Mercury and other element exposure to tree swallows (Tachycineta bicolor) nesting on Lostwood National Wildlife Refuge, North Dakota

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Environmental Pollution 155 (2008) 217e226 www.elsevier.com/locate/envpol

Mercury and other element exposure to tree swallows (Tachycineta bicolor) nesting on Lostwood National Wildlife Refuge, North Dakota Thomas W. Custer a,*, Christine M. Custer a, Kevin M. Johnson b, David J. Hoffman c a

US Geological Survey, Upper Midwest Environmental Sciences Center, 2630 Fanta Reed Road, La Crosse, WI 54603, USA b US Fish and Wildlife Service, North Dakota Field Office, 3425 Miriam Avenue, Bismarck, ND 58501-7926, USA c US Geological Survey, Patuxent Wildlife Research Center, 12011 Beech Forest Road, Laurel, MD 20708, USA Received 18 July 2007; received in revised form 26 November 2007; accepted 6 December 2007

Mercury concentrations in tree swallows nesting in the prairie wetlands at Lostwood National Wildlife Refuge were not elevated. Abstract Elevated mercury concentrations in water were reported in the prairie wetlands at Lostwood National Wildlife Refuge, ND. In order to determine whether wildlife associated with these wetlands was exposed to and then accumulated higher mercury concentrations than wildlife living near more permanent wetlands (e.g. lakes), tree swallow (Tachycineta bicolor) eggs and nestlings were collected from nests near seasonal wetlands, semi-permanent wetlands, and lakes. Mercury concentrations in eggs collected near seasonal wetlands were higher than those collected near semi-permanent wetlands or lakes. In contrast, mercury concentrations in nestling livers did not differ among wetland types. Mercury and other element concentrations in tree swallow eggs and nestlings collected from all wetlands were low. As suspected from these low concentrations, mercury concentrations in sample eggs were not a significant factor explaining the hatching success of the remaining eggs in each clutch. Published by Elsevier Ltd. Keywords: Mercury; Tree swallows; Metals; Elements; Oxidative stress

1. Introduction Lostwood National Wildlife Refuge (Lostwood) is a 26,904-acre rolling prairie/wetland ecosystem located in the Missouri Coteau physiographic region of northwestern North Dakota (Fig. 1). Nearly 20% (5381 acres) of Lostwood is comprised of depressional (pothole) prairie wetlands that are poorly integrated by surface drainage, and have a tremendous range in size, hydro-period and water quality. Surface water samples taken at Lostwood in 2003 by the U.S. Geological Survey documented that methylation of inorganic mercury (Hg) was pronounced, however, no information was available on possible site-specific cause and effects. * Corresponding author. Tel.: þ1 608 781 6375; fax: þ1 608 783 6066. E-mail address: [email protected] (T.W. Custer). 0269-7491/$ - see front matter Published by Elsevier Ltd. doi:10.1016/j.envpol.2007.12.003

Concentrations of methyl Hg (MeHg) in the water samples from Lostwood (median ¼ 0.63 ng MeHg/L, calculated from Sando et al., 2007) were well within the range observed in the Florida Everglades (Cleckner et al., 1998), where some of the most severe cases of MeHg exposure have been documented. The suspected primary sources of Hg were two coal-fired power plants in Estevan, Saskatchewan, approximately 40 km upwind of Lostwood. Mercury output from these two power plants in 2001 totaled 555 lbs (Environment Canada National Pollution Release Inventory web-site). Additional sources of Hg within Lostwood’s air-shed and suspected of contaminating the refuge were two gasification plants and extensive oil development. Swallows, especially tree swallows (Tachycineta bicolor) are being widely used as a study species to quantify distribution and effects of local sediment contamination (Custer et al.,

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218

Thompson Lake

S-1

S-2 Alberta

Saskatchewan

Refuge Headquarters

Manitoba

Estevan

Auto Tour Route North Dakota

HWY 8

Lostwood National Wildlife Refuge

SP-1

S-3 SP-2 S-4

N 2 KM

Rock Slough S = seasonal wetland SP = semi-permanent wetland

HWY 50

Fig. 1. Tree swallow study sites (black ovals) at Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005.

2001, 2003a,b, 2006 for metals and other elements; see McCarty, 2001 for summary of other swallow studies). Tree swallows will readily use nest boxes, so study areas can be established at specific locations of interest. They feed near their nest box (within 400 m, Quinney and Ankney, 1985) on emergent aquatic insects (Blancher and McNicol, 1991) so residues in their tissues reflect sediment contamination for those chemicals that transfer into the biota (Fairchild et al., 1992). They also will nest relatively densely, therefore, adequate sample sizes can usually be obtained. Concentrations in tree swallow tissues are reflective of sediment concentrations over small geographic and temporal time scales (Custer et al., 2005). Additionally, data are now available on exposure and effects of elements in tree swallows at a number of locations across North America (Kraus, 1989; Bishop et al., 1995; Custer et al., 2001, 2003a, 2002, 2006, 2007a,b; Gerrard and St. Louis, 2001).

The objectives of this study were to (1) determine Hg concentrations in tree swallow eggs and nestlings from nests near wetlands of differing methylation potential on Lostwood and (2) evaluate the effects of Hg contamination on reproductive success in tree swallows at Lostwood.

2. Material and methods 2.1. Study sites and field data collection Ten to 30 swallow nest boxes per location were attached to posts near eight wetlands at Lostwood in 2004 and 2005 (Fig. 1, Table 1). Nest boxes were placed approximately 30 m apart and protected from predators with stovepipe. Four wetlands with high methylation potential (seasonal wetlands), two wetlands with moderate to low methylation potential (semi-permanent wetlands), and two lakes with low methylation potential were selected at Lostwood (Table 1). Methylation potential was based on results of MeHg concentrations

Table 1 Description of eight wetlands where tree swallow boxes were erected on Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005 and methylmercury concentrations in water in 2004 Wetland

Description

Latitude

S-1 S-2 S-3 S-4 SP-1 SP-2 Thompson Lake Rock Slough

Seasonal Seasonal Seasonal Seasonal Semi-permanent Semi-permanent Lake Lake

48.65125 48.63292 48.59258 48.58268 48.60733 48.58200 48.64900 48.56347

Longitude

N N N N N N N N

102.4231 102.4150 102.4646 102.4685 102.4391 102.4559 102.3990 102.4453

Total a b

Data from Sando et al. (2007). Data are from two seasonal ponds near box location.

