Seasonal responses of avian communities to invasive bush ...

Biol Invasions (2010) 12:2459–2470
DOI 10.1007/s10530-009-9655-5

ORIGINAL PAPER

Seasonal responses of avian communities to invasive bush
honeysuckles (Lonicera spp.)

Courtney E. McCusker • Michael P. Ward •
Jeffrey D. Brawn

Received: 28 June 2009 / Accepted: 10 November 2009 / Published online: 25 November 2009
Ó Springer Science+Business Media B.V. 2009

Abstract Invasive bush honeysuckles, Lonicera Keywords Avian communities Á
spp., are widely viewed as undesirable; however, the Invasive plants Á Lonicera Á Honeysuckle
effects of Lonicera spp. on native fauna are largely
unknown. We investigated how breeding and over- Introduction
wintering bird communities respond to the presence of
Lonicera spp. by comparing communities in forested Invasive species are a growing global problem for the
areas with Lonicera spp. to those with a native shrub conservation of native biodiversity and ecological
understory. The dense understory created by Lonicera integrity (Pimentel et al. 2000). The response of
spp. was associated with a change in the breeding bird native species and communities to invasive species
community. We found large increases in the densities can be positive, negative, or both (e.g. increased
of understory bird species (e.g. northern cardinals) and species richness but decreased fecundity; Sax et al.
decreases in select canopy species (e.g. eastern wood- 2005). The negative impacts of invasives on native
pewees) in Lonicera spp. sites. In winter, we observed biota are well known; however, there is potential for
greater densities of frugivorous birds (e.g. American invasions to have positive effects on some native
robins) likely due to the fruits that remain on Lonicera species through the provision of limited food
spp.; however, there was no difference in the com- resources or modification of habitat (Rodriguez
munity composition between sites with and without 2006). Understanding the full spectrum of ecological
Lonicera spp. Given the widespread distribution of effects produced by invasives is therefore needed to
Lonicera spp., this invasive species may facilitate the inform managers about the costs and benefits of
population increase and range expansion of selected eradication programs.
bird species. Many bird species appear to utilize
Lonicera spp. for nesting and foraging; therefore, its Lonicera spp. were introduced to North America
removal should be accompanied by restoring native from Eurasia during the mid-1700 and 1800s as
shrubs that provide needed resources. ornamental shrubs and began spreading across the
eastern United States and into Canada in the mid-
C. E. McCusker (&) Á M. P. Ward Á J. D. Brawn 1900s (Pringle 1973; Luken and Thieret 1996).
University of Illinois at Urbana-Champaign, Champaign, Several species of Lonicera were introduced to the
IL, USA United States; all of the invasive bush honeysuckles
e-mail: [email protected] are upright, multi-stemmed, deciduous shrubs that
develop bright red fruits in the late summer and fall
that persist into winter (Dirr 1975; Luken and Thieret

123

2460 C. E. McCusker et al.

1996). Negative ecological effects of Lonicera spp. American robins and cedar waxwings (Bombycilla
on native plant communities are well documented cedrorum), are the major consumers and dispersers of
and include diminished native plant richness, abun- Lonicera spp. fruits (Bartuszevige and Gorchov
dance, and fitness; these effects are mainly due to the 2006) and may track these fruits during winter
dense understory structure created by Lonicera spp. months when resources are limited. If birds are
that ultimately results in a Lonicera spp. monoculture tracking these resources, then their distributions and
(Gould and Gorchov 2000; Gorchov and Trisel 2003; abundances may differ between sites with and
Miller and Gorchov 2004). Due to its negative without Lonicera spp. The presence of Lonicera
effects, management strategies often call for eradi- spp. fruits may result in greater local abundances of
cation of Lonicera spp. While removal may be frugivorous species in the winter with resultant
beneficial to native plant communities, very few changes in overall community structure, i.e. the
studies have addressed the impact of Lonicera spp. on density and distribution of birds in an area.
constituent animal communities.
Studies of bird behavior and habitat preferences are
The impact of Lonicera spp. on avian communities often limited to the breeding season; however, in the
is unclear. Several species of birds readily nest in case of Lonicera spp. they can impact birds both in the
Lonicera spp., including wood thrushes (Hylocichla summer and winter via habitat modification and the
mustelina), gray catbirds (Dumetella carolinensis), provision of food resources. To address the impacts of
American robins (Turdus migratorius) and northern Lonicera spp. on avian communities we conducted a
cardinals (Cardinalis cardinalis). Breeding pairs of the multi-seasonal study comparing communities of birds
latter two species experience greater rates of nest loss within forested areas invaded by Lonicera spp. and
when nesting in Lonicera spp. versus native plants forested areas with native shrubs. We specifically
(Whelan and Dilger 1992; Schmidt and Whelan 1999; compared densities of individual bird species, habitat
Borgmann and Rodewald 2004). These lower rates of and diet guilds, species richness, and species compo-
reproductive success, however, were only seen early in sition between forests with and without Lonicera spp.
the season for northern cardinals in Ohio; late in the We investigated these impacts in east central Illinois,
breeding season reproductive rates were higher than where Lonicera spp. are abundant (Edgin 2007).
nests in the native plants, suggesting a possible
ephemeral trap (Rodewald et al. 2009). Lonicera spp. Methods
earlier leaf phenology, leading to earlier nest initiation,
and dense branch architecture, leading to increased Study sites
predator movement, may allow increased predation,
but can also provide nesting substrate that results in We characterized vegetation structure and avian
increasing density of breeding birds that use shrubs as communities at ten rural forests in east central Illinois
nesting substrate in invaded areas (Whelan and Dilger located in Piatt, Champaign and Vermilion counties;
1992; Schmidt and Whelan 1999; Rodewald et al. five sites contained Lonicera spp. (Kickapoo State
2009). Northern cardinals were positively associated Park, property of William Taylor, Homer Lake Forest
with dense understory vegetation (primarily due to the Preserve and University of Illinois’s Philips Tract and
presence of Lonicera spp.) during the breeding season Nanney Woods) and five contained a native shrub/
in Ohio (Leston and Rodewald 2006). Other species, sapling understory (Middle Fork Woods Nature
such as the American robin or gray catbirds, may also Preserve and the University of Illinois’s Allerton
increase in abundance in areas with Lonicera spp. due Park, Rutan Woods and two sites at the Vermilion
to the dense vegetation structure and, therefore, the River Observatory; hereafter referred to as native
increased number of nesting sites. sites; Fig. 1). One site (Homer Lake) had active
eradication of Lonicera spp.; however, the eradica-
Lonicera spp. has the potential not only to affect tion areas were not within our study areas and had no
the breeding bird community, but also the overwin- impact on our surveys. Sites were located in forested
tering bird community. Lonicera spp. fruits persist areas, however the surrounding landscape varied with
into winter and are eaten by overwintering birds either more forest, agriculture (corn or soybeans) or
(Ingold and Craycraft 1983; White and Stiles 1992;
Bartuszevige and Gorchov 2006). Frugivores, such as

