Avifaunal Collapse in West African Forest Fragments

Avifaunal Collapse in West African Forest Fragments
PAUL BEIER,* MARYANN VAN DRIELEN,† AND BRIGHT O. KANKAM‡
*School of Forestry, Northern Arizona University, Flagstaff, AZ 86011–5018, U.S.A., email [email protected]
†4010 Lugano Way, Flagstaff, AZ 86004–6834, U.S.A.
‡Forest Research Institute of Ghana, UST Box 63, Kumasi, Ghana
Abstract: Despite the fact that West African tropical forests are the most fragmented in Africa, there has been
no published research on biodiversity in these fragments. To determine how forest birds respond to five factors—patch size, patch isolation, canopy density, abundance of large trees, and proximity to forest edge—in
these forests, we surveyed 60 species of forest birds on 121 transects (2.5 ha each) in 35 forest fragments in
the semideciduous forest zone of Ghana. Species richness per transect increased with patch size over the entire range of patch sizes observed (3–33,000 ha). The diversity of forest birds (22 species) on a single transect
in a large forest patch was similar to the cumulative diversity (25 species) on all 17 transects in 13 small
patches. Twenty-two of 60 species were area sensitive, 15 of which were never found in small patches. These
results suggest that only large forests will conserve many species of West African forest birds. Nine species
were edge sensitive, 7 of which were also area sensitive. However, forest structure near patch edges was not
consistent with bird responses to canopy and tree density, suggesting that mechanisms other than microclimate or structural changes (perhaps predation or nest parasitism) underlie the response of most species that
are sensitive to both edge and area. Regression of critical patch size (the smallest patch size in which a species
was detected) on logarithm of body mass (an index of home range size) for 22 area-sensitive species suggests
that area-sensitive species are unlikely to occur in patches smaller than several home-range areas. Canopy
density influenced 13 species (11 positively, 2 negatively), and abundance of large trees influenced 8 species
(3 positively, 5 negatively). Forest birds did not respond to isolation (distance from a patch to a large forest)
for isolation distances of 1–25 km, suggesting that island biogeographic mechanisms had less influence on
birds than other potential mechanisms of area sensitivity. Although small patches contributed little to the conservation of forest birds—species found in small patches were well represented in large patches—small
patches are probably important for supporting generalist bird species that provide ecological services in the
agricultural matrix and serving as nuclei for future ecosystem recovery.
Colapso de la Avifauna en Fragmentos de Bosque en África Occidental
Resumen: A pesar de que los bosques tropicales de África Occidental son los más fragmentados en África, no
existe información publicada sobre la biodiversidad de esos fragmentos. Para determinar como responden
las aves de bosque a cinco factores (tamaño del fragmento, aislamiento del fragmento, densidad del dosel,
abundancia de árboles grandes y proximidad al borde bosque) en estos bosques, tomamos muestras de 60 especies a lo largo de 121 transectos (2.5 Ha cada uno) en 35 fragmentos de bosque en la zona de bosque
semidecíduo en Ghana. La riqueza de especies por transecto incrementó con el tamaño del fragmento en
todo el rango de tamaños de fragmento (3 a 30,000 Ha). La diversidad de aves de bosque (22 especies) a lo
largo de un solo transecto fue comparable a la diversidad acumulada (25 especies) en 17 transectos en 13
fragmentos pequeños. Veintidós de 60 especies fueron sensibles al tamaño del fragmento, de las cuales 15
nunca fueron encontradas en fragmentos pequeños. Estos resultados sugieren que muchas especies de aves
de bosque en África Occidental se conservarán sólo en fragmentos grandes. Nueve especies fueron sensibles al
borde del bosque, de las cuales 7 también fueron sensibles al tamaño del fragmento. Sin embargo, la estructura del bosque cerca del borde de los fragmentos no se correlacionó con las respuestas de las aves a los cinco
factores, lo que sugiere que en la respuesta de muchas especies sensibles tanto al borde como al área subyacen mecanismos distintos al microclima o cambios estructurales ( probablemente depredación o parasi-
Paper submitted January 3, 2001; revised manuscript accepted September 19, 2001.
1097
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Volume 16, No. 4, August 2002
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Birds in West African Forest Fragments
Beier et al.
tismo de nidos). La regresión del tamaño crítico del fragmento (el fragmento más pequeño en que se detectó
la especie) en el logaritmo de la masa corporal (un índice del rango de hogar) en 22 especies sensibles al área
sugiere que las especies sensibles al área probablemente no ocurran en fragmentos de menor tamaño que
varias áreas de rango de hogar. La densidad del dosel influyó a 13 especies (11 positivamente, 2 negativamente), y la abundancia de árboles grandes influyó a 8 especies (3 positivamente, 5 negativamente). Las
aves de bosque no respondieron al aislamiento (distancia del fragmento a un bosque extenso) en distancias
de 1 a 25 km, lo que sugiere que los mecanismos de biogeografía de islas tuvieron menos influencia en aves
que otros mecanismos potenciales de sensibilidad al área. Aunque los fragmentos pequeños contribuyeron
poco a la conservación de las aves de bosque (especies encontradas en fragmentos pequeños estuvieron bien
representadas en fragmentos grandes), los fragmentos pequeños probablemente son importantes para aves
generalistas que proporcionan servicios ecológicos en la matriz agrícola y funcionan como núcleos para la
futura recuperación de ecosistemas.
Introduction
Occupying 7% of the world’s land mass, tropical forests
harbor 50% of all plant and animal species (Myers 1992;
Bowles et al. 1998). As a group, birds are closely associated with forests, and approximately 30% of the world’s
species of birds are so restricted to tropical forests (either
for winter or year-round habitat) that they would disappear if all tropical forests were lost (Myers 1992). Excluding the effects of selective logging, these forests are being
lost at a rate of about 1.2% annually (Food and Agriculture
Organization 1993). Given the needs of expanding human populations and the agricultural economies of many
tropical countries, tropical forests will increasingly become fragments in agricultural landscapes. Until economies mature and some agricultural lands can revert to forest, these fragments will be refuges for tropical
biodiversity, and it is important to understand the dynamics of biodiversity in these fragments.
Bird response to tropical-forest fragmentation has been
studied in Central America, South America, and Asia, but
there have been only two studies (Newmark 1991;
Brooks et al. 1999) in Africa. Some studies have documented change in avifaunas during the process of fragmentation (Bierregaard & Stouffer 1997; Stratford &
Stouffer 1999) or by comparing current to pre-isolation inventories (Willis 1974; Leck 1979; Kattan et al. 1994; Renjifo 1999). Such studies have the advantage of documenting extinction events, but require prefragmentation data.
A more common approach (which we used) is to compare faunas in various fragments and large habitat areas
and to attribute the absence of species from fragments to
mechanisms related to fragmentation, as done by Bond
(1957 ), Galli et al. (1976), Martin (1980), Soulé et al.
(1988), Robbins et al. (1989), Newmark (1991), Robinson
et al. (1995), Warburton (1997), Crooks & Soulé (1999),
and van Balen (1999). Results from all these studies suggest that some species are absent or rare in small patches.
Robbins et al. (1989) called these area-sensitive species.
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Volume 16, No. 4, August 2002
Previous studies have also identified several causes of
area sensitivity. Although these causes are not mutually
exclusive, each mechanism carries certain expectations
about area sensitivity ( Table 1). We attempted to discern whether four of these mechanisms were operating
on forest birds in West Africa by looking for evidence for
their distinguishing expectations. We assessed the response of forest birds to canopy closure and density of
large trees to help investigate these mechanisms and to
evaluate how timber harvest, which reduces canopy and
numbers of large trees, influences these birds ( Johns
1997; Thiollay 1997).
