Journal of Field Ornithology
J. Field Ornithol. 84(1):1–12, 2013
DOI: 10.1111/jofo.12000
Microhabitat associations of terrestrial insectivorous
birds in Amazonian rainforest and second-growth forests
Jeffrey A. Stratford1,3 and Philip C Stouffer2
1
2
Department of Health and Biological Sciences, Wilkes University, Wilkes-Barre, Pennsylvania 18766, USA
School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, Louisiana
70803-6202, USA
Received 12 January 2012; accepted 29 October 2012
ABSTRACT. Across the Neotropics, small-bodied terrestrial insectivores are sensitive to forest fragmentation
and are largely absent from second-growth forests. Despite their sensitivity to forest structure, the microhabitat
relationships of these birds have not been quantified. From July 1994 to January 1995 in central Amazonia, we
characterized habitat at sites where nine species of terrestrial insectivores were observed foraging, as well as at
randomly selected sites in continuous forest and two types of 10–15-yr-old second-growth forest common in
Amazonia (Vismia- and Cecropia-dominated). We used factor analysis to find suites of correlated variables. From
each factor, we selected a representative variable that was relatively easy to measure. We used Bayesian analysis to
estimate means and standard deviations of these variables for each species and for each type of habitat. All nine
focal species were associated with ranges of microhabitat variables, such as leaf litter depth and tree densities, often
absent in second-growth forests. At least in the early stages of regeneration, neither type of second-growth forest
provides suitable structure for the terrestrial insectivores in our study. The large leaves of Cecropia trees that make
up the thick leaf litter may preclude the use of Cecropia-dominated second growth by our focal species, many of
which manipulate leaves when foraging. The leaf litter in Vismia-dominated second growth was also thicker than
sites used for foraging by our focal species. In addition, Vismia-dominated growth had more small trees and small
nonwoody vegetation, perhaps impeding movement by terrestrial birds. In continuous forest, our focal species
foraged in microhabitats with characteristics that generally overlapped those of randomly selected sites. Thus, our
results are consistent with the hypothesis that microhabitat differences make second-growth forests unsuitable for
our focal species.
RESUMEN. Asociación de aves insectı́voras terrestres con el micro hábitat en la selva
Amazónica y bosques de crecimiento secundario
A lo largo del Neotropico, aves insectı́voras terrestres de tamaño corporal pequeño son sensibles a la fragmentación
del bosques y en gran parte están ausentes en los bosques de crecimiento secundario. A pesar de su sensibilidad
a la estructura del bosque, las relaciones de estas aves con el micro hábitat no han sido cuantificadas. Desde
julio de 1994 hasta enero de 1995 en la Amazonia central caracterizamos hábitats en lugares en donde nueve
especies de aves insectı́voros terrestres fueron observadas buscado alimento, al igual que en lugares seleccionados
aleatoriamente en un bosque continuo y en dos tipos de bosques secundarios de 10 y 15 años, comunes en la
Amazonia (Vismia-dominado y Cecropia-dominado). Usamos un análisis factorial para encontrar el conjunto de
variable que se correlacionaron. También usamos un análisis bayesiano para estimar el promedio y las desviaciones
estándar de estas variables para cada especie y cada tipo de hábitat. Las nueve especies focales se asociaron con
elementos variables del micro hábitat, tales como profundidad de la hojarasca y densidad de arboles, usualmente
ausentes en bosques de crecimiento secundario. Al menos en los estadios tempranos de regeneración ninguno de los
tipos de crecimiento secundario provee una estructura adecuada para los insectı́voros terrestres de nuestro estudio.
Las largas hojas de los arboles de Cecropia que crean una hojarasca mas gruesa pueden evitar el uso de bosques de
crecimiento secundario dominado Cecropia por parte de nuestras especies focales, muchas de las cuales manipulan
hojas cuando están buscando alimento. La hojarasca de los bosques de crecimiento secundario dominados por
Vismia también fue mas gruesa respecto a los lugares usados por nuestras especies focales para buscar alimento.
Adicionalmente, los bosques dominados por Vismia tuvieron mas arboles pequeños y pequeña vegetación no leñosa,
que puede impedir el movimiento de las aves terrestres. En bosques continuos, nuestras especies focales buscaron
alimento en micro hábitats con caracterı́sticas que generalmente se superpusieron con las de los lugares escogidos
aleatoriamente. En consecuencia, nuestros resultados son consistentes con la hipótesis que diferencias en micro
hábitat hacen que los bosques de crecimiento secundario sean lugares inadecuados para nuestras especies focales.