123

Seasonal responses of avian communities 2461

Fig. 1 Locations of the ten sites in east central Illinois. Light number of points within each site differed according
gray circles indicate sites with Lonicera spp. Black triangles to area sampled and ranged from two to six, summing
indicate native sites to 20 points in Lonicera spp. sites and 18 in native
sites. Census points were[200 m apart, and each one
grassland. The forested areas sampled and forest tract was visited twice each summer and five times each
sizes (i.e. forest around the sampled sites) were winter. Observers sampled at each point for 5 min and
similar between the two groups of sites (sampled recorded the estimated distance to each bird encoun-
area: t = -0.523, P = 0.617; tract size: t = 0.007, tered to the nearest five meters. All counts were
P = 0.994; df = 8). conducted between sunrise and 1000 hours in summer
and between 0800 and 1300 hours in winter.
We chose the native sites specifically to contain a
native shrub/sapling layer; however, there were low Sampling of avian habitat
densities of non-native shrubs [multi-flora rose (Rosa
multiflora), European privet (Ligustrum vulgare), and Surveys of vegetation structure and composition were
autumn olive (Elaeagnus umbellata)] present in these based on the BBIRD field protocol and were
sites as well as in Lonicera spp. sites. In addition, conducted during the summer of 2006 (Martin et al.
three of the native sites contained small numbers of 1997). At each point where we conducted avian
Lonicera spp. shrubs. Collectively, the non-native surveys, four 5 m 9 5 m plots were established for
shrubs contributed to \1% of the total shrub cover in vegetation sampling. Each plot was a randomly
native sites. There were many shrub and sapling chosen distance (up to 50 m) and direction from the
species within each site (see McCusker 2008 for a survey point with the restriction that one plot was
complete list), however very few produce fruits that placed in each surrounding quadrant (e.g. 0°–90°).
remain available during the winter. Other than
Lonicera spp., the invasives (multi-flora rose, Euro- To estimate density of woody vegetation, all
pean privet and autumn olive) can retain fruit while woody plants were counted and identified to species
only three of the native species in the sites will retain or genus within each plot. We classified woody plants
their fruits over the winter [blackhaw (Viburnum with a diameter at breast height (dbh) of 7 cm or
prunafolium), flowering dogwood (Cornus florida), greater as trees (tree density). Woody plants with
and coralberry (Symphoricarpos orbiculatus)]. Of dbh \ 7 cm were classified as shrub/saplings and
these native shrubs only coralberry was observed considered part of the understory. We counted and
with fruits during the winter months and all three of identified all individual shrub/sapling stems at 10 cm
the invasive shrubs retained fruits into the winter, above the ground (shrub density). We only counted
although autumn olive was depleted by the beginning Lonicera spp. that were at least 1 m tall as smaller
of December (C. McCusker pers. obs.). plants are not reproductive and will not produce fruit
(Deering and Vankat 1999). Shrub species richness
Sampling of the avian community was estimated as the average number of shrub/sapling
species per quadrat. Percent understory cover of
We surveyed bird communities in the summers (May– Lonicera spp. and total shrub layer were visually
June) of 2006 and 2007 and winters (December- estimated to the nearest 10% within the plot.
February) of 2006–2007 and 2007–2008 using unlim-
ited radius point counts (Ralph et al. 1995). The We used a spherical crown densiometer to esti-
mate canopy closure from the center of the plot in
each of the four cardinal directions and derived an
average canopy closure of the four measurements
(Lemmon 1956). Canopy height varied depending on
the age of the site, however both treatments contained
young and old stands of trees. To estimate overall
ground cover, we placed a 1 m 9 1 m quadrant
randomly within each sampling quadrant and esti-
mated percent cover of herbs (all plants \1 m tall),
bare ground, and litter to the nearest 10%.

