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Foraging Birds during Migratory Stopovers in the New York Metropolitan Area: Associations with Native and Non-native Plants
Rachel B. Bricklin, Ellen M. Thomas, James D. Lewis, and J. Alan Clark

Urban Naturalist, No. 11 (2016): 1–16

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Urban Naturalist 1 R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 22001166 URBAN NATURALIST No. 11N:1o–. 1161 Foraging Birds during Migratory Stopovers in the New York Metropolitan Area: Associations with Native and Non-native Plants Rachel B. Bricklin1,*, Ellen M. Thomas2,3,4, James D. Lewis1, and J. Alan Clark1 Abstract - With urbanization, stopover habitats for migrating birds are increasingly located in disturbed areas where non-native plants are common. In this study, we describe the plant composition and associated food resources available for migrating birds at 2 stopover sites in the New York metropolitan area. Because birds have co-evolved with native plants, which can differ from non-native plants in both food resources and phenology, we predicted that birds would forage more often on native plants than non-native plants relative to plant availability. We also predicted that birds would forage disproportionally on plant species with more available food resources (i.e., fruits and invertebrates). We observed that birds foraged on both native and non-native plants in our study plots. Birds appeared to forage on non-native plants most frequently when these plants provided resources (such as fruit) that were not present on native plants in the study plots. Given that removal of non-native plant species is a common management practice in urban parks, our techniques might also be useful for other researchers who wish to quantify how non-native plant management practices affect foraging birds. Introduction The prevalence of non-native plants has increased dramatically over the past century, particularly in urban landscapes (Aronson et al. 2007, DeCandido 2004, Vitousek et al. 1996). Thus, in urban stopover sites, migrating birds likely rely to some extent on the ecological resources provided by non-native plants. These resources might differ in phenology, food type, and quality from those provided by native plants (Burghardt and Tallamy 2013, Shustack et al. 2009, Smith et al. 2013, Tallamy 2009). Further, the effect of non-native plants on food availability may differ between spring and fall migration. During spring migratory stopovers, birds tend to feed mostly on arthropods and stopover habitats often have high arthropod abundance (Blake and Hoppes 1986, Graber and Graber 1983, McGrath et al. 2009, R.J. Smith et al. 2007). Non-native plants support different arthropod communities than native plants (Burghardt et al. 2008). For example, Tallamy (2009) and Burghardt et al. (2010) observed that native plants supported a greater diversity of invertebrates than did non-native plants in suburban yards. In addition, differences in the timing of bud break or flowering between native and non-native plants can influence both arthropod availability and 1Department of Biological Sciences, Fordham University, Bronx, NY 10458. 2Mianus River Gorge, Inc., Bedford, NY 10506. 3Blind Brook High School, Rye Brook, NY 10573. 4Lafayette College, Easton, PA 18042. *Corresponding author - bricklin@fordham.edu. Manuscript Editor: Kristi MacDonald Urban Naturalist R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 2 species diversity (Crawley and Akhteruzzaman 1988, Hunter 1992, McGrath et al. 2009, Shustack et al. 2009, Strode 2009). During fall migratory stopovers, birds often feed on both arthropods and fruit (Parish 1997, S.B. Smith et al. 2007, Smith and McWilliams 2010). In addition to native plants supporting different arthropod communities than non-native plants, native fruit can be of higher quality (higher energy density, lipid content, and antioxidant content) than non-native fruit (Bolser et al. 2013, Drummond 2005, S.B. Smith et al. 2007, Smith and McWilliams 2010, Smith et al. 2013, White and Stiles 1992). However, some non-native fruit can nonetheless support mass gain in birds (e.g., Gleditsch and Carlo 2014). Studies of native versus non-native plant selection by foraging migrants often compare fruit-removal rates on plant species that are ecologically similar (e.g., Bolser et al. 2013, Smith et al. 2013). However, birds do not always have ecologically equivalent native or non-native species to choose from at stopover sites. Thus, quantifying the plant composition of stopover sites and then observing how birds forage on the plants in these habitats can be critical to understanding how birds utilize the plant resources that are available to them and to predicting