One potential difficulty with the approach of comparing avifaunas in various fragments is that large patches
( like large quadrats) always contain more species than
small patches (Haila 1983; Hill et al. 1994; May & Stumpf
2000). We standardized our effort by using timed area
counts so that we could provide a clear answer to the
question of whether several small patches might conserve as many species as a single large patch of the same
total size.
Our goals were to quantify the degree of area sensitivity and edge sensitivity in forest birds of West Africa, to
make some preliminary inferences about which mechanisms underlie area sensitivity, and to identify the species most vulnerable to fragmentation. To achieve this,
we surveyed forest birds in 35 forest fragments in the
moist and dry semideciduous forest zones of Ghana.
Methods
Study Area
The most fragmented tropical forests occur in the Philippines, peninsular Malaysia, Ghana, and Costa Rica (Whitmore 1997 ), so these are appropriate locations for an
observational study of avian response to fragmentation
of tropical forests. We studied birds in the semideciduous forest zones within the upper Guinea forests of
Beier et al.
Table 1.
Birds in West African Forest Fragments
1099
Mechanisms responsible for area sensitivity in birds.
Mechanism*
(1) Island biogeography theory: extinction and
colonization in patches is a function of patch
size and distance from source populations
(2) Structural and microclimate changes near the
patch edge make the patch unsuitable for some
bird species
(3) Increased predation and nest parasitism near
patch edge, typically due to predators-parasites
characteristic of the matrix habitat
(4) Isolated patches are too small relative to the
home range size of area-sensitive species
(5) Mesopredator release: in patches too small to
harbor top predators, smaller predators that
specialize on birds will increase
(6) Displacement of forest specialists by
generalists and species associated with
disturbance
Condition or prediction unique to
this mechanism
(1) species richness is a function of
isolation
(2) rare species—those that exist at
naturally low densities—tend to be
area sensitive
(1) some area-sensitive species are
also edge sensitive
(2) increased dessication, wind
speeds, timber harvest,
blowdowns, and vine growth
create a more open forest at the
edge
(3) edge-sensitive species avoid this
altered structure
some area-sensitive species are also
edge-sensitive species, but edge
vegetation need not differ from
interior vegetation
(1) species with large home ranges
tend to be area sensitive
(2) minimum patch size for areasensitive species is scaled to home
range size; these species will be
absent from patches smaller than a
few home ranges
small patches lack large predators and
have increased abundance of small
predators that specialize on birds
small patches show increased
abundance of generalist species
that compete with area-sensitive
species
Citations
MacArthur & Wilson 1967; Newmark
1991
Karr 1982; Lovejoy et al. 1986;
Saunders et al. 1991; Laurance et
al. 1997; Burke & Nol 1998
Yahner & Scott 1988; Donovan et al.
1995; Robinson et al. 1995
Stratford & Stouffer 1999
Soulé et al. 1988; Sieving 1992;
Crooks & Soulé 1999
Ambuel & Temple 1983; Grey et al.
1998
*Mechanisms are not mutually exclusive. For the first four mechanisms, we looked for evidence that the conditions and predictions unique to
each mechanism operated on forest birds in West Africa.
Ghana. Bird Life International (Slattersfield et al. 1998)
ranked the upper Guinea forests of West Africa fifteenth
in its world priority list of 218 centers of bird endemism
based on biological importance and current level of
threat. Forests now cover 20% of their original extent
in Ghana (Hall & Swaine 1981). The closed forest is divided into 4 major zones. The wet evergreen type (annual rainfall 1500–2100 mm, about 8% of the total Ghanaian forest zone) and moist evergreen type (1500–1700
mm, 22%) are relatively intact. We chose to study fragments in the moist semideciduous (1200–1800 mm, 40%
of the forest zone) and dry semideciduous zones (1250–
1500 mm, 26%) because of their high-value timber trees,
high human population, ideal climate for raising cocoa,
and recurring fires that have fragmented a formerly unbroken forest into distinct patches within a nonforest
matrix. Our study area spanned a northwest-to-southeast
band from about lat. 728N, long. 235W, to about lat.
615N, long. 020W.
The moist semideciduous forests are characterized by
such tree species as utile ( Entandrophragma utile), African mahogany (Khaya ivorensis), and wawa ( Triplochiton sclerozylon ). Characteristic species of dry
semideciduous forests include Hymenostegia spp., ebony (Diospyros mespiliformis), and Anogeissus leiocarpus ( Hall & Swaine 1981). Two exotic species, namely
york ( Broussonetia papyrifera) and cedrela (Cedrela
odorata), rapidly invade disturbed sites and were numerically dominant in some forest patches, although
usually mixed with native canopy-emergent and understory species.
The forests were surrounded by several types of nonforest matrix. The dominant matrix land use was cropland, consisting of small farms and fallows, with scattered native (and some exotic) trees. Dominant crops
were plantain (Musa paradisiaca), cocoyam (Xanthosoma sagittifolium ), corn ( Zea mays ), tomatoes
(Solanum lycopersicum), garden eggs (Solanum mel-
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Volume 16, No. 4, August 2002
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Birds in West African Forest Fragments
ongena), and cassava (Manihot esculenta). Cocoa farms
usually retained the overstory of native tree species and
thus were most similar to the natural forest type. Fire savanna occurred in sites where the combined effects of
timber overharvest, invasion of fire-adapted pioneer species, and annual fires have replaced forests with a low
(1–3 m tall), dense vegetation dominated by elephant
grass (Pennisetum purpureum), Guinea grass (Panicum maximum), centro (Centrosema pubescens), Siam
weed (Chromolaena odorata), and other weedy species. Plantations of oil palm (Elaeis guineensis) or nonnative teak (Tectona grandis) were adjacent to a few of
the forest patches; these plantations were bereft of forest birds (P.B. & B.O.K., unpublished data).
Selection of Forest Patches
We selected 35 forest patches in forest reserves, national
parks, sacred groves (areas protected by local taboo or
as royal burial grounds), and field stations (Table 2). In
each such area, the extent of natural forest was less (often far less) than the gazetted size due to unsustainable
timber harvest, repeated fires, teak plantations, and agricultural encroachment. Four forest areas each contained
two patches where fire, farming, or teak monocultures
created a discontinuity 500 m wide. We selected forest
patches in each of three size classes: 3–11, 20–700, and
1000 ha. We also selected patches both near (10 km)
and far from large (1000 ha) areas of relatively undisturbed forest. We anticipated that smaller fragments would
be more isolated because of the geometry of the fragmentation (Gardner et al. 1987; Gustavson & Parker 1992;
Andrén 1994), leading to an unbalanced study design.
To avoid this problem, we attempted to find more small
patches close to large forests and more medium-sized
patches far from large forests, but were unable to do so.
During September–December 1999, we identified 15
patches in each size class. By the time of our first visit to
collect data (February 2000), however, three small
patches and one medium-sized patch were destroyed by
fire, two medium-sized patches became small patches as
a result of fire damage, one large patch was rendered inaccessible by active fires, and one small patch was being
logged. In addition, after we unexpectedly found that
forest birds readily used areas dominated by the exotic
trees Broussonetia and Cedrela (P.B. & B.O.K., unpublished data), we had to treat three sites (originally classed
as fragments) as parts of larger patches. Patches were
not geographically clumped with respect to size or isolation (map at http://www.for.nau.edu/pb1/images/
GhanaPatchMap.pdf).
Selection of Target Species
We restricted our attention to bird species that we expected to be associated with forests and that we could
Conservation Biology
Volume 16, No. 4, August 2002
Beier et al.
survey reliably. We first identified 97 diurnal species
that at least two of four previous studies found to be
strongly associated with forests in Ghana (Grimes 1987;
Dutson & Branscombe 1990; Holbech 1999) or neighboring Cote d’Ivoire (Gartshore et al. 1995). We also
included one nocturnal species identified as a forest species in these studies (the Red-chested Owlet [Glaucidium
tephronotum]) because this species responds in daytime to whistled renditions of its song. Of these 98 species, we made or obtained recordings of the songs of 81
species whose songs were distinctive enough to allow
auditory detections; these became the “target species”
for our study (Table 3). Twenty-one of these species (Table 3, footnote a) were not detected on any transect, although some were detected outside transects. We believe that these species were absent or silent in the
transects we sampled, but we cannot rule out the possibility that we failed to detect them.