Key words:
Conopophaga, Corythopis, Formicarius, Grallaria,habitat selection, Hylopezus, microhabitat,
Myrmornis, Myrmothera, terrestrial insectivores, vegetation structure
Studies of Neotropical birds have revealed that
most small-bodied terrestrial insectivores are
sensitive to forest fragmentation (Stouffer and
Bierregaard 1995, Robinson 1999, Stratford
3
Corresponding author. Email: jeffrey.stratford@
wilkes.edu
C 2013
C 2013 Association of Field Ornithologists
The Authors. Journal of Field Ornithology 1
2
J. A. Stratford and P. C. Stouffer
and Stouffer 1999). Other studies have confirmed the sensitivity of terrestrial insectivores
to fragmentation (Kattan 1992, Renjifo 1999,
Sekercioglu et al. 2002, Lees and Peres 2010),
selective logging (Mason 1996, Aleixo 1999,
Bicknell and Peres 2010), and other forms of
habitat modification such as plantations (Canaday 1997, Barlow et al. 2007). In addition,
most Neotropical insectivorous birds are rarely
found in young (<15 yr) second growth (Borges
and Stouffer 1999, Blake and Loiselle 2001)
that initially develops when deforested areas are
abandoned (Borges and Stouffer 1999, Wright
and Muller-Landau 2006). However, as second
growth ages, terrestrial insectivores are more
likely to move through it (Blake and Loiselle
2001, Antongiovanni and Metzger 2005). For
example, temporal changes in the abundance
of birds in fragments of Brazil’s Biological Dynamics of Forest Fragments Project (BDFFP)
were found to be strongly influenced by the age
and type of second-growth matrix surrounding
the fragments (Stouffer and Bierregaard 1995,
Stouffer et al. 2006, 2011). Fragments surrounded by Cecropia-dominated second growth
regained more species of birds lost after fragmentation than fragments surrounded by Vismia-dominated second growth (Stouffer and
Bierregaard 1995). The area consisting of second growth is rapidly expanding across the
Amazon (Neeff et al. 2006, Foley et al. 2007),
and understanding how terrestrial insectivores
respond to the different types and ages of second
growth is crucial to their conservation (Antongiovanni and Metzger 2005, Gardner et al. 2007,
Chazdon 2008).
Several hypotheses have been proposed to
explain why terrestrial insectivores are sensitive
to alteration of forest structure (Stratford and
Robinson 2005). One hypothesis is that terrestrial insectivores are closely associated with a
particular forest physiognomy and topography
and, if key elements are missing, terrestrial insectivores avoid these areas (Stratford and Robinson
2005). This hypothesis is difficult to test because
the microhabitats (physiognomy) used by most
terrestrial insectivores have yet to be evaluated,
with microhabitat defined as a subset of habitat
(e.g., continuous forest) with particular environmental conditions, including vegetation structure (James 1971). Due to microhabitat preferences, areas within broadly suitable habitat may
go unused for a particular species. Understand-
J. Field Ornithol.
ing such microhabitat associations is necessary
for predicting responses to forest fragmentation,
selective logging, and other activities that alter
forest structure (Holmes and Robinson 1981,
Deppe and Rotenberry 2008).
Our objective was to provide a quantitative
description of the microhabitat associations of
nine species of terrestrial insectivores in a wellstudied Amazonian forest. By comparing the
characteristics of microhabitats where birds forage to those of randomly selected sites in continuous forest and second-growth sites, we can
gain a better understanding of habitat selection
by terrestrial insectivores. Typical of microhabitat studies, we quantified several microhabitat variables that we believed were potentially
important to terrestrial insectivores. However,
collecting these data took considerable time and
effort so a secondary objective was to identify a
reduced set of variables to recommend for use in
future studies of these species.
METHODS
Study sites. From July 1994 to January
1995, we collected microhabitat data at sites that
were part of the BDFFP, a large-scale, long-term
research project sponsored by the Smithsonian
Tropical Research Institute and Brazil’s National
Institute for Amazon Research (Bierregaard and
Gascon 2001). The continuous forest site is
located in terra firme forest ∼60 km north of
Manaus, Brazil (see http://pdbff.inpa.gov.br/ for
maps). Annual rainfall averages 2500 mm with
a distinct rainy season from February to May
(Stouffer and Bierregaard 1993). Soils in the
area are sandy and nutrient poor (Laurance et al.
1999), but tree diversity is exceptionally high
(Oliveira and Mori 1999). At the continuous
forest site, canopy height varied, but is typically
between 30 and 37 m (Gascon and Bierregaard
2001). Lianas and vines are common (Roeder
et al. 2010) and the understory is dominated by
palms such as Astrocaryum spp. and Bactris spp.
