Geographic and Seasonal Variation in Mercury Exposure of the Declining Rusty Blackbird

Home , Euphagus, Rusty blackbird

Geographic and Seasonal Variation in Mercury Exposure of the Declining Rusty Blackbird (Variación Geográfica y Estacional en la Exposición al Mercurio de la Especie en Disminución Euphagus carolinus) Author(s): Samuel T. Edmonds, David C. Evers, Daniel A. Cristol, Claudia Mettke-Hofmann, Luke L. Powell, Andrew J. McGann, Jacob W. Armiger, Oksana P. Lane, David F. Tessler, Patti Newell, Kathryn Heyden, and Nelson J. O'Driscoll Reviewed work(s): Source: The Condor, Vol. 112, No. 4 (November 2010), pp. 789-799 Published by: University of California Press on behalf of the Cooper Ornithological Society Stable URL: http://www.jstor.org/stable/10.1525/cond.2010.100145 . Accessed: 14/10/2012 16:02

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http://www.jstor.org Special Section: Rangewide Ecology of the Declining Rusty Blackbird 11/25/10 3:29:24 PM

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Warnell SchoolWarnell of Forestry, University E Green of Georgia, Street, 170 Athens, 30602 GA r e examined mercury concentrations in blood and feathers from the wetland obligate and rapidly de 8 T. W K. C. Irving Environmental Science Centre, Department of Earth and Environmental Sciences,

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. eog rnithological Society 2010 School of Natural Sciences and Psychology, Liverpool John Moores University, James Parsons Building, Key words: Key Resumen. Abstract. 4 Euphagus carolinus DOI L G . mérica del del mérica a m u e l p n feathers,n mercury concentrations insamples from the Vol. 112, 112, Vol. invernales mostraronreproductivas niveles de mercurio (0.07 en sangre μg g aproximadamente un orden de magnitud menor que los de aves I adverse effects on birds (8.26 μg g the contiguous en aves canoras,aves y las especies que se alimentan en humedales pueden estar ante unriesgo mayor de bioacumulación de mercurio que aquellas que viven enen otros cinco regiones a lo largo hábitats. de A and species that forage in wetlands may be at a greaterbioaccumulationmercurya risk at of beof wetlandsspecies other andin thatthanmay forage are thoseof habitats. (geometricg μg mean 0.94 concentrations we report in blood and feathers of theconcentrations feathers andreportof blood inwe blood mercuryblood approximately levels an ordermagnitude of than lower those breeding of birds μg g (0.07 provincias marítimas de C ores que las observadas en otras regiones. L vestres de paserinos de sitiosun sin colaborador una fuente potencial local en de la mercurio disminución conocida. drástica E de las poblaciones de esta especie en N las poblaciones de poblaciones las excedieron los niveles mínimos publicados para efectos adversos (8.26 μg g (media geométrica 0.94 μg g clining Rusty Blackbird ( of northeastern A y en dos áreas de reproducción en los bosques boreales occidentales de A the highestMercurymercury.thereportedpasserinesknown source populationswildlocal of withouta of sites for at dramaticinpopulationdeclinespecies’ potentialthecontributor toa consideredas be should Maritimemercuryhigh.areas bioavailabilityotherwhereprovincesinof is and [email protected] S u k e ooper O nfo.as L I he C urrentRenewableaddress: of School -mail: Institute Integrative for Bird Behavior Studies, Department of Biology, College of William and 23187 Mary, Williamsburg, VA 3 E C Manuscript received 30 July 2010; acceptedSeptember 9 2010. Manuscript2010; July 30 received 10 11 Condor, The allrequests permissionfor photocopyto reproduceor article content through the The Condor 112(4):789–799  T reprint 18_MS100145.indd 789 . a l

e t dmonds rnithological Society, 2010 xposure of the RustythexposureBlackbird of E . E T ooper O Mercury Samuel he C 0 0 0 0 30 July 2010 9 September 2010 © T 2010 790 SAMUEL T. EDMONDS e t a l .

INTRODUCTION and urban areas. While breeding they eat both terrestrial and

d aquatic invertebrates; during the autumn and winter their diet The Rusty Blackbird (Euphagus carolinus) has experienced

r includes a greater percentage of vegetable matter (primarily i a population decline of >85% since the 1960s and, on the ba- seeds and tree mast; Beal 1900, Ellison 1990, Avery 1995). b sis of the Breeding Bird Survey, may be losing population at a Consumption of organisms high in the food web and foraging rate of −13% per year, a rate of decline exceeding that of other in acidic wetlands favorable for Hg methylation could predis- boreal breeding birds (Greenberg and Droege 1999, Niven et pose this species to higher MeHg exposure. Our objectives for al. 2004, Sauer et al. 2008). Several factors have been pro- this study were to determine if Rusty Blackbirds accumulate posed as possible drivers for this dramatic population loss, in- MeHg to levels that are known to have negative effect on fit- cluding anthropogenic effects on both breeding and wintering ness and to determine whether there are geographic or sea- habitat, climate change, and increases in environmental con- ty Black ty sonal variations in their MeHg exposure.