how they might respond to common management practices such as non-native plant removal or native plant addition. In this study, we investigated the foraging behavior of birds during spring and fall migration at 2 stopover sites in a major metropolitan area to determine if foraging birds associate primarily with native rather than with non-native trees, shrubs, and vines. Because native bird species co-evolved with the resources and phenologies of native plants rather than non-native plants and because native plants often support higher invertebrate diversity (Burghardt et al. 2010, Tallamy 2009) and provide higher quality fruit than non-native plants, we predicted that birds would forage more on native than on non-native plants relative to their availability during both migration seasons. We also predicted that birds would forage disproportionally on plant species with more available food resources such as fruit. Methods Study sites We studied birds during migration at 2 contrasting stopover sites in the densely populated New York metropolitan area: Bronx Park (40°51'5"N, 73°52'27"W) and the Mianus River Gorge (Mianus, 41°11'15"N, 73°37'17"W). Bronx Park is a 229- ha New York City park that includes the properties of the Bronx Zoo and New York Botanical Garden in Bronx County, NY, USA (population density: 12,707 people/ km2; 2010 US Census). This site and its use by migrants are described in more detail in Seewagen and Slayton (2008) and Seewagen et al. (2011). Mianus is a privately managed 355-ha nature preserve located 50 km north of Bronx Park in Westchester County, NY, USA (847 people/km2; 2010 US Census) acquired for its old-growth Tsuga canadensis L. (Eastern Hemlock) forest and unique topography (Goodwin 1961). Both sites are bisected by rivers (the Bronx River and Mianus River, respectively) and contain both mature forest as well as shrub-dominated areas. The Bronx Urban Naturalist 3 R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 Park forest is dominated by Quercus rubra (Red Oak), Liquidambar styraciflua (American Sweetgum), and Prunus serotina (Black Cherry); the Mianus forest is dominated by Acer rubrum (Red Maple), Acer saccharum (Sugar Maple), and Fraxinus sp. (ash). Despite high human-population density throughout the New York metropolitan area, many species of migratory birds are known to utilize stopover sites in this region during spring and fall migration (Seewagen and Slayton 2008, Seewagen et al. 2011). We chose our particular sites because both sites contain similar structural habitats that are favorable for migratory bird stopovers, such as forested and shrubland areas (Bonter et al. 2009, Rodewald and Brittingham 2004), yet show differing levels of surrounding urbanization. Bronx Park is part of a habitat island in the midst of expansive development, while Mianus is part of a network of protected habitats. In addition to varying in surrounding population density, the sites vary in surrounding development as well. Bronx Park is adjacent to highways, cultural attractions, schools, and businesses, while Mianus is adjacent to lightly traveled roads, houses, and yards. Mianus, like much of Westchester County, has a large population of Odocoileus virginianus Zimmermann (White-tailed Deer) that has largely removed much of the native understory, and thus non-native shrubs are generally more prevalent than native shrubs (Weckel et al. 2006). Deer are not present at Bronx Park. Observations of foraging birds We observed birds at Bronx Park and Mianus during spring (9 April through 18 May) 2012 and fall (8 August through 25 October) 2011 and 2012. Though we conducted a pilot study during spring 2011, we were not able to use data from 2011 in our analysis. We alternated days between Bronx Park and Mianus because the same observers collected data at both sites. We conducted all surveys from sunrise until 4 hours after sunrise. We did not conduct fieldwork in the rain to avoid differences in bird behavior that might be due to such weather. At each site, observers recorded bird behaviors at 4 vegetation plots selected to represent the site as a whole. The boundary of each plot was flagged at 5-m intervals to designate the observation area. Plot size ranged from approximately 300 to 800 m2, and plots were a minimum distance of 100 m apart. We used the same plots in both seasons and observed each vegetation plot from the same location in each plot for 1 hour twice weekly during the study seasons. The first observation hour began at sunrise each day, and we rotated the observation order among plots so that a different plot was observed first each day. We selected vegetation plots that contained plant compositions representative of the site and concentrations of bird activity during a pilot