123

2462 C. E. McCusker et al.

Analysis of avian habitat vegetation (P. atricapillus) chickadees into ‘Paridae’ for density
estimation, and we considered them an individual
We used principal component analysis (PCA) to group. Since DISTANCE requires a minimum num-
reduce the dimensionality of vegetation data. Vari- ber of 40 detections to obtain reasonable estimates of
ables used in the PCA included stem density and density, we could only obtain estimates for relatively
percent cover of Lonicera spp. and shrubs, canopy common species. Guild assignations were based on
closure, tree density, shrub species richness, and information in The Birds of North America (Poole
percent cover of herbs, bare ground and litter. We 2005). Habitat guilds within breeding birds included
based the retention of components on the Kaiser- canopy, midstory, and understory species and were
Guttman criterion of eigenvalues [1 and scree plots based on where species forage and nest. Winter guilds
(McGarigal et al. 2000). Factor scores for each site based on diet included non-frugivorous (species that
from the retained principle components were used as never consume fruits), facultative frugivorous (spe-
predictor variables to explain avian densities. cies that will eat fruits if they were present; \50% of
diet), and frugivorous (fruit comprises [50% of diet).
Modeling avian survey data
Once we generated density estimates, we compared
We used Program DISTANCE 5.0 (Thomas et al. the individual species and guild estimates between
2006) to estimate densities of birds (birds per hectare) Lonicera spp. sites and native sites with repeated-
within each site. Point count data were modeled with measures ANOVA. In addition, we calculated effect
DISTANCE to account for heterogeneity in detect- sizes using Cohen’s d test (Cohen 1988; Thalheimer
ability with distance from the observer. Due to sample and Cook 2002). Effect size estimates were interpreted
size requirements, we could not derive individual based on Cohen’s (1988) classification: 0.2 are small,
detection functions and density estimates for each 0.5 are medium and 0.8 are large effects. To further
site; therefore, we pooled data across sites to estimate investigate the role of Lonicera spp. on the avian
detection functions. DISTANCE computations are community, we used robust linear regression to assess
robust to pooling of heterogeneous data; however, to associations between density estimates of the guilds
account for this heterogeneity, we included covariates (summer and winter) and the factor scores from the
that may play a role in the observer’s ability to detect a habitat ordination. To accommodate year to year
bird (Buckland et al. 2001, 2004). We included year, variation, we analyzed each year separately. Robust
percent total shrub cover per site (‘shrub’) and the regressions were used to minimize effects of outliers
presence/absence of Lonicera spp. (‘Lonicera’) as with small sample size (Gotelli and Ellison 2004).
covariates that may affect detection probabilities.
Each model contained one of the following covariate To assess variation in avian community composi-
combinations: none, Lonicera, shrub, year, Loni- tion, we used density estimates (averaged over the
cera ? shrub, shrub ? year, Lonicera ? year or Lo- two sampling years) to ordinate the sites based on
nicera ? shrub ? year. As shrub density increases, bird species composition and density in a PCA.
an observer’s ability to detect a bird may decrease, Discriminant function analysis comparing the Loni-
especially visually. In addition, year was included as a cera spp. and native sites was not feasible owing to a
covariate due to potential changes in the author’s low sample size. Finally, avian species richness,
(CM) ability to detect birds over the two years. We calculated as the average number of species detected
used Akaike’s Information Criterion (AIC; Burnham per point, was compared between the two types of
and Anderson 2002) to select among the candidate sites using univariate t-tests.
models for estimating density of individual bird
species or guilds. Results

Density estimates were derived in DISTANCE for Ordination of vegetation
individual species, habitat guilds (summer only) and
diet guilds (winter only). Due to identification issues, Ordination using PCA resulted in the retention of the
we grouped tufted titmice (Baeolophus bicolor) and first three components which accounted for 86.0% of
Carolina (Poecile carolinensis) and black-capped the variance in the data across all ten sites. The first

123

Seasonal responses of avian communities 2463

factor (accounting for 51% of sample variance) was Fig. 2 Plot of the first and second factor scores of the habitat
associated with cover of Lonicera spp., total shrub principal component analysis
and bare ground and contrasted these vegetation
attributes with the amount of litter cover (Table 1). observed 68 species and 2076 individuals. We were
Variation along the second principle component was able to estimate abundances of seventeen species
affiliated with canopy cover, shrub species richness (including the species pooled into Paridae) and three
and herb cover (22.9%). The third factor accounted habitat-use guilds (Table 2). Estimated densities of
for approximately 12% of the sample variance and four species [American robin, gray catbird, northern
was associated with tree density. cardinal and blue jay (Cyanocitta cristata)] were
markedly different between Lonicera spp. and native
Ordination of the sites based on vegetation structure sites; all were more common in the Lonicera spp.
indicated that total shrub and Lonicera spp. density sites. In contrast, the eastern wood-pewee (Contopus
differentiated sites with and without Lonicera spp. virens) and the Parids were about half as common in
Overall, Lonicera spp. sites have a denser understory Lonicera spp. sites. Birds of the mid- and understory
(Fig. 2). Mean estimates of Lonicera spp. cover guilds were more common in Lonicera spp. areas, but
ðx"Lonicera ¼ 48:8 Æ 24:2%; x"native ¼ 0:0%Þ and total abundances of canopy birds were similar between the
shrub cover ðx"Lonicera ¼ 62:6 Æ 12:8%; x"native ¼ two types of site. Effect size estimates indicate that
40:5Æ 15:7%Þ revealed large differences in understory many additional species may be affected by the
density between the types of sites. While bare ground presence of Lonicera spp. The effect size analysis
and litter cover were also included in this first factor suggest that the presence of Lonicera spp. has an
score, percent of bare ground was relatively low additional positive effect on densities of Carolina
between site types ðx"Lonicera ¼ 16:7 Æ 6:9%; x"native ¼ wrens (Thryothorus ludovicianus), common yellow-
5:8 Æ 5:5%Þ and percent litter cover was relatively throats (Geothlypis trichas) and wood thrushes, and a
high between site types ðx"Lonicera ¼ 70:9 Æ 14:3%; negative effect on eastern towhees (Pipilo erythr-
x"native ¼ 91:5 Æ 7:4%Þ. ophthalmus) and red-bellied woodpeckers (Melaner-
pes carolinus).
Breeding bird communities and Lonicera spp.
Variation in the habitat, derived from the habitat
Over the two summers combined, we surveyed our 38 PCA scores, explained about half of the variation in
points four times for a total of 80 surveys in Lonicera understory bird density in 2006 (R2 = 0.47) and 2007
spp. sites and 72 surveys in native sites. In total, we (R2 = 0.57); in both years the dominant trend was
greater densities of understory birds as shrub density,
Table 1 Component loadings from the habitat principal and therefore Lonicera spp., increased. Densities of
component analysis birds associated with the midstory were not strongly
associated with habitat variation in either year (2006:
Habitat variable Component loading R2 = 0.37 and 2007: R2 = 0.20). In 2006, about half

123 123

Lonicera spp. stems/hectare 0.97 -0.06 -0.12
% Lonicera spp. cover 0.94 -0.21 -0.05
% Bare ground 0.87
% Total shrub cover 0.86 0.06 0.31
% Litter -0.84 0.20 0.01
Total shrub stems/hectare 0.79 -0.22 -0.04
Shrub species richness -0.53 0.50 -0.21
% Herb cover -0.33 0.76 0.19
Canopy closure -0.12 0.87 0.08
Trees/hectare 0.24 -0.72 0.47
0.21 0.87

Habitat variables with component loadings [0.6 were used to
interpret the location of sites in ordination space

123 2464

Table 2 Mean density of birds (birds/hectare ± 1 SE) in Lonicera spp. and native sites in the summers of 2006 and 2007 and the effect of site type and year on summer bird
densities