s taminants, but there is no consensus (Greenberg et al. 2011). Environmental mercury (Hg) pollution has been blamed for METHODS reduced productivity of birds of both aquatic and terrestrial habitats (Brasso and Cristol 2008, Burgess and Meyer 2008), Study sites and Hg has been shown to accumulate in songbirds from a va- We collected samples from five regions across the range of riety of habitats (Evers et al. 2005, Rimmer et al. 2005, Shriver the Rusty Blackbird (Fig. 1). Breeding-season samples (May– et al. 2006). As the Rusty Blackbird has several character- July) came from sites across the Acadian forest ecoregion istics that may predispose it to a high uptake of Hg, and as of New England and the Canadian Maritimes (Maine, New the mechanism(s) for its population decline is not well under- Brunswick, New Hampshire, Nova Scotia, and Vermont) and eclining Ru eclining stood, we found it prudent to investigate the exposure of this from sites across the western boreal forests of Alaska. Winter- D disappearing species to this toxicant. range samples (December–April) came from three regions Heavy metals are well-known toxicants in the environ- of the U.S.: the Atlantic coastal plain (North Carolina, South ment, and even minimal exposures have been shown to cause Carolina, and Virginia), the central Ohio River valley in west- sublethal chronic effects in birds (Scheuhammer 1987). Un- ern and central Kentucky, and the Mississippi Alluvial Valley like most heavy metals, Hg can undergo both long-distance (Arkansas, Louisiana, and Mississippi). transport and biomagnification through food chains (Fitzger- ald et al. 1998). Hg is present in several forms in the environ- Tissue sampling

ment, such as Hg(0), Hg(II), and CH3Hg, with methylmercury We sampled blood and/or flight feathers from 579 Rusty (CH3Hg, hereafter MeHg) being the most toxicologically sig- Blackbirds for total Hg (includes organic and inorganic forms, nificant in birds because of its high bioavailability (Heinz hereafter THg) between 2005 and 2010. As Rusty Blackbirds

cology of the of cology 1974, Wolfe et al. 2007). Even in remote locations songbirds are territorial during the breeding season and gregarious in E can be exposed to Hg through atmospheric deposition (Rim- winter, we used different strategies for sampling on the breed- mer et al. 2005), and aquatic point-source contamination can ing and wintering grounds. In winter we targeted flocks and enter adjacent terrestrial food webs (Cristol et al. 2008). High acquired many replicate samples from fewer sites. Conversely, Hg levels in blood and feathers have been correlated with phys- we sampled breeding pairs at many different sites with less iological and reproductive effects in an insectivorous song- replication from each site. At all sites, birds were captured bird (Tree Swallow, Tachycineta bicolor; Brasso and Cristol in nylon mist nets (3 or 12 × 2.6 m, with 33-, 36-, or 61-mm 2008, Franceschini et al. 2009, Hawley et al. 2009, Wada et al. mesh). Breeding birds were often attracted with audio record- 2009). Mercury exposure through biomagnification depends ings and captured through the strategic placement of nets and upon several factors, including foraging guild, habitat, sea- decoys along observed flight paths.W intering blackbirds were son, and geographic region (Kidd et al. 1995, Evers et al. 2005, captured in mist nets; net sites were occasionally baited with Rimmer et al. 2009). Wildlife is at greater risk for Hg expo- a mix of boiled eggs and cracked corn set 2 to 4 days prior to sure in regions of higher atmospheric Hg deposition, such as attempts to net (described by Mettke-Hofmann et al. 2010). in the New England and Canadian Maritime region (Evers et Bait was quickly consumed, and telemetry suggests that indi- al. 2007), and at sites of point-source contamination (Cristol vidual birds spent little time at the bait stations (<10% of their et al. 2008, Hill et al. 2008). foraging time, Mettke-Hofmann, unpubl. data). Therefore, we The Rusty Blackbird breeds almost exclusively in forested assumed that the effect of the bait on THg concentrations in wetlands across Canada, Alaska, and northern New England circulating blood was limited. Individuals were banded with a (Avery 1995). It winters primarily in the southeastern U.S. unique U.S. Geological Survey band. in habitat with shallow standing water (Jaramillo and Burke Blood samples (20 to 70 μL) were collected from the cuta- 1999, Niven et al. 2004). Nonbreeding Rusty Blackbirds may neous ulnar vein in a heparinized capillary tube, stored on ice

Special Section: Rangewide Section: Special be less selective about habitat use and are sometimes found in a Vacutainer, and frozen within 24 hr until analysis. Blood in drier habitats such as pecan orchards, agricultural fields, THg concentrations represent uptake of MeHg during the

18_MS100145.indd 790 11/25/10 3:29:26 PM MERCURY EXPOSURE OF THE RUSTY BLACKBIRD 791 Special Section: Rangewide E cology of the

Figure 1. Regions and sites serving as sources of Rusty Blackbird tissue for analysis of mercury (Hg).

previous days or weeks (Evers et al. 2005, Hill et al. 2008). portion of each feather was weighed to the nearest 0.1 mg and D

