ECOGRAPHY

Research
Diverse temperate forest bird assemblages demonstrate
closer correspondence to plant species composition than
vegetation structure

Bryce T. Adams and Stephen N. Matthews

B. T. Adams (https://orcid.org/0000-0002-7830-6523) ✉ (adams.861@osu.edu) and S. N. Matthews, School of Environment and Natural Resources,
The Ohio State Univ., Columbus, OH 43210, USA.

Ecography
42: 1–13, 2019
doi: 10.1111/ecog.04487
Subject Editor: Cagan Sekercioglu
Editor-in-Chief: Miguel Araújo
Accepted 22 June 2019
The aggregate structure of vegetation has long provided a strong conceptual basis for
understanding the ecological separation of faunal species, while correspondence with
plant species composition remains largely underdeveloped and considered secondary
to structure. Longstanding ecological debate on the matter has likely been sustained by
statistical methods incapable of accommodating an entire species composition in the
explanatory role. We used direct ordination methodologies (predictive co-correspon-
dence and canonical correspondence analyses) that allow the comparison of prediction
levels between composition and structure for understanding avian assemblage com-
position in a temperate forestland in southeastern Ohio. Compositional (birds and
woody plants) and structural (both vertical and horizontal dimensions) data were col-
lected from point samples comprising a spectrum in topography and successional state.
Total woody plant composition (11.22%) explained more (cross-validatory) variation
in avian species composition than structure, quantified with dense LiDAR recordings
(7.35%) and field methods (6.31%). Plant composition assumed an integrative char-
acter, synthesizing aspects of environmental condition, structure, and most likely spe-
cies-specific preferences for tree and shrub species that structural indices alone could
not for predicting avian species composition. These results conflict with the traditional
view that structure be most influential to avian assemblage composition. Instead these
results demonstrate that plant and avian assemblages are closely linked, and that plant
species per se can be a powerful tool for predicting avian habitat. More importantly,
in furthering ecological understanding, it is critical to consider the complex web of
interacting processes that make up temperate forest ecosystems, in which composition
occupies a key position.

Keywords: birds, co-correspondence analysis, composition versus structure,

MacArthur, temperate forests

––––––––––––––––––––––––––––––––––––––––
© 2019 The Authors. Ecography © 2019 Nordic Society Oikos
www.ecography.org

