The Avifauna of Rio Doce Valley, Southeastern Brazil, a Highly Fragmented Area

Author(s): Ricardo Bomfim Machado and Gustavo Alberto Bouchardet Da Fonseca

Source: BIOTROPICA, 32(4):914-924. 2000.
Published By: The Association for Tropical Biology & Conservation
DOI: http://dx.doi.org/10.1646/0006-3606(2000)032[0914:TAORDV]2.0.CO;2
URL: http://www.bioone.org/doi/full/10.1646/0006-3606%282000%29032%5B0914%3ATAORDV%5D2.0.CO
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BIOTROPICA 32(4b): 914–924 2000

The Avifauna of Rio Doce Valley, Southeastern Brazil, a Highly

Fragmented Area1

Ricardo Bomfim Machado2

Curso de Ecologia, Manejo e Conservação de Vida Silvestre—Universidade Federal de Minas Gerais, Minas
Gerais, Brazil
and
Gustavo Alberto Bouchardet Da Fonseca
Conservation International do Brazil, Av. Antônio Abrahão Caram, 820/302, Belo Horizonte, MG, Brazil.

ABSTRACT
We analyzed the avifauna from four areas of the Rio Doce basin (the municipal districts of Nova Era [NE], Antônio Dias
[AD], Caratinga [BSC], and Marliéria [RDSP]) located in eastern Minas Gerais state. Based on captures with mist nets, 75
bird species belonging to 15 families were inventoried; however, the species composition varied greatly among the study
areas. Fifty species and 231 of the 466 individuals recorded during this study were captured at NE. In the AD area, 33
species and 132 individuals were captured. The other two areas, BSC and RDSP, contributed only 103 captures and 22
species. By analyzing species composition as a function of altitude of the study areas, it was verified that a variation of 500
m altitude was sufficient in determining the difference in existing bird communities. Formicariidae species, such as Dry-
mophila squamata, Thamnophilus punctatus, and Conopophaga melanops, were captured exclusively in the BSC and RDSP
areas, located below the 500 m altitude limit while their congeners (D. ochropyga, T. caerulescens, and C. lineata) were found
exclusively in the highest areas (NE and AD). Significant seasonal variations in the species composition were observed
(Green’s test: Q ⫽ 12.79 in NE, 12.84 in AD, 12.4 in BSC, and 20.68 in RDSP; P ⬍ 0.05), and we believe that such
variations could be associated with seasonal movements between the highest and lowest areas of the Rio Doce basin. As
such, the impacts of fragmentation to the Atlantic Forest along this stretch of the Rio Doce basin may have affected the
natural dynamics of avian movements. The destruction of ⬎ 90 percent of the original Atlantic Forest vegetation cover
already may have seriously compromised the population viabilities of birds endemic to this area.

RESUMO
Nesse estudo analisamos a avifauna em quatro localidades na bacia do rio Doce: nos municı́pios de Nova Era (NE),
Antônio Dias (AD), Caratinga (BSC) e Marliéria (RDSP), situados no leste do estado de Minas Gerais. Com base em
capturas com redes de neblina, foram levantadas 75 espécies de aves pertencentes a 15 famı́lias. Entretanto, a composição
de espécies variou enormemente entre as áreas de estudo. Em NE, foram obtidas 50 espécies e 231 dos 466 indivı́duos
capturados durante o estudo. Na área AD, foram capturadas 33 espécies e 132 indivı́duos. As outras duas áreas, BSC e
RDSP, contribuı́ram com apenas 103 capturas e apenas 22 espécies. Analisando a composição das espécies em função da
altitude das áreas estudadas, constatou-se que uma variação de apenas 500 m de altitude é suficiente para determinar a
existência de diferentes comunidades de aves. Espécies de formicariı́deos como Drymophila squamata, Thamnophilus
punctatus, Conopophaga melanops foram capturadas exclusivamente nas áreas BSC e RDSP, localizadas abaixo da cota de
500 m de altitude enquanto suas congêneres (D. ochropyga, T. caerulescens e C. lineata) são exclusivas das áreas mais
elevadas (NE e AD). Uma vez que foi observada uma variação significativa na composição (teste de Green: Q ⫽ 12,79
em NE, 12,84 em AD, 12,4 em BSC e 20,68 em RDSP; P ⬍ 0,05) ao longo do ano, acreditamos que tal variação
possa estar associada a movimentos sazonais de deslocamentos entre as regiões mais altas e as mais baixas da bacia do rio
Doce. Sendo assim, os impactos da fragmentação da Mata Atlântica desse trecho da bacia do rio Doce podem ter afetado
essa dinâmica natural de deslocamentos e a destruição de mais de 90 porcento da cobertura original da Mata Atlântica
já pode ter comprometido seriamente a viabilidade das populações das aves endêmicas dessa região.

