Effects of mercury exposure on the reproductive success of tree swallows (Tachycineta bicolor)

Ecotoxicology (2008) 17:133 141 DOI 10.1007/s10646-007-0163-z Effects of mercury exposure on the reproductive success of tree swllows (Tchycinet bicolor) Rebeck L. Brsso Æ Dniel A. Cristol Accepted: 20 July 2007 / Published online: 14 August 2007 Ó Springer Science+Business Medi, LLC 2007 Abstrct An experimentl tree swllow popultion ws estblished in the hedwters of the Shenndoh River, Virgini, USA to ssess the ccumultion nd effects of mercury contmintion on birds tht et emergent qutic insects. One tributry, the South River, ws contminted with mercury before 1950. Reproductive success of swllows nesting within 50 m of this river ws compred to tht of three uncontminted reference tributries in 2005 nd 2006. Femle swllows on the contminted stretch of river hd significntly elevted blood nd fether totl mercury (blood: 3.56 ± 2.41 ppm ww vs. 0.17 ± 0.15 ppm reference; fether: 13.55 ± 6.94 ppm vs. 2.34 ± 0.87 ppm reference), possibly the highest ever reported for n insectivorous songbird. Insects collected by the swllows to be fed to nestlings verged 0.97 ± 1.11 ppm dw totl mercury, significntly higher thn on reference sites. Swllows in the contminted re produced fewer fledglings thn those in reference res. The effect of mercury contmintion on productivity ws detectble only for young femles in the contminted re tht were breeding for the first time in 2006, segment of the popultion tht my lredy hve been stressed by inexperience. Tree swllows served s prcticl nd effective biomonitors for mercury levels nd effects nd hve gret potentil s proxy biomonitors for more logisticlly chllenging birds such s loons or egles. Keywords Mercury Productivity Tree swllow Tchycinet bicolor Reproductive success R. L. Brsso D. A. Cristol (&) Deprtment of Biology, Institute for Integrtive Bird Behvior Studies, The College of Willim nd Mry, P.O. Box 8795, Willimsburg, VA 23187-8795, USA e-mil: dcris@wm.edu Introduction The tree swllow (Tchycinet bicolor), n insectivorous psserine, is found cross North nd Centrl Americ (Robertson et l. 1992). Adults typiclly forge within 400 m of their nests nd remin even closer when feeding nestlings (McCrty 2001; Mengelkoch et l. 2004). Thus, most contminnts ccumulted by swllows during the breeding seson originte from smll re round the nest. Tree swllows hve been used in mny studies of environmentl contminnts, including mercury, PCBs, nd pesticides. As of 2006, there were t lest 44 completed or on-going studies in North Americ on the uptke of contminnts nd the effects of nthropogenic stressors in tree swllows (McCrty 2001). Despite the growing use of this species, mny studies hve reported lck of significnt reproductive or survivorship responses to these environmentl stressors (McCrty 2001). Reproduction hs been identified s one of the most sensitive endpoints of mercury toxicity, primrily from cptive dosing studies (Wolfe et l. 1998). Decreses in reproductive success of 35 50% hve been observed in birds with high dietry methylmercury uptke, even in the bsence of impirment in the dults (USDI 1998). In generl, effects such s decresed egg weight, htchbility, nd chick survivl re seen t egg mercury levels of 0.5 6.0 ppm ww in lbortory studies (Thompson 1996; Burger nd Gochfield 1997). Impirments nd deformities of chicks occur t mercury concentrtions s low s 1.0 ppm ww in lbortory-dosed eggs (Heinz nd Hoffmn 2003). Reproductive effects hve been more elusive in field studies, but one recent exmple is tht egg volumes in common loons (Gvi immer) decresed s mercury loding of femles incresed (Evers et l. 2003). Another study suggests tht brin mercury residues

