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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
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.
Urban Naturalist, No. 11 (2016)
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.
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Urban Naturalist
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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
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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
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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.
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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.
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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).
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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
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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
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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).
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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
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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).
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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
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R.B. Bricklin, E.M. Thomas, J.D. Lewis, and J.A. Clark
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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
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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.
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