Science of the Total Environment 463-464 (2013) 42–50

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Riparian swallows as integrators of landscape change in a multiuseriver system: Implications for aquatic-to-terrestrialtransfers of contaminants

Jeremy M. Alberts a,⁎, S. Mažeika P. Sullivan b, A. Kautza b

a Department of Biological Sciences, University of Cincinnati, 2600 Clifton Ave., Cincinnati, OH 45221, United Statesb School of Environment & Natural Resources, The Ohio State University, 2021 Coffey Rd., Columbus, OH 43210, United States

H I G H L I G H T S

• We characterized the land use and land cover (LULC) of 11 riverine study sites.• We examined selenium (Se) and mercury (Hg) concentrations in riparian swallows.• Relationships were evident between LULC and contaminant concentrations.• Contaminant concentrations were higher in adult than in juvenile birds.

⁎ Corresponding author. Fax: +1 513 556 5299.E-mail address: albertjy@mail.uc.edu (J.M. Alberts).

0048-9697/$ – see front matter © 2013 Elsevier B.V. Allhttp://dx.doi.org/10.1016/j.scitotenv.2013.05.065

a b s t r a c t

a r t i c l e i n f o

Article history:Received 21 January 2013Received in revised form 12 May 2013Accepted 13 May 2013Available online xxxx

Editor: Christian E.W. Steinberg

Keywords:Riparian swallowsBiomagnificationAquatic–terrestrial linkages

Recent research has highlighted the transfer of contaminants from aquatic to terrestrial ecosystems via predation ofaquatic emergent insects by riparian consumers. The influence of adjacent land use and land cover (LULC) onaquatic-to-terrestrial contaminant transfer, however, has received limited attention. From 2010 to 2012, at 11river reaches in the Scioto River basin (OH, USA), we investigated the relationships between LULC and selenium(Se) andmercury (Hg) concentrations in four species of riparian swallows. Hg concentrations in swallowswere sig-nificantly higher at rural reaches than at urban reaches (t = −3.58, P b 0.001, df = 30),whereas Se concentrationswere positively associated with adjacent land cover characterized bymature tree cover (R2 = 0.49, P = 0.006). Toan extent, these relationships appear to bemediated by swallow reliance on aquatic emergent insects. For example,tree swallows (Tachycineta bicolor) at urban reaches exhibited a higher proportion of aquatic prey in their diet, fed ata higher trophic level, and exhibited elevated Se levels. We also found that both Se and Hg concentrations in adultswallowswere significantly higher than those observed in nestlings at both urban and rural reaches (Se: t = −2.83,P = 0.033, df = 3; Hg: t = −3.22, P = 0.024, df = 3). Collectively, our results indicate that riparian swallows in-tegrate contaminant exposure in linked aquatic–terrestrial systems and that LULC may strongly regulate aquaticcontaminant flux to terrestrial consumers.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction

Movement of materials across the landscape has been central to thestudy of food webs (Polis et al., 1997, 2004). At the aquatic–terrestrialinterface, ecological subsidies, or the flux of material from one habitator ecosystem to another (Nakano and Murakami, 2001) has emergedas a central theme of cross-boundary linkages (Akamatsu et al., 2004;Vander Zanden and Sanzone, 2004; Ballinger and Lake, 2006).Whereasthe contribution of terrestrial systems to aquatic foodwebs via inputs ofnutrients and organic matter is well recognized, recent investigationshave focused on the importance of aquatic prey subsidies to the energybudgets of riparian consumers (reviewed in Baxter et al., 2005).

rights reserved.

A classic example is the reliance of grizzly bears (Ursus arctos horribilis)on fish as an important nutrient source (Mattson and Reinhart, 1995;Varley and Schullery, 1996). Others have shown that aquatic preyrepresent important food sources to riparian bats (Fukui et al., 2006;Hagen and Sabo, 2012), raccoons (Procyon lotor) (Bigler et al., 1975;Lord et al., 2002), piscivorous birds (Vessel, 1978; Hamas, 1994), lizards(Sabo and Power, 2002), and terrestrial arthropods (Henschel et al.,2001; Paetzold et al., 2005; Dreyer et al., 2012).

In particular, aquatic insects that emerge from the stream as adults(hereafter, ‘aquatic emergent insects’) can be a critical food source forinsectivorous riparian bird species (Keast, 1990; Iwata et al., 2003).For example, Sweeney and Vannote (1982) found that swarmingactivity by mayflies attracted nighthawks (Chordeiles minor) to areasof emergence, and Iwata et al. (2003) reported that flycatchers andgleaners foraged intensively on aquatic emergent insects in a pattern

43J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50

that mirrored aquatic insect distribution, suggesting that the dynamicsof insect emergence can influence avian foraging behavior.

Within the context of the energetic pathways that link aquatic andterrestrial ecosystems, there is growing interest in food-web studiesat the land–water ecotone. Many investigators have found that thehigh reliance of riparian birds on aquatic prey resources can exposethem to contaminants found in aquatic systems (see Sullivan andRodewald, 2012). Cristol et al. (2008) demonstrated that mercury(Hg) can bioconcentrate in terrestrial bird species living near contam-inated water sources, while Wada et al. (2009) found that adreno-cortical responses and thyroid hormones were suppressed in treeswallows (Tachycineta bicolor) living near a river contaminatedwith mercury. In the Chilliwack River of southern British Columbia,resident American Dippers (Cinclus mexicanus) (i.e., those birds whoremain in the mainstem Chilliwack River year-round and have highproportions of contaminated salmon fry in their diet) were found tohave higher polychlorinated biphenyl (PCB) and Hg concentrationsthan their migratory counterparts (i.e., those birds who are foundon the Chilliwack mainstem only during the winter and that havea significantly smaller proportion of fish fry in their diet; Morrisseyet al., 2004). Several studies have described the bioconcentration ofPCBs in tree swallows from aquatic insect prey (Echols et al., 2004;Maul et al., 2006). Echols et al. (2004), for instance, found that PCBconcentrations in tree swallow nestlings closely tracked concentra-tions in aquatic insects. Maul et al. (2006) implicated aquatic insectsof the family Chironomidae as the key vector of PCBs to nestlingtree swallows from a lake in Illinois, USA.

Differences in age-related contaminant exposure patterns amongbirds have also been documented. For example, Malinga et al. (2010)noted a positive correlation between age and biomagnification ofcontaminants in Glaucus gulls (Larus hyperboreus) in the Arctic. Like-wise, Evers et al. (2005) found that concentrations of methylmercury(MeHg) in adult tree swallows were higher than in nestlings. The au-thors suggest that differences in prey intake between adult and juvenilebirds, as well as the ability of young to transfer MeHg from blood intofeathers during rapid growth,may account for such age-based variation.