Species or guild 2006 2007 Site Year Site 9 Year Effect
P SS F
Mean in Lonicera Mean in native Mean in Lonicera Mean in native SS F size
sites sites sites sites P SS F P

American robin 2.63 ± 0.65 0.75 ± 0.29 2.48 ± 1.49 0.38 ± 0.17 19.84 13.11 0.01 0.34 0.78 0.40 0.06 0.14 0.72 2.56
0.10 ± 0.07 1.83 ± 0.45 1.10 ± 0.34 5.92 9.31 0.02 2.02 2.04 0.19 0.67 0.68 0.44 2.16
Blue jay 1.56 ± 0.51 3.23 ± 0.65 3.05 ± 0.84 1.58 ± 0.31 0.48 0.39 0.55 1.25 0.72 0.42 6.67 3.86 0.09 0.44

Brown-headed 2.39 ± 0.32 0.15 ± 0.09 0.41 ± 0.11 0.15 ± 0.07
cowbird 0.26 ± 0.12 0.23 ± 0.11 0.20 ± 0.09

Carolina wren 0.30 ± 0.10 0.81 ± 0.22 0.43 ± 0.11 0.82 ± 0.17 0.21 3.00 0.12 0.01 0.65 0.44 0.02 0.76 0.41 1.23
1.73 ± 0.48 0.89 ± 0.21 1.29 ± 0.27 0.09 2.11 0.18 0.13 7.61 0.03 0.05 2.76 0.14 1.03
Common 0.48 ± 0.08 0.40 ± 0.28 4.00 ± 1.10 0.88 ± 0.60
yellowthroat 0.47 ± 0.14 0.33 ± 0.14 0.48 ± 0.12

Eastern wood-pewee 0.23 ± 0.09 0.63 ± 0.30 1.94 ± 0.59 0.86 ± 0.42 1.16 5.04 0.06 0.06 0.44 0.53 0.04 0.32 0.59 1.59
2.23 ± 0.44 2.53 ± 0.44 2.98 ± 0.38 2.22 2.38 0.16 0.16 0.27 0.62 0.34 0.59 0.46 1.09
Eastern towhee 0.80 ± 0.26 1.49 ± 0.35 4.15 ± 0.48 2.97 ± 0.55 47.68 13.32 0.01 1.27 0.40 0.55 0.00 0.00 0.98 2.58
0.22 ± 0.06 0.29 ± 0.08 0.58 ± 0.09 0.04 0.47 0.52 0.01 0.15 0.71 0.01 0.22 0.65 0.48
Gray catbird 3.47 ± 0.82
0.56 ± 0.26 0.79 ± 0.19 1.56 ± 0.50
Great-crested 0.43 ± 0.15 0.35 ± 0.10 0.19 ± 0.09 0.38 ± 0.15
flycatcher
0.23 ± 0.19 0.88 ± 0.30 0.49 ± 0.21
House wren 1.02 ± 0.36 4.04 ± 1.25 2.14 ± 0.69 3.50 ± 0.72 2.66 0.76 0.41 1.66 7.88 0.02 0.60 2.84 0.13 0.62
6.82 ± 1.62 4.91 ± 0.71 8.20 ± 1.51 0.00 0.00 0.95 0.36 0.32 0.59 1.15 1.00 0.35 0.04
Indigo bunting 2.74 ± 0.41 1.44 ± 0.66 3.75 ± 0.78 3.29 ± 0.85 6.46 6.43 0.04 11.66 13.05 0.01 0.01 0.01 0.92 1.79
9.53 ± 1.21 17.92 ± 1.75 12.47 ± 1.54 0.09 1.55 0.25 0.22 4.47 0.07 0.12 2.40 0.16 0.88
Northern cardinal 2.58 ± 0.35

Red-bellied 0.24 ± 0.07
woodpecker

Red-eyed vireo 0.13 ± 0.10 1.79 1.13 0.32 3.44 19.68 0.00 0.15 0.85 0.39 0.75
0.01 0.10 0.76 0.07 1.18 0.31 0.11 1.94 0.20 0.22
White-breasted 0.45 ± 0.14
nuthatch

Wood thrush 0.75 ± 0.23 1.01 3.01 0.12 0.18 0.67 0.44 0.02 0.08 0.79 1.23
17.79 3.95 0.08 0.00 0.00 1.00 1.44 0.40 0.55 1.40
Paridae 1.61 ± 0.84 31.85 1.03 0.34 1.86 0.28 0.61 2.98 0.44 0.52 0.72
20.54 6.22 0.04 0.40 0.07 0.80 12.28 2.14 0.18 1.76
Canopy 5.07 ± 1.46 128.27 3.81 0.09 55.41 7.52 0.03 0.74 0.10 0.76 1.38

Midstory 5.03 ± 1.74 C. E. McCusker et al.

Understory 14.21 ± 1.33

Results are from a repeated measures ANOVA based on the presence and absence of Lonicera spp. df = 1,8 for all tests. Effect size was calculated with Cohen’s d test

Seasonal responses of avian communities 2465

of the variation in canopy bird density was explained The second component explained 19.6% of the
by habitat variation (R2 = 0.45) and in 2007 about variance and contrasted the densities of eastern
60% of the variation in canopy birds was explained towhees, great-crested flycatchers (Myiarchus crin-
(R2 = 0.64). Canopy bird densities decreased as total itus) and indigo buntings (Passerina cyanea) with red-
shrub and Lonicera spp. density increased. eyed vireos (Vireo olivaceus) and Carolina wrens. The
third factor score was associated with densities of
Ordination of the breeding bird communities using wood thrushes, brown-headed cowbirds (Molothrus
estimated densities of seventeen species revealed ater) and house wrens (Troglodytes aedon; 18.3%).
strong apparent differences between Lonicera spp. Avian species richness was nearly identical in
and native sites (Fig. 3a). The first three component Lonicera spp. sites and native sites (2006:
scores explained 75.2% of the variation in bird x"Lonicera ¼ 9:6; x"native ¼ 7:9, t1,8 = -1.13, P = 0.30;
densities across the sites. The first score contrasted 2007: x"Lonicera ¼ 10:2; x"native ¼ 9:5, t1,8 = -0.57,
the understory birds with the canopy birds and P = 0.58).
explained 37.3% of the sample variance (Table 3).
Winter avian communities and Lonicera spp.
(a)
Over the two winters, we surveyed our 38 points ten
times, with 200 total surveys in Lonicera spp. sites
and 180 in native sites. During the winters we
observed 36 species and 2693 individuals. We
obtained density estimates for nine species (including
Paridae) and three diet guilds (Table 4). Estimated
densities of four species (American goldfinch

