Download Local Extinctions of Terrestrial Insectivorous Birds in a Fragmented

Local Extinctions of Terrestrial Insectivorous Birds in a
Fragmented Landscape near Manaus, Brazil
JEFFREY A. STRATFORD* AND PHILIP C. STOUFFER
Department of Biological Sciences, Southeastern Louisiana University, Hammond, LA 70402–0736, U.S.A., and
Biological Dynamics of Forest Fragments Project, Instituto Nacional de Pesquisas de Amazonia, CP478, Manaus,
AM 69011, Brazil
Abstract: We examined the distributions of nine species of terrestrial insectivorous birds in 4- to 14-year-old
rainforest fragments north of Manaus, Brazil. We surveyed 11 fragments of 1, 10, and 100 ha, 95 ha of secondary vegetation, and nine continuous forest plots (controls) of 1–100 ha. We augmented standard spotmapping with extensive playback surveys. The fragments had been sampled with mist nets before isolation,
so our results could be compared with the pre-isolation distribution. For the nine species, there were 55 cases
of local extinction in the 11 fragments between about 1 year after isolation and the time of our surveys. This
corresponds to 74% extinction of the local populations in fragments. These extinctions occurred despite the
second-growth connection of some fragments to continuous forest as little as 70 m away. Three apparent colonization events by species not detected before isolation also occurred, but these may also reflect inadequate
sampling before isolation. Our comparison of fragments and similar-sized control plots in continuous forest
showed an area effect on species richness in both fragments and control plots, but fragments had fewer species than control plots of equal size. In a fragmented Amazonian landscape, the full suite of terrestrial insectivores would persist in the short term only in large fragments (.100 ha), although much larger areas are
probably necessary for the long-term persistence of their populations.
Extinciones Locales de Aves Insectívoras Terrestres en un Paisaje Fragmentado Cercano a Manaos, Brazil
Resumen: Examinamos las distribuciones de nueve especies de aves de insectívoros terrestres en fragmentos
de bosque lluvioso de 4 a 14 años cercanos a Manaos, Brazil, Muestreamos once fragmentos de 1, 10 y 100
ha de vegetación secundaria y nueve áreas de bosque continuo (control) de 1–100 ha. Aumentamos el mapeo de puntos convencionales con muestreos extensivos. Los fragmentos fueron muestreados con redes antes
del aislamiento, por lo que nuestros resultados pueden ser comparados con distribuciones pre-aislamiento.
Para las nueve especies hubieron 55 casos de extinción local en los 11 fragmentos entre cerca de 1 año posterior al aislamiento y el tiempo del muestreo. Esto corresponde a una extinción de un 74% de las poblaciones
locales en los fragmentos. Estas extinciones ocurrieron a pesar de conecciones de segundo grado de algunos
fragmentos con bosques continuos a tan solo 70 m de distancia. Tres eventos aparentes de colonización por
especies no detectadas antes del aislamiento tambien ocurrieron, pero esto puede ser reflejo de un inadecuado muestreo antes del aislamiento. Nuestra comparación de fragmentos y áreas control de similar
tamaño en bosques continuos muestra un efecto de área en la riqueza de especies tanto en sitios fragmentados como controles, pero los fragmentos tuvieron menos espeies que los sitios control de similar tamaño. En
un paisaje Amazónico fragmentado la totalidad de insectívoros terrestres persistirá en un corto plazo únicamente en los fragmentos grandes (.100 ha), aunque probablemente se necesitarán áreas mucho mas
grandes para la persistencia de sus poblaciones a largo plazo.
* Current address: Department of Zoology and Wildlife, 331 Funchess Hall, Auburn University, Auburn, AL 36849–5414, U.S.A.,
email antbirds@hotmail.com
Paper submitted October 15, 1998; revised manuscript accepted April 28, 1999.