(Scariot 1999, de Castilho et al. 2006). Small
streams, often with steep banks, dissect the area.
Higher, flat areas or plateaus are found between
streams (Bueno et al. 2011, Cintra and Naka
2012). Isolated treefalls and blowdowns occur
sporadically throughout the site (Nelson et al.
1994). The continuous forest site is embedded
within a large forest that is largely intact for
hundreds of kilometers with the exception of
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Microhabitats of Amazonian Insectivores
Manaus, a large urban center. A gridded trail
system was set up at the continuous forest site
with parallel trails spaced every 100 m.
The BDFFP study area includes large patches
of second growth (see map in Stratford and
Stouffer 1999). Most of the second growth is
one of two types that are largely distinct in the
early stages of regeneration (Norden et al. 2011).
Patches of second growth we sampled were
10–15 yr old. At this age, Cecropia dominates
areas that were cut and abandoned, whereas
Vismia-dominated second growth occurs where
the forest was burned before abandonment
(Mesquita et al. 2001). Floristically, Cecropiadominated second growth has more plant
species and families than Vismia-dominated areas (Mesquita et al. 2001).
Bird and vegetation sampling. Our focal species were terrestrial insectivores with
a range of responses to fragmentation and
second-growth forest (Borges and Stouffer 1999,
Stratford and Stouffer 1999; Table 1). Sensitivity to fragmentation was determined by
the probability that a species will go locally
extinct after fragmentation (Stratford and Stouffer 1999). We sampled three fragmentationsensitive species that were missing from all or
most BDFFP fragments and that did not use
second-growth forest (Wing-banded Antbirds,
Myrmornis torquata, Variegated Antpittas, Grallaria varia, and Spotted Antpittas, Hylopezus macularius), five moderately sensitive species missing from small BDFFP fragments and that rarely use second-growth
forest (Ferruginous-backed Antbirds, Myrmeciza ferruginea, Rufous-capped Antthrushes,
Formicarius colma, Black-faced Antthrushes,
Formicarius analis, Chestnut-belted Gnateaters,
Conopophaga aurita, and Ringed Antpipits,
Corythropis torquatus), and Thrush-like Antpittas (Myrmothera campanisona), a fragmentationtolerant species found in fragments of all sizes
as well as in second-growth forest. Our focal species are present in continuous terra
firme forest throughout the BDFFP (Cohn-Haft
et al. 1997, Stouffer 2007).
Most birds were observed while we opportunistically spot-mapped a 500-ha plot in the
gridded trail system at the continuous forest site
(Stouffer 2007). Trails followed compass bearings, passing through the various topographic
elements in the area, including stream beds,
steep stream banks, and flat plateaus. Micro-
3
habitats were sampled only where birds were
observed foraging and, to avoid sampling areas
used by the same individuals, we only considered
individuals observed >500 m from a previous
observation of a bird of the same species. The
site of each initial observation served as the
center of an 8-m-radius (∼0.02 ha) vegetation
sampling plot. We chose 8-m radius sampling
units as a compromise between being consistent
with published methods, i.e., James and Shugart
(1970) and Marra and Remsen (1997) used 10m-radii sample units, and our desire to finely
quantify foraging microhabitat used by our focal
species. In addition, small-scale sampling units
can capture the vegetation structure associated
with the edges and interiors of treefalls in tropical forests (Fetcher et al. 1985, Uhl et al. 1988).
We quantified vegetation using a modified
version of methods described by James and
Shugart (1970). Within each plot, we measured
23 variables to quantify vegetation structure
and topography. For topography, we noted if
the center of a plot was in a stream bed (flat
areas adjacent to running water) or on a stream
bank (signs of flooding, such as leaf packs),
dry slope (no signs of flooding), or flat plateau
(higher areas with no slope). Due to small sample
sizes, plots were later categorized as simply either
riparian (stream beds and their occasionally
flooded banks) or upland (unflooded slopes and
the higher elevation plateaus). In each plot, we
counted all trees (woody vegetation > 2 m in
height) and categorized them into five size classes
based on diameter at breast height (dbh): trees
≤ 7 cm, trees > 7–15 cm, trees > 15–23 cm,
trees > 23–30 cm, and trees > 30 cm. There
were few trees >15 cm in plots and histograms
of counts per plot were highly skewed, so we
used three size classes of trees for analysis: small
trees (dbh ≤ 7 cm), medium trees (dbh > 7–15
cm), and large trees (dbh > 15 cm). We did not
identify tree species because tree diversity at our
site is exceptionally high, with more than 200
species/ha and perhaps as many as 1000 species
in the area (Prance 1990, Rankin-de-Mérona
et al. 1992). We also counted all palms (Arecaceae) >1 m in height, and woody vines in three
