Society for Conservation Biology

Plant Succession, Landscape Management, and the Ecology of Frugivorous Birds in

Abandoned Amazonian Pastures
Author(s): Jose Maria Cardoso da Silva, Christopher Uhl and Gregory Murray
Source: Conservation Biology, Vol. 10, No. 2 (Apr., 1996), pp. 491-503
Published by: Wiley for Society for Conservation Biology
Stable URL: http://www.jstor.org/stable/2386864
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 Plant Succession, Landscape Management, and the
Ecology of Frugivorous Birds in Abandoned
Amazonian Pastures

JOSE MARIA CARDOSO DA SILVA,* CHRISTOPHER UHL,t? AND

GREGORY MURRAYt
*Zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2 100 Copenhagen, Denmark
tDepartment of Biology, The Pennsylvania State University, University Park, PA 16802 U.S.A.
t Department of Biology, Hope College, Holland, MI 49423 U.S.A.

Abstract: From towers constructed at the interface between second-growth forest and an active and an aban-
doned pasture, we observed inter-habitat movements of fruit-eating birds in eastern Amaz6nia. The aban-
donedpasture was composed of grasses andforbs with a scattering of shrubs and small trees. The active pasture
contained a low, uniform bed of grass. A total of 47 frugivorous bird species was recorded in the second-
growth forest. We observed that 18 of these species frequented the adjacent abandoned pasture but only 3
were found in the adjacent active pasture. Fruit-eating birds flying from second-growth forest typically spent
only a few minutes in the abandoned pasture, and their movements were generally restricted to a pasture
belt of 1-80 m along the border with the second-growth forest. Most inter-habitat movement occurred during
the rainy season, which coincided with a peak in fruit availability in the abandoned pasture. Just three bird
species, Ramphocelus carbo, Tachyphonus rufus, and Thraupis episcopus, accounted for an estimated 70% of
the total movement offrugivores between the second-growth forest and the abandoned pasture. All three spe-
cies spent most of their time in the abandoned pasture foraging on shrubs and trees but exhibited differences
in their preference for specific habitat elements and in their seed-defecation habits. An understanding of bird
behaviors in altered landscapes provides important information to planners and policy makers concerned
with protecting regional biodiversity and maintaining landscape integrity. This research provides a rationale
for placing limits on the size of clearings in the Brazilian Amazon.

La sucesi6n vegetal, el manejo del paisaje y la ecologia de las aves frugivoras en pasturas abandonadas de la Ama-
zonia

Resumen: Desde torres construidas en la interface, entre un bosque de crecimiento secundario y una pas-
tura abandonada, observamos movimientos entre habitats de las avesfrugfvoras en la Amazon[a oriental.
La pastura abandonada se encontraba compuesta de pastos yforbias, con arbustos y arboles pequefnos espar-
cidos. La pastura activa contenfa una cubierta de pasto baja y uniforme. Un total de 47 especies de aves
frugivoras fue registrado en el bosque de crecimiento secundario. Observamos que 18 de estas especies fre-
cuentaron la pastura adyacente abandonada, pero solo 3 se encontraron en la pastura adyacente activa. Las
avesfrugfvoras que volaban del bosque secundario, se quedaban, en la mayoria de los casos, por s6lo unos
pocos minutos en la pastura abandonada y sus movimientos se encontraron generalmente restringidos a un
cintur6n de pasturas de 1-80 m de ancho a lo largo del borde con el bosque secundario. La mayorfa del mov-
imiento entre habitats ocurri6 durante la estaci6n lluviosa, que coincidi6 con el pico de disponibilidad de
frutas en la pastura abandonada. Solo tres especies de aves, Ramphocelus carbo, Tachyphonus rufus y Thrau-
pis episcopus, fueron responsables del 70% del total de los movimientos de frugfvoros entre el bosque de cre-

Direct all correspondence to C. Uhl, 208 Mueller Lab, The Pennsylvania State University, University Park, PA 16802, US.A., email cful @Ipsu.edu
?Brazilian affiliation: Instituto do Homem e Meio Ambiente da Amazonia (IMAZON), Caixa Postal 1015, Bel6em, 66,000, Pard, Brazil.
Paper submitted October 17, 1994; revised manuscript accepted May 30, 1995.

491

Conservation Biology, Pages 491-503

Volume 10), No. 2, April 1996

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 492 Frugivorous Birds and Landscape Management da Silva et al.

cimiento secundario y la pastura abandonanda. Las tres especies ocuparon la mayor parte de su tiempo en la
pastura abandonada alimentandose en arbustos y arboles, pero exhibieron diferencias en su preferencia por
los elementos especificos del habitaty en sus habitos de defecaci6n de semillas. Una comprensi6n del compor-
tamiento de las aves en paisajes alterados provee importante informaci6n para los planificadores y aquellas
personas involucradas en la toma de decisiones en relaci6n con la protecci6n de la biodiversidad regional y
el mantenimiento de la integridad delpaisaje. Esta investigaci6n provee unajustificaci6n para la imposici6n
de limites en el tamafno de los clareos de la Amazonia brasilefia.