134 R. L. Brsso nd D. A. Cristol >2.0 ppm in dult loons my hve led to reduced territoril drive, decresed incubtion nd bndonment of territories (Brr 1986). No growth deformities or other reproductive effects relted to mercury contmintion hve been reported in tree swllows. Between 1929 nd 1950 mercuric sulfte entered the South River ( tributry to the South Fork Shenndoh River) from n cette fiber mnufcturing plnt in Wynesboro, Virgini, USA (Crter 1977). To ssess the mount of mercury recently ccumulted by dult nd nestling tree swllows long this polluted tributry, we smpled blood from dults nd nestlings during the nestling period. To eliminte the influence of tmospheric deposition or bckground mercury contmintion, we compred mercury levels of birds nesting long the contminted South River to the levels of birds from reference res on three nerby uncontminted rivers in the sme wtershed. Reproductive success ws monitored throughout two breeding sesons to compre clutch size nd dte of initition, egg volume nd htchbility, nd offspring survivl. Methods Study design This study ws crried out on the contminted portion of the South River (pproximtely 40 km). The North nd Middle Rivers, s well s the section of the South River upstrem of Wynesboro, were the uncontminted reference res (Fig. 1). A pilot study ws lso crried out downstrem of the confluence of the contminted nd reference rivers on the South Fork Shenndoh River in 2005. Beginning in Februry 2005, we erected 102 nest boxes in the contminted re on the South nd South Fork Fig. 1 Mp of nest box sites long the South, Middle, North, nd South Fork Shenndoh Rivers, August nd Rockinghm counties, Virgini, USA. Blck circles re nest box clusters in contminted res; grey circles re nest box clusters in reference res. The source of contmintion is lbeled with n sterisk in Wynesboro

Mercury nd reproduction in tree swllows 135 Shenndoh Rivers, nd 89 nest boxes in reference res on the South, Middle, nd North Rivers. All nest boxes long the South Fork Shenndoh River (n = 42) were removed before the 2006 breeding seson, fter it ws determined tht mercury levels were intermedite between the contminted nd reference res, nd these were not included in ny nlyses. We incresed the number of nest boxes to 119 in the contminted re nd 167 in the reference res prior to the 2006 breeding seson. Nest boxes were 25 50 m prt with the entrnce holes oriented towrds the river. We checked them weekly beginning in the first week of April. We incresed checking to every 3 4 dys beginning in the first week of My, nd then removed nesting mteril from nest boxes fter the chicks hd fledged. We did not include dt from lte femles inititing nests fter the first round of nesting: 3 June, 2005 or 2 June, 2006. Femle tree swllows mintin brown plumge until the end of their second summer nd thus cn be identified in the field s second-yer (herefter, SY ), in contrst to blue-plumged, fter-second yer (herefter, ASY ) femles. Mercury smpling We used smll guge (26G ½ in.) needle to puncture the cutneous ulnr vein, nd then collected pproximtely 100 ll of blood in three 75 ll heprinized cpillry tubes. Tubes were seled with Crito-cps 1 nd plced into 10cc BD 1 vcutiner to prevent brekge. Smples were stored on ice for 3 6 h, fter which they were frozen t 25 C until nlysis. Fether smples in this study were collected from subsmple of ASY femles in 2006 to provide longerterm estimte of body-burden during the previous breeding seson. These fethers lso provide comprbility with other studies in which fethers, but not blood, hve been smpled. When birds bnded in 2005 returned to the breeding grounds in 2006, we plucked the innermost primry fether (P1) from ech wing. As fether molt typiclly begins in July (Stutchbury nd Rohwer 1990), the mercury present in P1 during the 2006 breeding seson would indicte body burden from 2005. Prey smpling Becuse we cptured swllows s they entered nest boxes to feed nestlings, we were usully ble to collect the bolus of food in glss jr directly from the prent s bek. These were weighed s whole bolus, frozen, identified to orders, freeze dried, re-weighed, homogenized nd nlyzed for mercury. Lbortory nd sttisticl nlysis Results re reported only for dult femles unless otherwise noted. All mercury nlysis took plce t the Trce Element Reserch Lbortory of Texs A&M University. Smples were nlyzed for totl mercury with Milestone 1 DMA 80 using cold vpor tomic bsorption spectroscopy. Becuse pproximtely 95% of the mercury in vin blood nd fethers is MeHg (Evers et l. 2005), totl mercury vlues will ccurtely reflect the mount of