Bird Extinctions in Atlantic Forest Fragments
of the Viçosa Region, Southeastern Brazil
RÔMULO RIBON,∗ †§ JOSÉ EDUARDO SIMON,‡ AND GERALDO THEODORO DE MATTOS†
∗
Programa de Pós-Graduação em Ecologia, Conservação e Manejo de Vida Silvestre, Instituto de Ciências
Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte-MG, 31270–901, Brazil
†Museu de Zoologia João Moojen de Oliveira, Centro de Ciências Biológicas, Universidade Federal de Viçosa, Vila Gianetti 32,
Viçosa-MG, 36570–000, Brazil
‡Museu de Biologia Prof. Mello Leitão, Avenida José Ruschi, 4, Santa Teresa-ES, 29650–000, Brazil
Abstract: We studied the conservation status of Atlantic forest birds in 43 forest fragments ranging in size
from 1 to 384 ha in the Viçosa region of southeastern Brazil. We compared data from 15 years of field
work with historical records from the region, mainly originating from specimens collected by João Moojen
during the 1930s. We used published studies associated with museum data and current field work to assess
the decline of forest birds during the last 70 years and to relate their disappearance to forest fragmentation
and destruction. At least 28 bird species have become locally extinct, 43 are critically endangered, and 25 are
vulnerable, representing 60.7% of the original forest bird community known to exist in the region. Vulnerability
to fragmentation differed among guilds, forest strata, and endemicity status. Birds that feed on fruit and seeds,
and those that feed on insects, were more threatened than omnivores and carnivores. Nectarivorous species
were less threatened than other guilds. Moreover, terrestrial and understory birds or birds using only one forest
stratum also were more likely to have been threatened. Finally, Atlantic forest endemics were more likely to
have become extinct than nonendemic species. In general, sensitivity to environmental disturbance at the local
level was similar to the predicted vulnerability to regional disturbance derived from the literature. Our results
indicate that a serious decline of Atlantic forest birds is underway and that many other species of birds, not
previously recognized as threatened, are of conservation concern.
Key Words: Atlantic forest, bird diversity, Brazil, foraging strata, extinction, forest fragmentation
Extinciones de Aves en Fragmentos de Bosque Atlántico de la Región de Viçosa, Sureste de Brasil
Resumen: Estudiamos el estado de conservación de aves de bosque atlántico en 43 fragmentos de 1 a 384
ha en la Región Viçosa, al sureste de Brasil. Comparamos datos de 15 años de trabajo de campo con registros
históricos de la región, principalmente de especimenes colectados por João Moojen durante la década de los
años 30. Utilizamos estudios publicados asociados con datos de museo y de trabajo de campo reciente para
analizar la disminuición de aves de bosque durante los últimos 70 años y para relacionar su desaparición
con la fragmentación y destrucción del bosque. Se han extinguido por lo menos 28 especies de aves localmente,
43 están crı́ticamente en peligro y 25 son vulnerables, lo cual representa el 60,7% de la comunidad de aves de
bosque conocida para la región. La vulnerabilidad a la fragmentación fue diferente entre gremios, estratos de
bosque y estado de endemismo. Las aves que se alimentan de frutos y semillas y aquéllas que se alimentan
de insectos están más amenazadas que las omnı́voras y carnı́voras. Las especies nectarı́voras están menos
amenazadas que otros gremios. Más aun, las aves terrestres y de sotobosque o las que utilizan sólo un estrato
del bosque también tienen mayor probabilidad de estar amenazadas. Finalmente, las aves endémicas al
bosque atlántico tienen mayor probabilidad de extinción que las no endémicas. En general, la sensibilidad a
la perturbación ambiental a nivel local fue similar a la vulnerabilidad a la perturbación regional predicha,
§Current address: R. Ver. José Valentino da Cruz, 54/204 36570–000, Viçosa–Minas Gerais, Brazil, email [email protected]
Paper submitted August 6, 2001; revised manuscript accepted February 12, 2002.
1827
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Volume 17, No. 6, December 2003
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Atlantic Forest Bird Extinction
Ribon et al.
derivada de la bibliografı́a. Nuestros resultados indican que existe una seria declinación de aves de bosque
atlántico y que muchas otras especies de aves, no reconocidas como amenazadas previamente, son de interés
para la conservación.
Palabras Clave: Bosque atlántico, Brasil, diversidad de aves, estratos de forrajeo, extinción, fragmentación de
bosque
Introduction
Destruction and fragmentation of tropical forests are the
main cause of species loss throughout the world (Turner
& Corlett 1996). The few initial studies on the subject focused primarily on birds in Manaus, Brazil, but these have
been augmented by studies on many organisms throughout the world (e.g., Rosenfield et al. 1992; Turner 1996;
Laurance & Bierregaard 1997; Laurance 1999).
The abundance of bird species in forest fragments increases immediately after their isolation and then, after a
short period, is reduced to levels below those found in
the previously continuous forest (Bierregaard & Lovejoy
1989; Hagan et al. 1996). Fragmentation therefore results
in reduced population size and an increased vulnerability
to the “immediate causes of extinction,” such as stochastic events (disease outbreaks, hurricanes, and fires) (Simberloff 1988, 1994). The tendency of birds to become extinct in fragmented landscapes has been attributed to endemism, habitat specialization, life-history characteristics
(e.g., survival rates, clutch size, ground-nesting behavior),
foraging strata, body size, low dispersion capacity, diet,
taxon, and association with other species (Willis 1979;
Diamond 1981; Bierregaard & Lovejoy 1989; Kattan et al.
1994; Goerck 1997; Sieving & Karr 1997; Renjifo 1999;
Villa & Zabala 2000).
Only 7% of the Atlantic forest remains (da Fonseca
1985; Mittermeier et al. 1999), and <1% is considered
pristine (Secretaria de Estado do Meio Ambiente 1996).
This high level of destruction and large number of rare and
endemic taxa in the Atlantic forest have led conservation
biologists to warn that a large number of bird species may
quickly become extinct (Brooks & Balmford 1996; Stotz
et al. 1996; Goerck 1997; Mittermeier et al. 1998).
Comparisons between historical records and recent
field inventories are important to our understanding of
the extinction process. However, this method is underemployed in South America because of the lack of
historical data. As a result, few papers have addressed
bird extinction in the continent (Leck 1979; Willis 1979;
Kattan et al. 1994; Christiansen & Pitter 1997; Robinson
et al. 2000; Villa & Zabala 2000).
We documented the local extinction and decline of
bird species in the Atlantic forest in southeastern Brazil.
