Island vs. countryside biogeography: An examination of how Amazonian birds respond to forest clearing and fragmentation

Abstract

Avian diversity in fragmented Amazonian landscapes depends on a balance between extinction and colonization in cleared and disturbed areas. Regenerating forest facilitates bird dispersal within degraded Amazonian landscapes and may tip the balance in favor of persistence in habitat patches. Determining the response of Amazonian birds to fragmentation may be hindered because many species use adjacent second growth matrices thereby limiting the applicability of island biogeography to predict species loss; alternatively, a countryside biogeographic framework to evaluate the value of regenerating forest may be more appropriate. Here, we used point-count and capture data to compare Amazonian bird communities among continuous forest, 100 ha forest fragments with adjacent second growth, young and older second growth plots, and 100 ha forested islands bounded by water, to test the applicability of island biogeography on the mainland and to assess the ecological value of a regenerating matrix. Among foraging guilds, understory insectivores and flocking species were nearly absent on true islands. Fragments surrounded by young second growth were species rich, suggesting that a developing matrix may mitigate extinction associated with fragmentation. Our findings reinforce that true islands are often extinction driven systems with distinct, depauperate communities. In contrast, succession of bird communities in second growth facilitates recolonization of forest fragments, permitting fragments as small as 100 ha to support bird communities similar to continuous forest.

Full text

Island vs. countryside biogeography: an examination of how
Amazonian birds respond to forest clearing and fragmentation
JARED D. WOLFE,
1,2,3,4,
PHILIP C. STOUFFER,
1,4
KARL MOKROSS,
1,4
LUKE L. POWELL,
1,4
AND MARINA M. ANCIA
˜ES
5
1
School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, Louisiana 70803-6202 USA
2
USDA Forest Service, Pacific Southwest Research Station, Redwood Sciences Laboratory, Arcata, California 95521 USA
3
Klamath Bird Observatory, Ashland, Oregon 97520 USA
4
Biological Dynamics of Forest Fragments Project, Instituto Nacional de Pesquisas da Amazˆ
onia, Manaus 69011 Amazonas, Brazil
5
Coordena¸ca˜o de Pesquisa em Ecologia, Instituto Nacional de Pesquisas da Amazˆ
onia, Manaus 69011 Amazonas, Brazil
Citation: Wolfe, J. D., P. C. Stouffer, K. Mokross, L. L. Powell, and M. M. Ancia˜es. 2015. Island vs. countryside
biogeography: an examination of how Amazonian birds respond to forest clearing and fragmentation. Ecosphere
6(12):295. http://dx.doi.org/10.1890/ES15-00322.1
Abstract. Avian diversity in fragmented Amazonian landscapes depends on a balance between
extinction and colonization in cleared and disturbed areas. Regenerating forest facilitates bird dispersal
within degraded Amazonian landscapes and may tip the balance in favor of persistence in habitat patches.
Determining the response of Amazonian birds to fragmentation may be hindered because many species
use adjacent second growth matrices thereby limiting the applicability of island biogeography to predict
species loss; alternatively, a countryside biogeographic framework to evaluate the value of regenerating
forest may be more appropriate. Here, we used point-count and capture data to compare Amazonian bird
communities among continuous forest, 100 ha forest fragments with adjacent second growth, young and
older second growth plots, and 100 ha forested islands bounded by water, to test the applicability of island
biogeography on the mainland and to assess the ecological value of a regenerating matrix. Among foraging
guilds, understory insectivores and flocking species were nearly absent on true islands. Fragments
surrounded by young second growth were species rich, suggesting that a developing matrix may mitigate
extinction associated with fragmentation. Our findings reinforce that true islands are often extinction-
driven systems with distinct, depauperate communities. In contrast, succession of bird communities in
second growth facilitates recolonization of forest fragments, permitting fragments as small as 100 ha to
support bird communities similar to continuous forest.
Key words: Balbina; central Amazon; continuous forest; countryside biogeography; forest fragment; island
biogeography; second growth matrix; species richness; tropical bird.
Received 27 May 2015; revised 12 August 2015; accepted 17 August 2105; published 22 December 2015. Corresponding
Editor: D. P. C. Peters.
Copyright: Ó2015 Wolfe et al. This is an open-access article distributed under the terms of the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited. http://creativecommons.org/licenses/by/3.0/
E-mail: jdw@klamathbird.org
INTRODUCTION
The utility of island biogeography to predict
species loss within mainland habitat patches has
frequently been questioned (Mendenhall et al.
2012, 2014, Fahrig 2013). Criticism towards
applying the theory of island biogeography
(‘island model’hereafter) on the mainland stem
from variation in the hostility of the matrix,
where the surrounding landscape interspersed
between habitat patches are often more salubri-
ous than water surrounding true islands (Men-
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denhall et al. 2014). Differences in matrix
hostility, such as water (hostile) versus regener-
ating forest, determines how animals use and
disperse through the landscape, thereby resulting
in divergent biogeographic processes and differ-
ent rates of species loss in habitat patches. In fact,
the matrix surrounding remnant habitat patches
may even provide some ecological value to
wildlife which led Daily (1997) to suggest a
new theoretical framework, called ‘countryside
biogeography’, to study the diversity, abun-
dance, conservation and restoration of species
in human-dominated landscapes. More specifi-
cally, countryside biogeography recognizes that
many human-dominated landscapes are not
analogous to inhospitable bodies of open water
interspersed between islands of habitat—a nec-
essary assumption of the island model.
Countryside biogeography is particularly rele-
vant to tropical forest-dwelling birds that may be
dispersal limited and reliant upon human-dom-
inated matrices to maintain metapopulation
connectivity in heterogeneous landscapes (Seker-
cioglu et al. 2002). For example, Stouffer et al.
(2011) demonstrated that Amazonian forest birds
were able to disperse from source populations in
pristine habitat through a regenerating pastoral
matrix to recolonize previously depauperate
forest fragments, suggesting that species are lost
following isolation, but the trajectory of loss does
not continue downward when coupled with
matrix recovery (Marsden et al. 2003, Ferraz et
al. 2007, Laurance 2008, Stouffer et al. 2011). Not
only does an adjacent matrix facilitate fragment
recolonization, but it may also dampen predicted
area effects associated with the island model
(Zimmerman and Bierregaard 1986) as demon-
strated in the central Amazon where fragments
of different sizes yielded similar estimates of
species richness as the adjacent matrix matured
(Stouffer et al. 2006). Additionally, many species
recolonize Amazonian forest fragments, even if
they do not persist (Stouffer et al. 2011) demon-
strating that presence or absence of a matrix will
result in the disproportionate influence of either
extinction or colonization on Amazonian bird
assemblages in forest fragments and islands
bounded by water, respectively (Terborgh et al.
2001).
Conversely, forest patch size within a regener-
ating matrix in Costa Rica yielded a strong
influence on hummingbird abundance and the
subsequent seed set of native plants species they
pollinate (Hadley et al. 2014). These results
suggest that habitat patches in Costa Rica may
act more like true islands where some humming-
birds may respond to the regenerating matrix as
extremely hostile and are, therefore, subject to
area effects as predicted by the island model.
Although the response of birds to fragmentation
appear contradictory in the aforementioned
studies from the Amazon and Costa Rica, the
ecological value of landscape matrices from both
study sites was measured within fragments,
rather than within the matrix itself. Clearly,
measuring birds within the matrix to quantify
the ecological value of a regenerating tropical
forest represents a critical step towards predict-
ing species loss in the Neotropical countryside
(Gardner et al. 2007).
To date, research that has sampled birds within
the matrix to assess its ecological value mostly
relied on examining species richness between
regenerating and pristine forest; these studies
have produced largely contradictory and region-
dependent results. For example, Barlow et al.
(2007) found fewer species in regenerating matrix
relative to primary forest in Brazil, while Blake
and Loiselle (2001) documented more species
within young matrix relative to primary forest in
Costa Rica. The influence of region on patterns of
species richness within the matrix was exempli-
fied by Martin and Blackburn (2014 ) where
endemic species in Honduras were found to be
less common in the matrix relative to primary
forest, when compared with bird communities in
similar aged forests in Sulawesi. Dissimilar
responses of matrix bird communities probably
reflect four differences among the aforemen-
tioned studies: (1) differences in avifauna and
their respective ability to exploit resources; (2)
differences in successional pathways; (3) differ-
ences in distance to source populations; and (4)
differences in matrix age. Regional dissimilarities
are potentially further complicated by the asym-
metric response of foraging guilds to the age of
regenerating matrix. In general, frugivorous and
nectivorous birds, which are relatively more
common in Neotropical forests, often fare better
when subjected to clearing and subsequent forest
regeneration (although see Hadley et al. 2014)
relative to their insectivorous counterparts (Karr
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WOLFE ET AL.