Key words: altitudinal gradient; Atlantic Forest; birds; bird communities; Brazil; conservation; habitat fragmentation.

BRAZIL RANKS THIRD OF ALL COUNTRIES with respect
to having the highest diversity of bird species (Mit-
1 Received 13 August 1998; revision accepted 4 October
1999.
2 Corresponding author: Departamento de Ecologia,
UnB, C.P. 4474, 70919-970, Brası́lia, DF, Brazil. E-mail:
ricardobm@uol.com.br
termeier et al. 1997). There are almost 1700 species
(Meyer de Schauensee 1982; Ridgely & Tudor
1989, 1993; Sick 1997) that are distributed
throughout five large biomes covering ca 8.5-mil-
lion km2.
In the Atlantic Forest, the third largest biome
of Brazil, up to 850 bird species (47% of Brazil’s
avian richness [Machado 1995]) can be found, but

914

regional variation along this biome is enormous.
According to Bibby et al. (1992), eight areas of bird
endemism (endemic bird areas, EBA) can be de-
tected in the Atlantic Forest. Of the 182 species
considered endemic to Brazil (Sick 1997), 113
(64.2%) occur in the Atlantic Forest; however, this
diversity is highly threatened. Most of the men-
tioned EBAs already are considered as being in crit-
ical states (Bibby et al. 1992), due mainly to two
factors: high endemism and intense deforestation.
Compiling the data published by the Fundação
SOS Mata Atlântica and INPE (1993), it can be
noted that on a national average the native Atlantic
Forest cover has been reduced to 8.7 percent of the
original total (ca 1-million km2). Seventy-five bird
species from the Atlantic Forest are currently
threatened with extinction, and one species (Mitu
mitu) is considered as being extinct in nature (Col-
lar et al. 1992). This total represents 68.8 percent
of the taxa present in the Official Brazilian List
(Edict 1.522 of 19 December 1989, of the Brazil-
ian Institute of the Environment and Renewable
Natural Resources—IBAMA).
The Rio Doce basin mirrors the general situa-
tion of the Atlantic Forest. It is an area of Minas
Gerais state that presents high species richness, in
which about a third of the Brazilian birds may oc-
cur (Meyer de Schauensee 1982; Ridgely & Tudor
1989, 1993; Sick 1997). Several species endemic
to Brazil (20% of the birds mentioned previously)
occur in the Rio Doce basin, as well as 17 taxa
officially considered as threatened with extinction
(Bernardes et al. 1990).
While the area has been one of the most recent
mining areas within the Atlantic Forest to be ex-
plored (Fonseca 1985), the resulting picture is ex-
tremely troubling. In some regions, deforestation
has eliminated 93.9 percent of the original vege-
tation cover (Machado 1995). Studies conducted
by Machado (1995), indicated that almost all of
the remaining areas of original vegetation cover are
composed of small fragments (x ⫽ 22.6 ha, N ⫽
1313) with low connectivity (average distance be-
tween fragments ⫽ 840 m). The largest areas are
those that had been transformed into conservation
units (e.g., the Rio Doce State Park with 35,000
ha).
Studies of the regional avifauna are in large part
limited to species inventories, few of which have
been published (Carnevalli 1980, Monteiro et al.
1983, Monteiro & Mattos 1984, Willis & Oniki
1991, Machado & Lamas 1996). Thus, the objec-
tives of this study were to characterize the bird
communities in different fragments of the mid-Rio
Avifauna of Rio Doce Valley, Brazil 915
Doce and to evaluate the effects of fragmentation
on the avifauna along this stretch of the Minas
Gerais Atlantic Forest.
METHODS
STUDY AREAS.—For the avifauna inventories, we se-
lected four areas of the mid-Rio Doce, located in
the municipal districts of Nova Era (NE), Antônio
Dias (AD), Caratinga (BSC), and Marliéria
(RDSP; Fig. 1). All areas were originally covered
by semi-deciduous or montane pluvial forests
(IBGE 1993), according to the classifications of
Rizzini (1979). Data collected from the BSC area
indicated an average annual maximum temperature
varying between 21 and 24⬚C and minimum tem-
peratures of 14 to 16⬚C. Precipitation averages ca
1250 mm, and a dry season occurs from April until
September, with greater concentrations of rain
from October to March.
In NE (19⬚42⬘S, 43⬚04⬘W), we selected an area
of ca 500 ha located on the margin of the Córrego
do Peixe (Fish Creek). The average altitude was
800 m and the area was composed of private land
predominated by dairy cattle ranches. In AD
(19⬚08⬘S, 42⬚56⬘W) we selected an area of ca 300
ha surrounded by pastures and eucalyptus planta-
tions, located at the headwaters of the Córrego do
Machado (Machado’s Creek) at an altitude of 750
m. In BSC (19⬚44⬘S, 41⬚49⬘W), we established an
area close to the Córrego de Jaó (Jaó’s Creek); this
was within the limits of the Caratinga Biological
Station, a privately owned conservation unit of ca
880 ha, at an average altitude of 480 m. The last
area was established in the Vinhático forest, located
in the southern portion of Rio Doce State Park
(RDSP). The park is a state conservation unit that
contains about 35,000 ha, at an average altitude of
350 m.
CAPTURES WITH NETS.—Birds were captured with
the use of mist nets (ATX 12 ⫻ 2.5 m with 3.5-
mm mesh) in the four chosen areas. In each area,
a battery of ten nets were mounted and left open
in the morning (four hours) and afternoon (three
hours) for three consecutive days, resulting in a to-
tal capture effort of 840 net h/mo. Four sampling
periods were carried out, during August (1992),
October (1992), February/March (1993), and May
(1993), which corresponded to spring, autumn,
and winter, respectively.
We used aluminum bands donated by the Cen-
ter of Researches for the Conservation of Wild
Birds (CEMAVE) to detect recaptures. We consid-
916 Machado and Fonseca

