BIOTROPICA 39(4): 489–495 2007
10.1111/j.1744-7429.2007.00285.x
Cutting More from Cut Forests: Edge Effects on Foraging and Herbivory
of Leaf-Cutting Ants in Brazil
Pille Urbas1,3 , Manoel V. Araújo Jr.2 , Inara R. Leal2 , and Rainer Wirth2
1 Plant
Ecology & Systematics, University of Kaiserslautern, PO-Box 3049, 67663 Kaiserslautern, Germany
2 Departamento
de Botânica, Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/no, 50670-901 Recife, PE, Brazil
ABSTRACT
Edge-mediated changes in species composition are known to result in modified species interactions. Because of the crucial trophic position of herbivores and their
far-reaching impact on plant communities, it is important to understand how edge influences herbivory. In the present paper, we investigated whether and how
leaf-cutting ant foraging is altered in the forest edge, as this habitat is characterized by an increased proportion of pioneer species. We assessed basic foraging data as
well as the herbivory rate (i.e., the proportion of the leaf material harvested by a colony in relation to the available leaf area in the foraging area) of Atta cephalotes
colonies at the edge versus interior sites of a large remnant of the Atlantic forest in Northeast Brazil. Our results indicated clear edge effects on leaf-cutting ants: equally
sized A. cephalotes colonies located at the forest edge removed about twice as much leaf area from their foraging grounds than interior colonies (14.3 vs. 7.8%/col/yr).
This greater colony-level impact within the forest edge zone was a consequence of markedly reduced foraging areas (0.9 vs. 2.3 ha/col/yr) and moderately lower leaf
area index in this habitat, whereas harvest rates were the same. Our results suggest that forest edges induce increased leaf-cutting ant herbivory, probably via the release
of resource limitation. Together with the increase of leaf-cutting ant populations along forest edges, this may amplify environmental changes induced by habitat
fragmentation.
Key words: Atlantic forest; Atta cephalotes; bottom-up control; foraging area; Northeast Brazil.
DESTRUCTION OF NATURAL HABITATS, HABITAT LOSS, AND FRAGMENTATION have become the most important threats to biodiversity and
ecosystem function worldwide (Gascon et al. 2001). Today, tropical
deforestation exceeds 150,000 km2 annually, leading to an alarming
rate of forest fragmentation (Whitmore 1997). Fragmentation leads
to a drastic increase in the extent of forest edge, and the increased
edge/forest interior ratio is thought to be one of the main driving
forces behind the striking physical and biological changes in fragmented versus continuous forests (e.g., Saunders et al. 1991, Murcia
1995). Abiotic edge effects include microclimatic alterations near
edges, such as reduced humidity, greater temperature variability,
increased light penetration, and wind disturbance relative to the
forest interior (reviewed in Laurance et al. 2002). These changes in
the physical environment accompany modifications in forest structure and species composition along the forest edges, although the
specific responsible mechanisms may be complex and often remain
poorly understood. For example, wind damage and habitat desiccation in edge habitats may lead to sharply elevated rates of tree
mortality (Lovejoy et al. 1986, Ferreira & Laurance 1997) that in
turn result in increased gap formation and light penetration into
the forest understory (Laurance et al. 1998a, Rankin-de-Mérona
& Hutchings 2001). As a consequence, trees regenerating within
forest edge zones are significantly biased toward fast-growing pioneer species and against shade-tolerant forest species (Laurance
et al. 1998a, b; Oliveira et al. 2004).
Such direct edge effects (sensu Murcia 1995) inevitably cause
higher-order biotic effects with possible repercussions for ecosystem
Received 13 April 2006; revision accepted 2 September 2006.
Current address: Institute of Botany and Ecology, University of Tartu, Lai 40,
Tartu 51005, Estonia.
4 Corresponding author; e-mail: [email protected]
3
functioning (Laurance et al. 2002). Hence, edge-mediated changes
in species composition may result in modified species interactions,
as has been shown for modified patterns of parasitism, predation,
seed dispersal, and pollination (Murcia 1995, Didham et al. 1996,
Laurance et al. 2002, Tscharntke et al. 2002). Despite the crucial
position of herbivores in the trophic web of ecosystems and their
far-reaching impact on plant community dynamics (Huntly 1991),
edge effects on herbivory have rarely been investigated. It is widely
believed that herbivory levels are higher in edge versus interior forests
(Murcia 1995, Fagan et al. 1999, Laurance et al. 2002), but empirical
data are surprisingly scarce and rather inconsistent (Cadenasso &
Pickett 2000, Benitez-Malvido 2001, Benitez-Malvido & LemusAlbor 2005). The available evidence is often indirect because it refers
to increased abundance of herbivores (Sork 1983, Lovejoy et al.
1986, Barbosa et al. 2005) or to studies on forest fragments rather
than edges of continuous forests (Rao 2000, Arnold & Asquith
2002).
Leaf-cutting ants (LCA) are dominant herbivores in the
neotropics and play an important role in structuring forest
communities (Wirth et al. 2003). In the last decades, LCA colony
density has been reported to increase sharply in secondary forests
(e.g., Vasconcelos & Cherrett 1995, Moutinho et al. 2003), in small
forest fragments (Vasconcelos 1988, Rao 2000), and along forest edges (Wirth et al., in press). A proposed mechanism for high
colony densities in secondary forests and forest fragments is the high
availability of pioneers (i.e., the “palatable forage hypothesis” sensu
Farji-Brener 2001), which are known as preferred food plants of
LCAs (e.g., Wirth et al. 2003).