W W W W W W W W

No. of boxes

No. of boxes used 2004

2005

20 19 10 11 25 30 30 30

9 8 4 6 15 20 17 23

19 19 10 10 24 28 30 30

175

102

170

Methylmercury, whole-water (ng/L) 2004a

pH (standard units) 2004a

0.27 0.10 0.60 0.17, 0.38b 0.90 0.17 0.17 0.14

9.6 9.7 7.7 9.5, 9.7b 8.2 9.0 9.1 8.7

T.W. Custer et al. / Environmental Pollution 155 (2008) 217e226 in surface water samples taken in 2003 by North Dakota Department of Health and the U.S. Geological Survey (Sando et al., 2007). Next boxes were checked at least once per week beginning in the spring of each year to quantify nesting chronology. Two eggs were randomly collected from each nest during incubation. Eggs that failed to hatch were also collected. Egg contents were pooled by nest and emptied into chemically clean jars. Because Hg exposure has elicited oxidative stress responses in laboratory and field studies with mallards (Anas platyrhynchos) and other species of aquatic birds (Custer et al., 1997, 2000; Hoffman and Heinz, 1998; Hoffman et al., 1998), nestling livers were analyzed for five measures of oxidative stress. Basic methods and assay conditions are described by Hoffman and Heinz (1998). Indicator assays included reduced glutathione (GSH), total sulfhydryl (TSH), protein bound thiol (PBSH), thiobarbituric acid reactive substances (TBARS), oxidized glutathione (GSSG), and the ratio GSSG/GSH. Two young per box were randomly collected for chemical analysis from five nest boxes per site when the young reach 12-days-of-age. Within 2 h of collection, nestlings were weighed (0.1 g) and decapitated, an approved euthanasia procedure (AVMA, 1993). Within 10 min after death, livers were removed from tree swallow nestlings, weighed (0.1 g), and about 0.3 g from one nestling per brood was placed into a cryotube for measurement of oxidative stress. The cryotube was then placed into liquid nitrogen and later transferred to an ultracold freezer (80  C) for storage until processing. Stomach contents were removed, pooled by site, and placed in a chemically clean jar. That liver remainder and the liver from the sibling nestling were pooled by nest and placed in a chemically clean jar. The two nestling carcasses per nest were stored individually in chemically clean jars; one carcass was analyzed and one archived. Pooling of eggs or livers by nest and diet by site ensured sufficient sample mass for chemical analysis. All egg, liver, carcass, and diet samples were frozen at 20  C. Food boli were collected from the throats of 8e12-day-old nestlings for diet composition in 12 nests in mid-July, 2005 using electrical zip ties (Johnson et al., 1980). Young were sampled from five nests at Rock Slough, three nests at SP-1, and four nests at SP-2. Lotic Inc., Unity, ME, identified prey items in one to four boli per nest (24 total boli), usually to genus and characterized these as aquatic or terrestrial. The invertebrates were then desiccated and a dry weight (0.001 g) obtained. Percent frequency and percent mass of aquatic invertebrates were calculated from all the boli from each nest and the mean percentages for all nests were then averaged.

2.2. Chemical analyses Up to 10 egg samples per site from first clutches were randomly selected from those available for element analysis. Chemical analyses were done by Texas A&M Research Foundation, College Station, Texas. In summary, tissue samples were homogenized, freeze dried and then ground to 100 mesh. The dried sample was digested and then analyzed for arsenic (As), cadmium (Cd), molybdenum (Mo), nickel (Ni), and vanadium (V) by graphite furnace and cold vapor atomic absorption spectrophotometry and inductively coupled plasma mass spectrophotometry. Aluminum (Al), barium (Ba), beryllium (Be), boron (B), chromium (Cr), copper (Cu,) iron (Fe), magnesium (Mg), manganese (Mn), selenium (Se), strontium (Sr), and zinc (Zn) were analyzed by inductively coupled plasma-atomic emission spectrophotometry, and total Hg and lead (Pb) were done by cold vapor atomic absorption spectrophotometry. Nominal levels of detection (mg/g dry weight) were Al (1.0), As (0.2), Ba (0.1), B (1.0), Be (0.05), Cd (0.02 in 2004, 0.01 in 2005), Cr (0.5), Cu (0.5), Fe (1.0), Hg (0.02 in 2004, 0.002 in 2005), Mg (1.0), Mn (0.2), Mo (1.0), Ni (0.5), Pb (0.05 in 2004, 0.01 in 2005), Se (0.05), Sr (0.05), V (1.0), and Zn (0.5). Blanks, spikes, and duplicates (10% of total analyzed) were run each year along with certified reference material, all met quality assurance standards of the Analytical Control Facility (U.S. Fish and Wildlife Service, Leetown, West Virginia). Percent recovery averaged 102% for all elements. Concentrations were not adjusted for percent recovery. We did not analyze samples for MeHg, the more toxic form of Hg. An earlier study (Gerrard and St. Louis, 2001) demonstrated that almost all Hg in tree swallow tissues was MeHg. Concentrations of elements are reported on a dry-weight basis; approximate wet-weight values can be calculated by using the mean percent moisture for tree swallow eggs (80.4%), livers (68.9%), carcasses (70.2%), and diet (72.1%) in this study.