study in spring 2011, but we also selected plots to be roughly equidistant from each other and with good visibility across the plots for observations. Though visibility at each study site varied during the spring depending on amount of leaf-out, visibility was similar among plots at the same site on the same day. We kept the total area observed as consistent as possible across plots while maximizing the observation area. We combined all plots at each site for analyses. The total plot area observed at Bronx Park was ~2100 m2, and the total plot area observed at Mianus was ~2780 m2. Urban Naturalist R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 4 During observation periods, observers remained in one location and recorded the number, species, and behaviors of all foraging birds as well as the plant species that these birds associated with while foraging. We defined an associated plant as a plant that a bird (1) obtained food from (either by consuming part of the plant or gleaning items off the surface of the plant) or (2) was in physical contact with while foraging. We considered the following behaviors as indicative of foraging (Hutto 1981): gleaning (picking food from a surface while stationary), sallying (flying out after airborne prey), hovering (picking food from a surface while in stationary flight), and jumping (jumping up, picking food from the underside of a surface). We sometimes observed individual birds foraging on multiple species of plants during the observation period. In those cases, we counted each plant association as 1 foraging observation. For example, a bird that foraged on 3 different species of trees counted as 1 foraging observation on each tree species. We focused on plant associations of migratory passerines (i.e., within the order Passeriformes and identified as migratory in The Birds of North America Online species accounts [Rodewald 2014]). Though it was often difficult to observe what birds were eating, we identified food items whenever possible. In the spring, we recorded the extent of budding and leaf-out in each plant in each plot during each observation period (Augspurger and Bartlett 2003, Strode 2009). In the fall, we recorded any plants with flowers, green fruit, or ripe fruit in each plot. Plant composition, plant availability, and over/under-utilized plant species We identified all trees, shrubs, and vines in each plot. We defined trees as woody plants with diameter at breast height (DBH) ≥ 7.5 cm and shrubs as woody plants with DBH < 7.5 cm (James and Shugart 1970) or as bushy woody plants with single or multiple stems between 0.5 and 5.0 m in height (Federal Geographic Data Committee 2008, United States Department of Agriculture 2014). Because some plant species included both trees and shrubs based on these definitions, we classified any plant species that included at least 1 individual in the tree category as a tree. We defined vines as either woody or herbaceous long-stemmed plants that climbed/ twined on any shrub or tree (United States Department of Agriculture 2014). We categorized each plant species as native or non-native using the New York Flora Atlas (New York Flora Atlas 2014) to determine if the plant was native to New York. Trees and shrubs include most of the foraging substrates known to be used by the birds we observed (Rodewald 2014). We distinguished vines growing on trees and shrubs because we often observed birds foraging on these plants and, although they appeared to be associated with birds foraging on trees or shrubs, they were often used differently (R.B. Bricklin, pers. observ.). To determine plant availability, we calculated a relative density value for native and non-native plants within each plant category (tree, shrub, or vine). Relative density was calculated as the number of plants of that species in that category per acre divided by the total number of plants in that category per acre. We then multiplied the total number of birds observed foraging on plants in that category by the relative density values of native and non-native plants, respectively, to obtain expected numbers of birds foraging on native and non-native plants based on plant availability. Urban Naturalist 5 R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 We considered plant species to be over-utilized if birds foraged on these species more often than expected based on plant availability, and we considered plant species to be under-utilized if birds foraged on these species less often than expected based on plant availability. To obtain the expected number of birds foraging on each plant species, we multiplied the total number of birds observed foraging on plants in that category by the relative density value of that plant species. For each over- or under-utilized