Introduction Study Area

The construction of the Belem-Brasilia Highway in the
late 1950s and early 1960s opened up the eastern Ama-
zonian landscape to settlement. Most land clearing in
this region was for ranching, but pastures were fre-
quently abandoned after 4-8 years of use because of
problems with weed invasion and overgrazing (Serrao &
Toledo 1990). Currently, perhaps one-third of the pas-
ture clearings in the eastern Amazon are abandoned.
When pastures are used for only a short time and then
abandoned, forest succession is rapid; the return to for-
est is slow when the pasture-use period is long or abu-
sive (UJhl 1988). After abandonment, heavily used pas-
tures are dominated by herbs and forbs and take on the
appearance of old fields of the temperate zone.
The boundaries between pastures and adjacent ma-
ture or second-growth forest are frequently sharp in this
region. These boundaries may influence the rates and di-
rections of movement of organisms between forest and
pasture clearings (Wiens et al. 1985; di Castri et al. 1988;
Wiens 1992). This, in turn, may significantly influence
rates of plant succession in abandoned pastures.
Studies of seed rain in abandoned pastures at our
study site (E. Wiener, unpublished) revealed that seeds
dispersed by birds are much more numerous than those
dispersed by bats or wind. This suggests close links be-
tween bird movements, seed dispersal, and plant succes-
sion in abandoned pastures, perhaps similar to those
suggested for old fields in the United States (McDonnell
& Stiles 1983; McDonnell 1986), Mexico (Guevara et al.
1986), and Mediterranean France (Debussche et al.
1982; Debussche & Isenmann 1994).
We identify the frugivorous bird species that occur in
a landscape mosaic composed of active pasture, aban-
doned pasture, and second-growth forest in Eastern Am-
azonia. Then we describe the movement and behavior
patterns of three bird species that frequently crossed the
boundary between the second-growth forest and the
pasture study sites and discuss how spatial and temporal
variation in bird movements may affect seed deposition
and, ultimately, forest regeneration in abandoned pas-
tures. Finally, we provide examples of how the results of
our research might be used by both land owners and
policy makers.
We conducted our study from November 1989 to Octo-
ber 1990 at Fazenda Vit6ria (2? 59'S, 47?31'W), 6.5 km
northeast of Paragominas, Para, Brazil. Average annual
precipitation at Paragominas is 1750 mm, and there is a
pronounced dry season between July and November
(average monthly rainfall is less than 50 mm during
these months). Soils are deep, well-drained Oxisols. The
natural vegetation is evergreen tropical forest (Pires &
Prance 1985).
For our observations we selected an abandoned pas-
ture and an active pasture, both bordered by the same
tract of second-growth forest. The abandoned pasture
(7.5 ha) was planted with Panicum maximum in 1971,
used for 13 years, and then abandoned in 1984. At the
time of our study the site was dominated by grasses and
forbs, with scattered shrubs and young trees, mostly 1-4
m tall. The density of shrubs 1 m tall and larger was 2.9
individuals/100 m2, whereas the density of trees was
0.9/100 M2. The most common shrubs were Cordia
multispicata and Solanum crinitum, whereas the most
common trees were Vismia guianensis, Rollinia exsucca,
and Cecropia palmata. The active-pasture study area
presented a low, uniform bed of grass with only three
widely separated trees. This pasture was ploughed, fertil-
ized, and planted with Brachiaria bryzantha in 1988.
The second-growth forest (approximately 100 ha) that
was adjacent to both pasture sites was cleared and
grazed for only a few years before being abandoned in
the late 1970s. At the time of our study the vegetation
was composed largely of trees and vines, and the canopy
was 8-12 m high. The species composition of this site
was typical of other young, second-growth forests of the
region (UJhl et al. 1988).
Methods
Bird Counts and Behavior
In a general study of bird composition, diet, and feeding
behavior conducted in 1986 and 1989-1990, we identified
all frugivorous bird species breeding in the second-
growth forest at Fazenda Vit6ria (J. M. Silva, unpub-

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Volume 10, No. 2, April 1996

