Riparian Swallows As Integrators of Landscape Change in a Multiuse River System: Implications for Aquatic-To-Terrestrial Transfers of Contaminants

Home , Petrochelidon, Riparia, Stelgidopteryx, Tachycineta, Tree swallow

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

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Science of the Total Environment

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Riparian swallows as integrators of landscape change in a multiuse river system: Implications for aquatic-to-terrestrial transfers 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 States b School of Environment & Natural Resources, The Ohio State University, 2021 Coffey Rd., Columbus, OH 43210, United States

HIGHLIGHTS

• 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.

article info abstract

Article history: Recent research has highlighted the transfer of contaminants from aquatic to terrestrial ecosystems via predation of Received 21 January 2013 aquatic emergent insects by riparian consumers. The influence of adjacent land use and land cover (LULC) on Received in revised form 12 May 2013 aquatic-to-terrestrial contaminant transfer, however, has received limited attention. From 2010 to 2012, at 11 Accepted 13 May 2013 river reaches in the Scioto River basin (OH, USA), we investigated the relationships between LULC and selenium Available online xxxx (Se) and mercury (Hg) concentrations in four species of riparian swallows. Hg concentrations in swallows were sig- fi − b Editor: Christian E.W. Steinberg ni cantly higher at rural reaches than at urban reaches (t = 3.58, P 0.001, df = 30), whereas Se concentrations were positively associated with adjacent land cover characterized by mature tree cover (R2 =0.49,P = 0.006). To Keywords: an extent, these relationships appear to be mediated by swallow reliance on aquatic emergent insects. For example, Riparian swallows tree swallows (Tachycineta bicolor) at urban reaches exhibited a higher proportion of aquatic prey in their diet, fed at Biomagnification a higher trophic level, and exhibited elevated Se levels. We also found that both Se and Hg concentrations in adult Aquatic–terrestrial linkages swallows were 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 aquatic contaminant flux to terrestrial consumers. © 2013 Elsevier B.V. All rights reserved.

1. Introduction A classic example is the reliance of grizzly bears (Ursus arctos horribilis) on fish as an important nutrient source (Mattson and Reinhart, 1995; Movement of materials across the landscape has been central to the Varley and Schullery, 1996). Others have shown that aquatic prey study of food webs (Polis et al., 1997, 2004). At the aquatic–terrestrial represent important food sources to riparian bats (Fukui et al., 2006; interface, ecological subsidies, or the flux of material from one habitat Hagen and Sabo, 2012), raccoons (Procyon lotor)(Bigler et al., 1975; or ecosystem to another (Nakano and Murakami, 2001)hasemerged Lord et al., 2002), piscivorous birds (Vessel, 1978; Hamas, 1994), lizards as a central theme of cross-boundary linkages (Akamatsu et al., 2004; (Sabo and Power, 2002), and terrestrial arthropods (Henschel et al., Vander Zanden and Sanzone, 2004; Ballinger and Lake, 2006). Whereas 2001; Paetzold et al., 2005; Dreyer et al., 2012). the contribution of terrestrial systems to aquatic food webs via inputs of In particular, aquatic insects that emerge from the stream as adults nutrients and organic matter is well recognized, recent investigations (hereafter, ‘aquatic emergent insects’) can be a critical food source for have focused on the importance of aquatic prey subsidies to the energy insectivorous riparian bird species (Keast, 1990; Iwata et al., 2003). budgets of riparian consumers (reviewed in Baxter et al., 2005). For example, Sweeney and Vannote (1982) found that swarming activity by mayflies attracted nighthawks (Chordeiles minor)toareas fl ⁎ Corresponding author. Fax: +1 513 556 5299. of emergence, and Iwata et al. (2003) reported that ycatchers and E-mail address: [email protected] (J.M. Alberts). gleaners foraged intensively on aquatic emergent insects in a pattern