1
Introduction
The cumulative response of individual organisms to ecologi-
cal and environmental variation plays a critical role in shaping
biological communities. While individual species respond to
such variation simultaneously across a range of organizational
levels, the most direct interactions are expected to occur at
relatively fine levels (Wiens 1989, Cushman and McGarigal
2004). Here, biotic conditions defined by vegetation struc-
ture (VS, hereafter) and plant species composition (PSC,
hereafter) are considered most influential to many species
(Block and Brennan 1993, Quine et al. 2007). Numerous
studies support and continue to demonstrate the importance
of such factors on avian assemblages and selected focal spe-
cies in emblematic forest ecosystems among mature stands
(Virkkala and Liehu 1990, Rodewald and Abrams 2002,
Lee and Rotenberry 2005, Hewson et al. 2011, Yen et al.
2011, Kellner et al. 2018), but also early-successional stands
(King et al. 2009) and other habitats alike (Wiens et al. 1987,
Rotenberry and Wiens 2009). Of these factors, however, VS
is often considered the primary driver of avian assemblage
variation (Jones 2001) and other taxa (see Schaffers et al.
2008 regarding arthropods). Efforts to understand how the
interactions between VS and PSC on avian species scale-up to
the assemblage-level have contributed to a long-standing eco-
logical debate on the relative importance of vegetation factors
for faunal assemblages (Anderson and Shugart 1974, Wiens
and Rotenberry 1981, Rotenberry 1985, Mac Nally 1990,
Fleishman and Mac Nally 2006, Müller et al. 2010).
Observations on the vertical profiling of forest habi-
tats have favored the importance of structural diversity for
the diversity of avian assemblages for some time (Dunlavy
1935). The pioneering work by MacArthur and MacArthur
(1961), with their structural index relating to the distribu-
tion of foliage over height, known as foliage height diver-
sity (FHD), provided the first quantitative assessment of
such relationships between plant and avian assemblages.
MacArthur’s results and prior observations were interpreted
to be the result of the exploitation of individual bird spe-
cies to the potential increases in niche space afforded by VS,
despite the confounding relationship between physiognomic
diversity and plant species diversity (MacArthur 1958, Mac
Nally et al. 2002). The effects of PSC were thought to oper-
ate solely through its impacts to VS and contribute little to
avian niche space directly (MacArthur and MacArthur 1961,
Mac Nally et al. 2002). This implies that individual tree and
shrub species are otherwise functionally-redundant as long
as the replacement of one species by another imparts little
to no change to the structural configuration of vegetation
(Rotenberry 1985, Fleishman et al. 2003, Veen et al. 2010).
Strong individualistic preferences for certain tree and
shrub species are indeed recognized for many bird species
(Holmes and Robinson 1981, Gabbe et al. 2002, Hartung
and Brawn 2005), even among closely-related species
(Veen et al. 2010). Additionally, emergent relationships
between birds and vegetation are often revealed among
2
models including both VS and PSC variables that were not
otherwise present among models restricted to VS variables
alone (Hewson et al. 2011). These plant-specific preferences
likely manifest from differences in the provisioning of spe-
cific resources by different tree species, such as food (e.g.
invertebrates, seeds and fruits) and nest sites (Rotenberry
1985, Holmes and Schultz 1988, Shutt et al. 2018). For
example, species of the genus Quercus (oaks) often host
more diverse and abundant lepidopteran assemblages than
any other co-occurring species in eastern deciduous forests
(Summerville et al. 2003, Tallamy and Shropshire 2009).
In addition, species-specific foliage architecture and growth
form can influence foraging behavior and concealment from
predators (Robinson and Holmes 1982, Whelan 2001,
Wood et al. 2012, Muiruri et al. 2016). Ultimately, these
studies support species-specific adaptations that define avian
niche parameters according to plant-specific food resources
and foraging substrates (Holmes et al. 1979, Holmes and
Robinson 1981). Therefore, plant species per se also likely
contribute to the differential partitioning of bird species in
some way (Holmes et al. 1979). Methodological expres-
sions of assemblage variation have likely contributed to
the underappreciation of PSC in faunal assemblage studies
(Rotenberry 1985, Schaffers et al. 2008).
Quantifying plant–faunal correspondences have recently
experienced a methodological advancement. Inference on
this matter has largely followed conclusions made by correla-
tions between univariate descriptors, such as plant and avian
diversity, or independent ordinations/dissimilarity matrices
of avian and plant assemblages (MacArthur and MacArthur
1961, Rotenberry 1985, Lee and Rotenberry 2005). However,
assemblage data are intrinsically multivariate, and such varia-
tion is obscured by simplifying assemblage composition to
simple indices (Rotenberry 1985). Specifically, raw species
identities must be preserved to resolve cross-taxon correspon-
dences among species of either assemblage (Schaffers et al.
2008). Direct ordinations, particularly canonical corre-
spondence analysis, are better suited to this task (ter Braak
1986). Until now, however, direct ordinations were limited
in scope by the number of variables that may be reliably fit to
community data, and, thus, incapable of accommodating a
second species assemblage in the predictor role. Predictive co-
correspondence analysis was recently developed by adapting
aspects of canonical correspondence analysis to finally allow
a compositional data set (e.g. plants) to predict the species
composition of another (e.g. birds) (ter Braak and Schaffers
2004). Quantified prediction levels based on PSC can now be
directly compared to those obtained by canonical correspon-
dence analysis parameterized with VS variables, circumvent-
ing the information loss that results from correlating simple
diversity indices (ter Braak and Schaffers 2004). Moreover,
ordinations provide a means for the visual inspection of
emergent relationships between species and variables in
ordination diagrams. Meanwhile, advanced remote sensing
technologies, such as LiDAR, provide unparalleled windows
into the structural arrangement of habitats for examining
organismic response to VS (Hinsley et al. 2006, Müller et al.
2010, Swatantran et al. 2012).
There is developing interest in the role of PSC on faunal
assemblages and identifying and reevaluating the factors
considered important to avian resource utilization and
community structure is important for adapting manage-
ment response to environmental and ecological change.
Specifically, concrete efforts in establishing plant–fau-
nal links at local scales could provide immense support
to ongoing efforts examining faunal response to apparent
proximate signals of shifting vegetation pressures, including
climate change (Rodenhouse et al. 2008, Matthews et al.
2011, Buchanan et al. 2016, Iverson et al. 2018). We used
predictive ordination techniques to compare PSC and VS
for explaining avian assemblage composition in a temper-
ate forestland in southeastern Ohio. Our objectives are to
establish a better link between plant and avian assemblages
in temperate forestlands and demonstrate the utility of PSC
for predicting avian habitat. We expect that some of the
associations that emerge be the result of the interrelation-
ships between PSC and VS (Mac Nally 1990, Fleishman
and Mac Nally 2006, Hewson et al. 2011). However, we
predict that the effects of PSC not operate solely through
variation in VS, and these tools support clarity into the
multiple interacting pathways that structure avian response
to forest habitats across successional and environmental
gradients.
Methods
Study area and sampling design
We sampled the composition of bird and plant assemblages
from point samples distributed across five study sites in
an actively managed, mixed-used forest landscape (~1300
km2) in southeastern Ohio’s Central Hardwoods (Fig. 1a,
Supplementary material Appendix 1). A total of 210 points
were distributed >150 m from one another and <400 m
from roads to facilitate landscape-scale coverage according to
a generalized random tessellation stratified sampling design
(Fig. 1b) (Stevens and Olsen 2004). Floristic assemblages
closely track the topographic contours of the unglaciated
Allegheny Plateaus physiographic region, which features
dissected terrain with <100 m local relief. The connection
between floristic variation and topography has constituted
a fundamental component of ecological classification in the
study area based on an ecological landtype (ELT) concept
(Hix and Pearcy 1997, Iverson et al. 2018). Though not
used directly for predicting avian species composition, each
point sample was labeled according to three ELTs to support
interpretation of avian and floristic gradients (Fig. 1c, addi-
tional information on species associations and an indicator
species analysis can be found in Supplementary material
Appendix 1). In general, mixed-oak assemblages, primarily
composed of Quercus and Carya genera, dominate the 1) dry
ridgetops and southwestern hillslopes (n = 96 points) and
transition to mesophytic assemblages on opposing, mesic,
2) northeastern hillslopes (n = 59 points) and 3) bottom-
lands (n = 55 points), with considerable species-level varia-
tion in between (Fig. 2a). In fact, the region is particularly
speciose, harboring 75 tree species (Prasad et al. 2007). In
addition, the overall sampling design was inclusive to a wide
spectrum of native forest type (<1% plantation) and growth
stage, including open-canopy stands like MacArthur and
MacArthur (1961), maximizing the ecological coverage and
comprehensiveness of our data set.
Compositional data sets
Bird surveys followed the standard point count protocol
(Ralph et al. 1995). Trained observers performed counts
for 10 min over six surveys, three in each year (2015–
2016), from mid-May to early-July on mornings (half-hour
before sunrise to the hour of 10:30 EST) with minimal
wind or precipitation interference. We used detections
≤50 m from the observation point to ensure that only
birds using the habitat being sampled were included in
the analysis. Recent studies support the use of fixed-radius
counts over model-based solutions, particularly for lim-
ited observation radii and comparably large sample sizes
(Johnson 2008, Hutto 2016). Thus, we used raw counts
as an index of relative abundance and limited our analysis
to only passerines because members of this group (except
for American crow Corvus brachyrhynchos and blue jay
Cyanocitta cristata) feature similar body sizes, insectivo-
rous diets during the breeding period, and defense of rela-
tively small discrete territories. We summed all detections
(auditory and visual) over the six surveys and arranged
these data into a matrix of bird species composition by
point (hereafter denoted as [B]).
We assessed PSC through three compositional matrices:
tree, shrub and total woody plant composition. Live woody
stems (≥1 m height) were sampled at each point loca-
tion from either two or three 11.3-m radius circular plots
(~400 m2), depending on logistical constraints, and in two
stem size classes (i.e. physiognomies): large-diameter stems
(i.e. trees) were ≥8 cm diameter at breast height (DBH),
and small-diameter stems (i.e. shrubs and young trees)
were <8 cm DBH. Plots were arranged into 3 × 3 arrays
on point center, in which the center plot was sampled first
and additional plots (either one or two) selected randomly.
Large stems were counted and DBH recorded within the full
plot, while small stems were counted (DBH omitted) from
a nested subplot (5-m radius; ~100 m2). All woody stems
were identified to species following Braun (1961), except
for members of the genera Carya, Crataegus, Salix, Smilax,
Vaccinium and Vitis due to difficulties in field identification.
Stem counts were summarized across the multiple plots per
point into local stem densities (no. stems ha−1) for each plant
taxon, generating two physiognomically-defined matrices,
representing the composition of the shrub/regeneration
3
Figure 1. Study area (a) and distribution of 210 point samples located in southeastern Ohio (b). Panel (c) shows and an example of three
points distributed across ecological landtypes that support diverse forest types and used here for interpretation of results. Panel (d) shows
LiDAR returns for an example point (StructureLiDAR, [L] matrix) with horizontal lines indicating vertical layers used to quantify foliage
height diversity (FHD). LiDAR-derived vertical profiles of points (including sample sizes) by ecological landtype (gray line indicates the
profile of the example point) (e). Finally, violin plots in panels (f ) and (g) show stem densities (no. stems ha−1) and canopy cover (%) of
points by ecological landtype (StructureField, [F]).

