Composition Changes in a Subandean Avifauna after Long

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Composition Changes in a Subandean Avifauna after Long
Society for Conservation Biology
Composition Changes in a Subandean Avifauna after Long-Term Forest Fragmentation
Author(s): Luis Miguel Renjifo
Source: Conservation Biology, Vol. 13, No. 5 (Oct., 1999), pp. 1124-1139
Published by: Blackwell Publishing for Society for Conservation Biology
Stable URL: http://www.jstor.org/stable/2641746
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Composition
Long-Term
Changes
Forest
in
a
Subandean
Avifauna
after
Fragmentation
LUIS MIGUELRENJIFO*
International Center for Tropical Ecology, Department of Biology, University of Missouri-St. Louis, 8001 Natural
Bridge Road, St. Louis, MO 63121-4499, U.S.A., and Fundaci6n Herencia Verde, A.A. 2681, Armenia, Columbia
Abstract: Current understanding of the effects offorestfragmentation is based largely on studies in temperate regions, Australia, and Neotropical lowlands. In contrast, the consequences of anthropogenic forest fragmentation for Andean avifaunas are poorly understood, despite large-scale habitat loss and fragmentation. I
assessed the effects of long-termnfragmentation on a subandean avifauna in Colombia by comparing the occurrence of bird species in forestfragments isolated over 50-90 years with the original avifauna. Prefragmentation bird composition was based on historical records and current species composition in continuous forest.
The original avifauna had approximately 139 forest species and 45 species of open habitats. Among forest
species, 30% wverecurrently extinct in fragmentedforest and 4% were regionally extinct. At least 23 nonforest
species colonized the region from the lowlands following deforestation. Species with small geographic ranges
and those that wverelocally)scarce or rare throughout their ranges were likely to be locally extinct. Forest raptors, terrestrial insectivores, and large frugivores were highly extinction prone, whereas nectarivores, small
frugivores, and aerial insectivores were highly resilient; other guilds were intermediate. Antbirds (Fornicariidae, Thamnophilidae), Cotingas, and, especially, Icterids were highly extinction prone. Large body size was
not a determinant of vulnerability except among frugivores. Sixty-two percent of the species of special conservation concern wvereextinct in fragments. These results suggest that only large forest tracts will ensure the
survival of a large proportion of subandean avifaunas. Fragments of mature forest, however, may support a
diverse avifauna, including small populations of globally endangered species several decades after isolation.
Th-esefragments could play an imnportantrole in the restoration of local avifaunas. A good understanding of
the mechanisms that allow persistence in such fragments may prove essential for the conservation of those
species for which no large tracts of suitable habitat remzain.
Cambios en la Composici6n de la Avifauna Subandina despues de una Fragmentaci6n de LargoPlazo del Bosque
Resumen: El entendimiento que se tiene actualnente de los efectos de lafragmentaci6n de bosques esta basado en gran parte en sobre estudios de zonas templadas, Australia y tierras bajas del Neotr6pico. Por otra
parte, las consecuencias de la fragmentaci6n antropogenica de bosques sobre las avifaunas andinas son
poco conocidas, a pesar de la perdida yfragmentaci6n de habitats a gran escala. Evalue los efectos de la fragmentaci6n a largo plazo sobre una avifauna subandina en Colombia, comparando la avifauna en fragmentos aisladospor mas de 50-90 afnos con la avifauna original. La composici6n original de la avifauna se bas6
en registros hist6ricos y la conzposici6n actual en bosque continuio. La avifauna original tenfa aproximadamente 139 especies de bosque y 45 especies de habitats abiertos. El 30% de las aves de bosque se han extinguido en los bosquesfragmentados y el 4% se han extinguido regionalmente. Al menos 23 especies de zonas
abiertas colonizaron la regi6n desde las tierras bajas siguiendo la deforestaci6n. Las especies con distribuciones geogrdficos restringidas, escasas localmente o raras a lo largo de su distribuci6n fueron propensas a
extinguirse localmente. Las rapaces de interior de bosque, los insectfvoros terrestres y losfrugfvoros grandes
fueron altaimente propensos a extinguirse; mientras que los nectarivoros, frugivoros pequenios e insectfvoros
aereos fueron resilientes; otros gremniosfueron intermedios. Los hormigueros (Formicariidae y Thamnophil-
' Current address: Institutto de Investigaci6n de Recursos Biol6gicos Alexander von Humboldt, A.A. 8693, Santafe de Bogotd, Colombia,
email [email protected]
Paper submittedJaune 19, 1998; revised manuscript accepted Februa;y 3, 1999.
1124
Conservation Biology, Pages 1124-1139
Volume 13, No. 5, October 1999
Renjifo
Long-Term
Effectsof ForestFragmentatioz
1125
idae), las Cotingas y especialmente los Icteridos fueron altamente vulnerables. Tener un taman-o corporal
grande no fue un determinante de vulnerabilidad excepto entre los frugivoros. El sesenta y dos porciento de
las especies de preocupaci6n especial para la conservaci6n se extinguieron en los bosques fragmentados. Estos resultados sugieren que s6lamente areas grandes de bosque continuo asegurardn la supervivencia de
una proporci6n grande de las avifaunas subandinas. Sin embargo, los fragmentos de bosque maduro
pueden soportar una avifauna diversa que incluye poblaciones pequefnas de especies amenazadas mundialmente despues de varias decadas de aislamiento. Estos fragmentos podrian jugar un papel importante en la
restauraci6n de avifaunas locales. Un buen entendimiento de los mecanismos que permiten la persistencia
en fragmentos puede ser escencial para la conservaci6n de aquellas especies para las que no quedan remanentes de hdbitat grandes.
Introduction
Habitat fragmentation is one of the primary threats to
bird populations throughout the world. Current understanding of the processes that lead to changes in fragmented ecosystems is based largely on studies in temperate regions, Australia,or Neotropical lowlands (Laurance
& Bierregaard1997). Effects of anthropogenic forest fragmentation on tropical montane avifaunasare poorly documented, even though many montane species are particularly vulnerable because of small geographic ranges and
narrow habitat requirements (Kattan 1992; Balmford &
Long 1994; Renjifo et al. 1997). Lowland and montane
avifaunasdiffer in trophic structure and taxonomic composition (Renjifo et al. 1997) and may, therefore, differ in
their response to forest fragmentation.
Several ecological and biogeographical traits have
been associated with likelihood of extinction. For example, large species and species of forest interior that are
reluctant to cross open areas are consistently reported
to be extinction prone, whereas edge species are reported as resilient (Willis 1974, 1979; Leck 1979; Karr
1982; Stouffer & Bierregaard 1995a). Species that depend on spatially and temporally variable resources,
such as fruit and nectar, often need to move over large
areas and are also thought to be highly susceptible to
fragmentation (Loiselle & Blake 1992). Frugivores, especially large species, are consistently found to be extinction prone (Restrepo et al. 1997). Some nectarivores,
however, have been reported as resilient (Stouffer &
Bierregaard1995b).
Rarity also has been recognized as a predictor of extinction. Rare species include those with a small geographic distribution, narrow habitat specificity, or small
population size (Terborgh & Winter 1980; Rabinowitz et
al. 1986). In some Neotropical regions, such as the Colombian Andes and the Atlantic forest of Brazil, most
species are rare in one or more of these dimensions
(Kattan 1992; Goerck 1997). Species near the limits of
their geographic range often are locally rare and, therefore, prone to extinction (Karr 1977; Rosenzweig & Lomolino 1997). In addition, demographic characteristics
of populations play an important role in the extinction
of local populations. Species with low adult survival
rates or high population variability are extinction prone
(Karr 1990).