size classes: vines > 0–0.5 cm dbh, vines > 0.5–
2 cm dbh, and vines > 2 cm dbh. We found
few vines >0.5 cm dbh, and their histograms
of counts per plot were highly skewed, so we
combined the two larger size classes of vines into
large vines (dbh > 0.5 cm). After consolidating
4
J. A. Stratford and P. C. Stouffer
J. Field Ornithol.
Table 1. Morphological and behavioral attributes of the nine focal species. We also indicate fragmentation
sensitivity, or the probability that a species will go locally extinct after fragmentation. Species that are
fragmentation-sensitive will be missing from all fragments, including those ≥ 100 ha in size. Moderately
sensitive species will be missing from the smallest forest fragments, and species that are not sensitive will
be found in fragments of all sizes. Occurrence of each species in second-growth forest was based on Borges
(1995).
Mass Fragmentation
(g)b
sensitivity
Species
Na
Myrmeciza ferruginea
23
26
Moderate
Ferruginous-backed Antbird
Myrmornis torquata
12
47
Yes
Wing-banded Antbird
Formicarius colma
17
47
Moderate
Rufous-capped Antthrush
Formicarius analis
12
62
Moderate
Black-faced Antthrush
Grallaria varia
4
119
Yes
Variegated Antpitta
Hylopezus macularius
3
44
Yes
Spotted Antpitta
Myrmothera campanisona
8
47
No
Thrush-like Antpitta
Conopophaga aurita
4
27
Moderate
Chestnut-belted Gnateater
Corythropis torquatus
13
14
Moderate
Ringed Antpipit
a
N = number of sites where each species was observed foraging.
b
From Dunning (1992).
c
Based on Ridgely and Tudor (1994).
these variables, we entered 15 variables into the
factor analysis (Table 2).
In each vegetation plot, an 8-m transect was
established from the center of the plot to the
edge in a random direction and a second 8-m
transect was established by subtracting 90◦ from
the original transect. The first direction was
selected from a random number table (Rohlf and
Sokal 1981). All nonwoody plants within 0.5 m
of transects (i.e., herbs, grasses, and ferns) as well
as all woody stems <2 m in height were counted
and placed into two height categories: short
plants (height ≤ 1 m) and tall plants (height >
1–2 m). The total area sampled for plants in
plots was 15.75 m2 . Along the entire length of
transects, 20 points were randomly selected from
a random number table and, at each point, we
measured leaf litter depth, counted the number
of dead leaves, and noted the presence or absence
of live vegetation at five heights: <0.5 m, >0.5–
3 m, >3–10 m, >10–20 m, and >20 m. For
heights <0.5 m, we determined the presence or
Occurs in
second growth
Cecropia
Foraging
strategyc
Surface of leaf litter
Cecropia
Tosses litter
Both
Surface of leaf litter
No
Surface of leaf litter
Cecropia
Cecropia
Surface of leaf litter,
under leaf litter
Surface of leaf litter
Cecropia
Surface of leaf litter
No
Surface of leaf litter
Vismia
Undersides of leaves
absence of live vegetation if vegetation touched
a 1.27-cm-diameter pole with one end placed
directly on the sample point. Between 0.5 and
3 m, we determined the presence of vegetation
if any part of a live plant crossed over an
imaginary line running directly up from the
sample point. Above 3 m, we used a rangefinder
to determine heights and sighted through a tube
with crosshairs. Three evenly spaced hanging
weights were placed inside the tube to vertically
align the tube while the observer straddled the
point. Where leaf litter depth was <3 cm deep,
a pin (38 mm × 0.55 mm) was used to pierce
leaves until the pin touched soil. The pin was
then removed and the depth of the leaf litter
was measured to the nearest 0.1 mm with digital
calipers. We also counted the number of leaves
the pin pierced. When leaf litter was >3 cm
deep, we used a 150 mm × 1 mm pin at the
back end of a dial caliper created by opening
dial calipers. The pin was pressed through the
leaves until it touched soil.
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Microhabitats of Amazonian Insectivores
Table 2. Results of factor analysis to identify suites
(factors) of correlated variables for sites where birds
were observed foraging and randomly selected sites.
We included all 208 samples, including random sites
in continuous and second-growth forest and sites
where focal species of birds were observed foraging.
Bolded numbers in the same column represent variables with loadings >0.50 onto a factor. Underlined
variables are those included in the Bayesian analysis.