0048-9697/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.scitotenv.2013.05.065 J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50 43 that mirrored aquatic insect distribution, suggesting that the dynamics aquatic emergent insects, and riparian swallows would be greater at of insect emergence can influence avian foraging behavior. urban than at rural reaches. Consequently, we anticipated that contam- Within the context of the energetic pathways that link aquatic and inant exposure to swallows would also differ by LULC class, but would terrestrial ecosystems, there is growing interest in food-web studies be mediated by the degree of aquatic resource utilization such that at the land–water ecotone. Many investigators have found that the swallows feeding at rural reaches (i.e., comprised of a mixture of forest, high reliance of riparian birds on aquatic prey resources can expose grassland, and agriculture) would exhibit greater reliance on aquatic them to contaminants found in aquatic systems (see Sullivan and emergent insects than swallows feeding at urban reaches, where aquatic Rodewald, 2012). Cristol et al. (2008) demonstrated that mercury emergent insect communities have been shown to exhibit reduced (Hg) can bioconcentrate in terrestrial bird species living near contam- diversity (Stepenuck et al., 2002)andbiomass(Lenat and Crawford, inated water sources, while Wada et al. (2009) found that adreno- 1994; Meyer and Sullivan, in press). Finally, we expected that adult cortical responses and thyroid hormones were suppressed in tree swallows would exhibit greater biomagnification of contaminants than swallows (Tachycineta bicolor) living near a river contaminated nestlings at both urban and rural reaches. with mercury. In the Chilliwack River of southern British Columbia, resident American Dippers (Cinclus mexicanus) (i.e., those birds who 2. Materials and methods remain in the mainstem Chilliwack River year-round and have high proportions of contaminated salmon fry in their diet) were found to 2.1. Study system and experimental design have higher polychlorinated biphenyl (PCB) and Hg concentrations than their migratory counterparts (i.e., those birds who are found The Scioto River is a multiuse river that drains ~16,882 km2 in on the Chilliwack mainstem only during the winter and that have central and southern Ohio, flowing for 372 km through agricultural a significantly smaller proportion of fish fry in their diet; Morrissey (69%), forested (21%), and urban (9%) landscapes (White et al., et al., 2004). Several studies have described the bioconcentration of 2005; Blocksom and Johnson, 2009). The Olentangy River meets the PCBs in tree swallows from aquatic insect prey (Echols et al., 2004; Scioto in Columbus, the 15th largest city in the US by population Maul et al., 2006). Echols et al. (2004), for instance, found that PCB (1,178,899 people; USCB, 2010). Once downstream of the city, the concentrations in tree swallow nestlings closely tracked concentra- Scioto is free-flowing and exhibits riparian zones dominated by deciduous tions in aquatic insects. Maul et al. (2006) implicated aquatic insects forest, row crops (corn and soybean), and smaller urban centers. of the family Chironomidae as the key vector of PCBs to nestling From 2010 to 2012, we conducted coordinated sampling of ripar- tree swallows from a lake in Illinois, USA. ian swallows, riverine sediment and aquatic insects, and aquatic and Differences in age-related contaminant exposure patterns among riparian vegetation at eleven river reaches [defined as a river seg- birds have also been documented. For example, Malinga et al. (2010) ment based on similar valley features and channel geomorphology noted a positive correlation between age and biomagnification of (~1 kilometer [km] for this study)] of the Scioto River watershed, contaminants in Glaucus gulls (Larus hyperboreus)intheArctic.Like- representing a gradient of urban to rural (i.e., mixture of forest, wise, Evers et al. (2005) found that concentrations of methylmercury grassland, and agriculture) landscapes (Fig. 1). Study reaches were (MeHg) in adult tree swallows were higher than in nestlings. The au- distributed along the length of the river and were separated by an thors suggest that differences in prey intake between adult and juvenile average distance of 18.4 river kilometers (km), although there was birds, as well as the ability of young to transfer MeHg from blood into significant variability (SD = 16.8 km). Because of the spatial distri- feathers during rapid growth, may account for such age-based variation. bution of LULC patterns in the basin, a degree of clustering among Given the widespread contamination of aquatic systems LULC types was unavoidable. We used ArcGIS 10.1 (ESRI, Redlands, (Fitzgerald et al., 1998; Hammerschmidt and Fitzgerald, 2005; CA, USA) to calculate percent cover by vegetation class within Blocksom et al., 2010), the amount of currently available informa- 500 meters (m) of the channel following Zelt and Johnson (2005), tion on aquatic-to-terrestrial contaminant fluxes does not reflect and performed ground-based surveys to document bridge crossings, the potential scale of the problem. In particular, although the impacts vegetation structure, and vegetation composition. of land use and land cover (LULC) on riparian birds have been widely investigated (Sullivan et al., 2007; Luther et al., 2008; Pennington et al., 2.2. Field and laboratory methods 2008; Oneal and Rotenberry, 2009), the relationships between LULC and contaminant exposure to riparian birds from aquatic systems is 2.2.1. Sediment poorly understood. For example, riparian swallow species [e.g., bank In either 2010 or 2012, we collected five sediment cores (~10 cm (Riparia riparia), northern rough-winged (Stelgidopteryx serripennis), in depth) from each reach at approximately equidistant locations tree, and cliff (Petrochelidon pyrrhonota) swallows] are susceptible along the length of the reach (Walters et al., 2010). We collected to biomagnification of contaminants because of their dependence on a sediment cores by push-coring approximately 2 cm with a polycarbonate mixture of stream, riparian, and terrestrial food sources and habitats coring device. We sealed sediment composite samples in plastic sleeves, (Harris and Elliot, 2000; Dods et al., 2005; Custer, 2011). During the placed them on ice, and froze them at −20 °C until analysis (Lutz, 2008). reproductive season, riparian swallows tend to forage within several hundred meters (m) of their nest sites (Quinney and Ankney, 1985; 2.2.2. Periphyton and vegetation Dunn and Hannon, 1992), making them apt bioindicators of local Following methods used in Bartel et al. (2010) and Pennington stream and riparian conditions. Land-management practices that alter and Blair (2011), we surveyed riparian vegetation along three 100-m aquatic resource utilization by swallows might be expected to strongly transects (upstream, middle, downstream) along both banks (perpen- influence their exposure to aquatic contaminants. Roux and Marra dicular to the stream, n = 6/reach) at each reach. At each transect, we (2007), for instance, found that lead (Pb) concentrations in urban established three 5 m × 5 m quadrats, located at 0, 50, and 100-m passerine birds were significantly higher than in their rural counterparts, from the river's edge. We then estimated vegetation cover by height which corresponded with relative Pb concentrations found in soils. (b3m,3–5 m, and >5 m) and identified all trees, shrubs, grasses, Our objective was to explore the relationships between adjacent and other herbaceous plants to species. We visually estimated the (to the river) patterns in LULC and the magnitude of Hg and Se percent coverage of vegetation overhanging the water's edge along concentrations in four species of riparian swallows as mediated by both banks and counted standing dead trees of diameter at breast aquatic-to-terrestrial contaminant fluxes. Because of historic and height (dbh) >10 cm. contemporary differences in land-management and chemical use, we For stable isotope analysis, we collected five terrestrial vegetation hypothesized that concentrations of contaminants in river sediments, samples per transect on both sides of the river (along survey transects): 44 J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50

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. three samples from the numerically dominant tree species and two nests were sampled per reach. At all other reaches, variability in samples from the dominant species among the shrubs, grasses, herbs the accessibility and abundance (i.e., colony-nesting cliff swallows and sedges. We stored leaf samples in paper bags until further process- at some reaches, couple/few pairs of northern rough-winged swal- ing in the laboratory. We collected periphyton by scrubbing a 25-cm2 low at others) of swallows constrained sample size. However, we section of the dominant hard substrate (cobble) at each of the five collected blood from a minimum of four swallows at all non-nest transects within each reach following Reavie et al. (2010). The samples box reaches, except at the study reach “Mosquito”, where we were were composited by reach into a single polyethylene jar and preserved only able to capture three birds. Once drawn, we immediately trans- in 70% ethanol solution until analysis. ferred blood samples to centrifuge tubes where it was stored in 70% ethanol for later stable isotope analysis. We placed additional blood 2.2.3. Riparian swallows on Dried Blood Spot cards (PerkinElmer, Waltham, MA, USA) for We selected a suite of riparian swallow species (tree, cliff, bank, contaminant analysis. DBS cards are an appropriate technique and northern rough-winged swallows) that were common to the to sample blood from small-bodied animals (b20 g; mean weight study system. These swallow species are obligate aerial insectivores of birds in our study at collection was 16.6 g, SD = 3.8 g), from that naturally breed in riparian habitats (riparian tree cavities, which adequate sample volume can preclude traditional methods riverbanks, cliffs and bridges, etc.) (Robertson et al., 1992; Brown and (Shlosberg et al., 2011). Brown, 1995; DeJong, 1996; Garrison, 1999). Given potential differences in species-specific exposure patterns to contaminants, we ideally would have focused our efforts on one riparian swallow species. 2.2.4. Invertebrates However, the distribution of swallow species in the study system Adult tree swallows typically return to the nest with a bolus of precluded this option, as there was no one species of swallow found invertebrate prey carried in their beaks, which we removed from their at all the study reaches. Others have also used a foraging guild-based mouths before the parent fed the nestlings at nest box reaches approach to investigate contaminant exposure in birds (e.g., Jackson (McCarty and Winkler, 1999; Echols et al., 2004). At all other reaches, et al., 2011). We conducted all sampling during the swallow reproduc- we deployed six floating aquatic emergent insect traps (i.e., pyramid tive season (May–early August in 2011 and 2012). traps) per reach as described by Aubin et al. (1973). We deployed At seven of the eleven research reaches, we captured swallows using traps along both banks of the reach such that they represented mist nets set over the river or in the riparian zone. We erected six nest dominant flow habitats (i.e., riffle, pool/run). For terrestrial insects, we boxes at each of four additional reaches, following design protocols set suspended half-sized Malaise traps (1-m high, 1-m long, 0.6-m wide, by the Golondrinas de las Américas (2011) project at Cornell University. 0.5-mm mesh, MegaView Science Co., Taichung, Taiwan; Townes, All nest boxes were placed within or along the edge of the riparian zone 1972) from trees at 10 m and 50 m from the active river channel approx- and were within 100 m from the river on the average. We equipped imately in the middle of the study reach, on both banks. We collected all each box with an external trapping mechanism (i.e., wig-wag), which invertebrates five and ten days after trap deployment. allowed the capture of adult tree swallows while they were inside the Upon collection, we placed all invertebrates in jars, put them nest box. At first capture, we banded all birds with aluminum USFWS on ice for transport, and froze them at −20 ° C until analysis (Lutz, size 0 bands for tree, bank, and northern rough-winged swallows, and 2008). In the laboratory, we identified all individuals to family size 1 bands for cliff swallows. We drew blood from the jugular vein using Johnson and Triplehorn (2004). For bolus invertebrates, we to be used for stable isotope and contaminant analyses (Ardia, 2005; also classified all individuals by their origin (i.e., aquatic or terrestrial Sullivan and Vierling, 2012). We collected blood from a minimum of according to their larval habitat). Following identification, we dried three adults and four nestlings during the second week after hatching and weighed invertebrates by family (total dry mass per reach at each of the experimental nest box reaches, where at least two [mg m−2 d−1]; Iwata et al., 2003). J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50 45