layer by the small-diameter size class (i.e. shrubs, [S]) and densities, [S] + [T]) representing total woody plant composi-
midstory and overstory tree composition by the large- tion ([A]). The number of sample plots (either two or three)
diameter size class (i.e. trees, [T]), and a combined matrix had no effect on the total species richness summarized per
including all stems from both size classes (summed species point (p = 0.453).

4
 (a) Indicator species analysis

Acer rubrum
Acer saccharinum
Acer saccharum
Amelanchier arborea
Betula nigra
Cornus amomum
Fraxinus pennsylvanica
Lindera benzoin
Nyssa sylvatica
Oxydendrum arboreum Indicator value
Populus grandidentata 10
20
Quercus alba
30
Quercus coccinea 40
Quercus montana 50
Quercus velutina 60
Rhus copallinum
Rhus glabra
Rosa multiflora
Sassafras albidum
Smilax spp
Toxicodendron radicans
Ulmus americana
Ulmus rubra
Vaccinium spp
Viburnum dentatum

Northeastern Bottomlands points Ridgetops and

hillslopes points southwestern
hillslopes points

(b) Total woody plant composition, [A] (c) Bird composition, [B]

Ridgetops and
southwesternv
hillslopes

Northeastern
hillslopes

Bottomlands

10 15 20 25 30 35 40 10 15 20 25

Woody plant richness (NO species) Bird richness (NO species)

Figure 2. Compositional variation, including indicator values of diagnostic woody plant species (a) and species richness (no. species) of
plants (total composition, [A]) (b) and birds (birds, [B]) (c) by ecological landtype.

Vegetation structure data sets
Vegetation structure, emphasizing both vertical and hori-
zontal dimensions, was derived from publicly available
LiDAR data ([L]) (<http://ogrip.oit.ohio.gov/Home.aspx>;
accessed 13 October 2014), collected in 2007, and through
the field ([F]) methods for two structural predictor matrices
(Supplementary material Appendix 2). We chose to develop
structural variable sets from different sources to leverage the
potential unique information provided by conventional field
methods and remote sensing as part of our overall evalua-
tion and to foster robust comparisons with PSC. Field-
derived variables, collected among the vegetation plots at
each point, included composite (i.e. across all species) stem
density (combined size classes) (Fig. 1f ), composite basal area
(m2 ha−1) (large size class only), (mean) canopy cover (%)
(Fig. 1g) and (mean) canopy height (m). Canopy cover was
estimated at each vegetation plot using a convex, spherical
densiometer and averaged for each point. The LiDAR data
set, including filtered ground and vegetation returns, had an
average spacing and density of 1.27 m and 0.27 returns m−2,
respectively. We computed the maximum, mean and SD
of the canopy surface for each point from a 5-m resolution
canopy height model. Three penetration ratios (number
of LiDAR returns <2 m divided by the number of returns
<50 and <10 m, including returns <2 m; and the number