Removed from the factor analysis were leaf litter
depth, trees > 7–15 cm dbh, large vines, number
of Vismia stems, and number of Cecropia stems.
Variablea
Factor1
Factor2
Factor3
LEAFNO
0.538 −0.221
−0.044
COVHALF
−0.912 −0.160
0.113
COVER10
0.584
0.105
0.201
COVER20
0.625
0.430
0.119
−0.013
PLANTS1
−0.858 −0.210
COVER20+
0.065
0.798
0.064
0.164
LGTREE
0.119
0.838
PALMS
0.131
0.818
0.113
COVER3
−0.088
0.171
0.504
PLANTS2
−0.114
0.087
0.625
SMTREE
0.359
0.254
0.779
SMVINE
0.290 −0.278
0.537
SS loadings
2.856
2.502
1.653
Proportion Var
0.238
0.208
0.138
Cumulative Var
0.238
0.446
0.584
a
LEAFNO: number of dead leaves penetrated by
a pin; COVHALF: presence or absence of live
vegetation < 0.5 m above ground; COVER10:
presence or absence of live vegetation > 3–10 m
above ground; COVER 20: presence or absence of
live vegetation > 10–20 m above ground; PLANTS1:
number of plants ≤ 1 m tall; COVER20+: presence
or absence of live vegetation > 20 m above ground;
LGTREE: number of trees with dbh > 15 cm;
PALMS: number of palms > 1 m tall; COVER3:
presence or absence of live vegetation > 0.5–3 m
above ground; PLANTS 2: number of plants > 1–2
m tall; SMTREE: number of trees with dbh ≤ 7 cm;
and SMVINE: number of vines with dbh ≤ 0.5 cm.
We also sampled randomly selected points
in continuous forest (N = 44) and in both
Vismia- (N = 40) and Cecropia-dominated
(N = 28) second-growth forest. Vismia- and
Cecropia-dominated second growth occurred in
large (>200 ha) patches in abandoned pastures
between 18 and 38 km from the continuous
forest site. Second-growth areas were in pastures
abandoned for 10–15 yr and had vegetation
at least 2 m in height. To sample vegetation
5
in areas of second growth, we located plots
at random distances along 500-m trails and
random distances within 100 m of the trails.
Trails in second growth were 500 m apart and
were created to sample avian communities in
secondary growth (Borges and Stouffer 1999).
To determine the location of points in continuous forest, we randomly selected an intersection in the gridded system of trails that runs
north–south and east–west. From the intersection, we randomly selected a point within 100 m
north and 100 m east.
Statistical analysis.
Using R 2.11.1 (R
Development Core Team 2010), we used factor
analysis of the vegetation variables to identify suites (factors) of correlated (redundant)
variables for sites where birds were observed
foraging and randomly selected sites. We started
with six factors and reduced the number until
each factor had at least two variables loading
(>0.45) on each factor (Hair et al. 2010). The
variables leaf litter depth and medium trees
were removed from the analysis because they
loaded on the first two and the second and
third factors, respectively. One variable (large
vines) was removed from the final factor analysis
because it did not load on any of the factors
(Hair et al. 2010). From each factor, we selected
a single representative variable that could be
easily and accurately measured in the field. We
decided to select the variables small plants, large
trees, and small trees from the three factors for
subsequent analysis.
We used Bayesian inference to estimate
means, standard deviation, and Bayesian 95%
credible intervals (Gelman et al. 2003) of the
selected subset of variables (small plants, large
trees, and small trees) and variables removed
from the factors (leaf depth, medium trees, and
large vines). We used OpenBUGS 3.2.2 (Lunn
et al. 2000) for all Bayesian analyses. For count
variables, we assumed a Poisson distribution of
each observation, but allowed for extra variation around the Poisson mean. For continuous
variables, we assumed a normal distribution
for each observation. We assumed estimates
of group means were normally distributed and
used uninformative priors (␮ = 0, ␶ = 0.001),
where ␶ is precision and is the inverse of the
variance. We also used uninformative priors for
the estimates of group standard deviation. For
each estimate, we ran a million iterations with a
burn-in of 20,000. We estimated means,
6
J. A. Stratford and P. C. Stouffer
standard deviations, and 95% credible intervals
for plots where the study species were observed
foraging, for random sites in continuous forest,
and for random sites in both types of secondgrowth forest. Bayesian 95% credible intervals
can be interpreted as standard statistical tests
(Gelman et al. 2003). Means and standard deviations for the original variables using traditional
methods are available in Stratford (1997).