In the present study, we investigated whether and how LCA
foraging is influenced by edge, as this habitat is characterized by
an increased proportion of pioneer species. We expected that the
C 2007 The Author(s)
C 2007 by The Association for Tropical Biology and Conservation
Journal compilation 489
490
Urbas, Araújo Jr., Leal, and Wirth
colonies reduce the foraging effort and increase leaf harvest and
herbivory rate (i.e., the proportion of leaf material removed from
the available foliage in the forest canopy). More specifically, we
tested if LCA colonies at the forest edge: (1) use a smaller foraging
area; (2) harvest more plant material; and consequently (3) increase
herbivory in the corresponding foraging area. To examine these
hypotheses, we compared LCA foraging and stand-level herbivory
in colonies in the forest edge zone versus colonies in the interior of
a large remnant of Atlantic rainforest in Northeastern Brazil.
METHODS
STUDY SITE.—We conducted our study in the state of Alagoas,
Northeast Brazil (9◦ S, 35◦ 52 W) at the Usina Serra Grande, a
22,000-ha private sugar-cane farm. The area holds 9000 ha of forest
comprising dozens of fragments, all of them completely surrounded
by sugar-cane fields. The largest fragment, locally known as Coimbra, covers 3500 ha and is considered the single largest remnant of
the Northeastern Atlantic forest (Oliveira et al. 2004). Coimbra is
an old fragment (at least 60 yr), currently lacking any large-scale
human disturbance. Its 40 km of borders represent relatively stable
environments because they consist of dense, old second growth, and
are therefore particularly suitable for assessing the long-term effects
of edge creation (Saunders et al. 1991).
Coimbra is located on the low-elevation plains (500–600 m
asl) of the Borborema Plateau, a mountain chain stretching north
and south along the northeastern coast of Brazil. The prevailing
soils of the study area are latosols and podzols (IBGE 1985).
Annual rainfall is ca 2000 mm (data provided by Usina Serra
Grande), with a 5-mo dry season (<110 mm/mo) from September
to January. The vegetation largely consists of well-conserved oldgrowth forest and has been classified as lower mountain rain forest,
with Leguminosae, Lauraceae, and Sapotaceae as the richest
families in terms of tree species (Tavares et al. 1971). The forest
is surrounded by plantations of sugar cane and the edge zone has
been shown to be largely dominated by pioneer species. Of 134 tree
species identified in Coimbra, Oliveira et al. (2004) found twice as
many pioneer species along the 100-m edge zone as compared to the
forest interior (83% vs. 37%). Pioneers represented over 90 percent
of the adult trees at the edge and 27 percent in the forest interior
(Grillo 2005).
STUDY SPECIES.—We studied Atta cephalotes, one of the most common LCA species in the region (Corrêa et al. 2005). Atta cephalotes
has a wide distribution, from Mexico to the Amazon, with an additional disjunct occurrence in NE Brazil (Kempf 1972, Corrêa et al.
2005). The species builds compact nests that are easy to define and
monitor. Unlike other Atta species, which prefer open and disturbed
habitats, A. cephalotes is known as a “woodland species” commonly
found in mature or old-growth forests (Rockwood 1973). In 42
forest fragments surveyed in the Northeastern Atlantic forest, A.
cephalotes was strongly associated with well-conserved remnants including Coimbra (Corrêa et al. 2005). Within the large forest remnant of Coimbra, the vast majority of the LCA colonies (including
A. sexdens) are located in a 100-m edge zone, with the density of
Atta spp. about six times higher in the forest edge zone than in the
forest interior (Wirth et al., in press).
In this study, we did not include Atta sexdens, the second common LCA species in the area, because it builds nests with widely
scattered entrance holes and subterraneous foraging galleries (Vasconcelos 1990), so that dependable monitoring of foraging trails
and harvested plant material was not possible.
STUDY DESIGN.—To investigate putative edge effects on foraging
performance of A. cephalotes, we assessed the foraging area, the
foraging trail length, the available leaf area, the harvest rate, and the
herbivory rate of ten adult colonies, five at the forest edge (hereafter
“edge colonies”) and five in the forest interior (“interior colonies”).
Edge colonies were chosen within 100 m from the forest border
(sensu Laurance et al. 1998a) along different portions of the 40 km
perimeter of the Coimbra forest. The distance among the studied
edge colonies was 2.0 ± 1.4 km (mean ± SD). Interior colonies were
located more than 200 m from the forest margin, with inter-colony
distances averaging 1.1 ± 0.4 km. The colony sites were chosen to
include the considerable variation in vegetation composition and
structure in different stretches of this large forest remnant. We
selected equally sized colonies across the two habitats, so that nest
surface areas of edge and interior colonies did not differ (mean ±
SD: 79.0 ± 44.7 m2 and 92.4 ± 24.26 m2 , respectively; t =
0.59, P = 0.57, df = 8). The same nest size suggests that colonies
were approximately even-aged, and the size of a LCA nest typically
correlates with the foraging area of a colony (Bitancourt 1941).