Table 3 Component loadings from the principal component
analysis on summer bird species

Species Component loadings

(b) 123

Fig. 3 Plot of the first and second factor scores for the avian Northern cardinal 0.90 0.00 -0.25
community principal component analysis averaged over the Paridae -0.88 0.17 0.21
2 years in a the summer and b the winter. Over the summer, Eastern wood-pewee -0.88 0.29 0.20
the first factor score contrasted canopy birds with shrub birds Gray catbird 0.25 0.16
and factor two contrasted eastern towhees and great-crested American robin 0.80 0.42 0.08
flycatchers with indigo buntings, red-eyed vireos and Carolina Common yellowthroat 0.79 -0.44 0.21
wrens. Over the winter, factor one was associated with downy Red-bellied woodpecker 0.69 -0.12 0.27
woodpeckers, red-bellied woodpeckers, white-breasted nut- Red-eyed vireo -0.67 0.66 0.17
hatches and parids. Factor two associated with American White-breasted nuthatch -0.67 -0.24 0.59
goldfinches, Carolina wrens and northern cardinals Blue jay -0.53 0.30
Eastern towhee 0.51 -0.88 -0.15
Indigo bunting -0.10 -0.69 -0.36
Carolina wren 0.39 0.67
Great-crested flycatcher 0.37 -0.67 0.28
Wood thrush -0.39 -0.17 0.53
Brown-headed cowbird 0.45 0.06 0.47
House wren 0.35 -0.07 0.81
0.21 0.75
0.69

Species with component loadings [0.6 were used to interpret
the location of sites in ordination space

123

123 2466

Table 4 Mean density of birds (birds/hectare ± 1 SE) in Lonicera spp. and native sites in the winters of 2006–2007 and 2007–2008 and effects of site type and year on winter
bird densities

Species or guild 2006–2007 2007–2008 Site Year Site 9 Year Effect
SS F SS F size
Mean in Lonicera Mean in native Mean in Lonicera Mean in native P
sites sites sites sites P SS F P

American goldfinch 1.20 ± 0.75 0.12 ± 0.08 0.49 ± 0.16 0.39 ± 0.25 1.74 4.27 0.07 0.25 0.51 0.50 1.20 2.42 0.16 1.46
American robin 1.24 ± 0.99 0.21 ± 0.14 0.75 ± 0.46 0.03 ± 0.05 3.83 3.82 0.09 0.55 1.02 0.34 0.13 0.23 0.64 1.38
Blue jay 0.43 ± 0.17 0.34 ± 0.16 0.76 ± 0.21 0.95 ± 0.23 0.01 0.04 0.84 1.11 11.03 0.01 0.10 1.03 0.34 0.14
Carolina wren 0.13 ± 0.07 0.11 ± 0.07 0.11 ± 0.05 0.02 ± 0.02 0.01 1.02 0.34 0.02 5.82 0.04 0.01 2.15 0.18 0.71
Downy woodpecker 1.14 ± 0.39 0.61 ± 0.28 0.96 ± 0.33 0.39 ± 0.16 1.52 3.97 0.08 0.19 1.83 0.21 0.00 0.02 0.90 1.41
Northern cardinal 2.45 ± 0.57 1.17 ± 0.40 1.96 ± 0.47 1.42 ± 0.55 4.16 4.02 0.08 0.08 0.21 0.66 0.69 1.78 0.22 1.42
Red-bellied 0.34 ± 0.11 0.32 ± 0.11 0.53 ± 0.14 0.88 ± 0.20 0.14 1.19 0.31 0.71 8.09 0.02 0.16 1.87 0.21 0.77

woodpecker 0.54 ± 0.26 0.68 ± 0.18 0.70 ± 0.28 0.79 ± 0.27 0.07 0.18 0.69 0.10 0.67 0.44 0.00 0.03 0.88 0.30
White-breasted
1.65 ± 0.50 1.24 ± 0.51 1.98 ± 0.51 2.01 ± 0.77 0.18 0.13 0.72 1.51 1.53 0.25 0.24 0.24 0.64 0.26
nuthatch 2.62 ± 0.74 1.85 ± 0.40 1.92 ± 0.51 2.81 ± 1.05 0.02 0.01 0.94 0.08 0.10 0.77 3.46 4.05 0.08 0.05
Paridae 3.05 ± 0.76 1.63 ± 0.39 2.75 ± 0.52 3.32 ± 0.68 0.90 0.36 0.56 2.42 2.42 0.16 4.96 4.96 0.06 0.43
Non-frugivorous
Facultative 5.96 ± 1.50 2.89 ± 0.68 5.40 ± 1.06 4.22 ± 1.02 22.58 3.68 0.09 0.76 0.37 0.56 4.43 2.17 0.18 1.36

frugivorous
Frugivorous

Results are from a repeated measures ANOVA based on the presence and absence of Lonicera spp. df = 1,8 for all tests. Effect size was calculated with Cohen’s d test