Species that move between fragments are less likely to
go locally extinct because their populations could be
supplemented through immigration and recolonization
(Burkey 1989). For instance, although migratory species
breeding in fragmented temperate forest often exhibit
negative rates of recruitment, they persist because of
their ability to recolonize fragments when arriving from
their wintering grounds (Haila et al. 1993; Robinson et
al. 1995; Brawn & Robinson 1996).
Documentation of avian extinction in fragmented forests has followed two basic approaches (Kattan et al.
1994): a size-based and a historical-based approach. The
first compares avifaunas in forest fragments of different
size (e.g., Terborgh et al. 1997), and the second follows
changes in avifauna composition over time at an area
once covered by extensive forest that has been fragmented (e.g., Bierregaardet al. 1992). The historical approach offers a more direct measurement of extinctions,
but, given that long-term historical data on the composition of specific avifaunas are rarely available, it is usually
restricted to the short-term effects of fragmentation (but
see Willis 1974; Kattan et al. 1994).
The purpose of my study was to document changes in
the avifauna of a subandean region (i.e., midmontane)
85 year after large-scale deforestation and fragmentation
and to evaluate the association of extinction with factors
such as body size, trophic group, phylogenetic background, migratory strategy, and rarity. I used a combination of historical and area-based data to overcome some
of the limitations encountered previously. The study
was possible due to a unique suite of characteristics in
the study region. First, historical records of forest cover
and avifauna predate landscape transformation. The
study region was not settled in the eighteenth century
and was covered by unbroken forest. In 1801 Alexander
von Humboldt described it as "thick forest, completely
uninhabited, with not a single cabin nor a means of subsistence" (in Santa 1993). Clearing of the forest began
during the second half of the nineteenth century, with
the establishment of five towns within the study region
or immediate proximity (Valencia 1964; Santa 1993).
The region was still primarily covered by extensive for-
Conservation Biology
Volume 13, No. 5, October 1999
1126
Long-TermEffectsofForestFragmentation
Renjifo
est in 1911 when the avifauna was first documented
(Chapman 1917) but was extensively deforested shortly
thereafter. Second, a large tract of forest remains in the region, which allows comparison between continuous forest
and forest fragments. Finally, there are fragments of mature forest that allow the control of confounding effects of
comparing prefragmentationmatureforest with secondary
forest fragments. This study may help us understandwhat
could happen if deforestation eliminates the last tracts of
continuous forest in the CordilleraCentralof Colombia.
lesser extent, exotic-tree plantations (i.e., Pinus, Cupressus, and Eucalyptus). Fragments are relatively small,
usually <20 ha, but a few large remnants (>100 ha) occur in inaccessible canyons. The northwestern part of
the study region, within Ucumari Regional Park and
Otuin-QuimbayaFauna and Flora Sanctuary, is covered
by extensive mature and secondary subandean forest
(hereafter called continuous forest). There, subandean
forest covers several thousand hectares and is continuous toward the north and east of the study region with
tens of thousands of hectares of Andean forest.
Methods
DataCollection
StudyRegion
The avifaunaof the southern part of the study region was
examined in 1911 by ArthurAllen and Leo Miller during
an expedition of the American Museum of NaturalHistory
(AMNH).Detailed accounts of species collected, description of collecting sites and explored areas, and landscape
photographs were published by Chapman (1917). In addition, I examined voucher specimens, field notes on species seen but not collected, and numerous unpublished
photographs of Salento, Filandia, and surrounding landscapes obtained during the expedition at the archives of
the AMNH.These sources provided data on the avifauna
and extent of forest cover in 1911.
I studied current bird species composition from January
1996 to January 1997 in eight fragments surrounded by
pastures, eight fragments surrounded by exotic-tree plantations, and eight plots within continuous forest. Study
sites ranged from 1.5 to 16.2 ha. All fragments were remnants of mature forest that had been isolated for 50-90
years. The avifaunaat each study site was determined by
The study region encompassed an area of approximately
21,000 ha with elevations between 1750 and 2100 m,
and ran north-south on the west slope of the Cordillera
Central of the Colombian Andes (lat 04041'N, long
75?35'W) in the municipalities of Circasia, Salento, Filandia (Quindio Department), Pereira, and Santa Rosa de
Cabal (Risaralda Department) (Fig. 1). The area has a
mild climate with an average annual rainfallof 2515 mm,
170 C yearly mean temperature, and daily variation exceeding monthly variation in temperature; frost is absent
(Corporacio6nAutonoma Regional del Quindio and Instituto Nacional de Estudios Ambientales, unpublished
data). The rainfall pattern is bimodal, with drier periods
toward the beginning and middle of the year (Witte
1995), and the area is classified as subandean forest
(sensu Cuatrecasas 1958).
Forest fragments in the study region exist in humanmodified landscapes dominated by pastures and, to a
b)
a)
inFigure
2100m
1700m
----------- ...............
*
CaribbeanSea
tion of the study region in the Cordillera Central. Shaded areas
within the study region (b) indi-
sAo
4zw
PacT1ic
Ocean
l
_
t!
7
o
t
COLOMBIA
\
t/
F_| 'a
**
?_*
** {<t_,
7roads
\
n
* * .
iii
*a/ento
J/
~
ircasi
2km
Crai2
1999
cate largeforest tracts; towns are
shown in black. Light black lines
indicate contour lines (1700 m,
_~
~**9
<
Conservation Biology
Volume 13, No. 5, October
_
,9
*J_
_/lt>\
\
1. Location of the study region (a) and study sites within the
region (b). Shaded areas within the
map of Colombia (a) indicate
mountains above 1000 m, and a
circle with a star shows the loca-
SaIento\
W
2100 m); heavy black lines mark
connecting towns. Fragments
within pastures are represented by
asterisks, fragments within exotictreeplantations are represented by
stars, andplots within continuous
forest are represented by circles
with a star.
Long-Term Effects ofForest Fragmentation
Renjifo
point counts (Blondel et al. 1981) and systematic followup sampling. Each count lasted 15 minutes, and all individuals seen or heard were recorded. Counts were followed by a 1-hourperiod of systematic sampling covering
the interior of the fragment or plot to record species not
detected during point counts. I visited each site every 4-6
weeks, for a total of 10 visits. A visit consisted of two or
three point counts plus an hour of follow-up sampling;
the number of counts varied with fragment size. Counts
were done between 0620 and 1030 hours except on
mornings with strong winds or rain. Identification of bird
calls was assisted by recordings obtained with a tape recorder equipped with a semidirectional microphone and
by comparison with a reference collection. When I was in
doubt, determinations were verified or made by specialists (F. G. Stiles, Universidad Nacional de Colombia; M.
Isler and P. Isler, SmithsonianInstitution;T. Schulenberg,
Field Museum of NaturalHistory);unidentified bird voices
accounted for <0.5% of the records. In addition, I recorded species I observed throughout the study region,
especially in the landscape matrices, between August
1995 and May 1997. A complementary study of the avifauna associated with pastures and exotic-tree plantations
was done by Calvachi(1999).