All variables (see below) were measured in bimonthly intervals
over a period of one year from September 2002 until August 2003
during the colony-specific time peak of daily activity. Peak activity
was preliminarily determined by a single 24-h count of harvest rate
per colony (Wirth et al. 1997) and constantly checked throughout the study. One interior colony died during the study and was
therefore excluded from the analysis.
FORAGING TRAILS AND FORAGING AREA.—To obtain an estimate of
the annual foraging area of the colonies, we monitored their foraging trails throughout the study year. Long-term foraging activities
of Atta colonies are largely focused along the trunk trail system,
which makes up only parts of the potentially available foraging
range around the nest (Wirth et al. 2003, Kost et al. 2005). Each
bimonthly survey of the foraging trails was conducted during a
single observation day around the colony-specific time peak of daily
activity. All active foraging trails were followed up to the cutting
site or the location where ants ascended into the canopy. The trails
were charted by measuring compass bearings and lengths of all
quasi-linear trail segments (the total of which is hereafter referred to
as “foraging trail length”). Maps of the foraging trail systems were
generated using the software package Corel Draw 8.0 (Corel Corporation, Ottawa, Canada). To determine the annual foraging area
of a colony, we delineated a 20-m zone around all trails, and superpositioned the six bimonthly contour maps to generate an overall
annual trail map. The 20-m width has been considered a reasonable
approximation of the mean expansion of LCA harvesting zones (see
Edge Effects on Leaf-Cutting Ant Foraging
Wirth et al. 2003 for more details on the estimation of LCA foraging
areas).
AVAILABLE LEAF AREA.—To assess the foliage area available to an LCA
colony, we estimated the leaf area index (LAI, total one-sided area of
leaves per unit ground surface area) by means of digital hemispherical photographs (Frazer et al. 2001). Hemispherical photographs
capture the light obstruction/penetration patterns in the canopy
and supply gap fraction data that calculate LAI by mathematical inversion of a light interception model (Norman & Campbell 1989,
Chen & Black 1992). We sampled LAI within the putative foraging
range of the colonies along two pairs of parallel north–south transects (80 m long, spaced 20 m apart). Each pair was set up 20 m
west and east of the nest in order to avoid the impact of the
vegetation-free nest area on LCA nests (Farji-Brener & Illes 2000).
Along each transect, five hemispherical photos were taken at 20-m
intervals, resulting in a total of 20 photos per colony. Measurements
were taken once during nine consecutive days in early December
2002. Large-scale seasonal changes of LAI are negligible in semideciduous forests (Wirth et al. 2001). Photos were taken 1 m above
ground level (Nikon Coolpix 990 with FC-E8 fisheye converter)
at dawn before sunrise or at dusk after sunset to avoid direct solar
radiation in any part of the canopy (Whitmore et al. 1993). The
photographs were analyzed using the image analysis software Gap
Light Analyzer 2.0 (Frazer et al. 2001). Each photograph was analyzed twice to compensate for any subjective aspect of the threshold
adjustments. For the final LAI values, the estimates of the effective
LAI integrated over the zenith angles 0◦ to 60◦ (LAI 4 Ring) were
used (Frazer et al. 2001).
The standing foliage was calculated as the product of LAI and
the foraging area (see above). To calculate the available leaf area, the
leaf area harvested by the colony was added to the standing foliage,
assuming no compensatory growth (Wirth et al. 2003).
491
of each active foraging trail (see Wirth et al. 1997). The first 300
leaf fragments from this combined sample were then analyzed. The
area of the harvested leaf fragments did not differ between the wet
(mean ± SD: 1.38 ± 0.16 cm2 ) and dry season (1.41 ± 0.08 cm2 ,
paired t-test, t = −0.94; P = 0.37, df = 9). Therefore, the annual
mean for each colony was used in further calculations.
HERBIVORY RATE.—The herbivory rate of A. cephalotes colonies was
assessed as the leaf area harvested by a colony relative to the leaf
area available in the annual foraging area (see above, sensu Wirth
et al. 2003). Similarly to the leaf harvest rates, the daily totals of the
herbivory rate were extrapolated to achieve bimonthly values for the
corresponding two months. The bimonthly values were summed to
yield an annual estimate.
STATISTICAL ANALYSIS.—To test for edge effects on the annual foraging area, foraging trail length, annual harvest, and herbivory rates,
we performed one-way ANCOVAs with habitat as the main factor,
and nest surface area as a covariable. A t-test was used to analyze
habitat differences of LAI. Additionally, we analyzed for effects of
sampling time on LCA harvest and herbivory rates using a repeatedmeasure ANCOVA with sampling time (September, November,
January, March, May, July) as a repeated measure factor, habitat as
the main factor, and nest surface area as a covariable. Data on foraging area, foraging trails, and available leaf area were log-transformed
and data of monthly herbivory rate were square-root-transformed
to comply with the assumptions of normality and homoskedasticity.
We report untransformed means for these variables in the Results
section. All procedures are properly described in Zar (1999), and
analyses were carried out using STATISTICA v. 5.1 (StatSoft Inc,
Tulsa, OK, U.S.A.).
RESULTS
LEAF HARVEST RATE.—Leaf harvest rates were obtained from estimates of daily leaf intake into the ant nests during a single observation day. Daily totals were predicted from instantaneous foraging
rates at the time peak of daily activity (Wirth et al. 1997, 2003).