Placing Transects in Patches
We used three types of 2.5-ha, rectangular transects: interior, edge, and matrix. Many patches had all three
types of transect (Table 2), but we could not place interior transects in the smallest patches because they
lacked any 2.5-ha area 50 m from an edge. In several
patches, topography or a contorted edge prevented us
from establishing an edge transect. We placed each
transect 100 m (usually 250 m) from any other
transect and collected data on birds and vegetation from
a single assessment line running the length of the
transect. Each interior transect extended for 50 m on either side of a 250-m-long assessment line; the entire
transect area was 50 m from any forest edge. The assessment line was either a narrow, straight line we cut
with a machete, an existing compartment line within a
forest reserve, or a relatively straight portion of an existing footpath. The entire area of each edge transect was
within 50 m of the forest edge. For all but eight of the
patches with edge transects, the edge transect was assessed via a 500-m-long, straight, cleared line along the
interface between the forest patch and the matrix habitat. Each 500-m-long matrix transect was adjacent to,
and paired with, an edge transect and was accessed by
the same line used to survey the edge transect. In eight
patches (Table 2, footnote d ), edge transects lacked
paired matrix transects. Each of these patches lacked
any forest 50 m from an edge and had irregular edges
that precluded a reasonably straight assessment line
along the edge. In these cases, we placed a central assessment line of sufficient length to ensure that 2.5 ha of
forest were sampled.
We attempted to place transects in such a way that
each was internally homogeneous with respect to canopy closure and density of large trees and to ensure that
multiple transects within a single patch differed from
Beier et al.
Table 2.
Birds in West African Forest Fragments
1101
Forest patches sampled for birds in the semideciduous forest zone of Ghana, February–June 2000.
Patch namea
Bepoase SG
Ofin Headwaters FR
Ongwam II FR East
Crops Research Institute
Kwasi Anyinama FR West
Nkwateng SG
Kato SG
Kajease SG
Bonwire SG
Ongwam II FR West
Jachie SG
Kwasi Anyinama FR East
Bunso
Anumsu FR
Boabeng SG
Kukurantumi SG
Opro River FR, Southeast
Kumanin North
Kumanin South
Gianima FR
Ajenjua Bepo FR
Asufu West FR
Prakaw FR
Owabi WS
Kade Bepo FR
Kajease FR
SouthFumansu FR
North Fumansu FR
Bobiri FR
Mirasa Hills FR
Dome River FR
Worobong South FR
Tinte Bepo FR
Nsuensa complex (Nsuensa,
Aiyola, Mamang River;
Bediako FRs; Adwafo SG)
Afram complex (Afram
Headwaters, Opro River,
and Kwamisa FRs)
Total transects
Sizeb (ha)
Distance to
largec forest (km)
3
4
4
5
5
5
5
6
8
8
9
10
10
20
20
50
80
100
300
400
450
700
1,000
1,200
1,500
1,800
3,100
4,700
5,000
6,000
8,000
8,000
9,900
14,000
3
19
24
14
4
1
5
9
15
23
19
5
7
15
50
20
0.5
1
1
5
4.5
3
—
—
—
—
—
—
—
—
—
—
—
—
33,000
—
Nearest
large forest a
Afram complex
Afram complex
Afram complex
Owabi WS
Kajease FR
Nsuensa complex
Tain II FR
Owabi WS
Bobiri FR
Afram complex
Bosumptwi Range FR
Kajease FR
Atewa Range FR
Bobiri FR
Afram complex
Atewa Range FR
Afram complex
Nsuensa complex
Nsuensa complex
Afram complex
Nsuensa complex
Afram complex
Number of transects
interior
edge
d
matrix
0
0
0
0
1
0
0
0
1
0
1
0
0
0
3
0
2
1
2
3
3
4
3
3
3
3
4
3
4
4
4
4
2
8
1
1d
1d
1d
0
1
1d
1
1
1
1
2d
2d
2d
0
2
1
1
1
1
1
1
1
1
0
1
0
2
1
1
3
1
2
4
0
0
0
0
0
1
0
1
1
0
1
0
0
0
0
2
1
1
1
1
1
1
1
1
0
1
0
2
1
1
3
1
2
4
14
0
0
80
41
29
a
FR, forest reserve; SG, sacred grove; WS, wildlife sanctuary.
Size is estimated from gazetted size ( Hawthorne & Abu-Juam 1995), reduced by areas known, based on Forest Department records or our observations, to be in farms, teak plantation, fire savannah, or water.
c
Large forest is 1,000 ha or larger.
d
It was impossible to locate an interior transect in these patches (due to lack of interior habitat) or to locate a relatively straight assessment line
on the interface between forest and matrix (due to highly irregular patch boundary).
b
one another with respect to these variables. Prior to bird
surveys, we flagged each assessment line at 50-m intervals.
Measuring Patch Characteristics
We estimated patch size from 1:50,000 maps of each reserve, deducting areas converted to farm, teak plantation, or fire savannah, as indicated by Hawthorne and
Abu-Juam (1995), local managers, and our assessment on
the ground. Isolation is the distance (km) to the nearest
large (i.e., 1000-ha) patch, estimated to the nearest 0.5
km from 1:50,000 maps. Using a natural breakpoint (Table 2), we categorized small and medium-sized patches
as near (isolation distance 10 km) or far (10 km) from
large forests.
We estimated the abundance of large trees and the
density of the forest canopy at sampling points located
at the start and end point of, and every 50 m along, the
assessment line of each transect. At each sampling point,
the number of large (i.e., 60 cm diameter at breast
height) trees per hectare was calculated as 10,000/
(3.414*r 2 ), where r is distance to the large tree closest to
Conservation Biology
Volume 16, No. 4, August 2002
1102
Table 3.
Birds in West African Forest Fragments
Beier et al.
Target species detecteda on at least one transect in the semideciduous forests of Ghana, February–June 2000.