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 da Silva et al. Frugivorous Birds and Landscape Management 493
OLD-GROWTH FOREST
p1 @ \> Itation of the approach used to
SECOND-GROWTH FOREST second-growth forest to aban-
*i i ,fi -- g |set-up was used to make obser-
JL S J JJJ 5X1 L 11 < il < ^ tive pasture.
lished data). We considered a species frugivorous if it in-
cluded a substantial portion of fruit in its diet at least
during some seasons (Moermond & Denslow 1985). All
species we considered frugivorous were potential seed
dispersers for many of the woody plants found in the
second-growth forest at Fazenda Vitoria.
To determine the relative abundance of frugivorous
bird species in the second-growth forest study site, we
tallied and identified all frugivorous birds during five
counting periods of 2 hours each in November 1989.
Counts were made between 0700 and 0900 hours. We
followed a network of transects (approximately 3 km)
that covered much of the second-growth forest area. We
recorded only those individuals observed within 20 m
on each side of the transect lines. We calculated an in-
dex of relative abundance for each species by dividing
the total number of individuals found in all five count
periods by the total number of survey hours (10 hours).
The movements of frugivorous species from the sec-
ond-growth forest to both the abandoned and active pas-
tures were sampled from December 1989 to October
1990 at two-month intervals. In each survey period ob-
servations were made for one day from 0600 to 1200
hours from each of two wooden towers (12.5 m tall)
constructed at the borders between the second-growth
forest and the abandoned pasture (tower 1, Fig. 1) and
between the second-growth forest and the active pas-
ture (tower 2). Observations from each tower were
made by the same observer on alternate days. From each
tower approximately 300 m of forest-pasture border was
monitored for bird crossings.
We conducted detailed observations within the aban-
doned pasture of the movement patterns and behaviors
of the three most common frugivorous bird species,
Ramphocelus carbo (Silver-beaked Tanager), Tachypho-
nus rufus (White-lined Tanager), and Thraupis episco-
pus (Blue-gray Tanager). Six hours (from 0600 to 1200)
of observations were made daily from tower 1 during 4
consecutive days at 2-month intervals between Decem-
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< f -> er - -\ | Figure 1. A schematic represen-
-A11 R I follow the m
haviors of birds crossing from
donedpasture at Fazenda
Vit6ria, Para, Brazil. A similar
vations at the interface of the
I ; I 1 Isecond-growth forest and the ac-
ber 1989 and October 1990. Individuals of these three
species crossing from the second-growth forest to the
abandoned pasture were chosen arbitrarily and followed
until the bird returned to the second-growth forest. All
activities and movements of each selected individual were
timed (to nearest 10 sec) and mapped by two observers.
Activities within the abandoned pasture were classi-
fied in three discrete categories: foraging (acts directly
associated with search and ingestion of food), vocalizing
(including a few records of antagonistic behavior), and
maintenance (including preening, defecating, resting,
and other comfort movements). Vegetation components
visited by birds in the abandoned pasture were classified
as (1) grasses (0.5-1.5 m tall); (2) Cordia multispicata, a
spreading shrub (1-2 m tall); (3) Solanum crinitum, a
low, spreading tree (2-4 m tall); (4) Cecropia palmata,
an erect tree (3-12 m tall); and (5) mixed tree species-
other tree species in a variety of sizes and shapes. We
measured the proportion of each of these vegetation
components in the abandoned pasture site by mapping
vegetation cover in the entire 7.5-ha plot between Octo-
ber and November 1989. This entailed dividing the site
into a matrix of 25 X 25-m subplots and mapping and
directly measuring canopy cover for all vegetation com-
ponents.
In sum, for a given visit to the pasture by a given bird,
the data consisted of the vegetation components visited,
the time spent in each component, the activities in each
component, the linear distance flown between each
component (determined by diagramming bird move-
ments on the vegetation map), and the maximum dis-
tance reached from the edge of the second-growth forest.
Fruit Phenology and Seed Dispersal
To compare fruit availability in the second-growth forest
and the abandoned pasture, we monitored the phenol-
ogy of some shrub and tree species that we knew, from
previous studies, were important in the diet of frugivo-
Conservation Biology
Volume 10, No. 2, April 1996
 494 Frugivorous Birds and Landscape Management da Silva et al.
rous birds. In the abandoned pasture we monitored Cor-
dia multispicata (n = 20), Lantana camara (n = 15),
Cecropiapalmata (n = 8), and Solanum crinitum (n =
10). In the second-growth forest we monitored Rollinia
exsucca (n = 15), Vismia guianensis (n = 10), Cecro-
pia palmata (n = 14), Cordia multispicata (n = 5),
and Banara guianensis (n = 14). All plants were
checked for fruit presence once each month over the
one-year study period. We used the percentage of total
individuals with ripe fruits as a rough estimate of fruit
availability in these two habitats.
To confirm that the bird species under observation
were transporting seeds, we captured birds in mist nets
at 2-month intervals during the year-long study. At each
sample period lines of five nets (2.6 m tall and 12 m
long, with 3.6-cm mesh) were set up in four locations
within the abandoned pasture. Captures were made be-
tween 0600 and 1000 hours during three consecutive
days. Upon capture birds were identified and retained for
3 hours in paper bags for seed collection, then released.
Seeds encountered in the feces were counted and identi-
fied by using a reference collection prepared during a
previous study in the same area (Uhl et al. 1991).
Statistical Analyses
A chi-square test was used to examine seasonal differ-
ences in bird-species movements between second-growth
forest and the active and the abandoned pasture. In
cases where the number of crossings by a species was
less than five in one or both seasons, we used the bino-
mial test.
We also used also a chi-square test to compare the pro-
portion of each vegetation component (measured by
percent cover) in the abandoned pasture with the pro-
portion of total observations (records) for bird species
(e.g., R. carbo, T rufus, and T episcopus) in these vege-
tation components, irrespective of the time spent in
each vegetation component. But the chi-square test
showed only whether or not there were differences be-
tween observed and expected use of habitat compo-
nents, but not which habitats were more or less pre-
ferred. Hence, we used the method of Neu et al. (1974;
see also Haney & Solow 1992) for evaluating preference
or avoidance of specific vegetation components. For this
method we established confidence limits, based on Bon-
ferroni's adjustment of the significance level, that were
wider for each of the multiple estimates than for an esti-
mate of only one parameter. A significant preference or
avoidance at 5% was indicated by expected values not
included in the 95% confidence limits for the observed
values (Haney & Solow 1992; Andrem & Delin 1994).
We analyzed five aspects of the movements of the
three most common frugivorous species that visited the
abandoned pasture: (1) visit length, (2) maximum dis-
tance out into the pasture, (3) number of movements
Conservation Biology
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(individual flights from vegetation component to vegeta-
tion component within the degraded pasture), (4) time
between two successive movements, and (5) distance
between two successive movements. These measures
were log-transformed and analyzed using a two-way
analysis of variance (two-way ANOVA) to examine possi-
ble differences between species and seasons, or differ-
ences due to the interaction between species and sea-
sons. If significant differences were found, then a Tukey
"honestly significant" (HSD) test was performed.
All statistical tests were evaluated at the p < 0.05 level
of significance. In all analyses the rainy season corre-
sponded to the period from November to May, and the
dry season to the period from June to October.
Results
Species Richness and Abundance of Frugivorous Birds
We recorded 47 frugivorous bird species in the second-
growth forest at Fazenda Vitoria (Table 1). Eighteen of
these species moved to the abandoned pasture site, but
only 3 species moved to the active pasture. The 3 spe-
cies recorded in the active pasture were among those
observed in the abandoned pasture. The majority (83%)
of the species observed in the pastures have a body mass
less than 40 g; only 1 species, Ortalis motmot, had a
body mass greater than 100 g (Table 1).
Bird Movements Across Habitats
Three species, Ramphocelus carbo, Tachyphonus ru-
fus, and Thraupis episcopus, accounted for 70% of all
movements of frugivorous birds from the second-growth
forest to the abandoned pasture. These three species
were also the most frequent in the bird counts con-
ducted in the second-growth forest (Table 1).
In both seasons the total number of species and the to-
tal number of individual birds crossing from the second-
growth forest into the abandoned pasture were greater
than the crossings between the second-growth forest
and the active pasture (Table 1). Furthermore, the num-
ber of crossings into both pasture types was reduced sig-
nificantly during the dry season (Table 1). This seasonal
reduction was most dramatic for the five species that
moved most frequently between the second-growth for-
est and the abandoned pasture: Tachyphonus rufus,
Ramphocelus carbo, Thraupis episcopus, Thraupis pal-
marum, and Saltator maximus (Table 1).
The vegetation cover of the abandoned pasture study
site was 61% grass, 30% C. multispicata (low shrub), 3%
S. crinitum (small tree), 1% C palmata (tall tree), and
4% mixed trees. The use of these vegetation compo-
nents by the three most common frugivorous species
differed significantly from the expected based on the
 da Silva et al Frugivorous Birds and Landscape Management 495