Species Classificationand Analysis
Species were categorized into subgroups for data analysis according to their diets, migratory strategy, rarity, elevational center of abundance, body weight, and habitat
association by means of data from literature accounts
(Hilty & Brown 1986; Isler & Isler 1987; Stiles & Skutch
1989; Karr et al. 1990; Arango 1993; Stotz et al. 1996;
Restrepo & G6mez 1998; Stattersfield et al. 1998) and
field observations. Raritywas evaluated at three different
scales: geographic range size, local relative abundance,
and relative abundance in the Neotropics. Geographic
range was classified as small (?50,000 km2) or large
(>50,000 kM2) (Stattersfield et al. 1998). Local relative
abundance was based on number of records during 180
point counts within the eight continuous forest plots:
rare, 0-2; uncommon, 2-10; moderately common, 1130; common, >30. For comparative purposes, relative
abundance of migrants was based on point counts conducted during the months when they were present in
the region. Relative abundance in the Neotropics was
based on data of Stotz et al. (1996). Elevational center of
abundance followed data of Stotz et al. (1996): lowland,
0-900 m; foothill, 900-1600 m; subandean, 1600-2600
m; high Andean, above 2600 m. Center of abundance
was adjusted to match the actual distribution of the species in the Cordillera Central, which in some cases differs from that elsewhere in the Neotropics (Hilty &
Brown 1986). For instance, Russet-backed Oropendolas
(Psarocolius angustifrons) and Scarlet-rumpedCaciques
(Cacicus uropygialis) are montane species in the An-
1127
dean region of Colombia, although the former is common in the Amazonian lowlands and the latter is common in Choc6 and the Central American lowlands (Hilty
& Brown 1986).
Species were assigned to four size classes based on
body weights: 1, ?25 g; 2, 25-50 g; 3, 50-100 g; 4,
> 100 g. Species associated with forest, forest edges, and
open areas were treated separately. Forest species reported by the AMNHwere regarded as part of the original avifauna. Forest species recorded during this study
were also assumed part of the original avifauna unless
they were clearly outside of their usual distribution. Species recorded once or twice during field work and outside of their normal distribution were classified as vagrants and excluded from analysis. The region's birds
were classified as extant if they were present in both
continuous forest and fragments, regionally extinct if
they were present at the beginning of the century and
currently absent from both fragmented landscapes and
continuous forest, and extinct in the modified landscapes if absent in forest fragments but present in continuous forest; thus, the latter category includes the second category. The modified landscapes are called
Salento-Filandia.Forest species recorded three or fewer
times in only one fragment were considered greatly reduced and were coded as absent from fragmented landscapes. Association of extinction with different ecological traits were analyzed with G tests, Mann-Whitney U
tests, and Fisher exact tests, contingent upon the nature
of the data. When expected frequencies were needed,
random extinctions were assumed and categories were
pooled or removed to fit the assumptions of the test
used (Sokal & Rohlf 1995). Small numbers per category
prevented meaningful statistical analysis in some instances. Where this was the case, trends are discussed
rather than tested. Results and discussion focus on forest
species unless otherwise stated.
Results
Even by 1911, substantial deforested areas existed along
the trail from Filandia to Salento, around both towns,
and in the valley along the Quindio River close to
Salento. Nevertheless, open areas likely covered <20%
of the study region in 1911; continuous forest covers
<20% of the region today. Landscape photographs suggest that some fragments included in this study were already isolated from continuous forest in 1911.
AvifaunaComposition
A total of 249 bird species has been reported within the
study region: 132 species during the AMNH expedition,
109 additional species found during my study, and eight
species recorded in 1989 by Naranjo (1994) and in 1997
Conservation Biology
Volume 13, No. 5, October 1999
1128
Lonag-Term
Effectsof ForestFragmentation
Renjifo
Table 1. Speciespresent at the beginningof the centuryand currentlyabsentfrom the studyregion accordingto their center of abundance,
trophicgroup, relativeabundance,size class, and geographicrange.
Common name
Forest species
Barred Forest-Falcon
Yellow-eared Parrot
Rufous-breasted Antthrush
Russet-backed Oropendola
Scarlet-rumped Cacique
Red-bellied Grackle
Vagrants
Red-bellied Macaw
Bar-bellied Woodpecker
Tyrannine Woodcreeper
Plain Xenops
Black-capped Tyrannulet
Slaty-backed Chat-Tyrant
Long-billed Gnatwren
Center of
abundancea
Scientific name
Trophic
groupb
Relative
abundancec
Size
classd
Micrastur ruficollise
Ognorbyncb.us icteroitsf
Formicarius rttfipectuse
Psarocolius angustifronse
Cacicus uropygialise
Hypopyrrbus pyrobypogasterf
L
HA
SU
SU
SU
SU
R/D
FR
I
FR-I
FR-I
FR-I
M
R
U
C
C
R
4
4
3
4
3
3
Ara severaeg
Veniliornis nigricepse,b
Dendrocincla tyranninae
Xenops minzuttst'g
Pbyllonij4as nigrocapillusf?
Ocbtboeca cinnarnomeiventrisebi,
Rampbocaenus
melanuruseg
L
HA
HA
L
HA
HA
L
FR
I
I
I
I
I
I
M
M
U
M
U
M
M
4
2
3
1
1
1
1
aCent.erof abundance: L, lowland; SU, subandean; HA, high Andean.
bTJ)ophic group: R/D, raptor diurnal; I, insectivore; FR,frugivore; FR-I,frugivore-insectivore.
cRelative abundance in the Neotropics: C, commton;M, moderately commnon;U, uncomnmon;R, rare.
dSee textfor size classes.
eLarge range, >50 000 kmn.
fSmstallrange, ?50 000 km12.
'Iowland species usually found well belouwthe study area.
"High Andeaan species usually found
'Associated with streams.
well above the study) area.
by Calvachi (1999). Of the 249 species, the original forest avifauna of the region was estimated at 139 species
(Table 1; Appendix), with an additional 34 edge species,
35 nonforest species, and 41 species that were vagrants,
nocturnal, or associated with aquatic habitats.The AMNH
recorded by 7 species that seemed to be outside their
usual elevational range (Table 1). The status of these
species prior to fragmentation is not known, however,
so I conservatively regarded them as vagrants rather
than as extinct.
Before assessing the relationship between traits and extinction, I tested the independence of some of these
traits. Body size and membership in trophic groups were
associated. Although insectivores, frugivores, and frugivore-insectivores overlapped broadly in body size, the
relative distributions among size classes differed significantly (G = 42.04, p << 0.001); to match the test's assumptions I excluded other trophic groups (Fig. 2). Insectivores had more small-bodiedspecies and no species that
reached 300 g, whereas frugivores had more large-bodied
species, with 9 or 27 frugivores exceeding 300 g. Frugivore-insectivores were intermediate in body size. Not included in this analysiswere 12 species of nectarivores (all
< 10 g), one vulture, and three forest raptors (all > 100 g).
Trophic group and phylogenetic background were tightly
correlated. For instance, nectarivores were Trochilidae;
raptorswere Falconifornies;all Furnaridae,Formicariidae,
Parulinae, and most Tyrannidae were insectivores; and
nearly all Thraupidae were frugivore-insectivores (Ap-
Conservation
Biology
Volume 13, No. 5, October 1999
pendix). Therefore, it was not possible to isolate the relative importance of trophic group from evolutionary history in determining vulnerabilityto fragmentation.
RegionalExtinctions
A relatively intact condition of the fauna within continuous forest in the region is indicated by the current pres-
70
EZ|1Insectivores
Fru-insectiv.
Frugivores
60 50 -
<
a,)
U)
4..