MeHg present. Prey items, which were primrily insects in the orders Dipter nd Ephemeropter, were not nlyzed for MeHg. Smples were homogenized to llow representtive liquot to be tken for nlysis nd typiclly weighed 0.01 g. Reproductive success prmeters We determined the dte of clutch initition by the presence of fresh egg during our frequent nest box checks. The initition dte of the first clutch in the entire study re ws denoted Julin dy 1 in nlyses (29 April in 2005, 18 April in 2006). The proportion of eggs tht htched ws the number of htchlings divided by the mximum clutch size. The number of nestlings tht left the nest (fledglings) ws our primry mesure of productivity. This ws determined by counting the number of nestlings live on the lst visit (dy 14 16 post-htching) nd then subtrcting ny ded nestlings found on the post-fledging visit. Productivity ws lterntely expressed s proportion of htched nestlings tht fledged, to emphsize ny mortlity differences during the nestling period. Finlly, to correct for differentil femle effort (i.e., clutch size vrition) we estimted productivity s the proportion of eggs tht survived to fledge. In 2006 we mesured 94 eggs from 16 nests in the contminted re nd 79 eggs from 14 nests from reference res. The mximum length nd width of ech egg ws mesured to the nerest 0.1 mm. Egg volume (V) ws determined by the formul, V ¼ LW 2 0:51 where L = length, W = width, nd 0.51 is the volume coefficient constnt (Hoyt 1979). The South River is referred to s the contminted tretment throughout. Sttisticl nlyses were done using MINITAB sttisticl softwre (version 14.2, LEAD Technologies, Stte College, PA). Mercury levels nd nesting success were compred using n nlysis of vrince. We combined ll dt from femles in both yers nd used tretment group, femle ge, nd yer s fctors with

136 R. L. Brsso nd D. A. Cristol tretment group femle ge, tretment group yer, femle ge yer, nd tretment group femle ge yer s interction terms. Tukey s HSD test ws used for multiple post-hoc comprisons. We report only those fctors nd interctions tht were significnt (P < 0.05). All mens re presented ± SD, except in figures where SE is used. The proportion of eggs htched, nestlings fledged, nd eggs fledged were normlized by rcsine squre-root trnsformtion before sttisticl nlysis, but untrnsformed dt re shown. Results Mercury level There ws significnt effect of tretment on the blood mercury levels of dult femles cross both yers (F 1,116 = 89.41, P < 0.0001). The blood mercury level of femles nesting in the contminted re (3.56 ± 2.41 ppm) ws more thn n order of mgnitude higher thn tht of reference femles (0.17 ± 0.15 ppm). Mercury level in femles lmost doubled from 2005 to 2006 (2005: 2.29 ± 1.48 ppm; 2006: 4.14 ± 2.53 ppm; F 1,116 = 4.94, P = 0.02; Fig. 2). Only in 2006 were there enough ASY femles to compre the ge clsses. Post-hoc comprison indicted tht mercury level ws significntly higher in ASY thn SY femles (Tukey s HSD 95% CI: 3.01, 0.01). Broods of nestling tree swllows in the contminted re hd higher mercury levels thn broods in reference res in 2005 (contminted: 0.23 ± 0.17 ppm, reference: 0.02 ± 0.04 ppm; F 1,37 = 29.26, P < 0.0001). To llow comprisons with studies in which sexes re not seprted, we lso report the mercury level in ll mles from the contminted re (4.22 ± 2.43 ppm), nd ll dult swllows in the contminted re (3.69 ± 2.40 ppm). The totl mercury of fethers tht grew during the 2005 breeding seson ws significntly relted to the mercury level in blood smpled from the sme birds (F 1,24 = 51.50, r 2 = 0.68, P < 0.0001; Fig. 3). There ws significnt effect of tretment on fether mercury level (F 1,21 = 23.04, P < 0.0001); the fether mercury level of femles nesting in the contminted re (13.55 ± 6.94 ppm) ws lmost six fold higher thn tht of reference femles (2.34 ± 0.87 ppm). Effects on eggs There ws no detectble difference between contminted nd reference femles in terms of clutch initition dte (F 1,178 = 0.15, P = 0.70) or clutch size (F 1,178 = 0.49, P = 0.48; Tble 1). There ws significnt effect of femle ge on clutch initition dte (F 1,178 = 15.35, P = 0.0001), with ASY femles nesting pproximtely 