et al. 1990, Sekercioglu et al. 2002).
Stouffer et al. (2006) and Powell et al. (2013)
demonstrated that the presence of insectivorous
birds on the periphery of Amazonian forest
fragments was positively correlated with age of
the surrounding matrix, with fewer birds cap-
tured in fragments bordered by young forest. In
particular, forest-obligate guilds such as terres-
trial insectivores, ant-followers, flock obligates
and arboreal insectivores were found to be most
sensitive to surrounding matrix age, possibly
reflecting an inability of certain foraging guilds to
disperse through young second growth to
recolonize isolated forest fragments (Stouffer et
al. 2006). Antithetically, hummingbirds, gap
specialists and some frugivores exhibited in-
creased abundances within fragments surround-
ed by a young matrix (Stouffer et al. 2006).
Clearly, the age of regenerating Amazonian
forest wields influence over how bird species
perceive and use the matrix.
A better understanding of how a range of
matrix conditions (i.e., water, young and mature
second growth) affect bird communities within
isolates as well as within the matrix would have
significant theoretical and conservation implica-
tions. The complex nature of historic and
continued degradation within the Amazon basin
provides a unique opportunity to conduct such a
study.HabitatlossintheAmazonbasinis
dynamic due to ecological and economic forces,
as reflected by hydroelectric development, large-
scale pasture abandonment and subsequent
forest regeneration (Neeff et al. 2006 ). In this
study we worked within the heterogeneous
central Amazonian landscape, using multiple
methods to describe bird communities on true
islands bounded by water, in fragments within a
matrix, in second growth of two ages, and in
continuous forest. In general, our study focused
on determining the applicability of island or
countryside biogeographic frameworks to study
birds in degraded and heterogeneous forests in
the Amazon.
More specifically, our study aimed to test the
following hypothesis: if birds can disperse
through young and mature second growth,
presumably at different rates, but rarely over
water, then forest fragments within a regenerat-
ing matrix will be subject to more colonization
and islands bounded by water to more extinc-
tion. To test this central hypothesis, we measured
four predictions: (1) birds can disperse through a
regenerating matrix to recolonize forest frag-
ments but will be less able to disperse over water,
thus, true islands will be less species rich when
compared to similarly-sized forest fragments
embedded within a regenerating matrix; (2)
because birds are more prone to disperse through
mature second growth (25 years old) relative to
young second growth (15 years old), young
second growth will be significantly less species
rich than mature second growth; (3) forest-
obligate birds (terrestrial insectivores, ant-follow-
ers, flock obligates and arboreal insectivores) are
dispersal limited, therefore true islands will have
different community structure driven by the lack
of forest-obligate birds compared to similarly-
sized forest fragments; and (4) forest-obligate
birds (terrestrial insectivores, ant-followers, flock
obligates and arboreal insectivores) are more
prone to disperse through mature second growth
(25 years old) relative to young second growth
(15 years old), therefore young second growth
will have a significantly different community
structure driven by the lack of forest-obligate
birds compared to mature second growth.
METHODS
The study was conducted in terra firme forest
at the Biological Dynamics of Forest Fragments
Project (BDFFP), about 80 km north of Manaus,
Brazil and on two islands, each about 100 ha in
size (Sapopara and Relo´ gio), in the Balbina
reservoir, approximately 150 km north of Man-
aus. Balbina dam construction was completed in
1989; Sapopara and Relo´gio have been isolated
since then. Forest fragments at BDFFP, including
two 100-ha fragments, were isolated from 1980
through 1990. We also worked in 15- and 25-
year-old second growth and continuous primary
forest at the BDFFP (Fig. 1). For more informa-
tion about the study site see Stouffer et al. (2006 ).
To test the four aforementioned predictions we
employed both understory mist-netting and
point counts to account for birds in each stratum
of forest. Point counts can detect species that are
vocal, conspicuous, or occupy the canopy and
mid-story. Conversely, mist-netting is useful for
detecting quiet or skulking understory species
(Ralph et al. 1995). Mist netting and point counts
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WOLFE ET AL.