We previously established a linear regression equation relating 24-h
counts of leaf fragments to the respective 5-min counts at the daily
foraging peak based on seven A. cephalotes colonies (fragments 24h =
672.45 fragments 5min = 14863; R2 = 0.917, P = 0.0036, N =
7). Short-term foraging rates were then obtained for each study
colony by counting laden ants passing a fixed point close to the nest
entrance of each foraging trail for five minutes. The daily totals of
the leaf harvest were extrapolated to achieve bimonthly values for
the corresponding two months. These bimonthly values were then
summed to estimate the annual rate of leaf harvest.
To calculate the annual leaf area harvested, the total number
of harvested leaf fragments was multiplied by the average area of
the leaf fragments. Average leaf fragment area was determined for
two samples of 300 harvested leaf fragments per colony (during
wet and dry season, respectively) using a leaf area meter (LI 3050
A, LI-COR Inc, Lincoln, NE, U.S.A.). The samples were collected
using a rechargeable vacuum cleaner for 2 min close to the entrance
Foraging trail length of A. cephalotes colonies varied from 41m to
529 m. At the forest edge, foragers traveled about half as far than in
the forest interior (F 1,6 = 8.61, P = 0.026; Fig. 1A). This reduced
foraging trail length translates into a significantly smaller (less than
half ) annual foraging area of edge colonies as compared to interior
colonies (F 1,6 = 14.93, P = 0.008; Fig. 1B).
The LAI estimated for forest stands around the study colonies
ranged from 3.96 to 4.62 m2 /m2 . At the forest edge, mean LAI
was slightly (< 10%) but significantly smaller than in the interior
(t [7] = 4.67, P = 0.002; Fig. 1C). Because of the smaller foraging
area (Fig. 1B), however, the amount of the leaf area available to a
colony in the foraging area was drastically lower at the forest edge
than in the interior (F 1,6 = 18.71, P = 0.005; Fig. 1D).
The total leaf area consumed by a colony during one year varied
from 4721.55 to 10,916.9 m2 with no significant habitat-related
differences (F 1,6 = 0.59, P = 0.47; Fig. 1E). But mean monthly
leaf harvest varied markedly throughout the year (effect of sampling
time: F 5,35 = 4.25, P = 0.004; Fig. 2A). In both habitats, mean
monthly harvest rates were highest in January, the peak of the dry
season (Fig. 2A).
492
Urbas, Araújo Jr., Leal, and Wirth
FIGURE 1.
Estimated means (± SD) of foraging trail length (A), annual foraging area (B), leaf area index (C), available leaf area (D), annual leaf harvest rate (E),
and annual herbivory rate (F) of Atta cephalotes colonies at the forest edge (N = 5) and interior (N = 4) of a remnant of the Atlantic forest in Northeast Brazil.
Finally, when relating leaf harvest to the available leaf area of
a colony we achieved annual herbivory rates ranging from 4.69 to
19.21 percent. Atta cephalotes colonies located at the forest edge
removed about twice as much leaf area from their foraging grounds
as interior colonies (F 1,6 = 10.87, P = 0.016; Fig. 1F). Again, there
was significant temporal variation (effect of sampling time: F 5,35 =
2.63, P = 0.04; Fig. 2B), with the highest herbivory during January
and March. The interaction between habitat and time was nonsignificant for both harvest and herbivory rates. The effect of the
covariate (nest surface area) was not significant in any of the above
analyses of covariance.
DISCUSSION
Our results show clear and significant forest edge effects on the
foraging behavior of LCAs. The single most important finding was
that herbivory by A. cephalotes colonies considerably increased at
the edge of the forest. This greater colony-level impact was not a
consequence of increased harvesting rates but of markedly reduced
foraging areas per colony and moderately lower LAI in this habi-
tat. Considering the fact that high population densities of LCA
are closely associated with forest fragmentation, edge creation, and
disturbance, our results may have important implications for the
overall impact of LCA.
Our first hypothesis is corroborated by the observation that
annual foraging areas of A. cephalotes colonies decreased from more
than 2 ha in the forest interior to around 1 ha in the forest edge
zone. This reduction of foraging areas can be plausibly explained by
the greater abundance of palatable plants (e.g., Quinn et al. 1997).
In fact, at the edge of the studied forest, pioneers dominate in
terms of species and stem number. Of 134 tree species identified at
the study site, Oliveira et al. (2004) found twice as many pioneer
species along the edge as compared to the forest interior (83% vs.
37%), and pioneers represented over 90 percent of the stems of
adult trees at the edge (vs. 27% in the interior; Grillo 2005). An
inverse relationship between resource density and foraging area is
consistent with predictions of the optimal foraging theory (Ford
1983) and is well documented in various groups of animals (e.g.,
Jorge & Peres 2005), including lower attine ants (Leal & Oliveira
2000), and Atta (Rockwood 1973). On the other hand, reduced
foraging areas could be a result of increased intraspecific competition in high-density populations (Bernstein 1975). However, if
Edge Effects on Leaf-Cutting Ant Foraging
FIGURE 2.