We tested several correlates of vulnerability to fragmentation as a function of ecology (trophic guilds and foraging strata) and geographical distribution (endemism).
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Volume 17, No. 6, December 2003
We also determined whether local threat status can be
predicted from reported sensitivity to environmental disturbances in the Neotropics or at a regional level (derived
from Parker et al. 1996).
We tested the following hypotheses: (1) differential extinction exists among species of different trophic guilds
and vegetation strata; (2) species that forage in only one
strata are more sensitive to forest fragmentation and destruction and are therefore more prone to become locally threatened than species that forage in two strata; (3)
Atlantic forest endemic species are more sensitive than
nonendemic species; and (4) the local conservation status
of birds in the Viçosa region is consistent with global sensitivity to environmental disturbance as scored by Parker
et al. (1996). Because of the consistency between regional
and local sensitivity, species considered by these authors
as having low, medium, and high sensitivity would show
similar differential response to habitat disturbance in the
study area.
Study Area
We conducted our study in forest fragments in the townships of Cajuri (lat 20◦ 47 S, long 42◦ 49 W), Paula Cândido
(lat 20◦ 49 S, long 42◦ 56 W ), and Viçosa (20◦ 45 S, long
42◦ 52 W) in southeastern Minas Gerais, Brazil (Fig. 1).
The study area, in the upper Rio Doce basin, covers
roughly 120 km2 in the hilly “Zona da Mata” region. The
original vegetation was submontane, semideciduous forest with strong floristic links to lowland rain forests of
Espı́rito Santo and southern Bahia states (Oliveira-Filho
& Fontes 2000). Currently, secondary forest fragments
remain dominated by arboreal species such as Anadenanthera sp., Newtonia sp., Piptadenia sp. (LeguminosaeMimosoidae), Cecropia spp. (Moraceae), Xilophia sp.
(Annonaceae), and Mabea fistulifera (Euphorbiaceae)
(A. F. Silva, personal commentary). According to longtime landowners, most of the current fragments are 20–
60 years old, although some are 70–90 years old. Pristine
vegetation is extremely rare (<1% of the fragments).
The climate is mesothermic humid, with rains concentrated in the summer, dry winters, and mean temperature of the warmest month higher than 22◦ C (Cwa in
Köppen’s classification) (Vianello & Alves 1991). Monthly
precipitation varies from 19 mm ( June) to 245 mm (December), and mean annual rainfall is 1221 mm. Minimum
Ribon et al.
Atlantic Forest Bird Extinction
1829
Figure 1. Location of Viçosa
study area where birds have
been sampled.
and maximum mean temperatures are 15.4◦ C ( July) and
22.3◦ C (February). The annual mean temperature is 19.4◦
C, and relative humidity reaches 81% (Departamento Nacional de Meteorologia 1992). Elevation varies between
550 and 750 m above sea level.
History of the Destruction and Fragmentation of the Region
In 1817 the region was probably dominated by pristine
forests with a few small farms (von Spix & von Martius
1976) and, likely, some small, scattered patches of secondary forest resulting from subsistence agriculture by
indigenous people (Dean 1996). Large-scale destruction
and fragmentation of the forest began in earnest in the
1870s, when extensive coffee plantations in Minas Gerais
State were planted (Valverde 1958). By 1930 most of the
current forest fragmentation had occurred (Comissão Geographica e Geológica de Minas Geraes 1930). Since 1930
the number of forest fragments in the region has probably increased as old coffee plantations regenerated (R.
R. & C. R. M. Abreu, unpublished data). Currently, forest
fragments cover approximately 33% of the study area (Ribon 1998; Pereira 1999). Most fragments are smaller than
50 ha, but a few larger fragments exist that cover up to
380 ha (Pereira 1999; R. R. & C. R. M. Abreu, unpublished data). Most fragments are still subjected to fire,
logging, selective wood exploitation, invasion by cattle,
and poaching. Almost all forest remnants are located on
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Atlantic Forest Bird Extinction
hillsides and hilltops, rarely in ravines, and extremely
rarely in the lowlands (Valverde 1958; Ribon 1998).
In the beginning of the twentieth century, the vegetation and land-use patterns around the forest fragments
consisted mainly of coffee plantations, pasturelands of
Melinis minutiflora, small orchards, and some subsistence crops (corn, rice, and beans) (Valverde 1958). This
landscape remains essentially unchanged, except for the
introduction of a few small eucalyptus plantations (Eucalyptus spp.) and some abandoned pastures (scrubs or
capoeiras) (Ribon 1998; Pereira 1999).
History of Ornithological Studies in the Region
The first ornithological records in the area date from
1932–1936 (Moojen 1943; collection of the Museu de Zoologia João Moojen de Oliveira, Universidade Federal de
Viçosa [MZ-UFV]; and specimens at Museu Nacional do
Rio de Janeiro– [MNRJ]). Entomologist J. C. Carvalho sporadically collected birds between 1937 and 1938 (specimen labels at MZ-UFV). From 1959 to 1963 and 1966 to
1967, H. T. Erickson watched birds in the region. He was
followed by R. E. Mumford. Between 1966 and 1973 Mumford collected some specimens, which were deposited
at MZ-UFV, Purdue University Wildlife Laboratory, and
Academy of Natural Sciences of Philadelphia (Erickson
& Mumford 1976). Other surveys were conducted during
the 1980s and 1990s (Monteiro et al. 1983; Monteiro & de
Mattos 1984; Cândido 1988; Vieira et al. 1992). More detailed ecological studies were conducted in the region in
the latter 1990s by Ribon (1998) and Maldonado-Coelho
(2000).
Methods
We determined the threatened status of birds in the region
by comparing field studies conducted during the last two
decades (1986–2000) with historical records from published accounts and museum data. Our primary historical
records are based on the 328 specimens of 92 species
collected by Moojen and Carvalho. Current records are
based on our observations in five fragments (1986–1995)
and later in 41 fragments by R.R. (1996–1999). Three of
the fragments R.R. studied during the latter period were
the same as those sampled from 1986 to 1995. From 1986
to 1995, we conducted observations almost weekly (approximately 5 hours/week) during early morning (0500–
1000 hours) and late afternoon (1600–1900 hours),
mostly at the largest and more protected fragments. From
1996 to 1999, R.R. distributed 236 point-count stations
among 41 fragments and sampled these stations for 10
minutes six times each. Sampled fragments ranged from
1 to 384 ha. Approximately 8000 hours of observations
were conducted during the 15 years of research.
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Ribon et al.
In the present analysis we included only species categorized as forest species in the literature (Parker et al.