2.2.5. Contaminant and stable isotope analysis were retained for use in subsequent linear regression models All sediment, bolus, and swallow blood samples were analyzed for (Rencher, 1995; Sullivan and Watzin, 2008). We used weighted linear Hg and Se concentrations [parts per billion (ppb) dry weight] at regression to examine the best LULC predictors of contaminant the Diagnostic Center for Population and Animal Health, Toxicology concentrations in swallows. We used two-sample t-tests to test for Section, Michigan State University. ICP-AES (Varian Vista, now part potential differences in (1) the contribution of aquatic resources to of Agilent, Santa Clara, CA) and ICP-MS (Agilent 7500ce) instruments swallows and (2) contaminant concentrations in sediment, aquatic were calibrated with standards derived from NIST-traceable stock so- insects, and riparian swallows between LULC types. We used paired lutions for each element (GFS Chemicals, Inc., Cincinnati, OH). Quality t-tests to test for differences between contaminant concentrations was assured in each sequence run by analyzing lab reagent blanks, in (1) adult and nestling swallows and (2) aquatic and terrestrial in- NIST (National Institute of Standards & Technology, Gaithersburg, sects from bolus samples. To avoid potential pseuodreplication at nest MD)-traceable Multi-mix (Alfa Aesar Specpure, Ward Hill, MA) and box reaches where multiple nestlings were sampled from the same digests of NIST Standard Reference Materials (SRM), including Mussel box, mean contaminant concentrations of nestlings per nest box Tissue 2976, Trace Elements in Water 1643e and/or Montana II Soil were used in the analysis. Data were tested at the α = 0.05 level. 2711a, as appropriate. Mercury was analyzed by cold vapor atomic However, given multiple regression tests, the Bonferroni adjustment absorption spectrometry (CETAC CVAA, Omaha, NB) with similar for α was α / k = 0.05 / 5 = 0.010, where k is the number of tests calibration and QC. Analysis of blood was performed by methods (Wright, 1992). Prior to the analysis, concentrations of Se and Hg outlined in Lehner et al. (in press) with reference to BioRad (Hercules, were log10 were transformed to normalize data and eliminate CA) Lypochek 2 and 3 standards for verification of accuracy. heteroscedasticity (Zar, 1984). Terrestrial vegetation, terrestrial insects (Curculionidae, Doli- chopodidae, and Cicadellidae), periphyton, aquatic emergent insects (Chironomidae, Hydropsychidae, and Heptageniidae), and bird blood 3. Results samples were analyzed for 13Cand15N stable isotopes using continuous flow isotope ratio mass spectrometry (EA-IRMS) at the University of Sediment concentrations of Se ranged from 367 to 2440 ppb, Washington Stable Isotope Core (Pullman, WA, USA). The isotopic while sediment Hg ranged from 31 to 137 ppb. Neither Se (t =1.14, composition of samples was expressed using the δ13Cnotation P =0.327,df = 7) nor Hg (t = 0.157, P = 0.881, df =7)insediment defined as follows: was 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, hi 13 13 12 df = 7) in aquatic emergent insects was different between urban and δ C ¼ R =R –1 1000; where R is C= C ð1Þ sample standard rural reaches. Concentrations of Se and Hg in riparian swallows varied widely across study reaches (Supplemental Data Table 1). Hg con- where parts per thousand (‰) are the atomic ratios of the number centrations in swallows were positively related to Hg concentrations of atoms in the sample or standard. Typical analytical precision in sediment (Fig. 2), although no relationship was evident be- was +/-0.2‰ for δ13C determination. tween Se in swallows and in sediment. Se concentrations were greater in aquatic (mean = 3956 ppb, SD =2039) than in terres- 2.2.6. Numerical and statistical analyses trial (mean = 1132 ppb, SD = 1089) invertebrate swallow prey Because of the largely longitudinal distribution of our study reaches (t = −4.11, P = 0.027, df = 2). A similar, but weaker relationship along the river system, we considered testing for spatial autocorrelation was found for Hg (aquatic: mean = 66.3 ppb, SD = 28.3, terrestrial: of all measured variables. However, the focus of our study was on the mean = 32.7 ppb, SD = 10.8; t = −2.17, P = 0.081, df =2).Moran's role terrestrial environmental characteristics played in mediating fluxes I indicated that there was no spatial clustering of swallow contaminant of contaminants to riparian consumers, and not on the distribution of concentrations (P > 0.05 in all cases), suggesting that observations river contaminants themselves. Therefore, we used Moran's I (1950) from nearby study reaches were independent from one another. statistic (Cliff and Ord, 1973) to describe spatial patterns of swallow contaminant concentrations only. Positive and significant (P b 0.05) Moran's I values indicate a more spatially-clustered distribution than would be expected if the underlying spatial processes were random, whereas negative values indicate greater spatial dispersion. Because we observed no differences in δ13Candδ15N values between adult and nestling swallows based on paired t-tests, we grouped nestlings and adults by species for each study reach. We then analyzed the contributions of aquatic and terrestrial food sources to riparian swallows at each study reach using (1) dual isotope plots of δ13Cand δ15N, (2) linear regression between δ13C of swallows and periphyton (i.e., gradient approach; Jardine et al., 2012), and (3) invertebrates from bolus samples. For dual-isotope plots, spatial correspondence between δ13Candδ15N values in swallows and aquatic prey indicates greater use of aquatic prey (DeNiro and Epstein, 1978, 1981). We created one plot for each land-use class (i.e., urban and rural) and plotted δ13C and δ15N values for swallows by species, given potential variability in isotopic signatures among species. Because of an unbalanced number of swallows at each reach, we used weighted linear regression to deter- mine the degree to which swallow δ13C tracked periphyton δ13Cacross all study reaches. We used invertebrate composition from bolus samples Fig. 2. Relationship between Hg concentrations (log10) in riparian swallows and sediment fi to further inform aquatic:terrestrial prey use by tree swallows. (log10) (ppb). The slope for the regression model was signi cant (y = 0.39x + 3.25, R2 =0.33,P = 0.008). Two data points (open circles) were considered outliers and omitted We performed principal component analysis (PCA) on riparian from the analysis, although the regression was also significant with these two points included LULC variables that we had selected a priori as candidate predictors (y = 0.46x + 2.95, R2 = 0.23, P = 0.030). Dashed lines represent confidence curves at of riparian swallow prey utilization. PCA axes with eigenvalues > 1 α = 0.05. 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 −26.77 to −20.29‰ for δ13C and from 6.63 to 12.74‰ for δ15N. Signatures for aquatic emergent insect δ13Crangedfrom−28.27 to −27.04‰,while δ15N ranged from 10.04 to 12.31‰. Terrestrial insect δ13Crangedfrom −25.84 to −22.47‰ whereas δ15N of terrestrial insects ranged from 5.10 to 8.74‰. Terrestrial vegetation δ13C ranged from −31.53 to −28.00‰,andδ15N from 2.72‰ to 4.68‰. Periphyton exhibited the greatest variation, ranging from −21.46 to −11.26‰ for δ13C, and from 6.14 to 12.39‰ for δ15N. We found no significant differences 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 the stream–riparian food web (Fig. 3a & b). For rural (Fig. 3a) and urban (Fig. 3b) reaches, isotope plots indicated that swallows were reliant on a mixture of aquatic and terrestrial food resources, although swallows were presumably more δ15N enriched at urban reaches (based on the lower δ15N enrichment of primary producers at urban reaches along with the invariant swallow δ15N signatures for swallows at both urban and rural reaches). Swallow δ13C negatively tracked periphyton δ13C at urban, but not rural, reaches (Fig. 4), indicating that swallows were not heavily reliant on instream primary productivity at urban reaches. However, this relationship does not preclude swallow reliance on aquatic emergent insects, which can be highly reliant on terrestrial inputs of vegetation, as in this study (Fig. 3a and b). The variability explained by this regression serves as our minimum contribution of Fig. 3. Dual isotope plots of δ13C and δ15N values (mean ± 1 SE) for the Scioto River aquatic emergent insections to swallow diet (Fig. 4). basin (Ohio, USA) aquatic and terrestrial food-web components of the Scioto River Bolus results from the four nest box reaches indicated that basin (Ohio, USA) in (a) rural and (b) urban reaches. swallows at urban locations relied more heavily on aquatic insects than at rural locations (Fig. 5). By weight, aquatic emergent insects comprised 84.0% of swallow diet (vs. 16.0% from terrestrial inverte- 3.2. Influence of LULC brates) at urban locations, whereas aquatic emergent insects comprised only 46.4% of swallow diet (vs. 53.6% from terrestrial invertebrates) Principal component analysis of eleven LULC measures identified at rural nest box locations. Individuals of the family Coenegrionidae three axes with eigenvalues > 1 (Table 2). The first principal com- (narrow-winged damselflies) made up nearly 30% of all aquatic individ- ponent (PC1) captured 54.4% of the variance, and was mainly driven uals collected, whereas Aeshnidae (hawkers or darners) represented by factors related to urbanized landscapes (e.g., population density the largest-bodied prey item. [r2 = 0.91, + correlation], % impervious surface coverage [r2 =0.86, Concentrations of Se in riparian swallows were linked with both +], % agriculture [r2 =0.86, −]). Accordingly, this PC was named δ15Nandδ13C isotopic values (Fig. 6a and b). Swallow Se concentrations ‘Urbanization Axis’. The second principal component explained about increased with δ15Nenrichmentandδ13C depletion, both of which are 19% of the variation that remained and was driven almost solely by % isotopic signals indicative of a shift toward aquatic prey resources in tall tree cover (r2 = 0.86, +), and is hereafter referred to as “Mature our system. Concentrations of Hg were not related to either swallow Trees Axis”. No other metric within this axis had a correlation > 0.32. δ15N(P = 0.971) or δ13C(P =0.152)signatures. The third PC, “Shoreline Habitat Axis”, explained about 14% of the