219

2.3. Statistical analyses Non-metric multi-dimensional scaling plots (Kruskal, 1964) were constructed to display patterns among sample groups. Analysis of similarity tests (ANOSIM, PRIMER-E) were used to test hypotheses regarding the pattern of elements in eggs, nestling livers, nestling carcasses, nestling diet, and oxidative stress measures among wetlands and years (Clarke and Warwick, 2001). These initial multivariate tests were used to protect against Type I errors which can occur when many univariate tests are run on a single data set. Analysis of similarity is a multivariate analogue of analysis of variance, it is built on a simple non-parametric permutation procedure and applied to the rank similarity matrix underlying the ordination of samples. The test statistic, ‘‘R’’, may vary from þ1 to 1. An R value close to þ1 indicates that there are very clear differences in patterns among the groups being tested. A value near zero means that the distribution of patterns is as similar among the groups as within the groups. R is considered significant based on its ‘p’ value (e.g. p < 0.05). Because R can be significantly different from zero yet inconsequentially small, the size of R indicates the degree of difference. Clear differences in patterns are evident when R is 0.4. There is some support for pattern differences when R is 0.3 to <0.4, and patterns barely differ when R is <0.3 (adapted from Clarke and Warwick, 2001). Marginal effects of site and year were assessed using the equivalent of a 2-way ANOVA without interaction (termed ‘‘2-way crossed analysis’’). Variables were included in the analyses if 50% of samples had detectable values; one-half the detection limit was assigned to samples below the detection limit. Element data were logtransformed prior to ANOSIM analysis and BrayeCurtis similarity measures were used. Because of differing measurement scales, oxidative stress measures were normalized (Clarke and Warwick, 2001). Comparisons among wetland types and years for individual elements were made using analysis of variance (1- and 2-way ANOVA) when justified by the multivariate analysis. Because Hg was the focus of the study, Hg concentrations in eggs, livers, carcasses, and diet were evaluated with ANOVA regardless of the ANOSIM results. Nestling carcasses do not include livers for estimates of element concentrations, but carcasses do include livers for the estimates of mercury mass. Mass of Hg in nestlings was calculated by multiplying the concentration (mg/g) by the sample weight (g) and then adding it to the mass in the liver. Based on visual inspection of residuals from models of log-transformed measures, models appeared to satisfy homogeneity of variance assumptions. Sample means were compared using a Bonferroni correction, and an overall alpha level of 0.05. Oxidative stress measures were correlated with Hg concentrations using Pearson’s correlation coefficients. Geometric means (antilog of mean log values) and 95% confidence intervals (CIs) are presented in the tables and text. Daily nest survival probability for the incubation and nestling periods was calculated and compared among sites using the Mayfield’s estimate of survival and associated statistics (Mayfield, 1961, 1975; Hensler and Nichols, 1981). Percent nest success during the incubation and nestling period was then calculated by raising the daily nest survival rate to the 13th power for the incubation period and 12th power for the nestling period. The incubation period was defined as the number of days from the date the last egg was laid (day 0) until the first egg hatched (day 13) and the nestling period was defined as the number of days from the date the first egg hatched (day 0) until that nestling reached 12-days-of-age. Egg probability was the total number of eggs that hatched divided by the total number of eggs in nests where at least one egg hatched. Nestling probability was total number of nestlings alive at 12-daysof-age divided by the total number of nestlings in nests where at least one nestling survived to 12-days-of-age. Nests or eggs lost because of cattle tipping the boxes over or because of human error were not included in the analysis. In 2005, a protracted period of low temperatures combined with rain during the egg-laying and early incubation periods seemed to result in nest abandonment at four of the eight sites. The number of nestling produced per nest to 12days-of-age was estimated as the product of the probability of an egg surviving to 12-days-of-age and the mean clutch size. Because eggs were collected for chemical analysis, this estimate assumes that survival in the nest is independent of the number of eggs or young in the nest. The response of hatching success to Hg concentrations in samples eggs was modeled using logistic regression (Hosmer and Lemeshow, 1989). This statistical approach was chosen because egg success was a binary dependent

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variable (i.e. either an egg hatched or it did not). We included the possibility of extrabinomial variation, which is greater variance than the binomial distribution, by estimating an extrabinomial scale parameter as the deviance divided by its degrees of freedom (McCullagh and Nelder, 1989). For the binomial distribution, this scale parameter is exactly one, and larger values indicate the presence of extrabinomial variation in the data. Our tests of significance are adjusted for this scale parameter. The Hosmer and Lemeshow (1989) goodness-of-fit test was used to determine whether the data adequately fit the logistic function, a p value >0.05 indicates adequate fit.

3. Results 3.1. Frequency of detection Copper, Fe, Hg, Mg, Mn, Se, Sr, and Zn were detected in all eggs (random selection, n ¼ 143), nestling livers (n ¼ 79), and nestling carcasses (n ¼ 79, Table 2). For eggs, Be, V, and Cd were not detected in any samples; Al, Cr, Ni, and Mo in fewer than 10 samples; As, B, and Pb in 89, 38, and 53 samples; and Ba in all eggs. For nestling livers, Al and Be were not detected in any samples; B, Cr, Ni, and V in fewer than 10 samples; Ba, Cd, and Pb in 22, 61, and 61 samples; and As and Mo in all livers. For nestling carcasses, Be, V, and Mo were not detected in any samples; Al, Ni, and Pb in fewer than 10 samples; Cr, As, B, and Cd in 16, 39, 39, and 33 samples; and Ba in all carcasses. Except for Cr, the other elements were detected in nearly all dietary samples (Table 2). 3.2. Multivariate pattern analysis of elements and oxidative stress The pattern of Hg and other elements (Cu, Fe, Mg, Mn, Se, Sr, and Zn) differed significantly ( p < 0.001) among matrices (eggs, nestling livers, nestling carcasses, and nestling diet) and years. This pattern was well separated among matrices (global R ¼ 0.97) but not among years (R ¼ 0.22) (Table 3, Fig. 2); all paired comparisons between matrices were well separated ( R > 0.86). Based on mean comparisons, differences in element concentrations among matrices identified in Table 3 were influenced by higher concentrations of Hg in eggs, Fe and Se in nestling livers, Mg in nestling carcasses, and Cu, Mg, Mn, Sr, and Zn in nestling diet (Table 2). The 2-way ANOVA also indicated higher concentrations of Hg, Se, and Sr in 2005 than 2004, but no yearly differences for Cu, Fe, Mg, Mn, and Zn (data not shown). The pattern of elements within eggs, nestling livers, and nestling carcasses but not nestling diet or measures of oxidative stress differed significantly among wetland types (Table 4). Based on low R values, the differences among wetland types for eggs, nestling livers, and nestling carcasses were inconsequential. Element patterns differed significantly between years for eggs, nestling livers, nestling carcasses, and measures of oxidative stress (Table 4). Yearly patterns of elements for carcasses were well separated (R ¼ 0.762) and inconsequential for eggs (R ¼ 0.059). There was some support for yearly differences for nestling livers (R ¼ 0.287) and measures of oxidative stress (R ¼ 0.365). Yearly differences in oxidative stress were influenced by higher activities of TSH, PBSH, GSSG

and the ratio of GSSG to GSH in 2004 and higher activities of GSH, in 2005 (Table 5). 3.3. Mercury concentrations Mercury concentrations in tree swallow eggs were higher from seasonal wetlands than semi-permanent wetlands or lakes (Table 6). In 2004, Hg concentration and Hg mass in 12-day-old nestling carcasses were higher in nestlings associated with seasonal wetlands than those associated with lakes (Table 7). In contrast, Hg concentrations in livers in 2004 and 2005 did not differ among wetland types (Table 7). Additionally, Hg concentrations and Hg mass in nestling carcasses in 2005 did not differ among wetland types (Table 7). Mercury concentrations in nestling stomach contents did not differ among wetland types (Table 8). Mercury concentrations in eggs and nestling livers, carcasses, and stomach contents were higher in 2005 than 2004 (Tables 6e8). Mercury concentrations in nestling livers were significantly correlated with TSH (r ¼ 0.41, p ¼ 0.0002), GSH (r ¼ 0.24, p ¼ 0.03), PBSH (r ¼ 0.47, p ¼ <0.0001), and GSSG (r ¼ 0.25, p ¼ 0.03), but not with TBARS (r ¼ 0.10, p ¼ 0.38), or GSSG/GSH (r ¼ 0.21, p ¼ 0.07). 3.4. Reproductive success Of the 175 boxes, 102 and 170 were used one or more times in 2004 and 2005 (Table 1). There were 315 nest attempts, which include 56 nest attempts that were determined to be abandoned because of bad weather conditions in 2005. The daily probability of nest success did not differ among wetland types during the incubation period in 2004 nor the nestling period in 2004 and 2005 (Table 9). Daily nest success during the incubation period in 2005 was significantly higher for seasonal wetlands (0.90), than for semi-permanent wetlands (0.55), or for lakes (0.68) ( p < 0.001). The estimated number of nestlings per nest attempt that survived to 12-days-of-age varied from 2.2 to 5.0 among wetland types and years. Mercury concentrations in sample eggs (n ¼ 120) were not a significant factor in hatching success of tree swallow clutches (logistic regression p ¼ 0.96). The distribution of data conformed to the logistic model (goodness-of-fit p ¼ 0.10). 3.5. Diet composition Diptera accounted for 79% of the prey items identified in 24 food boli from 12 tree swallow nests. Prey items by frequency of occurrence averaged 55.1% of aquatic origin among nests. Aquatic invertebrates were found in 11 of the 12 nests; terrestrial invertebrates were found in all 12 nests. When converted to mass, the prey items were 46.9% of aquatic origin. 4. Discussion 4.1. Mercury Mercury concentrations in tree swallow eggs and nestlings (mean ¼ 0.2 mg/g dry weight for eggs, nestling livers, and

