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Leaf-cutting ants as ecosystem engineers: Topsoil and litter perturbations

around Atta cephalotes nests reduce nutrient availability

Article in Ecological Entomology · June 2013

DOI: 10.1111/een.12043

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Ecological Entomology (2013), 38, 497–504 DOI: 10.1111/een.12043

Leaf-cutting ants as ecosystem engineers: topsoil

and litter perturbations around Atta cephalotes nests
reduce nutrient availability
S E B A S T I A N T . M E Y E R,1 M E I K E N E U B A U E R,1 E M M A J . S A Y E R,2
I N A R A R . L E A L,3 M A R C E L O T A B A R E L L I 3 and R A I N E R W I R T H 1
1
Plant Ecology and Systematics, University of Kaiserslautern, Kaiserslautern, Germany, 2 Department of Environment, Earth and
Ecosystems, The Open University, Milton Keynes, U.K. and 3 Departamento de Botânica, Universidade Federal de Pernambuco,
Recife, Brazil

Abstract. 1. Despite considerable research into the effects of leaf-cutting ant nests,
the potential occurrence of low-nutrient soils at nest sites has hitherto gone undetected.
2. Leaf litter cover and topsoil conditions (organic carbon, total nitrogen, soil acidity,
cation exchange capacity) were assessed along transects running from nests of eight
adult Atta cephalotes colonies into the understorey of Atlantic forest to examine the
extent of nest effects.
3. Nests were virtually free of leaf litter (c. 150 g m−2 ) and litter cover increased
along a saturating curve with nest distance, reaching 1300 g m−2 in the undisturbed
forest. Soil acidity and nutrient concentrations were strongly correlated with leaf litter
cover (r = 0.66–0.72) for both soil types occurring in the study region. Total soil
nitrogen concentration varied from 0.2 g kg−1 in sandy nest soil and 0.5 g kg−1 in
clay-rich nest soil to 0.5 and 1.3 g kg−1 , respectively, at a distance of 24 m from nests,
while soil carbon concentration ranged from 2.1 to 6.1 g kg−1 (sandy soil) and 4.5
to 15.7 g kg−1 (clay-rich soil) over the same distance. Nest-associated variations in
edaphic parameters suggest that each colony affected an area of up to 0.5 ha.
4. In contrast to the common perception that leaf-cutting ant activities increase
nutrient availability, our results suggest that their territories are characterised by
reduced levels of leaf litter and, consequently, soil nutrients.
5. The observed nutrient depletion must be taken into account when considering the
potential impacts of ant nests for plant regeneration.
Key words. Attini, Atlantic Forest, Brazil, herbivory, leaf litter, nest effects, nest soil,
nutrient dynamics.

Introduction surface area) formed by a system of subterranean tunnels and

Leaf-cutting ants are the dominant insect herbivores of the
Neotropics (Wirth et al., 2003; Herz et al., 2007) and also act
as ecosystem engineers, altering forest structure, microclimate
and regeneration (Meyer, 2008; Corrêa et al., 2010; Meyer
et al., 2011b). Adult colonies construct large nests (50–160 m2
Correspondence: Sebastian T. Meyer, Terrestrial Ecology Group,
Department of Ecology and Ecosystem Management, Technische Uni-
versität München, Hans-Carl-von-Carlowitz-Platz 2, 85350 Freising-
Weihenstephan, Germany. E-mail: Sebastian.T.Meyer@tum.de
chambers that can reach depths of up to 7 m in the soil (Farji-
Brener & Illes, 2000 and references therein). Nest architecture
is adapted to provide optimal cultivation conditions for the
ants’ symbiotic fungus in terms of temperature and humidity
(Kleineidam & Roces, 2000; Roces & Kleineidam, 2000;
Bollazzi et al., 2008). During the construction of these
underground networks, up to 23 m3 (Autuori, 1942) or 40 tons
(Wirth et al., 2003) of soil are moved to and deposited at
the nest surface. Thereby, a single species of leaf-cutting ant
(Atta cephalotes L.; Hymenoptera: Formicidae) is estimated
to cause a complete turnover of the soil in a Costa Rican