1996; Goerck 1997; Sick 1997) or according to our field
experience (Simon et al. 1999). Some species that occur
in open vegetation in other biomes were recorded only in
forest fragments during our study; we considered these
to be forest species. Species of indeterminate status were
not considered in the statistical analysis.
We also did not consider habitat generalists because our
aim was to discuss the situation of forest birds. We define
habitat generalists as those species that occur commonly
outside forest fragments, based on literature accounts or
field observations.
We based the local conservation status of forest species
on the number of records and/or the number of forest
fragments in which each species was observed. We arbitrarily defined five categories of local conservation status, analogous to those defined by the World Conservation Union (1994, 1996) but with necessary adjustments required by the scale of the work: (1) extinct, no
records during the last 15 years; (2) critically endangered,
1–10 records during the last 15 years or 1–50 records
from three or fewer forest fragments; (3) vulnerable, 11–
50 records during the last 15 years or >50 records in
only four to eight forest fragments and/or under strong
pressure from poaching and the illegal pet trade; (4) indeterminate, nocturnal forest species with few records
(amount of nocturnal field work was insufficient for analysis); (5) not threatened, ≥50 records or recorded in more
than eight sites. In category 5 we also included some
species assigned by Parker et al. (1996) as forest species
that were recorded in our study area just outside forest
habitats. We used the term threatened when referring to
extinct, critically endangered, and vulnerable species.
We based a species’ susceptibility to extinction on four
parameters: (1) trophic guild, (2) foraging strata; (3) Atlantic forest endemism, and (4) sensitivity to environmental disturbance. Trophic guilds were defined according to literature accounts (Moojen et al. 1941; Schubart
et al. 1965; Motta 1990; Collar et al. 1992; Remsen et al.
1993; Sick 1997), data labels in the scientific collections of the MZ-UFV, MNRJ, Museu de Biologia Mello
Leitão (MBML) (Santa Teresa-ES, Brazil), and Universidade Federal de Minas Gerais (Belo Horizonte-MG, Brazil),
and our field observations. We used the following guild
categories: carnivorous, insectivorous, omnivorous, nectarivorous, and frugivorous/granivorous. Foraging strata
follows that of Parker et al. (1996) (five categories): terrestrial, understory, medium stratum, canopy, and aerial.
We also followed Parker et al. (1996) for Atlantic forest endemics (endemic or not endemic) and for degree
to which species were sensitive to environmental disturbances (low, medium, and high). We used chi-square
goodness-of-fit tests to examine whether or not birds from
different groups were differentially threatened. It was not
our aim to control for phylogeny.
Ribon et al.
Global, national, and state conservation status of the
species followed BirdLife International (2000), Bernardes
et al. (1990), and Lins et al. (1997). We followed Parker
et al. (1996) for conservation priority ranking in the
Neotropical region. Nomenclature mainly follows that of
Sick (1997), but we also followed Raposo (1997) for Arremon (Emberezidae). We identified species subject to
poaching or the illegal pet trade based on interviews
with local landowners, some of them ex-hunters and birdcatchers, and confirmed exploitation, for some species,
through direct observations.
Results
Local Conservation Status of Forest Birds
We recorded 221 bird species in the forest fragments: 58
habitat generalists and 163 forest birds (Appendices 1 &
2). Among the forest species, 28 (17.2%) were already locally extinct, 43 (26.4%) were critically endangered, and
25 (15.3%) were vulnerable. Thus, a total of 96 (59%)
taxa were considered threatened. Five species (3%) were
of indeterminate status, and the remaining 62 (38%) were
not threatened (Appendix 1). Literature accounts include
another 24 forest species known from only one record.
We considered these 24 species as either vagrants, incorrect additions to the area, or misidentified birds (Ribon
1998 and unpublished data). Consequently, we excluded
these species from our analysis based on our field experience and on their range given by Pinto (1952, 1978),
Mitchell (1957), Ridgely and Tudor (1989, 1994), Sick
(1997), and Parker et al. (1996). Their exclusion was necessary to avoid incorrectly labeling species as extinct or
threatened.
Among the 96 locally threatened species, 6 (Claravis
godefrida, Leucopternis lacernulata, Biatas nigropectus, Onychorynchus swainsoni, Lipaugus lanioides, and
Amazona vinacea) were threatened, and 7 (Tinamus
solitarius, Piculus aurulentus, Baillonius bailloni, Drymophila ochropyga, Procnias nudicollis, Psiloramphus
guttatus, and Amaurospiza moesta) were near threatened at the global level (BirdLife International 2000);
and 16 were threatened at the national level (Bernardes
et al. 1990) (Appendix 1). Twenty species were threatened and 12 were considered “presumably threatened”
at the state level (Lins et al. 1997). Among the latter,
6 (Columba plumbea, Pyrrhura frontalis, Melanerpes
flavifrons, Philydor lichtensteini, Hemitriccus diops,
and Passerina brissonii) were already extinct in the
Viçosa region, 7 were critically endangered (Spizaetus
ornatus, S. tyrannus, Lophornis magnifica, Ramphastos
vitellinus, Chamaeza meruloides, Cranioleuca pallida,
and Sclerurus sacansor), and 1 (Drymophila ferruginea)
was vulnerable (Appendix 1). In contrast, 18 of the 28 locally extinct species, 31 of the 43 critically endangered
Atlantic Forest Bird Extinction
1831
species, and 21 of the 25 vulnerable species were not
threatened in the state. Of the 31 forest species in our
study of conservation priority in the Neotropics (Parker et
al. 1996), 22 were medium-priority, 8 were high-priority,
and 1 was assigned to the urgent category (Appendix 1).
Until a few decades ago, five locally extinct species
(Tinamus solitarius, Odontophorus capueira, Columba
plumbea, Procnias nudicollis, and Passerina brissonii)
suffered from poaching or collection for the pet trade by
local people. Those activities seemed to occur until the
1960s, when the disappearance of those species forced
people to stop their persecution. According to landowners, however, T. solitarius and P. nudicollis, seemed to be
eliminated before the 1960s. Poaching for meat and collecting for the pet trade continues for nine locally threatened species (meat, Crypturellus obsoletus, Penelope
superciliaris, Penelope obscura, Leptotila rufaxilla,
Chamaeza meruloides; pet trade, Amazona vinacea,
Propyrrhura maracana, Ramphocelus bresilius, and
Saltator similis) (Appendix 1).
Extinction Patterns
Among frugivores/granivores, a significant number of
species (84.4%) were threatened to some extent (χ 2 =
8.98, df = 1, p = 0.002), and a significant number (34.4%)
have become extinct (χ 2 = 7.07, df = 1, p = 0.007).