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Table 2 Element concentrations in tree swallow eggs and nestling livers, carcasses, and diet from Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005 Element

Geometric mean/(95% CI)/[range] mg/g dry weight Eggs (n ¼ 143)

Livers (n ¼ 79)

Nestlings (n ¼ 79)

Diet (n ¼ 16)

[72nde40]

41.8 (27e64) [10.2e224]

[40nde4.1]

0.818 (0.59e1.14) [0.34e2.65]

[77nde8.36]

[40nde3.06]

4.82 (3.5e6.5) [1.81e21.6]

2.84 (2.6e3.1) [0.824e10.8]

[57nde0.433]

4.52 (4.1e5.0) [1.31e9.67]

7.96 (5.6e11) [2.98e43.5]

[143nd]

0.033 (0.03e0.04) [18nde0.155]

[46nde0.12]

0.417 (0.30e0.58) [0.159e2.05]

[135nde2.64]

[71nde3.61]

[63nde3.74]

[14nde0.772]

Aluminum

Arsenic

[140ndae8.48]

[79nd]

0.166 (0.15e0.18) [54nde0.889]

0.278 (0.25e0.31) [0.156e0.786]

Boron [105nde2.53] Barium

Cadmium

Chromium

b

Copper

2.43 D (2.3e2.5) [1.40e5.08]

20.5 B (19e22) [13e69]

6.13 C (6.0e6.3) [5.15e8.31]

25.2 A (23e28) [16.7e37.1]

Iron

108 D (104e112) [54e170]

1177 A (1091e1271) [485e2440]

127 C (123e131) [98.6e192]

673 B (548e825) [375e1592]

Mercury

0.204 A (0.12e0.22) [0.036e0.809]

0.16 B (0.15e0.18) [0.017e0.363]

0.18 AB (0.16e0.19) [0.057e0.414]

0.047 C (0.04e0.06) [1nde0.091]

Magnesium

368 C (357e379) [274e648]

756 B (744e768) [651e892]

893 A (879e907) [761e1040]

978 A (661e1447) [388e8615]

Manganese

2.29 C (2.2e2.4) [1.13e4.79]

4.94 B (4.8e5.1) [3.6e6.97]

2.58 C (2.4e2.7) [1.56e6.05]

42.8 A (30e61) [24.6e423]

[142nde1.18]

2.41 (2.3e2.5) [1.56e10.8]

[79nd]

1.10 (0.89e1.3) [3nde1.98]

[90nde0.405]

0.034 (0.03e0.04) [18nde0.313]

[72nde0.709]

0.145 (0.11e0.19) [0.05e0.486]

Selenium

2.10 C (2.0e2.2) [1.37e3.44]

4.74 A (4.5e5.0) [3.0e9.61]

2.51 B (2.4e2.6) [1.63e4.06]

1.50 D (1.3e1.8) [0.815e2.99]

Strontium

7.73 C (7.2e8.3) [3.38e26.9]

0.167 D (0.16e0.18) [0.076e0.304]

17.6 B (16.8e18.5) [11.4e28.1]

23.3 A (17e31) [9.19e73.6]

Zinc

61.2 D (60e63) [35.4e123]

79.5 C (77e82) [61.9e133]

98.7 B (97e100) [86e110]

166 A (93.7e273) [78.5e273]

Molybdenum

Lead

a

The number before ‘nd’ is the number of samples that had undetected values. Means were not calculated if <50% had detectable concentrations. Means sharing the same letter among eggs, livers, nestlings, and diet for the elements Cu, Fe, Hg, Mg, Mn, Se, Sr, and Zn are not significantly different (results 2-way ANOVA). b

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222

Fig. 2. Non-metric multi-dimensional scaling plot of element patterns in tree swallow eggs and nestling livers, carcasses, and diet collected from Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005. Copper, Fe, Hg, Mg, Mn, Se, Sr, and Zn were included in the analysis. Note that the axes of non-metric multi-dimensional scaling plots are without units.

nestling carcasses) at Lostwood were low compared to levels reported in tree swallows from other North American locations. Mercury concentrations in tree swallows from the Arkansas River, CO (Custer et al., 2003a); North Platte River, WY (Custer et al., 2001); Mississippi River, MN (Custer et al., 2007b); Agassiz National Wildlife Refuge, MN (Custer et al., 2006); northwestern Ontario (Gerrard and St. Louis, 2001); Housatonic River, MA (Custer et al., 2003b); several sites in ME and MA (Longcore et al., 2007), and the Carson River, NV (Custer et al., 2007a) averaged 0.2, 0.3, <0.3, 0.2, 0.3e0.4, 0.6, 1.3e3.0 (estimated from wet weight assuming 80% moisture), and >6.2 mg/g dry weight in eggs, respectively. Mercury concentrations in tree swallow nestlings for these same locations were 0.1, 0.2, 0.2, 0.2, not available (NA), NA, NA, and >2.8 mg/g dry weight in livers, respectively. The low Hg concentrations in tree swallows at Lostwood seem to be an anomaly given the high concentrations of MeHg reported in the water and sediment samples from prairie wetlands at Lostwood in 2003 (Sando et al., 2007). One explanation for this unexpected result may be that the lower MeHg Table 3 Analysis of similarity for element patterns among tree swallow eggs and nestling livers, carcasses, and diet from eight wetlands on Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005 Comparison

R-statistic

p

2-Way crossed analysisa Matrix Egg, carcass Egg, liver Egg, diet Carcass, liver Carcass, diet Liver, diet