C. E. McCusker et al.

Seasonal responses of avian communities 2467

(Carduelis tristis), American robin, downy wood- (2006–2007: x"Lonicera ¼ 3:9; x"native ¼ 3:1, t1,8 = -
pecker (Picoides pubescens) and northern cardinal) 1.38, P = 0.21; 2007–2008: x"Lonicera ¼ 3:8; x"native ¼
were markedly greater on sites dominated by Loni- 3:7, t1,8 = -0.14, P = 0.89).
cera spp. Of the guilds examined, only frugivorous
birds were more common in Lonicera spp. sites. Discussion
Effect sizes indicated large site effects on the above
four species and the frugivorous guild—all with The presence of Lonicera spp. was associated with
increased densities in Lonicera spp. sites. With the both the breeding and wintering bird communities in
exception of the frugivorous guild (2006–2007: central Illinois. During the summer, the presence of
R2 = 0.83 and 2007–2008: R2 = 0.53), factor scores Lonicera spp. accompanied a change in the overall
from the habitat PCA explained little variation in avian community structure with a positive association
densities (facultative frugivorous: 2006–2007: R2 = found for understory birds, including American rob-
0.04 and 2007–2008: R2 = 0.33; non-frugivorous: ins, northern cardinals and gray catbirds. In addition,
2006–2007: R2 = 0.10 and 2007–2008: R2 = 0.23). canopy birds, especially eastern wood-pewees, were
Frugivorous birds increased in density as Lonicera negatively associated with Lonicera spp. Overwinter-
spp. and total shrub density increased. ing species were less affected by the presence of
Lonicera spp.; however, frugivorous species did have
Ordination of winter communities indicated little increased densities in areas with Lonicera spp. Despite
variation between communities of birds in Lonicera the negative affects that Lonicera spp. have on other
spp. and native sites (Fig. 3b). The first four compo- native biota, their overall associations with local
nents were retained and explained 89.3% of the data. abundances of breeding and overwintering bird com-
The first factor score represented 31.2% of the data, munities appears to be positive.
and corresponded to the number of parids, white-
breasted nuthatches (Sitta carolinensis), red-bellied Facilitation, the interaction between two species
woodpeckers and downy woodpeckers (Table 5). The that results in a beneficial response for at least one
second factor score corresponded to northern cardi- species, is often overlooked when considering
nals, Carolina wrens and American goldfinches responses of native species to invasive species
(26.6%). The third factor score contrasted densities (Rodriguez 2006). Facilitation can occur through
of American goldfinches and red-bellied woodpeck- many different mechanisms and here the presence of
ers (18.4%) and the fourth factor score accounted for Lonicera spp. results in habitat modification and
densities of blue jays (13.0%). Over the two winters, possible trophic subsidization. Understory birds dur-
avian species richness was not different between sites ing the breeding season most likely responded
positively to the modified habitat (i.e. increased
Table 5 Component loadings from the principal component shrub density), while overwintering frugivorous birds
analysis on winter avian species likely responded to the provision of a limited food
resource (i.e. fruit in winter).
Species Component Loadings
Increased shrub density was also positively asso-
1234 ciated with the number of northern cardinals using
forested areas during the breeding season in Ohio
Paridae 0.84 0.12 -0.37 0.12 (Leston and Rodewald 2006). In the present study,
White-breasted nuthatch 0.80 0.24 0.34 0.19 not only were northern cardinals more common in
Red-bellied woodpecker 0.64 -0.26 0.61 0.06 Lonicera spp. sites, but so were American robins,
Downy woodpecker 0.64 0.50 -0.43 gray catbirds and other understory birds; all being at
Northern cardinal -0.53 0.79 -0.21 0.05 least 29 more abundant in Lonicera spp. sites and all
Carolina wren 0.28 0.72 0.22 0.13 using shrubs as nesting substrate. The facilitated
American goldfinch 0.18 0.66 0.54 -0.11 response of understory birds to Lonicera spp. may,
American robin -0.46 0.51 -0.44 however, only be related to local abundances of birds.
Blue jay -0.24 0.41 -0.69 0.85 Lonicera spp. dense understory may provide an
0.38 increased number of nest sites that are attractive to

-0.17 123

Species with component loadings [0.6 were used to interpret
the location of sites in ordination space

2468 C. E. McCusker et al.

these birds; however, while nest success was not observations of cedar waxwings only occurred in
estimated in our study, others have reported lower Lonicera spp. sites, indicating a preference for sites
reproductive success of American robins and north- with Lonicera spp. (C. McCusker pers. obs.). While
ern cardinals that nest in Lonicera spp. compared to shrub density was higher in all Lonicera spp. sites
those nesting in native shrubs (Whelan and Dilger compared to native sites, birds are more likely to
1992; Schmidt and Whelan 1999; Borgmann and respond to food resources during the winter. Birds,
Rodewald 2004). Rates of reproductive success were including frugivores, will track food resources which
also found to change over the breeding season in can lead to increases in density and differences in
Lonicera spp. in Ohio, indicating that nesting in distributions of birds where resources are abundant
Lonicera spp. may be an ephemeral trap (Rodewald (Rey 1995; Moegenburg and Levey 2003). There
et al. 2009). The viability of populations of species were almost no fruits available in the native sites
nesting in Lonicera spp. is therefore questionable, (compared to the thousands of fruits produced by
and while there may be a positive association of local Lonicera spp.) over the winter months (C. McCusker
bird density with Lonicera spp., other aspects, like pers. obs.). Some of these frugivorous birds exclu-
fecundity, may be negatively affected. Further study sively consume fruits during the winter, indicating
is required to assess whether Lonicera spp. is harmful that they are likely tracking the resources provided by
to these avian populations. Lonicera spp. Several of these species were also more
common in Lonicera spp. during the breeding season
Lonicera spp. did have a negative impact on the indicating that perhaps they never left the sites and
density of one species in particular, the eastern wood- remained in these areas over the winter; however a
pewee. Other studies report that removal of understory concurrent study with American robins did not
shrubs in forests leads to greater abundances of eastern support this conclusion. A radio telemetry study of
wood-pewees (Wilson et al. 1995; Rodewald and 42 robins in the area found that all left their breeding
Smith 1998). In addition, management plans including territories in late summer and all individuals that
prescribed fires to create savanna habitats (lowering were tracked in early winter migrated south (M. Ward
both shrub and canopy density) lead to increased unpublished data), indicating that at least in our areas,
abundances of eastern wood-pewees and other species the American robins present in the summer were
that forage in relatively open habitat (Artman et al. unlikely to be the same ones present during the
2001; Brawn 2006). Eastern wood-pewees forage winter.
aerially; thus, when a more open habitat is created,
more opportunities for efficient foraging are available While the differences in frugivorous bird densities
(Rodewald and Smith 1998; Hartung and Brawn 2005). were not enough to affect the overall community
The dense understory created by Lonicera spp. likely structure, the addition of Lonicera spp. fruit resources
prohibits efficient foraging by the eastern wood- may have caused more widespread change in bird
pewee, and management strategies calling for its species’ survival and wintering ranges (White and
removal may be beneficial for the pewee. Stiles 1992). Critical analyses are needed, but the
winter ranges of two of the four species that appear to
During the winter, facilitative responses of frugiv- be positively affected by the presence of Lonicera
orous birds were seen in Lonicera spp. sites. Frugiv- spp., American robins and northern cardinals, have
orous bird densities were higher in Lonicera spp. expanded northward (Graber and Graber 1963; Dow
sites, and several of these species were observed and Scott 1971). These bird species may have a
consuming Lonicera spp. fruits over the two winters, mutualistic relationship with Lonicera spp. whereby
including northern cardinals, American robins and they feed on the fruits in winter in order to survive
cedar waxwings. In addition, we observed two and in turn spread Lonicera spp. throughout the
facultative frugivorous species, American goldfinches region (White and Stiles 1992). Both of these bird
and house finches (Carpodacus mexicanus), consum- species have increased their ranges north in areas
ing Lonicera spp. fruits. Cedar waxwings have been where Lonicera spp. is common, and over the same
reported to be a primary consumer of Lonicera spp. time frame Lonicera spp. have spread across the
fruits (Ingold and Craycraft 1983; Bartuszevige and region (Graber and Graber 1963; Dow and Scott
Gorchov 2006), and although density estimates could 1971). A study by Stiles (1982) found that a
not be obtained due to a low sample size, all