Among the insectivores, 51.4% were threatened, a significantly higher proportion than in the other guilds (χ 2 =
4.81, df = 1, p = 0.028). Despite the high proportion of
carnivores threatened (85.7%), they were only marginally
more threatened than expected (χ 2 = 3.57, df = 1,
p = 0.058). Omnivores were not more threatened than expected by chance (χ 2 = 0.452, df = 1, p > 0.50), whereas
nectarivores were marginally less threatened than other
guilds (χ 2 = 3.31, df = 1, p = 0.068), although this was
based on a single threatened species (20%) (Fig. 2).
Terrestrial and understory species had relatively more
threatened species (82.6%, χ 2 = 5.03, df = 1, p = 0.024;
44.7%, χ 2 = 7.201, df = 1, p = 0.007) than did birds that
used medium, canopy, and aerial strata (χ 2 = 0.94, df = 1,
p = 0.331; χ 2 = 0.146, df = 1, p = 0.702; and χ 2 = 0.144,
df = 1, p = 0.703, respectively) (Fig. 2). Birds that used
only a single stratum (67%) were more threatened than
those that used two strata (50%), a significant difference
(χ 2 = 4.42, df = 1, p = 0.035).
Atlantic forest endemics had proportionally more
threatened species (68.8%) and extinct species (29.5%
of endemic species were extinct, and 62% of the extinct species were endemic) than did nonendemic species
(11.3% of nonendemics were extinct, and 37.9% of the extinct species were nonendemics) (χ 2 = 8.17, df = 1, p =
0.004) (Fig. 3).
We compared the sensitivity status of Parker et al.
(1996) for locally threatened and nonthreatened or locally
extinct and nonextinct taxa. In both cases, more of the
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Atlantic Forest Bird Extinction
Ribon et al.
Figure 2. Percentage of
threatened species in (a)
each guild ( V,
furgivores/granivores; C,
carnivores; O, omnivores; I,
insectivores; N, nectarivores)
and ( b) different strata (T,
terrestrial plus terrestrial
and some other strata; U,
understory plus understory
and some other strata; M,
midstory plus midstory and
some other strata; C, canopy
plus canopy and some other
strata; A, aerial plus aerial
and some other strata).
locally threatened taxa (χ 2 = 8.20, df = 2, p = 0.016) or
extinct taxa (χ 2 = 14.50, df = 2, p = 0.0007) were found
among more sensitive categories. Among them, 44.2% of
Parker et al.’s (1996) low-sensitivity status, 64.2% of the
medium-sensitivity status, and 80% of the high-sensitivity
status were locally threatened.
Discussion
Conservation Status
Figure 3. Percentage of threatened species among
endemic (En) and nonendemic (N En) species in
forest fragments of the Visçosa region, Brazil, and
percentage of extinct speices among endemic and
nonendemic species.
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Volume 17, No. 6, December 2003
In our study area, the Atlantic forest contains an astonishing number and percentage of locally threatened species.
And this number is likely conservative because other
widespread forest species that probably occurred in the
area (such as Harpy Eagle [Harpia harpyja]) or some elusive species (Phylloscartes flycatchers) have never been
recorded by researchers, likely because they were extirpated prior to the 1930s (or after) or because these
species are rare in tropical forests everywhere (Terborgh
et al. 1990; Robinson et al. 2000).
The Viçosa region, where this research was conducted,
maintains some of the highest percentages of Atlantic forest in Minas Gerais (Ribon 1998; Pereira 1999). Consequently, our results likely represent an optimistic view of
the overall status of many of the species in the Atlantic
forest (Willis 1979; Christiansen & Pitter 1997).
The majority of ornithological studies of Atlantic forest bird communities were conducted in reserves, which
still preserve large subsets of their original species assemblages and are far more “attractive” to ornithologists and
birdwatchers than fragmented and degraded areas. Such
areas are the exception rather than the rule in the Atlantic
forest. Although many species in fragmented landscapes
are declining, they receive little attention or protection.
Because many of these species are still frequently seen in
reserves, their vulnerability has not yet been perceived.
After Willis’s (1974) work in Barro Colorado Island, Robinson (1999) demonstrated, as in our study, that extinction
in tropical forests is an extremely persistent process, with
few chances for the species’ reestablishment.
Ribon et al.
Extinction Patterns
GUILD VULNERABILITY
Frugivorous and granivorous birds were particularly sensitive to habitat degradation. This trend has also been noted
by others (Willis 1979; Thiollay 1992; Kattan et al. 1994;
Goerck 1997; Renjifo 1999). Additionally, two omnivorous birds that feed mostly on fruits were locally extinct
(Trogon viridis and T. rufus). Insectivorous species were
also sensitive to fragmentation, as has been shown by
other studies in the Neotropics (Willis 1979; Kattan et al.
1994; Stouffer & Bierregaard 1995; Bierregaard & Stouffer 1997; Goerck 1997) and in sites with “sustainable”
forestry (Thiollay 1992).
Carnivorous species were not more threatened than expected by chance. However, many forest-dwelling raptors
are especially affected by forest fragmentation and disturbance because of their natural rarity and their susceptibility to hunting in fragmented areas (Willis 1974, 1979; Leck
1979; Thiollay 1989, 1992; Sick 1997; Renjifo 1999). Accipiter poliogaster, an extremely rare species (Robinson
1994), is extinct in the region and is considered extinct in
the state of Minas Gerais (Vasconcelos 1998). Three other
large forest raptors, Spizaetus tyrannus, Spizaetus ornatus, and Spizastur melanoleucus, are threatened with
extinction at the state and/or national level (Bernardes
et al. 1990; Lins et al. 1997). Records during the last 15
years indicate these species still occur in the area. Two
records of juveniles of S. ornatus from 1998 suggest that
the species breeds in the area and that successful reproduction might be maintained in moderately fragmented
landscapes (Andrén 1994).
Omnivores are normally known for their strong resilience to forest fragmentation (Willis 1979; Goerck
1997; Renjifo 1999), as we found for Viçosa’s birds.
Lophornis magnifica, an inconspicuous species, was the
only locally threatened hummingbird. Our results support
the conclusion that nectarivorous birds are weakly affected by forest fragmentation (Kattan et al. 1994; Bierregaard & Stouffer 1997; Renjifo 1999; but see Willis 1979).