Given the widespread contamination of aquatic systems(Fitzgerald et al., 1998; Hammerschmidt and Fitzgerald, 2005;Blocksom et al., 2010), the amount of currently available informa-tion on aquatic-to-terrestrial contaminant fluxes does not reflectthe potential scale of the problem. In particular, although the impactsof land use and land cover (LULC) on riparian birds have beenwidely in-vestigated (Sullivan et al., 2007; Luther et al., 2008; Pennington et al.,2008; Oneal and Rotenberry, 2009), the relationships between LULCand contaminant exposure to riparian birds from aquatic systems ispoorly understood. For example, riparian swallow species [e.g., bank(Riparia riparia), northern rough-winged (Stelgidopteryx serripennis),tree, and cliff (Petrochelidon pyrrhonota) swallows] are susceptibleto biomagnification of contaminants because of their dependence on amixture of stream, riparian, and terrestrial food sources and habitats(Harris and Elliot, 2000; Dods et al., 2005; Custer, 2011). During thereproductive season, riparian swallows tend to forage within severalhundred meters (m) of their nest sites (Quinney and Ankney, 1985;Dunn and Hannon, 1992), making them apt bioindicators of localstream and riparian conditions. Land-management practices that alteraquatic resource utilization by swallows might be expected to stronglyinfluence their exposure to aquatic contaminants. Roux and Marra(2007), for instance, found that lead (Pb) concentrations in urbanpasserine birdswere significantly higher than in their rural counterparts,which corresponded with relative Pb concentrations found in soils.

Our objective was to explore the relationships between adjacent(to the river) patterns in LULC and the magnitude of Hg and Seconcentrations in four species of riparian swallows as mediated byaquatic-to-terrestrial contaminant fluxes. Because of historic andcontemporary differences in land-management and chemical use, wehypothesized that concentrations of contaminants in river sediments,

aquatic emergent insects, and riparian swallows would be greater aturban than at rural reaches. Consequently, we anticipated that contam-inant exposure to swallows would also differ by LULC class, but wouldbe mediated by the degree of aquatic resource utilization such thatswallows feeding at rural reaches (i.e., comprised of a mixture of forest,grassland, and agriculture) would exhibit greater reliance on aquaticemergent insects than swallows feeding at urban reaches, where aquaticemergent insect communities have been shown to exhibit reduceddiversity (Stepenuck et al., 2002) and biomass (Lenat and Crawford,1994; Meyer and Sullivan, in press). Finally, we expected that adultswallows would exhibit greater biomagnification of contaminants thannestlings at both urban and rural reaches.

2. Materials and methods

2.1. Study system and experimental design

The Scioto River is a multiuse river that drains ~16,882 km2 incentral and southern Ohio, flowing for 372 km through agricultural(69%), forested (21%), and urban (9%) landscapes (White et al.,2005; Blocksom and Johnson, 2009). The Olentangy River meets theScioto in Columbus, the 15th largest city in the US by population(1,178,899 people; USCB, 2010). Once downstream of the city, theScioto is free-flowingandexhibits riparian zonesdominatedbydeciduousforest, row crops (corn and soybean), and smaller urban centers.

From 2010 to 2012, we conducted coordinated sampling of ripar-ian swallows, riverine sediment and aquatic insects, and aquatic andriparian vegetation at eleven river reaches [defined as a river seg-ment based on similar valley features and channel geomorphology(~1 kilometer [km] for this study)] of the Scioto River watershed,representing a gradient of urban to rural (i.e., mixture of forest,grassland, and agriculture) landscapes (Fig. 1). Study reaches weredistributed along the length of the river and were separated by anaverage distance of 18.4 river kilometers (km), although there wassignificant variability (SD = 16.8 km). Because of the spatial distri-bution of LULC patterns in the basin, a degree of clustering amongLULC types was unavoidable. We used ArcGIS 10.1 (ESRI, Redlands,CA, USA) to calculate percent cover by vegetation class within500 meters (m) of the channel following Zelt and Johnson (2005),and performed ground-based surveys to document bridge crossings,vegetation structure, and vegetation composition.

2.2. Field and laboratory methods

2.2.1. SedimentIn either 2010 or 2012, we collected five sediment cores (~10 cm

in depth) from each reach at approximately equidistant locationsalong the length of the reach (Walters et al., 2010). We collectedsediment cores by push-coring approximately 2 cmwith apolycarbonatecoring device. We sealed sediment composite samples in plastic sleeves,placed them on ice, and froze them at−20 °C until analysis (Lutz, 2008).

2.2.2. Periphyton and vegetationFollowing methods used in Bartel et al. (2010) and Pennington

and Blair (2011), we surveyed riparian vegetation along three 100-mtransects (upstream,middle, downstream) along both banks (perpen-dicular to the stream, n = 6/reach) at each reach. At each transect, weestablished three 5 m × 5 m quadrats, located at 0, 50, and 100-mfrom the river's edge. We then estimated vegetation cover by height(b3 m, 3–5 m, and >5 m) and identified all trees, shrubs, grasses,and other herbaceous plants to species. We visually estimated thepercent coverage of vegetation overhanging the water's edge alongboth banks and counted standing dead trees of diameter at breastheight (dbh) >10 cm.

For stable isotope analysis, we collected five terrestrial vegetationsamples per transect on both sides of the river (along survey transects):

Fig. 1. Eleven study reaches of the Scioto River basin, Ohio, USA. Open circles in popouts indicate study reaches. Circles in right-hand popout represent nest box locations.Popouts are not to scale.

44 J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50

three samples from the numerically dominant tree species and twosamples from the dominant species among the shrubs, grasses, herbsand sedges. We stored leaf samples in paper bags until further process-ing in the laboratory. We collected periphyton by scrubbing a 25-cm2

section of the dominant hard substrate (cobble) at each of the fivetransects within each reach following Reavie et al. (2010). The sampleswere composited by reach into a single polyethylene jar and preservedin 70% ethanol solution until analysis.

2.2.3. Riparian swallowsWe selected a suite of riparian swallow species (tree, cliff, bank,

and northern rough-winged swallows) that were common to thestudy system. These swallow species are obligate aerial insectivoresthat naturally breed in riparian habitats (riparian tree cavities,riverbanks, cliffs and bridges, etc.) (Robertson et al., 1992; Brown andBrown, 1995; DeJong, 1996; Garrison, 1999). Given potential differ-ences in species-specific exposure patterns to contaminants, we ideallywould have focused our efforts on one riparian swallow species.However, the distribution of swallow species in the study systemprecluded this option, as there was no one species of swallow foundat all the study reaches. Others have also used a foraging guild-basedapproach to investigate contaminant exposure in birds (e.g., Jacksonet al., 2011). We conducted all sampling during the swallow reproduc-tive season (May–early August in 2011 and 2012).

At seven of the eleven research reaches,we captured swallows usingmist nets set over the river or in the riparian zone. We erected six nestboxes at each of four additional reaches, following design protocols setby the Golondrinas de las Américas (2011) project at Cornell University.All nest boxes were placedwithin or along the edge of the riparian zoneand were within 100 m from the river on the average. We equippedeach box with an external trapping mechanism (i.e., wig-wag), whichallowed the capture of adult tree swallows while they were inside thenest box. At first capture, we banded all birds with aluminum USFWSsize 0 bands for tree, bank, and northern rough-winged swallows, andsize 1 bands for cliff swallows. We drew blood from the jugular veinto be used for stable isotope and contaminant analyses (Ardia, 2005;Sullivan and Vierling, 2012). We collected blood from a minimum ofthree adults and four nestlings during the second week after hatchingat each of the experimental nest box reaches, where at least two

nests were sampled per reach. At all other reaches, variability inthe accessibility and abundance (i.e., colony-nesting cliff swallowsat some reaches, couple/few pairs of northern rough-winged swal-low at others) of swallows constrained sample size. However, wecollected blood from a minimum of four swallows at all non-nestbox reaches, except at the study reach “Mosquito”, where we wereonly able to capture three birds. Once drawn, we immediately trans-ferred blood samples to centrifuge tubes where it was stored in 70%ethanol for later stable isotope analysis. We placed additional bloodon Dried Blood Spot cards (PerkinElmer, Waltham, MA, USA) forcontaminant analysis. DBS cards are an appropriate techniqueto sample blood from small-bodied animals (b20 g; mean weightof birds in our study at collection was 16.6 g, SD = 3.8 g), fromwhich adequate sample volume can preclude traditional methods(Shlosberg et al., 2011).