123

Seasonal responses of avian communities 2469

frugivorous species, in this case the northern mock- Conclusions
ingbird (Mimus polyglottos), expanded its range
during the winter with the provision of multi-flora Breeding and overwintering communities of birds
rose hips. Lonicera spp. provides a similar limited are responding to the presence of Lonicera spp.
food source and may facilitate range expansion of Responses are different across seasons, but overall, in
birds that utilize this species. the short-term, Lonicera spp. are leading to increased
densities of many avian species. Long-term effects of
Management implications Lonicera spp. on avian communities is in need of
further study, and may include increased survival and
Due to the negative effects of Lonicera spp. on native expanding ranges. Overwintering birds may also
plant communities (Gould and Gorchov 2000; Gorc- facilitate the spread of Lonicera spp. which can lead
hov and Trisel 2003; Miller and Gorchov 2004), to mutualistic relationships between the plant and
restoration programs commonly call for their frugivorous birds. Management strategies for removal
removal. Forested areas invaded by Lonicera spp. of Lonicera spp. need to address how birds respond to
often have little remaining native shrub cover and the presence of Lonicera spp. and the short-term
virtually no understory after Lonicera spp. are effects removal has on avian communities.
removed. Birds that utilize Lonicera spp. or other
shrubs therefore lose key resources. A total loss of the Acknowledgments We thank M. Alessi, T. Beveroth, R.
shrub layer could discourage many birds from using Johnson, T. McCusker and K. McCusker for help in the field and
restored areas until native shrubs emerge. Whereas J. Ellis for plant identification. Access to field sites was obtained
the effect may be ephemeral, more data on the effects from the Illinois Department of Natural Resources, University of
of complete removal of Lonicera spp. would be Illinois, Illinois Nature Preserve Commission, Champaign
helpful in assessing the impact of eradication. County Forest Preserve and William Taylor. Funding was
Lonicera spp. are difficult to eradicate, and control provided by the Illinois Natural History Survey and the Illinois
methods may need to go beyond simple removal of Wildlife Preservation Fund. We appreciate helpful comments
the species as it may take several years for a native from Daniel Simberloff and two anonymous reviewers.
shrub understory to reestablish (Luken et al. 1997;
Hartman and McCarthy 2004; Runkle et al. 2007). References

Another obstacle for managers to consider when Artman VL, Sutherland EK, Downhower JF (2001) Prescribed
restoring areas invaded by Lonicera spp. is the burning to restore mixed-oak communities in southern
likelihood of their reinvasion and reestablishment. Ohio: effects on breeding-bird populations. Conserv Biol
Lonicera spp. have become successful invaders 15:1423–1434
because dispersal of seeds is facilitated by several
species of birds, including American robins, that Bartuszevige AM, Gorchov DL (2006) Avian seed dispersal of
defecate viable Lonicera spp. seeds and will carry an invasive shrub. Biol Invasions 8:1013–1022
seeds to favorable habitats for germination (Bart-
uszevige and Gorchov 2006). Since birds often travel Borgmann KL, Rodewald AD (2004) Nest predation in an
long distances, they can carry seeds to new or urbanizing landscape: the role of exotic shrubs. Ecol Appl
restored habitats and initiate new invasions. Ameri- 14:1757–1765
can robins were strongly associated with the presence
of Lonicera spp. in this study and may be participat- Borgmann KL, Rodewald AD (2005) Forest restoration in
ing in a mutualistic interaction with Lonicera spp. urbanizing landscapes: interactions between land uses and
Many factors can enhance the spread of Lonicera exotic shrubs. Restor Ecol 13:334–340
spp., such as light availability and distance to urban
areas. Management strategies need to account for the Brawn JD (2006) Effects of restoring oak savannas on bird
possibility of reintroduction in recently restored areas communities and populations. Conserv Biol 20:460–469
and focus on restoring areas where reintroduction is
less likely to occur (Luken et al. 1995; Borgmann and Buckland ST, Anderson DR, Burnham KP, Laake JL, Borchers
Rodewald 2005). DL, Thomas L (2001) Introduction to distance sampling:
estimating abundance of biological populations. Oxford
University Press, New York

Buckland ST, Anderson DR, Burnham KP, Laake JL, Borchers
DL, Thomas L (2004) Advanced distance sampling:
estimating abundance of biological populations. Oxford
University Press, New York

Burnham KP, Anderson DR (2002) Model selection and mul-
timodel inference: a practical information-theoretic
approach, 2nd edn. Springer, New York