Species
Common name
d
Alethe diademata
Apalis sharpii
Apaloderma narina e
Baeopogon indicator e
Bleda canicapilla d
Bleda syndactyla d
Buccanodon duchaillui
Bycanistes (Ceratogymna) cylindricus e
Bycanistes (Ceratogymna) subcylindricus e
Calyptocichla serina e
Campethera caroli
Campethera maculosa
Cercococcyx olivinus d
Cercotrichas leucosticta e
Chrysococcyx flavigularis
Columba malherbii (iriditorques)
Columba unicincta
Coracina azurea d
Criniger barbatus d
Criniger caluruse
Criniger olivaceous
Dryoscopus sabini
Erythrocercus mccallii f
Fraseria ocreata
Glaucidium tephronotumd
Gymnobucco calvus
Halcyon badia d
Hieraaetus (Spizaetus) africanus
Hylia prasina
Indicator exilis
Indicator maculatus
Ixonotus guttatus f
Lamprotornis cupreocauda
Macrosphenus concolor
Macrosphenus flavicans d
Malaconotus cruentus d
Malimbus malimbicus f
Malimbus nitens
Malimbus rubricollis
Mesopicos (Dendropicos) pyrrhogaster
Neocossyphus poensis e
Nicator chloris
Phoeniculus bollei
Platysteira (Dyphorophyia) blissetti
Platysteira castanea
Platysteira concreta
Poeoptera lugubris f
Pogoniulus atro-flavus
Prionops caniceps
Saruthrura pulchra d
Stiphrornis erythrothorax e
Stizorhina (Neocossyphus) fraseri d
Tauraco macrorhyncus
Tockus camuruse
Trichostoma (Illadopsis) cleaveri f
Trichostoma (Illadopsis) rufescens f
Trochocercus nitens d
Tropicranus (Tockus) albocristatus e
Turtur brehmeri
Urotriorchis macrourus
Fire-crested Alethe
Sharpe’s Apalis
Narina’s Trogon
Honey-guide Greenbul
Grey-headed Bristlebill
Bristle-bill
Yellow-spotted Barbet
Brown-cheeked Hornbill
Black-&-white-casqued Hornbill
Serine Greenbul
Brown-eared Woodpecker
Golden-backed Woodpecker
Olive long-tailed Cuckoo
Northern Bearded Scrub-robin
Yellow-throated Green Cuckoo
Bronze-naped Pigeon
Afep Pigeon
Blue Cuckoo-shrike
Bearded Greenbul
Red-tailed Greenbul
Yellow-throated Olive Greenbul
Sabine’s puff-back Flycatcher
Chestnut-capped Flycatcher
Forest Flycatcher
Red-chested Owlet
Naked-faced Barbet
Chocolate-backed Kingfisher
Cassin’s Hawk-eagle
Green Hylia
Least Honeyguide
Spotted Honeyguide
Spotted Greenbul
Copper-tailed Glossy Starling
Grey Longbill
Kemp’s Longbill
Fiery-breasted Bush-shrike
Crested Malimbe
Blue-billed Malimbe
Red-headed Malimbe
Fire-bellied Woodpecker
White-tailed Ant-thrush
West African Nicator
White-headed Wood-hoopoe
Red-cheeked Wattle-eye
Chestnut Wattle-eye
Yellow-bellied Wattle-eye
Narrow-tailed Starling
Red-rumped Tinker-bird
Red-billed Shrike
Pygmy Rail
Forest Robin
Rufous Flycatcher
Black-tip Crested Turaco
Red-billed Dwarf Hornbill
Black-cap Illadopsis
Rufous-winged Illadopsis
Blue-headed Crested Flycatcher
White-crested Hornbill
Blue-headed Dove
Long-tailed Goshawk
Feeding guild b
Percent occurrence c
Acronym
TI
CI
CI
F
TI
TI
FI
FI
FI
FI
CI
CI
CI
TI
CI
F
F
CI
FI
CI
CI
CI g
CI
CI
I, P
F
TI
P
CI
FI, wax
I, wax
FI
Fg
CI
CI
CI g
CI g
CI g
CI g
CI
TI
FI g
CI
CI
CI
CI
Fg
CI
CI g
TI
TI
CI
F
CI
TI g
TI g
CI
FI
F
P
17
70
17
36
70
16
1
1
1
1
0
5
10
8
1
2
2
27
30
45
2
22
1
3
2
69
10
2
97
1
2
1
9
77
2
16
0
2
31
16
4
46
1
3
41
0
4
22
7
27
18
34
2
7
3
6
30
67
9
1
ALDI
APSH
APNA
BAIN
BLCA
BLSY
BUDU
BYCY
BYSU
CASE
CACA
CAMA
CEOL
CERCL
CHFL
COMA
COUN
COAZ
CRBA
CRCA
CROL
DRSA
ERMC
FROC
GLTE
GYCA
HABA
HIAF
HYPR
INEX
INMA
IXGU
LACU
MACO
MAFL
MACR
MAMA
MANI
MARU
MEPY
NEPO
NICH
PHBO
PLBL
PLCA
PLCO
POLU
POAT
PRCA
SAPU
STER
STFR
TAMA
TOCA
TRCL
TRRU
TRNIT
TRAL
TUBR
URMA
a
An additional 21 target species were never detected: Brown-chested Alethe (Alethe poliocephala)d, Black-capped Apalis (Apalis nigriceps), Green-tailed Bristlebill (Bleda
eximea), Buff-spotted Woodpecker (Campethera nivosa), Black-casqued Hornbill (Ceratogymna atrata)e, Yellow-casqued Hornbill (Ceratogymna elata)e, Dusky long-tailed
Cuckoo (Cercococcyx mechowi ), Great Blue Turaco (Corythaeola cristata), Shining Drongo (Dicrurus atripennis), Forest Francolin ( Francolinus lathami), Lyre-tailed Honeyguide ( Melichneutes robustus), White-breasted Negrofinch ( Nigrita fusconota), Thick-billed Cuckoo ( Pachycoccyx audebertii), Dusky Tit ( Parus funereus), Forest WoodHoopoe ( Phoeniculus castaneiceps), White-throated Greenbul ( Phyllastrephus albigularis), African Pitta ( Pitta angolensis), Crowned Hawk-Eagle (Stephanoaetus coronatus), Lemon-bellied Crombec (Sylvietta denti), Black Dwarf Hornbill (Tockus hartlaubi)e, and Dusky Crested Flycatcher (Elminia nigromitratus).
b
Feeding guilds: TI, terrestrial insectivore; CI, canopy insectivore; F, frugivore; FI, frugivore-insectivore; and P, predator.
c
Percent occurrence is the mean across patches, after the average across forested transects within a patch is first computed.
d
The primary observer whistled the song of this species during the second visit to each transect.
e
A second observer broadcast a recorded song of this species during the second visit to each transect.
f
We suspect that we occasionally (perhaps often) overlooked the unobtrusive calls of these species. Because of this failure, we did not build any single-species models
for these species.
g
The five existing volumes of Fry et al. (1982–1997) do not include this species. Feeding guild based on description of genus or family given by Serle et al. (1977) or
on our field observations.
Conservation Biology
Volume 16, No. 4, August 2002
Beier et al.
the sampling point on one side of the assessment line.
On transects within forest, we measured distances to
two trees per sampling point, one on each side of the assessment line. On assessment lines on the interface between forest and matrix, we measured distance to the
nearest large tree on the forested side of the line. Because assessment lines along the forest-matrix interface
were twice as long as interior lines, this resulted in an
equivalent number and geometry of measurements on
all lines. Transects fell into three equal-sized classes with
respect to abundance of large trees: low (2.4–13.3/ha),
medium (13.3–26.5/ha), and high (26.6–81.4/ha). We
measured canopy density (%) as the average percent
canopy on the distal half of a spherical densiometer facing perpendicular to the assessment line at each sampling point. We took readings to the right and left of
sampling points on transects within forest, but only on
the forested side of assessment lines on the interface between forest and matrix. Roughly equal numbers of
transects fell into each of three canopy classes: open
(25–93%), medium (94–97%), and closed (98–100%).
Sampling Birds
We made a compact disk of the songs and calls of the 81
target species from recordings produced during 1974–
1980 by the Societe d’etude’s Ornithologiques de France
(4 ave du Petit Chateau–F-91800 Brunoy, France, seof@
mnhn.fr), tapes from the British Library ( London, [email protected]), and our own field recordings. One
observer was trained to recognize the songs on the disk
with 100% accuracy before the surveys began. All surveys were completed from 0550 to 1050 hours. On each
transect, the observer walked the assessment line and
listened and looked for birds up to 50 m on each side of
the line, spending 6 minutes on each 50-m segment of
the line. Each species was marked as present if it was detected by song or sight in the transect area during either
of two visits. The first visit was from 27 February
through 13 April (late dry season), and the second visit
was from 21 April through 1 June (early rainy season).
At least 4 weeks elapsed between visits. On the second
visit to a patch, the order of the transects visited on a
given day was reversed from that of the first visit.
On the second visit we increased the detectability of
28 species by whistling imitations of their songs or
broadcasting recorded songs (Table 3, footnotes d & e).
The first observer whistled an imitation of the song of
each of 14 species twice per 250 m of transect length.
Whistling was confined to periods when no target species was singing. A second observer played recorded
songs of another 14 species once per 250 m of transect
length, staying 100 m from the first observer, and recorded the responses of those 14 species. We did not
whistle or broadcast a song of a species if it had previously been detected on the transect.