RESULTS
We quantified the characteristics of 96 sites
where our focal species were observed foraging
and 112 randomly selected sites (continuous
forest N = 44, Vismia second growth N =
40, and Cecropia second growth N = 28). All
observations of foraging birds were in continuous forest except for two Thrush-like Antpittas
observed in Cecropia-dominated sites.
Factor analysis was able to capture 58% of
the total variance in the vegetation data in
three factors (Table 2). The first factor was
associated with the ground and midstory layers
and accounted for 24% of the total variance.
From this factor, we identified small plants as an
element of the ground layer that would be easy to
measure. The second factor was associated with
elements of the canopy and accounted for 21%
of the total variance. We selected large trees from
this factor as the variable that would describe
the canopy and was easy to measure. The third
factor was associated with the midstory and
accounted for 14% of the variance. From this
factor, we selected small trees as the variable
that would be easily measured and described the
midstory.
Microhabitats and topography in
second-growth versus continuous forest.
Riparian sites were found in all three habitats,
although second-growth areas had fewer than
the continuous forest (Fig. 1). The vegetation
structure of the two types of second growth
differed from that of continuous forest. Leaf
litter in Vismia- and Cecropia-dominated
second growth was ∼1 and 4 cm thicker,
respectively, than in continuous forest (Fig. 2A).
Structurally, Vismia-dominated second growth
had more small plants than either continuous
forest or Cecropia-dominated second growth
(Fig. 2B) and more small trees than Cecropiadominated second growth and continuous
forest (Fig. 2C). Vismia-dominated second
J. Field Ornithol.
growth also had fewer medium and large trees
and large vines than either continuous forest
or Cecropia-dominated second growth (Figs.
2D–F).
Compared to the continuous forest site,
Cecropia-dominated second growth had fewer
small plants, with just six small plants/transect
(Fig. 2B), but a similar number of small
trees (Fig. 2C) as continuous forest. Cecropia-dominated second growth also had more
medium trees than continuous forest sites
(Fig. 2D). Large trees were largely absent from
Cecropia-dominated second growth, with an
average of one large tree per sample. However, if
large and medium tree size classes were pooled,
there were similar numbers of trees in Cecropiadominated second growth (∼21 trees/plot) and
continuous forest (∼18 trees/plot).
Topography and microhabitats of sites
used by terrestrial insectivores.
Five of
the nine terrestrial insectivores (Rufous-capped
Antthrushes, Thrush-like Antpittas, Spotted
Antpittas, Variegated Antpittas, and Chestnutbelted Gnateaters) were only observed in upland
sites (Fig. 1). Black-faced Antthrushes were most
associated with riparian habitats, with nearly
one-third (0.31) of all observations in riparian
areas.
None of the 95% credible intervals for leaf
litter depth at sites where terrestrial insectivores
were observed exceeded those of random samples from continuous forest (Fig. 2A). None of
our nine focal species were observed foraging
at sites with leaf litter as thick as the leaf
litter in Cecropia-dominated second growth,
which was ∼4 cm thicker than the leaf litter
at sites where our focal species were observed
foraging. Ferruginous-backed Antbirds, Wingbanded Antbirds, Rufous-capped Antthrushes,
Black-faced Anttrushes, and Variegated Antpittas were observed foraging in areas with less
leaf litter than that in Vismia-dominated second growth (Fig. 2A). Leaf litter depths where
we observed Thrush-like Antpittas, Chestnutbelted Gnateaters, and Ringed Antpipits foraging overlapped the leaf litter depth in Vismiadominated second growth. Variation in leaf
litter depth where antpittas and Chestnut-belted
Gnateaters foraged was greater than that where
the other focal species foraged and at random
sites in continuous forest (Fig. 2A). Among our
focal species, only Ferruginous-backed Antbirds
and Thrush-like Antpittas differed from each
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Microhabitats of Amazonian Insectivores
7
Fig. 1. Proportion of sites that were riparian (water flowing or flooded) and upland (never flooded) for plots
in continuous forest, second growth or where the focal species were observed foraging.
other, with Thrush-like Antpittas foraging at
sites with deeper leaf litter than Ferruginousbacked Antbirds (Fig. 2A).
The numbers of small plants in random plots
in continuous forest sites and sites in Vismiadominated second growth overlapped with those
of the foraging sites of all focal species (Fig. 2B).
However, none of the sites where our focal
species were observed foraging had as few
small plants as the random plots in Cecropiadominated second growth. Variation in the
number of small plants at sites where we observed antpittas and Chestnut-belted Gnateaters
foraging was greater than that at sites where the
other focal species foraged and at random sites
in the three available habitats (Fig. 2B).