0.970 0.859 1.000 1.000 1.000 0.998 1.000

0.001 0.001 0.001 0.001 0.001 0.001 0.001

Year

0.222

0.001

a

Elements included in the analysis were Cu, Fe, Hg, Mg, Mn, Se, Sr, and Zn.

concentrations in water in 2004 in combination with higher pH in 2004 influenced the low Hg concentrations measured in tree swallows. Concentrations of MeHg in water from Lostwood wetlands in 2004 were about half that of 2003 (median MeHg ¼ 0.27 ng/L in 2004 and 0.63 ng/L in 2003; calculated from Sando et al., 2007). Methylmercury concentrations in water samples in 2004 from the seasonal and semi-permanent wetlands used in this study varied from 0.1 to 0.9 ng/L and averaged ¼ 0.33 ng/L (Table 1). Even though MeHg concentrations in 2004 were lower than the 2003 levels, the concentrations were still elevated. Methylmercury concentrations in natural surface waters generally range from 0.02 to 0.1 ng/L (Bloom, 1989). Additionally, pH was higher at four wetlands measured in both 2004 (Table 1) and 2003 (S-4 pH ¼ 6.5, SP-1 pH ¼ 7.1, Thompson Lake pH ¼ 8.8, Rock Slough pH ¼ 8.3). Another explanation for the low Hg concentrations in tree swallows may be the high concentrations of dissolved organic carbon (DOC) in these wetlands (Krabbenhoft, 1996). Mesocosm studies employing the use of DOC dosing in wetlands resulted in the formation of high MeHg concentrations, but the DOC also appeared to prevent MeHg transfer to the food web. This investigation suggests that the very high levels of DOC (about 80 mg/L) present in the surface water at Lostwood retards the transfer of MeHg to the food web (D. Krabbenhoft, personal communication). Our results are consistent with the hypothesis that prairie wetlands because of their drying and flooding cycles increase Hg exposure to wildlife. Mercury concentrations in eggs were higher from nests near seasonal wetlands than either semipermanent wetlands or lakes. Additionally, in 2004 Hg concentration and mass in nestlings were higher from nests near seasonal wetlands compared to lakes. Methylation of inorganic Hg is enhanced by decomposition of organic carbon in flooded soils (Wiener et al., 2003) and Hg thus becomes more available to vertebrates that forage in these flooded wetlands. Mercury burdens in tree swallow nestlings almost doubled following the creation of a reservoir in northwestern Ontario (Gerrard and St. Louis, 2001). Mercury exposure and accumulation in tree swallows at Lostwood were similar to a Canadian study of tree swallows following the creation of an experimental reservoir (Gerrard and St. Louis, 2001). Methyl Hg in water at the Canadian reservoir pre- and post-flood averaged 0.1 and 0.9 ng/L. These water concentrations were comparable to those found in lakes and other wetlands at Lostwood in 2004 (range 0.1e 0.9 ng Hg/L, Table 1). Mercury concentrations in tree swallow eggs from the Canadian study (geometric mean of 6 years after flood ¼ 0.32 mg/g dry weight) were only slightly higher than those at Lostwood (geometric mean ¼ 0.20 mg/g dry weight). Also, MeHg concentration in dipterans, potential prey of tree swallows, from the reservoir pre- and post-flood were 0.044 and 0.111 mg/g dry weight; total Hg concentrations in tree swallow stomach contents from Lostwood averaged 0.05 mg/g dry weight. Finally, no effects of Hg on tree swallow reproduction were reported in either study.

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223

Table 4 Analysis of similarity for element patterns of tree swallow eggs and nestling livers, carcasses, diet, and oxidative stress indicators from three wetland types at Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005 Comparison

R-statistic/( p) Eggsa

2-Way crossed analysis Wetlandf Seasonal vs. lake Seasonal vs. semi Lake vs. semi

0.080 0.123 0.081 0.004

Year (2004 and 2005)

0.059 (0.01)

(0.01) (0.01) (0.01) (0.37)

Liversb

Carcassesc

Dietd

0.114 0.084 0.137 0.123

0.112 0.129 0.146 0.038

0.169 0.089 0.125 0.125

(0.01) (0.08) (0.02) (0.01)

0.287 (0.001)

(0.005) (0.03) (0.01) (0.18)

Oxidative stress indicatorse (0.86) (0.61) (0.70) (0.78)

0.209 (0.98)

0.762 (0.001)

0.016 0.031 0.028 0.059

(0.33) (0.27) (0.27) (0.98)

0.365 (0.001)

a

Elements included in the analysis were As, Ba, Cu, Fe, Hg, Mg, Mn, Se, Sr, and Zn. b Elements included in the analysis were As, Cd, Cu, Fe, Hg, Mg, Mn, Pb, Se, Sr, and Zn. c Elements included in the analysis were Ba, Cu, Fe, Hg, Mg, Mn, Se, Sr, and Zn. d Elements included in the analysis were Al, As, Ba, B, Cd, Cu, Fe, Hg, Mg, Mn, Mo, Pb, Se, Sr, and Zn. e Indicators included in the analysis were reduced glutathione (GSH), total sulfhydryl, protein bound thiol, thiobarbituric acid reactive substances, oxidized glutathione (GSSG), and the ratio GSSG/GSH. f Wetlands included in the analysis were seasonal ponds, semi-permanent ponds, and lakes.

Mercury concentrations in tree swallow eggs (mean ¼ 0.2 mg/g dry weight) at Lostwood were below toxic levels. Impairment of reproductive success has been associated with egg concentrations of 2.5e10 mg/g dry weight (Thompson, 1996, converted to dry weight assuming 80% moisture). Barn swallow (Hirundo rustica) eggs in Texas averaged 0.1 mg/g dry weight Hg (maximum value was 0.71 mg/g dry weight), and no reproductive effects were noted (King et al., 1994). Reduced hatching success was associated with Hg concentrations in eggs >6.0 mg/g dry weight for tree swallows nesting on the Carson River, NV (Custer et al., 2007a). Table 5 Mean oxidative stress measurements in nestling livers at Lostwood National Wildlife Refuge, North Dakota during 2004 and 2005 Bioindicator

Geometric mean/(95% CI)/[range] 2004

2005

Reduced glutathione (GSH)

2.09 Ba (1.8e2.4) [0.42e3.4]

2.71 A (2.4e3.0) [1.2e5.4]

Total sulfhydryl (TSH)

21.4 A (20.9e21.9) [17.9e23.8]

18.6 B (18.1e19.1) [14.4e22.6]

Protein bound thiol (PBSH)

19.1 A (18.6e19.7) [15.8e22.3]

15.7 B (15.3e16.2) [12.6e18.1]

Thiobarbituric acid reactive substances (TBARS)

23.8 A (20.4e27.7) [12.7e141]

23.3 A (22.1e24.5) [15.7e32.4]

Oxidized glutathione (GSSG)