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Volume 13, No. 6, December 1999
Stratford & Stouffer
Introduction
The effects of habitat fragmentation on avian communities are well documented in various parts of the temperate zone. For forest-interior species, fragmentation reduces abundance and richness (e.g., Saunders 1989;
Askins et al. 1990). If habitats are fragmented throughout the landscape, population characteristics such as dispersal (Matthysen et al. 1995), philopatric returns of migrants (Villard et al. 1995), and demography (Verboom
et al. 1991) will be affected. Isolated and reduced populations may also have reduced genetic variation (Frankham
1996). Forest fragmentation has effects on fitness through
increased egg predation (Yahner & Scott 1988), increased
brood parasitism (S. K. Robinson et al. 1995), and reduced pairing success (Van Horn et al. 1995). Forest-interior species may also be excluded by species associated
with disturbance (Ambuel & Temple 1983; Grey et al.
1998). Fragmentation may have more direct consequences by affecting microclimate (Saunders et al.
1991).
Human settlement patterns in the Amazon tend to
leave forest remnants amid deforested areas, as is the
case in the temperate zone (Dale et al. 1994; Skole et al.
1994), but the effects of forest fragmentation on Neotropical birds are not as well understood. Local extinction
has been suggested from indirect evidence or documented for unreplicated sites (e.g., Willis 1974, 1979;
Leck 1979; Karr 1982; Thiollay 1996; W. D. Robinson
1999), but there is less direct evidence of extinction
caused by forest fragmentation from replicated fragments.
The most complete study of the effects of fragmentation on a tropical avian community has been the longterm mist-netting program of the Biological Dynamics of
Forest Fragments Project (BDFFP) near Manaus, Brazil.
Some of the results of this study are reported by Stouffer
and Bierregaard (1995a, 1995b), Bierregaard and Stouffer
(1997), and Stouffer and Borges (2000). The BDFFP data
are unique because replicated treatments (fragments)
were sampled before they were isolated from the continuous forest surrounding them. Long-term data of the
BDFFP show that terrestrial insectivores are particularly
sensitive to fragmentation. Abundance, measured by
mist-net captures, declined with decreasing fragment
size and over the 9 years of study (Stouffer & Bierregaard
1995a). Other studies of fragmentation and habitat alteration in the Neotropics also suggest negative effects on
terrestrial insectivores (Willis 1974, 1979; Leck 1979;
Karr 1982; Canaday 1996). Borges (1995) found terrestrial insectivores rare or absent in the secondary forest at
the BDFFP site.
We examined the distribution of nine species of terrestrial insectivores in forest fragments, second growth,
and continuous forest at the BDFFP site. The data from
fragments can be compared to results from the same ar-
Birds in Amazonian Forest Fragments
1417
eas before they were isolated. Although some of the
study species were probably overlooked in the pre-isolation surveys, we designed our sampling to minimize the
chance of overlooking birds.
Methods
Study Site and Species
The study was conducted approximately 80 km north of
Manaus in the Brazilian state of Amazonas (lat 293099 S,
long 609W; Fig. 1). The area is a mosaic of terra firme
forest, cattle ranches, secondary areas, and fragments of
primary forest. Lovejoy and Bierregaard (1990) provide a
detailed account of the study site. In continuous forest,
canopy height averages 30–37 m, with occasional emergents up to 55 m. The understory is open and dominated
by palms. The area has relatively pronounced wet and
dry seasons. Rainfall at Reserva Ducke, approximately
50 km south of the study site, averaged 2500 mm per
year from 1966 to 1990, with the greatest amount of
rainfall from January to April and a dry season from June
to September (Stouffer & Bierregaard 1993). There are
several small streams in the forest, some of which have
flowing water only during the wet season.