The number of small trees at sites where
our focal species foraged was similar to that
at randomly selected sites in the continuous
forest (Fig. 2C). There were more small trees
in Cecropia-dominated second growth than in
microhabitats used by the two antthrushes; otherwise, the number of small trees in Cecropiadominated second growth was similar to that at
sites used by our focal species. The number of
small trees in Vismia-dominated second growth
also exceeded the number of small trees at sites
used by Chestnut-belted Gnateaters, Ringed
Antpipits, and the two antthrushes. Sites where
the two species of antthrushes foraged had fewer
small trees than sites used by four other focal
species (Ferruginous-banded Antbird, Ringed
Antpipit, Thrush-like Antpitta, and Variegated
Antpitta).
Random sites in Vismia-dominated second
growth had far fewer medium trees than sites
where all the focal species were observed foraging
(Fig. 2D). For large trees, only sites where
Thrush-like Antpittas were observed foraging
had fewer large trees than random sites in
continuous forest (Fig. 2E). Foraging sites of
all nine focal species had more large trees than
randomly selected sites in either type of second
growth. However, the number of large vines at
sites where most of the focal species foraged
did not differ from that in the random sites in
continuous forest; the only exception was that
there were fewer large vines at sites where Ringed
Antpipits foraged (Fig. 2F). All sites where focal
species were observed foraging had more large
vines than random sites in Vismia-dominated
second growth.
In general, microhabitats available in secondary growth differed from those available
in continuous forest. The deeper leaf litter in
both types of second growth was a particularly
striking difference that may be directly relevant
to foraging by terrestrial birds; most of our
focal species preferred the shallower leaf litter
available in continuous forest (Fig. 2A). We
found a similar pattern with the number of large
trees, with most of our focal species preferring
areas of continuous forest with relatively high
numbers of large trees (Fig. 2E). Other variables
exhibited more variation among focal species,
and characteristics of sites used by our focal
species sometimes differed from one or both
types of second-growth forest.
8
J. A. Stratford and P. C. Stouffer
J. Field Ornithol.
Fig. 2. Bayesian estimates of means (circles), standard deviations (boxes), and credible intervals (vertical lines)
for (A) leaf litter depth, (B) plants ≤ 1 m tall, (C) small trees (dbh ≤ 7 cm), (D) medium trees (dbh >
7–15 cm), (E) large trees (dbh > 15 cm), and (F) large vines (dbh > 0.5 cm) at sites where nine species of
terrestrial insectivores were observed foraging and at randomly selected sites in the three types of available
habitat (continuous forest and Cecropia- and Vismia-dominated second growth). Dotted horizontal lines show
the upper and lower bounds of the standard deviations for randomly selected sites in the continuous forest
sites for comparison with sites where birds were observed foraging and randomly selected sites in Vismia- and
Cecropia-dominated second growth.
Vol. 84, No. 1
Microhabitats of Amazonian Insectivores
DISCUSSION
We found that most microhabitat characteristics of sites where our nine focal species
of Neotropical terrestrial insectivores foraged
broadly overlapped those of randomly selected
sites in continuous forest. However, our focal
species foraged in microhabitats that differed
from those in second-growth forest in several
respects, including leaf litter depth, density of
small plants and trees, and density of large
trees. Our focal species are generally absent from
second-growth areas (Borges and Stouffer 1999)
and our results are consistent with the hypothesis that microhabitat differences make secondgrowth forests unsuitable for our focal species.
In particular, the thick leaf litter of Vismia- and
Cecropia-dominated second growth may interfere with normal foraging behaviors. Although
Stouffer and Bierregaard (1995) and Borges and
Stouffer (1999) found that our focal species may
use Cecropia-dominated second growth more
readily than Vismia-dominated second growth,
Cecropia leaves are typically 30–40 cm across
(Parolin 2002) and their presence in the leaf
litter may impede foraging behavior or even
terrestrial movement. This would be particularly
true for species that forage by actively tossing leaf
litter, such as Wing-banded Antbirds. Ringed
Antpipits, which glean from live leaves as they
walk, may also find Cecropia-dominated second
growth suboptimal for foraging because plants <
1 m in height were sparse in this habitat.
Our focal species may also avoid secondgrowth forests due to microclimate conditions
that are correlated with vegetation structure
or edaphic conditions. For example, Karr and
Freemark (1983) found that understory birds
in Panama were associated with specific microclimate conditions and changed their use
of the forest during the year, indicating the
relative importance of microclimate compared
to vegetation. In the tropics, the near-ground
microclimate of second-growth forests is both
hotter and drier than that in continuous forests
(Fetcher et al. 1985, Uhl and Kauffman 1990),
and such environmental conditions may exceed
the physiological tolerances of our focal species
(Stratford and Robinson 2005).