FIGURE 1. Rio Doce Valley in eastern Minas Gerais state and the location of the study sites. The numbers represent:
1 ⫽ Rio Doce State Park (RDSP); 2 ⫽ Biological Station of Caratinga (BSC); 3 ⫽ Nova Era (NE); 4 ⫽ Antônio
Dias (AD); 5 ⫽ Station of Research and Environmental Development (PETI); 6 ⫽ Biological Station of Mata do
Sossego (BSMS).

ered recaptures only as those banded individuals
that were captured during different periods. Iden-
tifications were made to species level, following the
nomenclature of Sick (1997). To complement the
bird inventories made with mist nets in the study
areas, observed species also were recorded nonsys-
tematically during the fieldwork.
OTHER SOURCES OF DATA.—To complement the
analyses made with capture data for species simi-
larity among the study sites, we used lists of species
known from the study areas and included data
from two other areas of the Rio Doce basin, de-
scribed here. For the RDSP area, we used the lists
of Carnevalli (1978, 1981) and Willis and Oniki
(1991). For AD, we used two lists from Machado
and Lamas (1996) and Machado and Figueiredo
(1996). For BSC, we used a list by Carnevalli et
al. (1989).
We included data from the Peti Research and
Environmental Development Station (PETI) and
the Mata do Sossego Biological Station (BSMS),
both located in the Rio Doce basin, Minas Gerais.
PETI is a privately owned reserve of the Minas
Gerais State Central Energy (CEMIG) with an area
of 780 ha, and is at an average altitude of 850 m.
It is located in the municipal district of Santa Bár-
bara at 19⬚53⬘S, 43⬚21⬘W (Fig. 1). For this loca-
tion, a list of 250 species from Machado et al.
(1988), was used. BSMS, an area of private land
 Avifauna of Rio Doce Valley, Brazil 917

TABLE 1. Total number of species recorded in the study areas, number of species (and percentage) per distribution, and
threatened categories for Brazil (IBAMA) and the state of Minas Gerais (MG). Observation: RDSP ⫽ Rio
Doce State Park; BSC ⫽ Caratinga; NE ⫽ Nova Era municipality; AD ⫽ Antônio Dias municipality county;
PETI ⫽ Environmental Development and Research Station; BSMS ⫽ Biological Station of Mata do Sossego.

Conservation status
Large Near Threatened Threatened Total number
Area distribution endemic Endemic IBAMA1 MG2 of species
RDSP 249 (83.3) 27 (9.0) 23 (7.7) 15 (5.0) 17 (5.7) 299
BSC 164 (80.3) 25 (12.2) 15 (7.3) 8 (3.9) 13 (6.4) 204
NE 102 (81.6) 13 (10.4) 10 (8.0) 2 (1.6) 4 (3.2) 125
AD 125 (80.1) 14 (9.0) 17 (11.0) 2 (1.3) 2 (1.3) 156
PETI 210 (84.0) 20 (8.0) 20 (8.0) 2 (0.8) 2 (0.8) 250
BSMS 65 (64.3) 21 (20.8) 15 (14.8) 2 (2.0) 4 (4.0) 101
Total 306 (77.1) 49 (12.3) 38 (9.5) 16 (4.0) 21 (5.3) 397
Observation:
1 Edict 1.522 of 19 December 1989 of the Brazilian Institute of the Environment and Renewable Natural Resources–
IBAMA.
2 Deliberation 41/95 of the Commission of Environmental Politics of Minas Gerais State—COPAM.