Estimated monthly means (± SD) of leaf harvest rate (A), and
herbivory rate (B) of Atta cephalotes colonies at the forest edge (N = 5) and
interior (N = 4) of a remnant of the Atlantic forest in Northeast Brazil.
such competition for resources occurred, harvesting success should
be limited in high-density edge habitats and hence a colony at the
edge should harvest less than its equally sized counterpart in the
forest interior. Consequently, our findings of equal colony harvest
rates, together with high resource density, provide convincing evidence of smaller spatial requirements of LCA foraging along the
forest edge, although we cannot entirely rule out the possibility of
intraspecific competition. Exclusion experiments would be necessary to conclusively evaluate this possibility, yet the LCA system is
hardly amenable to this approach.
Pioneers are highly palatable to LCA (Farji-Brener 2001) and
generally known to have lower levels of quantitative defenses and
higher nutritive status than shade-tolerant species (Coley 1980).
As a consequence, workers do not have to travel far to find their
food plants, and can therefore restrict foraging to a smaller area
(this work), or to a narrower diet breadth (Shepherd 1985, Wirth
et al., in press). Thereby, the edge habitat allows LCA colonies a
significant reduction of the overall foraging costs. Interestingly, and
contrary to our prediction (hypothesis 2), colonies at the forest edge
did not make use of this situation by collecting greater quantities of
both leaf area and biomass (data not shown). Whether the resulting
surplus of energy can be allocated to other life processes such as
growth or reproduction (cf. Karsai & Wenzel 1998), thus allowing
increased colony fitness in high-resource environments, remains
open to further research.
493
The third hypothesis of edge effects on herbivory by LCA can
also be accepted and adds empirical evidence to the widely held but
poorly documented view, that herbivory levels are higher in edge
versus interior forests (Murcia 1995, Fagan et al. 1999, Laurance
et al. 2002). We showed that the annual proportion of leaf material
removed from the standing leaf crop within the foraging area almost
doubled from 7.8 percent for interior colonies to 14.4 percent for
edge colonies. To date, Atta herbivory has not been estimated in
edge vs. interior forest habitats, despite the immense importance
of several Atta species as herbivores and their well-known association with natural and man-made disturbances (e.g., Vasconcelos &
Cherrett 1995, Moutinho et al. 2003). Published estimates of LCA
herbivory are only available for single colonies and/or habitats (e.g.,
Lugo et al. 1973, Blanton & Ewel 1985, Wirth et al. 2003), and
the results vary largely depending on the scale (e.g., plant-, colony-,
or landscape level) and the methodological approaches used (see
Wirth et al. 2003 for detailed discussion). The increased herbivory
of edge vegetation was largely due to the considerable reduction of
the colony foraging area, and to a lesser extent to the lower LAI
at the forest edge. Lower LAI in early-successional forests has been
explained by decreased forest complexity (Kalácska et al. 2004).
Along the forest edge, increased tree mortality and the abundance
of light gaps (Saunders et al. 1991, Laurance et al. 1998a) may also
contribute to lower LAI, but explicit information about edge effects
on LAI in tropical forests is presently lacking.
Our study has several implications. First, the fact that edge
colonies removed equal amounts of plant material from much
smaller foraging areas than interior colonies suggests that the damage level per ha of foraging area rises significantly. In other words,
edge forests experience a spatial concentration of LCA damage. Together with the higher number of LCA colonies along the forest edge
(Wirth et al., in press), this increased colony impact becomes relevant at the landscape scale. If we assume that higher herbivory levels
result from the increased abundance of pioneer species, it is plausible
to expect that our findings generally apply to disturbed/secondary
forests, where high Atta densities are also well documented (Vasconcelos & Cherrett 1995, Rao 2000, Moutinho et al. 2003).
Second, our results imply a considerable role for resource availability in the regulation of LCA populations (i.e., bottom-up control). The increased proportion of highly palatable pioneer species
at the edge of the studied forest (Oliviera et al. 2004), smaller
colony foraging areas, and increased herbivory rates suggest a reduced strength of bottom-up forces in this habitat. Enhanced herbivory in small fragments or edge habitats has often been attributed
to the release of consumer-driven (i.e., top-down) forces (Lovejoy
et al. 1986, Kareiva 1987, Kruess & Tscharntke 1994) and the
loss of natural enemies has been regarded as the primary cause for
high Atta densities (Rao 2000, Terborgh et al. 2001). Such effects
have also been shown at the study site, where edge colonies experienced significantly fewer attacks by parasitic phorid flies than
interior colonies (Almeida 2004). As an additional mechanism, we
suggest that edge creation and habitat fragmentation contribute significantly to increased herbivory via the attenuation of bottom-up
forces. We believe that this is especially true for generalist herbivores
because Atta species are among the most polyphagous herbivorous
494
Urbas, Araújo Jr., Leal, and Wirth
insects known (Lugo et al. 1973, Wirth et al. 2003), and generalist
herbivores are known to benefit from early-successional (Coley &
Barone 1996), less defended plant species (Coley 1980). Whether
the reduced strength of bottom-up forces is more relevant in edge
habitats, while top-down factors may predominate in small fragments, with only a subset of predators, should be addressed in
future research.