0
30-
~20-
10
< 25 g
25-50 g
50-100Og
>lOO0g
Size Classes
Figure 2. Size-class distribution for the 63 insectivores,
33 frugivore-insectivores, and 2 7frugivores found in
the study region.
Long-Term
Effectsof ForestFragmentation
Renjifo
ence of top predators, such as Black-and-chestnutEagles
(Oroaetus isidori) and Collared Forest-Falcons (Micras-
tur semitorquatus), and by large and scarce avian frugivores, such as Cauca Guans (Penelope perspicax) and
the Andean Cock-of-the-Rock (Rupicola peruviana).
This is corroborated by the presence of large mammals
such as pumas (Puma concolor), spectacled bears,
(Tremarctos
ornatus),
and mountain
tapirs (Tapirus
pinchaque) in continuous forest (L.M.R., unpublished
data). Nevertheless,
six bird species (4.3% of the original
forest avifauna) were regionally extinct (Table 1). Regionally extinct species were on average larger than extant species (U test, p = 0.006; 6 extinct, 133 extant).
None of the regionally extinct species weighed <50 g,
whereas 67%of all forests species weigh < 50 g. Nevertheless, the largest species were still present in the region, including raptors and cracids. There were no regional extinctions among nectarivores, vultures, or NeotropicalNearctic migrants.
Species outside their elevational centers of abundance
yet within their usual distribution were not more likely
to be regionally extinct than were species close to their
centers of abundance (exact test, p = 0.59). For this
analysis, I combined subandean (92 extant, 4 extinct)
and foothill (18 extant, 0 extinct) for the category "close
of center of abundance," and lowland (13 extant, 1 extinct) and high Andean (10 extant, 1 extinct) for the category "farfrom center of abundance."
1129
their capacity to survive in fragmented landscapes and
were not included in the analysis: two hummningbirds
(Schistes geoffroyi and Colibri delpbinae) were recorded once each in continuous forest and in forest fragments, and the Turquoise Dacnis-Tanager (Pseudodacnis hartlaubi) was recorded once in a forest fragment.
Of the 41 species missing from fragments, two were
Neotropical-Nearctic migrants: Cerulean Warblers (Dendroica cerulea) and Golden-winged Warblers (Vermivora chrysoptera).
In contrast with regional extinctions, body size was
not significantly associated with extinctions in fragmented forest when examined for all trophic groups
combined
(G = 2.02, df = 3, p = 0.56) or when ana-
lyzed within insectivores and frugivore-insectivores (U
tests, p > 0. 5). Only among frugivores was there a trend
90 -
a)
80
70u) 60 .a:) 50
soa)
U/) 40030
x 20 -35
Extinctionsin FragmentedLandscapes
au 63
Forty-one forest species were extinct in fragmented
landscapes (i.e., Salento-Filandia),which represent 30%
of the original forest avifauna (Appendix). Three other
species were too rare to allow any conclusion about
R
U
MC
C
10
90
b)
80-
Table2. Incidenceof extinctions
pertrophicgroupandguildof
forestsin Salento-Filandia.
forestspeciesin fragmented
'1'
~70-
64
30
33
64
33
Mc
C
ui) 60-
Trophic group
and gutild
All species*
Diurnal raptors
Vultures
Nectarivores (hummingbirds)
Insectivores
Aerial
Canopy - foliage
Understory - foliage
Bark
Terrestrial
Frugivores
Large
Small
Frugivore-insectivores
Extinction
(%/,)
Extant
Extinct
95
0
1
9
43
3
41
3
0
1
0
29.9
100.0
0.0
10.0
31.7
0.0
13
16
8
8
38.1
4
5
4
7
7
0
10
20.0
38.5
57.1
25.9
35.0
0.0
31.3
3
20
13
7
22
20
*Three species were too rare to allow evaluation of their capacity to
survive infragmentedforest and wverenot included in these nunmbers.
bar)
o50-
U) 40030-
-35
x 20
LU
10
0
1
R
U
Figure 3. Incidence of extinction within relative abuindance categories.-local relative abundance (a) and relative abundance in the Neotropics (b). R, rare; U, uncommon; MC, moder-ately common; C, commnon.Total
nuimber of species in each category is inzdicatedinside
bars.
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1999
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Long-Term
EffectsofForestEragmentation
Renjifo
for large species to be more vulnerable, with no extinctions among small species (i.e., <50 g; Table 2). Body
size was not associated with extinction when analyzed
within six families with eight or more species (i.e., hummingbirds, woodcreepers, antbirds,flycatchers, warblers,
tanagers; U tests, p > 0.1).
Overall, the original forest avifauna was composed of
118 genera. Seventeen genera had two or more forest species. All species of Micrastur,Phyllomyias, and Diglossopis
went extinct in fragments.All species of Pionus, Phaethornis, Colibri, Aulacorhynchus, Phylloscartes, Turdus, Piranga, and Basileuterus were present in fragments. Six
genera had at least one species extinct and one extant in
forest fragments (i.e., Grallaria, Pachyrhamphus, Chlorospingus, Columba, Tangara, and Dendroica) (Appendix). A paired-samplet test comparing mean weight of extant species versus mean weight of extinct species within
a genus showed no association between body size and extinction (t = 0.378, df = 5, p > 0.5). Thus, body size per
se was not a good predictor of extinction.
Different scales of rarity were moderate to good predictors of extinction. Species with small geographic
ranges had a greater proportion of extinct species in
fragments (43%) than species with large geographic
ranges (29%). Local relative abundance and extinction
were strongly associated such that rare and uncommon
species were more likely to be extinct than common or
fairly common species (G = 12.34, df = 3,p < 0.01; Fig.
3). Relative abundance in the Neotropics and extinction
were also strongly associated (G = 10.41, df = 2, p <
0.01 for rare and uncommon species combined). In contrast, species extinction was independent of position relative to elevational center of abundance (G = 4.84, df =
4, p > 0.15). Therefore, species out of their center of
abundance but within the usual range were not more
prone to extinction than species at or close to their elevational centers of abundance (Appendix).
Table 3.
Extinction was unequally distributed among trophic
groups (Table 2). Only 1 in 10 hummingbird species but
all three forest raptors were absent from fragments. Insectivores, frugivores, and frugivore-insectivores were
evenly susceptible (G = 0.43, df = 2,p > 0.80). The majority of terrestrial insectivores were extinct in fragmented landscapes, whereas the majority of understory
foliage insectivores were present in fragments.
There were five families with 10 or more species
(hummingbirds, antbirds, flycatchers, tanagers, warblers), of which only antbirds were more extinction
prone in fragments than the rest of the avifauna (exact
test, p = 0.04). Icterids were highly vulnerable, with all
three forest species not only extinct in forest fragments
but in the entire region; a fourth species associated with
forest edge was regionally extinct as well. Cotingas were
highly susceptible to forest fragmentation, with two of
three species extinct in fragments and a third species
found in only a few fragments (Appendix).
Thirteen species from the original avifauna are of particular conservation concern because they are globally
threatened or near-threatened (Baillie & Groombridge
1996; Stattersfield et al. 1998): 11 are associated with
forest, 1 with forest edge, and 1 with forest rivers (Table
3). These species had little resilience to fragmentation; 8
were extinct in fragmented landscapes and 2 were regionally extinct.