Atlantic Forest Bird Extinction
1833
areas these species are susceptible to “mesopredator effects” (Terborgh 1992). These effects occur when large
predators are removed, allowing smaller predators, which
depredate nests and birds, to become more common. Although an experiment in 18 of the 45 forest fragments we
surveyed did not show any difference in predation rates in
different fragment size classes (Leite & Marini 1999), it is
plausible that predation rates in the landscape as a whole
were already high enough to have affected terrestrial forest bird populations. In addition, the intense grazing by
cattle in almost all fragments destroys or strongly modifies foraging and nesting microhabitats for birds (Naranjo
2000).
Although all medium-stratum species were not sensitive, many species that use that stratum were critically endangered or vulnerable (e.g., Micrastur ruficollis, Campephilus robustus, Xiphocolaptes albicollis, and
Pyroderus scutatus), and others are extinct (e.g., Trogon
rufus, Philydor atricapillus, and P. lichtensteini). The
elimination of food sources, nesting microhabitats, and
other crucial resources was probably the main reason for
the decline of medium-stratum species in the study area.
It is possible, however, that their sensitivity might be due
to characteristics other than stratum.
Understory species are frequently considered sensitive, especially the insectivores and bamboo and vinetangle specialists (Willis 1979; Stotz et al. 1996). Many
of the Viçosa’s locally extinct or critically endangered
understory species were associated with bamboo (Claravis godefrida, Dromococcyx pavoninus, Psilorampus
guttatus, Syndactila rufosuperciliata, and Hemitriccus
diops). Bamboo specialists that seek seed booms in dying
bamboo stands or that search for insects in live stands depend on the spatial and temporal distribution of the scattered bamboo patches in the forest matrix (Janzen 1976).
By creating a hostile matrix and destroying considerable
amounts of bamboo stands, forest fragmentation disrupts
the temporal and spatial distribution of bamboos, making
them more difficult for specialized birds to track.
ATLANTIC FOREST ENDEMICS
FORAGING STRATA
Birds that exploit different strata respond differently to
habitat disturbance (Willis 1979; Karr 1982; Bierregaard
& Lovejoy 1989; Sieving & Karr 1997). However, the association between the number of strata and vulnerability,
as found in this study, is not indicated in the literature.
Species that use two strata or more were less affected
than those occupying one stratum, possibly because of
the greater ecological plasticity of the first group, which
buffers species from habitat alterations.
Terrestrial species, especially those that feed on insects,
are highly prone to extinction in fragmented areas (Willis
1979; Sieving & Karr 1997; Renjifo 1999). In fragmented
Atlantic forest endemic species are more threatened than
nonendemic species (Brooks & Balmford 1996; Stotz
et al. 1996; Goerck 1997). As in the Viçosa region, endemics as a group are sensitive to disturbance in Tanzania
(Newmark 1991) and Colombia (Renjifo 1999; Villa
& Zabala 2000), although not on a Chilean island ( Willson
et al. 1994, but see Frankham 1998).
Species losses caused by the loss of other species
are difficult to prove, but some clues are in the literature (Bierregaard & Lovejoy 1989; Terborgh 1992). Some
species that disappeared from the Viçosa region are common mixed-species flock members, such as Pachyramphus castaneus, which is associated with Philydor rufus and Cranioleuca pallida (Willis 1989; R.R., personal
Conservation Biology
Volume 17, No. 6, December 2003
1834
Atlantic Forest Bird Extinction
observation), both of which are critically endangered in
our study area. Other examples are Philydor atricapillus, a nuclear species in mixed-species flocks of Atlantic
forests (Develey 1997), and Phylidor lichtensteini and Biatas nigropectus, which are also extinct in the Viçosa region and are members of mixed-species flocks elsewhere
(Willis 1989). At least for these species it is possible, therefore, that the loss of one or more species in the Viçosa region could have led to the disappearance of others, as suggested by Bierregaard and Lovejoy (1989) and Bierregaard
and Stouffer (1997) for Amazonian birds. The presence
of understory mixed-species flocks in some of the fragments we sampled is determined by the presence of the
Red-crowned Ant-tanager (Habia rubica), an already vulnerable species in our classification (Maldonado-Coelho
2000). In French Guyana, mixed-species flocks are extremely sensitive to disturbance caused by selective logging (Thiollay 1992).
RELATIONSHIP BETWEEN EXTINCTION AND LOSS OF LOWLAND AND
FLOODPLAIN FORESTS
Because the current landscape in the study area is almost
completely lacking lowland and ravine forest patches, one
would expect that species showing association with these
habitats would be especially prone to local extinction.
Specialization of birds in large forested floodplains in tropical forests, such as the Amazon basin, is well known (e.g.,
Novaes 1970; da Silva & Constantino 1988; Terborgh et
al. 1990; Sick 1997). However, a more subtle association
between antshrikes and antvireos (Thamnophilidae) and
more humid parts of forest fragments in ravines and lowlands was recently found in the study area (Ribon 1998). A
similar pattern was reported for Barro Colorado, Panama
(Robinson et al. 2000), and occurs among species of other
families (R.R., unpublished data).
Because of this association, we suggest that many extinctions may result from the loss of the floodplains and
lowland parts of the forest in the Viçosa region. This realization has important implications for conservation planning in tropical areas. As in our study area, forests are often left only on hillsides and along hilltops. In these areas,
forests in floodplains, lowlands, and ravines are cleared
and used for agriculture and cattle grazing.
EFFECT OF HUNTING AND TRADE ON BIRDS
Bird hunting and collection for the pet trade has had a
strong influence on the population decline of a number
of bird species (BirdLife International 2000). Based on
information gathered in interviews, some of these hunted
and traded species occurred in considerable numbers in
the Viçosa region until a few decades ago, a long time
after the first large colonization wave.
Although still common in the study area, Saltator similis is currently the songbird considered most valuable
Conservation Biology
Volume 17, No. 6, December 2003
Ribon et al.
and is sought after by bird trappers (R.R., unpublished
data). If the pressure on its population continues, we expect its complete extirpation in the area, as has happened
to Cyanocompsa brisonii and Oryzoborus angolensis.
Both species are among the most appreciated Brazilian
songbirds. Oryzoborus angolensis, an inhabitant of cattail swamps, is also extinct in the Viçosa region (unpublished data) and in almost the entire state of Minas Gerais
(Machado 1998).
EXTINCTION OR RECOLONIZATION?
Many of the fragments in the study area are only 20–
70 years old (Ribon 1998) and have apparently regenerated following a more widespread deforestation. We
believe that, some decades ago, the number and percent
cover of forest fragments in the area was smaller than
it is currently. Among this smaller number of fragments,
however, we expected a higher proportion to be larger
and to have a vegetation structure more closely approximating natural conditions, judging from the bird species
collected by Moojen. Consequently, we hypothesize that
local extinction reflects the difficulties of some species
in recolonizing regenerated patches. If this is true, reintroductions may be possible, and regional diversity may
increase as species gradually recolonize the area. An alternative hypothesis is that there were always many fragments available and that the structure of the landscape
has not changed over the past decades. In this case, extinction is an ongoing process related to small population
size and fragmentation, and more extinctions are to be expected. These two hypotheses are not mutually exclusive
and may be species dependent.