Finally, if the above interpretation of less bottom-up control
of LCA populations in edge habitats holds, we expect a synergism
between anthropogenic edge creation and LCA activities leading to
detrimental consequences for fragmented neotropical forests. On
the one hand, edge creation and fragmentation of tropical rain
forests are pervasive (Whitmore 1997) and secondary habitats support more LCA colonies (Vasconcelos & Cherrett 1995, Rao 2000,
Moutinho et al. 2003, Wirth et al., in press). On the other hand,
increased colony densities along with increased herbivory rates are
expected to amplify the environmental changes suffered by the
edge habitat in the case higher herbivory promotes increased light
penetration and consequently greater variation in temperature and
humidity (see Laurance et al. 2002 for a review). In synthesis, we
suggest that edge creation promotes high LCA density, which, in
turn, reinforces the deleterious effects of forest fragmentation.
ACKNOWLEDGMENTS
The study was supported by German Science Foundation (DFG,
project WI 1959/1-1), Fundação Coordenação de Aperfeiçoamento
de Pessoal de Nı́vel Superior (CAPES, project 007/01), and
Conselho Nacional de Desenvolvimento Cientı́fico e Tecnológico
(CNPq, project 540322/01-6). We thank Conservation International do Brasil, Centro de Estudos Ambientais do Nordeste and
Usina Serra Grande for providing infrastructure during the field
work. Many thanks to Marcelo Tabarelli, Bettina Engelbrecht, Heraldo Vasconcelos, and two anonymous reviewers for valuable comments on the manuscript.
LITERATURE CITED
ALMEIDA, W. R. 2004. Fragmentação florestal: redução no controle da formiga
cortadeira Atta cephalotes por moscas parasitóides. MSc thesis. Universidade Federal de Pernambuco, Recife, Brazil.
ARNOLD, A. E., AND N. M. ASQUITH. 2002. Herbivory in a fragmented tropical
forest: Patterns from islands at Lago Gatun, Panama. Biodiv. Conserv.
11: 1663–1680.
BARBOSA, V. S., I. R. LEAL, L. IANNUZZI, AND J. ALMEIDA-CORTEZ. 2005.
Distribution pattern of herbivorous insects in a remnant of Brazilian
Atlantic forest. Neotrop. Entomol. 34:1–11.
BENITEZ-MALVIDO, J. 2001. Regneration in tropical rainforest fragments. In R.
O. Bierregaard Jr., C. Gascon, T. E. Lovejoy, and R. Mesquita (Eds.).
Lessons from Amazonia. The Ecology and Conservation of a fragmented
forest, pp. 136–146. Yale University Press, New Haven, Connecticut.
BENITEZ-MALVIDO, J., AND A. LEMUS-ALBOR. 2005. The seedling community
of tropical rain forest edges and its interaction with herbivores and
pathogens. Biotropica 37: 301–313.
BERNSTEIN, R. A. 1975. Foraging strategies of ants in response to variable food
density. Ecology 56: 213–219.
BITANCOURT, A. 1941. Expressão matemática do crescimento de formigueiros
de Atta sexdens rupropilosa representado pelo aumento do numero de
olheiros. Arq. Inst. Biol. São Paulo 12: 229–236.
BLANTON, C. M., AND J. J. EWEL. 1985. Leaf-cutting ant herbivory in successional and agricultural tropical ecosystems. Ecology 66: 861–869.
CADENASSO, M. L., AND S. T. A. PICKETT. 2000. Linking forest edge structure
to edge function: Mediation of herbivore damage. J. Ecol. 88:31–44.
CHEN, J. M., AND T. A. BLACK. 1992. Defining leaf area index for non-flat
leaves. Plant Cell Environ. 15: 421–429.
COLEY, P. D. 1980. Effects of leaf age and plant life history patterns on herbivory.
Nature 284: 545–546.
COLEY, P. D., AND J. A. BARONE. 1996. Herbivory and plant defenses in tropical
forests. Annu. Rev. Ecol. Syst. 27: 305–335.
CORRÊA, M. M., A. G. D. BIEBER, R. WIRTH, AND I. R. LEAL. 2005. Occurrence
of Atta cephalotes (Linnaeus) (Hymenoptera: Formicidae) in Alagoas,
Northeast Brazil. Neotrop. Entomol. 34: 695–698.
DIDHAM, R. K., J. GHAZOUL, N. E. STORK, AND A. J. DAVIS. 1996. Insects in
fragmented forests: A functional approach. Trends Ecol. Evol. 11;255–
260.
FAGAN, W. E., R. S. CANTRELL, AND C. COSNER. 1999. How habitat edges
change species interactions. Am. Nat. 153:165–182.
FARJI-BRENER, A. G., 2001. Why are leaf-cutting ants more common in early
secondary forests than in old-growth tropical forests? An evaluation of
the palatable forage hypothesis. Oikos 92: 169–177.
FARJI-BRENER, A. G., AND A. E. ILLES. 2000. Do leaf-cutting ant nests make
“bottom-up” gaps in neotropical rain forests?: A critical review of the
evidence. Ecol. Lett. 3: 219–227.
FERREIRA, L. V., AND W. F. LAURANCE. 1997. Effects of forest fragmentation on
mortality and damage of selected trees in Central Amazonia. Conserv.
Biol. 11: 797–801.
FORD, R. G. 1983. Home range in a patchy environment: Optimal foraging
predictions. Am. Zool. 23: 315–326.
FRAZER, G. W., R. A. FOURNIER, J. A. TROFYMOW, AND R. J. HALL. 2001. A
comparison of digital and film fisheye photography for analysis of forest
canopy structure and gap light transmission. Agric. Forest Meteorol.