4 dys erlier thn SY femles. There ws lso significnt effect of yer on clutch initition dte (F 1,178 = 33.62, P < 0.0001). The nesting seson begn n verge of five dys erlier in the contminted nd seven dys erlier in reference res in 2006 thn it did in 2005. ASY femles lso hd lrger clutches thn SY femles (F 1,178 = 7.29, P = 0.008) cross both yers by pproximtely 0.5 eggs. There ws no detectble effect of tretment (F 1,178 = 2.55, P = 0.11; Tble 1) or femle ge (F 1,178 = 2.64, P = 0.11) on the proportion of eggs tht htched cross both yers. However, there ws significnt effect of yer (F 1,178 = 5.48, P = 0.02); the men proportion of eggs htched per clutch ws lower in 2006 thn in 2005 (Tble 1). 5 b 38 30 Femle blood mercury (ppm) 4 3 2 1 0 19 2005 2006 Contminted c 29 c 38 2005 2006 Reference Fether mercury (ppm) 25 20 15 10 5 0 0 1 2 3 4 Blood mercury (ppm) y = 2.419 + 4.024 x 5 6 Fig. 2 Adult femle blood mercury levels were significntly higher in 2006 thn in 2005 in contminted res (ANOVA, F 1,116 = 4.94, P = 0.02). There ws no difference in mercury levels of dult birds in reference res between 2005 nd 2006. Error brs represent one SE of the men. Brs with different letters differed significntly Fig. 3 Reltionship between fether nd blood mercury for individul femle tree swllows (r 2 = 0.68, P < 0.0001). Fethers grew t the end of the breeding seson in which the blood ws collected. Closed circles represent individuls from the contminted re; open circles represent individuls from reference res

Mercury nd reproduction in tree swllows 137 Tble 1 Comprison of nesting success between tretments nd yers Prmeter Yer C or R N Men SD Clutch size 2005 Contminted 27 5.56 0.85 2005 Reference 46 5.80 0.83 2006 Contminted 67 5.76 0.89 2006 Reference 98 5.80 0.92 Proportion eggs htched 2005 Contminted 26 0.93 0.09 2005 Reference 45 0.93 0.17 2006 Contminted 67 0.76 0.28 2006 Reference 98 0.87 0.22 Proportion nestlings fledged 2005 Contminted 26 0.91 0.17 2005 Reference 44 0.91 0.24 2006 Contminted 60 0.83 0.31 2006 Reference 93 0.95 0.16 Proportion eggs fledged 2005 Contminted 26 0.85 0.17 2005 Reference 44 0.86 0.25 2006 Contminted 60 0.69 0.30 2006 Reference 93 0.86 0.22 Number fledglings produced 2005 Contminted 26 4.65 1.09 2005 Reference 44 5.05 1.66 2006 Contminted 60 4.00 1.89 2006 Reference 93 5.06 1.48 The proportion of eggs tht survived to produce fledgling ws significntly lower in the contminted re (F 1,173 = 8.00, P = 0.005). Post-hoc comprisons indicted significnt difference between the contminted nd reference res in 2006 (Tukey s HSD 95% CI: 0.15, 0.46; Tble 1); however, no corresponding difference ws detected in 2005. Among femles in the contminted re in 2006, the proportion of eggs fledged ws significntly higher for ASY femles thn for the younger SY femles (Tukey s HSD 95% CI: 0.51, 0.10). ASY femles in the contminted re did not differ from those in reference res in terms of the proportion of eggs producing fledglings, wheres SY femles in the contminted re were significntly lower thn SY reference femles (Tukey s HSD 95% CI: 0.12, 0.54; Tble 2). In 2006, we mesured volume of eggs t rndom subsmple of nests in the contminted nd reference res. Reference eggs were lrger thn those from the contminted re (F 1,151 = 13.57, P < 0.0001); however, there ws significnt interction of femle ge nd tretment group (F 1,151 = 14.45, P < 0.0001) such tht SY femles lid smller eggs thn ASY femles in the contminted re, but not the reference res (Fig. 4). Post-hoc comprisons indicte tht SY femle eggs in the contminted re were significntly smller thn both SY (Tukey s HSD 95% CI: 0.12, 0.51) nd ASY (Tukey s HSD 95% CI: 0.10, 0.45) eggs in reference res. There ws no difference in egg size between the ge clsses in the reference res. Eggs from ASY femles in the contminted re were not significntly different in size from SY (Tukey s HSD 95% CI: 0.09, 0.16) or ASY (Tukey s HSD 95% CI: 0.10, 0.09) eggs in reference res (Fig. 4). It should be noted tht we did not smple n dequte number of SY femles to drw nything but tenttive conclusions bout egg volume. Effects on nestlings Femles in the contminted re produced fewer fledglings (F 1,173 = 9.54, P = 0.002); there ws significnt effect of femle ge (F 1,173 = 6.34, P = 0.01) nd significnt interction between yer nd femle ge (F 1,173 = 4.34, P = 0.04). In 2006, femles nesting in the contminted re produced fewer fledglings thn reference femles (Tukey s HSD 95% CI: 0.43, 1.74); however, no corresponding difference ws found in 2005 (Tble 1). SY femles in the contminted re produced significntly fewer fledglings thn ASY femles in the contminted re (Tukey s HSD 95% CI: 3.05, 0.73) or either ge clss in reference res (Tukey s HSD 95% CI ASY: 1.48, 3.58; SY: 0.31, 2.73), but only in 2006 (Fig. 5). When we mesured productivity s proportion of nestlings tht survived to fledge, rther thn bsolute number of fledglings, the results were similr. Femles in the

138 R. L. Brsso nd D. A. Cristol Tble 2 Comprison of nesting success between femle ge clsses in 2006 Prmeter C or R Age N Men SD Clutch initition dy Contminted ASY 33 15.61 8.54 Contminted SY 28 23.86 9.20 Reference ASY 58 15.90 6.29 Reference SY 28 21.75 7.93 Clutch size Contminted ASY 33 6.03 0.81 Contminted SY 28 5.57 0.92 Reference ASY 58 6.03 0.72 Reference SY 28 5.43 0.96 Proportion eggs htched Contminted ASY 33 0.88 0.18 Contminted SY 28 0.76 0.19 Reference ASY 58 0.92 0.15 Reference SY 28 0.87 0.17 Proportion nestlings fledged Contminted ASY 33 0.92 0.17 Contminted SY 26 0.72 0.40 Reference ASY 57 0.98 0.06 Reference SY 27 0.94 0.12 Proportion eggs fledged Contminted ASY 33 0.81 0.22 Contminted SY 26 0.54 0.33 Reference ASY 57 0.90 0.16 Reference SY 27 0.83 0.21 Number fledglings produced Contminted ASY 33 4.85 1.42 Contminted SY 26 2.96 1.93 Reference ASY 57 5.49 1.21 Reference SY 27 4.48 1.31 contminted re fledged smller proportion of nestlings (F 1,173 = 4.22, P = 0.04) nd there ws gin significnt interction of femle ge nd yer (F 1,173 = 4.73, P = 0.03). Post-hoc comprisons indicted only SY femles in 2006 experienced reduction in the proportion of nestlings fledged. (mm^3) Egg volume 2.0 1.6 1.2 0.8 0.4 78 (13) b 10 (2) 47 (8) 20 (4) Number fledglings produced 6 5 4 3 2 33 b 26 57 27 0.0 ASY SY Contminted ASY SY Reference Fig. 4 SY femles in the contminted res lid smller eggs thn ASY femles in contminted nd reference res (ANOVA, F 1,151 = 14.45, P < 0.0001). Eggs of SY femles in contminted res were smller thn eggs of SY femles in reference res (Tukey s HSD 95% CI: 0.12, 0.51). Error brs represent one SE of the men. Smple size, totl number of eggs mesured, nd number of clutches mesured (in prenthesis) provided bove the error br. Brs with different letters differed significntly 1 0 ASY SY Contminted ASY SY Reference Fig. 5 In 2006, SY femles in contminted res produced significntly fewer fledglings thn ll other femles. The number of fledglings produced by ASY femles in the contminted res did not differ significntly from SY or ASY femles in reference res. Error brs represent one SE of the men. Brs with different letters differed significntly. See text for sttisticl nlysis

Mercury nd reproduction in tree swllows 139 Effects of individul mercury levels We used liner regression to test for reltionship between reproductive success nd the level of mercury in n individul femle s blood, using ll femles. The four mesures relted to htching nd survivorship of eggs or nestlings ll hd significnt, negtive reltionships with blood mercury concentrtions of femle swllows (Tble 3); however, the reltively low r 2 vlues indicte wek reltionships with little explntory power. Mercury in prey items Insects brought bck to nestlings hd significntly higher totl mercury levels on contminted sites (0.97 ± 1.11 ppm dw, n = 29 boluses) thn those on reference sites (0.04 ± 0.04 ppm dw, n = 27 boluses; Mnn-Whitney test P < 0.0001). Becuse prey ws delivered in lrge boluses contining 1 57 invertebrtes, it ws not possible to pinpoint the species of invertebrtes delivering the most mercury. Of the four highest boluses, two contined only Dipterns (flies, including some, but not ll species with qutic lrve), nd two contined only Ephemeropterns (myflies with qutic lrve). Overll, 60% of the 953 individuls identified were Dipter, nd 22% were