg Dynamics Component analyses demonstrated that Hg increased between first and second captures for Nelson's (n = 9) and Seaside Sparrows (n = 23). Capture Frequency and Survival Component analyses detected a negative relationship between Hg and capture frequency in Nelson's Sparrows (n = 315). However, MARK models detected no effect of Hg on apparent survival in any species. CONCLUSION AND SIGNIFICANCE: This study indicates that current Hg exposure places a considerable proportion of each population at risk. In particular, 52% of all sampled Saltmarsh Sparrows exhibited first primary feather Hg concentrations exceeding those associated with a >60% reduction in reproductive success in other species. This study reports evidence for net annual bioaccumulation, indicating an increased risk in older individuals. These data can be used to inform future population assessments and management for these species.

Mercury in Nelson's Sparrow subspecies at breeding sites.

BACKGROUND: Mercury is a persistent, biomagnifying contaminant that can cause negative effects on ecosystems. Marshes are often areas of relatively high mercury methylation and bioaccumulation. Nelson's Sparrows (Ammodramus nelsoni) use marsh habitats year-round and have been documented to exhibit tissue mercury concentrations that exceed negative effects thresholds. We sought to further characterize the potential risk of Nelson's Sparrows to mercury exposure by sampling individuals from sites within the range of each of its subspecies. METHODOLOGY/PRINCIPAL FINDINGS: From 2009 to 2011, we captured adult Nelson's Sparrows at sites within the breeding range of each subspecies (A. n. nelsoni: Grand Forks and Upham, North Dakota; A. n. alterus: Moosonee, Ontario; and A. n. subvirgatus: Grand Manan Island, New Brunswick) and sampled breast feathers, the first primary feather (P1), and blood for total mercury analysis. Mean blood mercury in nelsoni individuals captured near Grand Forks ranged from 0.84 ± 0.37 to 1.65 ± 1.02 SD ppm among years, between 2.0 and 4.9 times as high as concentrations at the other sites (P<0.01). Breast feather mercury did not vary among sites within a given sampling year (site means ranged from 0.98 ± 0.69 to 2.71 ± 2.93 ppm). Mean P1 mercury in alterus (2.96 ± 1.84 ppm fw) was significantly lower than in any other sampled population (5.25 ± 2.24-6.77 ± 3.51 ppm; P ≤ 0.03). CONCLUSIONS/SIGNIFICANCE: Our study further characterized mercury in Nelson's Sparrows near Grand Forks; we documented localized and potentially harmful mercury concentrations, indicating that this area may represent a biological mercury hotspot. This finding warrants further research to determine if wildlife populations of conservation or recreational interest in this area may be experiencing negative effects due to mercury exposure. We present preliminary conclusions about the risk of each sampled population to mercury exposure.

Understanding associations between nitrogen and carbon isotopes and mercury in three Ammodramus sparrows.

We analyzed nitrogen and carbon stable isotope ratios and mercury (Hg) in breast feathers from three species of closely related sparrows, Saltmarsh, Seaside, and Nelson's Sparrows (Ammodramus caudacutus, A. maritimus, and A. nelsoni, respectively), to assess if trophic position and food web structure influence Hg exposure in these species. Sparrows were captured during the non-breeding season from 2006 to 2008 in North Carolina salt marshes near Wrightsville Beach, New Hanover County. Generalized linear models were used to test for the influence of species, δ(15)N, and δ(13)C on breast feather Hg. The most parsimonious model included species, δ(15)N, and their interaction term and explained 36% of the variation in breast feather Hg. Each species exhibited a different association between breast feather δ(15)N and Hg with Seaside Sparrows showing a positive correlation (r=0.27, P=0.03), Nelson's Sparrows a negative correlation (r=-0.28, P=0.01), and Saltmarsh Sparrows with no significant association. For Saltmarsh Sparrows, δ(15)N and Hg revealed decoupling between breast feather Hg and trophic position. Our results demonstrate that the influence of δ(15)N on breast feather Hg is likely indicative of geographic variation in δ(15)N baselines rather than trophic position.

Mercury in non-breeding sparrows of North Carolina salt marshes.

We captured Nelson's, Saltmarsh and Seaside Sparrows (Ammodramus nelsoni, A. caudacutus and A. maritimus) at three salt marsh sites near Wrightsville Beach, North Carolina during five non-breeding seasons (September through April, 2006-2011). We analyzed breast feather samples from all of these seasons and blood and first primary feather (P1) samples from three seasons (2008-2011) for mercury (Hg). Generalized linear models were used to test for the impact of species, season, site and month on blood Hg, species, season and site on P1 Hg and species and season on breast feather Hg. The best-fit model for blood indicated that Hg varied among species, seasons and months. Saltmarsh Sparrows maintain higher blood Hg than Nelson's and Seaside Sparrows during the non-breeding season while they are feeding in mixed flocks. In Nelson's and Seaside Sparrows, blood Hg decreased during mid-winter compared to early fall and late spring. Breast feather and P1 Hg varied among species with Saltmarsh Sparrows exhibiting higher concentrations than the other two species, while Nelson's Sparrows had lower concentrations than the other two species. Breast feather Hg was higher in the final three seasons than in the first two. Our results indicate that Hg exposure on breeding sites may be increasing and that high levels of Hg exposure during the breeding season may affect blood Hg concentrations year-round in Saltmarsh Sparrows. Our data thus provide a baseline for future Hg assessments in these species in NC.

Fluoxetine effects on sheepshead minnow (Cyprinodon variegatus) locomotor activity.

Fluoxetine (FLX), a selective serotonin reuptake inhibitor, is among the top 100 drugs prescribed annually in the United States and the United Kingdom and is one of many pharmaceutical products that have been detected in global surface waters. Our study used sublethal concentrations to assess the impact of FLX exposure on sheepshead minnow (Cyprinodon variegatus) locomotor behavior. Exposures lasted for 56 hours, and fish were recorded for locomotor behavior assessment at six timepoints between 1-56 h post-dose. Behavior was recorded to quantify locomotor activity using line crossing counts. Animals treated with 300 µg L(-1) FLX exhibited reduced locomotor activity at 1, 25, 32, 49 and 56 h post-dose. An EC(25) value of 2 µg L(-1) (lower and upper 95 % confidence limits at 1.3, 43 µg L(-1), respectively) was determined for locomotor activity at 32 h of exposure. Changes in locomotor activity due to FLX exposure may have implications for the ecological response of populations to other natural and anthropogenic stressors.