© 2013 The Royal Entomological Society 497

498 Sebastian T. Meyer et al.
rainforest within 200–300 years (Perfecto & Vander Meer,
1993). In addition to soil bioturbation, these ants are known
to alter forest structure as foraging and nest-clearing activities
create gaps above nests that extend from the forest understorey
to the canopy (Farji-Brener & Illes, 2000; Corrêa et al.,
2010; Meyer et al., 2011b). Such gaps cause drastic shifts
in microclimatic conditions, particularly in light availability,
soil temperature and soil water potential (Meyer et al., 2011b).
By modifying the forest environment, Atta nests can act as
ecological filters for plant recruitment (Meyer et al., 2011a)
and are considered a major disturbance with the potential to
alter the structure and plant species composition of tropical
forests (reviewed in Farji-Brener & Illes, 2000; Rico-Gray &
Oliveira, 2007). In addition, trophic effects of leaf-cutting ants
can impact ecosystem functioning as adult colonies frequently
collect more than 250 kg of plant biomass per colony a
year (up to 900 kg year –1 per colony; Herz et al., 2007 and
references therein); plant material (predominantly leaves) is
carried into the nest and degraded by a symbiotic fungus, which
constitutes the ants’ main food source. Degraded substrate
and fungal remains are deposited in subterranean or external
refuse dumps (depending on the Atta species; Farji-Brener
& Medina, 2000), which are very high in available nutrients
(Wirth et al., 2003).
The pioneering work by Haines on Atta colombica Guérin-
Méneville, one of the few species with external refuse dumps,
has been the basis for ongoing interest in the impact of leaf-
cutting ant nests on nutrient cycling (Haines, 1978, 1983)
and ensuing effects on vegetation dynamics (Haines, 1975;
Haines et al., 1990). In the more widespread case of leaf-
cutting ant species with subterranean refuse deposition, deep
nest soils are also enriched in nutrients, e.g. Atta sexdens (L.)
(Moutinho et al., 2003; Verchot et al., 2003), Atta leavigata (F.
Smith) (Sousa-Souto et al., 2008), and A. cephalotes (Alvarado
et al., 1981). In combination with observations of other ant
species (e.g. Lobry de Bruyn & Conacher, 1994), the above
evidence has led to the common perception that leaf-cutting
ant activities increase nutrient availability for plants. Despite
two recent studies documenting reduced nutrient levels for
topsoil at leaf-cutting ant nests (Jiménez et al., 2008; Hudson
et al., 2009), present investigations have largely neglected to
address the topsoil on and around nests, focusing on deep
nest soil (or studies did not differentiate between topsoil
and deeper soil horizons in their conclusions). There are at
least two compelling reasons to expect differences between
topsoil and deep nest soil: (i) mineral soil with low nutrient
concentrations is moved to the nest surface during excavation
(Farji-Brener & Illes, 2000); and (ii) the accumulation of
nutrients in the refuse dumps is caused by foliage removal
from the foraging area and its concentration within a limited
area (Hudson et al., 2009). The removal of foliage is likely
to affect litterfall and litter cover on the soil surface at
nest sites. To date, this remains uninvestigated despite the
importance of litter for element cycles and nutrient availability
in tropical forests (e.g., Vitousek, 1984; Dent et al., 2006;
Sayer et al., 2006; Weerakkody & Parkinson, 2006). The