5
of returns <1 m divided by the number of returns <5 m,
including returns <1 m) were also computed to charac-
terize the degree of canopy openness (0–2/0–50 m ratio),
amount of midstory foliage (0–2/0–10 m ratio) and amount
of understory foliage (0–1/0–5 m ratio) (Müller et al. 2010,
Melin et al. 2018). Finally, we computed FHD in a manner
similar to MacArthur and MacArthur (1961) by clustering
returns within three vertical layers, 0–5, 5–25 and >25 m,
and calculating the diversity (Shannon’s index) of vegeta-
tion hits throughout the vertical profile of each point loca-
tion (Melin et al. 2018) (Fig. 1c–d): −∑pi ln pi; where pi
is the proportion of the total LiDAR returns within the ith
vertical layer.
Data analysis
The study area includes active forest management in which
timber harvests occurred at some of the point locations since
the acquisition of LiDAR. We excluded those points, as
recommended in studies featuring non-coincident LiDAR
and wildlife survey data (Vierling et al. 2014), and points
<30 m from roads for the final sample of 210 points used
in this study. We applied log (x + 1) transformations to the
compositional ([B], [S], [T] and [A]) and structural ([L]
and [F]) data sets before analysis. In addition, we used
only species recorded in ≥5 (2%) point locations for each
compositional data set to reduce noise associated with the
effect of rare species on the exaggeration of the distinctive-
ness of sample units according to the X2 distance measure
(McCune et al. 2002).
We used a predictive version of canonical correspondence
analysis (partial least squares [PLS] extension; ter Braak and
Verdonschot 1995, ter Braak and Schaffers 2004) to pre-
dict species composition with the structural data ([L] or
[F]), and (predictive) co-correspondence analysis (ter Braak
and Schaffers 2004, Schaffers et al. 2008) to predict spe-
cies composition (such as [B]) with the compositional data
of another assemblage (such as [A]). Both approaches are
similar in many ways, such as assuming a unimodal spe-
cies response (ter Braak and Schaffers 2004, Schaffers et al.
2008). Model fit was determined by a predictive, leave-one-
out cross-validatory procedure. Accordingly, a series of PLS
regression models were tuned, each time withholding an
individual point location for use as test data, until all point
samples were used in validation. Prediction accuracies (i.e.
cross-validated explained variance) were quantified by com-
paring the predicted composition of each point to the actual
species data using the cross-validatory fit: 100 × (1 − sspa/
ssp0); where sspa is the sum of squared prediction errors for
the model and a given axis solution, and ssp0 is the squared
prediction error under the null expectation of equal relative
abundances. This robust estimator produces model fits that
are usually lower than those customary for explanatory meth-
ods, but do not imply weak relationships (Schaffers et al.
2008). In fact, models are implicitly validated when cross-
validatory fit exceeds zero (ter Braak and Schaffers 2004,
Schaffers et al. 2008). These methods yield multidimensional
6
solutions in which model fit varies according to the num-
ber of ordination axes. To help facilitate the selection of
final predictive models, permutation tests (999 permuta-
tions) were used to determine the significance of each axis
combination. In all cases, we chose the number of ordina-
tion axes for final interpretation according to the maximum
predictive fit (i.e. global maximum) (Schaffers et al. 2008)
among those statistically significant (p < 0.05). Finally, the
statistical difference in model fit between the individual pre-
dictor sets was determined with two-sided randomization
tests (999 permutations) (van der Voet 1994). All analyses
were conducted in the R statistical environment (< https://
cran.r-project.org/ >). Specifically, co-correspondence
analysis utilized various functions in the cocorresp package
(Simpson 2016), whereas canonical correspondence analysis
was implemented by adapting functions in cocorresp and
scripts provided in supplementary materials of ter Braak and
Schaffers (2004).
Data deposition
Data are available from the Dryad Digital Repository:
< http://dx.doi.org/10.5061/dryad.k48h616 > (Adams and
Matthews 2019).
Results
Our final data set included 48 bird species and 65 plant
taxa (Supplementary material Appendix 3). Mean richness
was 16.58 (± 3.97 SD) bird species and 19.76 (± 6.03 SD)
woody plant taxa per point (Fig. 2b–c). The five predictive
data sets based on PSC and VS included cross-validatory fits
greater than zero, exceeding the null expectation of no rela-
tionship with bird species composition. Plotting model fit
percentages against the number of ordination axes revealed
unique trends among each predictor set (Fig. 3; filled sym-
bols indicate significant axis solutions). While only margin-
ally greater than local maxima in some instances, we selected
the final predictive models based on the global maximum
for each data set. Final models included six, three, four, five
and four axes solutions for [L], [F], [T], [S] and [A], respec-
tively (Table 1). The decision to use global maxima did not
qualitatively change the results. Total woody plant composi-
tion ([A]) explained the most variation in [B] at 11.22%,
which was significantly greater than the remaining predic-
tor sets according to the randomization tests: [L] (p = 0.048),
[F] (p = 0.015), [S] (p = 0.001) and [T] (p = 0.001) (see
Supplementary material Appendix 4 for randomization test
results). Structural predictor sets, [L] and [F], exhibited
moderate predictive capacity, according to the range in fits,
at 7.35% and 6.31%, respectively. The fit of [S] was slightly
greater than the two structural data sets at 9.11%, but statis-
tically indifferent. The weakest prediction level was observed
for [T] at 3.45%. The difference between [S] and [T] was
significant (p = 0.014), while the fits between [L], [F] and [T]
were similar. Correspondingly, total PSC, considering both
Figure 3. Prediction levels (% cross-validatory fit) of bird species composition by the structural and compositional predictor data sets and
methods (CCA-PLS = canonical correspondence analysis-partial least squares extension; CoCA = co-correspondence analysis). Displayed is
the cross-validatory fit plotted against the number of ordination axes for 12 axes. The filled symbols indicate significant axis solutions deter-
mined by permutation tests. Final models are indicated by horizontal bars and were selected according to the global maximum.

stem size classes ([A]), provided the best explanation of bird
species composition ([B]) (Table 1).
Examining the model with most support reveals sensible
ecological gradients in ordination space (Fig. 4; points are
shaded according to ELT and vectors of structural variables
are fitted post hoc to assist interpretation (Oksanen et al.
2018)). The primary and secondary axes display topographic
and structural gradients, respectively. However, these factors
appear to interact and vary in a more diagonal fashion with
respect to the origin, where shifts in ELT relates to some
variation in VS and vice versa. For example, canopy height
among dry ridgetops (and southwestern hillslopes) was
2.61–6.07 m (95% C.I.) and 1.86–5.42 m (95% C.I.) less
than that of northeastern hillslopes and bottomlands, respec-
tively, explaining the positioning of those points towards
the lower-right of the diagram with respect to the ELT
and structural gradients. Plant species typical of inundated
floodplains, such as the indicator species Acer saccharinum
and Betula nigra (Supplementary material Appendix 1), and
wetland bird species, red-winged blackbird (Agelaius phoeni-
ceus) and common yellowthroat (Geothlypis trichas), occupy
the upper-left section of the diagram, while the other end
includes taxa typical of drier site conditions and sparse, oak-
dominated canopies, such as Vaccinium spp., Quercus coccinea

Table 1. Prediction levels (% cross-validatory fit) of the final models (dimensionality given in parentheses) for the taxonomic composition of
avian and plant assemblages constrained by vegetation structure or plant composition. Statistical comparisons in model fit (determined
by two-sided randomization tests; p < 0.05) are coded by letters where statistically similar fits are represented by similar letters
(CCA-PLS = canonical correspondence analysis-partial least squares extension; CoCA = co-correspondence analysis).