Birds in West African Forest Fragments
1103
Data Analysis
We assessed bird occurrence with respect to five forest
traits (Table 4). Prior to analyses, we applied natural-logarithm transformations to patch size, patch isolation, and
abundance of trees, and arcsine-square-root transformations to canopy density. Two traits, size and isolation, were
patch characteristics, whereas the other three were measured at the level of the individual transect. The existence
of two types of variables presents a problem in making statistical inferences, because any omnibus test including all
five variables as independent variables is necessarily pseudoreplicated with respect to the patch-level characteristics.
To minimize this problem, we present results at the patch
level whenever appropriate. When we used transect-level
analyses to gain insight into bird response to canopy closure, large-tree density, and forest edge, we evaluated apparent trends in light of pairwise correlations among independent variables, and we evaluated additional models or
contrasts by using appropriate subsets of data.
We used pairwise correlations, scatterplots, analysis of
variance ( ANOVA), and group means to evaluate how
the five independent variables influenced species richness (number of forest species in a transect) and the
likelihood of occurrence of individual species of forest
birds. When multicollinearity was observed (strong correlation between 2 independent variables such that
each appeared to have a strong effect on the occurrence
of forest birds), we calculated partial correlation coefficients, conducted an ANOVA with the other variable(s)
as covariate(s), or examined an appropriate subset of
the data. The partial correlation coefficient between an
independent variable Y and dependent variable X2 controlling for X1 is the correlation between the residuals
from a regression of Y and X1 and the residuals from a
regression of X2 on X1 (Zar 1996). We used logistic stepwise regression (forward entry, p to enter 0.05, p to
remove 0.10) for individual species to confirm
whether a variable with a strong univariate correlation
with species occurrence added any explanatory power
to a model with fewer variables. We evaluated the effect
of edge location on birds with paired t tests by using
only data from the 18 patches that had both edge and interior transects. In statistical tests based on small and
medium-sized patches (n 22) or based on the patches
with both edge and interior transects (n 18), we used
an alpha of 0.10 to attribute significance to observed
trends. For tests based on individual transects (n 121)
or all patches (n 35), we used an alpha of 0.05.
We used chi-square tests to determine whether five foraging guilds differed in their sensitivity to patch size or forest edges. We classified most birds into feeding guilds (Table 3) based on species accounts given by Fry et al. (1982–
1997). For 11 species not described in these volumes, we
relied on the description of the genus or family given by
Serle et al. (1977) or our field observations.
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Volume 16, No. 4, August 2002
1104
Birds in West African Forest Fragments
Beier et al.
Table 4. Bird species-richness (number of species) correlations with explanatory variables, as indicated by Spearman correlation coefficients.a
Species richness
Density of large trees
Canopy density
Isolation
Patch size
Density of large trees
Canopy density
Isolation
Patch size
Edge locationb
0.08
0.19*
0.22*
0.41c,d*
0.38g**
0.02g
0.93e**
0.03
0.05
0.39*
0.29 f**
0.25**
0.05
0.32**
0.41**
a
Significance levels: *p 0.05; **p 0.01. Except as footnoted, all correlations are based on n 121 forested transects (29 matrix transects excluded).
b
Binary variable; 1, edge; 0, interior of patch.
c
Correlation based on n 22 small and medium-sized patches for which isolation is defined.
d
The apparent effect of isolation on species richness was due to confounding of isolation and patch-size effects. Partial correlation controlling
for patch size yielded r 0.14 ( p 0.53)
e
Correlation based on n 35 patches.
f
Edge effect persisted after patch size was controlled for (paired t test, t 3.5, 17 df, p 0.002).
g
Correlation based on n 45 transects in 22 patches for which isolation is defined.
The above analyses helped us assess the importance of
four potential mechanisms influencing forest birds in
West African forest patches (Table 1). To further evaluate the importance of island biogeography, we regressed
an index of area sensitivity (the slope of the regression
of probability of occurrence on patch size for a given
species) on natural abundance (abundance of that species in large forests in our study area). To discriminate
between the two mechanisms involving edge effects,
we compared forest edge and forest interior with respect to canopy closure and density of large trees and
evaluated whether edge-sensitive species avoided the
canopy closure and large tree densities characteristic of
edges. Finally, we evaluated whether area sensitivity
might be related to the home-range size of a species. Although home-range size is unknown for forest bird species in West Africa, home range size scales to body mass
in many taxa ( McNab 1963; Harestad & Bunnell 1979;
Lindstedt et al. 1986), including birds ( Mace & Harvey
1983). We therefore used body mass as an index of
home-range size in a regression of area sensitivity
(above) on the logarithm of body mass, and in a regression of critical-patch size (the smallest patch in which an
area-sensitive species was found) on the logarithm of
body mass. Body mass for each species was taken from
Dunning (1993). We used masses of similar-length congeners for a few species not listed by Dunning.
Results
Species Richness
Species richness—the number of target species detected
on two visits to a transect—varied from 1 to 22 species
on forested transects (mean 11.9, n 121) and from 0
to 8 on matrix transects (mean 2.6, n 29). All further
discussion is restricted to data from forested transects.
Species richness on forested transects was correlated
with four of the five independent variables. Richness
Conservation Biology
Volume 16, No. 4, August 2002
was positively correlated with patch size and canopy
density and negatively correlated with patch isolation
and edge location, but it was not correlated with density
of large trees ( Table 4). As expected, there were also
strong correlations among the independent variables
( Table 4). In particular, patch size, which had the strongest influence on species richness (r 0.93), was negatively correlated with patch isolation (i.e., the smallest
patches tended to be farthest from large forests) and
edge location (i.e., edge transects tended to occur in
small patches, reflecting the fact that small patches are
“all edge”). This collinearity among independent variables required subsequent analyses to rule out or confirm alternative interpretations of the results.
Species richness per transect increased with patch
size over the entire range of patch sizes we observed
( Fig. 1), and patch size was far more important than the
other four factors as a determinant of species richness
( Table 4). To rule out the possibility that the effect of
patch size might be an artifact of the combined influence of isolation and edge location, the two variables
that were also correlated with size, we conducted an
analysis biased against patch size (ANOVA of richness by
patch-size class, with edge location and isolation distance as covariates). This test confirmed the relative importance of patch size ( p 0.046 for size class, p 0.32 for edge location, and p 0.19 for isolation distance; n 30 patch-location combinations).
Each transect in a small patch tended to support the
same species as other small-patch transects, so the entire
collection of 13 small patches (17 transects) contained a
total of 25 species. In contrast, the 9 medium-sized
patches (28 transects) harbored a total of 40 species.
The 13 large patches (76 transects) harbored all 60 of
the focal species detected during the study. The 6 most
diverse single transects in large patches contained 21–22
species each, nearly as many as the cumulative total of
25 species in all small patches.
The apparent influence of isolation on species richness (Table 4) was apparently an artifact of the high cor-
Beier et al.
Birds in West African Forest Fragments
1105
Figure 1. Number of forest bird species per transect increased over the full range of patch sizes for 35 patches
in Ghana, West Africa (r 2 0.83, p 0.0005, semi-log
regression). Relatively isolated patches (circles) had no
fewer species than similarly sized patches that were
10 km from the nearest large patch (1000 ha, triangles). The most extreme outliers are labeled (Afram
complex formed a large forest patch dominated by the
exotic tree species Broussonetia papyrifer, and BoabengFiema was the most isolated patch).
relation between isolation and patch size. Isolation had
no effect on species richness in analyses that controlled
for patch size (partial correlation of species richness,
with isolation distance controlling for patch size: r 0.14, p 0.53 for 22 patches; also ANOVA of species
richness by isolation with patch size as a covariate: p 0.9
for n 22 small and medium-sized patches, and p 0.9 for n 13 small patches). The lack of an isolation effect is also evident in a scatterplot (Fig. 1).