were conducted in five treatments: 100-ha forest
fragment (surrounded by a 50-m buffer of 15-
year-old second growth followed by a secondary
50-m buffer of 25-year-old second growth adja-
cent to continuous forest), 100-ha island (sur-
rounded by at least 300 m of open water within a
landscape of larger islands and continuous
forest), older second growth forest (25 years old
adjacent to continuous forest), young second
growth forest (15 years old adjacent to continu-
Fig. 1. Map of study regions at the Balbina reservoir and Biological Dynamics of Forest Fragments Project 80
km and 150 km north of Manaus, Brazil, respectively.
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WOLFE ET AL.

ous forest) and continuous forest. Treatments
were aggregated into five regions: Dimona (two
transects within a 100-ha forest fragment, two
transects within older second growth and two
transects within continuous forest), Porto Alegre
(two transects within a 100-ha forest fragment
and two transects within continuous forest),
Colosso (two transects within older second
growth forest, two transects within young second
growth forest and two transects within continu-
ous forest), KM41 (two transects within contin-
uous forest), and Balbina (one transect on each of
two 100-ha islands). Each BDFFP region was up
to 50 km apart, and Balbina was 70 km to the
north of the nearest BDFFP region (Fig. 1).
Despite a distance of 70 km between Balbina
and the other regions, each region is character-
ized by terre firme forest occurring on ancient
soils within the Guinean Shield, resulting in
comparable bird communities. Our assumption
of similar bird communities across the study area
is verified by earlier work that documented
remarkably similar bird communities throughout
the Guinean shield, from Manaus through
French Guiana (Willis and Oniki 1988, Johnson
et al. 2011). Furthermore, we only captured one
resident species (in addition to a single migrant)
at Balbina that we didn’t capture at BDFFP
further emphasizing the similarity of these
communities.
Each transect was 200 m in length, at least 200
m apart from any neighboring transect, and
hosted three point count locations at 0 m, 100 m
and 200 m along the transect. Twenty minute
point counts were conducted in 2012 during our
study area’s prolonged dry season, June through
November; each point count occurred between
05:55 and 07:20 am. Given the diversity of bird
species in the central Amazon, we used 20
minutes (as opposed to five or 10 minutes) to
maximize the number of species encountered at
each transect. For each point count, the number
of individuals per species was conservatively
estimated using song, call and visual documen-
tation within a 50 m radius; flyovers were not
included in the analysis. Each point-count station
was visited twice by J. D. Wolfe on different days,
yielding 12 20-minute point counts per treatment
in each area. Each transect also hosted a line of 16
mist-nets (NEBBA-type ATX, 36 mm mesh, 12 32
m),with nets set with the bottom at ground level
and opened from 0600 to 1400 for a single day of
sampling. All captured birds were banded with
uniquely numbered aluminum bands. We mist-
netted between June and November in 2010–
2013, where we collected 4 days of capture data
at 100-ha island transects, 4 days of capture data
at young second growth transects, and 6 days of
captureat100-haforestfragmenttransects,
continuous forest transects and older second
growth transects.
To measure differences in species richness
between forest fragments, islands, regenerating
matrix and continuous forest (see predictions 1
and 2), point count and capture data were
organized by number of individuals per species
by treatment. For capture data, the number of
species captured at each transect was divided by
associated effort (mist net hours) then multiplied
by 100 to yield a standard number of species
captured per 100 mist net hours across each
transect irrespective of differences in sampling
effort. We used program EstimateS (Colwell
2005) to produce Chao1 abundance-based esti-
mates of species diversity and Chao-Jaccard
abundance-based similarity indices to compare
treatments. The Chao1 diversity index uses the
ratio of ‘singletons’and ‘doubletons’(species
detected only once or twice, respectively) to
generate predicted estimates of species richness.
Significance between Chao1 estimates are based
on non-overlapping 95%confidence intervals
generated through a bootstrapping routine in
EstimateS. The formula used for Chao1 estimates
are based on Chao (1987) where S
obs
refers to
total number of species observed in all samples
pooled and F
1
and F
2
refer to singletons and
doubletons (species detected only once or twice),
respectively:
ˆ
Schao1 ¼Sobs þF2
1
F2
2
:
To measure overall community similarity
between forest fragments, islands, regenerating
matrix and continuous forest (see predictions 3
and 4) we used Chao’s abundance-based Jaccard
community similarity indices. According to
Colwell (2005), Chao’s abundance-based Jaccard
community similarity indices are based on the
probability that two randomly chosen individu-
als, one from each of the two samples, both
belong to species shared by both samples (but
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WOLFE ET AL.