One to two flight feathers (first primary or second secondary) placed directly in a combustion boat. THg was determined eclining Ru were pulled or clipped at the calamus and stored in a plastic by EPA method 7473 (U.S. EPA 1998). Internal quality con- envelope until analysis. MeHg is bound to the feather’s protein trol included initial and continuing verification of calibration, matrix during its active growth, allowing for the sequestra- blanks, sample replication, and certified reference materi- tion and removal of the contaminant from the body (Dauwe als (DOLT-3, DOLT-4, and/or DORM-3, National Research et al. 2003). In the Rusty Blackbird, the annual pre-basic molt Council of Canada, Ottawa, Canada) every 10 to 15 samples. of flight and tail feathers follows breeding (Mettke-Hofmann The relative percent difference (RPD) for duplicate samples et al. 2010). THg concentrations in flight feathers, therefore, was 4 ± 2% SD (n = 17) for blood and 16 ± 20% SD (n = 44) should be similar year round and roughly indicate the burden for feathers. Mean recovery of certified reference materials of MeHg during feather growth in late summer. was 95% for each batch analyzed with an overall mean recov- s > ty Black ery of 102 ± 3% SD (n = 220). Laboratory analysis We analyzed a subsample of five blood and five feathers Using gold-amalgamation atomic absorption spectroscopy from 10 individuals for MeHg at Acadia University to con- with a Milestone DMA-80 or a Nippon MA-2000 direct Hg firm thatTH g in these tissues was representative of MeHg, as analyzer, we analyzed blood and feather samples for THg at demonstrated in previous studies (Evers et al. 2005, Rimmer Acadia University, Nova Scotia; BioDiversity Research In- et al. 2005, Wada et al. 2009). Each sample was weighed to the

stitute, Maine; College of William and Mary, Virginia; and nearest 0.1 mg, digested in 10 mL of 25% KOH/MeOH, shaken b i

Trace Element Research Lab at Texas A&M University, Texas. for 1 hr, and placed in a dry bath for 2 hr at 95 °C, methods r

Blood samples were thawed, expressed from capillary tubes similar to those of Cai and Bayona (1995). A sample aliquot d into combustion boats, and weighed to the nearest 0.1 mg. (20 μL) was transferred to a reaction bubbler and analyzed for Feathers were clipped at the calamus and at 1 to 2 cm from MeHg through ethylation and purge-and-trap gas chromatog- the distal end for use in other studies; the remaining central raphy prior to detection by atomic fluorescence spectrometry

18_MS100145.indd 791 11/25/10 3:29:30 PM 792 SAMUEL T. EDMONDS e t a l .

(Brooks Rand Model III) by EPA method 1630 (U.S. EPA concentrations in μg g−1 wet weight for blood and μg g−1 fresh

d 2001). Quality assurance included analytical sample replica- weight for feathers, ± SD.

r tion (RPD blood = 2 ± 1%; RPD feathers = 0.1 ± 0.05%), inter- In Alaska we concentrated our sampling at five distinct i nal standards, method blanks, and certified reference material study areas around the state (Fig. 1): Bethel (lower Yukon b (DOLT-4, mean recovery = 98 ± 4% SD, n = 3). River), Anchorage (lower Eagle River), Cordova (lower Cop- per River), Yukon Flats National Wildlife Refuge (NWR, up- Statistical analysis per Yukon River), and Fort Wainwright (lower Tanana River).

Data were log10-transformed prior to analysis to meet the as- We present THg concentrations in blood for each of these sumption of normality and normalize the residuals. We used five study areas for subregional comparison of Hg exposure, analysis of variance (ANOVA) with Tukey’s honestly signif- though sample sizes for some study areas were limited.

ty Black ty icant difference (HSD) to separately test for differences by s region in the means of THg concentrations in blood and feath- RESULTS ers. We used ordinary least-squares regression to separately test the relationship between THg in blood and feathers of We found both geographic and seasonal differences in THg breeding and wintering Rusty Blackbirds. Statistical analy- concentrations in blood of Rusty Blackbirds (Fig. 2, 3). Of the ses were run in SYSTAT 12.0 (SYSTAT 2007). We used α = five regions,TH g concentrations in blood were highest in the 0.05 to denote statistically relevant differences in population Acadian forests, with the single greatest concentration sam- means. Arithmetic and geometric means are provided for Hg pled in a male near Kejimkujik National Park in Nova Scotia eclining Ru eclining D cology of the of cology E

Figure 2. total Hg concentrations in μg g−1 wet weight (ww) Figure 3. total Hg concentrations in μg g−1 fresh weight (fw) in in blood of the Rusty Blackbird (Euphagus carolinus) from five re- feathers of the Rusty Blackbird (Euphagus carolinus) from five regions of North America on a log scale. Boxes are notched at the median gions of North America on a log10 scale. Boxes are notched at the 10 median and return to full width at the upper and lower limits of con- and return to full width at the upper and lower limits of confidence fidence intervals; outer limits of the box mark the lower and upper intervals; outer limits of the box mark the lower and upper quartiles. quartiles. Whiskers represent data within 1.5 H-spreads of the in- Whiskers represent data within 1.5 H-spreads of the interquartile terquartile range, asterisks represent outlier values between 1.5 and range, asterisks represent outlier values between 1.5 and 3 H-spreads, 3 H-spreads, and circles represent values beyond 3 H-spreads. The and circles represent values beyond 3 H-spreads. The horizontal Special Section: Rangewide Section: Special horizontal dashed line designates an estimated lower adverse-effects dashed line designates the minimum level for adverse effects on birds level of 1 μg g−1 for THg in Rusty Blackbird blood. recommended by Burger and Gochfeld (1997) for THg in feathers.