123

2470 C. E. McCusker et al.

Cohen J (1988) Statistical power analysis for the behavioral McGarigal K, Cushman S, Stafford S (2000) Multivariate
sciences, 2nd edn. Erlbaum Associates, Hillsdale statistics for wildlife and ecology research. Springer, New
York
Deering RH, Vankat JL (1999) Forest colonization and
developmental growth of the invasive shrub Lonicera Miller KE, Gorchov DL (2004) The invasive shrub, Lonicera
maackii. Am Midl Nat 141:43–50 maackii, reduces growth and fecundity of perennial forest
herbs. Oecologia 139:359–375
Dirr MA (1975) Manual of woody landscape plants: their
identification, ornamental characters, culture, propagation Moegenburg SM, Levey DJ (2003) Do frugivores respond to
and uses. Stipes Publishing Company, Champaign fruit harvest? An experimental study of short-term
responses. Ecology 84:2600–2612
Dow DD, Scott DM (1971) Dispersal and range expansion by
cardinal—Analysis of banding records. Can J Zool Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environ-
49:185–198 mental and economic costs of nonindigenous species in
the United States. Bioscience 50:53–65
Edgin B (2007) Vegetation management guideline: bush
honeysuckles: tartarian, morrow’s, belle and Amur Poole AE (2005) The birds of North America Online:
honeysuckle (Lonicera tatarica L., L. morrowii Gray, http://bna.birds.cornell.edu/BNA/. Cornell Laboratory of
L. 9 bella Zabel, and L. maackii (Rupr.) Maxim.). In: Ornithology, Ithaca
Illinois nature preserve management guidelines.
http://dnr.state.il.us/INPC/Management_guidelines.htm. Pringle JS (1973) Lonicera maackii Caprifoliaceae adventive
Accessed 12 Oct 2008 in Ontario. Can Field-Nat 87:54–55

Gorchov DL, Trisel DE (2003) Competitive effects of the Ralph CJ, Sauer JR, Droege S (1995) Monitoring bird popu-
invasive shrub, Lonicera maackii (Rupr.) Herder (Capri- lations by point counts. US Forest Service Gen Tech Rep
foliaceae), on the growth and survival of native tree PSW-GTR-149
seedlings. Plant Ecol 166:13–24
Rey PJ (1995) Spatiotemporal variation in fruit and frugivorous
Gotelli NJ, Ellison AM (2004) A primer of ecological statistics. bird abundance in olive orchards. Ecology 76:1625–1635
Sinauer Associates, Sunderland
Rodewald PG, Smith KG (1998) Short-term effects of understory
Gould AMA, Gorchov DL (2000) Effects of the exotic invasive and overstory management on breeding birds in Arkansas
shrub Lonicera maackii on the survival and fecundity of oak-hickory forests. J Wildl Manag 62:1411–1417
three species of native annuals. Am Midl Nat 144:36–50
Rodewald AD, Shustack DP, Hitchcock LE (2009) Exotic
Graber RR, Graber JW (1963) A comparative study of bird shrubs as ephemeral ecological traps for nesting birds.
populations in Illinois, 1906–1909 and 1956–1958. Illi- Biol Invasions doi: 10.1007/s10530-009-9426-3
nois Natural History Survey, Champaign, pp 383–528
Rodriguez LF (2006) Can invasive species facilitate native
Hartman KM, McCarthy BC (2004) Restoration of a forest species? Evidence of how, when, and why these impacts
understory after the removal of an invasive shrub, Amur occur. Biol Invasions 8:927–939
honeysuckle (Lonicera maackii). Restor Ecol 12:154–165
Runkle JR, DiSalvo A, Graham-Gibson Y, Dorning M (2007)
Hartung SC, Brawn JD (2005) Effects of savanna restoration Vegetation release eight years after removal of Lonicera
on the foraging ecology of insectivorous songbirds. maackii in west-central Ohio. Ohio J Sci 107:125–129
Condor 107:879–888
Sax DF, Kinlan BP, Smith KF (2005) A conceptual framework
Ingold JL, Craycraft MJ (1983) Avian frugivory on honey- for comparing species assemblages in native and exotic
suckle (Lonicera) in southwestern Ohio in fall. Ohio J Sci habitats. Oikos 108:457–464
83:256–258
Schmidt KA, Whelan CJ (1999) Effects of exotic Lonicera and
Lemmon PE (1956) A spherical densiometer for estimating Rhamnus on songbird nest predation. Conserv Biol
forest overstory density. For Sci 2:314–320 13:1502–1506

Leston LFV, Rodewald AD (2006) Are urban forests ecolog- Stiles EW (1982) Expansions of mockingbird and multiflora
ical traps for understory birds? An examination using rose in the northeastern United States and Canada. Am
Northern cardinals. Biol Conserv 131:566–574 Birds 36:358–364

Luken JO, Thieret JW (1996) Amur honeysuckle, its fall from Thalheimer W, Cook S (2002) How to calculate effect sizes
grace. Bioscience 46:18–24 from published research articles: A simplified methodol-
ogy. http://work-learning.com/effect_sizes.htm. Accessed
Luken JO, Tholemeier TC, Kuddes LM, Kunkel BA (1995) 26 Nov 2008
Performance, plasticity, and acclimation of the nonindig-
enous shrub Lonicera maackii (Caprifoliaceae) in con- Thomas L, Laake JL, Strindberg S, Marques FFC, Buckland
trasting light environments. Can J Bot 73:1953–1961 ST, Borchers DL, Anderson DR, Burnham KP, Hedley
SL, Pollard JH, Bishop JRB, Marques TA (2006) Distance
Luken JO, Kuddes LM, Tholemeier TC (1997) Response of 5.0. Release beta 5. Research Unit for Wildlife Population
understory species to gap formation and soil disturbance Assessment, University of St. Andrews, UK
in Lonicera maackii thickets. Restor Ecol 5:229–235
Whelan CJ, Dilger ML (1992) Invasive, exotic shrubs: a par-
Martin TE, Paine CR, Conway CJ, Hochachka WM, Allen P, adox for natural area managers? Nat Areas J 12:109–110
Jenkins W (1997) BBIRD field protocol. Montana
Cooperative Wildlife Research Unit, University of Mon- White DW, Stiles EW (1992) Bird dispersal of fruits of species
tana, Missoula introduced into eastern North America. Can J Bot
70:1689–1696
McCusker CE (2008) Seasonal responses of avian communities
to invasive bush honeysuckles (Lonicera spp.). Thesis, Wilson CW, Masters RE, Bukenhofer GA (1995) Breeding
University of Illinois bird response to pine grassland community restoration for
red-cockaded woodpeckers. J Wildl Manag 59:56–67

123