0.72 A (0.64e0.82) [0.29e1.5]

GSSG/GSH

0.344 A (0.28e0.42) [0.09e1.8]

a

4.2. Other elements Selenium, an element associated with negative impacts on birds (US Department of the Interior, 1998), was at background concentrations in Lostwood eggs (mean ¼ 2.1 mg/g dry) and nestling livers (mean ¼ 4.7 mg/g dry weight). Background concentrations in bird eggs are generally <5 mg/g dry weight and an embryo viability threshold is estimated at 10 mg/g dry weight (US Department of the Interior, 1998). Background hepatic concentrations are typically <10 mg/g dry weight, and a threshold for juvenile and adult toxicity is estimated at 30 mg/g dry weight (US Department of the Interior, 1998). Concentrations of other elements in tree swallow eggs and livers (Al, B, Ba, Cd, Cr, Cu, Fe, Mg, Mn, Mo, Sr, and Zn) were found at comparable or lower concentrations than similar tree swallow samples from the North Platte River, WY (Custer et al., 2001), the Arkansas River, CO (Custer et al., 2003a), Mississippi River, MN (Custer et al., 2007b); Agassiz National Wildlife Refuge, MN (Custer et al., 2006); the Carson River, NV (Custer et al., 2007a); and the Housatonic River, MA (Custer et al., 2003b). With the exception of Hg and Se and to some degree Fe, Mo and Cu, most elements based on dietary exposure were Table 6 Mercury concentrations in tree swallow eggs collected from seasonal wetlands, semi-permanent wetlands, and lakes at Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005 N

Geometric mean mg Hg/g dry weight 95% CI

0.57 B (0.53e0.62) [0.29e1.1]

Wetland Seasonal Semi-permanent Lake

63 40 40

0.23 Aa 0.19 B 0.19 B

0.21e0.25 0.16e0.22 0.16e0.21

0.211 B (0.18e0.25) [0.09e0.61]

Year 2004 2005

65 78

0.16 B 0.25 A

0.14e0.18 0.23e0.26

Means sharing the same letter between years were not significantly different (results 2-way ANOVA where p of some year combinations was <0.05 but wetland p and wetland  year p were >0.05).

a

Means sharing the same letter within wetlands and between years are not significantly different (2-way ANOVA, wetland p ¼ 0.04, year p ¼ <0.001, wetland  year p ¼ 0.44).

T.W. Custer et al. / Environmental Pollution 155 (2008) 217e226

224

Table 7 Mercury concentrations (mg Hg/g dry weight) and mass (mg) in 12-day-old tree swallow nestlings collected from seasonal wetlands, semi-permanent wetlands, and lakes at Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005 Year

N

Wetland

Geometric mean 95% CI mg Hg/g dry weight

mg Hg

Livers

Carcasses þ liver

Carcasses

2004

Seasonal Semi-permanent Lake

16 10 10

0.15 BCDa 0.12 DC 0.10 D

0.13e0.16 0.10e0.13 0.08e0.12

0.16 B 0.13 BC 0.10 C

0.14e0.17 0.12e0.15 0.09e0.13

1.0 B 0.84 BC 0.66 C

0.89e1.12 0.77e0.93 0.53e0.81

2005

Seasonal Semi-permanent Lake

20 10 10

0.18 ABC 0.23 AB 0.24 A

0.14e0.24 0.20e0.26 0.20e0.28

0.21 A 0.24 A 0.26 A

0.20e0.23 0.22e0.26 0.21e0.32

1.47 A 1.56 A 1.67 A

1.39e1.57 1.37e1.77 1.38e2.03

2004 2005

All wetlands All wetlands

36 40

0.12 Bb 0.21 A

0.11e0.14 0.18e0.24

0.13 B 0.23 A

0.12e0.15 0.21e0.25

0.85 B 1.54 A

0.77e0.94 1.45e1.65

a Means sharing the same letter among wetlands by matrix are not significantly different (results of 1-way ANOVA following a 2-way ANOVA with significant interactions [wetland  year]). One-way ANOVA p values are all <0.0001. b Means sharing the same letter between years by matrix are not significantly different (results of 1-way ANOVA following a 2-way ANOVA with significant interactions [wetland  year]). One-way ANOVA p values are all <0.0001.

not accumulated or bio-magnified to tree swallow eggs and nestling tissues. Tree swallows were exposed to Al, B, Cd, and Pb in their diet but these elements were not accumulated in eggs or nestlings. Arsenic, Ba, Mg, Mn, Sr, and Zn were accumulated but not bio-magnified. Iron, Mo, and Cu concentrations in livers were comparable to dietary concentrations. In contrast, Hg and Se concentrations are 3e4 times higher and 1.5e3 times higher in eggs and nestling tissues than in the diet. 4.3. Oxidative stress The values reported here for GSH, TSH, TBARS, and PBSH are comparable to values from nestling swallows collected from Agassiz National Wildlife Refuge, MN (Custer et al., 2006) and those nesting near the Mississippi River near La Crosse, WI (Custer et al., 2007b). In those studies, trace element concentrations including Hg were also at low levels. The negative Hg correlations with oxidative stress measures are consistent with the literature in general but not for swallows with these low element concentrations. The negative relationship between Hg concentrations in livers and TSH, PBSH, and GSSG were reported for other species and locations Table 8 Mercury concentrations in tree swallow nestling stomach contents collected from seasonal wetlands, semi-permanent wetlands, and lakes at Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005 Wetlanda

N Geometric mean mg Hg/g dry weight 95% CI (by year) 2004 2005b

Seasonal 4 Semi-permanent 2 Lakes 2

0.032 0.036 0.032

0.01e0.07 0.03e0.04 0.02e0.04

0.066 0.068 0.071

0.05e0.08 0.06e0.08 0.05e0.1

Overall

0.033

0.02e0.05

0.068

0.06e0.08

a

8

Results of 2-way ANOVA were wetland p ¼ 0.96, year p ¼ 0.01, wetland  year p ¼ 0.97. b The 2005 samples are the average of two samples from each wetland.