18_MS100145.indd 792 11/25/10 3:29:33 PM MERCURY EXPOSURE OF THE RUSTY BLACKBIRD 793 Special Section: Rangewide Table 1. Mean concentrations of total Hg in blood (μg g−1, wet weight) and feathers (μg g−1 fresh weight) of adult Rusty Blackbirds (Euphagus carolinus) by region. Overall means are weighted by regional sample sizes.

Blood Feathers

Arithmetic mean ± SD, 95% confidence Arithmetic mean ± SD, 95% confidence Study region or area (season) (n); geometric mean limits (n); geometric mean limits

Acadian forests (breeding) 1.06 ± 0.54 (59) 0.94 0.92; 1.20 19.57 ± 12.91 (45) 8.26 15.69; 23.46 Alaska: Anchorage (lower Eagle River, 0.30 ± 0.21 (53) 0.25 0.25; 0.36 — NA breeding) Alaska: Bethel (lower Yukon River, 0.15 ± 0.11 (9) 0.14 0.06; 0.23 3.45 ± 2.02 (10) 3.34 2.00; 4.89 breeding) Alaska: Cordova (lower Copper River, 0.18 ± 0.06 (3) 0.18 0.04; 0.33 — NA breeding) Alaska: Fort Wainwright (lower Tanana 0.59 ± 0.24 (25) 0.51 0.46; 0.66 2.04 ± 1.65 (3) 1.06 −2.05; 6.14 River, breeding) Alaska: Yukon NWR (upper Yukon 0.17 ± 0.12 (25) 0.15 0.12; 0.22 0.42 (1) 0.42 NA River, breeding) Alaska (breeding) 0.31 ± 0.24 (115) 0.25 0.27; 0.36 2.93 ± 2.03 (14) 1.11 1.76; 4.10 Atlantic coastal plains (wintering) 0.14 ± 0.19 (209) 0.10 0.11; 0.16 3.83 ± 2.95 (147) 2.29 3.35; 4.31 Central Ohio River valley (wintering) 0.07 ± 0.10 (31) 0.05 0.04; 0.11 3.98 ± 2.86 (31) 3.30 2.93; 5.02 Mississippi Alluvial Valley (wintering) 0.04 ± 0.04 (92) 0.03 0.03; 0.05 3.24 ± 3.06 (72) 2.04 2.52; 3.96 Overall breeding 0.57 0.51 (174) 0.39 0.49; 0.64 15.62 13.35 (59) 2.19 12.14; 19.10 ± ± E

Overall wintering 0.10 ± 0.17 (332) 0.07 0.09; 0.12 3.68 ± 2.97 (250) 2.30 3.31; 4.05 cology of the Overall mean 0.26 ± 0.39 (506) 0.12 0.23; 0.30 5.96 ± 7.93 (309) 2.26 5.07; 6.85

−1 (3.42 μg g wet weight, Table 1, F4,501 = 261.5, P < 0.001). THg were found along the lower Tanana River at Fort Wainwright, concentrations in blood were significantly higher in both re- with the maximum value for Alaska from a female sampled at gions of the breeding range examined than in either region of this site (1.11 μg g−1). the winter range, being at least 7× greater in the Acadian for- THg concentrations in feathers from the Acadian forests

ests than in either region of wintering (Table 2). differed from those of the other four regions (Table 2, F4,304 = Within Alaska, a comparison of 95% confidence limits 78.1, P < 0.001), being 3× to 7× greater than those observed for THg concentrations in blood suggests differences by sub- elsewhere (Table 1, 2). Other regions did not differ significantly,

region (Table 1). The greatest THg concentrations in blood except between the coastal plains and Mississippi Alluvial D eclining eclining Ru

Table 2. tukey’s pair-wise comparison of total Hg concentrations in blood (F4,501 = 261.5; P < 0.001) and feathers (F4,304 = 78.1; P < 0.001) of the Rusty Blackbird (Euphagus carolinus) by region.

Blood Feathers

Magnitude of Magnitude of Difference difference Difference difference between least- between between least- between

Regional comparison with direction of difference squares means geometric means squares means geometric means s ty ty Black Acadian forests > Alaska 0.59a 4× 0.85a 7× Acadian forests > Atlantic coastal plains 0.97a 7× 0.69a 4× Acadian forests > central Ohio River valley 1.31a 19× 0.68a 3× Acadian forests > Mississippi Alluvial Valley 1.53a 31× 0.81a 4× Alaska > Atlantic coastal plains 0.38a 3× −0.16c NA Alaska > central Ohio River valley 0.72a 5× −0.16c NA Alaska > Mississippi Alluvial Valley 0.95a 9× −0.04c NA Atlantic coastal plains > central Ohio River valley 0.34a 2× −0.01c NA b a b i Atlantic coastal plains > Mississippi Alluvial Valley 0.57 3× 0.12 1× r a c

Central Ohio River valley > Mississippi Alluvial Valley 0.23 2× 0.12 NA d aP < 0.05 bP < 0.1 cP > 0.1

18_MS100145.indd 793 11/25/10 3:29:35 PM 794 SAMUEL T. EDMONDS e t a l . d r i b ty Black ty s

Figure 4. Relationship between THg concentrations (μg g−1) in blood and feathers of breeding (a, R2 = 0.44) and wintering (b, R2 = 0.02) Rusty Blackbirds. Circles, birds breeding in the Acadian forest (a) or wintering on the Atlantic coastal plains (b); solid circles, birds breeding eclining Ru eclining in Alaska (a) or wintering in the Mississippi Alluvial Valley (b); solid squares, birds wintering in the central Ohio River valley (b). Center

D line is linear line of best fit; outer lines mark the upper and lower limits of the 95% confidence interval.