2.2.4. InvertebratesAdult tree swallows typically return to the nest with a bolus of

invertebrate prey carried in their beaks, which we removed from theirmouths before the parent fed the nestlings at nest box reaches(McCarty and Winkler, 1999; Echols et al., 2004). At all other reaches,we deployed six floating aquatic emergent insect traps (i.e., pyramidtraps) per reach as described by Aubin et al. (1973). We deployedtraps along both banks of the reach such that they representeddominant flow habitats (i.e., riffle, pool/run). For terrestrial insects, wesuspended half-sized Malaise traps (1-m high, 1-m long, 0.6-m wide,0.5-mm mesh, MegaView Science Co., Taichung, Taiwan; Townes,1972) from trees at 10 mand50 m from the active river channel approx-imately in the middle of the study reach, on both banks. We collected allinvertebrates five and ten days after trap deployment.

Upon collection, we placed all invertebrates in jars, put themon ice for transport, and froze them at −20 ° C until analysis (Lutz,2008). In the laboratory, we identified all individuals to familyusing Johnson and Triplehorn (2004). For bolus invertebrates, wealso classified all individuals by their origin (i.e., aquatic or terrestrialaccording to their larval habitat). Following identification, we driedand weighed invertebrates by family (total dry mass per reach[mg m−2 d−1]; Iwata et al., 2003).

Fig. 2. Relationship betweenHg concentrations (log10) in riparian swallows and sediment(log10) (ppb). The slope for the regression model was significant (y = 0.39x + 3.25,R2 = 0.33, P = 0.008). Twodata points (open circles)were considered outliers andomittedfromtheanalysis, although the regressionwas also significantwith these twopoints included(y = 0.46x + 2.95, R2 = 0.23, P = 0.030). Dashed lines represent confidence curves atα = 0.05.

45J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50

2.2.5. Contaminant and stable isotope analysisAll sediment, bolus, and swallow blood samples were analyzed for

Hg and Se concentrations [parts per billion (ppb) dry weight] atthe Diagnostic Center for Population and Animal Health, ToxicologySection, Michigan State University. ICP-AES (Varian Vista, now partof Agilent, Santa Clara, CA) and ICP-MS (Agilent 7500ce) instrumentswere calibrated with standards derived from NIST-traceable stock so-lutions for each element (GFS Chemicals, Inc., Cincinnati, OH). Qualitywas assured in each sequence run by analyzing lab reagent blanks,NIST (National Institute of Standards & Technology, Gaithersburg,MD)-traceable Multi-mix (Alfa Aesar Specpure, Ward Hill, MA) anddigests of NIST Standard Reference Materials (SRM), including MusselTissue 2976, Trace Elements in Water 1643e and/or Montana II Soil2711a, as appropriate. Mercury was analyzed by cold vapor atomicabsorption spectrometry (CETAC CVAA, Omaha, NB) with similarcalibration and QC. Analysis of blood was performed by methodsoutlined in Lehner et al. (in press) with reference to BioRad (Hercules,CA) Lypochek 2 and 3 standards for verification of accuracy.

Terrestrial vegetation, terrestrial insects (Curculionidae, Doli-chopodidae, and Cicadellidae), periphyton, aquatic emergent insects(Chironomidae, Hydropsychidae, and Heptageniidae), and bird bloodsampleswere analyzed for 13C and 15N stable isotopes using continuousflow isotope ratio mass spectrometry (EA-IRMS) at the University ofWashington Stable Isotope Core (Pullman, WA, USA). The isotopiccomposition of samples was expressed using the δ13C notationdefined as follows:

δ13C ¼ Rsample=Rstandard

� �–1

h i� 1000; where R is 13C=12C ð1Þ

where parts per thousand (‰) are the atomic ratios of the numberof atoms in the sample or standard. Typical analytical precisionwas +/-0.2‰ for δ13C determination.

2.2.6. Numerical and statistical analysesBecause of the largely longitudinal distribution of our study reaches

along the river system,we considered testing for spatial autocorrelationof all measured variables. However, the focus of our study was on therole terrestrial environmental characteristics played in mediating fluxesof contaminants to riparian consumers, and not on the distribution ofriver contaminants themselves. Therefore, we used Moran's I (1950)statistic (Cliff and Ord, 1973) to describe spatial patterns of swallowcontaminant concentrations only. Positive and significant (P b 0.05)Moran's I values indicate a more spatially-clustered distribution thanwould be expected if the underlying spatial processes were random,whereas negative values indicate greater spatial dispersion.

Because we observed no differences in δ13C and δ15N values be-tween adult and nestling swallows based on paired t-tests, we groupednestlings and adults by species for each study reach. We then analyzedthe contributions of aquatic and terrestrial food sources to riparianswallows at each study reach using (1) dual isotope plots of δ13C andδ15N, (2) linear regression between δ13C of swallows and periphyton(i.e., gradient approach; Jardine et al., 2012), and (3) invertebratesfrom bolus samples. For dual-isotope plots, spatial correspondencebetween δ13C and δ15N values in swallows and aquatic prey indicatesgreater use of aquatic prey (DeNiro and Epstein, 1978, 1981).We createdone plot for each land-use class (i.e., urban and rural) and plotted δ13Cand δ15N values for swallows by species, given potential variability inisotopic signatures among species. Because of an unbalanced numberof swallows at each reach, we used weighted linear regression to deter-mine the degree to which swallow δ13C tracked periphyton δ13C acrossall study reaches.We used invertebrate composition from bolus samplesto further inform aquatic:terrestrial prey use by tree swallows.

We performed principal component analysis (PCA) on riparianLULC variables that we had selected a priori as candidate predictorsof riparian swallow prey utilization. PCA axes with eigenvalues > 1

were retained for use in subsequent linear regression models(Rencher, 1995; Sullivan andWatzin, 2008). We used weighted linearregression to examine the best LULC predictors of contaminantconcentrations in swallows. We used two-sample t-tests to test forpotential differences in (1) the contribution of aquatic resources toswallows and (2) contaminant concentrations in sediment, aquaticinsects, and riparian swallows between LULC types. We used pairedt-tests to test for differences between contaminant concentrationsin (1) adult and nestling swallows and (2) aquatic and terrestrial in-sects from bolus samples. To avoid potential pseuodreplication at nestbox reaches where multiple nestlings were sampled from the samebox, mean contaminant concentrations of nestlings per nest boxwere used in the analysis. Data were tested at the α = 0.05 level.However, given multiple regression tests, the Bonferroni adjustmentfor α was α / k = 0.05 / 5 = 0.010, where k is the number of tests(Wright, 1992). Prior to the analysis, concentrations of Se and Hgwere log10 were transformed to normalize data and eliminateheteroscedasticity (Zar, 1984).