Dependent matrix
Independent matrix (model) Tree composition, [T] Shrub composition, [S] Total composition, [A] Bird composition, [B]
StructureLiDAR, [L] (CCA-PLS) 1.71 (2) 2.35 (2) 2.66 (2) 7.35 (6) a, b
StructureField, [F] (CCA-PLS) 1.23 (1) 3.56 (2) 3.45 (2) 6.31 (3) a, b
Tree composition, [T] (CoCA) – 8.72 (8) – 3.45 (4) a
Shrub composition, [S] (CoCA) 13.41 (7) – – 9.11 (5) b
Total composition, [A] (CoCA) – – – 11.22 (4) c

7
8
Bird composition, [B]
a Acadian Flycatcher (Empidonax virescens)
b American Crow (Corvus brachyrhynchos)
c American Goldfinch (Spinus tristis)
d American Redstart (Setophaga ruticilla)
e American Robin (Turdus migratorius)
f Baltimore Oriole (Icterus galbula)
g Black−and−white Warbler (Mniotilta varia)
h Blue−gray Gnatcatcher (Polioptila caerulea)
i Brown−headed Cowbird (Molothrus ater)
Total woody plant composition, [A]
35
1 boxelder (Acer negundo)
2 red maple (Acer rubrum)
3 silver maple (Acer saccharinum) 25
4 sugar maple (Acer saccharum)
5 yellow buckeye (Aesculus flava)
6 tree−of−heaven (Ailanthus altissima) 15
7 downy serviceberry (Amelanchier arborea)
8 paw paw (Asimina triloba)
9 river birch (Betula nigra)

Canopy height (m)

5
j Blackburnian Warbler (Setophaga fusca) 10 American hornbeam (Carpinus caroliniana)
k Blue Jay (Cyanocitta cristata) 11 hickory (Carya spp)
l Brown Thrasher (Toxostoma rufum) 12 American chestnut (Castanea dentata) Ridgetops and southwestern hillslopes points StructureLiDAR, [L]
m Black−throated Green Warbler (Setophaga virens) 13 hackberry (Celtis occidentalis) Northeastern hillslopes points StructureField, [F]
n Blue−winged Warbler (Vermivora cyanoptera) 14 eastern redbud (Cercis canadensis) Bottomlands points
o Carolina Chickadee (Poecile carolinensis) 15 alternate leaf dogwood (Cornus alternifolia) 3
p Carolina Wren (Thryothorus ludovicianus) 16 silky dogwood (Cornus amomum)
Structural ea
q Cedar Waxwing (Bombycilla cedrorum) 17 flowering dogwood (Cornus florida) _m s
r Cerulean Warbler (Setophaga cerulea) 18 American hazelnut (Corylus americana) vector key: e ig ax _ba
s Chipping Sparrow (Spizella passerina) 19 hawthorn (Crataegus spp) h m m ea
n_ _ te en a _m

chm_std
t Common Yellowthroat (Geothlypis trichas) 20 autumn olive (Elaeagnus umbellata) 3 ca hm g_s Ev me vr
c i g _ co
u Eastern Phoebe (Sayornis phoebe) 21 American beech (Fagus grandifolia) b e m _
v h n
c a
v Eastern Towhee (Pipilo erythrophthalmus) 22 white ash (Fraxinus americana) c 0
_1
w Eastern Wood−Pewee (Contopus virens) 23 green ash (Fraxinus pennsylvanica) n2
2 pe
x Eastern Tufted Titmouse (Baeolophus bicolor) 24 witch hazel (Hamamelis virginiana)
y Field Sparrow (Spizella pusilla) 25 shrubby St. Johns wort (Hypericum spathulatum)
8
z Great Crested Flycatcher (Myiarchus crinitus) 26 black walnut (Juglans nigra)
A Gray Catbird (Dumetella carolinensis) 27 spicebush (Lindera benzoin) −0.75 53
pen1_5
B Hooded Warbler (Setophaga citrina) 28 tulip poplar (Liriodendron tulipifera)

CoCA axis 2
C Indigo Bunting (Passerina cyanea) 29 Japanese honeysuckle (Lonicera japonica) 16 6
D Kentucky Warbler (Geothlypis formosa) 30 amur honeysuckle (Lonicera maackii) 59
E Louisiana Waterthrush (Parkesia motacilla) 31 black gum (Nyssa sylvatica) 13
F Northern Cardinal (Cardinalis cardinalis) 32 eastern hophornbeam (Ostrya virginiana)
1

_
−0.75 5723

0
G Northern Parula (Setophaga americana) 33 sourwood (Oxydendrum arboreum)

m
_5 n

e
st
H Ovenbird (Seiurus aurocapilla) 34 virginia creeper (Parthenocissus quinquefolia) 27

n2 de
R 2 = 0.05 G

ll_
pe
I Pine Warbler (Setophaga pinus) 35 pitch pine (Pinus rigida)