plant species, we noted the leaf-out or budding status and any fruit on these plants at the time that birds foraged as well as the leaf-out or budding status and any fruit of other plants in that category at the time that birds foraged. Statistical testing We used Pearson’s chi-squared tests to determine if birds associated with native and non-native plants according to availability as measured by our relative density measures. We analyzed birds’ associations with trees, shrubs, and vines separately and analyzed data from each season separately because different plant and invertebrate resources are available in the spring and fall. We combined data for the 2 fall seasons because the same plant resources were available during both years. We also used Pearson’s chi-squared tests to determine if birds associated with each plant species according to availability as measured by our relative density measures. To designate plant species as over- or under-utilized by birds relative to plant availability, we identified plant species whose contribution to the overall test statistic was significant on its own at the degrees of freedom for the entire category. Because we used independent statistical tests for each category and season, we accepted significance at P < 0.01 rather than < 0.05 for all analyses to be more conservative in our rejection of the null hypothesis that birds associated with plants based on availability. Results Plant composition We identified 51 total plant species at the 2 study sites (Table 1). Of these plant species, 7 were present at both sites (4 in the native trees category, 2 in the native shrubs category, and 1 in the native vines category; Table 1). Overall, plant species richness was higher at Bronx Park (33 species) than at Mianus (25 species) (Table 1). The number of plant species m-2 was also higher at Bronx Park (0.016) than at Mianus (0.009). Twenty seven of the 33 plant species were native (81.8%) at Bronx Park while 19 of the 25 plant species were native (76.0%) at Mianus (Table 1). Based on plant relative density values, our observation plots at Bronx Park contained more native than non-native trees and vines in each of these groups (Table 1). Bronx Park plots did not include any non-native species of shrubs, though the site contained multiple non-native tree and vine species (Table 1). Observation plots at Mianus did not include any non-native tree and vine species, but did include more non-native than native shrub species based on relative density values (Table 1). Urban Naturalist R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 6 Table 1. Plant species, plant availability (expressed as a relative density value; RD%), and percent of foraging birds observed on each species at Bronx Park and the Mianus River Gorge (Mianus). To obtain plant RD%, we first calculated the relative density of each plant species in each plant category (see text for explanation of plant categories). We then summed these values to obtain an RD for each plant category at each site and then converted these values by dividing each RD by the sum of RD values in each plant category. * indicate sites and seasons during which plant species were over- or under-utilized relative to availability. Bronx Park Mianus % spring % fall % spring % fall Plant species RD% foraging birds foraging birds RD% foraging birds foraging birds Native trees Acer negundo L. (Ashleaf Maple) 12.2 6.4 5.1 Acer rubrum L. (Red Maple) 1.4 0.7 2.0 13.6 28.6 5.7 Acer saccharinum L. (Silver Maple) 1.4 Acer saccharum Marsh. (Sugar Maple) 25.0 42.9 20.8 Alnus incana (L.) (Gray Alder) 6.8 5.7 Aronia arbutifolia (L.) Pers. (Red Chokeberry) 2.3 Betula lenta L. (Sweet Birch) 2.7 0.7 2.5 Carpinus caroliniana Walter (American hornbeam) 2.3 15.1* Carya glabra (Mill.) Sweet (Pignut Hickory) 8.1 0.7 10.2 Carya ovate (Mill.) K. Koch (Shagbark Hickory) 2.3 Castanea pumila L. Mill. (Northern Catalpa) 1.4 2.1 1.5 Cornus florida L. (Flowering Dogwood) 1.4 0.7 6.1 Fraxinus americana L. (White Ash) 2.7 7.1 1.0 Fraxinus pennsylvanica Marsh. (Green Ash) 6.8 1.9 Hamamelis virginiana L. (American Witchhazel) 2.3 Juglans cinera L. (White Walnut) 1.4 Liquidambar styraciflua L. (Sweet Gum) 5.4 1.4 Platanus occidentalis L. (American Sycamore) 2.3 Prunus serotina Ehrh. (Black Cherry) 21.6 15.7 7.1 6.8 3.8 Quercus alba L. (White Oak) 2.7 13.6* 5.6 Quercus coccinea Münchh. (Scarlet Oak) 1.4 2.1 1.0 Quercus rubra L. (Red Oak) 5.4 10.0 9.6 2.3 Quercus velutina Lam. (Black Oak) 1.4 0.5 Ulmus rubra Muhl. (Slippery Elm) 2.7 6.4 14.7* 25.0 28.6 47.2 Viburnum lentago L. (Nannyberry) 2.3 Urban Naturalist 7 R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 Table 1, continued. Bronx Park Mianus % spring % fall % spring % fall Plant species RD% foraging birds foraging