3. Results

Sediment concentrations of Se ranged from 367 to 2440 ppb,while sediment Hg ranged from 31 to 137 ppb. Neither Se (t =1.14,P = 0.327, df = 7) nor Hg (t = 0.157, P = 0.881, df = 7) in sedimentwas significantly different between urban and rural reaches. Likewise,neither Se (t = 1.77, P = 0.160, df = 7) nor Hg (t = 0.31, P = 0.766,df = 7) in aquatic emergent insects was different between urban andrural reaches. Concentrations of Se and Hg in riparian swallows variedwidely across study reaches (Supplemental Data Table 1). Hg con-centrations in swallows were positively related to Hg concentrationsin sediment (Fig. 2), although no relationship was evident be-tween Se in swallows and in sediment. Se concentrations weregreater in aquatic (mean = 3956 ppb, SD =2039) than in terres-trial (mean = 1132 ppb, SD = 1089) invertebrate swallow prey(t = −4.11, P = 0.027, df = 2). A similar, but weaker relationshipwas found for Hg (aquatic: mean = 66.3 ppb, SD = 28.3, terrestrial:mean = 32.7 ppb, SD = 10.8; t = −2.17, P = 0.081, df = 2). Moran'sI indicated that there was no spatial clustering of swallow contaminantconcentrations (P > 0.05 in all cases), suggesting that observationsfrom nearby study reaches were independent from one another.

Fig. 3. Dual isotope plots of δ13C and δ15N values (mean ± 1 SE) for the Scioto Riverbasin (Ohio, USA) aquatic and terrestrial food-web components of the Scioto Riverbasin (Ohio, USA) in (a) rural and (b) urban reaches.

46 J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50

3.1. Contribution of aquatic resources to swallow diet

Isotopic values (Table 1) for riparian swallows ranged from−26.77to −20.29‰ for δ13C and from 6.63 to 12.74‰ for δ15N. Signatures foraquatic emergent insect δ13C ranged from −28.27 to −27.04‰, whileδ15N ranged from 10.04 to 12.31‰. Terrestrial insect δ13C ranged from−25.84 to −22.47‰ whereas δ15N of terrestrial insects ranged from5.10 to 8.74‰. Terrestrial vegetation δ13C ranged from −31.53 to−28.00‰, and δ15N from 2.72‰ to 4.68‰. Periphyton exhibitedthe greatest variation, ranging from −21.46 to −11.26‰ for δ13C,and from 6.14 to 12.39‰ for δ15N. We found no significant dif-ferences for either δ13C (t = −0.12, P = 0.455, df = 3) or δ15N(t =1.33, P = 0.137, df = 3) between adult (δ13C: mean = −24.2,SD = 0.99; δ15N: mean = 10.1, SD = 1.35) and juvenile (δ13C:mean = −24.4, SD = 0.72; δ15N: mean = 10.4, SD = 1.06) swallows,although the sample size was small (n = 10).

Swallows at both rural and urban reaches are plotted within thestream–riparian food web (Fig. 3a & b). For rural (Fig. 3a) and urban(Fig. 3b) reaches, isotope plots indicated that swallows were relianton a mixture of aquatic and terrestrial food resources, although swal-lows were presumably more δ15N enriched at urban reaches (basedon the lower δ15N enrichment of primary producers at urban reachesalong with the invariant swallow δ15N signatures for swallows at bothurban and rural reaches). Swallow δ13C negatively tracked periphytonδ13C at urban, but not rural, reaches (Fig. 4), indicating that swallowswere not heavily reliant on instream primary productivity at urbanreaches. However, this relationship does not preclude swallow relianceon aquatic emergent insects, which can be highly reliant on terrestrialinputs of vegetation, as in this study (Fig. 3a and b). The variabilityexplained by this regression serves as our minimum contribution ofaquatic emergent insections to swallow diet (Fig. 4).

Bolus results from the four nest box reaches indicated thatswallows at urban locations relied more heavily on aquatic insectsthan at rural locations (Fig. 5). By weight, aquatic emergent insectscomprised 84.0% of swallow diet (vs. 16.0% from terrestrial inverte-brates) at urban locations, whereas aquatic emergent insects comprisedonly 46.4% of swallow diet (vs. 53.6% from terrestrial invertebrates)at rural nest box locations. Individuals of the family Coenegrionidae(narrow-winged damselflies)made up nearly 30% of all aquatic individ-uals collected, whereas Aeshnidae (hawkers or darners) representedthe largest-bodied prey item.

Concentrations of Se in riparian swallows were linked with bothδ15N and δ13C isotopic values (Fig. 6a and b). Swallow Se concentrationsincreased with δ15N enrichment and δ13C depletion, both of which areisotopic signals indicative of a shift toward aquatic prey resources inour system. Concentrations of Hg were not related to either swallowδ15N (P = 0.971) or δ13C (P = 0.152) signatures.

Table 1δ13C and δ15N values for riparian swallows, periphyton, riparian vegetation, aquatic emergOhio, USA. Reaches are presented upstream to downstream. Note: CLSW= cliff swallow, BA

Study reach Land use Swallows Periphyton

Species δ13C δ15N δ13C

1 (Highbanks) Rural TRSW −24.69 10.016 N/A2 (Wetlands) Urban TRSW −24.55 11.00 −18.493 (Fawcett) Urban TRSW −24.42 10.80 N/A4 (Horseshoe) Urban CLSW −23.24 9.04 −17.695 (Berliner) Urban TRSW −26.14 12.39 −11.266 (Mosquito) Rural NRWS −24.61 11.77 −18.797 (Darby) Rural TRSW −24.07 10.00 N/A8 (Gravel Bar) Rural BANS −24.42 10.37 −11.689 (Piketon) Rural CLSW −23.35 7.91 −21.4610 (Treefall) Rural BANS −25.15 10.87 −14.8211 (Last) Rural BANS −23.98 11.13 −13.41

Note: N/A = not applicable because diet composition was analyzed directly using bolus sa

3.2. Influence of LULC

Principal component analysis of eleven LULC measures identifiedthree axes with eigenvalues > 1 (Table 2). The first principal com-ponent (PC1) captured 54.4% of the variance, and was mainly drivenby factors related to urbanized landscapes (e.g., population density[r2 = 0.91, + correlation], % impervious surface coverage [r2 = 0.86,+], % agriculture [r2 = 0.86, −]). Accordingly, this PC was named‘Urbanization Axis’. The second principal component explained about19% of the variation that remained and was driven almost solely by %tall tree cover (r2 = 0.86, +), and is hereafter referred to as “MatureTrees Axis”. No other metric within this axis had a correlation > 0.32.The third PC, “Shoreline Habitat Axis”, explained about 14% of the

ent insects, and terrestrial invertebrates for all study reaches in the Scioto River basin,NS = bank swallow, TRSW = tree swallow, NRWS= northern rough-winged swallow.

TerrestrialVegetation

AquaticEmergent Insects

Terrestrial Insect

δ15N δ13C δ15N δ13C δ15N δ13C δ15N

N/A N/A N/A N/A N/A N/A N/A6.88 −30.96 2.72 −27.41 11.29 −27.78 11.15N/A N/A N/A N/A N/A N/A N/A6.14 −30.37 3.08 −27.51 10.04 −27.97 12.317.35 −30.81 4.22 −28.27 11.09 −27.99 12.668.42 −28.06 4.68 −27.04 11.55 −27.34 11.83N/A N/A N/A N/A N/A N/A N/A12.39 −28.00 3.74 27.78 11.15 −25.09 6.798.66 −31.52 4.53 −27.97 12.31 −25.09 7.748.78 −31.53 3.27 −27.99 12.66 −23.83 8.319.64 −30.56 2.89 −27.34 11.83 −25.42 7.64

mples.