Table 1 δ13C and δ15N values for riparian swallows, periphyton, riparian vegetation, aquatic emergent insects, and terrestrial invertebrates for all study reaches in the Scioto River basin, Ohio, USA. Reaches are presented upstream to downstream. Note: CLSW = cliff swallow, BANS = bank swallow, TRSW = tree swallow, NRWS = northern rough-winged swallow.

Study reach Land use Swallows Periphyton Terrestrial Aquatic Terrestrial Insect Vegetation Emergent Insects

Species δ13C δ15N δ13C δ15N δ13C δ15N δ13C δ15N δ13C δ15N

1 (Highbanks) Rural TRSW −24.69 10.016 N/A N/A N/A N/A N/A N/A N/A N/A 2 (Wetlands) Urban TRSW −24.55 11.00 −18.49 6.88 −30.96 2.72 −27.41 11.29 −27.78 11.15 3 (Fawcett) Urban TRSW −24.42 10.80 N/A N/A N/A N/A N/A N/A N/A N/A 4 (Horseshoe) Urban CLSW −23.24 9.04 −17.69 6.14 −30.37 3.08 −27.51 10.04 −27.97 12.31 5 (Berliner) Urban TRSW −26.14 12.39 −11.26 7.35 −30.81 4.22 −28.27 11.09 −27.99 12.66 6 (Mosquito) Rural NRWS −24.61 11.77 −18.79 8.42 −28.06 4.68 −27.04 11.55 −27.34 11.83 7 (Darby) Rural TRSW −24.07 10.00 N/A N/A N/A N/A N/A N/A N/A N/A 8 (Gravel Bar) Rural BANS −24.42 10.37 −11.68 12.39 −28.00 3.74 27.78 11.15 −25.09 6.79 9 (Piketon) Rural CLSW −23.35 7.91 −21.46 8.66 −31.52 4.53 −27.97 12.31 −25.09 7.74 10 (Treefall) Rural BANS −25.15 10.87 −14.82 8.78 −31.53 3.27 −27.99 12.66 −23.83 8.31 11 (Last) Rural BANS −23.98 11.13 −13.41 9.64 −30.56 2.89 −27.34 11.83 −25.42 7.64

Note: N/A = not applicable because diet composition was analyzed directly using bolus samples. J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50 47

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 regression model 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).