NonforestSpecies
Before settlement, natural disturbances such as floods
and landslides likely maintained some semi-open habitats and associated avifauna within the region. In fact,
some open-habitat species such as Black-winged Saltators (Saltator atripennis) and Black-and-white Seedeaters (Sporophila luctuosa) are subandean elements. Natural occurrence of grasslands, however, was unlikely.
Species of global conservation concern (Baillie & Groombridge 1996; Stattersfield et al. 1998).
Common name
Fasciated Tiger-Heron
Black-and-chestnut Eagle
Cauca Guan
Wattled Guan
Chestnut Wood-Quail
Golden-plumed Parakeet
Yellow-eared Parrot
Black-billed Mountain-Toucan
Moustached Antpitta
Yellow-headed Manakin
Multicolored Tanager
Turquoise Dacnis-Tanager
Red-bellied Grackle
Scientific name
Tigrisomafasciatum
Oroaetus isidori
Penelopeperspicax
Aburria aburri
Odontophorus hyperythrus
Leptosittaca branickii
Ognorhynchus icterotis
Andigena nigrirostris
Grallaria alleni
Chloropipoflavicappilla
Chlorochrysa nitidissima
Pseudodacnis hartlaubi
Hypopyrrhus pyrobypogaster
Global statusa
NT
NT
EN,
NT
NT,
VU
CR
NT
EN,
NT,
VU,
VU,
EN,
SR
SR
SR
SR
SR
SR
SR
aCR,critically endangered; EN, endangered; VU, vulnerable; NT, near threatened; SR, small geographic range.
bEF,extinct in fragmented landscapes; PF,present in fragments; RE, regionally extinct.
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Volume 13, No. 5, October 1999
Regional statusb
RE
EF
PF
EF
PF
EF
RE
EF
EF
PF
PF
PF
RE
Table4.
1131
Long-Term Effects of ForestEragmentation
Renjifo
Speciesassociatedwith edges and pasturesrecordedwithinthe studyregion.
Presence in
191la
Lowland
Presence in
colonizationb
Edge Species
19 lja
Lowland
colonizationb
Pasture Species
Accipiter striatus
Buteo magnirostris
Buteo platypterus
Columba cayennensis
Leptotila verreauxi
Nyctidromus albicollis
Colibri coruscans
Colibri thalassinus
Amazilia franciae
Acestrura mulsant
Picumnus granadensis
Melanerpesformicivorus
Synallaxis albescens
Synallaxis azarae
Elaeniafrantzii
Poecilotriccus ruficeps
Todirostrum cinereum
Catharus aurantiirostris
Atlapetes gutturalis
Pheucticus ludovicianus
Saltator atripennis
Pirangaflava
Ramphocelus flammigerus
Thraupis episcopus
Thraupispalmarum
Euphonia musica
Tangara gyrola
Chlorophanes spiza
Pseudodacnis hartlaubi
Diglossa albilatera
Diglossa sittoides
Dendroica castanea
Icterus chrysater
Amblycercus holosericeus
Carduelis xanthogastra
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Bubulcus ibis
Coragyps atratus
Polyborusplancus
Falco sparverius
Vanellus chilensis
Zenaida auriculata
Columbina talpacoti
Crotophaga ani
Chlorostilbon melanorhynchus
Amazilia tzacatl
Elaeniaflavogaster
Myiophobusfasciatus
Pyrocephalus rubinus
Pitangus sulphuratus
Myiozetetes cayanensis
Tyrannus m.elancholicus
Notiochelidon cyanoleuca
Stelgidopteryx ruficollis
Troglodytes aedon
Mimus gilvus
Turdus ignobilis
Zonotrichia capensis
Sicalis citrinac
Emberizoides berbicola
Volatiniajacarina
Sporophila luctuosd
Sporophila nigricollis
Sporophila minuta
Tiaris olivacea
Tangara vitriolina
Tangara cyanicollis
Tangara beinei
Molothrus bonariensis
Scaphidura oryzivora
Carduelispsaltria
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Nonforest vagrants
Phimosus infuscatus
Elanus leucurus
Buteo swainsoni
Leptotila plumbeicepsd
Forpus conspicillatus
Tapera naevia
Amazilia saucerotteid
Tyrannus savana
Hirundo rustica
Hemispingus melanotis
Tachyphonus
+
rufusd
Coereba flaveola
Vireo flavifrons
Leistes militaris
aSpecies recorded in 1911 are marked; species not marked were recorded only during this study.
bSpecies that colonized from the lowlands; these species were not recorded in the subandean regions of Colombia at the beginning of the century or were noted at that time to be expanding into subandean regions following deforestation, often following trails (Chapman 1917).
cRecorded by Calvachi (1999).
dRecorded by Naranjo (1994).
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Long-Term
Effectsof ForestFragmentation
The extent to which the region's nonforest avifauna has
changed with deforestation is less documented than for
the forest avifauna. There were already substantial clearings by 1911. Allen and Miller recorded 16 of the region's 31 edge species and 13 of the region's 36 species
associated with pastures, including species such as the
Southern Lapwing (Vanellus chilensis), which inhabits
short pastures (Chapman 1917). Allen and Miller recognized that the avifauna of open areas was similar then to
the open habitants in the Cauca Valley (lowlands) but
with many species missing. Their failure to report colnspicuous species such as the Great Kiskadee (Pitangus
sulphuratus) and the Gray-capped Flycatcher (Myfozetetes cayennensis) indicates that some species had not
yet colonized the region following deforestation. This is
likely given the expedition's purpose to record all species, including common and widespread ones (Chapman 1917). There was a marked asymmetry in the direction of colonization of deforested areas. Following
deforestation, at least 23 species moved up into the region from the Cauca Valley lowlands following deforestation (Table 4). No species, however, or at most the Rufous-collared Sparrow (Zonotrichia capensis), moved
from the extensive open habitats above timberline (i.e.,
paramo) down into the study region. This asymmetric
colonization of deforested montane areas seems widespread in Colombia (L.M.R.,personal observation).
In addition to the six regionally extinct forest species,
there were six other species associated with habitats
other than forest interior which were collected in 1911
and not found during this study. Three species are associated with streams or marshy vegetation: Fasciated TigerHeron (Tigrisoma fasciatum), Northern Waterthrush
(Seiurus noveboracensis), and Subtropical Doradito
(Pseudocolopteryx acutipennis). The habitatsof these species were not systematicallysampled duringmy study, so it
is possible that a more detailed search might prove that
they are not extinct. The other three missing species
were found elsewhere at forest edges or pastures: Grayish Piculet (Picumnus granadensis), Bran-colored Flycatcher (Myiophobus fasciatus), and Yellow-billed Cacique (Amblycercus holosericeus); their absence likely
means they are extinct in the region.
Discussion
Many patterns of species extinction found in other regions were revealed my study. For instance, forest interior raptors, terrestrialinsectivores, large frugivores, antbirds, and cotingas were extinction prone. Similarly,
species with small geographic ranges and species that
are locally scarce or rare throughout their range also
were extinction-prone (Leck 1979; Willis 1979; Terborgh & Winter 1980; Kattan 1992). Hummingbirds
were resilient (Stouffer & Bierregaard 1995b), as were
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Volume 13, No. 5, October
1999
Renijifo
migrants. Both migrants absent in fragments have also
experienced long-term declines on their breeding
grounds (Sauer & Droege 1992).
More intriguing are those patterns not reported previously or not duplicated by this study: extinction in fragmented forest was independent of body size, species out
of their center of abundance were not more likely to go
extinct, forest icterids were highly extinction prone,
and understory insectivores were moderately resilient.