not necessarily to the same shared species; Chao
et al. 2005, Colwell 2005). This approach has been
shown to substantially reduce the negative bias
that undermines the usefulness of traditional
similarity indexes, especially with incomplete
sampling of rich communities (Chao et al. 2005,
Colwell 2005). The formula used for Chao-
Jaccard abundance-based similarity indices are
based on Chao et al. (2005), and described by
Colwell (2005) where Q
1
is the frequency of
uniques,Q
2
the frequency of duplicates
vˆ
arðˆ
Schao2Þ¼Q2þ1
2
Q1
Q2

2
þQ1
Q2

3
þ1
4
Q1
Q2

4
"#
and
ˆ
Schao2 ¼Sobs þQ2
1
Q2
:
To measure community similarity between
forest fragments, islands, regenerating matrix
and continuous forest with respect to foraging
guild (see predictions 3 and 4), we separately
categorized mist-netting and point count data by
foraging guild and species (following Stouffer et
al. 2006; Appendix: Tables A1 and A2). We used
package Vegan in Program R (Dixon 2003, R
Development CoreTeam 2010) to separately
ordinate capture and point count data, catego-
rized by foraging guild and species within
treatment, via a Detrended Correspondence
Analysis (DCA). We statistically examined dif-
ferences among bird communities within each
treatment, by foraging guild and species, via a
permutation test using 1000 iterations in package
Vegan. In addition to estimating diversity,
community similarity and ordinations, we used
package Car (Fox et al. 2012) in program R to
employ a two-way ANOVA using type III sum of
squares to test guild and treatment effects on
species abundance for both point count and
capture data. We choose type III sum of squares
ANOVA because it relies on unweighted means
that account for correlations between indepen-
dent variables due to unequal sample sizes.
Because our chosen diversity estimator
(Chao1), community similarity metric (Chao-
Jaccard abundance-based similarity index) and
ordination methodology (DCA) may be sensitive
to variation in effort and sample size, we also
conducted a sensitivity test to ensure our results
are robust. We accounted for unequal effort
among transects and treatments using the sensi-
tivity test by randomly selecting four capture and
four point count occasions per treatment (con-
tinuous, 100-ha fragment, 100-ha island, young
and mature second growth) thereby creating
complete equal effort among the subset of data,
then repeated a portion of the above analysis on
the subset of data. More specifically, we gener-
ated Chao1 diversity estimates, compared com-
munities using the Chao-Jaccard abundance-
based similarity index, and finally used package
Vegan in Program R to ordinate and compare
communities categorized by species for each
treatment.
RESULTS
We recorded 3,339 individual birds represent-
ing 180 species during point counts (Appendix:
Table A1). We banded 3,916 individual birds
representing 121 species (Appendix:Table A2).
Our first prediction, that islands are less species
rich than fragments, was supported by point
count data where we found significantly fewer
bird species on true islands compared to frag-
ments and all other treatments except young
second growth (Fig. 2). Although not significant,
capture data also yielded the lowest number of
species on true islands relative to fragments and
all other treatments (Fig. 2). Similarly, point
count and capture data supported our second
prediction that young second growth would host
fewer species than mature second growth; young
second growth was the most species depauperate
compared to all other non-island treatments (Fig.
2). Our third prediction, that island and fragment
bird communities would be significantly differ-
ent, was supported by both point count and
capture data. For example, the Chao-Jaccard
abundance-based similarity index at the treat-
ment scale suggested that islands and fragments
were the third and second most dissimilar bird
community using capture and point count data,
respectively, when ranked against all other
possible treatment comparisons (Fig. 3). Similar-
ly, at the region scale, island bird communities
were the most dissimilar when compared to all
other regions (Appendix: Fig. A1). Supporting
the assertion that island communities are the
most dissimilar, Detrended Correspondence
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WOLFE ET AL.