We collected data from 11 fragments: five 1 ha, four
10 ha, and two 100 ha in size (for individual descriptions
of the fragments, see Lovejoy et al. 1986). The fragments
were created between 1980 and 1990 by cattle ranchers
working in collaboration with the BDFFP (10 of the 11
fragments were isolated by 1984; reviews in Lovejoy &
Bierregaard 1990; Bierregaard et al. 1992). Distances of
70–650 m separated fragments from the nearest continuous forest; 6 of the 11 fragments were separated by 100–
200 m. At 6 fragments, the surrounding vegetation was
burned, and cattle were allowed to graze around the
fragments. After several years, plant growth emerged,
dominated by trees in the genera Vismia (Clusiaceae)
and Bellucia (Melastomataceae). At 5 other fragments,
the felled vegetation was not burned, and Cecropia sciadophylla (Cecropiaceae) quickly dominated. Apart from
the cattle ranches, the sites were embedded in continuous forest unbroken for hundreds of kilometers.
We also sampled nine control plots in nearby continuous forest. Three 1-ha control plots were chosen a priori
based on topography to match the 1-ha fragments,
which were all relatively flat and without streams. We
also sampled four 10-ha plots, a 50-ha plot, and a 100-ha
plot. For our analyses, we consider the 50-ha continuous forest plot to be a replicate of the 100-ha plot because it contained all the possible species. All control
plots were at least 500 m apart. Secondary growth available for surveying was found around fragments or in pastures that were either abandoned or used infrequently
for grazing.
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Volume 13, No. 6, December 1999
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Stratford & Stouffer
Figure 1. Landsat TM image of the Biological Dynamics of Forest Fragments Project study site from 20 September
1995. The darkest shading is continuous forest. Lighter shading indicates nonforested areas, including roads, active and abandoned pastures, orchards, and second-growth forest up to approximately 15 years old. Numbers indicate fragments and continuous forest plots (for detailed descriptions of the individual fragments and continuous
forests plots, see Lovejoy et al. 1986). Locations are approximate for the continuous forest plots.
We surveyed nine species of birds: Myrmeciza ferruginea (Ferruginous-backed Antbird), Formicarius colma
(Rufous-capped Antthrush), Formicarius analis (Blackfaced Antthrush), Myrmornis torquata (Wing-banded
Antbird), Hylopezus macularius (Spotted Antpitta),
Myrmothera campanisona (Thrush-like Antpitta), Grallaria varia (Variegated Antpitta), Conopophaga aurita
(Chestnut-belted Gnateater), and Corythopis torquata
(Ringed Antpipit). All have stout bodies and short wings,
although they vary in mass from 15 g (Corythopis
torquata) to 120 g (Grallaria varia; Bierregaard 1988).
Our observations and published accounts suggest that
most of these species forage almost exclusively on the
ground. Conopophaga aurita, a difficult bird to observe, may be an exception. We have seen it on the
ground, but we have not observed it foraging. It was reported as terrestrial by Sick (1993:422), although
Ridgely and Tudor (1994) imply that Conopophaga feed
in low vegetation. Corythopis torquata forages both in
the litter and by stretching or jumping from the ground
to remove invertebrates from the underside of leaves.
Marra and Remsen (1997) and Stratford (1997) describe
the habitat used by some of these species. There are
other species of terrestrial insectivores at the site, but
we chose a subset that could be accurately sampled
with spot-mapping and tape playback (for a complete
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Volume 13, No. 6, December 1999
description of the BDFFP avifauna, see Cohn-Haft et al.
1997).
Survey Methods
We sampled birds from July 1994 through July 1995.
Surveys were conducted from 0530 to 0900 hours for 3
days in plots of 1–10 ha and for 6 days in larger plots.
Most plots were surveyed on consecutive days. The observer walked around the perimeter of the plot and on
trails through the interior, noting the location of any
study species seen or heard. Peak singing for the study
species is within about 30 minutes of sunrise (approximately 0530 to 0630 hours all year), although some species sing or call later in the day, especially around sundown. Surveys in the secondary growth were conducted
from trails, roads, and around fragments. Only birds
within 100 m of the trail were counted in secondgrowth surveys.