Ephemeropter, with the rest coming from t lest eight other invertebrte orders, including terrestril Arne (spiders), Coleopter (beetles) nd Homopter (true bugs). Discussion A popultion of tree swllows estblished in 2005 on contminted hedwter tributry of the Shenndoh River hd elevted mercury levels. Adult femles in the contminted re verged more thn 3.00 ppm totl mercury Tble 3 Reltionship of blood mercury concentrtion in femles tree swllows to mesured reproductive prmeters Prmeter n r 2 F P Clutch initition 118 0.002 0.24 0.62 Clutch size 118 0.009 1.11 0.30 Proportion eggs htched 118 0.07 8.37 0.005 * Proportion nestlings fledged 114 0.04 4.49 0.04 * Proportion eggs fledged 114 0.12 15.09 <0.001 * Number fledglings produced 114 0.08 9.05 0.003 * Averge egg size 13 0.07 0.88 0.37 * Indictes significnt reltionship Smple size is number of broods in blood, n order of mgnitude higher thn tht in the nerby reference res, nd perhps the highest vlue ever reported for songbird popultion. Mercury levels unexpectedly doubled between 2005 nd 2006, perhps due to incresed methylmercury vilbility resulting from extreme drought. Other explntions for the increse, such s greter bioccumultion by returning individuls, chnges in nest box loctions, or incresed tmospheric deposition re not consistent with our findings (Brsso 2007). Mercury in nestling blood, while elevted over tht of nestlings in reference res, ws n order of mgnitude lower thn tht of dults in the contminted re. This is consistent with the literture, s nestling birds pprently eliminte lrge mounts of blood mercury into their growing fethers (Splding et l. 2000). Femles in the contminted re produced fewer fledglings thn reference femles. This difference ws most pronounced in femles nesting for the first time (SY femles) in 2006. SY femles in the contminted re fledged pproximtely two fewer nestlings thn older (ASY) femles in contminted or reference res, nd pproximtely one less fledgling thn SY reference femles. Preliminry evidence suggests tht SY femles lso produced smller eggs thn other femles. In tree swllows, egg size nd qulity re directly relted to offspring survivl; clutches of lrger eggs produce more nd lrger nestlings tht grow fster (Ardi et l. 2006). Nesting in the contminted re did not detectbly ffect clutch size, clutch initition dte or htchbility of eggs. This is consistent with t lest one other study of mercury contmintion in songbird; gret tits nesting long contmintion grdient in Belgium did not vry in terms of clutch initition dtes nd clutch sizes (Jnssens et l. 2003). Contminted femles could suffer reduced reproductive success if they (1) under-provisioned eggs, (2) deposited enough mercury into eggs to reduce embryo vibility, or (3) filed to feed nestlings properly due to behviorl problems. Our results re consistent with the first explntion, becuse our preliminry dt indicte tht eggs of two SY femles in the contminted res were significntly undersized. Htchbility of eggs did not differ between contminted nd reference res, suggesting tht embryo vibility ws not ffected. SY femles in the contminted re my lso hve been feeding their nestlings less, becuse survivl rte ws depressed, but direct exmintion of feeding rtes is needed to test this hypothesis. We propose tht the combintion of inexperience nd mercury contmintion my hve led to smller eggs nd subsequent decresed offspring survivl. The fct tht this ws more evident in 2006 could hve been due to environmentl stress such s reduced food vilbility or to the higher mercury levels tht yer. Both nutritionl stress