birds RD% foraging birds foraging birds Non-native trees Acer platanoides L. (Norway Maple) 1.4 Ailanthus altissima (Mill.) Swingle (Tree of Heaven) 8.1 2.9 4.1 Alnus glutinosa (L.) Gaertn. (European Black Alder) 13.5 21.4 20.3 Morus alba L. (White Mulberry) 4.1 7.9 8.6 Native shrubs Aralia spinosa L. (Devil's Walkingstick) 20.9 14.3 Betula lenta L. (Sweet Birch) 13.3 48.3* Cornus sericea L. (Redosier Dogwood) 4.7 57.1* 21.4 Ilex verticillata (L.) A. Gray (Common Winterberry) 1.1 6.9 Lindera benzoin (L.) Blume (Northern Spicebush) 2.3 8.5 Rhus glabra L. (Smooth Sumac) 18.6 14.3 21.4 Sassafras albidum (Nutt.) Nees (Sassafras) 25.6 14.3 Smilax glauca Walter (Cat Greenbrier) 7.0 14.3 Staphylea trifolia L. (American Bladdernut) 11.6 Viburnum prunifolium L. (Blackhaw) 2.3 15.4 10.3 Viburnum recognitum Fernald (Northern Arrow-wood) 7.0 28.6 14.3 Non-native shrubs Berberis thunbergii DC. (Japanese Barberry) 27.1 Elaeagnus angustifolia L. (Russian Olive) 1.6 Euonymus alatus (Thunb.) Siebold (Winged Burning Bush) 11.2 68.8* 27.6 Ligustrum vulgare L. (Wild Privet) 10.1 31.3 3.4 Lonicera tatarica L. (Tatarian Honeysuckle) 9.6 3.4 Viburnum sieboldii Miq. (Siebold’s Arrowwood) 2.1 Native vines Vitis labrusca L. (Fox grape) 57.1 100.0 20.0 Parthnocissus quinquefolia (L.) Planch. (Virginia Creeper) 20.0 2.8 Toxicodendron radicans (L.) (Poison Ivy) 40.0 100.0 2.8* 42.9 80.0* Non-native vines Ampelopsis brevipedunculata (Maxim.) Trautv. (Porcelainberry) 30.0 94.4* Celastrus orbiculatus Thunb. (Oriental Bittersweet) 10.0 Urban Naturalist R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 8 Spring foraging In spring 2012, we observed foraging behavior for 9 days at Bronx Park and 10 days at Mianus. Birds were observed feeding on insects, green fruit, and flowers at Bronx Park. Birds were observed feeding on insects and seeds at Mianus. At Bronx Park, we observed 27 species of birds foraging, and the bird species that foraged on the greatest diversity of plant species were Setophaga coronata L. (Yellow-rumped Warbler), Mniotilta varia L. (Black-and-white Warbler), and Setophaga caerulescens Gmelin (Black-throated Blue Warbler). The most commonly observed foraging bird species was S. coronata (31.9% of total foraging observations). Foraging birds associated with native and non-native trees as expected based on plant availability (trees: χ 2 [1, n = 140] = 1.86, P = 0.17; Fig. 1a). Only 2 birds (M. varia and S. caerulescens) were observed foraging on vines, and they both foraged on the same native species, Toxicodendron radicans L. (Poison Ivy). All but one plant species (Cornus sericea L. [Redosier Dogwood]) showed at least partial leaf-out at the time of foraging; however, this native shrub was actually over-utilized by birds (χ2 [8, n = 7] = 41.47, P < 0.001; Table 1) and had begun leaf-out during the time of some foraging observations. The only over-utilized tree species at Bronx Park during the spring was the native Quercus alba L. (White Oak; χ2 [19, n = 140] = 61.19, P < 0.001; Table 1), and, like other plants on which birds foraged, individuals of this species showed partial to full leaf-out at the time that birds foraged. Figure 1. a–f. Bird associations with native and non-native trees and shrubs at Bronx Park and Mianus River Gorge (Mianus) during the spring of 2012. The number of observed and expected foraging birds was based on plant relative density (RD) values (expressed as a percent). Urban Naturalist 9 R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 At Mianus, we observed 7 species of birds foraging in the spring, and the bird species that foraged on the greatest diversity of plant species were Dumetella carolinensis L. (Gray Catbird), Zonotrichia albicollis Gmelin (White-throated Sparrow), Geothlypis trichas L. (Common Yellowthroat), and Passerina cyanea L. (Indigo Bunting). The most commonly observed foraging bird species was D. carolinensis (39.1% of total foraging observations). Birds only foraged on non-native shrubs, though native shrubs were present in the study plots, and only native trees and vines were available (Fig. 1d–f). The only over-utilized plant species at Mianus during the spring was the non-native shrub Euonymus alatus (Thunb.) Siebold (Winged Burning Bush; χ2 [9, n = 16] = 47.49, P < 0.001; Table 1). Birds foraged on this shrub during every stage of leaf-out, included flowering. Similar to Bronx Park, most plants on which birds foraged at Mianus also showed partial leaf-out. Fall foraging In fall 2011, we observed foraging birds for 17 days at Bronx Park and 13 days at Mianus. In fall 2012, we observed foraging birds for 18 days at Bronx Park and 20 days at Mianus. Birds were observed feeding on insects and fruit at both sites, and birds were also observed feeding on seeds and