109: 249–263.
GASCON, C., R. O. BIERREGAARD JR., W. F. LAURANCE, AND J. RANKIN-DE
MÉRONA. 2001. Deforestation and forest fragmentation in the Amazon.
In R. O. Bierregaard Jr., C. Gascon, T. E. Lovejoy, and R. Mesquita
(Eds.). Lessons from Amazonia: The ecology and conservation of a
fragmented forest, pp. 22–30. Yale University Press, London, UK.
GRILLO, A. S. 2005. As implicações da fragmentação e da perda de habitats sobre
a assembléia de árvores na floresta Atlântica ao norte do São Francisco.
PhD thesis, Universidade Federal de Pernambuco, Brazil.
HUNTLY, N. 1991. Herbivores and the dynamics of communities and ecosystems.
Annu. Rev. Ecol. Syst. 22: 477–503.
IBGE. 1985. Atlas Nacional do Brasil: Região Nordeste, IBGE, Rio de Janeiro,
Brazil.
JORGE, M. S. P., AND C. A. PERES. 2005. Population density and home range size
of red-rumped agoutis (Dasyprocta leporina) within and outside a natural
Brazil nut stand in southeastern Amazonia. Biotropica 37: 317–321.
KALÁCSKA, M., G. A. SÁNCHEZ-AZOFEIFA, B. RIVARD, J. C. CALVO-ALVARADO,
A. R. P. JOURNET, J. P. ARROYO-MORA, AND D. ORTIZ-ORTIZ. 2004.
Leaf area index measurements in a tropical moist forest: a case study
from Costa Rica. Remote Sens. Environ. 91: 134–152.
KAREIVA, P. 1987. Habitat fragmentation and the stability of predator-prey
interactions. Nature 326: 388–390.
KARSAI, I., AND J. W. WENZEL. 1998. Productivity, individual-level and colonylevel flexibility, and organization of work as consequences of colony size.
Proc. Nat. Acad. Sci. 95: 8665–8669.
KEMPF, W. 1972. Catálogo Abreviado das Formigas da Região Neotropical
(Hymenoptera: Formicidae). Studia Entomol. 15: 3–344.
KOST C., E. GAMA DEOLIVEIRA, T. KNOCH, AND R. WIRTH. 2005. Spatiotemporal permanence and plasticity of foraging trails in young and
mature leaf-cutting ant colonies (Atta spp.). J. Trop. Ecol. 21: 677–688.
Edge Effects on Leaf-Cutting Ant Foraging
KRUESS, A., AND T. TSCHARNTKE. 1994. Habitat fragmentation, species loss and
biological control. Science 264: 1581–1584.
LAURANCE, W. F., T. E. LOVEJOY, H. L. VASCONCELOS, E. M. BRUNA, R. K.
DIDHAM, P. C. STOUFFER, C. GASCON, R. O. BIERREGAARD, S. L. LAURANCE, AND E. SAMPAIO. 2002. Ecosystem decay of Amazonian forest
fragments: A 22-year investigation. Conserv. Biol. 16: 605–618.
LAURANCE, W. F., L. V. FERREIRA, J. M. RANKIN-DE-MORENA, AND S. G. LAURANCE. 1998a. Rain forest fragmentation and the dynamics of Amazonian tree communities. Ecology 79: 2032–2040.
LAURANCE, W. F., L. V. FERREIRA, J. M. RANKIN-DE-MORENA, S. G. LAURANCE,
R. HUTCHINGS, AND T. LOVEJOY. 1998b. Effects of forest fragmentation
on recruitment patterns in Amazonian tree communities. Conserv. Biol.
12: 460–464.
LEAL, I. R., AND P. S. OLIVEIRA. 2000. Foraging ecology of attine ants in a
neotropical savanna: Seasonal use of fungal substrate in the Cerrado
vegetation of Brazil. Insectes Soc. 47: 376–382.
LOVEJOY, T. E., R. O. BIERREGAARD, A. B. RYLANDS, J. R. MALCOLM, C. E.
QUINTELA, L. H. HARPER, K. S. BROWN, A. H. POWELL, G. V. N.
POWELL, H. O. R. SCHUBART, AND M. B. HAYS. 1986. Edge and other
effects of isolation on Amazon forest fragments. In M. E. Soule (Ed.).
Conservation biology: The science of scarcity and diversity, pp. 257–
285. Sinauer, Sunderland, Massachusetts.
LUGO, A. E., E. G. FARNWORTH, G. POOL, P. JEREZ, AND G. KAUFMANN. 1973.
The impact of the leaf-cutter ant Atta colombica on the energy flow of a
tropical wet forest. Ecology 54: 1292–1301.
MOUTINHO, P., D. C. NEPSTAD, AND E. A. DAVIDSON. 2003. Influence of
leaf-cutting ant nests on secondary forest growth and soil properties in
Amazonia. Ecology 84: 1265–1276.
MURCIA, C. 1995. Edge effects in fragmented forests: Application for conservation. Trends Ecol. Evol. 10: 58–62.
NORMAN, J. M., AND G. S. CAMPBELL. 1989. Canopy Structure. In R. W. Pearcy,
J. Ehleringer, H. A. Mooney, and P. W. Rundel (Eds.). Plant physiological
Ecology - field methods and instrumentation, pp. 301–326. Chapman
and Hall, London, UK.