(Henny et al., 2002; Custer et al., 1997, 2000). However, no significant negative correlations between Hg and these oxidative measures were reported in tree swallow nestlings at Agassiz National Wildlife Refuge, MN, a site with similar low concentrations of Hg and other elements (Custer et al., 2006). 4.4. Diet The dietary results support earlier studies that aquatic insects are a major component of tree swallow diet. Approximately half of the dietary items were aquatic based (55.1% by frequency, 46.9% by mass). Tree swallow nestling diet was 86% aquatic origin from the Arkansas River, Colorado (Custer et al., 2003a), 50% aquatic by frequency and >90% aquatic by mass from Agassiz National Wildlife Refuge, MN (Mengelkoch et al., 2004), and 52% aquatic origin by frequency and 65% aquatic origin by mass from Sudbury, Ontario, Canada (Blancher and McNicol, 1991). We cannot be certain that swallows fed on invertebrates at the wetland nearest their nest. At each of the selected wetlands, other wetlands were within the flight range of foraging tree swallows and Hg exposure to adults and chicks could have been diluted or enhanced. 4.5. Reproduction Because the concentrations of contaminants associated with decreased reproduction in birds (e.g. Hg, Se) were low at Lostwood in 2004 and 2005 (see earlier discussions), it was not surprising that the probability of an egg hatching in nests that hatched at least one egg (means ¼ 77e95%) and nestling survival to 12-days-of-age (means 94e100%) were not depressed. The nationwide average hatching success for tree swallows was 87% in nests where at least one egg hatched (Robertson et al., 1992). Based on low concentrations of Hg in eggs, it was also not surprising that there was no significant relationship between hatching success and Hg concentration in

T.W. Custer et al. / Environmental Pollution 155 (2008) 217e226

225

Table 9 Nest success, clutch size, and number of tree swallow nestlings produced to 12-days-of-age at three wetland types at Lostwood National Wildlife Refuge, North Dakota in 2004 and 2005 Year and wetland types

No. of nests

2004 Seasonal Semi-permanent Lake p 2005 Seasonal Semi-permanent Lake p a b c d

Nest successa

I$C

Egg probabilityb (PE)

Nestling probabilityc (PN)

Mean clutch size (S )

No. of nestlings to 12days-of-age (I$C$PE$PN$S )

Incubation (I )

Nestling (C )

28 37 43

0.94 Ad 0.86 A 0.83 A 0.19

0.96 A 1.00 A 0.94 A 0.93

0.90 0.86 0.78

0.92 0.86 0.88

1.0 0.96 0.94

6.0 6.0 5.6

5.0 4.3 3.6

62 67 78

0.90 A 0.55 B 0.68 B <0.001

1.00 A 1.00 A 0.98 A 1.00

0.90 0.55 0.67

0.89 0.77 0.95

0.98 0.95 0.97

6.2 5.5 6.1

4.9 2.2 3.8

Nest success is based on daily survival probabilities (Mayfield, 1961, 1975). The probability of an egg hatching in nests that hatched at least one egg. The probability of a chick surviving to 12-days-of-age in nests where at least one chick survived to 12-days-of-age. Nest success values among wetland types within year sharing the same letter are not significantly different.

sibling eggs. Lack of reproductive effects was also reported at a Canadian study site with comparable Hg concentrations in water, tree swallow eggs, and tree swallow nestlings (Gerrard and St. Louis, 2001). 5. Conclusions The pattern of elements within tree swallow eggs, nestling livers, and nestling carcasses differed significantly among wetland types at Lostwood, however, because of low R values, the differences were not considered important; nestling diet and measures of oxidative stress did not differ among wetland types. Mercury concentrations in eggs collected near seasonal wetlands were higher than those collected near semi-permanent wetlands or lakes in both 2004 and 2005. Mercury concentrations and mass in nestling carcasses from seasonal wetlands were higher than those from lakes in 2004, but there were no differences in concentrations among wetland types in 2005. Mercury concentrations in nestling livers did not differ among wetland types for either 2004 or 2005. Mercury and other element concentrations in tree swallow eggs and nestlings collected from all wetlands were low and below toxic levels. About one-half of the prey items in nestling diet were of aquatic origin. Hatching success of tree swallows at Lostwood (77e95%) was comparable to a nationwide average (87%). Mercury concentrations in sample eggs collected from tree swallow nests were not a significant factor explaining the hatching success of the remaining eggs in each clutch. Acknowledgments We thank Paul Dummer for field and statistical assistance, Brenda Curry and Dorothy Fecske for field assistance; Will Meeks for logistical support at Lostwood National Wildlife Refuge; David Krabbenhoft for assistance with data interpretation; and Gary Heinz and Miguel Mora-Zacarius for review of the manuscript.

References AVMA, 1993. Report of the AMVA panel on euthanasia. Journal of the American Veterinary Medical Association 202, 229e249. Bishop, C.A., Koster, M.D., Chek, A.A., Hussell, D.J.T., Jock, K., 1995. Chlorinated hydrocarbons and Hg in sediments, red-winged blackbirds (Agelaius phoeniceus) and tree swallows (Tachycineta bicolor) from wetlands in the Great Lakes e St. Lawrence River basin. Environmental Toxicology and Chemistry 14, 491e501. Blancher, P.J., McNicol, D.K., 1991. Tree swallow diet in relation to wetland acidity. Canadian Journal of Zoology 69, 2629e2637. Bloom, N.S., 1989. Determination of pictogram levels of methylmercury by aqueous phase ethylation, followed by cryogenic gas chromatography with cold vapor atomic fluorescence detection. Canadian Journal of Fisheries and Aquatic Sciences 46, 1131e1140. Clarke, K.R., Warwick, R.M., 2001. Change in Marine Communities: an Approach to Statistical Analysis and Interpretation, second ed. Plymouth Marine Laboratories, Plymouth, United Kingdom. Cleckner, L.B., Garrison, P.J., Hurley, J.P., Olson, M.L., Krabbenhoft, D.P., 1998. Trophic transfer of methyl mercury in the northern Florida Everglades. Biogeochemistry 40, 347e361. Custer, C.M., Custer, T.W., Archuleta, A.S., Coppock, L.C., Swartz, C.D., Bickham, J.W., 2003a. A mining impacted stream: exposure and effects of lead and other elements on tree swallows (Tachycineta bicolor) nesting in the upper Arkansas River basin, Colorado. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., J. (Eds.), Handbook of Ecotoxicology, second ed. CRC Press, Boca Raton, pp. 787e812. Custer, C.M., Custer, T.W., Dummer, P.M., Munney, K.L., 2003b. Exposure and effects of chemical contaminants on tree swallows nesting along the Housatonic River, Berkshire County, Massachusetts, USA, 1998e2000. Environmental Toxicology and Chemistry 22, 1605e1621. Custer, C.M., Custer, T.W., Rosiu, C.J., Melancon, M.J., Bickham, J.W., Matson, C.W., 2005. Exposure and effects of 2,3,7,8-tetrachlorodibenzop-dioxin in tree swallows (Tachycineta bicolor) nesting along the Woonasquatucket River, Rhode Island, USA. Environmental Toxicology and Chemistry 24, 93e109. Custer, C.M., Custer, T.W., Warburton, D.W., Hoffman, D.J., Bickham, J.W., Matson, C.W., 2006. Trace element concentrations and bioindicator responses in tree swallows from northwestern Minnesota. Environmental Monitoring and Assessment 118, 247e266. Custer, C.M., Custer, T.W., Hill, E.F., 2007a. Hg exposure and effects of cavity-nesting birds from the Carson River, Nevada. Archives of Environmental Contamination and Toxicology 52, 129e136. Custer, T.W., Hines, R.H., Melancon, M.J., Hoffman, D.J., Bickham, J.W., Martin, J.W., Henshel, D., 1997. Contaminant concentrations and