140 R. L. Brsso nd D. A. Cristol Tble 4 Comprison of tree swllow mercury levels long the South River to other studies using tree swllows s biomonitors Loction Species (ge) Tissue reported Blood Hg Author(s) ELARP, Cnd TRES (nestling) 0.13 ppm dw (whole body) Gerrrd nd St Louis (2001) Minnesot TRES (nestling) 0.13 0.24 ppm dw (whole body) Custer et l. (2006) ELARP, Cnd TRES (nestling) 1.21 ppm dw (fether) Gerrrd nd St Louis (2001) South River, VA TRES (nestling) 0.23 ppm ww This study Minnesot TRES (dult) 0.25 ppm ww (egg) 0.63 ppm ww Custer et l. (2006) Gret Lkes TRES (dult) 0.66 ppm ww (egg) 1.65 ppm ww Bishop et l. (1995) Msschusetts TRES (dult) 0.41 ppm ww (blood) Evers et l. (2005) South River, VA TRES (dult) 3.69 ppm ww This study Estimted blood mercury level bsed on inter-tissue comprtive rtio (Evers et l. 2005) nd higher methylmercury vilbility could hve resulted from the complete bsence of rin during 2006, but we did not directly mesure mercury or food vilbility. Though SY nd ASY femle tree swllows re esily distinguishble from ech other, this is the first report of ge-relted differences in the effects of mercury on reproduction in this or other species. Our finding tht blood mercury concentrtions mong individul femle swllows did not strongly predict their nesting success ws not novel. Bld egles (Hlieetus leucocephlus) nesting t lke with similr exposure to mercury s tree swllows in the present study did not show strong reltionship of eglet mercury level with productivity (Weech et l. 2006). As eglet blood nd dult egle blood were highly correlted, one cn deduce tht no reltionship existed between dult mercury nd productivity. The sme vribility of individul response to contminnts hs been reported for tree swllows nesting on PCB-contminted sites (Custer et l. 1998; Custer et l. 2003). Tree swllows s biomonitors for mercury A focus on mercury contmintion s solely n qutic problem (Weiner et l. 2003) hs led to the overwhelming use of piscivores s biomonitors. Mercury ccumultion in tree swllows hs been documented in severl studies in Cnd nd the northestern United Sttes. However, the mercury levels reported from the destructive smpling of nestling birds nd eggs in those studies mkes direct comprison with the non-lethl blood mercury levels reported here difficult. Evers et l. (2005) proposed rtio relting mercury levels in different tissues of common loons. The rtio of fether:blood (6:1) ccurtely predicted the 6:1 fether-to-blood rtio derived from dt for bld egles reported by Weech et l. (2006), nd tht of tree swllows in the present study (5.8:1), nd thus cn be used cutiously s n pproximtion to compre blood mercury concentrtions in our tree swllows to other published mercury dt for this species (Tble 4). The levels reported here for dult tree swllows of both sexes re the highest ever reported for this species. Across both yers of our study only 11% of dult swllows smpled in the contminted re hd blood mercury under 1.00 ppm; only 3% were below 0.50 ppm. In fct, dult belted kingfishers (Ceryle lcyon), obligte piscivores, nesting long the South River in 2005 2006, were no higher thn swllows, with blood mercury verging 3.35 ± 2.67 ppm (n = 21, unpublished dt). In this study of riverine mercury point source, tree swllows ccumulted mercury from contminted insects, some of which hd qutic lrve, to the sme level s piscivorous species. Becuse we were ble to quickly recruit lrge breeding popultion of swllows to specified reference nd contminted loctions, we detected subtle reproductive effects tht my hve been missed in twoyer study of one of the more populr species used s biomonitors for mercury. While most studies focus on piscivorous species (Scheuhmmer et l. 2007), tree swllows should be considered n importnt prt of the vin biomonitoring tool kit. Acknowledgements Funding ws provided by E. I. DuPont de Nemours, the Ntionl Science Foundtion UBM 0436318, nd the Office of the Vice Provost for Reserch t the College of Willim & Mry. We thnk Anne Condon, Rchel Fovrgue, Scott Friedmn, Kelly Hllinger, Dn Hwley, Rvi Jefferson George, Sen Koebley, Liz Lnger, Mryse Lendre, Adrin Monroe, Jck Reese, nd Ariel White for ssistnce with fieldwork. We re lso indebted to ll of the coopertive lndowners in the Shenndoh Vlley, grdute committee members John Swddle nd Rndy Chmbers, nd the entire South River Science Tem. References Ardi DR, Wsson MF, Winkler DW (2006) Individul qulity nd food vilbility determine yolk nd egg mss nd egg composition in tree swllows Tchycinet bicolor. J Avin Biol 37:252 259