that belongs to the Biodiversitas Foundation, has of the four sampling areas (NE, AD, BSC and
an area of 800 ha and lies at an altitude of 1200 RDSP), a cluster analysis was made (Euclidean dis-
m. It is located in the municipal district of Simo- tance, unweighted pair-groups method using arith-
nésia at 20⬚03⬘S, 35⬚42⬘W (Fig. 1). For this area, metic averages) based on a similarity matrix
we used a list of 101 species by Machado (1993). (Sørenson index, calculated according to Magurran
[1988]). For the index calculation, only the pres-
STATISTICAL ANALYSES.—We calculated the Shan- ence/absence of the captured species was consid-
non-Wiener diversity index (H⬘) for each sampling ered. The same method was used to corroborate
area in which captures were made and tested for the observational data from the four study areas
differences between indices of those areas, accord- with those species cited in the aforementioned spe-
ing to Magurran (1988). cies lists (PETI and BSMS).
Seasonal variation in the composition of bird The species richness in each of the six study
communities was tested according to Green areas was correlated with the size of the area, using
(1979). We used a chi-square (␹2) test and Fisher’s Spearman’s rank correlation. All differences were
exact test to compare capture frequencies among considered significant at P ⬍ 0.05.
areas in which mist nets were used, following Zar
(1984). We tested the null hypothesis of equality RESULTS
for capture frequency among areas. The ␹2 test was
used also to test for differences in capture frequen- CAPTURES WITH NETS.—We captured 466 individ-
cies among seasons. uals belonging to 75 species and 15 families. NE
For the comparison of bird species composition was the area with the greatest richness (50 spp.),
followed by AD (33 spp.), BSC (22 spp.) and
RDSP (21 spp.; Table 2). At NE, 231 captures
TABLE 2. Richness of species, number of individuals, and were registered, being the area presenting the high-
Shannon-Wiener diversity index (H⬘) for birds est capture frequency. Next were AD (132 cap-
captured in the sample areas of Nova Era tures), BSC (66), and RDSP (37; Table 2). NE
(NE), Antônio Dias (AD), Biological Station was the area with the highest diversity index (H⬘
of Caratinga (BSC), and Rio Doce State Park
(RDSP). ⫽ 3.3; Table 2). Second was AD, followed by BSC
and RDSP. No significant differences among H⬘
No. of Diversity values for the study areas were observed, except for
Area Richness individuals index (H⬘) NE and RDSP (t ⫽ 2.990, P ⬍ 0.05).
NE 50 231 3.3 The most abundant species was Pyriglena leu-
AD 33 132 3.1 coptera (captured exclusively in NE and AD) which
BSC 22 66 2.6 registered 59 captures, with 69.5 percent of that
RDSP 21 37 2.9
total being contributed by NE (Table 3). The fly-
918 Machado and Fonseca

TABLE 3. List of species with five or more captures in the sample areas of Rio Doce Valley. This species set (383 captures)
represents 83.4 percent of the total captures for all areas.

Species/areas NE % AD % BSC % RDSP % Total

Anabazenops fuscus 1 20.0 4 80.0 — — — — 5
Basileuterus culicivorus 10 58.8 7 41.2 — — — — 17
Chiroxiphia caudata 14 77.8 4 22.2 — — — — 18
Conopophaga lineata 6 35.3 11 64.7 — — — — 17
Dendrocincla turdina — — — — 3 60.0 2 40.0 5
Drymophila ochropyga 1 20.0 4 80.0 — — — — 5
D. squamata — — — — 5 100.0 — — 5
Dysithamnus mentalis 4 80.0 — — 1 20.0 — — 5
D. plumbeus — — — — 11 78.6 3 21.4 14
Hemitriccus diops — — 5 100.0 — — — — 5
Ilicura militaris 10 71.4 4 28.6 — — — — 14
Lathrotriccus euleri 3 42.9 2 28.6 2 28.6 — — 7
Lepidocolaptes fuscus 3 37.5 1 12.5 2 25.0 2 25.0 8
Leptopogon amaurocephalus 5 35.7 4 28.6 4 28.6 1 7.1 14
Malacoptila striata 3 37.5 1 12.5 4 50.0 — — 8
Manacus manacus 7 25.9 3 11.1 15 55.6 2 7.4 27
Mionectes rufiventris 8 72.7 3 27.3 — — — — 11
Myrmeciza loricata 1 20.0 4 80.0 — — — — 5
Phaethornis pretrei 7 100.0 — — — — — — 7
Platyrincus mystaceus 21 67.7 10 32.3 — — — — 31
Pyriglena leucoptera 41 69.5 18 30.5 — — — — 59
Saltator similis 4 66.7 2 33.3 — — — — 6
Sittasomus griseicapillus 5 55.6 4 44.4 — — — — 9
Tachyphonus coronatus 4 57.1 3 42.9 — — — — 7
Tangara cyanoventris 11 100.0 — — — — — — 11
Thalurania furcata 6 85.7 1 14.3 — — — — 7
T. glaucopis 2 40.0 2 40.0 1 20.0 — — 5
Thamnophilus caerulescens 1 14.3 6 85.7 — — — — 7
T. punctatus — — — — 5 62.5 3 37.5 8
Tolmomyias sulphurescens 5 83.3 1 16.7 — — — – 6
Trichothraupis melanops 8 38.1 12 57.1 — — 1 4.8 21
Turdus leucomelas 2 28.6 2 28.6 1 14.3 2 28.6 7
T. rufiventris 5 62.5 1 12.5 1 12.5 1 12.5 8
TOTAL 198 50.9 119 30.6 55 14.1 17 4.4 389