Table 1. Species of frugivorous birds found in the landscape formed by second-growth forest, abandoned pasture, and active pasture at
Fazenda Vit6ria, Para', Brazil.

No. of movements from forest

to pastureb
Species Body mass (g) Abundancea AbnR AbnD ActR ActD

Cracidae
Ortalis motmot 300 0.60 4 3 0 0
Ramphastidae
Pteroglossus inscriptus 120 0.10 0 0 0 0
P. bitorquatus 150 0.05 0 0 0 0
P. aracari 300 0.15 0 0 0 0
Picidae
Melanerpes cruentatus 60 0.20 0 0 0 0
Veniliornis affinis 30 0.30 0 0 0 0
Tyrannidae
Camptostoma obsoletum 10 0.55 5 6 0 0
Phaeomyias murina 12 1.15 6 5 0 0
Myiopagis caniceps 10 0.40 0 0 0 0
Myiopagis giamardii 10 0.20 0 0 0 0
Elaenia cristata 15 0.50 2 1 0 0
E flavogaster 25 0.75 5 3 0 0
Mionectes oleagineus 10 1.05 0 0 0 0
Tolmomyiasflaviventris 12 1.60 3 1 0 0
Attila cinnamomeus 40 0.20 0 0 0 0
Myiarchusferox 22 0.30 3 1 0 0
Megarbynchus pitangua 60 0.15 1 0 0 0
Myiozetetes cayennensis 22 0.35 6 2 0 0
M. similis 22 0.15 0 0 0 0
My/odynastes maculatus 50 0.15 1 0 0 0
Tityra cayana 70 0.50 0 0 0 0
T inquisitor 45 0.10 0 0 0 0
T semifasciata 80 0.25 0 0 0 0
Pipridae
Manacus manacus 15 1.85 0 0 0 0
Pipra rubrocapilla 10 0.75 0 0 0 0
Turdidae
Turdus leucomelas 58 1.75 0 0 0 0
Turdus nudigenis 60 0.30 0 0 0 0
Emberizidae
Arremon taciturnus 25 0.40 0 0 0 0
Saltator coerulescens 50 0.05 0 0 0 0
Saltator maximus 40 0.75 13 4c 0 0
Schistoclamys melanopis 35 0.10 8 2 3 2
Cissopis leveriana 75 0.15 0 0 0 0
Tachyphonus rufus 35 3.65 51 18d 5 2
Ramphocelus carbo 25 5.60 106 53d 7 2
Thraupis episcopus 35 2.90 25 9d 0 0
Thraupis palmarum 25 2.35 16 4d 0 0
Euphonia cayennensis 12 0.15 0 0 0 0
Euphonia violacea 15 0.75 0 0 0 0
Dacnis cayana 12 0.35 0 0 0 0
Chlorophanes spiza 15 0.30 0 0 0 0
Cyanerpes caeruleus 10 0.55 0 0 0 0
Cyanerpes cyaneus 12 0.25 0 0 0 0
Parulidae
Conirostrum speciosum 9 0.25 0 0 0 0
Coerebaflaveola 9 0.70 3 0 0 0
Vireonidae
Cychiarbis gujanensis 28 0.50 5 1 0 0
Icteridae
Icterus cayannensis 40 0.25 0 0 0 0
Cacicus ce/a 65-100 0.15 0 0 0 0
Total 263 113 15 6

a Relative abunda
hours).
bAbnR =number of movements from second-growth forest to abandoned pasture during the rainy season; AbnD =number
from second-growth forest to abandoned pasture during the dry season; ActR =number of movements from second-growth forest to active pas-
ture during the rainy season; ActD =number of movements from second-growth forest to active pasture during the dry season.
Cp < 0.05 for the comparisons of number of movements of each species from second-growth forest to pastures in different seasons.
dp < 0.001 for comparisons, as in footnote c.