a
R 2 = 0.25 9 5 d r m
J Prairie Warbler (Setophaga discolor) 36 eastern white pine (Pinus strobus) 30 24
R 2 = 0.55 58 E 4
K Rose−breasted Grosbeak (Pheucticus ludovicianus) 37 American sycamore (Platanus occidentalis)
L Red−eyed Vireo (Vireo olivaceus) 38 bigtooth aspen (Populus grandidentata) E M 50
4 p z 22 21
M Red−winged Blackbird (Agelaius phoeniceus) 39 black cherry (Prunus serotina)
t 37 V 64 10
K 32 Ia e
N Scarlet Tanager (Piranga olivacea) 40 white oak (Quercus alba) 1 28S55
A 34 F 15 xh jPL N
O Summer Tanager (Piranga rubra) 41 scarlet oak (Quercus coccinea) 0 60 u i11 H R
bD 14 UB 2w
62
P White−breasted Nuthatch (Sitta carolinensis) 42 shingle oak (Quercus imbricaria) 26 29 c f k g44 31
Q White−eyed Vireo (Vireo griseus) 43 chestnut oak (Quercus montana) 22 21 o 19 43
56 65q18 v 493517 40 712
O
R Worm−eating Warbler (Helmitheros vermivorum) 44 red oak (Quercus rubra) z C 63
l52 39 45 33
S Wood Thrush (Hylocichla mustelina) 45 black oak (Quercus velutina) Ia Q 51 54
10K e
T Yellow−breasted Chat (Icteria virens) 46 winged sumac (Rhus copallinum) 32 61
U Yellow−throated Vireo (Vireo flavifrons) 47 smooth sumac (Rhus glabra) h 48 41
28 S 42 20
V Yellow−throated Warbler (Setophaga dominica) 48 staghorn sumac (Rhus typhina) 15 55
x j PL
N 36
49 black locust (Robinia pseudoacacia) H n 25
50 multiflora rose (Rosa multiflora) −1 D 60 i 11 R 38
b u 47 s
51 blackberry (Rubus allegheniensis) 14
U B 2w
6231
52 raspberry (Rubus occidentalis)
f k g 44 T 46
53 elderberry (Sambucus canadensis)
17 43 J
54 sassafras (Sassafras albidum) 1819 49 35 40 7
55 green briar (Smilax spp) v
5q 12
56 steeplebush spirea (Spiraea tomentosa) O
57 American basswood (Tilia americana) y
63
39 45 33
58 poison ivy (Toxicodendron radicans) −2 l
59 American elm (Ulmus americana) 52
54
60 red elm (Ulmus rubra) 1
61 blueberry (Vaccinium spp)
62 mapleleaf viburnum (Viburnum acerifolium)
63 arrowwood viburnum (Viburnum dentatum)
64 blackhaw viburnum (Viburnum prunifolium) −5 −4 −3 −2 −1 0 1 5 15 25 35
65 grape vine (Vitis spp)
CoCA axis 1 Canopy height (m)

Figure 4. Predictive co-correspondence analysis ordination diagram of bird species composition constrained by total woody plant composition, [A]. Bird species are positioned
according to their normalized sites scores derived from the plants. Structural vectors (not used in the ordination) and the coloring of point samples by ecological landtype is used
to facilitate interpretation (see Supplementary material Appendix 2 for variable descriptions). In addition, variation in canopy height (m) is emphasized along each axis by the verti-
cal and horizontal bars. Two inset figures display a structural vector key and zoomed in view of the center of the ordination.
and worm-eating warbler Helmitheros vermivorum. The
second gradient, moving diagonally towards the upper-
right of the diagram, corresponds to a structural gradient
from open- to closed-canopy habitats. Early-seral forests/
shrublands, comprising species such as Rhus copallinum,
Hypericum spathulatum, prairie warbler Setophaga discolor,
and yellow-breasted chat Icteria virens, dominate areas with
comparably low axes scores. These assemblages transition to
structurally-complex stands, appearing in riparian habitats,
characterized by species such as Asimina triloba and north-
ern parula Setophaga americana, and northeastern hillslopes,
characterized by Fraxinus pennsylvanica and cerulean warbler
Setophaga cerulea.
Discussion
Bird species composition was best explained by the taxo-
nomic identity of vegetation rather than structure across the
floristically-speciose forest landscape in southeastern Ohio.
The predictive ordination techniques provided a unique
basis for resolving relationships between bird and plant
assemblages. In doing so, however, our analysis revealed that
associations with PSC were, as predicted, highly-complex.
Direct floristic effects likely explain much of the predictive
power of PSC in our study. For instance, numerous examples
identify species-specific selection of certain plants by birds
in our study area, such as the cerulean warbler utilizing
Vitis spp. bark for nest construction (Weakland and Wood
2005, Bakermans and Rodewald 2009) and the worm-eat-
ing warbler preferentially foraging among Quercus montana
trees (Greenberg 1987). Ordination diagrams are powerful
tools for displaying these patterns and it is noteworthy the
proximity of these species in the co-correspondence results.
In other systems, such as bird-seed dispersal networks, the
phenology and abundance of fruiting resources (Machado-
de-Souza et al. 2019) and sometimes morphological comple-
mentarity of birds and plants (e.g. fruit diameter and bill
length) (González-Castro et al. 2015) supports the under-
standing of the temporal and spatial distribution of species
interactions, demonstrating the often tight-linkage between
plant–avian assemblages.
The strength in this relationship, however, need not be
entirely due to direct floristic effects. This relationship could
emerge from the ability of PSC to also synthesize other fac-
tors that may be responsible for determining faunal resource
use, in addition to species-specific preferences. This is
because plants themselves are responding to environmental
condition, as well as defining and modifying their environ-
ment through growth (i.e. affecting VS), litter deposition
and competition (as interpreted by Schaffers et al. 2008).
Consequently, the correspondence could result from shared
responses to the same set of conditions, or the conditions
responsible for shaping plant assemblages may appear to
manifest as drivers of associated avian assemblages, despite
whether they directly interact with individual bird species
or not (Hawkins and Porter 2003, Gioria et al. 2010). Here
again, ordination diagrams provide meaningful context to
unpack the synthesizing nature of PSC. Topographic driv-
ers of PSC manifested along the co-correspondence analy-
sis, while this relationship was not portrayed when VS was
used to constrain bird species composition (regular canoni-
cal correspondence analysis results in Fig. 5). Additionally,
projecting structural variables onto the co-correspondence
results produced directional loadings towards expected plant
assemblages according to their observed structural proper-
ties. These visual observations suggest that PSC synthesized
some aspects of VS, highlighting the integrative character of
these data. This is not unlike the patterns observed in other
studies, demonstrating correspondence between PSC and
VS, albeit with univariate descriptors of diversity (MacArthur
and MacArthur 1961). It is indeed the plants themselves that
support structural variation of the vegetation.
Interestingly, however, VS, either LiDAR- or field-derived,
was not a strong predictor of woody PSC (Table 1). These
data domains typically obtained similar predictive fits, ulti-
mately indicating that, while the different domains likely
captured some different aspects of VS, no basis was more
useful than the other for predicting bird species composition
and even PSC in our study. This follows two realizations: 1)
despite the vast quantities of data obtained from LiDAR,
simple metrics such as canopy height are often strong
correlates of more complex metrics such as vertical vegetation
density (Jakubowski et al. 2013, Roussel et al. 2017); and 2)
metrics, such as the penetration ratios, serve as proxies for
in situ measurements of horizontal vegetation density. This
expresses the intrinsic gross structural relationships of forest
habitats that are expected along successional pathways and
supports that utility of advanced remote sensing technolo-
gies to efficiently describe VS (Falkowski et al. 2009). Why
VS did not capture PSC better could have resulted from a
high incidence of stands composed of similar gross structures
amid an overall more pronounced floristic gradient along the
successional pathway in the data set. Here, to some degree,
subtle compositional gradients do not appear to result in
aggregate structural change for certain plant assemblages
detectable by gross VS. For example, predictions based on VS
failed to partition the sparsely-treed stands, particularly open
floodplains and regenerating clear-cuts, from one another,
which are expected to function differently and host different
avian assemblages. These otherwise structurally-similar, albeit
floristically-different, habitats were closely related according
to their quantified structure, which resulted in weak predic-
tions of their corresponding avian assemblages as constrained
by VS. Additionally, predictions of avian species composition
by VS failed to distinguish mixed-oak and mesophytic for-
est types (noted by the overlap in ELT ellipses in Fig. 5),
which can be a strong determinant of avian community
structure (Rodewald and Abrams 2002). This largely follows
the misinterpretation in the traditional view of the impor-
tance of VS addressed by other authors that implies a cer-
tain degree of functional-redundancy in tree species as long
9
 35