catchers Platyrinchus mystaceus and Manacus man-
acus and the tanager Trichothraupis melanops were
among the most abundant species, with 31, 27,
and 21 captures, respectively (Table 3).
The capture data showed that several species
occur exclusively or preferentially in lower areas
(RDSP and BSC) or in higher altitude areas (NE
and AD), corroborating the results of the similarity
analysis (Fig. 3). Among the species that registered
five or more captures and were exclusively in the
lower area were Dendrocincla turdina, Drymophila
squamata, Dysithamnus plumbeus, and Thamnophi-
lus punctatus. The species exclusive to the highest
areas were Anabazenops fuscus, Basileuterus culivi-
vorus, Chiroxiphia caudata, Conopophaga lineata,
Drymophila ochropyga, Ilicura militaris, Mionectes
rufiventris, Myrmeciza loricata, Phaethornis pretrei,
Platyrinchus mystaceus, Pyriglena leucoptera, Saltator
similis, Sittasomus griseicapillus, Tachyphonus coron-
atus, Tangara cyanoventris, Thalurania furcata, and
Tolmomyias sulphurescens (Table 3).
Some cases of altitudinal allopatry were verified
for congeneric species; among the Drymophila, we
found D. ochropyga exclusively in the highest areas
(NE and AD) and D. squamata in the lower areas
(BSC and RDSP). Among the Dysithamnus, D.
plumbeus, a species threatened with extinction in
Brazil (Bernardes et al. 1990) and in Minas Gerais
(Machado et al. 1998), was captured exclusively in
the lowest areas (BSC and RDSP), while D. men-
talis occurred preferentially in the highest areas
(NE and AD; Fisher’s exact test ⫽ 6.67, P ⬍ 0.05).
Among Thamnophilus, T. punctatus was captured
exclusively in the lower areas and T. caerulescens in
the highest areas.
Other species pairs, although presenting lower
capture frequencies, also presented this same pat-
tern: Conopophaga (C. melanops captured exclusive-