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 Hg concentrations were significantly higher in rural than in urban reaches (t = −2.96, P = 0.003, df = 24), and marginally so for Se (t = −1.54, P = 0.068, df = 24). A combination of urban characteristics and minimal agricultural activity in the riparian zone appeared to be, in part, driving this association, as we found that 15 Fig. 6. Relationship between swallow Se concentration (log10) and (a) swallow δ N the Urbanization Axis was negatively related to both Hg (Fig. 7a) and (b) swallow δ13C. The slopes for the regression models were significant for and Se concentrations in swallows (Fig. 7b). Urbanization was both δ15N (y = 0.55x + 3.26, R2 = 0.76, P b 0.001) and δ13C(y=−0.30x − 1.90, 2 also negatively related to δ15N enrichment (Fig. 8),whichinour R = 0.27, P = 0.032). Dashed lines represent confidence curves at α = 0.05. system indicates a decreasing reliance on aquatic prey along this axis. 4. Discussion We found that Hg concentrations were significantly higher in adult swallows (mean = 183.1 ppb) than nestlings (mean = Aquatic emergent insects serve as important prey items for myriad 57.0 ppb) (t = −4.01, P =0.016, df = 4). Se concentrations in riparian consumers (Akamatsu et al., 2004; Ballinger and Lake, 2006). adults (mean = 9635 ppb) were also significantly higher than in As a result of these strong, cross-system linkages, terrestrial consumers nestlings (mean = 1997 ppb) (t = −3.10, P = 0.036, df = 4). Age- are exposed to aquatic contaminants (Akamatsu and Toda, 2011). dependent trends in contaminant concentration were consistent across Walters et al. (2008), for example, showed that aquatic emergent both urban LULC and rural LULC. insects transported PCBs from contaminated lake sediments into adjacent riparian food webs. Our understanding of the mechanisms

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

Urbanization Mature trees Shoreline habitat

Riparian landscape Loading r2 Loading r2 Loading r2 composition metrics

% Agriculture −0.38 0.86 0.08 0.01 0.02 0.00 % Shrub cover(1–3m) 0.34 0.69 0.02 0.00 −0.38 0.22 % Small tree cover (3–6m) 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 0.69 Riparian 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 0.01 Human population density 0.39 0.91 −0.10 0.02 0.13 0.03 (residents/km2) % Overhanging vegetation 0.26 0.40 0.13 0.04 0.56 0.48 Eigenvalue 5.98 2.10 1.53 Fig. 5. Contribution by weight of aquatic emergent and terrestrial insects to swallow % variance 54.4 19.1 14.0 boluses from nest box reaches (n = 40). Error bars represent ± 1 SE from the mean. 48 J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50

comprised of 54.9% aquatic insects by biomass. Similarly, Wayland et al. (1998) found that insects of aquatic origin made up 50–60% of tree swallow diet in western Canada. Collectively, our results indicate that swallows rely on a mixture of terrestrial and aquatic insects, but that reliance 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) aerial insect productivity between rural and urban reaches in the study system (Kautza and Sullivan, unpublished data). Many riparian swallow species tend to forage in open areas (Brown et al., 2002; Ghilain and Belisle, 2008), indicating a likely preference for feeding over open water vs. heavily-canopied riparian areas. Our urban reaches were gen- erally characterized by densely-forested strips in the immediate riparian zone, which may encourage foraging directly over water and explain why urban swallows fed more heavily on aquatic emergent insections than their rural counterparts. Contrary to our hypothesis, sediment contaminant concentrations did not differ between land-use classes. However, Hg and Se concentrations in riparian swallows were lower at urban than at rural reaches, despite the fact that urban nest box swallows depredated aquatic insects more commonly than terrestrial insects, and that bolus samples indicated that aquatic insects exhibited higher concentrations of Se and Hg than terrestrial insects. Concomitantly, concentrations of Hg in swallow blood and river sediment were positively related (Fig. 2), which suggests that riparian swallows are exposed to aquatic contaminants via aquatic prey. Likewise, Se concentrations in swallows were positively linked to both δ15Nenrichmentandδ13C 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. One

Fig. 7. Relationship between Urbanization Axis (i.e., PC1) and (a) Hg concentration possible explanation for this apparent discrepancy between contribu-