Fig. 4. Relationship between riparian swallow and periphyton δ13C at urban (solid line,closed circles) and rural (dotted line, open circles) reaches. The slope for the regressionmodel was significant for urban reaches (y = −0.25x − 28.8, R2 = 0.54, P = 0.001),but not significant for rural reaches (y = −0.07x − 25.4, R2 = 0.10, P = 0.132).

Fig. 6. Relationship between swallow Se concentration (log10) and (a) swallow δ15Nand (b) swallow δ13C. The slopes for the regression models were significant forboth δ15N (y = 0.55x + 3.26, R2 = 0.76, P b 0.001) and δ13C (y = −0.30x − 1.90,R2 = 0.27, P = 0.032). Dashed lines represent confidence curves at α = 0.05.

47J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50

remaining variance and was strongly influenced by standing dead trees(r2 = 0.69, +) and % overhanging vegetation (r2 = 0.48, +).

At a coarse landscape resolution, we found that swallow Hgconcentrations were significantly higher in rural than in urbanreaches (t = −2.96, P = 0.003, df = 24), and marginally so forSe (t = −1.54, P = 0.068, df = 24). A combination of urban char-acteristics and minimal agricultural activity in the riparian zoneappeared to be, in part, driving this association, as we found thatthe Urbanization Axis was negatively related to both Hg (Fig. 7a)and Se concentrations in swallows (Fig. 7b). Urbanization wasalso negatively related to δ15N enrichment (Fig. 8), which in oursystem indicates a decreasing reliance on aquatic prey along thisaxis.

We found that Hg concentrations were significantly higherin adult swallows (mean = 183.1 ppb) than nestlings (mean =57.0 ppb) (t = −4.01, P = 0.016, df = 4). Se concentrations inadults (mean = 9635 ppb) were also significantly higher than innestlings (mean = 1997 ppb) (t = −3.10, P = 0.036, df = 4). Age-dependent trends in contaminant concentration were consistent acrossboth urban LULC and rural LULC.

Fig. 5. Contribution by weight of aquatic emergent and terrestrial insects to swallowboluses from nest box reaches (n = 40). Error bars represent ± 1 SE from the mean.

4. Discussion

Aquatic emergent insects serve as important prey items for myriadriparian consumers (Akamatsu et al., 2004; Ballinger and Lake, 2006).As a result of these strong, cross-system linkages, terrestrial consumersare exposed to aquatic contaminants (Akamatsu and Toda, 2011).Walters et al. (2008), for example, showed that aquatic emergentinsects transported PCBs from contaminated lake sediments intoadjacent riparian food webs. Our understanding of the mechanisms

Table 2Adjacent (500 m on each side of river) land-use and land-cover (LULC) principalcomponent analysis: eigenvalues and the percent variance captured by the principalcomponents (eigenvalues > 1), along with each principal component's loadings andthe proportion of the variance (r2) each variable shared with the PCA axes. Bold typeindicates the axis used as successful predictor variable in regression models.

Urbanization Mature trees Shorelinehabitat

Riparian landscapecomposition metrics

Loading r2 Loading r2 Loading r2

% Agriculture −0.38 0.86 0.08 0.01 0.02 0.00% Shrub cover(1–3 m) 0.34 0.69 0.02 0.00 −0.38 0.22% Small tree cover (3–6 m) 0.30 0.54 0.31 0.20 0.05 0.00% Tall tree cover (>6 m) −0.01 0.00 0.64 0.86 0.17 0.04# Standing dead trees 0.00 0.00 −0.34 0.24 0.67 0.69Riparian forest width (m) −0.30 0.54 −0.10 0.02 −0.08 0.01# Bridge crossings 0.30 0.54 −0.39 0.32 −0.17 0.04% Impervious surface 0.38 0.86 −0.23 0.11 −0.04 0.00# Canopy layers 0.32 0.61 0.36 0.27 −0.09 0.01Human population density(residents/km2)

0.39 0.91 −0.10 0.02 0.13 0.03

% Overhanging vegetation 0.26 0.40 0.13 0.04 0.56 0.48Eigenvalue 5.98 2.10 1.53% variance 54.4 19.1 14.0

Fig. 7. Relationship between Urbanization Axis (i.e., PC1) and (a) Hg concentration(log10) and (b) Se concentration (log10) in riparian swallows. Degree of urbanizationincreases from −3 to 4. The slope for the regression model was significant forboth Hg (y = −0.11x − 4.91, R2 = 0.38, P = 0.004) and Se (y = −0.17x + 9.12,R2 = 0.63, P b 0.001). Dashed lines represent confidence curves at α = 0.05.

48 J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50

that influence and mediate these exposure pathways remains limited,but given the geographic range and abundance of aquatic emergentinsects and riparian consumers, and the global proliferation of aquaticcontamination (Menzie, 1980; Walters et al., 2008), an improvedgrasp of these cross-boundary flowswill be crucial formanaging terres-trial exposure risk from aquatic contaminants.

Many investigators have illustrated the variability in swallowdietary composition. For example, Blancher and McNicol (1991) deter-mined that the diet of non-egg-laying adult tree swallows was

Fig. 8. Relationship between Urbanization Axis (i.e., PC1) and δ15N in riparian swallows.Urbanization increases from−3.0 to 4.0. The slope for the regressionmodel was significant(y = −0.23x + 10.9, R2 = 0.38, P = 0.031). Dashed lines represent confidence curves atα = 0.05.

comprised of 54.9% aquatic insects by biomass. Similarly, Wayland etal. (1998) found that insects of aquatic origin made up 50–60% of treeswallow diet in western Canada. Collectively, our results indicate thatswallows rely on amixture of terrestrial and aquatic insects, but that re-liance on aquatic insects is likely greater at urban vs. rural reaches(Figs. 3a & b, 5) despite no significant differences in either aquatic(t = −0.121, P = 0.477) or terrestrial (t = 0.756, P = 0.908) aerialinsect productivity between rural and urban reaches in the study sys-tem (Kautza and Sullivan, unpublished data). Many riparian swallowspecies tend to forage in open areas (Brown et al., 2002; Ghilain andBelisle, 2008), indicating a likely preference for feeding over openwater vs. heavily-canopied riparian areas. Our urban reaches were gen-erally characterized by densely-forested strips in the immediate ripari-an zone, whichmay encourage foraging directly over water and explainwhy urban swallows fed more heavily on aquatic emergent insectionsthan their rural counterparts.

Contrary to our hypothesis, sediment contaminant concentrationsdid not differ between land-use classes. However, Hg and Se concentra-tions in riparian swallows were lower at urban than at rural reaches,despite the fact that urban nest box swallows depredated aquaticinsects more commonly than terrestrial insects, and that bolus samplesindicated that aquatic insects exhibited higher concentrations of Seand Hg than terrestrial insects. Concomitantly, concentrations of Hgin swallow blood and river sediment were positively related (Fig. 2),which suggests that riparian swallows are exposed to aquatic contami-nants via aquatic prey. Likewise, Se concentrations in swallows werepositively linked to both δ15N enrichment and δ13C depletion (Fig. 6),indicators of reliance on aquatic emergent insects in our study system.Swallows also fed at a higher trophic level at our urban reaches(Fig. 3), indicating a potential increase in aquatic prey utilization. Onepossible explanation for this apparent discrepancy between contribu-tion of aquatic prey and contamination patterns is that swallows wereactively selecting prey that were not dominant within the system,and therefore not included in our isotopic or contaminant analyses.Blancher and McNicol (1991) for example, found that mayflies werean important component of tree swallow diet despite composing asmall fraction of the insects caught in emergent traps. It is also possiblethat varying bioavailability among metal speciations found within thesediments leads to unequal transfer to swallows through predation ofaquatic emergent insects. For instance, Langner et al. (2012) observedthat blood Hg concentrations in osprey (Pandion haliaetus) chicks didnot reflect Hg concentrations in river sediments, which they suggestedwas due to decreased methylation, and thus bioavailability, of Hg.