FIGURE 2. Relationship between species richness and
area (log) for the six sample sites in the Rio Doce Valley
(R 2 ⫽ 0.8285, P ⬍ 0.05).
ly in lower and C. lineata in the highest areas),
Tachyphonus (T. cristatus in lower areas and T. co-
ronatus in the highest areas), and Myiobius (M. atri-
caudus in lower areas and M. barbatus in the high-
est areas; Table 3).
Species composition of the understory varied
significantly throughout the year in all areas
(Green’s test, Q ⫽ 12.79 [NE], 12.84 [AD], 12.4
[BSC], and 20.68 [RDSP]; P ⬍ 0.05). Some fru-
givorous species (e.g., I. militaris and Manacus
manacus) occurred preferentially in the summer pe-
riod (␹2 ⫽ 13.5 and 16.3; P ⬍ 0.05, respectively).
Among the insectivores, Pyriglena leucoptera oc-
curred preferentially in the summer (␹2 ⫽ 8.73, P
⬍ 0.05) while Leptopogon amaurocephalus was more
abundant in the autumn (␹2 ⫽ 11.0, P ⬍ 0.05).
AVIFAUNA RICHNESS OF THE MID-RIO DOCE.—By us-
ing the inventories made in the field and the sec-
ondary data obtained for the six areas of the Rio
Doce basin, 397 bird species were confirmed as
occuring in this region. RDSP was the area that
presented the greatest species richness (299 spe-
cies), followed by PETI (250), BSC (204), NE
(125), AD (156), and BSMS (101). Species rich-
ness was significantly correlated with forest patch
size on a logarithmic scale (r ⫽ 0.82857, P ⬍ 0.05;
Fig. 2).
Cluster analysis indicated the presence of three
area groups: RDSP and BSC; PETI, NE, and AD;
and a final group formed by BSMS (Fig. 3). Those
same groups were obtained when we analyzed the
altitudes of the areas: RDSP and BSC formed a
group located in the range of up to 500 m; NE,
AD, and PETI for the range between 500 and
1000 m; and BSMS for altitudes above 1000 m
(Fig. 3 and Fig. 4).
Of the species total compiled for the six areas
Avifauna of Rio Doce Valley, Brazil 919
FIGURE 3. Cluster analysis (UPGMA) for similarity of
species composition (presence/absence) calculated using
the Sørenson index for the sites in the Rio Doce Valley,
MG. A ⫽ data from captures in four areas of the study;
B ⫽ data from lists and captures in six areas.
(397 species), 38 (9.5%) were endemic to the At-
lantic Forest, but presented variation between areas
for the proportion of these listed taxa. RDSP pos-
sessesed the greatest number of endemic taxa (23
species), although this number corresponded to 7.7
percent of the list from this area. In other areas,
the percentages registered were 7.3 percent (15 of
204) for BSC, 8.0 percent (10 of 125) for NE,
11.0 percent (17 of 156) for AD, 8.0 percent (20
of 250) for PETI and 14.8 percent (15 of 101) for
BSMS (Table 1).
According to the official list of IBAMA (Ber-
nardes et al. 1990), 16 species threatened with ex-
tinction occurred in the six areas analyzed here. At
the state level, there were 21 threatened species (list
of the Commission of Environmental Politics of
Minas Gerais—COPAM [Machado et al. 1998];
Table1). The areas that sheltered a larger number
of threatened species were RDSP (15 species for
Brazil and 17 for Minas Gerais, respectively) and
BSC (8 and 13 for Brazil and Minas Gerais, re-
spectively). The number of threatened species was
much lower in the other areas (Table 1).
920 Machado and Fonseca
FIGURE 4. Relative altitudes and distances among the
six study sites used for the analyses of regional avifauna
diversity in the Rio Doce Valley.
DISCUSSION
Variations in species composition along altitudinal
gradients have been reported for diverse groups of
animals in several areas of the globe (bats: Gran-
ham 1983; Patterson et al. 1996; birds: Terborgh
1977; Noon 1981; Loiselle & Blake 1991; inver-
tebrates: Olson 1994; Ribeiro et al. 1994). Studies
in Peru (Terborgh 1971, 1977) and Costa Rica
(Noon 1981) indicated that climatic variations as-
sociated with altitudinal variations provide different
conditions for the establishment of plant species.
Consequently, there was a variation in the vegeta-
tion structure (Terborgh 1971, 1977; Lieberman et
al.1996) or differences in the availability of food
resources (Loiselle & Blake 1991), these factors be-
ing partially responsible for differences in bird
communities.
Despite the fact that altitudinal variation
among the study areas considered here was not as
pronounced as in the works cited previously, a dif-
ference of only 500 m altitude among areas was
enough to determine major variations in species
composition. Perhaps due to its reduced altitudinal
gradient, the Atlantic Forest has not been the sub-
ject of detailed studies concerning the altitudinal
effects on avifauna communities (Sick 1997).
The results of the net captures indicated that
several congeneric species have distributions re-
stricted to certain altitudes. Examples cited earlier,
and others (e.g., D. turdina, P. leucoptera, P. mys-
taceus), demonstrate that the size of these species’
distributions areas are quite small, limited to nar-
row altitudinal intervals. For primates of the genus
Callithrix, two endemics of the Atlantic Forest (C.
geoffroyi and C. flaviceps) occur in different altitu-
dinal zones (Mendes 1986).
This characteristic allows the existence of sev-
eral species of birds, and other groups of fauna to
be concentrated within small territories. If we trace
a relationship between the size and number of spe-
cies, the Atlantic Forest contains relatively three
times more species per unit area than Amazonia,
considering an estimated 850 bird species and an
area of 1-million km2 for the Atlantic Forest and
ca 1100 birds and ca 4 million km2 for Amazonia.
Besides having restricted occurrences to certain
altitudinal strips, the birds of the Atlantic Forest
are not very abundant. The mist net captures in-
dicated the presence of few dominant species in
each of the sampled areas and several species with
low density. In NE, the site that presented the
greatest richness and abundance of individuals as
indicated by the capture results, 46 percent of the
captures were represented by only 12 percent of the
species recorded. The other species (88%) repre-
sented a little more than half of the captures for
that area. This pattern does not differ from that
observed at other sampling sites in tropical areas
(e.g., Bierregaard & Lovejoy 1989), suggesting the
presence of a large number of not very abundant
species.
Goerck (1997) suggested that if we consider
distribution area, population size, and habitat spec-
ificity, about 68 percent of the Atlantic Forest birds
may be considered rare, the same pattern found for
the Manaus region (Amazonia) by Bierrergaard
(1990). The level of endemism is also high: 30
percent of the species are found to be restricted to
that biome (Goerck 1997). This high diversity,
however, is currently threatened with extinction.
The massive reduction of the native vegetation
in the Atlantic Forest is one of the primary threats
to the avifauna, especially when the reduced spe-
cies’ distribution size is considered (Goerck 1997,
Manne et al. 1999). The remaining cover in the
Rio Doce basin represents only 9.8 percent of the
original area, a figure that is just above the national
average for the Atlantic Forest (9.0% according to
Fundação SOS Mata Atlântica & INPE 1993). As
a result, various species of the Atlantic Forest are
threatened with extinction, nearly 70 percent of the
birds officially recognized by the Brazilian govern-
ment (Bernardes et al. 1990).
In spite of this scenario, only four species of
birds are considered to be extinct from the Rio
Doce basin in Minas Gerais: Harpia harpyja, Ac-
cipiter poliogaster, Myrmeciza ruficauda, and Ne-
mosia rourei (Machado & Cavalcanti 1998), al-
though this situation may be only transitory. A
model based on the size of the distribution area of
Passeriformes, elaborated by Manne et al. (1999),
indicated that more species threatened with extinc-
tion occur in the Atlantic Forest than would be