height (m)
Canopy
20

StructureLiDAR, [L]
Bird composition, [B]
2
a Acadian Flycatcher (Empidonax virescens)
b American Crow (Corvus brachyrhynchos)
c American Goldfinch (Spinus tristis)
d American Redstart (Setophaga ruticilla)
1

11__55
e American Robin (Turdus migratorius)
y
f Baltimore Oriole (Icterus galbula) J

ppeenn
g Black−and−white Warbler (Mniotilta varia) O 00
h Blue−gray Gnatcatcher (Polioptila caerulea) T ppeenn22_ s 22__11
i Brown−headed Cowbird (Molothrus ater) n _5500 v BH I
w ppeenn
Q o bz giL U

CCA2
j Blackburnian Warbler (Setophaga fusca) 0 q xk P
RNSa de r chm
C f p Dh K vveech m_mea
E _mea
cchm

ppee
k Blue Jay (Cyanocitta cristata) O ggE
l Brown Thrasher (Toxostoma rufum) A
l c F
u
V
j G E hm m__ vveenn
t mmaa
m Black−throated Green Warbler (Setophaga virens) xx

cchhm
n Blue−winged Warbler (Vermivora cyanoptera) s
−1

m__s
o Carolina Chickadee (Poecile carolinensis) Iw ppee M
5500

sttdd
p Carolina Wren (Thryothorus ludovicianus)
v iB H
q Cedar Waxwing (Bombycilla cedrorum) U
LPRN
r Cerulean Warbler (Setophaga cerulea) b a e r
z q D kg S
s Chipping Sparrow (Spizella passerina) −2 x
h d
t Common Yellowthroat (Geothlypis trichas) K
f p
u Eastern Phoebe (Sayornis phoebe)
v Eastern Towhee (Pipilo erythrophthalmus) V
w Eastern Wood−Pewee (Contopus virens) E
x Eastern Tufted Titmouse (Baeolophus bicolor) −3 F j G
Field Sparrow (Spizella pusilla)
u
y
z Great Crested Flycatcher (Myiarchus crinitus)
A Gray Catbird (Dumetella carolinensis)
−3 −2 −1 0 1 2 5 20 35
B Hooded Warbler (Setophaga citrina)
C Indigo Bunting (Passerina cyanea) Canopy
D Kentucky Warbler (Geothlypis formosa) CCA1 height (m)
E Louisiana Waterthrush (Parkesia motacilla)
F Northern Cardinal (Cardinalis cardinalis)
G Northern Parula (Setophaga americana)
H Ovenbird (Seiurus aurocapilla) 35
height (m)

I Pine Warbler (Setophaga pinus)

Canopy

J Prairie Warbler (Setophaga discolor)

K Rose−breasted Grosbeak (Pheucticus ludovicianus) 20
L Red−eyed Vireo (Vireo olivaceus)
M Red−winged Blackbird (Agelaius phoeniceus)
N Scarlet Tanager (Piranga olivacea) 5
O Summer Tanager (Piranga rubra)
P White−breasted Nuthatch (Sitta carolinensis)
Q White−eyed Vireo (Vireo griseus) StructureField, [F]
R Worm−eating Warbler (Helmitheros vermivorum) 2
S Wood Thrush (Hylocichla mustelina)
T Yellow−breasted Chat (Icteria virens)
U Yellow−throated Vireo (Vireo flavifrons)
eenn

V Yellow−throated Warbler (Setophaga dominica)

__dd

1
m
eem

ccaann
sstt

__hhee f
ll__

iigg__m
meea q s
aall

a m K D
zp j l
d F
O C Q
0 can_covr_mea r aw
can_covr_mea S
R
P
N g uv
BixM TJ
CCA2

e EULhk c t
G H b Ao n
ee

Ridgetops and southwestern bbaass I f

sstt

emm__ V
ll__

__sstte q
aall

hillslopes points −1
bbiig
g K
D
m
Northeastern hillslopes points d zp
j
F
O l
r v C
Bottomlands points mea
mea PBi xgMu
SR
awEUN h
e HL k t
StructureLiDAR, [L] vectors −2
G
c
A o
b
StructureField, [F] vectors s
I V
−3

−2 −1 0 1 2 3 4 5 20 35
Canopy
CCA1 height (m)

Figure 5. Regular canonical correspondence analysis ordination diagrams of bird species composition constrained by either LiDAR-
(StructureLiDAR, [L]) (top) or field-derived (StructureField, [F]) (bottom) vegetation structural predictor sets (see Supplementary material
Appendix 2 for variable descriptions).