flowers at Bro nx Park. At Bronx Park, we observed 28 species of birds foraging, and the bird species that foraged on the greatest diversity of plant species were D. carolinensis, Setophaga ruticilla L. (American Redstart), and Setophaga magnolia Wilson (Magnolia Warbler) (for information on plant composition, all foraging bird species, plant status, and food items at our study plots at Bronx Park, see Supplemental Table 1, available online at https://www.eaglehill.us/URNAonline/suppl-files/U119c-Bricklin- s1). The most commonly observed foraging bird species was D. carolinensis (29.5% of total foraging observations). Birds foraged on native and non-native trees as expected based on plant availability (χ2 [1, n = 197] = 3.56, P = 0.059; Fig. 2a). However, birds foraged on non-native vines more than native vines (χ2 [1, n = 36] = 44.46, P < 0.001; Fig. 2c). Most trees on which birds foraged did not have fruit. The only shrub species that had fruit available when birds foraged was the native Prunus serotina (Black Cherry). One native tree, Ulmus rubra (Slippery Elm), and 1 non-native vine species, Ampelopsis brevipedunculata (Porcelain Berry), were over-utilized in the fall (χ2 [19, n = 197] = 105.28, P < 0.001; and χ2 [3, n = 36] = 49.84, P < 0.001, respectively; Table 1), and 1 native vine species (T. radicans) was under-utilized (χ2 [3, n = 36] = 12.47, P = 0.0059; Table 1). The under-utilized T. radicans did not have any fruit available when birds foraged, while the overutilized A. brevipedunculata consistently had green or ripe fruit available at the time of foraging. However, the over-utilized U. rubra did not have fruit available. At Mianus in the fall, we observed 19 species of birds foraging, and the bird species that foraged on the greatest diversity of plant species were D. carolinensis, Regulus calendula L. (Ruby-crowned Kinglet), and S. coronata (for information on plant composition, all foraging bird species, plant status, and food items at our study plots at Mianus River Gorge, see Supplemental Table 2, available online at https://www.eaglehill.us/URNAonline/suppl-files/U119c-Bricklin-s1). The most commonly observed foraging bird species was D. carolinensis (23.3% of total Urban Naturalist R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 10 foraging observations). Foraging birds associated with native shrubs more than non-native shrubs (χ2 [1, n = 29] = 7.87, P = 0.0050; Fig. 2d). None of the native shrub species contained fruit at the time of foraging, although 2 of the 3 non-native shrub species did. The birds foraging on native shrubs were observed eating insects, but the birds foraging on non-native shrubs were observed eating fruit. As in the spring, birds foraged on native trees and vines, although there were no non-native tree or vine species available (Table 1). The native tree Carpinus caroliniana (American Hornbeam) and the native shrub Betula lenta (Sweet Birch) were over-utilized at Mianus (χ2 [12, n = 53] = 38.34, P < 0.001; and χ2 [9, n = 29] = 26.68, P = 0.0016; respectively, Table 1), although neither of these species had fruit available at the time of foraging. In contrast to Bronx Park, T. radicans was over-utilized at Mianus (χ2 [1, n = 25] = 8.05, P = 0.0046; Table 1), and this species did have ripe fruit available at the time of foraging. One of the over-utilized native tree species at Bronx Park, U. rubra, was also the tree species most commonly foraged on at Mianus during the fall (Table 1), though this species was not considered over-utilized by our definition at Mianus due to its high relative density (25.0) at this site. Bird species observed foraging on U. rubra trees varied between the 2 sites, with only 1 bird species observed at both sites (D. carolinensis [Gray Catbird]) out of a total of 10 bird species recorded. These bird species included omnivorous (e.g., Turdus migratorius [American Robin]), primarily frugivorous or granivorous (e.g., Quiscalus quiscula, L. [Common Grackle]), and primarily insectivorous (e.g., Cardellina Canadensis [Canada Warbler]) species (Rodewald 2014). Figure 2. a–f. Bird associations with native and non-native plants at Bronx Park and Mianus River Gorge (Mianus) during the fall of 2011 and 2012. The number of observed and expected foraging birds was based on plant relative density (RD) values (expressed as a percent). Urban Naturalist 11 R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 Discussion Overall, we observed that birds foraged on both native and non-native plants in our study plots. Non-native plants often dominate urban habitats, yet vegetation plots at our study sites were composed of more native than non-native plants overall. At Bronx Park, plots contained more native than non-native trees and vines, and plots