Influences of land cover on avian foraging behavior likely explainpatterns we observed in swallow contaminant concentrations.Ormerod and Tyler (1991) found that gray wagtails (Motacillacinerea) changed their diet to incorporate more lepidopteran larvaein broadleaved forests than in moorlands or coniferous forests inWales. Such dietary shifts in response to land-cover variation couldhave a profound effect on contaminant uptake. Biomagnification ofaquatic contaminants in tree swallows, for instance, is known to belinked with their reliance on aquatic emergent insects (Brasso andCristol, 2008; Hallinger et al., 2011; Jackson et al., 2011), which isconsistent with our results for Se (Fig. 6).

Our observation that contaminant biomagnification was higher inadult swallows relative to nestlings aligns with other studies and wasconsistent with our hypothesis. Evers et al. (2005), for instance, foundthat methylmercury (MeHg) concentrations were five to ten timeshigher in adult tree swallows than in nestlings. Although we did notobserve a difference in the dietary composition (aquatic vs. terrestrial)between adult and immature swallows, nestlings might efficientlyremove contaminants from their blood as they are deposited intogrowing feathers (Tsipoura et al., 2008). Alternatively, adult swallowsmay feed on larger-bodied aquatic insects, thereby increasing exposureto aquatic contaminants. In Canada, Quinney and Ankney (1985) foundthat Insects 1–6 mm in length made up between 80% and 86% of

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nestling tree swallow diet, whereas McCarty and Winkler (1999)found that adult tree swallows actively selected for larger-bodiedprey (e.g., Odonata) as compared to smaller-bodied insections (0–3 mmin length). Temporal disparities between aquatic insect emergence andterrestrial insect production might also influence prey availability andfeeding behavior (Nakano and Murakami, 2001; Jonsson et al., 2012),which could result in nestlings ingesting a higher proportion of terrestrialinsects, thereby decreasing their exposure to aquatic contaminants.

5. Conclusions

Overall, our results (1) support recent research examining thecross-system trophic linkages between aquatic emergent insects andriparian consumers (Ballinger and Lake, 2006; Fukui et al., 2006;Daley et al., 2011), and (2) implicate landscape alterations as a keyfactor in regulating aquatic-to-terrestrial contaminant transfers. Our re-sults also provide insight into the role of riparian swallows as integratorsof linked aquatic–terrestrial systems within the context of contaminantexposure risk. Specifically, the reliance of swallows upon a mixture ofterrestrial and aquatic invertebrate prey makes them highly vulnerableto contaminants from both terrestrial and aquatic systems. Their abilityto range freely and utilize multiple prey sources makes them excellentorganisms for examination of large, cross-boundary trophic andmaterialtransfer processes.

Building upon previous work (Blancher and McNicol, 1991;Bishop et al., 1999; Harris and Elliott, 2000; McCarty, 2002), wesuggest that riparian swallow species may capture system-levelmechanisms of contamination. We argue that the trophic dynamicsof riparian swallows and other insectivorous riparian birds representa critical pathway for cross-boundary contaminant transfer andmovement across linked aquatic–terrestrial landscapes. Studies acrossbroader geographical ranges and with increased sample sizes will behelpful in further testing this hypothesis as will additional research rel-ative to species-specific swallow feeding behavior, movement patterns,and resource utilization. The potential role of swallows themselves asvectors of contaminants (e.g., via feces, feathers, and nesting colonies)across both local (i.e., nesting) and broader (i.e., migratory) spatial scaleswill also be important in further understanding aquatic–terrestrialcontaminant fluxes. Lastly, continued research related to the mediatingrole of terrestrial landscapes on transfers of contaminants from aquaticto terrestrial systems will be critical for improved remediation andlong-term conservation of river ecosystems.

Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.scitotenv.2013.05.065.

Acknowledgments

Research support was provided by state and federal funds appro-priated to The Ohio State University, Ohio Agricultural Research andDevelopment Center. We would like to thank Paradzayi Tagwireyifor his help in the field.

References

Akamatsu F, Toda H. Aquatic subsidies transport anthropogenic nitrogen to riparianspiders. Environ Pollut 2011;159:1390–7.

Akamatsu F, Toda H, Okino T. Food source of riparian spiders analyzed by using stableisotope ratios. Ecol Res 2004;19:655–62.

Ardia DR. Tree swallows trade off immune function and reproductive effort differentlyacross their range. Ecology 2005;86:2040–6.

Aubin A, Bourassa JP, Pellissi M. Effective emergence trap for capture of mosquitoes.Mosq News 1973;33:251–2.

Ballinger A, Lake PS. Energy and nutrient fluxes from rivers and streams into terrestrialfood webs. Mar Freshw Res 2006;57:15–28.

Bartel RA, Haddad NM, Wright JP. Ecosystem engineers maintain a rare species ofbutterfly and increase plant diversity. Oikos 2010;119:883–90.

Baxter CV, Fausch KD, Saunders WC. Tangled webs: reciprocal flows of invertebrateprey link streams and riparian zones. Freshw Biol 2005;50:201–20.

Bigler WJ, Jenkins JH, Cumbie PM, Hoff GL, Prather EC. Wildlife and environmental health— raccoons as indicators of zoonoses and pollutants in southeastern United States.J Am Vet Med Assoc 1975;167:592–7.

Bishop CA, Mahony NA, Trudeau S, Pettit KE. Reproductive success and biochemicaleffects in tree swallows (Tachycineta bicolor) exposed to chlorinated hydrocarboncontaminants in wetlands of the Great Lakes and St. Lawrence River basin, USA andCanada. Environ Toxicol Chem 1999;18:263–71.

Blancher PJ, McNicol DK. Tree swallow diet in relation to wetland acidity. Can J Zool(Rev Can Zool) 1991;69:2629–37.

Blocksom KA, Johnson BR. Development of a regional macroinvertebrate index for largeriver bioassessment. Ecol Indic 2009;9:313–28.

Blocksom KA, Walters DM, Jicha TM, Lazorchak JM, Angradi TR, Bolgrien DW. Persistentorganic pollutants in fish tissue in the mid-continental great rivers of the UnitedStates. Sci Total Environ 2010;408:1180–9.

Brasso RL, Cristol DA. Effects of mercury exposure on the reproductive success of treeswallows (Tachycineta bicolor). Ecotoxicology 2008;17:133–41.

Brown CR, Brown MB. Cliff swallow (Hirundo pyrrhonota). In: Poole A, Gill F, editors. Thebirds of North America, 149. Washington, D.C.: The Academy of Natural Sciences,Philadelphia, PA, and The American Ornithologists' Union; 1995

Brown CR, Sas CM, Brown MB. Colony choice in cliff swallows: effects of heterogeneityin foraging habitat. Auk 2002;119:446–60.

Cliff A, Ord K. Spatial autocorrelation. London: Pion; 1973.Cristol DA, Brasso RL, Condon AM, Fovargue RE, Friedman SL, Hallinger KK, et al.