Mercury nd reproduction in tree swllows 141 Brr JF (1986) Popultion dynmics of the common loon (Gui immer) ssocited with mercury-contminted wters in northwestern Ontrio. Cndin Wildlife Service, Ottw, Ontrio, Cnd Bishop CA, Koster MD, Chek AA, Hussell DJT, Jock K (1995) Chlorinted hydrocrbons nd mercury in sediments, red-winged blckbirds (Agelius phoeniceus) nd tree swllows (Tchycinet bicolor) from wetlnds in the Gret Lkes-St. Lwerence River Bsin. Environ Toxicol Chem 14:491 501 Brsso R (2007) The effects of mercury on the nesting success nd return rte of tree swllows (Tchycinet bicolor). Msters thesis. The College of Willim nd Mry, Willimsburg, VA, USA Burger J, Gochfield M (1997) Risk, mercury levels, nd birds: relting dverse lbortory effects to field biomonitoring. Environ Res 75:160 172 Crter LJ (1977) Chemicl plnts leve unexpected legcy for two Virgini rivers. Science 198:1015 1020 Custer CM, Custer TW, Allen PD, Stromborg KL, Melncon, MJ (1998) Reproduction nd environmentl contmintion in tree swllows nesting in the Fox River dringe nd Green By, Wisconsin, USA. Environ Toxicol Chem 17:1786 1798 Custer CM, Custer TW, Dummer PM, Munney KL (2003) Exposure nd effects of chemicl contminnts on tree swllows nesting long the Houstonic River, Berkshire County, Msschusetts, USA, 1998 2000. Environ Toxicol Chem 22:1605 1621 Custer CM, Custer TW, Wrburton D, Hoffmn DJ, Bickhm JW, Mtson CW (2006) Trce element concentrtions nd bioindictor responses in tree swllows from northwestern Minnesot. Environ Monit Assess 118:247 266 Evers DC, Tylor KM, Mjor A, Tylor RJ, Poppeng RH, Scheuhmmer AM (2003) Common loon eggs s indictors of methylmercury vilbility in North Americ. Ecotoxicology 12:69 81 Evers DC, Burgess NM, Chmpoux L, Hoskins B, Mjor A, Goodle WM, Tylor RJ, Poppeng R, Digle T (2005) Ptterns nd interprettion of mercury exposure in freshwter vin communities of northestern north Americ. Ecotoxicology 14:193 221 Gerrrd PM, St Louis VL (2001) The effects of experimentl reservoir cretion on the bioccumultion of methylmercury nd reproductive success of tree swllows (Tchycinet bicolor). Environ Sci Technol 35:1329 1338 Heinz GH, Hoffmn DJ (2003) Predicting mercury in mllrd ducklings from mercury in choriollntoic membrnes. Bull Environ Contmin Toxicol 70:1242 1246 Hoyt DF (1979) Prcticl methods of estimting volume nd fresh weight of bird eggs. Auk 96:73 77 Jnssens E, Duwe T, Pinxten R, Eens M (2003) Breeding performnce of gret tits (Prus mjor) long grdient of hevy metl pollution. Environ Toxicol Chem 22:1140 1145 Mengelkoch JM, Niemi GJ, Regl RR (2004) Diet of the nestling tree swllow. Condor 106:423 429 McCrty JP (2001) Use of tree swllows in studies of environmentl stress. Rev Toxicol 4:61 104 Robertson RJ, Stutchbury BJ, Cohen RR (1992) Tree swllow. In: Poole A, Stettenheim P, Gill F (eds) The birds of North Americ, no. 11. Acdemy of Nturl Sciences, Phildelphi, nd Americn Ornithologists Union, Wshington DC Scheuhmmer AM, Meyer WM, Sndheinrich MB, Murry MW (2007) Effects of environmentl methylmercury on the helth of wild birds, mmmls, nd fish. Ambio 36:12 19 Splding MG, Frederick PC, McGill HC, Bouton SN, McDowell LR (2000) Methylmercury ccumultion in tissues nd its effects on growth nd ppetite in cptive gret egrets. J Wildl Dis 36:411 422 Stutchbury BJ, Rohwer S (1990) Molt ptterns in the tree swllow (Tchycinet bicolor). Cn J Zool 68:1468 1472 Thompson DR (1996) Mercury in birds nd terrestril mmmls. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmentl contminnts in wildlife: interpreting tissue concentrtions. Lewis Publishers, Boc Rton, FL, USA, pp 341 356 USDI (1998) Guidelines for the interprettion of the biologicl effects of selected constituents in biot, wter, nd sediment: mercury, Report No. 3. Ntionl irrigtion wter qulity progrm informtion, United Sttes Deprtment of the Interior Weech SA, Scheuhmmer AM, Elliott JE (2006) Mercury exposure nd reproduction in fish eting birds breeding in the Pinchi Lke region, British Columbi, Cnd. Environ Toxicol Chem 25:1433 1440 Weiner JG, Krbbenhoft DP, Heinz GH, Scheuhmmer AM (2003) Ecotoxicology of mercury. In: Hoffmn DJ,Rttner BA, Burton GA Jr, Cirns J Jr (eds) Hndbook of ecotoxicology. Lewis Publishing, Boc Rton, FL Wolfe MF, Schwrzbch S, Sulimn RA (1998) Effects of mercury on wildlife: comprehensive review. Environ Toxicol Chem 17:146 160