expected. This fact suggests a mass extinction pro-
cess for Passeriformes in the Atlantic Forest (Manne
et al.1999), and likely for other groups of fauna as
well.
One complicating aspect related to the state of
the vegetation cover in the Rio Doce basin, which
in a certain way corroborates the aforementioned
model, is that the 9.8 percent of remaining cover
is shredded into countless isolated fragments of
small size. Using Landsat MSS images, Machado
(1995) determined that the remnants of native veg-
etation in the studied municipal districts are of
small size (x̄ ⫽ 24.2 ha) and low connectivity (x̄ ⫽
840 m). Studies by Willis (1979) in similarly de-
forested areas, like the state of São Paulo, indicated
that the greatest losses of species occur in small
fragments (⬍ 250 ha), especially for particular
groups of species (e.g., large frugivores). Like Willis
(1979), Bierregaard and Stouffer (1997) showed
that the avian response to habitat fragmentation
can vary, and some groups (e.g., hummingbirds)
may become more abundant in small fragments
than in continuous areas of Amazonia. On the oth-
er hand, the understory insectivorous birds have
been shown to be more vulnerable to habitat frag-
mentation.
Species richness tends to decrease with a re-
duction of the area in which they occur (MacAr-
thur & Wilson 1967). Like Willis (1979), we also
found a significant relationship between species
richness and area size; however, a simple analysis of
species richness is not enough to understand the
variation observed among communities of frag-
mented areas. The smallest sampling area in this
study contained about 300 ha (NE); yet despite its
size, the greatest capture frequencies in the lower
strata of the forest as well (as the greatest species
richness) were obtained in this area. The RDSP
site, which had an area of 35,000 ha, presented the
lowest abundance of individuals and the lowest spe-
cies richness as recorded by net captures.
In general, the net capture data indicated that
the areas located at the lowest altitudes (RDSB and
BSC) possess a lower abundance than those found
in the highest areas (NE and AD). This situation
may be a natural characteristic of the birds in this
region. Manne et al. (1999) have suggested that
lower altitude species with small distribution areas
are proportionally more threatened, and therefore
more susceptible to extinction, than species of
higher altitudes. In fact, the proportion of threat-
ened species in RDSP and BSC areas was slightly
greater than the NE and AD (Table 3.); however,
it is important to point out that NE and AD were
Avifauna of Rio Doce Valley, Brazil 921
located in intermediate altitudes (500–1000 m)
and it is possible that the species associated with
this altitudinal strip could be relative generalists
and less associated with conserved environments
than species occupying the lowest and highest areas
(⬎ 1000 m).
The dominant species registered in intermedi-
ate areas were very abundant; P. leucoptera, P. mys-
taceus, and C. caudata were species that occurred
in most fragments along this stretch of Atlantic
Forest. The first two are insectivorous; P. leucoptera
is an obligatory follower of army ants, which are
very common in the area during the dry season
(June–September; Machado et al. 1988).
Nonetheless, it is still possible to find an con-
siderable portion of the original avifaunal richness
of the region. This may be because a mass extinc-
tion process, according to the prediction of Manne
et al. (1999), still has not been observed in the area.
Perhaps this situation is the result of compensatory
mechanisms that eventually allowed for the persis-
tence of species, even in highly fragmented envi-
ronments. According to our results, there is a var-
iation in the composition of species throughout the
year. The data suggest that species may be moving
among fragments within the region, and this strat-
egy may be facilitating a greater persistence of spe-
cies. Stouffer and Bierregaard (1996) showed that
near Manaus, some hummingbird species perform
seasonal movements among small fragments (even
as small as 1 ha), and these movements may explain
their persistence in fragmented areas. In the Atlan-
tic Forest, such movements may even occur be-
tween different altitudinal strips (see Sick 1997 for
examples of birds that make altitudinal movements
in the Atlantic Forest).
The ability of individuals to move among iso-
lated areas is viewed as an attenuating factor of
fragmentation. Simulation studies of population vi-
ability (Stacey & Taper 1992, Fahrig & Merriam
1994) have suggested that species that are capable
of maintaining a regime of colonizing/recolonizing
environments, tend to have greater viability. It is
possible that the current situation of populations
in the Rio Doce basin approaches that of a meta-
population concept (Levins 1969, 1970 in Andrén
1994), in which the exchange of individuals among
areas could be attenuating the effects of fragmen-
tation.
It is possible, however, that this situation will
not be maintained over the long term. It is neces-
sary to establish new conservation units to assure
the protection of nucleus populations, and the
landscapes of this region must be managed in a
922 Machado and Fonseca