For species that were not detected by 0630 hours, we
used playback to elicit a species-specific response. Playback has been recommended to survey secretive birds
and has been used successfully to census birds in North
America (Johnson et al. 1981; Marion et al. 1981) and for
experimental purposes in the Neotropics (S. K. Robinson
& Terborgh 1995; Stouffer 1997). Tapes were played at
Stratford & Stouffer
Birds in Amazonian Forest Fragments
the center and at the perimeter of each of the study
plots with using either a Sony TC-D5 Pro II or a Marantz
PMD222 with an Archer external speaker. All tapes included songs and calls recorded at the BDFFP sites.
After testing for normality, we used the results from
these surveys in a two-way analysis of variance to test for
the effects of plot size and fragmentation on species
richness. We tested for specific differences among the
1-, 10-, and 100-ha plots using a post-hoc GT2 comparison, a recommended comparison for means from unequal sample sizes (Sokal & Rohlf 1981).
We compared mist-netting data from fragments before
isolation with the presence-absence data from our surveys. We included 1 year of the post-isolation period
with the pre-isolation period because several fragments
had little pre-isolation sampling effort. Captures confirmed presence, but the lack of a capture does not confirm an absence, especially for species like the antpittas,
which seldom fall into mist nets (e.g., Stouffer & Bierregaard 1995a). Because all the study species respond to
playback, we doubt we overlooked any birds in our surveys. Thus we are more likely to assume falsely that a
species was absent before isolation than after isolation.
all 10-ha fragments were Myrmothera campanisona,
Corythopis torquata, Formicarius analis, Hylopezus
macularius, and Myrmornis torquata. A single 1-ha
fragment had a terrestrial insectivore (Myrmothera
campanisona).
Two to nine species were found in the control plots
(Table 2; Fig. 2). The 100- and 50-ha control plots each
contained all of the terrestrial insectivores. The 10-ha
control plots had four to six species. The 1-ha control
plots had two to three species. Formicarius colma was
found in all of the control plots. Conopophaga aurita
and Myrmeciza ferruginea were found in the three 10ha control plots. Formicarius analis was not detected
in any of the 1- or 10-ha plots. Myrmothera campanisona, Grallaria varia, and Conopophaga aurita
were not detected in any of the 1-ha plots.
A two-way analysis of variance of area and fragmentation (fragments vs. control plots; Fig. 2) revealed significant area effects and significant effects of fragmentation
but no significant interaction (area: F 5 71.15, df 5
1,14, p , 0.0001; fragmentation: F 5 62.59, df 5 1,12,
p , 0.0001; interaction: F 5 0.81, df 5 1,14, p 5 0.464).
Not surprisingly, 100-ha fragments and control plots had
more species than 1-ha fragments and control plots.
Fragments and control plots of 10 ha were intermediate.
Before isolation, five to nine species were recorded in
the plots that later became fragments (Table 1). Local
extinction occurred in all fragments, with the proportion of local populations that went extinct varying from
100% in 1-ha fragments to 31% in 100-ha fragments.
The most extinction-prone species were those that occurred in the most plots before isolation—Myrmornis
torquata, Corythopis torquata, Formicarius colma,
and Myrmeciza ferruginea—all of which went extinct
in at least 7 of the 11 fragments. Our results show three
possible colonizations (two by Myrmothera campanisona and one by Formicarius analis), although
Results
The fragments had zero to seven of the nine species at
the time of our surveys (Table 1; Fig. 2). The two 100-ha
fragments had six and seven species. Missing from both
100-ha fragments was Myrmornis torquata, which was
also absent from all the smaller fragments. Formicarius
analis and Myrmeciza ferruginea were also missing
from one 100-ha fragment, and Conopophaga aurita
was missing from the other 100-ha fragment. The 10-ha
fragments contained one to four species. Missing from
Table 1.