Microhabitat characteristics may also explain
why Thrush-like Antpittas, associated with large
treefalls in continuous forest (Stouffer 2007),
were able to use second-growth forests in our
9
study. Thrush-like Antpittas in our study preferred microhabitats that had dense understory
vegetation and fewer large trees, characteristics
typical of young treefall gaps (Fetcher et al.
1985). Thrush-like Antpittas are also found
in forest fragments and second growth; their
association with scrubbier vegetation in continuous forest may allow this species to persist
in fragmented landscapes, at least those that
include some forest and second-growth areas.
Compared to second growth, microhabitat
associations of our focal species in continuous
forest were more subtle, with more overlap in
the characteristics of foraging sites and randomly
selected sites. The density of small nonwoody
plants, for instance, was more variable at sites
used by our focal species than at randomly
selected sites, but reasons for such a difference
are unclear. The densities of medium and large
trees in plots where birds foraged were similar
among species and to those of randomly selected
sites in continuous forest. In addition, the leaf
litter depth at sites where our focal species
foraged was similar to that at randomly selected
sites in continuous forest. Our focal species
also preferred drier sites, which were available
throughout the continuous forest site.
The two antthrush species in our study were
associated with sites with fewer small trees,
whereas Variegated Antpittas and Ferruginousbacked Antbirds were associated with sites with
more small trees. For large vines, only sites used
by Ringed Antpipits differed from randomly
selected sites, using sites with relatively few large
vines. Although the reasons for these apparent
preferences are unclear, these subtle microhabitat associations might explain the patchiness
of distributions in continuous forest. Stouffer
(2007), for example, studied the same focal
species as in our study and found that they
were patchily distributed in the 100-ha plot
extensively searched in our study, with, on average, two-thirds of the study plot unoccupied by
particular species. In North American deciduous
forests, the distributions of terrestrial insectivores are closely tied to microhabitat features
(Holmes and Robinson 1988). In Neotropical
forests, terrestrial insectivores and other understory birds have been found to show preferences
for particular ranges of soil composition (Bueno
et al. 2011, Pomara et al. 2012), and topology
and forest structure (Marra and Remsen 1997),
which are potentially confounded (Cintra and
10
J. A. Stratford and P. C. Stouffer
Naka 2012). To better understand relationships
between microhabitat characteristics and the
distribution of terrestrial insectivores, experimental studies involving habitat manipulations
are needed. Habitat alteration caused by fires
and selective logging may, however, offer some
insight. Our focal species and other terrestrial
insectivores are known to be sensitive to the
impact of fire and low-intensity logging (Barlow
et al. 2002, 2006, Barlow and Peres 2004),
which may alter leaf litter depth and the density
of nonwoody plants, but have less of an impact
on the canopy.
A second objective of our study was to produce a smaller, more efficiently sampled set of
vegetation variables for use in future studies of
other terrestrial insectivores. From our initial
26 vegetation variables, we identified six that
captured the variation in vegetation structure.
Characterizing vegetation based on six variables
should significantly reduce the time needed to
sample each site, from the 1–2 h we required to
30 min or less. We are not suggesting that these
six variables actually determine if birds will be
present or absent, only that we identified vegetation characteristics associated with selection of
foraging habitat by the birds. More important
causal factors might be prey availability, foraging
efficiency, or predator avoidance, which are
influenced by vegetation structure. As long as
the correlative relationship between an easily
measured variable (such as the density of large
trees) is consistent with a causal factor (such as
prey density), measurement of vegetation structure is useful for describing essential elements
of the habitat that must be maintained for the
persistence of terrestrial insectivores. Because
our study species or their close relatives are
found throughout Neotropical rainforests from
Mexico to Argentina, we hope our approach
and results will be broadly applicable to their
conservation.
ACKNOWLEDGMENTS
We thank G. Rompre and M. Bugdal for helpful comments on the manuscript, M. Orme and M. McMarthy
for their help with analysis, and Flecha for many hours of
field assistance. The BDFFP is managed and supported
by the Instituto Nacional de Pesquisas da Amazônia and
the Smithsonian Institution. This is publication 607 of
the BDFFP Technical Series and 26 of the Amazonian
Ornithology Technical Series of the INPA Zoological
Collections Program. The manuscript was approved by
J. Field Ornithol.
the Director of the Louisiana State University Agricultural
Center as manuscript number 2012-241-7682.
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