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496 Frugivorous Birds and LandscapeManagement da Silva et al.

proportions of each component in the abandoned pas-

ture: R. carbo (X2 = 1368, df = 3, p < 0.001), T rufus
Romplocelus corbo (n 249)
(X2 = 1457.2, df 4,p < 0.001), and T. episcopus (X2 -
5808, df = 2, p < 0.001).
R. carbo did not use the grass component and used
70- mixed trees, S. crinitum, C palmata, and C multispi-
cata, significantly more than expected (Fig. 2). T rufus
used the mixed-tree, S. crinitum, and C. palmata com-
50 ponents more than expected, the C. multispicata com-
ponent within expected limits, and the grass compo-
nent much less than expected (Fig. 2). T episcopus did
30- not use the grass and C. multispicata components, used
S. crinitum within expected limits, and used the C. pal-
mata and mixed-tree components much more than ex-
_ 10 pected (Fig. 2). For all three species the pattern of habi-
tat use did not change seasonally.
0_
In any season R. carbo moved into the abandoned pas-
o Techyphonus rufus (n 142) ture mainly for foraging (Fig. 3). Foraging behavior for
this species was recorded mainly on C multispicata in
both rainy and dry seasons. During the rainy season vo-
calization behavior was recorded mainly on S. crinitum
*4-~ 70
and mixed trees, but during the dry season it was re-
corded mainly on C. multispicata and mixed trees (Fig.

~' 50-
3). Maintenance behavior was recorded in both seasons
mainly on S. crinitum and mixed trees (Fig. 3).
During both the rainy and dry seasons T rufus moved

30 into the abandoned pasture mainly for vocalizing and

foraging and concentrated these activities in C. multispi-
cata and S. crinitum. Maintenance behavior was re-

' 10L corded mainly on S. crinitum in rainy as well as dry sea-

sons (Fig. 3).
In both seasons T episcopus moved to the abandoned

o Throupis episcopus (n-43) pasture mainly for foraging (Fig. 3). During the rainy sea-
90- son foraging behavior was recorded mainly on C. pal-
mata and mixed trees, but during the dry season the
percentage of feeding behavior on C. palmata increased
significantly (Fig. 3). Vocalization and maintenance be-
haviors were recorded only during the rainy season and
mainly on C. palmata.
50-
R. carbo, T. rufus, and T. episcopus dispersed seeds
into the abandoned pasture mainly through their feces.
From our tower we observed seed defecation on 110 oc-
30 casions. Defecation was most common when birds were
perched on S. crinitum (43% of all defecation observa-
tions), followed by C. palmata (25%), and then C. multi-
10
spicata (7%). In the specific cases of R. carbo and T2 ru-
0 fus, defecation was observ-ed mostly associated with S.
crinitum, whereas for T episcopus it was most common
Vegetation components on C. palmata and the mixed-trees.

Vegetation components Figure 2. The percentage of the abandoned pasture

* Pa stu re area covered by eoch vegetation component
D1 Bird vis its to each vegetation component
site covered by five distinct vegetation components
and the percentage of total bird movements directed to
each of these vegetation components for each of three
tanagers at Fazenda Vit6ria, Parai, Brazil. The error
bars indicate the 95% confidence limits calculated ac-
cording to the method proposed by Neu et al. (1974).

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da Silva et al. Frugivorous Birds and Landscape Management 497

Romphocelus corbo Tochyphonus rufus Throupis episcopus

Rainy season Rainy season Rainy season

40 40 40

30- 30- 30-

20- 200 20

10- 10- 10-

U)

Dry season Dry season Dry season

o 40- 40- 80-

c0 70-
4) 30- 30- 60-

50-

20 20 40L

10- ~~~~~~~~~~~10- 20

10

0 0~~~~~~~~~~~~~~~~~
g \, \6\O\% P' \- \@ ec.,

Vegetation components

EZZiZI Foraging Vocalizing _ Maintenance

Figure 3. The distribution of bird activity dedicated to foraging, vocalizing, and maintenance activities in each oj
the five vegetation components for each of three tanagers at Fazenda Vit6ria, Para, Brazil.

Visits to the abandoned pasture varied from 0.5 to 23
minutes in length for R. carbo, T rufus, and T episco-
pus (Table 2). Visit length differed significantly among
species (two-way ANOVA, F = 10.4, p < 0.00 1) and sea-
sons (two-way ANOVA, F = 5.4, p < 0.05), but not be-
cause of the interaction between species and season
(F = 0.268, p < 0.76). There was no significant differ-
ence in visit length between R. carbo and T rufus (HSD,
p = 0.24), but visit length by both of these species was
significantly longer than for T episcopus (HSD, p <
0.01). Visits for all three species were longer in the rainy
season than during the dry season (HSD, p < 0.05).
The maximum distance out into the abandoned pas-
ture from the second-growth forest edge reached by the
three frugivorous species varied between 2 and 254 m
(Table 2), but most of the movements were between 1
and 80 m (Fig. 4). No significant difference in this pa-
rameter was found among species (two-way ANOVA,
F = 0.76, p = 0.38), between seasons (two-way
ANOVA, F = 1.60, p = 0.20), or due to the interaction
between species and season (two-way ANOVA, F
0.15,p = 0.85).
The number of movements among vegetation compo-
nents in the abandoned pasture during a given visit var-
ied between 2 and 12 for the three species (Table 2).
There was a significant difference in the number of
movements among species (two-way ANOVA, F = 9.59,
p < 0.001), but not between seasons (two-way ANOVA,
F = 1.85, p = 0.17) or due to the interaction between
species and season (two-way ANOVA, F = 0.53, p =
0.58). The number of individual flights (movements)
within the abandoned pasture did not differ between R.
carbo and T rufus, but both of these species had more
movements than T. episcopus (HSD, p < 0.00 1).
The distance covered in individual flights within the
abandoned pasture varied between 1 and 225 m for the
three species (Table 2). There were significant differ-
ences in this parameter among species (two-way ANOVA,
F = 7.77, p < 0.001) but not between seasons (two-way
ANOVA, F = 0.04, p = 0.83) or due to the interaction
between species and season (two-way ANOVA, F =
0.98, p < 0.37). The flight distance for T episcopus was
greater than that for either R. carbo or T rufus (HSD,
p < 0.001).

