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Proc Natl Acad Sci U S A. 2002 January 8; 99(1): 263–267. doi: 10.1073/pnas.012616199. | PMCID: PMC117549 |
Copyright © 2002, The National Academy of Sciences Ecology Disappearance of insectivorous birds from tropical
forest fragments Ça  an H. Şekercio lu, *† Paul R. Ehrlich, * Gretchen C. Daily, * Deniz Aygen, ‡ David Goehring, § and Randi F. Sandí ¶*Center for Conservation Biology, Department of Biological Sciences, Stanford University, Stanford, CA 94305-5020; ‡Coastal Virginia Wildlife Observatory, Cape Charles, VA 23310; and §Department of Ecology and Evolutionary Biology, Princeton University, ¶Copal de Agua Buena, Coto Brus 8257, Costa Rica Accepted November 19, 2001. Determining the impact of forest disturbance and fragmentation on
tropical biotas is a central goal of conservation biology. Among
tropical forest birds, understory insectivores are particularly
sensitive to habitat disturbance and fragmentation, despite
their relatively small sizes and freedom from hunting pressure. Why
these birds are especially vulnerable to fragmentation is not known.
Our data indicate that the best determinant of the persistence of
understory insectivorous birds in small fragments is the ability
to disperse through deforested countryside habitats. This finding
contradicts our initial hypothesis that the decline of insectivorous
birds in forest fragments is caused by impoverished invertebrate prey
base in fragments. Although we observed significantly fewer
insectivorous birds in smaller fragments, extensive sampling of
invertebrate communities (106,082 individuals) and avian diets (of 735
birds) revealed no important differences between large and small
fragments. Neither habitat specificity nor drier fragment microclimates
seemed critical. Bird species that were less affected by forest
fragmentation were, in general, those that used the deforested
countryside more, and we suggest that the key to their conservation
will be found there. Forest understory
insectivores, in general, have high habitat specificity, low mobility,
and are more confined to forest interior than other forest passerine
guilds, especially in the tropics where forest fragmentation and its
consequences are most dramatic ( 1– 5). Although over a dozen
hypotheses have been proposed to explain the disappearance of
insectivorous bird species from forested habitats around the world ( 2,
6), four of these are particularly relevant to explaining the decline
of understory insectivores. The food scarcity hypothesis states
that small fragments are impoverished in prey preferred by understory
insectivores ( 6– 8). The microclimate hypothesis proposes that these
birds are particularly sensitive physiologically to changes in
microclimate associated with forest fragmentation ( 2, 9). The habitat
specificity hypothesis states that the loss of some microhabitat
elements (such as army ant swarms, curled leaves, and dead trees) from
fragments may affect many understory insectivores negatively ( 2, 6).
Insectivores are more sensitive to such subtle changes because, unlike
fruits, flowers, and seeds, invertebrates actively avoid insectivores
and, as a result, insectivorous birds have evolved into many
specialized niches and seek prey in certain microhabitats. Finally,
according to the limited dispersal hypothesis, understory insectivores,
because of their relatively sedentary habits and possible psychological
avoidance of clearings ( 1, 10), may be less likely to disperse into
more favorable habitats after forest fragmentation and may disappear
from fragments as a result of stochastic events and other negative
consequences of fragmentation. Changes in invertebrate communities as a result of forest fragmentation
are well documented ( 11– 13). Leaf-litter and soil-dwelling
invertebrates decline as a result of desiccation in small forest
fragments and generalist edge species that prefer the dense vegetation
near fragment edges increase in number ( 12). Because many understory
insectivores forage in the dark and humid leaf litter in relatively
open understory and avoid dense vegetation ( 2), these changes can
diminish the birds' prey base. If the food scarcity hypothesis is
correct and a reduced resource base is the main reason for the decline
of insectivorous understory birds in smaller forest fragments, these
fragments should exhibit some combination of lower invertebrate
abundance and biomass. In addition, food limitation may be apparent in
the quantity and composition of invertebrates in the birds' diets.