1419
Distribution of terrestrial insectivorous birds in Amazonian forest fragments before and after isolation.a
Fragment size (ha)
Species
100
100
10
10
10
10
1
1
1
1
1
Myrmornis torquata
Corythopis torquata
Formicarius colma
Myrmeciza ferruginea
Conopophaga aurita
Hylopezus macularius
Formicarius analis
Grallaria varia
Myrmothera campanisona
Extinctions/colonizations
Location codeb
2
P
P
P
2
P
1
P
1
2/2
3304
2
P
P
2
P
P
2
P
P
3/0
2303
2
2
P
P
A
A
2
A
A
3/0
3209
2
2
P
P
P
2
A
P
A
3/0
1207
2
2
2
2
P
A
A
2
A
5/0
1202
2
2
2
2
2
2
A
P
A
6/0
2206
2
2
2
A
2
2
2
A
1
6/1
3114
2
2
2
2
2
A
2
A
A
6/0
2107
2
2
2
2
2
A
A
2
A
6/0
1104
2
2
2
2
2
2
A
2
A
7/0
1112
2
2
2
2
2
2
2
2
A
8/0
2108
Extinctions/
colonizations
11/0
9/0
7/0
7/0
7/0
5/0
5/1
4/0
0/2
55/3
a
2, present before isolation, absent after isolation (i.e., local extinction); 1, absent before isolation, present after isolation (i.e., colonization); P,
present before and after isolation; A, absent before and after isolation.
b
See Fig. 1.
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Volume 13, No. 6, December 1999
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Birds in Amazonian Forest Fragments
Stratford & Stouffer
and Myrmeciza ferruginea (one pair) were found in Cecropia forests. In 42 ha of Vismia-dominated vegetation,
only a single F. colma was detected.
Discussion
Figure 2. Species richness of nine terrestrial insectivores in 1-, 10-, and 100-ha fragments (circles) and
continuous forest control plots (squares) north of
Manaus, Brazil (11 fragments and 9 control plots).
Letters indicate significant differences between size
classes (all p , 0.05). Control plots had more species
than similar-sized fragments (p , 0.0001). In this
analysis the 50-ha control plot was combined with the
100-ha control plot because both had the full complement of species.
these species could have been overlooked in the pre-isolation survey.
Fifty-three ha of Cecropia-dominated vegetation was
sampled. Formicarius colma (two individuals or pairs),
Myrmothera campanisona (two individuals or pairs),
Table 2.
Three approaches have been used to study the effects of
fragmentation on forest taxa. One is to analyze patterns
of species richness in fragments of various sizes (e.g.,
Blake & Karr 1987). The drawback to this method is that
it is difficult to eliminate the effect of sampling area;
both fragmentation and decreasing sampling area should
result in decreasing species richness. Another method is
to sample fragments and similarly sized plots in continuous forest to test the hypothesis that fewer species are
found in fragments (e.g., Karr 1982). A weakness with
this and the first method is that the pre-isolation species
richness is unknown, so local extinction or colonization
after isolation cannot be shown directly. The third
method, sampling fragments before and after isolation,
can explicitly show changes after isolation (e.g., Stouffer
& Bierregaard 1995a).
We used all three methods to analyze terrestrial insectivorous bird distribution in Amazonian forest fragments. Both area effects and fragmentation effects were
significant; species richness increased with area, but
continuous forest plots always had more species than
did fragments of the same size (Fig. 2). More important,
comparing our surveys of the fragments with data collected in the same fragments before they were isolated
directly showed local extinction of most terrestrial insectivores in most of the fragments (Table 1).
We documented 55 cases of local extinction in the
fragments out of a possible maximum of 74 (74%). Our
extinction result is a minimum estimate because species
were more likely to be overlooked in the pre-isolation
mist-net surveys than in our intensive playback surveys.
Distribution of terrestrial insectivorous birds in plots within continuous Amazonian forest.a
Plot size (ha)
Species
Formicarius colma
Myrmeciza ferruginea
Conopophaga aurita
Myrmornis torquata
Grallaria varia
Hylopezus macularius
Corythopis torquata
Myrmothera campanisona
Formicarius analis
Total ssp.
Location codeb
a
b
P, present; A, absent.
See Fig. 1.