manner that will facilitate the displacement dynam-
ics for individuals among areas (between the low
and high altitude areas or among fragments of the
same altitudinal zone). The altitudinal strip be-
tween 500 and 1000 m should be a priority zone
for the definition of a new protected area; the Rio
Doce State Park (35,000 ha) and the Serra do Bri-
gadeiro State Park (20,000 ha) would thereby pro-
tect a portion of the avifauna from the low and
higher altitude areas, respectively. Even fragments
of small area should be protected and eventually
enlarged, as they play an important role in the
maintenance of local populations (Hanski & Sim-
berloff 1997) and may allow for stepping-stone
type movements (Stacey & Taper 1992, van Apel-
doorn et al. 1992, Fahrig & Merriam 1994).
For characteristically interior forest species,
which are not able to move over great distances of
open areas, the establishment of corridors, or
groups of forests that could function as such,
would be of fundamental importance to promote
movements among areas. The use of corridors to
minimize the effects of habitat fragmentation and
increase the probability of recolonization (Bierre-
gaard 1990) has been suggested in several studies
(Forman & Godron 1986, Laurance 1990, New-
mark 1991, Saunders et al. 1991). In the Rio Doce
basin, a large percentage of the forests are located
near rivers (Machado 1995), and considering the
legal mandate of maintaining vegetation strips
along water courses (areas of permanent preserva-
tion according to the definition of the Brazilian
Forestry Code), it would not be technically difficult
to implement such a management program. Final-
ly, we suggest that new research, such as in-depth
evaluations of the displacement dynamics occurring
among local fragments and different altitudinal
zones, as well as detailed avifaunal inventories,
should be developed to elucidate some of the
points raised in this study.
ACKNOWLEDGMENTS
This work was financed by the United States Fish and
Wildlife Service (USFWS), Conservation International of
Brazil (CI), World Wide Fund for Nature (WWF), De-
senvolvimento Biodiversidade’s Program, Economy
(PADCT-CIAMB), and CAPES. Other institutions pro-
vided logistic support during the field and laboratory
work. Among them were the Fundação Biodiversitas, the
Federal University of Minas Gerais, the State Forests In-
stitute, Center of Regional Development and Planning
(CEDEPLAR), and the Center for the Conservation of
Birds of Brazil (CEMAVE). We also thank Bernadete Vea-
do, Luciane Machado, Ludmilla Aguiar, Lı́via Lins, and
Eduardo Marcelino V. Veado for their help in the field.
Valuable criticism and suggestions were made by Lud-
milla Aguiar, Dr. Anthony Rylands, Dr. Roberto Caval-
canti, Dr. Rogério Parentoni, Dr. Jader Marinho-Filho,
Dr. Richard Bierregaard Jr., Andrew Whittaker, and Dr.
Nathaniel Wheelwright. Marc A. Johnson helped in the
translation and revision of the English text.

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