The extirpation of subpopulations of a given species
will eventually lead to its extinction (Caughley 1994;
Simberloff 1994; Sisk et al. 1994). Our results demonstrate that a large number of species, many of which
are considered stable or safe in the Atlantic forest, are
becoming extinct in fragmented areas, and they reinforce the idea that many Atlantic forest birds are on their
way to complete extinction (Terborgh 1992; Brooks &
Balmford 1996; Goerck 1997).
Species with small populations or restricted distributions are often more sensitive to extinction (e.g.,
Caughley 1994; Sisk et al. 1994; Lawton 1995). If this
generalization is valid for Atlantic forest birds—and there
is no reason to think otherwise— some opinions (e.g., Simon & Wildawsky 1993; Budiansky 1994) consider recent
previsions on current species extinctions to be overestimated must be revised.
Acknowledgments
The following organizations contributed financial support to R.R. and/or J.E.S. during different periods of this
Ribon et al.
work: Conselho Nacional de Desenvolvimento Cientı́fico
e Tecnológico (CNPq), Comissão de Aperfeiçoamento
de Pessoal de Ensino Superior, U.S. Fish and Wildlife
Service (USFWS)/Fundação Bioversitas/Programa de PósGraduação em Ecologia, Conservação e Manejo de
Vida Silvestre at Universidade Federal de Minas Gerais
(ECMVS-UFMG), American Bird Conservancy (Project
PMAY 00396), CNPq/Programa Nacional de Biodiversidade/Ministério do Meio Ambiente, and the “Programa
Natureza e Sociedade” of the World Wildlife Fund/U.S.
Agency for International Development project CSR 142–
00). The USFWS/Fundação Biodiversitas/ECMVS-UFMG
Program contributes to the implementation of the Convention on Nature Protection and Wildlife Preservation in
the Western Hemisphere (1940) and the Ramsar Convention on Wetlands (Ramsar, Iran, 1971). The manuscript
was greatly improved by comments from S. K. Robinson,
P. De Marco Jr., S. Pacheco, S. L. Mendes, R. P. Martins,
and an anonymous reviewer. C. E. A. Carvalho provided
the records on S. melanoleucos, H. diodon, and A. nitida, and on a juvenile and adult of S. ornatus. C. R. M.
Abreu aided in many field surveys and contributed some
records on S. tyrannus. J. B. Nacinovic kindly sent us data
on bird skins collected by J. Moojen and deposited in the
Museu Nacional. J. F. Cândido Jr. reevaluated his records
on M. axillaris, T. poliocephalus, and K. nigerrimus, and
allowed us to use them. J. F. Pacheco provided some historical information and identified or confirmed some taperecorded bird voices. M. M-Coelho gave records on M.
striata and Pyroderus scutatus. P. D. Marco Jr. and S.
Pacheco helped with the statistical analysis. R. Leonard
and B. A. Loiselle kindly revised the English. P. A. Ribeiro
and C. L. Barreto kindly produced the map. A check-list
of habitat generalists is available from the authors upon
request.
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Appendix 1. Conservation status, record sources, and natural history traits of threatened forest bird species of the Viçosa region, State of Minas
Gerais, southeastern Brazil.
Local conservation
status a
Extinct
Tinamus solitarius (p)
Accipiter poliogaster
Odontophorus capueira (p)
Columba plumbea (p)
Claravis godefrida
Pyrrhura frontalis
Macropsalis creagra
Trogon viridis
Trogon rufus
Chelidoptera tenebrosa
Selenidera maculirostris
Piculus aurulentus
Melanerpes flavifrons
Biatas nigropectus
Grallaria varia
Syndactyla rufosuperciliata
Philydor atricapillus
Philydor lichtensteini
Dendrocincla turdina
Hemitriccus diops
Onychorynchus coronatus
Myiobius atricaudus
Pachyramphus castaneus
Lipaugus lanioides
Procnias nudicollis (p)
Passerina brissonii (p)
Chlorophonia cyanea
Tangara cyanocephala
Critically endangered
Crypturellus obsoletus (p)
Chondrohierax uncinatus
Harpagus diodon
Accipiter bicolor
Buteo brachyurus
Asturnina nitida
Buteogallus urubutinga
Leucopternis lacernulata
Spizastur melanoleucus
Spizaetus ornatus
Spizaetus tyrannus
Micrastur ruficollis
Herpetotheres cachinnans
Penelope superciliaris (p)
Claravis pretiosa
Geotrygon montana
Amazona vinacea (p)
Lophornis magnifica
Recordsb
No. of records/
no. of
fragmentsc
3
1, 3
1, 3, 4, 6, 7,12
2, 4, 6, 7
1
1, 3, 4, 5, 6, 7
1, 3, 4
2, 3, 6, 7
1, 2, 3, 6
1, 3, 4, 6
2
1
1, 3, 4, 6, 7
1, 6
6
1
1, 5, 6
1
2, 3, 6
1, 6
6
1, 2, 7, 11
1, 3
1, 3, 7
12
1, 6
6
6, 7
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
1, 3, 6, 7, 11,12
11
11
1, 6, 10
10, 11
11
11
6, 11
6, 11
6, 11
6, 11
2, 10
6, 10, 11,12
3, 4, 5, 6, 10, 11,12
11
11
7, 10, 11
5, 6, 7, 10, 11
1/1
5 (4)/5 (4)
1/1
1/1
3/3
2/2
1/1
1/2
1/1
2/1
1/3
2 (2)/3 (2)
9 (6)/5 (5)
1/1
10/1
2/1
10 (5)/6 (5)
1/1
Natural history traits
Conservation
statusd
Conservation
prioritye
trophic
guild f
foraging
stratag
1nt 2t 3ce
2t 3pe
3v
3pt
1c 2t 3ce
3pt
2t 3v
m
m
m
v
c
i
v
v
v
i
o
o
i
v
i
o
i
i
i
i
i
i
i
i
i
i
o
f
g
f
f
t
c
t
c
t/m
c
t
c
m
c
c
m/c
c
u/m
t
u
m
m
u/m
u
m
u/m
m
m/c
c
u
c
c
o
c
i
c
c
c
c
i
c
c
c
i
c
v
v
v
v
n
t
c
c
c
c/a
c
t/c
m/c
c
m
m
m
c
t
t/m
t
c
c
u
m
m
1nt
3pt
1v 2pt 3ep
3v
3pt
3pt
1e 3ep
1v 2t 3v
1nt 3v
3pt
h
m
m
h
h
1v 2t 3ep
2t 3ep
2pt 3ep
2pt 3ep
h
1e 2t 3ep
3pt
h
endemismh
sensitivityi
x
m
h
h
h
h
m
m
m
m
l
m
m
m
m
h
m
h
h
m
m
h
m
m
h
m
m
m
m
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Conservation Biology
Volume 17, No. 6, December 2003
l
l
m
m
m
m
m
h
h
m
m
m
l
m
l
m
m
l
1838
Atlantic Forest Bird Extinction
Ribon et al.