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Volume 13, No. 6, December 1999
100
50
10
10
10
10
1
1
1
P
P
P
P
P
P
P
P
P
9
1501a
P
P
P
P
P
P
P
P
P
9
1501b
P
P
P
A
P
A
P
P
A
6
1204
P
P
P
P
A
P
A
A
P
6
1501c
P
P
P
A
P
A
P
A
A
5
1205
P
P
P
P
A
A
A
A
A
4
1201
P
P
A
P
A
A
A
A
A
3
1501d
P
A
A
P
A
A
A
A
A
2
1501e
P
A
A
A
A
P
A
A
A
2
1501f
Stratford & Stouffer
The most extinction-prone species in our sample was
Myrmornis torquata, which was captured in all of the
fragments before isolation but was not recorded by us in
any fragments (Table 2). This species was regularly
present in control plots, so its loss from fragments seems
directly related to the fragmentation process. Not all
species were found in all fragments before isolation, so
we could also consider colonization. We found only
three colonizations for the 25 possible vacancies (12%)
based on the pre-isolation surveys. Two of these colonizations were by Myrmothera campanisona, a species
that prefers treefall gaps and edges (Stratford 1997).
The most dramatic effect of fragmentation was in the
1-ha fragments. All terrestrial insectivores recorded in
these fragments before isolation were later absent in our
surveys. The single terrestrial insectivore found in a 1-ha
fragment was an individual Myrmothera campanisona
that colonized after isolation. Terrestrial insectivores
fared only slightly better in 10-ha fragments, with 68% of
the original 25 occurrences resulting in extinctions. The
100-ha fragments lost 31% of the original 16 occurrences
of terrestrial insectivores, although both of the possible
empty sites were colonized.
Our descriptive studies do not reveal the mechanisms
responsible for species loss in this system, although we
have evidence that the combination of large territory
sizes, sedentary lifestyles, and strong preference for oldgrowth forest makes terrestrial insectivores vulnerable
to local extinction in small fragments (see also Mac Nally
& Bennett 1997). These species all use territories of at
least 5 ha, with territories of .20 ha sometimes found
for Myrmornis torquata and Formicarius analis (Stouffer 1997 and unpublished data; see also Terborgh et al.
1990). Thus, no terrestrial insectivore can maintain even
20% of a normal territory in 1-ha fragments, and 10-ha
fragments may be too small for even a single territory of
some species. In 100-ha fragments the local populations
comprise a maximum of about 10 pairs, and this would
apply only to Myrmeciza ferruginea and Formicarius
colma, the two most common species (Stouffer 1997
and unpublished data).
Small populations in fragments make these species
vulnerable to local extinction through demographic stochasticity, even if conditions are suitable for reproduction and survival (Bolger et al. 1991). In fact, we suspect
that fragmentation leads to decreased survival or reproductive success. Stratford (1997) showed that several
species of terrestrial insectivores use microhabitats that
are more common in continuous forest than in the fragments we studied. Some leaf litter arthropods are less
abundant in these fragments than in continuous forest
(Didham 1997). We do not know if these are important
resources for our study species, but there is evidence
from a temperate system of reduced food affecting
breeding of a terrestrial insectivore (Burke & Nol 1998).
Increased stress or reduced food may also be related to
Birds in Amazonian Forest Fragments
1421
reduced rates of feather growth in fragments for two
common species at our site ( J.A.S. and P.C.S., unpublished data).
Interactions with invasive birds from nonforested habitats probably do not threaten the species we studied, although the influence of invasive predators remains unknown. The parasitic cowbirds Molothrus bonariensis
and Scaphidura oryzivora were present at our sites, but
we have no evidence that cowbird parasitism is a significant effect here, especially compared to some temperate
systems (e.g., Robinson et al. 1995). In addition to being
uncommon at our sites (Cohn-Haft et al. 1997), these
cowbirds are unlikely to parasitize forest species (Sick
1993). Neither interspecific aggression nor resource exploitation from invasive birds (Ambuel & Temple 1983;
Grey et al. 1998) is likely to be a contributor to loss of
terrestrial insectivores at our sites because the forest understory is largely unused by birds after fragmentation
(Stouffer & Bierregaard 1995a; Stouffer & Borges 2000).