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 498 Frugivorous Birds and Landscape Management da Silva et al

Table 2. Movement patterns for Ramphocelus carbo, Tachyphonus rufus, and Thraupis episcopus in the rainy and dry seasons in the
abandoned pasture study site at Fazenda Vit6ria, Para', Brazil.

Ramphocelus carbo Tachyphonus rufus Thraupis episcopus

Movementpatterns Rainy Dry Rainy Dry Rainy Dry

Visit length (min)

mean (SD) 5.7 (4.2) 4.2 (2.6) 6.5 (4.8) 4.9 (2.5) 3.5 (1.5) 2.3 (1.1)
min-max 1-23 1-14.5 2-23 2-11 1-8 0.5-4
n 56 54 26 30 25 10
Maximum distance (m)
mean (SD) 52 (41) 53 (46) 61 (40) 54 (45) 68 (55) 59 (17)
min-max 2-206 5-194 9-148 5-189 19-254 25-81
n 56 54 26 30 25 10
Number of movements
mean (SD) 3.5 (1.7) 2.9 (1.3) 3.8 (2.4) 3.2 (1.3) 2.2 (0.3) 2.2 (0.3)
min-max 2-11 2-7 2-12 2-7 2-3 2-3
n 56 54 26 30 25 10
Distance between movements (m)
mean (SD) 36 (28) 37 (28) 39 (35) 39 (33) 64 (53) 59 (46)
min-max 1-190 1-135 1-149 1-221 5-225 1-144
n 200 158 100 98 55 22
Time between movements (min)
mean (SD) 2.3 (2.0) 2.2 (1.4) 2.3 (2.3) 2.2 (1.5) 2.9 (1.6) 1.8 (0.8)
min-max 0.5-13 0.5-8 0.5-13 0.5-8 1-8 0.5-3
n 144 105 74 68 30 13

The time between successive movements varied be-
tween 0.5 and 13 minutes (Table 2). No significant dif
ferences were found in this parameter among species
(two-way ANOVA, F 0.67, p = 0.53), between sea-
sons (ANOVA, F - 2.04, p = 0. 15), or due to the interac-
tion between species and season (two-way ANOVA, F
2.24,p =0.10).
Seed Dispersal and Fruit Phenology
in the dry season; x2 = 0.55, p > 0.45, df = 1). In addi-
tion the species richness of seeds found in bird feces
was higher in the rainy season than in the dry season
(Table 3). Overall, no striking differences were apparent
in the species composition of seeds in the feces of the
three dominant tanager species; in all cases C. palmata
made up more than 50% of all seeds with the shrubs,
Lantana camara and C. multispicata, also in evidence
(Table 3).

Fruiting of the plant species that we studied was more

common in both the second-growth forest and the aban-
doned pasture during the rainy season than in the dry
season. There was a significant correlation between the
percentage of individuals with ripe fruits and monthly
precipitation in both the second-growth forest (Spear-
man rank correlation, Rs = 0.82, n = 11, p < 0.01) and
the abandoned pasture (Rs = 0.78, n = 11, p < 0.01).
Most of the seeds dispersed by frugivorous birds visit-
ing the pasture belonged to small-seeded shrubs and pio-
neer tree species (Table 3) that were common in both
the abandoned pasture and the second-growth forest.
Seeds of 17 plant species were recovered in 103 fecal
samples of 11 bird species that we captured in mist nets
in the abandoned pasture. The majority of these seeds
(88%) were from four plant species that were already
present as mature individuals in the abandoned pasture
(Table 3). In agreement with phenology data, the num-
ber of birds that had seeds in their feces was signifi-
cantly greater in the rainy season (74 versus 29; x2 =
19.6, p < 0.001, df = 1), even though the number of
birds captured in the mist nets did not differ between
seasons (115 total captures in the rainy season and 104
Discussion
Factors Affecting Bird Movements
The frugivorous birds inhabiting the second-growth for-
est that we studied may be grouped into three major cat-
egories according to their responses to the two bound-
aries examined: (1) species that did not cross either one
of the pasture boundaries (28 species, Table 1); (2) spe-
cies that crossed only the boundary between the sec-
ond-growth forest and abandoned pasture (15 species);
and (3) species that crossed both boundaries (3 spe-
cies). The second group is composed mainly of small-
bodied bird species (Table 1) that moved to the aban-
doned pasture mainly during the rainy season, when
small, fleshy fruits were available in this site. The third
group is also composed of small-bodied species (Table
1), two of which-R. carbo and T Rufus-are among
the most abundant species in disturbed environments in
eastern Amazonia (Novaes 1969, 1973).
Wiens (1992) suggested that the decision of an organ-
ism to cross a boundary between two patches (e.g., veg-

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da Silva et al. Frugivorous Birds and Landscape Managemsent 499

etation types) is likely to be based on a large number of

Ramphocelus corbo
factors related to the costs and benefits of occupying
60-
each patch. Some factors that could cause an organism
to cross from one patch to another include (1) improved
mating success, (2) greater reproductive output, (3)
lower physiological stress, (4) lower predation risk, (5)
40
reduced competition, (6) greater resource availability,
and (7) lower energy expenditure in foraging. In our
study the first two factors are not relevant because the
species moving between the second-growth forest and
20- the pastures did not breed in the pastures. Likewise, fac-
tors 3 and 4 are probably not strong causal elements be-
cause these bird species occupy exposed environments
in both patch types (i.e., tree tops and edges in the sec-
ond-growth forest and low-shrub and grass-forb cano-

Tochyphonus rufus
pies in abandoned and active pastures). Of the remain-
ing possibilities, a combination of greater resource
E 60
availability and lower energy expenditure in foraging
may be the most probable factor stimulating bird move-
0