Valley, which differed minimally. We recorded the highest among the winter regions, implying similar exposures across THg concentrations (52 μg g−1 fresh weight) from two males, the breeding range. Yet we found that THg concentrations in one from northeastern Vermont near Maidstone, the other feathers from the Acadian forests were 3× to 4× greater than from northern Nova Scotia near Antigonish. in those from the winter range, suggesting that Hg exposure is Mean percent MeHg of THg was 98 ± 2% (n = 5) in blood higher in the far eastern portion of the breeding range within and 97 ± 0.3% (n = 5) in feathers. The relationship between the Acadian forests than in the rest of the boreal forest. Sam- THg concentrations in blood and feathers of individual breed- pling of the breeding population across the boreal forest is ing Rusty Blackbirds was significant and positive n( = 57, necessary to clarify this result. cology of the of cology F 42.6, R2 0.44, P 0.001, Fig. 4). For wintering Rusty The Hg in blood and feathers was nearly 100% MeHg, as E 1,55 = = < Blackbirds, the relationship was positive but not significant found in other species of birds (Thompson and Furness 1989, 2 (n = 179, F1,177 = 2.95, R = 0.02, P = 0.09). Evers et al. 2005, Rimmer et al. 2005, Wada et al. 2009). Thus our use of the more abundant THg data as a proxy for the pres- DISCUSSION ence of the highly bioavailable MeHg was valid. Additionally, the THg concentration in feathers was more tightly related to Mercury exposure in the Rusty Blackbird the THg concentration in the blood of breeding birds than it The concentrations of THg in blood and feather tissue sam- was to that in the blood of wintering birds, consistent with the pled from Rusty Blackbirds breeding in the Acadian forests idea that Rusty Blackbirds accumulate much of their Hg bur- were significantly greater than those from the other four re- den during the summer period between the arrival on breed- gions sampled. Our current understanding of Rusty Blackbird ing grounds and the onset of the pre-basic molt. Sampling of migration suggests an east–west divide along the Appalachian diet items throughout the year will be necessary to identify Mountains that corresponds to a population division in the timing and sources of Hg exposures. eastern boreal breeding range, a pattern currently considered THg concentrations in blood generally reflect exposure unique to this species, as the division in the breeding range is from the diet during the previous few days or weeks (Evers not centered along a natural physiographic feature (Hobson et et al. 2005, Hill et al. 2008). Consequently, the elevated THg al. 2010). Accordingly, we predicted THg concentrations in concentrations in the blood of breeding birds, particularly in feathers from the regions of the south-central U.S. examined the Acadian forests, likely reflected local Hg exposure. El- in this study (Mississippi Alluvial Valley and central Ohio evated Hg concentrations in the Acadian forests have been River valley) to reflectH g exposures from the western boreal found in other wildlife with continent-wide distributions, region and those from the southeastern region (coastal plains) such as the Common Loon (Gavia immer; Evers et al. 2003). Special Section: Rangewide Section: Special to reflectH g exposures from the eastern boreal region. We de- These elevated concentrations are likely due to biogeochem- tected little to no difference in THg concentrations in feathers ical conditions conducive to methylation in a region with a

18_MS100145.indd 794 11/25/10 3:29:37 PM MERCURY EXPOSURE OF THE RUSTY BLACKBIRD 795 Special Section: Rangewide higher rate of Hg deposition and retention (O’Driscoll et al. apparent spatial patterns of Hg in Rusty Blackbirds in Alaska 2005). Northeastern North America has historically received will require continued sampling. the downwind transport of industrial emissions from the Ohio River valley, the mid-Atlantic states, and elsewhere, conse- Comparison of mercury values in Rusty quently increasing the Hg levels observed in the environment and Red-winged Blackbirds (Evers and Clair 2005, Keeler et al. 2005). Accordingly, five To provide a context for interpreting the elevated Hg levels we biological hotspots for Hg exposure have been identified in the observed in Rusty Blackbirds breeding in northeastern North region, including the area in and around Kejimkujik National America, we obtained unpublished data on THg in blood and Park in Nova Scotia (Evers et al. 2007). feathers collected from breeding Red-winged Blackbirds Habitat type is important in determining Hg availability (Agelaius phoeniceus) in the same region. The Red-winged to a species (Evers et al. 2005), and recent research suggests and Rusty Blackbirds, both icterids, overlap broadly in range, that microhabitat plays a critical role as well (Eagles-Smith et habitat, diet (Jaramillo and Burke 1999), and pattern of flight- al. 2009). In general, the wetlands in the Acadian forests that feather molt (Pyle 1997). We queried data on Hg in blood typify the Rusty Blackbird’s breeding habitat are characterized and feathers of the Red-winged Blackbird from MercNet, a by high levels of dissolved organic carbon (average 9.23 mg comprehensive national Hg database representing available −1 L ) and low pH (average 5.78, n = 21, Edmonds, unpubl. data). government data that has been compiled and maintained by High levels of dissolved organic carbon and low pH have both the BioDiversity Research Institute (Gorham, Maine). We been correlated with increased methylation, bioavailability, bounded our query by filtering for region and habitat and and retention of Hg (Scheuhammer 1991, O’Driscoll et al. separating point from nonpoint sources of Hg (date of query 2005, 2006, Harding et al. 2006).