10
their replacement by another species does not impart changes
to the structural configuration of vegetation (Holmes et al.
1979, Holmes and Robinson 1981, Fleishman et al. 2003).
It is possible that higher density LiDAR data could have pre-
dicted PSC better (Müller et al. 2010). However, in applica-
tion, it may be possible to overestimate the importance of
gross VS if such metrics characterize PSC so closely that they
are entirely redundant with PSC. In such case, predictions
could be falsely attributed to VS when in fact they are cap-
turing a floristic signal more closely, considering if species-
specific growth form and leaf architecture are detectable with
high-resolution remote sensing data. In total, however, in
situ measurement of PSC provided the best explanation of
bird species composition in this study, demonstrating that
this vegetation dimension should be explicitly considered, no
matter the means used, when examining avian assemblage
composition.
It was not our intention to combine environmental
parameters with VS. However, combining VS with ELT had
little effect on the predictive accuracy of bird species compo-
sition for the LiDAR- (7.31% fit) and field-derived (6.71%
fit) data sets in a post hoc examination, expecting that the
inclusion of ELT data could help to characterize PSC that VS
alone could not. However, these results suggest that the com-
bination of VS and landscape position does not provide the
information necessary for accurate predictions of bird species
composition as does highly-detailed PSC data. While ELT
data are suitable for generalizing PSC into syntaxonomic
units, avian assemblages appear to respond more closely
to subtle compositional gradients apparent among stands
of similar units. This is because PSC likely unfolds along a
continuum in topo-edaphic gradients rather than arbitrary
breaks in topographic contours. Moreover, the presence of
the ELT gradient, thus, likely emerged because of individual
plant species response rather than a direct determinant of
bird species.
These techniques support the power of PSC for the
prediction of arthropod assemblages as well (Schaffers et al.
2008, Gioria et al. 2010, Nyafwono et al. 2015). The strong
correspondence between arthropod and plant assemblages
could also explain much of the variation in direct floristic
effects likely occurring in this study, being that arthropods
make up a large portion of avian diets during the breeding
period (Rotenberry 1985, Holmes and Schultz 1988,
Gunnarsson et al. 2018). In another case examining predic-
tions by PSC and VS in a Bavarian forestland, VS emerged as
the best predictor of bird species composition (Müller et al.
2010). The difference in predictive powers based on tree/
shrub PSC between studies is particularly noteworthy
(1.91% versus 11.22%). These differences suggest that the
factors that underpin compositional turnover of avian assem-
blages may depend partly on the floristic variation, and, most
importantly, functional significance of individual plant spe-
cies within different forest ecosystems (Gabbe et al. 2002,
Muiruri et al. 2016). Indeed, considerable evidence for spe-
cies-specific preferences for certain tree species comes from
work in temperate forestlands (Holmes and Robinson 1981,
Robinson and Holmes 1982, Gabbe et al. 2002, Wood et al.
2012). This aspect could be missing in less diverse for-
ests in which VS alone may be most important in leverag-
ing competitive interactions among different bird species
(MacArthur 1958).
Examining the three PSC predictor matrices, we found
interesting support for the shrub layer ([S]) in comparison
to trees ([T]). This is not surprising, considering that many
forest bird species in our study area forage and nest among
the lower strata and utilize a variety of shrub species as sea-
sonal resources throughout the breeding period (Vitz and
Rodewald 2007). Additionally, this size class was present
across all point samples (i.e. present in early- and late-seral
stands) and likely presented greater potential for synthesizing
VS, as the different understory species respond to variation
in light regimes determined by canopy structure and open-
ness (Müller et al. 2010). In total, however, both stem size
classes ([A]) provided the best prediction of avian assemblage
composition, suggesting that total woody PSC is necessary
when evaluating resource use of bird species.
We demonstrate that statistical methods that account for
the total species composition of vegetation can provide novel
insight into the factors that support local avian assemblages.
The underappreciation for PSC has likely manifested from the
simplification of compositional data into univariate descrip-
tors (Rotenberry 1985). In furthering the debate, it is critical
to consider the multiple interacting processes that underpin
patterns in avian assemblages. Despite recognizing the associ-
ation between VS and PSC, these factors have generally been
considered rather separate. Our results support a perspective
in which variation in bird species composition and VS mani-
fests from PSC that otherwise unfolds along environmental
gradients and successional pathways. Most importantly, PSC
occupies a key position in determining and describing this
variation. Thus, PSC, being an important integrative indi-
cator, has great potential for explaining avian assemblages
at local scales in temperate forestlands (Rotenberry 1985,
Wiens et al. 1987, Mac Nally 1990, Fleishman et al. 2003).
In addition, our synthesis suggests that such relationships may
be context-dependent, contingent on the degree of functional
significance of individual tree species, notably in the presence
of diverse hardwood assemblages. While VS has proven to be
a strong generalizable framework in assessing avian–habitat
relationships and understanding of the ecological separation
of species, PSC harbors a practical synthesizing character,
accounting for the many decisive factors that determine fau-
nal resource use, including VS. Finally, plant species per se
do indeed support considerable faunal niche space, consider-
ing the strength in the relationship between avian and plant
assemblages, and that VS, being an emergent property of PSC
in most forests, is only one piece of the puzzle.
Acknowledgements – We thank Kaley Donovan, James Hanks,
Garrett Evans, Sara Zaleski, Alex Eberts and Daniel Hodges for
their field assistance. We thank Laura Kearns, Louis Iverson, Robert
Gates and Christopher Tonra for their input on early versions of
the manuscript.
11
Funding – This study was funded by the State Wildlife Grants
Program, administered jointly by the US Fish and Wildlife Service
and the Ohio Division of Wildlife, through the Ohio Biodiversity
Conservation Partnership. Additional support was provided by the
School of Environment and Natural Resources and the Terrestrial
Wildlife Ecology Laboratory at The Ohio State University.
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