E ments from the second-growth forest to the abandoned

40- pasture. During the dry season, birds crossings to the
abandoned pasture were reduced because fruits were
0
scarce, even though the structure of the habitat did not
change significantly. Regardless of the season, the active
20- pasture was less attractive to birds than the abandoned
pasture because the former has neither plants that pro-
duce fleshy fruits nor habitat structure (for perches) that
could be used for frugivorous bird species.
These results agree with the notion that old fields with
01
scattered trees and shrubs, such as our abandoned pas-
60 from Thredpis (piscopus ture are indeed more attractive to frugivorous birds than
homogeneous grasslands (McDonnell & Stiles 1983;
Guevara et al. 1986; McDonnell 1986; Campbell et al.
1990; Debussche & Isenmann 1994). Our findings also
40- suggest that the degree of attractiveness of an aban-
doned pasture to frugivorous birds will increase if the
scattered trees and shrubs produce an abundance of
small, fleshy fruits, at least during some seasons.

20-

Influence of Birds on Plant Succession

Because the movements of birds in the abandoned pas-

0-
'A1 r03 b, N0 \@ \?10\ \\113 \ro 0 1O0 1
0 e,~0 ~0 ~,0 O~o0 0 0,0%e0\ -7
Distance from the edge (in)
ture were directed to certain vegetation components
(trees and shrubs) that served as food sources and perch
sites, it follows that the seeds that these birds were car-
rying were being dispersed in a nonrandom fashion. Be-
cause frugivorous birds inhabiting second-growth for-
ests did not move very far into abandoned pastures, the

EZ I Wet season _ Dry season
Figure 4. Frequency distribution of the maximum dis-
tance out into the abandoned pasture (away from the
second-growth forest edge) reached by Ramphocelus
carbo, Tachyphonus rufus, and Thraupis episcopus on
individual visits at Fazenda Vitoria, Para, Brazil.
seeds dispersed by them were deposited mainly under
shrubs and trees in a pasture belt 1-80 m wide that bor-
dered the second-growth forest (Fig. 4). The resulting
seed shadows, therefore, were a combination of two dis-
tinct patterns: a general decrease in seed density in rela-
tion to the distance to the maternal plant (or source veg-
etation; Fig. 4) and a localized increase in seed density in

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 500 Frugivorous Birds and Landscape
Table 3. Seeds collected in the feces of frugivorous birds mist-netted in the abandoned pasture study site at Fazenda Vitoria, Para, Brazil.
Seed Plant Ramphocelus Tachyphonus Thraupis Other
Species size (mm)n form carbo
Cecropia palmata 1.0 tree
50 (0) 302
Lantana camara 2.8 shrub 73 (62) 33 (3) 39 (0) 33 (2)
Cordia multispicata 3.5 shrub 55 (22) 5 (7) 2 (0) 48 (48)
Rollinia exsuca 5.6 tree 10 (0) 0 (0) 18 (0) 31 (12)
Other (13 species) 1.0-13.0 shrub-tree 16 (8) 4 (9) 5 (0) 21 (82)
Total no. of captures with seeds 44 (9) 8 (5) 6 (0) 16 (15)
Total seeds 456 (95) 191
Total no. plant species 14
a Seed size is the average length along the longest axis.
b First number is rainy season total; number in parentheses is dry-season total.
relation to the existing vegetation components closely
linked with the perching and defecating behavior of
birds (Figs. 2 & 3).
Most of the seeds dispersed by frugivorous birds in
our study area were of small-seeded shrubs and pioneer
tree species (Table 3) that were common in both the
abandoned pasture and the second-growth forest. The
small size of the frugivorous birds moving into aban-
doned pastures undoubtedly places restrictions on the
size of the seeds that they are able to transport (Moer-
mond & Denslow 1985), but floristic composition of the
source vegetation may also be an important factor influ-
encing the species diversity and the overall size of the
seeds dispersed by birds into adjacent clearings. In con-
trast with our results, Guevara et al. (1986) found that
seeds recorded beneath isolated trees in grasslands in
Mexico were of primary forest species rather than pio-
neer species. A possible explanation for this might be
the difference in composition and structure between
the vegetation source that bordered the Mexican pas-
tures (mature forest) and that bordering our study area
(second-growth forest).
Work by Nepstad et al. (1991) revealed that most of
the small seeds dispersed by birds into Amazonian aban-
doned pastures have a low probability of establishment.
Seed and seedling predation by both leaf-cutter ants and
rodents takes a heavy toll, and drought stress also results
in seedling death, but some seeds do survive to germi-
nate and grow to maturity. Because frugivorous birds
disperse seeds to a restricted group of vegetation com-
ponents in the abandoned pasture, these sites play an
important role as centers of establishment and subse-
quent growth of bird-disseminated plant species (Mc-
Donnell & Stiles 1983; McClanahan & Wolfe 1987, 1993;
Campbell et al. 1990; Uhl et al. 1991; Robinson & Handel
1993; Desbussche & Isenmann 1994; Vieira et al. 1994).
The movements of frugivorous birds from second-
growth forests to abandoned pastures in eastern Amazo-
nia appear to be closely linked with foraging for fleshy
fruits during the rainy season. Hence, frugivorous birds
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Management da Silva et al.
Number of seedsb
rufus episcopus species
(3) 149 (0) 77 (0)
(19) 141 (0) 183 (144)
(3) 13 (2) 8 (0) 16 (7)
possibly do not play a decisive role as dispersal agents in
the very beginning of plant succession of abandoned
pastures, when pioneer trees and shrubs, which pro-
duce small and fleshy fruits, have not yet established.
Possibly bats play a more important role in this phase of
plant succession because some of the dominant pioneer
trees found in Amazonian abandoned pastures (e.g.,
Solcanum crinitum) are dispersed by bats. But when
some plants producing fleshy fruits have already been
established, certain bird species (e.g., T rufus, R. carbo,
T episcopus) start to move to abandoned pastures and
disperse seeds there. These frugivorous bird species
could be viewed as keystone species because they ap-
pear to play a pivotal role in moving seeds of woody spe-
cies out into clearings and thereby help ensure that for-
est succession begins.
The young secondary forests that slowly develop on
abandoned pastures appear to be similar to primary for-
est in terms of ftinction (Nepstad et al. 1995), but they
lack many of the plant and animal species typical of ma-
ture rainforest. It may take centuries before they could
approximate the biotic richness of the pre-existing forest.
Implications for Laiidscape Management
All segments of society should be concerned that land
and biological resources be used sensibly and respect-
ftilly. In Amazonia, where natural forest ecosystems are
being replaced by farms and pastures, the wisdom of
such development is still in question. Hence, it is pru-
dent to assure that forests could regrow on clearings if
development efforts fail. Our work and that of Nepstad
et al. (1991) provide evidence that one of the most se-
vere impediments to forest regeneration in severely de-
graded Amazonian clearings is the lack of seeds from
woody species. Animals that disperse seeds move into
small clearings, but seed dispersal decreases as clearing
size increases, and this retards plant succession.
Placing controls on the size of clearings in Amazonia
would help facilitate forest succession should clearings
da Silva et al. Frugivorous Birds and Landscape Management 501