Fig. 3. Chao’s abundance-based Jaccard community similarity indices based on point count data by treatment
shown with standard error bars. Filled circles represent point count and open boxes represent capture data.
Comparisons are ranked from most to least similar.
Fig. 2. Chao1’s estimated number of species by treatment (10-ha forest fragment, 100-ha island, continuous,
older second growth forest, and young second growth forest) and region. Filled circles represent point count and
open boxes represent capture data. All values are shown with 95%confidence intervals.
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WOLFE ET AL.

Analysis (DCA) results suggested that, based on
mist-net data, true islands represented signifi-
cantly different communities ( p,0.05) when
classified by foraging guild and species (Figs. 4
and 5). Guild ordinations based on point count
data also suggested that true islands approached
significance ( p,0.1). Support for our fourth
prediction, that young and mature second
growth bird communities would be significantly
different, was not supported by the Chao-Jaccard
abundance-based similarity index at the treat-
ment scale based on species captured (Fig. 3).
However, when grouped by guild, the DCA
ordination based on capture data yielded a
significant difference between young second
growth and mature second growth thereby
supporting our fourth prediction (Fig. 4). These
differences were driven by the abundance of non-
forest and hummingbird foraging guilds associ-
ated with young second growth (Appendix:
Table A1).
In general, continuous, forest fragment and
older second growth bird communities were
most similar irrespective of method (mist-netting
or point count). Estimated diversity and commu-
nity similarity analyses showed that bird com-
munities on true islands and in young second
growth forest were most depauperate and
dissimilar from communities in continuous for-
est. Interestingly, when classified by species,
forest fragment, older second growth, young
second growth and true islands all yielded
significantly different bird communities ( p,
0.05; Figs. 6 and 7). Our two-way ANOVA using
Fig. 4. Detrended correspondence analysis (DCA) ordination of capture data, classified by foraging guild and
treatment. Asterisks represent significance levels where * and ** represent p,0.1 and p,0.05, respectively.
Numbers in parentheses represent number of species within foraging guild and total number of individuals
captured within each foraging guild.
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WOLFE ET AL.

type III Sum of Squares based on foraging guild
classification, for point count (df ¼48, f-stat ¼
10.04, p,0.001) and mist-net data (df ¼44, f-stat
¼6.57, p,0.001) yielded highly significant
differences among treatments and guilds. Differ-
ences were driven by high number of core
frugivores in older second growth, and the
absence of flock obligates, flock dropouts and
terrestrial insectivores on true islands and in
young second growth (Appendix: Figs. A2 and
A3). Finally, our sensitivity test, where we
generated the same statistics using a subset of
data with equal effort, clearly demonstrated that
differences in sampling effort did not bias our
results where islands yielded half the number of
estimated species than forest fragments (Appen-
dix: Tables A3 and A4). Additionally, the DCA
ordination based on equal capture and point
count effort suggested that islands represented
significantly different bird communities (Appen-
dix: Figs. A4 and A5).
Several species intolerant to second growth
(e.g., documented in continuous forest but never
in regenerating forest) were found on true
islands: Piaya melanogaster,Celeus undatus,Tyr-
anneutes virescens,andRamphotrigon ruficauda.
Additionally, two species particularly common in
second growth samples were also found on true
islands: Myiarchus ferox and Notharchus macro-
rhynchus (although, N. macrorhynchus more asso-
ciated with older forest at BDFFP; Cohn-Haft et
al. 1997). In general, woodpeckers (Picidae) and
toucans (Ramphastidae) were well represented
on true islands while terrestrial insectivores (e.g.,
Formicarius colma,Corythopis torquatus and Scleru-
rus rufigularis) and obligate flocking species (e.g.,
Thamnomanes caesius and T. ardesiacus)were
absent from true islands (Appendix: Tables A1
and A2).
DISCUSSION
The succession of bird communities in second
growth facilitated the recolonization of forest
fragments, permitting fragments as small as 100
ha to support bird communities similar to
continuous forest. Clearly, a regenerating forest
matrix is not as hostile as open-water, thereby
demonstrating that island biogeography is not an
appropriate model to predict species loss in
forest fragments at our study site in the central
Amazon. We suggest future studies use a
Fig. 5. Detrended correspondence analysis (DCA) ordination of capture data, classified by foraging guild and
treatment. Asterisks represent significance levels where * and ** represent p,0.1 and p,0.05, respectively.
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WOLFE ET AL.