Appendix 1. (continued)
Local conservation
status a
Malacoptila striata
Ramphastos vitellinus
Psilorhamphus guttatus
Myrmeciza loricata
Chamaeza meruloides (p)
Xiphocolaptes albicollis
Cranioleuca pallida
Philydor rufus
Sclerurus scansor
Contopus cinereus
Attila rufus
Sirystes sibilator
Pachyramphus validus
Pyroderus scutatus
Knipolegus cyanirostris
Legatus leucophaius
Ilicura militaris
Thryothorus longisrostris
Cissopis leveriana
Pipraeidea melanonota
Amaurospiza moesta
Haplospiza unicolor
Euphonia violacea
Psarocolius decumanus
Cacicus haemorrhous
Vulnerable
Leptodon cayanensis
Micrastur semitorquatus
Penelope obscura (p)
Leptotila rufaxilla (p)
Propyrrhura maracana (p)
Dromococcyx pavoninus
Trogon surrucura
Baryphthengus ruficapillus
Baillonius bailloni
Campephilus robustus
Herpsilochmus
rufimarginatus
Drymophila ferruginea
Drymophila ochropyga
Myiopagis caniceps
Mionectes rufiventris
Muscipipra vetula
Manacus manacus
Schiffornis virescens
Platycichla flavipes
Hemithraupis ruficapilla
Habia rubica
Ramphocelus bresilius (p)
Arremon semitorquatus
Saltator similis (p)
Euphonia cyanocephala
Indeterminate
Pulsatrix koeniswaldiana
Strix hylophila
Nyctibius griseus
Lurocalis semitorquatus
Nyctiphrynus ocellatus
Recordsb
No. of records/
no. of
fragmentsc
6, 11
1, 3, 4, 6, 10, 11,12
11
1, 6, 10, 11
1, 6, 10,12
1, 3, 5, 6, 7, 10, 11
5, 11
1, 7, 10, 11
11
1, 5, 6,10, 11
5, 6, 7, 10, 11
1, 10, 11
6
3
1, 5, 6, 11
6, 7, 11
1, 5, 6, 7, 10, 11
11
1, 3, 6, 7, 10, 11
1, 5, 6, 7, 9, 10, 11
11
1, 11
1, 6
3, 6, 11
1, 3, 6
1/1
6 (4)/3 (1)
1/1
12 (4)/1 (1)
5 (3)/1 (1)
12 (7)/3 (3)
2/2
3/2
2/2
8 (3)/4 (3)
11 (8)/2 (2)
6 (2)/3 (2)
4 (1)/3 (1)
1/1
2/1
4 (1)/2 (1)
6 (2)/2 (2)
5 (2)/1 (1)
8/2
4 (1)/1 (1)
2/1
2/1
2/2
2/2
3 (2)/2 (2)
1, 3, 6, 10, 11
10, 11
1, 4, 6, 7, 10, 11,12
1, 3, 4, 5, 6, 10, 11
3, 10, 11
10, 11
1, 3, 4, 10, 11
1, 3, 6, 10, 11
1, 2, 3, 4, 5, 6, 7, 10, 11
1, 3, 4, 5, 10, 11
10, 11
18 (12)/6 (6)
8 (4)/4 (2)
>50 (121)/24 (24)
11–50 (48)/12 (12)
11–50 (42)/11 (11)
8 (4)/4 (4)
50 (39)/10 (10)
18 (15)/5 (5)
11–50 (38)/9 (9)
35 (22)/10 (9)
26 (20)/4 (4)
1, 5, 6, 7, 10, 11
1, 2, 6, 7, 10, 11
10, 11
10
1, 3, 5, 6, 10, 11
1, 3, 5, 6, 7, 10, 11
7, 10, 11
1, 6, 10, 11
6, 7, 10, 11
1, 5, 6, 7, 10, 11
1, 3, 5, 6, 10, 11
1, 5, 6, 7, 10, 11
1, 3, 5, 6, 7, 9, 10, 11
10
40 (21)/4 (3)
40 (34)/7 (5)
50 (40)/7 (7)
28 (25)/6 (6)
18 (12)/6 (4)
50 (39)/7 (7)
40 (31)/8 (8)
16 (13)/4 (4)
50 (42)/8 (8)
80 (40)/5 (5)
11-50/4
40 (20)/9 (9)
cca. 400 (245)/24 (24)
12 (11)/6 (6)
2, 6, 11
1, 5, 6, 7, 11
6, 11, 12
6, 11
10, 11
10–50/5
1/1
2/1
10–50/4
11–50/2
Natural history traits
Conservation Conservation
statusd
prioritye
3pt
1nt
m
m
3pt
m
3pt
3pt
m
m
2t, 3v
h
m
1nt 2t 3v
2t 3v
h
m
m
h
1nt 3v
2t, 3ep
m
m
3pt
1nt
m
m
m
m
m
trophic
guild f
foraging
stratag
i
o
i
i
i
i
i
i
i
i
i
i
i
f
i
i
f
i
f
o
g
g
f
o
f
u/m
c
u
t
t
m
m/c
c
t
u/c
m/c
c
c
m
t/c
c
m/c
u
u/c
m/c
u/m
m/c
c
c
m/c
c
i
v
v
v
i
o
o
v
i
i
c
c
t/c
t
c
t/u
c
u/m
c
m
0
i
i
i
o
i
o
o
o
o
o
o
f
o
f
u
u
c
u/m
c
u
u
m/c
c
u/m
u/m
t
m/c
c
c
c
i
i
i
c
c
c
a
t
endemismh
sensitivityi
x
m
h
m
m
m
m
m
m
h
l
m
m
m
m
l
l
m
l
l
l
m
m
l
m
l
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
x
m
m
m
m
m
h
m
m
h
m
m
m
m
m
m
l
m
m
l
h
l
m
l
l
h
h
l
m
m
a
In each category species arranged according to their systematic and phylogenetic position following Sick (1997) ( for Arremon semitorquatus following Raposo [1997]). A (p)
after the scientific name indicates the species suffers from hunting or exploitation by the pet trade. See text for criteria used to define conservation status.