OLIVEIRA, M. A., A. S. GRILLO, AND M. TABARELLI. 2004. Forest edge in the
Brazilian Atlantic forest: Drastic changes in tree species assemblages.
Oryx 38:1–6.
QUINN R., K. GASTON, AND D. BOY. 1997. Coincidence between consumer and
host occurrence: Macrolepidoptera in Britain. Ecol. Entomol. 22:197–
208.
RANKIN-DE-MÉRONA, J. M., AND R. W. HUTCHINGS. 2001. Deforestation effects
at the edge of an Amazonian forest fragment. In R. O. Bierregaard Jr., C.
Gascon, T. E. Lovejoy, and R. Mesquita (Eds.). Lessons from Amazonia:
The ecology and conservation of a fragmented forest, pp. 107–120. Yale
University Press, London, UK.
RAO, M. 2000. Variation in leaf-cutter ant (Atta sp.) densities in forest isolates:
The potential role of predation. J. Trop. Ecol. 16: 209–225.
ROCKWOOD, L. L. 1973. Distribution, density, and dispersion of two species of
Atta (Hymenoptera: Formicidae) in Guanacaste province, Costa Rica. J.
Anim. Ecol. 42: 803–817.
495
SAUNDERS, D. A, R. J. HOBBS, AND C. R. MARGULES. 1991. Biological consequences of ecosystem fragmentation: A review. Conserv. Biol. 5: 18–32.
SHEPHERD, J. D. 1985. Adjusting foraging effort to resources in adjacent
colonies of the leaf-cutter ant, Atta colombica. Biotropica 17: 245–
252.
SORK, V. L. 1983. Distribution of pignut hickory (Carya glabra) along a forest
to edge transect, and factors affecting seedling recruitment. Bull. Torrey
Bot. Club 110: 494–506.
TAVARES, S., F. A. F. PAIVA, E.J. TAVARES, O. F. MACHADO, J. L. S. LIMA, AND
S. A. SOUZA. 1971. Inventário florestal de Alagoas – Nova contribuição
para o estudo preliminar das Matas remanescentes do estado de Alagoas.
Bol. Rec. Nat. SUDENE 9: 5–122.
TERBORGH, J., L. LOPEZ, P. NUNEZ, M. RAO, G. SHAHABUDDIN, G. ORIHUELA,
M. RIVEROS, R. ASCANIO, G. H. ADLER, T. D. LAMBERT, AND L. BALBAS.
2001. Ecological meltdown in predator-free forest fragments. Science
294: 1923–1926.
TSCHARNTKE, T., I. STEFFAN-DEWENTER, A. KRUESS, AND C. THIES. 2002.
Characteristics of insect populations on habitat fragments: A mini review.
Ecol. Res. 17: 229–239.
VASCONCELOS, H. L. 1988. Distribution of Atta (Hymenoptera - Formicidae)
in a terra-firme rain forest of central Amazonia: density, species composition, and preliminary results on effects of forest fragmentation. Acta
Amaz. 18: 309–315.
VASCONCELOS, H. L. 1990. Habitat selection by the queens of the leaf-cutting
ant Atta sexdens L. in Brazil. J. Trop. Ecol. 6: 249–252.
VASCONCELOS, H. L., AND J. M. CHERRETT. 1995. Changes in leaf-cutting
ant populations (Formicidae: Attini) after the clearing of mature forest in Brazilian Amazonia. Stud. Neotrop. Fauna Environ. 30: 107–
113.
WHITMORE, T. C. 1997. Tropical forest disturbance, disappearance, and species
loss. In W. F. Laurance and R. O. Bierregaard Jr. (Eds.). Tropical forest remnants: Ecology, management, and conservation of fragmented
communities, pp. 3–12. University of Chicago Press, Chicago, Illinois.
WHITMORE, T. C., N. D. BROWN, M. D. SWAINE, D. KENNEDY, C. I. GOODWINBAILEY, AND W. K. GONG. 1993. Use of hemispherical photographs in
forest ecology: Measurement of gap size and radiation totals in a Bornean
tropical rain forest. J. Trop. Ecol. 9: 131–151.
WIRTH, R., W. BEYSCHLAG, R. J. RYEL, AND B. HÖLLDOBLER. 1997. Annual
foraging of the leaf-cutting ant Atta colombica in a semideciduous rain
forest in Panama. J. Trop. Ecol. 13: 741–757.
WIRTH, R., B. WEBER, AND R. J. RYEL. 2001. Spatial and temporal variability
of canopy structure in a tropical moist forest. Acta Oecol. 22: 235–
244.
WIRTH, R., W. BEYSCHLAG, R. J. RYEL, H. HERZ, AND B. HÖLLDOBLER. 2003.
Herbivory of leaf-cutting ants. A case study on Atta colombica in the
tropical rainforest of Panama. Springer-Verlag, Berlin, Heidelberg, New
York, New York.
WIRTH, R., S. T. MEYER, I. R. LEAL, AND M. TABARELLI In Press. Plant-herbivore
interactions at the forest edge. Progress in Botany.
ZAR, J. H. 1999. Biostatistical analysis. Prentice-Hall Inc., New Jersey.