The negative correlation between edge location and
patch size (Table 4) reflects the fact that in many small
patches, only edge transects were possible. To evaluate
the effect of edge location on species diversity, we controlled for patch size by analyzing data only for those 18
patches that had both edge and interior transects. This
analysis confirmed a substantial edge effect: interior
transects averaged 13.4 species per transect compared
with 11.1 species per transect on edge transects (paired
t test, t 3.5, 17 df, p 0.002).
Canopy density also influenced species diversity, although its effect was not as strong as that of patch size
or edge location. The positive influence of canopy density was a bit unexpected given the narrow range of observed values of this variable (80% of values were above
90%). The lack of strong correlation between species
richness and density of large trees reflects the fact ( below) that roughly equal numbers of bird species responded negatively and positively to this factor.
Responses of Individual Species
Three species—Hylia prasina, Gymnobucco calvus,
and Sarothrura pulchra—occurred in matrix habitats
often enough (Table 5) to suggest that they should not
be considered forest specialists. The other 57 target species were rarely or never detected outside of forests.
The responses of individual species to habitat fragmentation ( Table 5) were consistent with the observed
patterns of species richness. Univariate comparisons
and stepwise logistic regression models for individual
species showed that patch size was the most important
factor and that isolation was the least important factor
influencing the presence of individual bird species ( Tables 5 & 6).
Of the 23 species responding to patch size, 22 were
more likely to occur in larger patches (the exception
was Sarothrura pulchra, which in hindsight was not a
forest specialist). Fifteen of the 22 area-sensitive species
were never found on transects in small patches ( Table
5). In addition, another 14 species were never found in
small patches, although their overall rarity precluded statistical inference about their response to patch size.
Nine species were edge sensitive in univariate tests
( Table 5). In contrast to the strong threshold response
exhibited by most area-sensitive species, most responses
to edge were relatively subtle in that even the most
edge-sensitive species were sometimes encountered in
edge transects. The most extreme edge avoider was
Tockus camurus, which was present on 16% of interior
and 1% of edge transects.
Eleven species were more likely to be present as canopy density increased, and two species occurred more
often on transects with open canopies ( Table 6). As
with responses to edge, these responses were largely
matters of degree. More species (five) showed negative
responses to the density of large trees than positive responses (three species). Nicator chloris and Urotriorchis macrourus showed the strongest preferences for
areas with fewer large trees.
Only four species responded to patch isolation, all of
them negatively. The strongest response was from Trochocercus nitens, which was found in 46% of transects
in patches near a large forest, but never in transects in
patches far from a large forest. Ironically, this species
was common in areas with an open canopy and was one
of the few forest species regularly encountered in matrix transects (Table 5). Alethe diademata also showed
a strong negative response to isolation.
Overall, 37% of the forest species were area sensitive,
and 15% were edge sensitive. There were area-sensitive
Conservation Biology
Volume 16, No. 4, August 2002
1106
Birds in West African Forest Fragments
Beier et al.
Table 5. Percentage of transects in which each target bird species was detecteda illustrates the negative responses of 9 species to forest edges,
negative responses of 4 species to isolation, and positive responses of 21 species to patch size.
Location
Species
acronymb
ALDI
APNA
APSH
BAIN
BLSY
BYCY
CAMA
CERCL
CEOL
COAZ
COMA
CRBA
FROC
GYCA
HABA
HYPR
MACO
MARU
MEPY
NEPO
NICH
PRCA
SAPU
STER
STFR
TOCA
TRNIT
TUBR
URMA
Proximity to large forest
Patch-size class
interior
(n 18)
edge
(n 18)
matrix
(n 18)
pc
near
(n 13)
far
(n 9)
pd
small
(n 13)
medium
(n 9)
large
(n 13)
pe
34
25
85
38
28
2
12
11
16
57
4
39
8
81
16
99
74
48
30
6
47
17
14
30
37
16
43
21
1
22
10
61
41
7
0
2
4
1
25
0
21
1
83
6
100
89
30
19
7
52
6
25
28
56
1
48
6
0
0
0
11
7
0
0
0
0
0
0
0
0
0
53g
0
46 g
14
13
11
0
11
0
19 g
0
1
0
7
0
0
0.40
0.19
0.07f
0.77
0.06
0.19
0.04
0.26
0.05
0.01f
0.19
0.12
0.14
0.54
0.08 f
0.33
0.16 f
0.09
0.21
0.83
0.69
0.09
0.33
0.86
0.16 f
0.04 f
0.69
0.12
0.33
19
8
69
24
7
0
4
6
0
21
0
23
2
69
0
100
77
24
9
2
51
6
26
15
24
5
46
11
0
0
11
65
28
11
0
0
0
11
11
0
22
0
50
0
93
61
28
6
0
28
0
48
6
17
0
0
0
0
0.01
0.65
0.60
0.85
0.54
—
0.72
0.38
0.46
0.43
—
0.48
0.67
0.84
—
0.14
0.06 f
0.35
0.41
0.93
0.005 f
0.31
0.65
0.22
0.91
0.68
0.001 f
0.42
—
0
0
62
23
0
0
0
0
0
4
0
8
0
54
0
100
73
8
0
0
42
0
38
4
8
0
23
0
0
27
23
76
29
22
0
6
8
11
36
0
44
3
72
0
93
67
52
19
2
40
8
31
22
40
8
33
16
0
28
30
75
54
29
3
9
17
18
44
5
42
7
83
26
98
87
41
30
10
55
12
14
30
56
14
34
12
2
0.001 f
0.006
0.15
0.03 f
0.001f
0.006
0.03
0.001f
0.10
0.001
0.006 f
0.02
0.04
0.03 f
0.002 f
0.90
0.21
0.03
0.001
0.009 f
0.41
0.02
0.04h
0.002 f
0.001f
0.006 f
0.33
0.008 f
0.08
a
Each percentage is the mean across patches, after the average across transects within a patch was computed. Species not listed in this table
were not sensitive to edge, isolation, or area.
b
Species acronyms are defined in Table 3.
c
Significance level of a paired t test comparing probability of occurrence on interior transects to that on edge transects (n 18 patches with
both transects types). A p 0.10 is statistically significant.
d
Significance level of a partial correlation of probability of occurrence on isolation distance, controlling for patch size, for 22 small and medium patches (isolation is not defined for large patches). A p 0.10 is statistically significant.
e
Significance level of a regression of probability of occurrence on patch size (n 35 patches). A p 0.05 is statistically significant.
f
Stepwise logistic regression also identified this variable as influencing occurrence of this bird species.
g
The relatively high frequency of occurrence of these three species in matrix habitats suggests that they are not forest specialists.
h
This was the only species to show a preference for small patches.
species in each feeding guild, and differences among foraging guilds in area-sensitive and edge-sensitive species
were statistically weak ( p 0.11 for area and p 0.09
for edge; chi-square tests, 4 df ). Terrestrial insectivores
were most likely to be area sensitive (6 of 10 of species,
p 0.07; chi-square test, 1 df ). No frugivores (8 species) or frugivore-insectivores (9 species) were edge sensitive ( p 0.03 and p 0.04, respectively, chi-square
tests, 1 df ).
Mechanisms of Area Sensitivity of West African Forest Birds
ISLAND BIOGEOGRAPHY
Contrary to expectation, species diversity was not a function of isolation, and isolation was the least important
Conservation Biology
Volume 16, No. 4, August 2002
factor in single-species analyses. Furthermore, area sensitivity was not negatively correlated with natural abundance. In fact, area sensitivity (the slope of the line relating probability of occurrence to patch size) showed a
positive correlation with natural abundance (r 0.56,
p 0.001).
STRUCTURAL AND MICROCLIMATE CHANGES NEAR EDGES
Seven of 22 area-sensitive species were also edge sensitive. However, the density of large trees was 39% greater
near patch edges than in the forest interior, and, although edge transects did have a more open canopy
than interior transects, the difference was small ( Table
7). Nonetheless, the results could support the importance of an altered form of this mechanism if edge-sensi-
Beier et al.