The movement of aquatic mercury through terrestrial food webs. Science 2008;320:335-335.

Custer CM. Swallows as a sentinel species for contaminant exposure and effect studies.Wildlife Ecotoxicology: Forensic Approaches 2011;3:45–91.

Daley JM, Corkum LD, Drouillard KG. Aquatic to terrestrial transfer of sediment associatedpersistent organic pollutants is enhanced by bioamplification processes. EnvironToxicol Chem 2011;30:2167–74.

DeJong MJ. Northern rough-winged swallow (Stelgidopteryx serripennis). In: Poole A,Gill F, editors. The birds of North America, 234. Washington, D.C.: The Academyof Natural Sciences, Philadelphia, and The American Ornithologists' Union; 1996

Deniro MJ, Epstein S. Influence of diet on distribution of carbon isotopes in animals.Geochim Cosmochim Acta 1978;42:495–506.

Deniro MJ, Epstein S. Influence of diet on the distribution of nitrogen isotopes inanimals. Geochim Cosmochim Acta 1981;45:341–51.

Dods PL, Birmingham EM,Williams TD, IkonomouMG, Bennie DT, Elliott JE. Reproductivesuccess and contaminants in tree swallows (Tachycineta bicolor) breeding at a waste-water treatment plant. Environ Toxicol Chem 2005;24:3106–12.

Dreyer J, Hoekman D, Gratton C. Lake-derived midges increase abundance of shorelineterrestrial arthropods via multiple trophic pathways. Oikos 2012;121:252–8.

Dunn PO, Hannon SJ. Effects of food abundance and male parental care on reproductivesuccess and monogamy in tree swallows. Auk 1992;109:488–99.

Echols KR, Tillitt DE, Nichols JW, Secord AL, McCarty JP. Accumulation of PCB congenersin nestling tree swallows (Tachycineta bicolor) on the Hudson River, New York.Environ Sci Technol 2004;38:6240–6.

Evers DC, Burgess NM, Champoux L, Hoskins B, Major A, Goodale WM, et al. Patternsand interpretation of mercury exposure in freshwater avian communities in north-eastern North America. Ecotoxicology 2005;14:193–221.

Fitzgerald WF, Engstrom DR, Mason RP, Nater EA. The case for atmospheric mercurycontamination in remote areas. Environ Sci Technol 1998;32:1–7.

Fukui D, Murakami M, Nakano S, Aoi T. Effect of emergent aquatic insects on bat foragingin a riparian forest. J Anim Ecol 2006;75:1252–8.

Garrison BA. Bank swallow (Riparia riparia). In: Poole A, Gill F, editors. The birds ofNorth America, 414. Philadelphia, PA: The Birds of North America, Inc.; 1999.

Ghilain A, Belisle M. Breeding success of tree swallows along a gradient of agriculturalintensification. Ecol Appl 2008;18:1140–54.

Golondrinas de las Americas. Nest box design. http://golondrinas.cornell.edu/Data_and_Protocol/NestBoxDesignCentimeters.html, 2011 Accessed March 24,2010.

Hagen EM, Sabo JL. Influence of river drying and insect availability on bat activity alongthe San Pedro River, Arizona (USA). J Arid Environ 2012;84:1–8.

Hallinger KK, Cornell KL, Brasso RL, Cristol DA. Mercury exposure and survival infree-living tree swallows (Tachycineta bicolor). Ecotoxicology 2011;20:39–46.

Hamas MJ. Belted kingfisher (Cerlye alcyon). In: Poole A, Gill F, editors. The birds ofNorth America, 84. Washington, DC, USA: The American Ornithologists' Union;1994.

Hammerschmidt CR, Fitzgerald WF. Methylmercury in mosquitoes related to atmo-spheric mercury deposition and contamination. Environ Sci Technol 2005;39:3034–9.

Harris ML, Elliott JE. Reproductive success and chlorinated hydrocarbon contaminationin tree swallows (Tachycineta bicolor) nesting along rivers receiving pulp andpaper mill effluent discharges. Environ Pollut 2000;110:307–20.

Henschel JR, Mahsberg D, Stumpf H. Allochthonous aquatic insects increase predationand decrease herbivory in river shore food webs. Oikos 2001;93:429–38.

Iwata T, Nakano S, Murakami M. Stream meanders increase insectivorous bird abun-dance in riparian deciduous forests. Ecography 2003;26:325–37.

Jackson AK, Evers DC, Folsom SB, Condon AM, Diener J, Goodrick LF, et al. Mercuryexposure in terrestrial birds far downstream of an historical point source. Environ Pollut2011;159:3302–8.

Jardine TD, Kidd KA, Rasmussen JB. Aquatic and terrestrial organic matter in the diet ofstream consumers: implications for mercury bioaccumulation. Ecol Appl 2012;22:843–55.

Johnson NF, Triplehorn CA. Borror and Delong's introduction to the study of insects.Thomson Brooks/Cole; 2004.

50 J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50

Jonsson M, Strasevicius D, Malmqvist B. Influences of river regulation and environmentalvariables on upland bird assemblages in northern Sweden. Ecol Res 2012;27:945–54.

Keast A. The annual cycle and activity on the breeding grounds in a Canadianbroad-leafed deciduous forest bird community relationship to the prey resourcebase. V+410pIn: Keast a, editor. Biogeography and ecology of forest bird commu-nities. The Hague, Netherlands: Spb Academic Publishing Bv; 1990. p. 197–214.Illus Maps.

Langner HW, Greene E, Domenech R, Staats MF. Mercury and other mining-related con-taminants in ospreys along the Upper Clark Fork River, Montana, USA. Arch EnvironContam Toxicol 2012;62:681–95.

Lehner A, RumbeihaW, Shlosberg A, Stuart K, Johnson M, Domenech R, et al. Diagnosticanalysis of veterinary dried blood spots for toxic heavy metals exposure. J AnalToxicol 2013 In press.

Lenat DR, Crawford JK. Effects of land-use on water quality and aquatic biota of 3 NorthCarolina piedmont streams. Hydrobiologia 1994;294:185–99.

Lord CG, Gaines KF, Boring CS, Brisbin LL, Gochfeld M, Burger J. Raccoon (Procyon lotor)as a bioindicator of mercury contamination at the US Department of Energy'sSavannah River Site. Arch Environ Contam Toxicol 2002;43:356–63.

Luther D, Hilty J, Weiss J, Cornwall C, Wipf M, Ballard G. Assessing the impact of localhabitat variables and landscape context on riparian birds in agricultural, urbanized,and native landscapes. Biodivers Conserv 2008;17:1923–35.

Lutz MA. Procedures for collecting and processing streambed sediment and pore waterfor analysis of mercury as part of the National Water-Quality Assessment Program.Open File Report 2008;2008-1279.

Malinga M, Szefer P, Gabrielsen GW. Age, sex and spatial dependent variations in heavymetals levels in the Glaucous Gulls (Larus hyperboreus) from the Bjornoya and JanMayen, Arctic. Environ Monit Assess 2010;169:407–16.

Mattson DJ, Reinhart DP. Influences of cutthroat trout (Oncorhynchus clarki) on behaviourand reproduction of Yellowstone grizzly bears (Ursus arctos), 1975–1989. Can J Zool(Rev Can Zool) 1995;73:2072–9.