5 September 2009). The query yielded 59 Red-winged Black- E

The higher THg levels observed in the blood of breed- birds sampled on breeding grounds in the Northeast (New York, cology of the ing blackbirds could also reflect a seasonal trophic shift. Beal New England, and the Maritimes) and captured in wetland (1900) found that the stomachs of wintering Rusty Blackbirds habitat without a known point source for Hg pollution between contained primarily vegetable matter, including acorns, corn, May and August from 2003 to 2009 (Table 3). An additional and weed seeds, whereas those of breeding birds contained 21 samples were collected between 2003 and 2006 from wet- largely animal matter; four Rusty Blackbird stomachs col- lands along the Sudbury River in Massachusetts that were lected in August in Nova Scotia contained 97% insects and contaminated by industrial Hg (Wiener and Shields 2000). spiders. Anecdotally, we observed this change from a diet of We collected blood samples and analyzed them for THg by the insects in the breeding season to a broader diet in winter dur- same protocol as for the Rusty Blackbird; untrimmed flight ing our study. In winter, in addition to observing Rusty Black- feathers were collected and analyzed by the same protocol as birds occasionally foraging for invertebrates and small fish, for the Rusty Blackbird. we often observed them feeding on crushed pecans, acorns, THg concentrations in the blood of Rusty Blackbirds D and waste grain. In contrast, prey collected from captured breeding in the Acadian forest were approximately 4× the eclining Ru breeding adults included larvae of Diptera (flies), nymphs of Odonata (dragonflies), and larvae ofT richoptera (caddisflies), and we observed territorial birds foraging for emerging adult Table 3. total Hg concentrations (μg g−1) in blood and feathers Odonata and Ephemeroptera (mayflies; Edmonds, Newell, of adult Red-winged Blackbirds (Agelaius phoeniceus) breeding in wetlands, queried from MercNet database, BioDiversity Research and Tessler, unpubl. data). Institute (Gorham, Maine, 5 September 2009). While THg levels in the blood of breeding Rusty Black- birds in Alaska were lower than those found in the Acadian for- Source

ests, they were higher than those in the winter range and varied s New York, Industrially within Alaska. The seasonal change of Hg concentrations may ty Black New England, contaminated partially be explained by a change in diet, as suggested earlier. Maritime wetlands, Sudbury However, as the breeding diet is likely similar across Alaska, Tissue provinces River, Massachusetts the variation observed within that region suggests that local factors are also important in determining Hg burdens. Some Blood Arithmetic mean ± 0.39 ± 0.31 (50) 1.88 ± 2.97 (20) of the observed differences among sites may be due to (1) dif- SD (n) ferences in soil and water quality that enhance Hg methyla-

Geometric mean 0.22 0.53 b

tion (e.g., dissolved organic carbon and pH), (2) point-source 95% confidence limits 0.30; 0.48 0.48; 3.26 i Hg contamination, such as historic gold mining in some water- Feathers r sheds, (3) the addition of Hg to some watersheds via melting Arithmetic mean ± 1.08 ± 2.58 (40) 0.82 ± 0.62 (18) d permafrost (Klaminder et al. 2008), or (4) differences among SD (n) locales in the length of the food chain or the blackbird’s diet. Geometric mean 0.48 0.65 95% confidence limits 0.26; 1.91 0.51; 1.13 Determining the magnitude and underlying cause(s) of these

18_MS100145.indd 795 11/25/10 3:29:39 PM 796 SAMUEL T. EDMONDS e t a l .

geometric mean of those of breeding Red-winged Blackbirds species more closely related to the Rusty Blackbird than the

d from uncontaminated sites and twice those of Red-winged Red-winged Blackbird (Lanyon and Omland 1999)—had the

r Blackbirds from the contaminated site (Table 1, 3). THg con- lowest tolerance to lethal MeHg poisoning of three passerines, i centrations in feathers of the Rusty Blackbird were 17× higher including the Red-winged Blackbird. b than in those of breeding Red-winged Blackbirds away from Unfortunately, the egg-dosing study of Heinz et al. (2009) a point source and 13× higher than in those of Red-winged is not directly analogous to Hg deposition by a female into Blackbirds from the contaminated site. her egg; however, the study does suggest that blackbirds may We suspect that the differences in Hg concentrations be- be more sensitive during embryonic development than previ- tween the two species reflect differences in diet, the type of ously studied species such as waterfowl. There is currently no wetland the species uses, or both. Breeding Rusty Blackbirds basis in the literature for setting a level of concern for Hg in