226

T.W. Custer et al. / Environmental Pollution 155 (2008) 217e226

biomarker response in great blue heron eggs from 10 colonies on the upper Mississippi River, USA. Environmental Toxicology and Chemistry 16, 260e271. Custer, T.W., Custer, C.M., Hines, R.H., Sparks, D.W., Melancon, M.J., Hoffman, D.J., Bickham, J.W., Wickliffe, J.K., 2000. Mixed-function oxygenases, oxidative stress, and chromosomal damage measured in lesser scaup wintering on the Indiana Harbor Canal. Archives of Environmental Contamination and Toxicology 38, 522e529. Custer, T.W., Custer, C.M., Dickerson, K., Allen, K., Melancon, M.J., Schmidt, L.J., 2001. Polycyclic aromatic hydrocarbons, aliphatic hydrocarbons, trace elements, and monooxygenase activity in birds nesting on the North Platte River, Casper, Wyoming, USA. Environmental Toxicology and Chemistry 20, 624e631. Custer, T.W., Custer, C.M., Larson, S., Dickerson, K.K., 2002. Arsenic concentrations in house wrens from Whitewood Creek, South Dakota, USA. Bulletin of Environmental Contamination and Toxicology 68, 517e524. Custer, T.W., Dummer, P.M., Custer, C.M., Warburton, D., Melancon, M.J., Hoffman, D.J., Matson, C.W., Bickham, J.W., 2007b. Effects of water level management on contaminant exposure to tree swallows nesting on the Upper Mississippi River. Environmental Monitoring and Assessment 133, 335e345. Fairchild, W.L., Muir, D.C.G., Currie, R.S., Yarechewski, A.L., 1992. Emerging insects as a biotic pathway for movement of 2,3,7,8-tetrachlorodibenzofuran from lake sediments. Environmental Toxicology and Chemistry 11, 867e872. Gerrard, P.M., St. Louis, V.L., 2001. The effects of experimental reservoir creation on the bioaccumulation of MeHg and reproductive success of tree swallows (Tachycineta bicolor). Environmental Science and Technology 35, 1329e1338. Henny, C.J., Hill, E.F., Hoffman, D.J., Spalding, M.G., Grove, R.A., 2002. Nineteenth century mercury: hazard to wading birds and cormorants of the Carson River, Nevada. Ecotoxicology 11, 213e231. Hensler, G.L., Nichols, J.D., 1981. The Mayfield methods of estimating nesting success: a model, estimators and simulation results. Wilson Bulletin 93, 42e53. Hoffman, D.J., Heinz, G.H., 1998. Effects of Hg and selenium on glutathione metabolism and oxidative stress in mallard ducks. Environmental Toxicology and Chemistry 17, 161e166. Hoffman, D.J., Ohlendorf, H.M., Marn, C.M., Pendleton, G.W., 1998. Association of Hg and selenium with altered glutathione metabolism and oxidative stress in diving ducks from the San Francisco Bay region, USA. Environmental Toxicology and Chemistry 17, 167e172. Hosmer, D.W., Lemeshow, S., 1989. Applied Linear Regression. John Wiley and Sons, New York. Johnson, E.J., Best, L.B., Heagy, P.A., 1980. Food sampling biases associated with the ‘‘ligature method’’. Condor 82, 186e192.

King, K.A., Custer, T.W., Weaver, D.A., 1994. Reproductive success of barn swallows nesting near a selenium-contaminated lake in east Texas, USA. Environmental Pollution 84, 53e58. Krabbenhoft, D.P., 1996. Mercury Studies in the Florida Everglades. U.S. Geological Survey Fact Sheet FS-166-96. Kraus, M.L., 1989. Bioaccumulation of heavy metals in pre-fledgling tree swallows, Tachycineta bicolor. Bulletin of Environmental Contamination and Toxicology 43, 407e414. Kruskal, J.B., 1964. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29, 1e27. Longcore, J.R., Haines, T.A., Halteman, W.A., 2007. Mercury in tree swallow food, eggs, bodies, and feathers at Acadia National Park, Maine, and an EPA superfund site, Ayer, Massachusetts. Environmental Monitoring and Assessment 126, 129e143. Mayfield, H., 1961. Nesting success calculated from exposure. Wilson Bulletin 73, 255e261. Mayfield, H., 1975. Suggestions for calculating nest success. Wilson Bulletin 87, 456e466. McCarty, J.P., 2001. Use of tree swallows in studies of environmental stress. Reviews of Toxicology 4, 61e104. McCullagh, P., Nelder, J.A., 1989. Generalized Linear Models, second ed. Chapman and Hall, London. Mengelkoch, J.M., Niemi, G.J., Regal, R.R., 2004. Diet of the nestling tree swallow. Condor 106, 423e429. Quinney, T.E., Ankney, C.D., 1985. Prey size selection by tree swallows. Auk 102, 245e250. Robertson, R.J., Stutchbury, B.J., Cohen, R.R., 1992. Tree swallow Tachycineta bicolor. In: Poole, A., Stettenhein, P., Gill, F. (Eds.), The Birds of North America, No. 11. The Academy of Natural Sciences/The American Ornithologist Union, Philadelphia, Pennsylvania/Washington, DC. Sando, S.K., Krabbenhoft, D.P., Johnson, K.M., Lundgren, R.F., Emerson, D.G., 2007. Mercury and Methylmercury in Water and Bottom Sediments of Wetlands at Lostwood National Wildlife Refuge, North Dakota, 2003e04. U.S. Geological Survey Scientific Investigations Report 2007e5219, 66 pp. Thompson, D.R., 1996. Mercury in birds and terrestrial mammals. In: Beyer, W.N., Heinz, G.H., Redmon-Norwood, A.W. (Eds.), Environmental Contaminants in Wildlife, Interpreting Tissue Concentrations. Society of Environmental Toxicology and Chemistry Special Publication Series. Lewis Publishers, New York, pp. 341e356. US Department of the Interior, 1998. Guidelines for Interpretation of the Biological Effects of Selected Contaminants in Biota, Water, and Sediment. National Irrigation Water Quality Program Information Report 3, Denver, Colorado. Wiener, J.G., Krabbenhoft, D.F., Heinz, G.H., Scheuhammer, A.M., 2003. Ecotoxicology of mercury. In: Hoffman, D.J., Rattner, B.A., Burton Jr., G.A., Cairns Jr., J. (Eds.), Handbook of Ecotoxicology, vol. 2. Lewis Publishers, New York, pp. 409e463.