TRADITIONAL ALTERNATIVE
CLEARING APPROACH

E E

ACTIVE _V_ X V -1 JL 'A o CD-

PASTURE co a

L L L
50 -150 m 5 -10

FIVEYEARS AFTER
ABANDONMENT

TEN YEARS AFTER

ABANDONMENT L /

Primary forest Active pasture

Second-growth forest r7l Abandoned pasture

Figure 5. An illustration of how clearing size and shape may affect the rate offorest succession in abandoned pas-
tures in eastern Amazonia. Forest succession will be slow andfire will be likely in the case of the traditional clear-
ing. An alternative clearing approach would permit more-rapid colonization of woody plants following pasture
abandonment because animals dispersing seeds offorest tree species would move throughout these smaller clear-
ings and fire movement would be retarded.

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 502 Frugivorous Birds and Landscape Management da Silva et al.
be abandoned. One way to set limits on the size of clear-
ings would be first to list the animal species that are
known to disperse tree seeds. These dispersal agents
could then be studied to assess their importance in
terms of the type and amount of seeds they disperse and
the distance they move out into openings. With this in-
formation, criteria could be developed for limiting the
size of clearings. For example, if the analysis revealed
that the number of plant species likely to have their
seeds dispersed to clearings declined sharply beyond a
certain distance (say 200 m), this distance could then
form the basis for legislation to limit the size and/or
shape of openings. Concomitantly, it is essential to pro-
tect bird and mammal species that perform important
seed dispersal services from excessive hunting pressure.
Limits on the size of clearings need not lead to the
elimination of productive activities, but such limits may
change the geometry of clearings. For example, in Fig. 5
we show two pasture clearings. The first is a large,
square opening typical of present-day clearings. When
these large clearings (2-10 km across) are abandoned,
woody plants invade only slowly because the dispersal
of seeds by animals appears to be restricted largely to
the borders of such clearings. Furthermore, these huge
openings are hot and dry and bum frequently (Uhl et al.
1991). The second clearing type depicted in Fig. 5 is de-
signed so that no point in the pasture is more than a few
hundred meters from forest. Fingers of forest separate
the five pasture paddocks. In addition to assuring that
forest succession will proceed quickly should the site be
abandoned, this design provides better control of fire
and also of herd movements, but it would be more ex-
pensive to implement.
It is not too late to contemplate measures to place lim-
its on the size of clearings in Amazonia. Less than 10% of
the forested portion of the Brazilian Amazon has been
deforested (Skole et al. 1994), and there is a growing ap-
preciation for the benefits of forest cover. Forests are be-
ginning to be valued for their biodiversity (potential
sources of medicines and crop germ plasm), nontimber
forest products (dyes, oils, fibers), timber resources
(over 300 Amazonian tree species are now harvested for
their wood products; Martini et al. [1994]), and their
role in regulating regional climate. This increasing valua-
tion of standing forest is a strong impetus for taking mea-
sures to assure that forests can recover rapidly following
misguided deforestation schemes. Coupled with an ex-
isting law that limits to 50% the total deforestation on a
given property (Brazilian Forestry Code No. 4771), new
legislation placing restrictions on the size of clearings
would go a long way toward maintaining the integrity of
the Amazon landscape. With the availability of LANDSAT
imagery and the increasing use of global positioning sys-
tems and geographic information systems, it would be
possible to monitor and enforce such forvvard-looking
legislation (de Almeida & Uhl 1995).
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Acknowledgments
We are grateful to Jorge Vieira for field assistance, to Fla-
vio Figueiredo for drawing the figures, and to Ima C. Vie-
ira and Eric Wiener for supplying us with their unpub-
lished data. We thank Dan Nepstad, Jack Putz, Rob
Bierregard, S. Robinson, Jon Fjeldsa, Ellen Main, and two
anonymous referees for their comments on a draft of the
manuscript. The field study was supported by a grant
from the Natural Geographic Society. J. M. C. Silva is
supported on a scholarship of the Conselho Nacional
de Desenvolvimento Cientifico e Tecnologico (CNPq),
Brasilia, Brazil.
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