contained only native shrubs. At Mianus, plots contained only native trees and vines, but more non-native shrubs than native shrubs. Although our observation plots represent a sub-set of each site and plant composition likely varies throughout each site, shrub composition of Mianus might well be representative of the site as a whole, as wide-spread browsing by O. virginianus on native shrubs has dramatically affected the plant community (Weckel et al. 2006). Many of the observed passerine species foraged on multiple species of plants in our study plots, and, contrary to our expectations, we did not find that birds foraged on native plants more than non-native plants relative to plant availability overall. However, 6 of the 8 over-utilized plant species were native species. Birds foraged more on non-native than native vines at Bronx Park in the fall and also foraged more on native than non-native shrubs at Mianus in the fall. Birds foraged heavily on native plants in our study plots, yet they also foraged on the conspicuous resources provided by non-native plants. Birds appeared to forage on non-native plants most frequently when these plants provided resources not present on native plants in the study plots. For example, birds only foraged on non-native shrubs at Mianus in the spring during our observation periods, and these plants always showed more leaf-out (see Supplemental Table 2, available online at https://www.eaglehill.us/URNAonline/suppl-files/U119c-Bricklin-s1), which can attract both insects and birds (Crawley and Akhteruzzaman 1988, Hunter 1992, McGrath et al. 2009, Strode 2009), than native shrubs in the study plots. We also found that in the fall, the only over-utilized non-native plant species, A. brevipedunculata, always had fruit available at the time of foraging, while most other plants in the study plots did not. The non-native A. brevipedunculata has uniquely colorful fruit that can be attractive to frugivorous birds (Witty et al. 2010), and this species is common in parks in New York City (DeCandido 2004, Stalter et al. 2009, Yost et al. 1991), where it was likely first introduced as an ornamental plant (Yost et al. 1991). Spring leaf-out can occur earlier in non-native than native plants (Shustack et al. 2009), which might lead to birds foraging more often on non-native than native plants, as we found with shrubs at Mianus. A higher abundance of arthropods on plants with greater leaf out might help explain some of our results. Smith et al. (2013) observed that the abundance of midges, a common food source for migrants, was initially highest on a non-native shrub species that was the first to show leafout at spring stopover sites. Some fall studies found that passerines foraged more on native than non-native fruit during migratory stopovers (Baird 1980, Bolser et al. 2013, Smith et al. 2013, White and Stiles 1992), while other studies found that passerines foraged equally on both native and non-native fruit (Drummond 2005, Suthers et al. 2000). Though fall birds might select fruit based on such traits as ease Urban Naturalist R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 12 of access and colorfulness (Whelan and Willson 1994), native fruit can be higher quality than non-native fruit (Bolser et al. 2013, Drummond 2005, S.B. Smith et al. 2007, Smith and McWilliams 2010, Smith et al. 2013, White and Stiles 1992). If native fruit is generally of higher quality than non-native fruit, then fruit from non-native plants, such as A. brevipedunculata, might not be as beneficial to birds as native fruit and, in the most extreme cases, might cause a site to become an “ecological trap” for birds if birds are attracted to this site yet cannot obtain the nutrition necessary for effective migratory refueling (Rodewald 2012). However, while the nutritional quality of these fruits relative to native fruits is unknown, A. brevipedunculata does show antioxidant activity (Wu et al. 2004), though it also has a high lignin content (Witty et al. 2010) and thus might not be as nutrient-rich as other fruits. In addition, previous studies of migrants at Bronx Park found that birds can replenish both fat and lean body mass at this site (Seewagen and Guglielmo 2011, Seewagen and Slayton 2008, Seewagen et al. 2011). Thus, existing food resources at this site presumably can meet nutritional needs despite the prominence of such species as A. brevipedunculata. Besides A. brevipedunculata, other over-utilized plant species did not show clear patterns of higher leaf-out or more fruit present relative to other plant species. Ecological explanations for over-utilization of these species include that these plant species provide certain resources favored by birds. Methodological explanations for over-utilization