We have no data on predation on nests or adults, but
other Neotropical work suggests that predation is likely
higher in fragments than in continuous forest (Loiselle &
Hoppes 1983; Sieving 1992; Sieving & Karr 1997).
Our data also show that terrestrial insectivores generally avoid second growth (Borges 1995; Stouffer & Borges
2000). Like most other understory birds at our site, they
are more likely to be found in Cecropia- than in Vismiadominated growth (Stouffer & Bierregaard 1995a). Second-growth avoidance has two negative effects on persistence in fragments. First, birds in fragments cannot
augment their territories by using multiple fragments or
adjacent second growth (e.g., Howe 1984). Second, it
reduces colonization of fragments from nearby continuous forest. Results of long-term mist-net surveys show
that the abundance of terrestrial insectivores declines
gradually in fragments, even when rapidly growing second growth provides a link to continuous forest as little
as 75 m away (Stouffer & Bierregaard 1995a). This link
allows recolonization by some forest birds, suggesting
that other taxa are less specific in the habitats they will
cross. Most Amazonian forest understory species have
probably had little need to cross open or nonforested areas in their evolutionary history, so unwillingness to
leave old-growth forest cover may be an innate behavioral response (Greenberg 1989; see Sieving et al. 1996).
Because these species do not migrate, there is no mechanism for recolonization of truly isolated fragments, a
phenomenon that occurs annually in some temperatezone systems (Blake & Karr 1987). In addition to direct
avoidance, some species may be unable to use secondary growth areas because of constraints of morphology
or behavior (Winkler & Leisler 1985). For example, Myrmornis torquata, a bird that forages by tossing leaves, is
probably unable to manipulate the large fallen leaves of
Cecropia that dominate the litter of some secondary forests at our site.
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Birds in Amazonian Forest Fragments
If allowed to grow, second growth from logged areas
or abandoned cattle pastures will eventually converge
on the old-growth forest in our continuous forest sites,
but we predict that terrestrial insectivores will be
among the last birds to be able to use regenerated forest
(see also Loiselle & Blake 1994; Borges 1995). At the moment, we cannot tell how long it will take for the study
species to use second growth; we have seen little use of
second growth that has been growing for 15 years. Regardless of how these areas take to become suitable,
throughout the regrowth period terrestrial insectivores
will have little demographic linkage among fragments,
so subpopulations will remain isolated, small, and vulnerable to local extinction. Those subpopulations that
do persist also may be vulnerable to the genetic effects
of inbreeding (Frankham 1996), although we know too
little about demography to estimate this effect.
Our results demonstrated a rapid and pronounced loss
of ground-foraging, insect-eating birds after isolation of
Amazonian forest fragments. This augments a growing
body of evidence suggesting that terrestrial insectivores
are exceptionally vulnerable to forest fragmentation
(e.g., Karr 1982; Recher & Lim 1990; Stouffer & Bierregaard 1995a; Canaday 1996). In the landscape we studied, the fragments where birds went extinct were demographically isolated from the vast adjacent areas of
continuous forest where the birds persisted (Table 2;
Fig. 1). From this observation, we conclude that fragments of 1–100 ha will contribute little to the long-term
persistence of populations of these species, even in a
minimally fragmented landscape.
Acknowledgments
We thank R. Bierregaard and the banders and mateiros
who collected the mist-net data. C. Gascon and the Associação de Levantamento de Amazonas staff facilitated our
fieldwork. Reviews by D. Saunders and two anonymous
reviewers improved the manuscript. Financial support for
our surveys was provided by the Biological Dynamics of
Forest Fragments Project and Southeastern Louisiana University. This is publication number 233 in the BDFFP
Technical Series.
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