Given the centrality of food availability to the reproductive success
of songbirds in general ( 14), we decided to test the food scarcity
hypothesis in tropical humid forest, where it has received relatively
little attention ( 15). Research Site. We tested our predictions by sampling birds, bird diets, and
invertebrates in large and small forest fragments near Las Cruces,
southern Costa Rica. Data were collected between 1 July 1999–15
September 2000, in Las Cruces Forest and three smaller forest fragments
(8°47′N, 82°57′W). These fragments are Pacific premontane
(elevation 1,100 m) humid forest surrounded by pastures, plantations of
coffee and other crops, and human settlements. The fragments have been
isolated since the mid-1950s. Las Cruces Forest is the largest
midelevation fragment in the region [227 hectares (ha)]; in it, we
established three study transects (referred to below as “forest
transects”) separated from each other by 400-1000 m. The small
primary forest fragments (4–5 ha) studied were 400–2,300 m from Las
Cruces Forest and there was a study transect in each small fragment
(referred to below as “fragment transects”). Each of the six
transects was 200-m long and within 150 m of the forest edge, to
control for “edge effects” ( 16). Sampling Birds. We mist-netted in each transect with 12 12-m, 36-mm mesh nets, for a
total of 82,944 m h divided evenly between forest and fragment
transects, following published methodology ( 17). Sampling Invertebrates. We sampled invertebrates with pitfall traps [Bioquip (Gardena,
CA) product no. 2838A] filled with equal parts of ethylene
glycol and water, sticky traps, 30 cm × 30 cm plastic sheets
covered with Tangle-Trap (Bioquip product no. 2870C), and timed
searches. With this combination, we were able to sample both passive
and actively moving invertebrates on various substrates. The traps were
placed randomly along transects. The 1-week pitfall traps were active
for 1 week, 2-week sticky traps were active for 2 weeks, and other
traps were active for 1 day. For searches, each 200-m transect was
divided into 40 5-m sections. Two people spent 5 min searching each
section for invertebrates in flight, in the leaf litter, and on
vegetation; invertebrates longer than 5 mm were captured with nets and
forceps and placed in 70% alcohol. We identified all invertebrates to
order and measured their lengths. For 1-week pitfall traps and
searches, we measured only invertebrates longer than 5 mm and obtained
the cumulative dry weight of all of the specimens in each order for
each sample-day. Bird Diet. We obtained diet samples from insectivorous and omnivorous birds by
using nonlethal 1.5% potassium antimony tartarate, based on
established protocol ( 18). The first author examined each regurgitate
under a stereo microscope and estimated the number, length, and weight
of prey items eaten based on a reference collection and published
regressions of weight on length ( 19). Invertebrates were identified to
order, except Formicidae (ants), which were identified to
family. For 14 understory insectivorous species that occurred both in
forest and fragment transects, we had at least four diet samples from
each treatment. That is the minimum number thought to offer adequate
representation of the diet of a species within a given time period
( 20), and for 11 of these species, we had at least 10 diet samples from
each treatment. Vegetation. At 30 randomly selected points in each transect, we measured canopy
closure by taking photos of the canopy from ground-level with a 17-mm
lens and later analyzing them with Adobe Systems (Mountain View, CA)
photoshop. We assessed distribution of canopy height by
measuring the height of the highest vegetation above these points with
a rangefinder. Bird Community. We mist-netted 1,202 birds in forest transects and 1,096 birds in
fragment transects, representing 116 species (nomenclature based on
ref. 21). Overall daily capture rates did not differ between forest and
fragment transects ( t = 1.50, P =
0.137), but certain guilds and forest-dependence classes showed
pronounced differences (Fig.
). Most large and
specialized insectivorous species, such as black-faced antthrush
( Formicarius analis) and ruddy woodcreeper
( Dendrocincla homochroa), did not occur along fragment
transects and many of the remaining insectivores, such as
white-breasted wood-wren ( Henicorhina leucosticta) and
white-throated spadebill ( Platyrinchus mystaceus), occurred
there in significantly lower numbers than along forest transects (see
Table 2, which is published as supporting information on the PNAS web
site, www.pnas.org). Insectivorous species were significantly fewer in
the fragments than in Las Cruces Forest ( t = 3.08,
P = 0.028), especially those species feeding on large
invertebrates and small vertebrates ( t = 4.01,
P = 0.008); insectivores feeding on small invertebrates
tended to be fewer as well ( t = 2.45, P
= 0.058). Both sampled and estimated species richness was higher along
forest transects for all species and for insectivores (Fig.
C). As in previous studies ( 1, 3, 4), we observed
significantly fewer species and individuals of understory insectivores
in small fragments and none of the ground-foraging or army
ant-following species were observed in those fragments.
Invertebrate Community. Individuals/sample, average length, and dry biomass/sample of
invertebrates varied between forest and fragment transects with no
overall pattern (Fig.
). When we compared
these variables for some invertebrate orders and classes, we again
found no overall differences between forest and fragment transects
(Table 1). Overall, numbers of
individuals/sample and dry biomass/sample values were about 15% lower
in forest samples, but the differences were not significant. Of 319
independent t tests comparing individuals/sample, average
length, and dry biomass/sample values between forest and fragment
transects for different invertebrate taxa sampled with various methods,
69 tests were significant and greater values were almost equally
distributed between forest (35/69) and fragment transects (34/69).