Maul JD, Belden JB, Schwab BA, Whiles MR, Spears B, Farris JL, et al. Bioaccumulationand trophic transfer of polychlorinated biphenyls by aquatic and terrestrial insectsto tree swallows (Tachycineta bicolor). Environ Toxicol Chem 2006;25:1017–25.

McCarty. Use of tree swallows in studies of environmental stress. Rev Toxicol (Amsterdam)2002;4:61–104.

McCarty JP, Winkler DW. Foraging ecology and diet selectivity of tree swallows feedingnestlings. Condor 1999;101:246–54.

Menzie CA. Potential significance of insects in the removal of contaminants fromaquatic systems. Water Air Soil Pollut 1980;13:473–9.

Meyer LA, Sullivan SMP. Bright lights, big city: influences of ecological light pollutionon reciprocal stream–riparian invertebrate fluxes. Ecol Appl 2013 In press.

Morrissey CA, Bendell-Young LI, Elliott JE. Linking contaminant profiles to the dietand breeding location of American dippers using stable isotopes. J Appl Ecol 2004;41:502–12.

Nakano S, Murakami M. Reciprocal subsidies: dynamic interdependence betweenterrestrial and aquatic food webs. Proc Natl Acad Sci U S A 2001;98:166–70.

Oneal AS, Rotenberry JT. Scale-dependent habitat relations of birds in riparian corridorsin an urbanizing landscape. Landsc Urban Plann 2009;92:264–75.

Ormerod SJ, Tyler SJ. The influence of stream acidification and riparian land-use on thefeeding ecology of gray wagtails (Motacilla cinerea) in Wales. Ibis 1991;133:53–61.

Paetzold A, Schubert CJ, Tockner K. Aquatic terrestrial linkages along a braided-river:riparian arthropods feeding on aquatic insects. Ecosystems 2005;8:748–59.

Pennington DN, Blair RB. Habitat selection of breeding riparian birds in an urbanenvironment: untangling the relative importance of biophysical elements and spatialscale. Divers Distrib 2011;17:506–18.

Pennington DN, Hansel J, Blair RB. The conservation value of urban riparian areasfor landbirds during spring migration: land cover, scale, and vegetation effects.Biol Conserv 2008;141:1235–48.

Polis GA, Anderson WB, Holt RD. Toward an integration of landscape and food webecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst1997;28:289–316.

Polis GA, Sanchez-Pinero F, Stapp PT, Anderson WB, Rose MD. Trophic flows fromwater to land: marine input affects food webs of islands and coastal ecosystemsworldwide. In: Polis GA, Power ME, Huxel GR, editors. Food webs at the landscapelevel. Chicago, Illinois: University of Chicago Press; 2004. p. 200–16.

Quinney TE, Ankney CD. Prey size selection by tree swallows. Auk 1985;102:245–50.

Reavie ED, Jicha TM, Angradi TR, Bolgrien DW, Hill BH. Algal assemblages for large rivermonitoring: comparison among biovolume, absolute and relative abundancemetrics. Ecol Indic 2010;10:167–77.

Rencher AC. Methods of multivariate analysis. New York, NY, U.S.A.: Johny Wiley andSons, Inc.; 1995

Robertson RJ, Stutchbury BJ, Cohen RR. Tree swallow (Tachycineta bicolor). In: Poole A,Stettenheim P, Gill F, Poole A, Stettenheim P, Gill F, editors. The birds of North America,11. Philadelphia, PA: The Academy of Natural Sciences; 1992. (The American Ornithol-ogists' Union, Washington, D.C.).

Roux KE, Marra PP. The presence and impact of environmental lead in passerine birdsalong an urban to rural land use gradient. Arch Environ Toxicol Chem 2007;53:261–8.

Sabo JL, Power ME. Numerical response of lizards to aquatic insects and short-termconsequences for terrestrial prey. Ecology 2002;83:3023–36.

Shlosberg A, Rumbeiha WK, Lublin A, Kannan K. A database of avian blood spotexaminations for exposure of wild birds to environmental toxicants: the DABSEbiomonitoring project. J Environ Monit 2011;13:1547–58.

Stepenuck KF, Crunkilton RL, Wang LZ. Impact of urban land use on macroinvertebratecommunities in southeastern Wisconsin streams. J Am Water Resour Assoc2002;38:1041–51.

Sullivan SMP, Rodewald AD. In a state of flux: the energetic pathways that movecontaminants from aquatic to terrestrial environments. Environ Toxicol Chem2012;31:1175–83.

Sullivan SMP, Vierling KT. Exploring the influences of multiscale environmental factorson the American dipper Cinclus mexicanus. Ecography 2012;35:624–36.

Sullivan SMP, Watzin MC. Relating stream physical habitat condition and con-cordance of biotic productivity across multiple taxa. Can J Fish Aquat Sci2008;65:2667–77.

Sullivan SMP, Watzin MC, Keeton WS. A riverscape perspective on habitat associationsamong riverine bird assemblages in the Lake Champlain Basin, USA. Landsc Ecol2007;22:1169–86.

Sweeney BW, Vannote RL. Population synchrony in mayflies — a predator satiationhypothesis. Evolution 1982;36:810–21.

Townes H. A light weight malaise trap. Entomol News 1972;83:239–47.Tsipoura N, Burger J, Feltes R, Yacabucci J, Mizrahi D, Jeitner C, et al. Metal concentrations

in three species of passerine birds breeding in the Hackensack Meadowlands ofNew Jersey. Environ Res 2008;107:218–28.

United States Census Bureau. State and county quick facts. http://quickfacts.census.gov/qfd/states/39/39049.html, 2010 (Accessed July 29, 2012).

Vander Zanden MJ, Sanzone DM. Food web subsidies at the land–water ecotone. In:Polis GA, Power ME, Huxel GR, editors. Food webs at the landscape level. Chicago,USA: University of Chicago Press; 2004.

Varley JD, Schullery P. Yellowstone Lake and its cutthroat trout. Science and ecosystemmanagement in the national parks 1996;49–73.

Vessel RD. Energetics of the belted kingfisher (Megaceryle alcyon). Corvalis, OR, USA:Oregon State University; 1978.

Wada H, Cristol DA, McNabb FMA, Hopkins WA. Suppressed adrenocortical responsesand thyroid hormone levels in birds near a mercury-contaminated river. EnvironSci Technol 2009;43:6031–8.

Walters DM, Fritz KM, Otter RR. The dark side of subsidies: adult stream insects exportorganic contaminants to riparian predators. Ecol Appl 2008;18:1835–41.

Walters DM, Mills MA, Fritz KM, Raikow DF. Spider-mediated flux of PCBs from con-taminated sediments to terrestrial ecosystems and potential risks to arachnivorousbirds. Environ Sci Technol 2010;44:2849–56.

Wayland M, Trudeau S, Marchant T, Parker D, Hobson KA. The effect of pulp and papermill effluent on an insectivorous bird, the tree swallow. Ecotoxicology 1998;7:237–51.

White D, Johnston K, Miller M. Ohio river basin. Rivers of North America. Burlington,Massachusetts: Elsevier Academic Press; 2005. p. 375–424.

Wright SP. Adjusted p-values for simultaneous inference. Biometrics 1992;45:1005–13.Zar JH. Biostatistical analysis. Englewood Cliffs, New Jersey: Prentice-Hall; 1984.Zelt RB, Johnson MR. Protocols for mapping and characterizing land use/land cover

in riparian zones. U.S. geological survey open-file report; 2005. [2005-1302].