Body size per se was not a major determinant of vulnerability. Large species were not found to be more likely to
go extinct when the entire avifauna was analyzed or genus, family, or trophic group were controlled for.
Trophic group, pylogenetic background, and raritywere
more important determinants of vulnerability. Other
studies have found an association between evolutionary
history and rarity (Kattan 1992; Goerck 1997). Although
the six regionally extinct forest species were on average
larger than extant species, their demise seems related to
factors other than size: three were icterids, one was an
antbird (also terrestrial insectivore), one was a parrot in
critical danger of global extinction, and one was a small
raptor, a forest-falcon (Table 1). Regional extinctions
were likely to be driven by a reduction in the overall forest cover of the region, especially because forest cover
was even less extensive during the 1950s and 1960s
than it is presently (L.M.R.,unpublished data).
The lack of extinction of species out of their center of
abundance but within their usual distribution suggests
that they were located in "source" habitat (Pulliam
1988). Therefore, if deforestation cut them off from
other regions, they were nonetheless able to maintain local populations. Species at the very edge of their geographic range, however, are more likely to be located in
"sink"habitat, and deforestation may prevent recolonization. The current absence of some "vagrant"species
found in 1911 may result from loss of such sources at
lower elevations or from a decrease at higher elevations.
Continuous tracts of forest covering a broad elevational
range can be important even for species that do not migrate elevationally on a regular basis (Winker et al.
1997). These species, perceived as vagrants, might have
been more regular before deforestation because of
greater connectedness in the landscape.
Only the Yellow-backed Oriole (Icterus chrysater) remains of the icterids recorded in 1911 (although it was
found in only 2 of 24 study sites). Russet-backed Oropendolas (Psarocolius angustifrons), Red-bellied Grackles (Hypopyrrbus pyrobypogaster), and Yellow-billed
Caciques (Amblycercus bolosericeus) were common,
whereas Scarlet-rumpedCaciques (Cacicus uropygialis)
were uncommon. P. angustifrons was reported as one
of the most characteristic subandean species on the
western slope of the Central Andes (Chapman 1917). H.
pyrobypogaster was recorded in Ucumari Regional Park
as late as 1989 (Naranjo 1994), and a small flock of P.
Renjifo
angustifrons was seen there in November 1990 (L.M.R.,
personal observation). Although forest icterids were not
previously regarded as a group vulnerable to fragmentation, they seem to be more susceptible to long-term fragmentation than previously acknowledged. This may be
difficult to understand because they become more abundant at moderate levels of deforestation (S. Robinson,
personal communication). It is unlikely a coincidence
that P. angustifrons and P. decumanus have gone extinct in other Andean and inter-Andean regions following deforestation (Alvarez-L6pezet al. 1991; Kattan et al.
1994). H. pyrohypogaster has suffered a drastic geographic range contraction and is now a threatened species (Collar et al. 1992). Also, Willis (1979) reported the
loss of one Cacicus in large fragments in eastern Brazil.
A closer look at historical records elsewhere might provide further insights into this pattern. The social habits
and colonial nesting of some Icterids may make them
more vulnerable to extinction over the long term. Small
nesting colonies often fail to produce fledglings because
they are less capable of defending their nests from predators (Robinson 1985). Small forests likely harbor few
flocks and small colonies; consequently, successive nesting failure may lead them to extinction.
The best-documented long-term process of avian extinction in the Neotropics occurred on Barro Colorado
Island (BCI;Willis 1974; Karr 1982, 1990). The most important driving forces of extinction for forest species on
BCI were loss of wet microhabitats that could act as refuges during seasonal and aseasonal droughts (Karr 1982),
low adult survival rates, high population variability(Karr
1990), and increased nest predation due to increased
mesopredator populations (Terborgh & Winter 1980;
Loiselle & Hoppes 1983; Sieving 1992). In general, local
populations may fail to maintain themselves because of
increased nest predation or parasitism (Robinson et al.
1995).
Despite long-term forest fragmentation, there were 96
forest species in the fragments of Salento-Filandia.On
average, 71 species were recorded in each fragment.
Terborgh et al. (1997) recorded a mean of 21.5 species
in forested islands of the same size in the Guri Lake in
Venezuela after 7 years of isolation. Long-term extinctions have been documented in only one other subandean locality, namely San Antonio on the Cordillera Occidental of Colombia (Kattan et al. 1994). The original
avifaunas of San Antonio and Salento-Filandiawere similar, as was the proportion of extinction, 31% and 30%,
respectively. Understory insectivores were highly vulnerable in San Antonio, however, but were relatively resilient in Salento-Filandia.Also, 66.6% of large frugivores
went extinct in San Antonio, whereas only 33.3% went
extinct in my study.
Several interacting factors may account for the differences found between Salento-Filandiaand other regions,
including the availability of wet microhabitats, seasonal-
Long-Term
Effectsof ForestFragmentation
1133
ity, etective isolation, nesting success, anc numaninduced predation. Guri Lake'sislands and BCIwere created by impoundments. These islands are mountaintops
with little or no wet microhabitats, which may serve as
refuges during dry periods (Karr 1990; Terborgh et al.
1997). BCI and Guri also have a seasonal semideciduous
forest (Leigh et al., 1990; Terborgh et al. 1997). In contrast, 15 or 16 fragments studied in Salento-Filandiahad
permanent streams providing humid microhabitats. This
region has mild seasonality. As a result, drought-driven
extinctions are likely less frequent in Salento-Filandia.
Isolation by anthropogenic land uses may represent less
of a barrier than does water. Some weak fliers, such as
toucanets and guans, cross pastures by using isolated
tress as stepping stones, and the latter by walking
(L.M.R., personal observation). Small open areas, however, represent a barrier to dispersal for some understory and terrestrialbird species (Bierregaardet al. 1992;
Sieving et al. 1996).
Few comparative studies document adult survivalrates
of tropical and temperate birds. Among New World populations of Turdus, however, there is a strong negative correlation between survival rates and seasonality (as measured by temperature) and a weaker positive correlation
between survivalrates and precipitation; survivalrates increase from the lowlands to montane regions within the
tropics (Ricklefs 1997). If these patterns hold for other
avian taxa, relatively h-igh annual survival rates and thus
low extinction rates might be expected in Salento-Filandia, because it is a wet and mildly seasonal tropical montane region. Brood parasitism was not evaluated, yet it
seems unlikely to be prevalent because few brood parasites were encountered. Shliny Cowbirds (Molothrus
bonariensis) were recorded in small numbers in the region and never within study sites. The Giant Cowbird
(Scaphidura oryzivora), a selective brood parasite of corvids and icterids (Alvarez-L6pez 1975; Stiles & Skutch
1989), was encountered only four times.
Predation by humans, dogs, and cats is likely the cause
of higher extinction rates of large frugivores and understory insectivores in San Antonio than in Salento-Filandia.
Hunting is known to strongly affect large frugivores (Silva
& Strahl 1991; Redford 1992). Fragmentsin Salento-Filandia were in landscapes with a low density of houses; hunting was infrequent. Fragments in San Antonio were surrounded by a rural and suburban matrix with a h-igher
density of houses (Arango-V61ez& Kattan 1997) and were
more likely to be affected by people and domestic animals. Kattanet al. (1994) attribute five extinctions in San
Antonio to hunting, pet trade, and dog predation. ArangoVelez and Kattan (1997) documented artificial nest destruction by dogs in the area. Although cat predation was
not reported, it is likely to be frequent in SanAntonio and
to affect mainly small understory species.