(log10) and (b) Se concentration (log10) in riparian swallows. Degree of urbanization tion of aquatic prey and contamination patterns is that swallows were increases from −3 to 4. The slope for the regression model was significant for actively selecting prey that were not dominant within the system, 2 both Hg (y = −0.11x − 4.91, R = 0.38, P = 0.004) and Se (y = −0.17x + 9.12, and therefore not included in our isotopic or contaminant analyses. 2 b fi α R = 0.63, P 0.001). Dashed lines represent con dence curves at = 0.05. Blancher and McNicol (1991) for example, found that mayflies were an important component of tree swallow diet despite composing a that influence and mediate these exposure pathways remains limited, small fraction of the insects caught in emergent traps. It is also possible but given the geographic range and abundance of aquatic emergent that varying bioavailability among metal speciations found within the insects and riparian consumers, and the global proliferation of aquatic sediments leads to unequal transfer to swallows through predation of contamination (Menzie, 1980; Walters et al., 2008), an improved aquatic emergent insects. For instance, Langner et al. (2012) observed grasp of these cross-boundary flows will be crucial for managing terres- that blood Hg concentrations in osprey (Pandion haliaetus)chicksdid trial exposure risk from aquatic contaminants. not reflect Hg concentrations in river sediments, which they suggested Many investigators have illustrated the variability in swallow was due to decreased methylation, and thus bioavailability, of Hg. dietary composition. For example, Blancher and McNicol (1991) deter- Influences of land cover on avian foraging behavior likely explain mined that the diet of non-egg-laying adult tree swallows was patterns we observed in swallow contaminant concentrations. Ormerod and Tyler (1991) found that gray wagtails (Motacilla cinerea) changed their diet to incorporate more lepidopteran larvae in broadleaved forests than in moorlands or coniferous forests in Wales. Such dietary shifts in response to land-cover variation could have a profound effect on contaminant uptake. Biomagnification of aquatic contaminants in tree swallows, for instance, is known to be linked with their reliance on aquatic emergent insects (Brasso and Cristol, 2008; Hallinger et al., 2011; Jackson et al., 2011), which is consistent with our results for Se (Fig. 6). Our observation that contaminant biomagnification was higher in adult swallows relative to nestlings aligns with other studies and was consistent with our hypothesis. Evers et al. (2005), for instance, found that methylmercury (MeHg) concentrations were five to ten times higher in adult tree swallows than in nestlings. Although we did not observe a difference in the dietary composition (aquatic vs. terrestrial) between adult and immature swallows, nestlings might efficiently remove contaminants from their blood as they are deposited into growing feathers (Tsipoura et al., 2008). Alternatively, adult swallows Fig. 8. Relationship between Urbanization Axis (i.e., PC1) and δ15N in riparian swallows. may feed on larger-bodied aquatic insects, thereby increasing exposure Urbanization increases from −3.0 to 4.0. The slope for the regression model was significant (y = −0.23x + 10.9, R2 = 0.38, P = 0.031). Dashed lines represent confidence curves at to aquatic contaminants. In Canada, Quinney and Ankney (1985) found α =0.05. that Insects 1–6 mm in length made up between 80% and 86% of J.M. Alberts et al. / Science of the Total Environment 463-464 (2013) 42–50 49 nestling tree swallow diet, whereas McCarty and Winkler (1999) 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. found that adult tree swallows actively selected for larger-bodied J Am Vet Med Assoc 1975;167:592–7. prey (e.g., Odonata) as compared to smaller-bodied insections (0–3mm Bishop CA, Mahony NA, Trudeau S, Pettit KE. Reproductive success and biochemical in length). Temporal disparities between aquatic insect emergence and effects in tree swallows (Tachycineta bicolor) exposed to chlorinated hydrocarbon fl contaminants in wetlands of the Great Lakes and St. Lawrence River basin, USA and terrestrial insect production might also in uence prey availability and Canada. Environ Toxicol Chem 1999;18:263–71. feeding behavior (Nakano and Murakami, 2001; Jonsson et al., 2012), Blancher PJ, McNicol DK. Tree swallow diet in relation to wetland acidity. Can J Zool which could result in nestlings ingesting a higher proportion of terrestrial (Rev Can Zool) 1991;69:2629–37. insects, thereby decreasing their exposure to aquatic contaminants. Blocksom KA, Johnson BR. Development of a regional macroinvertebrate index for large river bioassessment. Ecol Indic 2009;9:313–28. Blocksom KA, Walters DM, Jicha TM, Lazorchak JM, Angradi TR, Bolgrien DW. Persistent organic pollutants in fish tissue in the mid-continental great rivers of the United 5. Conclusions States. Sci Total Environ 2010;408:1180–9. Brasso RL, Cristol DA. Effects of mercury exposure on the reproductive success of tree Overall, our results (1) support recent research examining the swallows (Tachycineta bicolor). Ecotoxicology 2008;17:133–41. cross-system trophic linkages between aquatic emergent insects and Brown CR, Brown MB. Cliff swallow (Hirundo pyrrhonota). In: Poole A, Gill F, editors. The birds of North America, 149. Washington, D.C.: The Academy of Natural Sciences, riparian consumers (Ballinger and Lake, 2006; Fukui et al., 2006; Philadelphia, PA, and The American Ornithologists' Union; 1995 Daley et al., 2011), and (2) implicate landscape alterations as a key Brown CR, Sas CM, Brown MB. Colony choice in cliff swallows: effects of heterogeneity – factor in regulating aquatic-to-terrestrial contaminant transfers. Our re- in foraging habitat. Auk 2002;119:446 60. Cliff A, Ord K. Spatial autocorrelation. London: Pion; 1973. sults also provide insight into the role of riparian swallows as integrators Cristol DA, Brasso RL, Condon AM, Fovargue RE, Friedman SL, Hallinger KK, et al. of linked aquatic–terrestrial systems within the context of contaminant The movement of aquatic mercury through terrestrial food webs. Science 2008;320: exposure risk. Specifically, the reliance of swallows upon a mixture of 335-335. Custer CM. Swallows as a sentinel species for contaminant exposure and effect studies. terrestrial and aquatic invertebrate prey makes them highly vulnerable Wildlife Ecotoxicology: Forensic Approaches 2011;3:45–91. to contaminants from both terrestrial and aquatic systems. Their ability Daley JM, Corkum LD, Drouillard KG. Aquatic to terrestrial transfer of sediment associated to range freely and utilize multiple prey sources makes them excellent persistent organic pollutants is enhanced by bioamplification processes. Environ Toxicol Chem 2011;30:2167–74. organisms for examination of large, cross-boundary trophic and material DeJong MJ. Northern rough-winged swallow (Stelgidopteryx serripennis). In: Poole A, transfer processes. Gill F, editors. The birds of North America, 234. Washington, D.C.: The Academy Building upon previous work (Blancher and McNicol, 1991; of Natural Sciences, Philadelphia, and The American Ornithologists' Union; 1996 Deniro MJ, Epstein S. Influence of