potential decrease in topsoil nutrient levels is clearly relevant
to gaining a better understanding of the impacts of leaf-cutting
© 2013 The Royal Entomological Society, Ecological Entomology, 38, 497–504
ants on the functioning of tropical ecosystems (Meyer et al.,
2011a) and plant species composition (Silva et al., 2012).
We addressed this by investigating the edaphic conditions at
nest sites of A. cephalotes in a large fragment of Atlantic
Forest. Specifically, we aimed to answer the following research
questions: (i) how do nutrient concentrations in the topsoil of
A. cephalotes nests compare with those in undisturbed forest
soil; (ii) is litter cover affected by ant foraging behaviour; and
(iii) are effects restricted to the immediate nest area, or do
they extend into the surrounding forest? Observed patterns
are discussed in terms of their potential impact on plant
regeneration, with special reference to the effects of leaf-
cutting ants as ecosystem engineers in human-modified forests.
Materials and methods
Study site and species
The study was conducted in the Coimbra Forest (9◦ S,
◦
35 52 W), a privately owned large fragment (c. 3500 ha) of
the Atlantic Forest in northeast Brazil, consisting of a largely
well-conserved patch of lowland rainforest (300–400 m above
sea level) that is completely surrounded by a homogenous
matrix of sugar cane fields (Santos et al., 2008). Such a human-
modified landscape is typical across the Atlantic Forest region.
The climate is tropical, with rainfall of c. 2000 mm year –1 and a
5-month dry season (rainfall < 110 mm month –1 ) lasting from
September to January. The prevailing soils in the area are
latosols and podzols (IBGE, 1985), which are acidic (pH 4.2),
old oxidised ferrous soils with high clay content (henceforth
called ‘red clay’). In addition, fluvial sediments occur close to
rivers and streams forming a second soil type dominated by
sand (henceforth ‘white sand’), which is slightly less acidic
(pH 4.5). These soil types can be readily distinguished based
on their colour and showed a markedly different grain size
distribution (see Figure S1 in Appendix S1).
We measured soil properties at eight nest sites of the
abundant leaf-cutting ant A. cephalotes, which is one of the
two co-occurring Atta species in northeast Brazil (Corrêa
et al., 2005) and is widespread throughout the Neotropics from
Mexico to Bolivia (Kempf, 1972). Colonies of A. cephalotes
are long-lived (life expectancy of 8 years; Meyer et al., 2009)
and occur almost 10 times more frequently within 50 m of the
edge of Coimbra Forest compared with the forest interior (2.8
vs. 0.3 colonies ha –1 ; Wirth et al., 2007). We selected nests
located 13–295 m away from the nearest forest edge, which
were surrounded by homogeneous forest with no openings
other than the colony itself (i.e. no tree-falls or other gaps),
as we aimed to document changes exclusively induced by ant
nests and their associated vegetation gaps. These colonies have
been previously examined in detail for forest structure and
climatic conditions at nest sites (Meyer et al., 2011b) and for
potential impact upon tree seedling regeneration (Meyer et al.,
2011a). Thus, the Coimbra Forest and its pool of focal colonies
are ideally suited for an investigation of nest-related edaphic
changes in a human-modified habitat that dominates modern
tropical landscapes, namely the edges of heavily fragmented
forests (Tabarelli et al., 2008).