A large tract of forest and some large forest fragments
in the region may serve as sources for recolonization.
Conservation Biology
Volume 13, No. 5, October 1999
1134
Long-Term
Effectsof ForestFragmentation
More intensive land use in the region would likely precipitate further avain extinctions. It is not known whether
these fragments act as population sources or sinks, but
the fact that some fragments still have terrestrial birds
highly reluctant to cross open areas (e.g., Scytalopus)
suggests that at least some species might be able to
maintain isolated populations.
Conclusion
My results indicate a severe impact of fragmentation on
this subandean avifauna. Of the 139 forest species recorded historically in Salento-Filandia,30%were extinct
in fragments, including many species of global conservation concern. This figure would probably be greater in
the absence of large forest tracts in the region. The future for the majority of subandean avifauna is only assured if large tracts of native forest are conserved. This is
of concern considering the widespread forest fragmentation in the tropical Andes. For instance, Colombia has
lost 73%of its continuous montane forest (Cavalier & Etter 1995), whereas the Cordillera Central has probably
lost over 90%of its continuous subandean forests (Fig. 2
in Cavalier& Etter 1995). These figures are probably not
too different from what would be found for other Andean regions. On the positive side, these fragments, especially if they contain mature forest, can still support a
diverse avifauna after several decades of isolation, including small populations of globally endangered species. Large forest tracts of subandean forest should be
given top priority for conservation wherever they exist.
Nevertheless, fragments of mature forest could play an
important role in the restoration of local avifaunas. Small
forest fragments, however, are unlikely to maintain
many species indefinitely. A good understanding of the
mechanisms that allow persistence in such fragments
and active management of their populations may prove
essential for the conservation of a number of species for
which no large tracts of habitat remain.
Acknowledgments
I thank B. Loiselle for invaluable advice through all the
stages of this project. Discussions and comments by J.
Blake, D. Clark, S. Robinson, W. Connett, C. M. Fisher,
G. Graham,L. Griz,J. Goerck, I. Jimenez, E. Main,J. PerezEman, D. Saunders, G. Servat, and J. Tello contributed
greatly to this paper. My colleagues S. Arango and W.
Vargas collaborated in many valuable ways. F. G. Stiles,
M. Isler, P. Isler, and T. Schulenberg identified some bird
calls. I am thankful to R. Zapata, B. Calvachi, H. Zapata,
H. Zuluaga, and R. Gutierrez for field assistance and to P.
Sweet for help at the American Museum of Natural History. This study was made possible by funding and logis-
Conservation Biology
Volume 13, No. 5, October 1999
Renfifo
tic support from Fundaci6n Herencia Verde, especially
from J. C. Riascos, D. Uribe, J. Ospina, A. Solarte, L.
Galvez, and G. Torres. I received generous funding from
the MacArthurFoundation, the Wildlife Conservation Society, the National Science Foundation, the International
Center for Tropical Ecology (Parker-GentryFellowship
and Compton Fellowship), the American Museum of
Natural History (Frank Chapman Fund), and the Graduate School of the University of Missouri-St. Louis (Summer Research Fellowship, three summers). I thank
Carder, Corporaci6n Regional del Quindio, and Unidad
Especial de Parques Nacionales (Ministry of the Environment, Colombia) for research permits and collaboration.
These three institutions, Smurfit-Cart6nde Colombia,
Bosquinsa, and numerous private landowners allowed
me to work on their lands. Smurfit-Cart6nde Colombia
provided copies of their maps of the region.
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Conservation Biology
Volume 13, No. 5, October
1999
1136
Long-Term
Effectsof ForestFragmentation
Renjifo
Appendix
Forestbird species present in the studyregion, accordingto family,elevationalcenter of abundance,local relativeabundance,tropic group,and
local status.a
Family, common
name, genus, species
Cathartidae (American vultures)
Cathartes aura
Accipitridae (hawks, eagles)
Chondrobierax uncinatus
Ictinia plumbeaf
Oroaetus isidori
Falconidae (falcons)
Micrastur ruficollis
Micrastur semitorquatus
Cracidae (guans)
Penelope perspicaxg
Aburria aburri
Chamaepetes goudotii
Odontophoridae (wood-quail)
Odontophorus byperythrusg
Columbidae (pigeons)
Columbafasciata
Columba subvinacea
Geotrygonfrenata
Psittacidae (parrots)
Aratinga wagleri
Leptosittaca branickii
Ognorhynchus icterotis
Bolborhynchus lineola
Pionus tumultuosus
Pionus chalcopterus
Amazona mnercenaria
Cuculidae (cuckoos)
Coccyzus
americanush
Piaya cayana
Strigidae (owls)
Otus choliba
Glaucidiumjardiniif
Ciccaba virgata
Nyctibiidae (Potoos)
Nyctibius griseus
Apodidae (swifts)
Cypseloides rutilus
Streptoprocne zonaris
Chaetura cinereiventris
Trochilidae (hummingbirds)
Doryfera ludovicae
Phaethornis guy
Phaethornis syrmatophorus
Colibri delphinae
Adelomyia melanogenys
Heliodoxa rubinoides
Coeligena coeligena
Coeligena torquata
Boissonneauaflavescens
Haplophaedia aureliae
Ocreatus underwoodii
Aglaiocercus kingi
Schistes geoffroyi
Trogonidae (trogons)
Pharomachrus auriceps
Trogon collaris
Momotidae (Motmots)
Momnotus momota
Bucconidae (Puffbird)
Malacoptila mystacalis
Center of abundancd'
Trophic groupd
Local statuse
R
CA
PF
L
L
SU
R
SN
I
R/D
V
V
EF
L
L
U
R/D
R/D
RE
EF
SU
SU
HA
F
R
R
FR
FR
FR
PF
EF
PF
SU
M
FR-I
PF
HA
L
SU
U
U
U
FR
FR
FR
PF
EF
PF
SU
HA
HA
SU
HA
SU
SU
R
R
FR
FR
FR
FR
FR
FR
FR
PF
EF
RE
PF