countryside biogeographic framework to exam-
ine how diverse Amazonian bird communities
perceive and use regenerating forest matrices. In
general, we found support for each of our four
predictions used to examine the processes re-
sponsible for differences in bird species richness
and community assemblages between islands
and forest fragments, and young and mature
second growth, respectively. With regard to
differences in diversity and community assem-
blages between islands and fragments (predic-
tions 1 and 3), our study demonstrated that
species richness in forest fragments within a
regenerating matrix is not driven by extinction
dynamics as predicted by the island model.
Instead, species richness appears to be dependent
on the permeability of the surrounding matrix,
which allows recovery of bird communities in
formerly isolated fragments. In contrast, for true
islands, small area coupled with the complete
absence of an adjacent second growth matrix
subjected each island to severe and irreconcilable
local extinction events despite the presence of
primary forest at our study site.
With regard to differences in diversity and
community assemblages between young and
mature regenerating forest (predictions 2 and
4), we found that bird communities varied
significantly, when separated by guild, between
young (15 year) and older (25 year) second
growth; such differences appear to have been
driven by the absence of terrestrial insectivores
and flocking species, and the abundance of
nonforest species, gap-specialists and humming-
birds in young second growth. Our study clearly
demonstrated that foraging guilds closely asso-
Fig. 6. Detrended correspondence analysis (DCA) ordination of capture data, classified by foraging guild and
treatment. Asterisks represent significance levels where * represents p,0.1. Numbers in parentheses represent
number of species within foraging guild and total number of individuals captured within each foraging guild.
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WOLFE ET AL.

ciated with forest, such as terrestrial insectivores
and flocking species, perceive and use young and
mature second growth very differently. Within 25
years of clearing, many forest-dwelling birds are
frequently encountered within second growth
thereby creating a community more reflective of
those found in continuous forest. Whether or not
these pioneering birds form stable populations in
mature second growth or persist through the
addition of dispersing individuals from source
populations is not known and represents an
important facet of further study.
We also found that young second growth was
species poor, with approximately the same
number of species as true islands. Despite similar
number of species, community structure at the
levels of both guild and species were statistically
different between true islands and young second
growth. Differences in community structure
coupled with low species richness suggest two
divergent responses to dissimilar system pertur-
bations: second growth bird communities reflect
the successional nature of regenerating forest
where gap specialists, nonforest species, and
hummingbirds are replaced by flocking and
insectivorous species as the forest approaches
25 years of age. Conversely, islands are charac-
terized by species capable of major dispersal
events and small remnant populations of forest-
obligate species.
Although the complexity of the landscape used
in this study hinders generalizing our results to
other tropical systems, our results do support
previous assertions that a species’capacity to
disperse through matrix to recolonize tropical
forest fragments ultimately determines metapop-
ulation connectivity in degraded landscapes
(Sekercioglu et al. 2002). Interestingly, several
species absent from second growth at BDFFP
were detected on true islands. Although we can’t
be sure, we believe these species are remnants
from populations present at the time the reser-
voir was flooded. Conversely, many solitary
ground-dwelling insectivores and core-flocking
species that are common in continuous forest and
easily detected with both sampling techniques
were conspicuously absent from true islands,
indicating the inability of these guilds to recolo-
nize islands across open water. This finding is not
surprising given previous studies found that
these same guilds were less apt to cross open
spaces and most prone to go extinct in forest
Fig. 7. Detrended correspondence analysis (DCA) ordination of capture data, classified by foraging guild and
treatment. Asterisks represent significance levels where ** represents p,0.05.
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WOLFE ET AL.

fragments immediately after isolation (Ferraz et
al. 2003, Laurance et al. 2004, Stouffer et al. 2006,
Stouffer et al. 2009). Although open water is not
suitable for many dispersing forest-dwelling
birds, the remains of dead trees above the water’s
surface are common throughout the reservoir
and presumably facilitate the dispersal of species
capable of utilizing snags (Appendix: Fig. A6 ). In
fact, that is what we found: woodpeckers and
toucans used snags on the open water and had
relatively high diversity on islands (Appendix:
Table A1).
Our results parallel findings from another
tropical reservoir where smaller and more
isolated islands (1–12 ha in size and 1 km 
from source populations) had fewer species and
fewer transient individuals capable of recoloni-
zation (Terborgh et al. 1997). Although we don’t
know the mechanism responsible for extinction
events within islands at our study sites, given
similarities between our findings and Terborgh et
al. (1997), we suspect that communities were
altered by biological (remnant mesopredators)
and stochastic (extinction) processes leading to a
dynamic equilibrium. Relative to Terborgh et al.
(1997), however, our island sites were larger (100
ha) and farther from source populations, thereby
reducing area effects associated with small
habitat patches (Terborgh et al. 1997, Stouffer et
al. 2006, 2009). We believe our depauperate true
island diversity estimate probably represents an
ongoing extinction debt which will result in
future equilibrium characterized by low species
richness, including only those birds most capable
of dispersing and most resilient to the effects of
fragmentation (Ferraz et al. 2003). Thus, we
recognize that differences in species assemblage
and richness between true islands and other
forest types may be dependent on how long the
islands have been isolated thereby determining if
an extinction debt has been paid in-full. Overall,
islands are an extinction driven system, forest
fragments in regenerating matrix are a recoloni-
zation driven system, and second growth is a
successional driven system at our study site in
the central Amazon.
In addition to informing ecological theory, our
study has important conservation implications.
For example, we provide evidence of a dynamic
relationship between bird communities and
degraded tropical landscapes, an understanding
that is important for conservation purposes for
regions with unparalleled diversity, such as the
Amazon basin. Over the last 20 years the Brazil-
ian government subsidized forest clearing to
enhance farming opportunities for an expanding
populace resulting in the loss of 328,000 km
2
of
Amazonian forest (INPE 2010). In addition to
agricultural expansion, the Brazilian government
authorized the construction of 30 additional
hydroelectric dams in the Amazon basin, result-
ing in, on average, one new dam being con-
structed every four months over the next seven
years (Eletrobra´s 1987, Ministe´rio de Minas e
Energia 2011). The threat of massive Amazon
forest loss due to hydroelectric development is
considerable given that a single dam in the
central Amazon, Balbina, flooded 2360 km
2
of
tropical rainforest (Fearnside 1989). Dams lead to
hilltop islands surrounded by water, a much
more static landscape than when forest is
removed for agriculture. Such differences mean
that islands and isolated habitats behave differ-
ently and represent a larger threat to the
preservation of biodiversity than habitat patches
within a matrix. These ecological, economic and
political realities coupled with our results sug-
gest that many more bird communities will be
subject to the deleterious effects of ecological
decay associated with hydroelectric develop-
ment.
ACKNOWLEDGMENTS
Thanks to the multitude of banders, assistants and
mateiros who helped collect the data. Logistical
support from the Biological Dynamics of Forest
Fragmentation Project, Brazil’s Instituto Nacional de
Pesquisas da Amazˆ
onia, and the Smithsonian Institu-
tion made this research possible. The quality of the
manuscript was greatly improved by Maria Uriarte
and two anonymous reviewers. This project would not
have been possible without the dedicated help of G. N.
Klein at REBIO Uatuma˜. Funding was provided by a
US National Science Foundation (LTREB 0545491)
grant and American Ornithologists’Union research
grant. Thanks to committee members and field
collaborators: Bruce Williamson, Robb Brumfield and
Gon¸calo Ferraz. This article was approved for publi-
cation by the Director of the Louisiana Agricultural
Experimental Station as manuscript no. 2015-241-
22665. This is publication 678 of the Biological
Dynamics of Forest Fragments Project Technical Series.
vwww.esajournals.org 12 December 2015 vVolume 6(12) vArticle 295
WOLFE ET AL.