Table 6.
Birds in West African Forest Fragments
Percentage of transects in which each target bird species was detected in relation to abundance of large trees and canopy density.a
Abundance of large trees
Species
acronymb
e
APNA
BLCA
BLSYe
BYCYe
CAMAe
CERCLe
CEOL
COAZe
CRBAe
CROL
DRSA
HABAe
MACO
MEPYe
NICH
PHBO
TOCAe
TUBRe
URMAe
1107
Canopy density
Mean
(n 121)
low
(n 39)
medium
(n 42)
high
(n 40)
pc
open
(n 35)
medium
(n 45)
closed
(n 41)
pd
22
69
24
3
7
18
12
37
37
3
28
13
79
22
48
2
12
12
2
18
87
10
5
5
28
5
21
36
8
21
5
72
18
69
3
10
10
5
24
60
31
2
7
12
12
45
38
0
33
21
83
26
43
2
10
10
0
25
63
30
3
8
15
18
45
37
3
30
12
83
23
33
0
18
15
0
0.58
0.04 f
0.03 f
0.21
0.65
0.03 f
0.08
0.02 f
0.40
0.03
0.35
0.10
0.03 f
0.31
0.002 f
0.15
0.46
0.44
0.03
14
54
14
3
9
11
0
31
20
3
20
9
86
9
40
6
6
9
3
20
82
18
2
9
16
11
40
33
2
22
9
76
24
53
0
11
9
0
32
68
39
5
2
27
22
39
56
5
41
22
78
32
49
0
20
17
2
0.01 f
0.08 f
0.002 f
0.02
0.02 f
0.003 f
0.03 f
0.72
0.001 f
0.82
0.02 f
0.03
0.69
0.03 f
0.51
0.002
0.03
0.03
0.05
a
Sign (,) indicates direction of significant responses. Species not listed in this table were not sensitive to the abundance of large trees or to
canopy density.
b
Species acronyms are defined in Table 3.
c
Significance level of correlation between the likelihood of species occurrence on a transect and the number of large trees per hectare on each
transect (n 121 transects).
d
Significance level of correlation between the likelihood of species occurrence on a transect and canopy closure on each transect (n 121
transects).
e
Area-sensitive species.
f
Stepwise logistic regression also identified this variable as influencing occurrence of this bird species.
tive species consistently avoided high densities of large
trees and open canopies. This was not the case for most
species. Three species avoided edges despite their preference for higher densities of large trees ( Table 7 ). Although four edge-sensitive species also preferred closed
canopies, two other species avoided edges despite their
preference for open canopy conditions. Thus, although
our evidence does not support the broad relevance of
this mechanism, structural changes near patch edges
may influence the edge sensitivity of Cercococcyx olivinus, Halcyon badia, and Tockus camurus (Table 7).
bility of occurrence and patch size) did not increase
with the logarithm of body mass (r 0.08, p 0.54).
However, critical patch size (the smallest patch in
which an area-sensitive species was found) showed a
strong positive correlation with logarithm of body mass
(Fig. 2). This relationship indicates that critical patch
size varies from about 10 ha for the 24-g Stiphrornis
erythrothorax to about 8000 ha for the 921-g Bycanistes
cylindricus. These critical patch sizes are probably
equivalent to several home ranges for these species.
INCREASED PREDATION AND NEST PARASITISM NEAR EDGES
Discussion
The fact that 7 of 22 area-sensitive species were also
edge-sensitive indicates that edge effects probably contribute to edge sensitivity in some species. The lack of
evidence for an edge effect due to changed forest structure is consistent with the hypothesis that some other
type of edge effect underlies the response of some of
these edge-sensitive species. Predation and parasitism
near edges are likely candidates.
INSUFFICIENT AREA FOR HOME RANGES
Contrary to expectation, our index of area sensitivity
(the slope of the relationship between a species’ proba-
Although all studies of fragmentation show that patch size
is positively correlated with species diversity per patch,
this is in part an artifact of greater sampling effort in large
patches and the fact that large quadrats contain more species than small quadrats (Haila 1983; Hill et al. 1994; May
& Stumpf 2000). By collecting data on a per-transect basis,
we have provided unambiguous answers to several important conservation questions in upper Guinean semideciduous forests. One hectare of forest in a small forest patch
harbors markedly fewer species of forest birds than one
hectare of forest in a large patch. Significant losses of forest birds occur in patches of several hundred hectares. At
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Volume 16, No. 4, August 2002
1108
Birds in West African Forest Fragments
Beier et al.
Table 7.
Response of edge-sensitive bird species to density of large trees and canopy closure.
Response of the nine edge-sensitive species to that variable b
Variable
Density of large trees
(trees per hectare)
Canopy closure (%)
Edgea
Interiora
pa
n 121 transects in 35 patches
27 (18)
19.4 (8.7)
0.036
92 (6.0)
94 (8.6)
0.09
positive responses: BLSY COAZ
negative response: none
positive responses: BLSY CEOL
HABA TOCA
negative response: CAMA
n 80 transects in the 18 patches
that had edge and interior transects
positive response: APSH
negative response: none
positive responses: BLSY HABA TOCA
negative responses: CAMA MARU
a
Means and standard deviations for 18 patches that had both edge and interior transects, and significance of a paired t test of the hypothesis of
no difference between means.
b
Partial correlation, patch size controlled for. Species acronyms are defined in Table 3.
least one-quarter of forest bird species will be absent from
a reserve system composed solely of small forest patches,
compared with a single large reserve. A predictable subset
of forest bird species disappeared as patch size decreased,
so management of larger patches should focus on species
and guilds, such as terrestrial insectivores, that are unlikely
to occur in smaller patches. Such management should
minimize disturbance to the forest canopy, because almost
half ( 9 of 22) of area-sensitive species showed a strong
positive response to closed forest canopies. Increased isolation distance did not decrease the conservation value of
a patch for most forest birds.
Our estimate of a 25% loss of species from small fragments may be a gross underestimate for three reasons.
First, some species may already have been lost from
even our largest fragments. Most of our “large” patches
were only a few thousand hectares in size, compared
with a single upper Guinea forest of several million hectares only a century ago. Brooks et al. (1999) suggest that
tropical forests of 1000 ha can expect to lose 50% of
their species within 50 years of fragmentation. Despite
the imprecision of Brooks’s predictions (based on mathematical relationships parameterized from only five fragments), our large fragments certainly may have lost
many species, which may account for some of the 21
target species we never detected. Second, much of the
fragmentation of Ghana’s forests has occurred within
the last 20–50 years, and if the process of relaxation—
loss of species until diversity reaches the equilibrium diversity of the fragment—has a half-life of about 50 years
(Brooks et al. 1999), then further losses can be expected
in patches of all sizes. Finally, rarity is a hallmark of most
species of birds in tropical forests, and it is difficult to
make statistical inferences about rare species. In addition to the 21 species whose area sensitivity was “statistically significant,” 14 rare species were detected in
large but not in small patches. Thus, there may be many
more area-sensitive species than can be identified by statistical inference in a study like ours. Without a sample
size (35 patches) that greatly exceeds other studies of
tropical forest fragmentation, it is doubtful that we
could have identified 22 area-sensitive species.
Conservation Biology
Volume 16, No. 4, August 2002
Although small forest patches do not contribute significantly to the conservation of forest birds, such patches
do harbor many species of native plants, insects, mammals, and birds. The avian habitat generalists that dominate small patches include pollinators, such as sunbirds
( Nectariniidae, over 25 species in West Africa), and insectivores, such as shrikes (Laniidae, over 20 species in
West Africa), that probably provide important ecosystem services in both the forest and the surrounding agricultural landscape. If West Africa manages to curb agricultural overuse and recurring wildfires in coming
decades, these small patches will be the nuclei for ecosystem recovery. We hope that our findings will be used
as motivation to halt or reverse the fragmentation of
West African forests, not to write off small patches as
having no value.