PF
PF
PF
I
V
I
PF
L
HA
L
R/N
R/N
R/N
PF
V
PF
L
I
PF
L
Local relative abundancef
R
U
R
U
L
L
M
SU
SU
F
R
R
U
I
I
I
PF
PF
PF
SU
F
SU
SU
SU
SU
SU
HA
SU
SU
SU
SU
SU
R
R
R
R
M
R
U
R
R
M
R
R
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
NI
PF
PF
PF
EF
PF
PF
PF
V
PF
PF
PF
EF
EF
SU
L
M
C
FR
FR-I
PF
PF
SU
F
FR-I
PF
F
U
I
PF
continued
Conservation Biology
Volume 13, No. 5, October 1999
Long-Term Effects of Forest Fragmentation
Renjifo
1137
Appendix(continued)
Family, common
name, genus, species
Capitonidae (Barbet)
Eubucco bourcierii
Ramphastidae (Toucan)
Aulacorbynchusprasinus
Aulacorbynchus haematopygus
Andigena nigrirostris
Picidae (woodpeckers)
Veniliornisfumnigatus
Piculus rubiginosus
Campephilus nmelanoleucos
Dendrocolaptidae (woodcreepers)
Sittasomus griseicapillus
Glyphoryncbus spirurus
Xiphocolaptes
promneropirhynchus
Dendrocolaptespicumnus
Xiphorbynchus triangularis
Lepidocolaptes caffinis
Campylorhamphuspusillus
Furnariidae (ovenbirds)
Cranioleuca erythrops
Premnornis guttuligera
Premnoplex brunnescens
Syndactyla subalaris
Anabacerthia striaticollis
Thripadectes holostictus
Xenops rutilans
Formicariidae (antbirds)
Thamnophilus unicolor
Dysithamnus mentalis
Myrmotherula schisticolor
Herpsilochmus aff: axilaris
Dryrmophila caudata
Terenura callinota
Formicarious rufipectus
Chbamaeza mollissimna
Grallaria allenig
Grallaria ruficapilla
Rhinocryptidae (tapaculos)
Scytalopus aff. spillmanni
Tyrannidae (tyrant flycatchers)
Phyllomnyias uropygialis
Phyllomyiasplumbeiceps
Phyllomyias cinereiceps
Zimmerius viridiflavus
Mionectes striaticollis
Leptopogon rufipectus
Phylloscartes ophthalmicus
Phylloscartes poecilotis
Pseudotriccuspelzelni
Pseudotriccus ruficeps
Lophotriccus pileatus
Myiophobusflavicans
Pyrrhomyias cinnarnomea
Empidonax virescensh
Myiarchus cephalotes
AMyiodynastes chrysocephalus
Pachyrazphuspolychopterus
Pachyramphus versicolor
Center of abundance"
Local relative abundancef
Trophic groupd
Local statuse
F
U
FR-I
PF
SU
F
HA
M
U
R
FR
FR
FR
PF
PF
EF
SU
SU
L
R
C
U
I
I
I
PF
PF
PF
L
L
SU
R
R
M
I
I
I
EF
EF
PF
SU
SU
SU
F
U
U
C
R
I
I
I
I
PF
EF
PF
EF
F
SU
SU
SU
SU
SU
SU
M
R
C
C
C
U
U
I
I
I
I
I
I
I
PF
EF
PF
PF
PF
PF
PF
SU
F
F
F
SU
SU
SU
SU
SU
SU
U
M
U
M
M
U
M
M
C
I
I
I
I
I
I
I
I
I
I
EF
PF
PF
EF
PF
EF
RE
EF
EF
PF
SU
C
I
PF
SU
SU
SU
SU
SU
SU
SU
SU
SU
HA
F
SU
SU
SU
SU
SU
L
SU
R
R
U
C
U
C
C
C
M
R
U
U
C
C
M
C
M
U
I
I
I
FR
FR
I
I
I
I
I
I
I
I
I
I
FR-I
FR-I
FR-I
EF
EF
EF
PF
PF
PF
PF
PF
PF
EF
PF
EF
EF
PF
PF
PF
PF
EF
continuted
Conservation Biology
Volume 13, No. 5, October 1999
1138
Long-Term
Effectsof ForestFragmentation
Renjifo
Appendix(continued)
Family, common
name, genus, species
Pipridae (manakins)
Chloropipo flavicapillag
Masius chrysopterus
Cotingidae (cotingas)
Pipreola riefferii
Pyroderus scutatus
Rupicola peruviana
Troglodytidae (wrens)
Thryothorus genibarbis
Henicorbina leucophrys
Cyphorbinus thoracicus
Turdidae (thrushes)
Myadestes ralloides
Catharus ustulatusb
Platycichla leucops
Turdusfuscater
Turdus serranus
Emberizidae (emberizids)
Atlapetes schistaceusf
Buarrem.on brunneinuchus
Thraupidae (tanagers)
Sericossypha albocristata
Chlorospingus ophthalmicus
Chlorospingus canigularis
Hemispingusfrontalis
Creurgops verticalis
Habia cristatag
Piranga rubra A
Piranga leucoptera
Anisognathusflavinucha
Pipraeidea melanonota
Euphonia xanthogaster
Chlorophonia cyanea
Chlorochrysa nitidissimaf
Tangara arthus
Tangara xanthocephala
Tangara ruficervix
Tangara labradorides
Tangara nigroviridis
Tangara vassorii
Diglossopis caerulescens
Diglossopis cyanea
Parulidae (wood-warblers)
Mniotilta variah
Vermivora chrysopterah
Vermivora peregrina b
Parula pitiayumi
Dendroica fusca "
Dendroica cerulea"
Setophaga ruticilla
Wilsonia canadensish
Myioborus miniatus
Basileuterus coronatus
Basileuterus tristriatus
Vireonidae (vireos)
Cyclarbis nigrirostris
Vireo leucophrys
Hylophilus semibrunneus
Icteridae (blackbirds)
Psarocolius angustifrons
Cacicus uropygialis
Hypopyrrhus pyrobypogaster
Center of abundance"
Local relative abundancec
Trophic groupd
Local statuge
SU
SU
R
U
FR
FR
PF
PF
SU
SU
SU
M
M
R
FR
FR
FR
EF
PF
EF
SU
SU
SU
R
C
C
I
I
I
PF
PF
EF
SU
SU
SU
HA
SU
C
R
M
R
U
FR
FR-I
FR-I
FR-I
FR-I
PF
PF
PF
PF
PF
HA
SU
C
FR-I
FR-I
V
PF
FR-I
FR-I
FR-I
FR-I
I
I
FR-I
FR-I
FR-I
FR-I
FR
FR
FR-I
FR-I
FR-I
FR-I
FR-I
FR-I
FR-I
FR-I-N
FR-I-N
EF
EF
PF
PF
EF
V
PF
PF
PF
PF
PF
PF
PF
PF
EF
EF
PF
PF
PF
EF
EF
I
I
I
I
I
I
I
I
I
I
PF
EF
V
PF
PF
EF
PF
PF
PF
PF
PF
I
I
I
PF
PF
PF
FR-I
FR-I
FR-I
RE
RE
RE
HA
SU
SU
SU
SU
F
L
SU
SU
SU
L
F
F
SU
SU
SU
SU
SU
HA
HA
HA
F
F
L
F
U
R
C
M
R
U
M
M
U
C
U
U
M
R
R
M
R
M
R
U
M
R
SU
L
SU
SU
SU
F
C
C
U
R
C
C
C
C
SU
SU
F
C
C
M
SU
SU
SU
SU
I
continued
Conservation Biology
Volume 13, No. 5, October
1999
1139
Long-Term Effects of Forest Fragmentation
Renjifo
Appendix(continued)
Family, common
name, genus, species
Center of abundancSP
Corvidae (jays)
Cyanocoraxyncas
SU
Local relative abundance'
M
Trophic groupd
I
Local statuse
PF
aTaxonomy follows that of Stotz et al. (1996).
bElevational center of abundance: L, lowland (0-900 m ); F,foothill (900-1600 m); SU, subandean (1600-2600 m); HA, high Andean (above
2600( m).
'Local relative abundance: C, common; M, moderately common; U, uncommon; R, rare.
dTrophic group; CA, carrion; SN, snails; RID, raptor diurnal; R/N, raptor nocturnal; FR,frugivore; FR-I,frugivore-insectivore; FR-I-N,frugivoreinsectivore-nectarivore; I, insectivore; NI, nectarivore.
eLocal status: EF, extinct in fragments; PR, present in fragments; RE, regionally extinct; V, vagrant.
fRecorded by Naranjo (1994).
gSmall geographic range.
bNeotropical-Nearctic migrant.
I
Conservation Biology
Vololme 13, No. 5, October 1999

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