These tests do not pose a multiple comparison problem because the null
hypothesis for each test was different ( 25).
| Table 1The distribution of significantly greater values of
invertebrate measures between forest and
fragment transects |
There were, however, two discernible trends. First, all eight
significantly greater values for Diptera were from fragment transects.
Second, a number of mainly forest floor/leaf-litter groups [such as
Annelida, Blattaria, Collembola, Decapoda (forest crabs), Dermaptera,
Isopoda, Mollusca, and Thysanura], which comprised 7.3% of the
individuals and 12.5% of the biomass sampled, were somewhat better
represented along forest transects. There were also significantly more
army ant (Eciton burchelli) swarms during searches along
forest transects (7 of 8 encounters, binomial test, P =
0.0313). Bird Diet. In bird diet samples, Coleoptera, Orthoptera, Formicidae, and Arachnida
were the most common prey, comprising about 75% of the individuals
found in diet samples. The taxonomic distribution of prey items in
forest and fragment diet samples did not differ significantly for any
bird group (all χ2 < 11.91, all
P > 0.99). Overall, estimated dry weight of invertebrates was not significantly
different between forest and fragment diet samples (F =
2.60, P = 0.108; two-factor ANOVA with origin of sample
and species as factors). The average number of prey items/diet sample (all t <
1.64, all P > 0.156) and estimated dry weight ( 19) of
consumed prey (all t < 1.60, all P >
0.111) values, although greater in general in forest samples, did not
differ significantly between forest and fragment samples for any of the
14 species with enough diet samples from both treatments (Table 3,
which is published as supporting information on the PNAS web site).
Even though the average lengths of invertebrates in diet samples were
greater in the forest samples of 11 species, the values differed
significantly only for Henicorhina leucosticta
( P = 0.016) and Sittasomus griseicapillus
( P = 0.008). When we compared the diet samples obtained in Las Cruces Forest of
insectivorous species present and absent from small fragments, prey
taxonomic distribution did not differ significantly for insectivores
with large prey (χ2 = 0.58, P
> 0.99) or with small prey (χ2 = 0.36,
P > 0.99). Nor did the estimated dry weight of
consumed prey of insectivores with large prey (t =
0.005, P = 0.996) or with small prey (t
= 0.262, P = 0.793). Vegetation Structure. Neither canopy closure (F = 0.414, P >
0.5) nor canopy height distribution (χ2 =
15.15, P > 0.1) differed significantly between forest
and fragment transects. Average canopy closure was around 80% for all
transects. Although there were significantly fewer understory
insectivores in small fragments, invertebrate abundance, average
length, and dry biomass values along forest and fragment transects were
surprisingly close. We obtained similar results from examination of
bird diets, with no significant differences in diet composition,
biomass, or prey items per sample, and only 2 of 14 bird species
exhibited significant differences in average length of invertebrates
eaten. Even though the significant reduction in army ant swarms in
small fragments may affect the three army ant-following species
negatively, the food scarcity hypothesis does not seem to be supported
as the primary cause of the disappearance of understory insectivorous
birds from small forest fragments around Las Cruces. This finding
differs from the findings of two recent studies in the temperate zone
where increased food abundance in larger forest fragments was
positively correlated with the abundance and reproductive performance
of the two understory insectivorous bird species studied ( 7, 8). The microclimate hypothesis, which states that sedentary understory
insectivores react more unfavorably to microclimate fluctuations in
forest fragments than more mobile species that are frequently exposed
to different microclimates, was not tested by our observations. We
tried to control for microclimate differences by sampling only near
forest edges, but this does not preclude the possibility that
understory insectivores in larger fragments may forage near edges and
seek shelter in the forest interior when climatic conditions become
intolerable. With respect to the habitat specificity hypothesis, some understory
insectivorous species may have disappeared from fragments because of
the reduction or disappearance of some critical habitat elements, such
as army ant swarms. However, the small fragment where we sometimes
observed army ant swarms (although only once during invertebrate
sampling) was also missing army ant-following bird species absent from
other fragments, and a number of bird species missing from small
fragments feed on invertebrate resources that were not significantly
different between forest and fragments sites. Thus, this hypothesis is
tentatively rejected. Dispersal, crucial in the colonization of habitat islands ( 26,
27), may be the key mechanism that makes it more likely that small and
short-lived bird species will go extinct as a result of habitat
fragmentation compared with large and long-lived species ( 28, 29).