include that low relative importance values for some of these plant species combined with small numbers of total birds observed foraging at that site during that season might have led to their characterization as over-utilized. In addition, birds might have been foraging more on these particular species merely by chance during observation periods. The over-utilization of U. rubra at Bronx Park and the frequent foraging on this species by birds at Mianus as well during the fall might be explained by this tree providing certain resources favored by birds. Strode (2009) found that Setophaga coronate L. (Yellow-rumped Warblers) over-utilized U. rubra relative to plant availability during the fall, but under-utilized this tree relative to plant availability in the spring, while Wood et al. (2012) found that multiple species of birds overutilized this tree during the spring. We observed S. coronate on U. rubra during both the spring and fall. In this study, we were constrained by small sample sizes and only 2 field sites, each of which differed in plant species composition and the density of the surrounding human population. Though observing 2 contrasting urban stopover sites for this study limited our ability to generalize our results, the longer observation times at these sites allowed us to build a broader understanding of how birds utilize available plant species during stopovers in highly variable urban landscapes. We were also only able to quantify the plants with which foraging birds associated rather than where birds obtained food and the quality of that food. Nonetheless, our results suggest that non-native plants influence foraging behavior of birds during migratory stopovers. We found that native plant species can be common and frequently foraged on at migratory stopover sites in urban areas. However, non-native plants Urban Naturalist 13 R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark 2016 No. 11 might likely be foraged on by birds if these plants show differences in phenology (such as earlier leaf-out) or resources (such as an abundance of conspicuous fruit) than native plants. Removal of non-native plant species is a common management practice in urban parks and other disturbed habitats (Reid et al. 2009, Stalter et al. 2009). Though native plant species often provide more insects (if at similar stages of leaf-out) and/or higher quality fruit than ecologically equivalent non-native plant species, ecologically equivalent native plant species are not always available. In such situations, birds might concentrate some of their foraging on non-native plants and be reliant on the resources that those plants provide. We support the recommendation of Reichard et al. (2001) that managers first plant native equivalents and then later remove non-native plants during seasons in which they are not heavily utilized by birds. Managers of sites where non-native plant species are common might also benefit by comparing arthropod diversity on these plants and/or nutritional quality of non-native fruits to ecologically equivalent native plants (such as native grape species in the case of A. brevipedunculata). Then, if native plants provide higherquality resources, management efforts can be concentrated on the replacement of the most prominent non-native species (as determined by observations of foraging migrants) with ecologically equivalent native species, and also strategies to attract birds to these native species. However, we urge managers to continue to observe birds, as we have done in this study, to determine the frequency at which migrants are actually foraging on the plant species present in a given habitat. Acknowledgments We are grateful to the staff of the Mianus River Gorge, particularly M. Weckel, R. Christie, and C. Nagy, for technical and field assistance throughout this project and to the Wildlife Conservation Society and the staff of the Bronx Zoo for allowing us access to Bronx Park. We thank T. Daniels, E. Hekkala, C. Seewagen, and B. Walker for feedback on this manuscript. We are grateful to R. Aracil, H. Birdsall, J. Burke, B. Cieri, A. Domeyko, D. Epp Schmidt, M. Oberkircher, T. Olson, K. Reinhardt, R. Sleith, and S. van Ryzin for assisting with field research. We also thank M. Sugantino, the Blind Brook High School Science Research Program, and the Mianus River Gorge Wildlife Technician Program for enabling E.M. Thomas to join our research team. Funding for this project was provided by the Mianus River Gorge Research Assistantship Program, the Clare Boothe Luce Program, the Graduate School of Arts and Sciences at Fordham University, and the Rusticus Garden Club. Literature Cited Aronson, M.F.J., S.N. Handel, and S.E. Clemants. 2007. 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