diet on distribution of carbon isotopes in animals. Bishop et al., 1999; Harris and Elliott, 2000; McCarty, 2002), we Geochim Cosmochim Acta 1978;42:495–506. suggest that riparian swallow species may capture system-level Deniro MJ, Epstein S. Influence of diet on the distribution of nitrogen isotopes in mechanisms of contamination. We argue that the trophic dynamics animals. Geochim Cosmochim Acta 1981;45:341–51. of riparian swallows and other insectivorous riparian birds represent Dods PL, Birmingham EM, Williams TD, Ikonomou MG, Bennie DT, Elliott JE. Reproductive success and contaminants in tree swallows (Tachycineta bicolor)breedingatawaste- a critical pathway for cross-boundary contaminant transfer and water treatment plant. Environ Toxicol Chem 2005;24:3106–12. movement across linked aquatic–terrestrial landscapes. Studies across Dreyer J, Hoekman D, Gratton C. Lake-derived midges increase abundance of shoreline – broader geographical ranges and with increased sample sizes will be terrestrial arthropods via multiple trophic pathways. Oikos 2012;121:252 8. Dunn PO, Hannon SJ. Effects of food abundance and male parental care on reproductive helpful in further testing this hypothesis as will additional research rel- success and monogamy in tree swallows. Auk 1992;109:488–99. ative to species-specific swallow feeding behavior, movement patterns, Echols KR, Tillitt DE, Nichols JW, Secord AL, McCarty JP. Accumulation of PCB congeners and resource utilization. The potential role of swallows themselves as in nestling tree swallows (Tachycineta bicolor) on the Hudson River, New York. Environ Sci Technol 2004;38:6240–6. vectors of contaminants (e.g., via feces, feathers, and nesting colonies) Evers DC, Burgess NM, Champoux L, Hoskins B, Major A, Goodale WM, et al. Patterns across both local (i.e., nesting) and broader (i.e., migratory) spatial scales and interpretation of mercury exposure in freshwater avian communities in north- will also be important in further understanding aquatic–terrestrial eastern North America. Ecotoxicology 2005;14:193–221. fl Fitzgerald WF, Engstrom DR, Mason RP, Nater EA. The case for atmospheric mercury contaminant uxes. Lastly, continued research related to the mediating contamination in remote areas. Environ Sci Technol 1998;32:1–7. role of terrestrial landscapes on transfers of contaminants from aquatic Fukui D, Murakami M, Nakano S, Aoi T. Effect of emergent aquatic insects on bat foraging to terrestrial systems will be critical for improved remediation and in a riparian forest. J Anim Ecol 2006;75:1252–8. Garrison BA. Bank swallow (Riparia riparia). In: Poole A, Gill F, editors. The birds of long-term conservation of river ecosystems. North America, 414. Philadelphia, PA: The Birds of North America, Inc.; 1999. Supplementary data to this article can be found online at http:// Ghilain A, Belisle M. Breeding success of tree swallows along a gradient of agricultural dx.doi.org/10.1016/j.scitotenv.2013.05.065. intensification. 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, Acknowledgments 2010. Hagen EM, Sabo JL. Influence of river drying and insect availability on bat activity along the San Pedro River, Arizona (USA). J Arid Environ 2012;84:1–8. Research support was provided by state and federal funds appro- Hallinger KK, Cornell KL, Brasso RL, Cristol DA. Mercury exposure and survival in priated to The Ohio State University, Ohio Agricultural Research and free-living tree swallows (Tachycineta bicolor). Ecotoxicology 2011;20:39–46. Hamas MJ. Belted kingfisher (Cerlye alcyon). In: Poole A, Gill F, editors. The birds of Development Center. We would like to thank Paradzayi Tagwireyi North America, 84. Washington, DC, USA: The American Ornithologists' Union; for his help in the field. 1994. Hammerschmidt CR, Fitzgerald WF. Methylmercury in mosquitoes related to atmospheric mercury deposition and contamination. Environ Sci Technol 2005;39: References 3034–9. Harris ML, Elliott JE. Reproductive success and chlorinated hydrocarbon contamination Akamatsu F, Toda H. Aquatic subsidies transport anthropogenic nitrogen to riparian in tree swallows (Tachycineta bicolor) nesting along rivers receiving pulp and spiders. Environ Pollut 2011;159:1390–7. paper mill effluent discharges. Environ Pollut 2000;110:307–20. Akamatsu F, Toda H, Okino T. Food source of riparian spiders analyzed by using stable Henschel JR, Mahsberg D, Stumpf H. Allochthonous aquatic insects increase predation isotope ratios. Ecol Res 2004;19:655–62. and decrease herbivory in river shore food webs. Oikos 2001;93:429–38. Ardia DR. Tree swallows trade off immune function and reproductive effort differently Iwata T, Nakano S, Murakami M. Stream meanders increase insectivorous bird abun- across their range. Ecology 2005;86:2040–6. dance in riparian deciduous forests. Ecography 2003;26:325–37. Aubin A, Bourassa JP, Pellissi M. Effective emergence trap for capture of mosquitoes. Jackson AK, Evers DC, Folsom SB, Condon AM, Diener J, Goodrick LF, et al. Mercury Mosq News 1973;33:251–2. exposure in terrestrial birds far downstream of an historical point source. Environ Pollut Ballinger A, Lake PS. Energy and nutrient fluxes from rivers and streams into terrestrial 2011;159:3302–8. food webs. Mar Freshw Res 2006;57:15–28. Jardine TD, Kidd KA, Rasmussen JB. Aquatic and terrestrial organic matter in the diet of Bartel RA, Haddad NM, Wright JP. Ecosystem engineers maintain a rare species of stream consumers: implications for mercury bioaccumulation. Ecol Appl 2012;22: butterfly and increase plant diversity. Oikos 2010;119:883–90. 843–55. Baxter CV, Fausch KD, Saunders WC. Tangled webs: reciprocal flows of invertebrate Johnson NF, Triplehorn CA. Borror and Delong's introduction to the study of insects. prey link streams and riparian zones. Freshw Biol 2005;50:201–20. 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 environmental Quinney TE, Ankney CD. Prey size selection by tree swallows. Auk 1985;102: variables on upland bird assemblages in northern Sweden. Ecol Res 2012;27:945–54. 245–50. Keast A. The annual cycle and activity on the breeding grounds in a Canadian Reavie ED, Jicha TM, Angradi TR, Bolgrien DW, Hill BH. Algal assemblages for large river broad-leafed deciduous forest bird community relationship to the prey resource monitoring: comparison among biovolume, absolute and relative abundance base. V+410pIn: Keast a, editor. Biogeography and ecology of forest bird commu- metrics. Ecol Indic 2010;10:167–77. nities. The Hague, Netherlands: Spb Academic Publishing Bv; 1990. p. 197–214. Rencher AC. Methods of multivariate analysis. New York, NY, U.S.A.: Johny Wiley and Illus Maps. Sons, Inc.; 1995 Langner HW, Greene E, Domenech R, Staats MF. Mercury and other mining-related con- Robertson RJ, Stutchbury BJ, Cohen RR. Tree swallow (Tachycineta bicolor). In: Poole A, taminants in ospreys along the Upper Clark Fork River, Montana, USA. Arch Environ Stettenheim P, Gill F, Poole A, Stettenheim P, Gill F, editors. The birds of North America, Contam Toxicol 2012;62:681–95. 