We caution against using our results to argue that extraction of large logs from the forest is compatible with
conservation of forest birds. Such an argument is suggested by the facts that (1) only three species of forest
Figure 2. Body mass was a good predictor of critical
patch size (i.e., the smallest patch in which an areasensitive species was detected) for 11 area-sensitive
species in Ghana, West Africa (r 2 0.57, p 0.005,
log-log regression). This suggests that area-sensitive
species tend to be absent from patches smaller than
several home-range areas.
Beier et al.
birds tended to avoid areas with low densities of large
trees, and none of these species showed an absolute
aversion to such areas; (2) five species (most notably
Urotriorchis macrourus) preferred logged areas; and
(3) logging operations typically extract 1.5 trees per
hectare per felling cycle (Hawthorne & Abu-Juam 1995).
In the moist semideciduous zone of nearby Cote d’Ivoire,
Waltert (2000) also found that bird abundance, species
richness, evenness, and diversity indices were nearly
identical in control and thinned forests (which exhibit
a 10% reduction in live basal area as a result of girdling
of medium-sized noncommercial trees and lianas). In a
typical logging operation, however, 6% to 20% of the
forest canopy is removed for skid trails, logging roads,
and destruction of nontarget trees that are pushed down
by the felled tree or pulled down by its lianas ( Johns
1997 ). In past decades, the canopy would recover in
2–5 years, but since about 1970 the fire-tolerant exotic
weed Chromolaena odorata has been rapidly invading
openings created by logging, suppressing forest regeneration, especially when a fire reaches the site in the first 3
years. This has made logging a major factor in the increased extent and severity of forest fires ( Hawthorne
1994). Thus, timber harvest is compatible with bird conservation only if harvest operations minimize collateral
damage and C. odorata invasion. In the absence of invasive exotics, Owiunji and Plumptre (1998) similarly found
only minor effects of selective logging on African forest
birds.
Our finding that isolation had a trivial effect on forestbird diversity applies only to isolation distances of 25
km. Our most extremely isolated fragment, BoabengFiema Sacred Grove, was 50 km from a large forest, compared to 24, 23, 20, 19, and 19 km for the next-most-isolated patches. Boabeng-Fiema’s extremely low diversity
(Fig. 1) suggests that a study including a larger number
of extremely isolated patches might reveal some important effects. However, Boabeng-Fiema was also our only
patch with high densities of two monkey species, Geoffroy’s Pied Colobus (Colobus vellerosus) and Campbell’s
Mona monkey (Cercopithecus mona campbelli ), both
of which may opportunistically prey on bird nests.
Terrestrial insectivores were most sensitive to fragmentation of upper Guinean forests, a result consistent
with observations in western Colombia (Kattan et al.
1994) and central Amazonia (Stouffer & Bierregaard
1995). Although terrestrial and understory insectivorous
birds may be vulnerable to microclimate change in more
open forests, either directly or because their foraging
substrates or food supplies are adversely affected ( Johns
1997), we did not find more open forest conditions as
patch size decreased (Table 3), and the canopy was only
slightly more open in patch edges than interiors (Table
7). Many of these terrestrial insectivores rely on foraging
columns of army ants (Eciton) to flush out insect prey.
Decreased abundance of army ants in small patches could
Birds in West African Forest Fragments
1109
underlie the increased area sensitivity of this feeding
guild (Stouffer & Bierregaard 1995).
Although hornbills require large trees for nesting cavities, they did not show a response to decreased abundance of large trees. Perhaps large cavities are not a limiting factor for hornbills, or perhaps these wide-ranging
birds are likely to be detected in a 2.5-ha transect that
lacks suitable nest sites.
Our data are consistent with two of the six mechanisms that cause birds to be area-sensitive in some contexts. About one-third of the area-sensitive species are
also edge-sensitive, so edge-related effects almost certainly contribute to area sensitivity for these species.
Our data suggest that structural and microclimate
changes near edges underlie edge avoidance by a minority of area-sensitive birds. Thus, increased predation and
nest parasitism near forest edges emerge as probable
causes of area sensitivity for the other edge-sensitive
species. In West Africa, at least 10 species of parasitic
cuckoos (Cuculidae) and two parasitic honeyguides (Indicatoridae) are common habitat generalists that might
increase in activity near forest edges. (Nest parasites in
the Ploceid genus Vidua are thought to parasitize only
savanna species.) Because all mammals (including small
predators) are heavily hunted, especially close to farms
and human habitations, it seems unlikely that mammalian predators characteristic of matrix habitats are affecting forest birds near patch edges. Although we never observed either of the two omnivorous corvids in forests
(not even in forest edges, although Pied Crows [Corvus
albus] were abundant in adjacent farmland), we cannot
rule out that other avian omnivores or predators might
be significant predators on adults or nestlings in forest
edges.
If home range size scales to body mass for West African forest birds, our results are consistent with the hypothesis that area-sensitive birds will be absent from
patches smaller than a few home range sizes (Stratford &
Stouffer 1999). Leck (1979) similarly observed that extinction proneness increased with avian body mass. Although each species probably can fly across farmlands
from large to small patches, many habitat-specialist birds
are remarkably sedentary, and forest terrestrial insectivores are the least mobile avifaunal guild (Sieving & Karr
1997).
Our results also suggest that island biogeography
(MacArthur & Wilson 1967) is not an important mechanism for area sensitivity of West African forest birds.
Contrary to this theory, isolation distance was not related to species richness in patches, and rarer species
were not more prone to be area sensitive. This should
not be surprising because true islands (the subject of
MacArthur and Wilson’s treatise)— unlike habitat fragments—are surrounded by a nonterrestrial matrix and
are not subject to edge effects. The lack of applicability
in this instance does not detract from the importance of
Conservation Biology
Volume 16, No. 4, August 2002
1110
Birds in West African Forest Fragments
this seminal work in stimulating the study of animal responses to habitat fragmentation.
We have no data relevant to the last two mechanisms in
Table 1, mesopredator release and competition from generalist birds. Most mammals (including predators) are
hunted in West Africa, however, with greatest hunting
pressure in the smallest patches, so mesopredator release
seems unlikely in these patches. Although we commonly
observed generalist species (such as Dicrurus adsmilis,
Oriolus brachyrhynchus, Pycnotus barbatus, Turtur
tympanistria, Passer griseus, and Tersiphone spp.) in
small patches, only a reciprocal removal experiment can
demonstrate whether increases in generalists are a cause
of or a response to the absence of forest birds.
As in many previous studies, we documented the profound effects of forest fragmentation on forest avifaunas,
begging the question of how avifaunal impoverishment
affects the remaining forest. Birds in tropical forests play
ecological roles as predators (on invertebrates and seeds)
and as seed dispersers (Silver et al. 1996). We hope future
work will document how ecological processes change in
patches lacking a large fraction of the native avifauna.
Acknowledgments
This study was funded by a grant from the U.S. Fulbright
Program. We thank W. Ossom of Kwame Nkrumah University of Science and Technology (KNUST), Kumasi,
for assistance in learning to identify birds in the field and
in meetings with managers of forest reserves, sacred
groves, and wildlife sanctuaries, and we thank W. Oduro
of KNUST for helpful advice. The Forest Research Institute of Ghana provided office space for P.B. and paid the
salary of B.K. throughout the study. We thank J. Mason
and P. Adjewodah of the Nature Conservation Research
Centre, Accra, for logistic support. F. Biah worked long
hours as the project driver. The staff at all Forest Department and Wildlife Department offices were helpful and
eager to assist, as were the chiefs and caretakers of the
sacred groves. We report species detected in each management unit and other detailed results at http://www.
for.nau.edu/pb1/ghanabirds.html.
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