LITERATURE CITED
Barlow, J., L. A. Mestre, T. A. Gardner, and C. A. Peres.
2007. The value of primary, secondary and planta-
tion forests for Amazonian birds. Biological Con-
servation 136:212–231.
Blake, J. G., and B. A. Loiselle. 2001. Bird assemblages
in second-growth and old-growth forests, Costa
Rica: perspectives from mist nets and point counts.
Auk 118:304–326.
Chao, A. 1987. Estimating the population size for
capture-recapture data with unequal catchability.
Biometrics 43:783–791.
Chao, A., R. L. Chazdon, R. K. Colwell, and T.-J. Shen.
2005. A new statistical approach for assessing
compositional similarity based on incidence and
abundance data. Ecology Letters 8:148–159.
Cohn-Haft, M., A. Whittaker, and P. C. Stouffer. 1997.
A second look at the ‘‘ species-poor’’ central
Amazon: the avifauna north of Manaus, Brazil.
Ornithological Monographs 48:205–235.
Colwell, R. K. 2005. EstimateS, version 7.5: statistical
estimation of species richness and shared species
from samples. http://purl.oclc.org/estimate
Daily, G. C. 1997. Countryside biogeography and the
provision of ecosystem services. Pages 104–113 in
P. Raven, editor. Nature and human society: the
quest for a sustainable world. National Research
Council, National Academy Press, Washington,
D.C., USA.
Dixon, P. 2003. VEGAN, a package of R functions for
community ecology. Journal of Vegetation Science
14:927–930.
Eletrobra´s. 1987. Plano 2010: Relato´rio Geral. Plano
Nacional de Energia Ele´trica 1987/2010 (Dezembro
de 1987). Centrais Ele´tricas do Brasil (ELETRO-
BRA
´S), Brası´lia, DF, Brazil.
Fahrig, L. 2013. Rethinking patch size and isolation
effects: the habitat amount hypothesis. Journal of
Biogeography 40:1649–1663.
Fearnside, P. M. 1989. Brazil’s Balbina Dam: environ-
ment versus the legacy of the pharaohs in
Amazonia. Environmental Management 13:401–
423.
Ferraz, G., J. D. Nichols, J. E. Hines, P. C. Stouffer, R. O.
Bierregaard, Jr., and T. E. Lovejoy. 2007. A large-
scale deforestation experiment: effects of patch area
and isolation on Amazon birds. Science 315:238–
241.
Ferraz, G., G. J. Russell, P. C. Stouffer, R. O. Bierre-
gaard, Jr., and S. L. Pimm. 2003. Rapid species loss
from Amazonian forest fragments. Proceedings of
the National Academy of Sciences USA 100:14069–
14073.
Fox, J., S. Weisberg, D. Bates, and M. J. Fox. 2012.
Package ‘‘car’’ . https://cran.r-project.org/web/
packages/car/index.html
Gardner, T. A., J. Barlow, L. W. Parry, and C. A. Peres.
2007. Predicting the uncertain future of tropical
forest species in a data vacuum. Biotropica 39:25–
30.
Hadley, A. S., S. J. K. Frey, W. D. Robinson, W. J. Kress,
and M. G. Betts. 2014. Tropical forest fragmentation
limits pollination of a keystone understory herb.
Ecology 95:2202–2212.
INPE [Brazilian National Space Research Institute].
2010. Projecto prodes: Monitoramento da flororesta
Amazonica Brasileira por satelite. Ministerio da
Ciencia e Tecnologia, Brazil.
Johnson, E. I., P. C. Stouffer, and C. F. Vargas. 2011.
Diversity, biomass, and trophic structure of a
central Amazonian rainforest bird community.
Revista Brasileira de Ornitologia 19:1–16.
Karr, J. R., S. K. Robinson, J. G. Blake, and R. O.
Bierregaard, Jr. 1990. Birds of four Neotropical
forests. Pages 237–269 in A. H. Gentry, editor. Four
neotropical forests. Yale University Press, New
Haven, Connecticut, USA.
Laurance, S. G., P. C. Stouffer, and W. F. Laurance.
2004. Road crossing by Amazonian understory
birds. Conservation Biology 18:1099–1109.
Laurance, W. F. 2008. Theory meets reality: how
habitat fragmentation research has transcended
island biogeographic theory. Biological Conserva-
tion 141:1731–1744.
Marsden, S., J. M. Whiffin, L. Sadgrove, and P. R.
Guimara˜ es, Jr. 2003. Bird community composition
and species abundance on two inshore islands in
the Atlantic Forest region of Brazil. Ararajuba
11:181–187.
Martin, T. E., and G. A. Blackburn. 2014. Conservation
value of secondary forest habitats for endemic
birds, a perspective from two widely separated
tropical ecosystems. Ecography 37:250–260.
Mendenhall, C. D., G. C. Daily, and P. R. Ehrlich. 2012.
Improving estimates of biodiversity loss. Biological
Conservation 151:32–34.
Mendenhall, C. D., D. S. Karp, C. F. Meyer, E. A.
Hadly, and G. C. Daily. 2014. Predicting biodiver-
sity change and averting collapse in agricultural
landscapes. Nature 509:213–217.
Ministe´rio de Minas e Energia. 2011. Plano Decenal de
Expansa˜ o de Energia 2020. MME, Empresa de
Pesquisa Energe´tica (EPE), Brası´lia, DF, Brazil.
Neeff, T., R. M. Lucas, J. R. Santos, E. S. Brondizio, and
C. C. Freitas. 2006. Area and age of secondary
forests in Brazilian Amazonia 1978–2002: an
empirical estimate. Ecosystems 9:609–623.
Powell, L. L., P. C. Stouffer, and E. I. Johnson. 2013.
Recovery of understory bird movement across the
interface of primary and secondary Amazon rain-
forest. Auk 130:459–468.
Ralph,C.J.,J.R.Sauer,andS.Droege.1995.
Monitoring bird populations by point count.
vwww.esajournals.org 13 December 2015 vVolume 6(12) vArticle 295
WOLFE ET AL.