ty Black ty are suspected to feed at a trophic level higher than do breed- Rusty Blackbird blood, though some bounds can be placed on s ing Red-winged Blackbirds, possibly feeding more frequently this number. Evers et al. (2008) detected reproductive effects on the more predaceous invertebrate taxa Odonata, Diptera, in Common Loons with 3 μg g−1 THg in blood, and Heinz et and Arachnida (Beal 1900, Beecher 1951, Ellison 1990, Avery al. (2009) demonstrated that Common Grackle embryos are 1995, Yasukawa and Searcy 1995). This suspicion of differ- more sensitive to injected MeHg than are those of many water ences in trophic position requires confirmation through stable- birds. For example, at a concentration that killed half of the isotope analysis. Shriver et al. (2006) speculated that a nearly Mallard (Anas platyrhynchos) embryos (1.8 μg g−1), 100% of two-fold difference in Hg concentration between the closely the Common Grackle embryos were dead (Heinz et al. 2009). related and co-occurring Saltmarsh Sparrow (Ammodramus Thus it seems reasonable to assume that for blackbirds adverse −1 eclining Ru eclining caudacutus) and Nelson’s Sparrow (A. nelsoni) was due to effects may occur between 1 and 3 μg g , and it would be pru-

D dietary differences. Simultaneous sampling from sites of co- dent to assume that the lowest observed adverse-effect level occurrence will be necessary to confirm and explain the may be lower than 1 μg g−1. In the Rusty Blackbirds sampled higher levels of Hg found in Rusty Blackbirds. for this study from the Acadian forest, THg concentrations exceeded 1 μg g−1 in 47%, suggesting that there is reason for Methylmercury toxicity and potential concern regarding the THg levels observed in the blood of this for population-level effects declining species (Fig. 2). MeHg is an extremely potent neurotoxicant, as well as an im- Reduced hatching of eggs has been documented when munotoxicant and genotoxicant, with negative effects on re- THg concentrations in feathers are between 5 and 40 μg g−1 production being one of the most sensitive endpoints (Wolfe (Burger and Gochfeld 1997). Provided that the feather samples et al. 1998, 2007). Decreased reproductive success from MeHg from the winter range fairly represent the Rusty Blackbird’s exposure has been observed in both laboratory and field stud- exposure before molt across the boreal forest, a relatively low cology of the of cology ies, and toxicity can result in decreased egg volume and em- percentage of Rusty Blackbirds may be at risk of negative ef- E bryo weight, shell thinning, abnormalities and deformities of fects from Hg (16%, Fig. 3). Feathers of over 95% of the birds embryos or hatchlings, and deleterious behavioral changes in sampled from the Acadian forests, however, exceeded this adults (Scheuhammer et al. 2007, Evers et al. 2008). Though threshold. some field studies ofH g exposure of birds have failed to detect Although THg concentrations in breeding Rusty Black- negative effects on health (Ackerman et al. 2008), recent field birds were elevated relative to what has been reported in the research on insectivorous Tree Swallows at Hg-contaminated literature for other passerines away from contaminated sites, sites indicates that Hg exposure alters a bird’s immune respon- and elevated compared to our unpublished sample of Red- siveness (Hawley et al. 2009) and thyroid hormone and corti- winged Blackbirds, there is currently no direct evidence for costerone profiles (Franceschini et al. 2009, Wada et al. 2009). population-level effects on the Rusty Blackbird resulting from While little research has focused on the effect of MeHg elevated Hg. As Rusty Blackbirds in the far eastern portion of on blackbirds, a recent experimental study by Heinz et al. the breeding range had higher levels of Hg than did those in (2009) suggests that passerines, particularly blackbirds, may other regions, it is worth asking whether this subpopulation be more sensitive to MeHg than are the waterbirds that have has suffered a more dramatic population decline than those received the bulk of study. Of 26 bird species studied, Heinz of other regions. Powell (2008) reported a range contraction et al. (2009) considered the two passerines, the Tree Swallow in Maine of 46% since 1983 despite the apparently suitable (Hirundinidae) and Common Grackle (Quiscalus quiscula, habitat, while Breeding Bird Survey data suggest a decline of Icteridae), to be moderately sensitive, and the grackle was −10% per year in the East (Sauer et al. 2008). The population more sensitive than the Tree Swallow, having a 100% lethal decline does not appear to be as dramatic in Alaska, where −1 concentration (LC100) for eggs of 0.8 μg g compared with Breeding Bird Surveys imply a nonsignificant annual popula- 1.6 μg g−1 for swallow eggs (Heinz et al. 2009). Similarly, tion decline of −5% (Sauer et al. 2008). Additionally, Machtans Special Section: Rangewide Section: Special Finley et al. (1979) found that the Common Grackle—a et al. (2007) found no evidence of a population change in the