Likewise, the limited dispersal capabilities of understory insectivores
( 1, 2) may be the most important factor in their sensitivity to
fragmentation. At our site, presence of a bird species in the
deforested open countryside around forest fragments was the best
determinant of its occurrence in smaller fragments, in agreement with
the limited dispersal hypothesis. Of the 18 species (15 insectivorous)
we caught significantly more times along Las Cruces Forest transects
than along fragment transects, only two (one insectivorous) were
detected in nonforest habitats in a separate study ( 30). In that study,
the average detection rate in nonforest for these 18 species was 0.0005
individuals/person-hour (3 of 5,007 observations) and none of the six
insectivorous species feeding on large prey were found in nonforest
habitats. Conversely, of the 12 species we caught significantly more
frequently along fragment transects (three insectivorous, all feeding
on small prey), 9 were present in nonforest ( 30), and the average
detection rate in nonforest was 0.296 individuals/person-hour (1,172 of
5,007 observations). Only one of these nine species was insectivorous
and it accounted for 1.8% of the observations. These detection rates
were significantly different (Mann–Whitney U test,
P = 0.004), and insectivores, especially those feeding
on large prey, were significantly under-represented both in forest
fragments and in nonforest habitats. There was also a significant positive correlation
( r2 = 0.714, P <
0.0001) between the number of species of a bird family present in
nonforest habitats ( 30) and the number of species of that bird family
present in small fragments (Fig. ).
Thus, ability to move through and possibly forage in deforested
habitats around forest fragments may link small populations that would
otherwise be isolated and vulnerable to edge effects and stochastic
events. This mobility may greatly enhance the “rescue effect”
( 31) and thus improve the survival chances of forest-dependent
organisms in forest fragments, as was observed in previous studies ( 1,
32). In addition, forest bird species frequently detected in the matrix
surrounding forest fragments are also likely to be more tolerant of
ecological changes in fragments, such as those resulting from edge
effects ( 16, 33), and may be more capable of occasionally foraging and
even nesting in some matrix habitats near fragments.
Thus, the limited dispersal hypothesis is best supported by our
study. Inability to use deforested countryside habitats, rather than
food scarcity in fragments, seems to be the major cause of the decline
of understory insectivores in forest fragments around Las Cruces. The
actual mechanism of decline, whether it is increased nest predation,
changes in microclimate, negative stochastic effects caused by small
population size, or a combination thereof, remains to be elucidated.
Although forest fragmentation and other forms of habitat disturbance
may reduce the breeding success of most forest bird species equally,
possibly as a result of increased nest predation of all species ( 33),
more sedentary species may be less able than other birds to
“commute” through nonforest from their breeding territories to
small fragments containing sufficient resources. Such regular
“commuting” from nesting areas to foraging areas that are
unsuitable for nesting has been observed in frugivorous bats in Mexican
lowland tropical forest fragments (M. Evelyn, unpublished data).
Increased mobility increases the chances of renesting in fragments if
conditions become more favorable, making it less likely that more
vagile species will become locally extinct. In addition, forest bird
species that are likely to move through nonforest habitats are more
likely to occasionally use those habitats for foraging and nesting,
mitigating the effects of fragmentation. Sedentary behavior can also
explain the decline of understory insectivores in unfragmented but
otherwise disturbed forests ( 2, 5). More research comparing the movement, foraging, and breeding patterns
of understory insectivores and other guilds in both forest fragments of
various sizes and in open countryside is needed to reveal the actual
mechanism(s) of the disappearance of understory insectivores.
Meanwhile, better integration of agricultural/human-dominated habitats
into conservation strategies, such as linking forest fragments with
shade coffee plantations, fence rows, and windbreaks composed of native
tree species, may make deforested areas more hospitable to understory
insectivores and other fragmentation-sensitive groups by enabling them
to disperse between forest fragments and prevent local extinctions. We thank the Costa Rican government and the Organization for
Tropical Studies for allowing us to work at Las Cruces Biological
Research Station (LCBRS), the staff of LCBRS for their support, and Tom
Davis, Forrest Fleischmann, Angelina Sanderson, Jason Sandí,
Jeisson Sandí, Audrey Tapia, and Parker VanValkenburgh for their
help with field work. We thank Walter Loewenstern and Thomas Brokaw for
graduate fellowships, the Bing undergraduate research fund, Sigma Xi
Grant-in-Aid of Research, the Winslow Foundation, and Peter and Helen
Bing for support. We appreciate critical comments from Richard
Bierregaard, Carol Boggs, Chris Canaday, Marcus Feldman, Oliver Komar,
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