General Technical Report PSW-149. USDA Forest
Service, Pacific Southwest Research Station, Arcata,
California, USA.
R Development Core Team. 2010. R:a language and
environment for statistical computing. R Founda-
tion for Statistical Computing, Vienna, Austria.
Sekercioglu, C. H., P. R. Ehrlich, G. C. Daily, D. Aygen,
D. Goehring, and R. F. Sandı´. 2002. The disappear-
ance of insectivorous birds from tropical forest
fragments. Proceedings of the National Academy
of Sciences USA 99:263–267.
Stouffer, P. C., R. O. Bierregaard, Jr., C. Strong, and
T. E. Lovejoy. 2006. Long-term landscape change
and bird abundance in Amazonian rainforest
fragments. Conservation Biology 20:1212–1223.
Stouffer, P. C., E. I. Johnson, R. O. Bierregaard, Jr., and
T. E. Lovejoy. 2011. Understory bird communities
in Amazonian rainforest fragments: species turn-
over through 25 years post-isolation in recovering
landscapes. PLoS ONE 6:e20543.
Stouffer, P. C., C. Strong, and L. N. Naka. 2009. Twenty
years of understorey bird extinctions from Amazo-
nian rain forest fragments: consistent trends and
landscape-mediated dynamics. Diversity and Dis-
tributions 15:88–97.
Terborgh, J., L. Lopez, P. V. Nun˜ez, M. Rao, G.
Shahabuddin, G. Orihuela, M. Riveros, R. Ascanio,
G. H. Adler, T. D. Lambert, and L. Balbas. 2001.
Ecological meltdown in predator-free forest frag-
ments. Science 294:1923–1926.
Terborgh, J., L. Lopez, J. Tello, D. Yu, and A. R. Bruni.
1997. Transitory states in relaxing ecosystems of
land bridge islands. Pages 256–274 in W. L.
LaurenceandR.O.Bierregaard,Jr.,editors.
Tropical forest remnants. University of Chicago
Press, Chicago, Illinois, USA.
Willis, E. O., and Y. Oniki. 1988. Aves observadas em
Balbina, Amazonas e os prova´veis efeitos da
barragem. Ciˆ
encia e Cultura 40:280–284.
Zimmerman, B. L., and R. O. Bierregaard, Jr. 1986.
Relevance of the equilibrium theory of island
biogeography and species-area relations to conser-
vation with a case from Amazonia. Journal of
Biogeography 13:133–143.
SUPPLEMENTAL MATERIAL
ECOLOGICAL ARCHIVES
The Appendix can be found online: http://dx.doi.org/10.1890/ES15-00322.1.sm
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