b
Codes: 1, skins at Museu de Zoologia João Moojen de Oliveira, Universidade Federal de Viçosa; 2, skins at Museu Nacional do Rio de Janeiro; 3, Moojen et al. (1941); 4, Moojen
(1943); 5, Erickson & Mumford (1976); 6, Monteiro et al. (1983); 7, Monteiro & de Mattos (1984); 8, Cândido (1988); 9, Vieira et al. (1992); 10, Ribon (1998); 11, unpublished
record by authors; 12, interviews with local landowners.
c
Number of records for threatened species during the last 15 years and number of forest fragments where the species were recorded. Numbers in parentheses indicate the number
of records and fragments recorded during point counts. Absence of a value in parentheses indicates that no birds were found during point counts.
d
Conservation status at global, national, and state levels: 1, BirdLife International (2000); 2, Bernardes et al. (1990); 3, Lins et al. (1997). Abbreviations: t, threatened; c, critical;
ce, critically endangered; e, endangered; nt, near threatened; pe, presumably extinct; pt, presumably threatened; vu, vulnerable. No code indicates the species was not considered
in any of the studies.
e
Abbreviations: h, high; m, medium; u, urgent (according to Parker et al. 1996). No code indicates the species has low conservation priority.
f
Abbreviations: c, carnivorous; i, insectivorous; o, omnivorous; n, nectarivorous; v, vegetarian.
g
Abbreviations: a, aerial; c, canopy; m, medium; t, terrestrial; u, understory.
h
An x indicates a species is endemic to the Atlantic forest (according to Parker et al. 1996).
i
Sensitivity to environmental disturbance: h, high; m, medium; l, low (according to Parker et al. 1996).
Conservation Biology
Volume 17, No. 6, December 2003
Ribon et al.
Atlantic Forest Bird Extinction
1839
Appendix 2. Unthreatened forest bird species recorded at forest fragments in the Vic¸osa region, State of Minas Gerais, southeastern Brazil.∗
Crypturellus tataupa (125/21, f, t, ne, l); Ictinia plumbea (5/2, c, ca, ne, m); Leptotila verreauxi (264/36, f, t/u, ne, l); Pionus maximilliani (307/30, f, c, ne, m);
Phaetornis squalidus (101/10, n, u, ne, m); Phaetornis ruber (68/13, n, u, ne, m); Melanotrochilus fuscus (53/14, n, m/c, ne, m); Thalurania glaucopis (92/17, n, u/m,
e, m); Clytolaema rubricauda (0/0, n, u/m, e, m); Pteroglossus aracari (89/17, v, c, ne, m); Picumnus cirratus (174/38, i, m/c, ne, l); Celeus flavescens (91/25, i, m/c,
ne, m); Veniliornis maculifrons (159/27, i, c, e, m); Mackenzianea severa (110/12, i, u, e, m); Thamnophilus caerulescens (848/41, i, u/m, ne, l); Dysithamnus
mentalis (281/17, i, u/m, ne, m); Formicivora serrana (168/24, i, u/m, e, l); Pyriglena leucoptera (680/26, i, u, e, m); Conopophaga lineata (778/37, i, u, e, m);
Synallaxis ruficapilla (432/31, i, u, e, m), Synallaxis cinerascens (161/17, i, u/m, ne, m); Anabazenops fuscus (280/14, i, m, e, h); Automolus leucophthalmus (128/11,
i, u, e, m); Xenops rutilans (133/24, i, c, ne, m); Sittasomus griseicapillus (97/10, i, m, ne, m); Lepidocolaptes squamatus (197/30, i, m/c, e, h); Lepidocolaptes fuscus
(61/13, i, u/m, e, h); Campylorhamphus falcularius (163/25, i, u/m, e, h); Phyllomyias fasciatus (32/15, i, c, ne, m); Myiopagis viridicata (50/16, i, c, ne, m);
Leptopogon amaurocephalus (245/26, i, u/m, ne, m); Corythopis delalandi (75/10, i, t, ne, m); Myiornis auricularis (103/11, i, m/c, e, l); Hemitriccus nidipendulus
(264/38, i, u/m, e, l); Todirostrum poliocephalum (109/16, i, m/c, e, l); Todirostrum plumbeiceps (195/22, i, u, ne, m); Tolmomyias sulphurescens (587/37, i, c, ne, m);
Platyrinchus mystaceus (286/30, i, u, ne, m); Lathrotriccus euleri (612/38, i, m, ne, m); Cnemotriccus fuscatus (25/11, i, u/m, ne, l); Myiarchus ferox (191/34, o, m/c,
ne, l); Myiarchus swainsoni (151/40, i, m/c, ne, l); Megarynchus pitangua (354/37, o, c, ne, l); Myiodynastes maculatus (138/35, o, m/c, ne, l); Empidonomus varius
(29/17, o, c, ne, l); Pachyramphus viridis (23/14, i, c, ne, m); Pachyramphus polychopterus (93/26, i, c, ne, l); Chiroxiphia caudata (706/24, o, u/m, e, l) Turdus
albicollis (326/31, o, u/m, ne, m); Vireo olivaceus (201/31, o, c, ne, l); Hylophilus amaurocephalus (378/39, i, u/c, ne, m); Basileuterus c. culicivorus (1777/41, i, u/m,
ne, m); Nemosia pileata (68/21, o, c, ne, l); Tachyphonus coronatus (128/23, o, m/c, ne, l); Trichothraupis melanops (307/29, o, u/m, ne, m); Piranga flava (8/5, o, c,
ne, l); Thraupis sayaca (574/41, o,c,ne,l); Thraupis ornata (0/0, o, c, e, m); Euphonia chlorotica (13/4, o, c, ne, l); Tangara cyanoventris (228/26, f, c, e, m); Dacnis
cayana (209/31, o, c, ne, l); Conirostrum speciosum (350/39, o, c, ne, l), Tiaris fuliginosa (2/2, v, u/m, ne, l).
∗
Codes indicate, respectively, estimated number of records and number of forest fragments where the species was recorded, guild, strata, endemism (e, endemic; ne, not
endemic), and sensitivity to disturbance (definitions of codes in Appendix 1 footnotes). Values given are only illustrative and originated from point counts; they do not include
many records between 1986 and 2000.
Conservation Biology
Volume 17, No. 6, December 2003