11. Philadelphia, PA: The Academy of Natural Sciences; 1992. (The American Ornithol- Lehner A, Rumbeiha W, Shlosberg A, Stuart K, Johnson M, Domenech R, et al. Diagnostic ogists' Union, Washington, D.C.). analysis of veterinary dried blood spots for toxic heavy metals exposure. J Anal Roux KE, Marra PP. The presence and impact of environmental lead in passerine birds Toxicol 2013 In press. along an urban to rural land use gradient. Arch Environ Toxicol Chem 2007;53: Lenat DR, Crawford JK. Effects of land-use on water quality and aquatic biota of 3 North 261–8. Carolina piedmont streams. Hydrobiologia 1994;294:185–99. Sabo JL, Power ME. Numerical response of lizards to aquatic insects and short-term Lord CG, Gaines KF, Boring CS, Brisbin LL, Gochfeld M, Burger J. Raccoon (Procyon lotor) consequences for terrestrial prey. Ecology 2002;83:3023–36. as a bioindicator of mercury contamination at the US Department of Energy's Shlosberg A, Rumbeiha WK, Lublin A, Kannan K. A database of avian blood spot Savannah River Site. Arch Environ Contam Toxicol 2002;43:356–63. examinations for exposure of wild birds to environmental toxicants: the DABSE Luther D, Hilty J, Weiss J, Cornwall C, Wipf M, Ballard G. Assessing the impact of local biomonitoring project. J Environ Monit 2011;13:1547–58. habitat variables and landscape context on riparian birds in agricultural, urbanized, Stepenuck KF, Crunkilton RL, Wang LZ. Impact of urban land use on macroinvertebrate and native landscapes. Biodivers Conserv 2008;17:1923–35. communities in southeastern Wisconsin streams. J Am Water Resour Assoc Lutz MA. Procedures for collecting and processing streambed sediment and pore water 2002;38:1041–51. for analysis of mercury as part of the National Water-Quality Assessment Program. Sullivan SMP, Rodewald AD. In a state of flux: the energetic pathways that move Open File Report 2008;2008-1279. contaminants from aquatic to terrestrial environments. Environ Toxicol Chem Malinga M, Szefer P, Gabrielsen GW. Age, sex and spatial dependent variations in heavy 2012;31:1175–83. metals levels in the Glaucous Gulls (Larus hyperboreus) from the Bjornoya and Jan Sullivan SMP, Vierling KT. Exploring the influences of multiscale environmental factors Mayen, Arctic. Environ Monit Assess 2010;169:407–16. on the American dipper Cinclus mexicanus. Ecography 2012;35:624–36. Mattson DJ, Reinhart DP. Influences of cutthroat trout (Oncorhynchus clarki)onbehaviour SullivanSMP,WatzinMC.Relating stream physical habitat condition and con- and reproduction of Yellowstone grizzly bears (Ursus arctos), 1975–1989. Can J Zool cordance of biotic productivity across multiple taxa. Can J Fish Aquat Sci (Rev Can Zool) 1995;73:2072–9. 2008;65:2667–77. Maul JD, Belden JB, Schwab BA, Whiles MR, Spears B, Farris JL, et al. Bioaccumulation Sullivan SMP, Watzin MC, Keeton WS. A riverscape perspective on habitat associations and trophic transfer of polychlorinated biphenyls by aquatic and terrestrial insects among riverine bird assemblages in the Lake Champlain Basin, USA. Landsc Ecol to tree swallows (Tachycineta bicolor). Environ Toxicol Chem 2006;25:1017–25. 2007;22:1169–86. McCarty. Useoftreeswallowsinstudiesofenvironmental stress. Rev Toxicol (Amsterdam) Sweeney BW, Vannote RL. Population synchrony in mayflies — a predator satiation 2002;4:61–104. hypothesis. Evolution 1982;36:810–21. McCarty JP, Winkler DW. Foraging ecology and diet selectivity of tree swallows feeding Townes H. A light weight malaise trap. Entomol News 1972;83:239–47. nestlings. Condor 1999;101:246–54. Tsipoura N, Burger J, Feltes R, Yacabucci J, Mizrahi D, Jeitner C, et al. Metal concentrations Menzie CA. Potential significance of insects in the removal of contaminants from in three species of passerine birds breeding in the Hackensack Meadowlands of aquatic systems. Water Air Soil Pollut 1980;13:473–9. New Jersey. Environ Res 2008;107:218–28. Meyer LA, Sullivan SMP. Bright lights, big city: influences of ecological light pollution United States Census Bureau. State and county quick facts. http://quickfacts.census. on reciprocal stream–riparian invertebrate fluxes. Ecol Appl 2013 In press. gov/qfd/states/39/39049.html, 2010 (Accessed July 29, 2012). Morrissey CA, Bendell-Young LI, Elliott JE. Linking contaminant profiles to the diet Vander Zanden MJ, Sanzone DM. Food web subsidies at the land–water ecotone. In: and breeding location of American dippers using stable isotopes. J Appl Ecol 2004;41: Polis GA, Power ME, Huxel GR, editors. Food webs at the landscape level. Chicago, 502–12. USA: University of Chicago Press; 2004. Nakano S, Murakami M. Reciprocal subsidies: dynamic interdependence between Varley JD, Schullery P. Yellowstone Lake and its cutthroat trout. Science and ecosystem terrestrial and aquatic food webs. Proc Natl Acad Sci U S A 2001;98:166–70. management in the national parks 1996;49–73. Oneal AS, Rotenberry JT. Scale-dependent habitat relations of birds in riparian corridors Vessel RD. Energetics of the belted kingfisher (Megaceryle alcyon). Corvalis, OR, USA: in an urbanizing landscape. Landsc Urban Plann 2009;92:264–75. Oregon State University; 1978. Ormerod SJ, Tyler SJ. The influence of stream acidification and riparian land-use on the Wada H, Cristol DA, McNabb FMA, Hopkins WA. Suppressed adrenocortical responses feeding ecology of gray wagtails (Motacilla cinerea) in Wales. Ibis 1991;133:53–61. and thyroid hormone levels in birds near a mercury-contaminated river. Environ Paetzold A, Schubert CJ, Tockner K. Aquatic terrestrial linkages along a braided-river: Sci Technol 2009;43:6031–8. riparian arthropods feeding on aquatic insects. Ecosystems 2005;8:748–59. Walters DM, Fritz KM, Otter RR. The dark side of subsidies: adult stream insects export Pennington DN, Blair RB. Habitat selection of breeding riparian birds in an urban organic contaminants to riparian predators. Ecol Appl 2008;18:1835–41. environment: untangling the relative importance of biophysical elements and spatial Walters DM, Mills MA, Fritz KM, Raikow DF. Spider-mediated flux of PCBs from con- scale. Divers Distrib 2011;17:506–18. taminated sediments to terrestrial ecosystems and potential risks to arachnivorous Pennington DN, Hansel J, Blair RB. The conservation value of urban riparian areas birds. Environ Sci Technol 2010;44:2849–56. for landbirds during spring migration: land cover, scale, and vegetation effects. Wayland M, Trudeau S, Marchant T, Parker D, Hobson KA. The effect of pulp and paper Biol Conserv 2008;141:1235–48. mill effluent on an insectivorous bird, the tree swallow. Ecotoxicology 1998;7: Polis GA, Anderson WB, Holt RD. Toward an integration of landscape and food web 237–51. ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst White D, Johnston K, Miller M. Ohio river basin. Rivers of North America. Burlington, 1997;28:289–316. Massachusetts: Elsevier Academic Press; 2005. p. 375–424. Polis GA, Sanchez-Pinero F, Stapp PT, Anderson WB, Rose MD. Trophic flows from Wright SP. Adjusted p-values for simultaneous inference. Biometrics 1992;45:1005–13. water to land: marine input affects food webs of islands and coastal ecosystems Zar JH. Biostatistical analysis. Englewood Cliffs, New Jersey: Prentice-Hall; 1984. worldwide. In: Polis GA, Power ME, Huxel GR, editors. Food webs at the landscape Zelt RB, Johnson MR. Protocols for mapping and characterizing land use/land cover level. Chicago, Illinois: University of Chicago Press; 2004. p. 200–16. in riparian zones. U.S. geological survey open-file report; 2005. [2005-1302].