18_MS100145.indd 796 11/25/10 3:29:40 PM MERCURY EXPOSURE OF THE RUSTY BLACKBIRD 797 Special Section: Rangewide Mackenzie River Valley, which is in the western boreal forest Caleb Fisher for Vermont, by Carol Foss for New Hampshire, and and near our interior Alaska study sites with lower Hg levels. by the Maritime Breeding Bird Atlas for New Brunswick and Nova Exposure to MeHg has been linked with reduced productiv- Scotia. Melissa Duron assisted with the database query. Housing and logistical support were provided by (in alphabetical order) the ity in the Common Loon (Burgess and Meyer 2008) and has Center for Bottomland Hardwoods, Chugach National Forest, Cor- been proposed as a factor potentially impeding the recovery of dova Ranger District, Elmendorf Air Force Base, Fort Richardson, populations of wading birds in southern Florida (Spalding et Fort Wainwright, K.C. Irving Center of Acadia University, Theo- al. 1994, Sundlof et al. 1994). Effects of MeHg exposure at the dore Roosevelt NWR Complex, U.S. Forest Service, and Yukon level of the individual should be considered among the pos- Flats NWR. Brainard Palmer-Ball, Cleaton Baptist Church, the Delta Research and Extension Center, Delta National Forest, Leroy sible explanations for the declines observed in the far eastern Percy State Park, Silvio O. Conte NWR, Theodore Roosevelt NWR portion of the Rusty Blackbird’s breeding range. Nevertheless, Complex, Vermont Department of Fish and Wildlife, Wagner Forest other stressors, such as habitat destruction (e.g., Powell et al. Management Ltd., Frederick Ballard, and others kindly permitted 2010), climate change, and additional contaminants may also access to their property. Funding was provided in part by the Alaska have an important effect on the eastern population and should Bird Observatory, Alaska Department of Fish and Game State Wild- life Grant Program, the Arthur-von-Gwinner Foundation, Canada be investigated. Foundation for Innovation, Canada Research Chairs Program, Cana- dian Wildlife Service, Chugach National Forest, the Department of Suggestions for future research Defense Legacy Program, Ducks Unlimited Canada, Friends of the National Zoo, German Ethological Society, Kentucky Department Future research should further quantify Hg burdens in breed- of Fish and Wildlife Resources State Wildlife Grant Program, Max ing Rusty Blackbirds. Additional effort should include other Planck Institute for Ornithology of Andechs, National Science and parts of the eastern breeding range such as Quebec, Ontario, Engineering Research Council of Canada, the Society for Tropical Ornithology, U.S. Fish and Wildlife Service, and the U.S. Geological

and New York, where elevated environmental Hg loads in E Survey. We thank Robert Taylor and Deborah Perry at the Department other birds such as the Common Loon have been documented. cology of the of Veterinary Anatomy and Public Health, Texas A&M University, More robust data sets are required to explain the spatial vari- Trace Element Research Lab, College Station, Texas, for providing ation of THg in the blood of Rusty Blackbirds breeding in Hg analysis during the early years of this study. Alaska. Continued and standardized continental sampling efforts will also help to measure changes in environmental Hg loads related to projected emission regulations in the U.S., LITERATURE CITED Canada, and potentially elsewhere. Ac k e r m a n , J. T., J. Y. Ta k e k awa , C. A. Ea g l e s -Sm i t h , a n d S. A. Future research should aim to clarify the role that Hg Iv e r s o n . 2008. Mercury contamination and effects on survival of and other environmental contaminants play in the continu- American Avocet and Black-necked Stilt chicks in San Francisco Bay. Ecotoxicology 17:103–116. ing population decline of the Rusty Blackbird. Researchers Av e r y M. L. 1995. Rusty Blackbird (Euphagus carolinus), no 200. should also seek to test the hypothesis that Hg contamination In A. Poole and F. Gill [e d s .], The Birds of North America. Acad- is contributing to the species’ population decline through ex- emy of Natural Sciences, Philadelphia. D amining individual- and population-level effects on reproduc- Be a l , F. E. L. 1900. Food of the Bobolink, blackbirds, and grackles. eclining Ru tion and survival. As the limited data available suggest the U.S. Department of Agriculture, Washington. Be e ch e r , W. J. 1951. Adaptations for food-getting in the American Rusty Blackbird enjoys high rates of hatching success (Powell blackbirds. Auk 68:411–440. 2008), we suggest studying not only nesting success but also Br a ss o , R., a n d D. Cr i s t o l . 2008. Effects of mercury exposure on juveniles’ survival rates, as Hg exposure may have increased the reproductive success of Tree Swallows (Tachycineta bicolor). developmental and survival risks after fledging (Spalding Ecotoxicology 17:133–141. et al. 2000, Condon and Cristol 2009). We further suggest Bu r g e r , J., a n d M. Go ch f e l d . 1997. Risk, mercury levels, and birds: relating adverse laboratory effects to field biomonitoring. greater sampling of species with stable or increasing popula- Environmental Research 75:160–172. tions within the same wetland complexes for direct compari- Bu r g e ss , N. M., a n d M. W. Me y e r . 2008. Methylmercury exposure s sons of Hg exposures. associated with reduced productivity in Common Loons. Eco- ty Black toxicology 17:83–92. ACKNOWLEDGMENTS Ca i , Y., a n d J. M. Ba y o n a . 1995. Determination of methylmercury in fish and river water samples using in situ sodium tetraethylbo- We thank the many field biologists and technicians who collected rate derivatization following by solid-phase microextraction and samples while conducting their own research, including Bud John- gas chromatography-mass spectrometry. Journal of Chromatog- son, Dave Loomis, Steve Matsuoka, Dave Shaw, and April Scurr, raphy A 696:113–122. who provided samples from Alaska. Russ Greenberg, S. Matsuoka, Co n d o n , A. M., a n d D. A. Cr i s t o l . 2009. Feather growth influences Anna Redden, and Claire W. V. Ramos, along with two anonymous blood mercury level of young songbirds. Environmental Toxicol- b i

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