Soil properties
Soils were examined during the peak of the dry season in late
2006 along one linear transect per colony, starting at the edge
of each nest. Transects extended 24 m into the forest; samples
were taken from the centre of the nest and then at intervals
of 3 m along each transect (n = 10 per transect). Care was
taken that sampling points did not fall onto foraging trails, and
ran parallel to any breaks in forest cover (forest edge, stream,
valley) to control for potential confounding effects.
At each sampling point, all litter was collected within an
area of 20 × 20 cm, coarse woody debris (> 2 cm diameter)
was removed and the remaining leaf litter was oven-dried to
constant weight. A topsoil sample was taken by extracting soil
cores of 6 cm diameter and 10 cm depth. Cores were pooled
by transect point and soil type (five colonies on red clay, three
on white sand) and mixed thoroughly, resulting in one sample
per soil type and distance from the nest (20 samples in total).
All soil samples were ground, sieved (2-mm mesh), air-
dried in the laboratory and then oven-dried at 40 ◦ C. Total
soil organic carbon (C) was determined by wet oxidation,
total nitrogen (N) was determined using Kjeldahl extraction;
phosphorus was determined using the phosphomolybdic acid
method recommended for soils with low phosphorus concen-
trations after overnight extraction with an HCl-H2 S04 -solution;
and effective cation exchange capacity (CEC) was calculated
as the sum of exchangeable cations, which was measured by
determining the exchangeable concentrations of aluminium,
calcium, magnesium, hydrogen (extraction with KCl and col-
orimetric determination), potassium and sodium (extraction
with HCl and photometric determination) at a specialised com-
mercial agronomic laboratory (AGROLAB, Análises Ambi-
entais Ltda, Casa Forte, Recife, PE, Brazil), following the
procedures recommended by the Brazilian Ministry of Agri-
culture for soil fertility analyses (Embrapa, 1997). Here, we
include only those soil parameters that varied along transects.
Phosphorus concentrations were not included in our statistical
analyses as they were at or below the analytical detection limit
in almost all soil samples; measured phosphorus concentrations
varied between the values 1 and 2 mg kg−1 in both soil types.
Statistical analysis
All statistical analyses were performed in r (version 2.6.0;
R Development Core Team, 2007). Litter cover was analysed
in a non-linear mixed-effects model with colony as a random
effect (Pinheiro & Bates, 2002) using the nlme function
(version 3.1-85; Pinheiro et al., 2012). This model also checked
for differences between the estimated model parameters due
to soil type by testing soil type as a covariate. Parameters
that were pooled over colonies (total N, organic C, H+
concentrations, and CEC) were related to distance from nests
by non-linear models, using the nls function. Ninety-five per
cent confidence bands around the nls fits were calculated
following a procedure recommended by Peter Dalgaard
(http://tolstoy.newcastle.edu.au/R/help/04/10/5119.html). Para-
meter estimates from minimum adequate models are presented,
together with the significance of the models based on
© 2013 The Royal Entomological Society, Ecological Entomology, 38, 497–504
Low-nutrient soils at leaf-cutting ant nests 499
comparisons to null models containing only a single constant.
The goodness of fit of models is expressed as the proportion
of variation in the observed values explained by the model
predictions. The parameterised exponential models make it
possible to estimate the height of the asymptote (undisturbed
forest values) from the measured points, even if the asymptote
is not reached. Relationships between litter cover and soil
parameters were tested using Pearson’s correlations.
Results
We observed a marked effect of A. cephalotes colonies on
soil properties. Nests were virtually free of any leaf litter (c.
150 g m−2 ) and litter cover increased in a saturating curve with
distance from nests, reaching a maximum of c. 1300 g m−2
on both soil types (Fig. 1, Table 1). The degree of curvature
differed between soil types, with a more pronounced curvature
in the white sand (Fig. 1, Table 1). Distance to the nests
alone explained 70% of the variation in measured litter cover
and the effect extended surprisingly far into the forest. The
parameterised exponential model showed that litter cover
reached undisturbed forest levels (90% of estimated asymptotic
litter cover) at a distance from the edge of the nests of c. 35 m
on red clay and c. 20 m on white sand. With an average
distance of 5 and 3.6 m from the nest centre to the nest edge, the
area affected by each colony amounted to 0.5 and 0.17 ha for
colonies in red clay and white sand, respectively (i.e. a circle
with a total radius of 40 m on red clay and 23.6 m on white
sand). Soil acidity (measured as H+ concentrations), organic C
and total N concentrations, as well as cation exchange capacity
were consistently higher in the red clay than in the white
sand. All of these soil variables were strongly correlated with
Fig. 1. Leaf litter cover along gradients from eight Atta cephalotes
nests into the surrounding Brazilian Atlantic Forest (‘0’ marks the
edge of the colonies’ understorey gap, ‘−4.6’ the average distance to
the centre of colonies). A clay-rich soil (‘red clay’, closed circles; five
colonies) and a soil with a higher sand concentration (‘white sand’,
open circles; three colonies) were present in the study area. The lines
represent the best-fit exponential model described in the text (solid
line, red clay; dashed line, white sand).
500 Sebastian T. Meyer et al.

Table 1. Statistical parameters describing the relationship between edaphic variables in relation to distance from Atta nests.

Parameter ± SE (random effect as SE) Residuals

Variable a b c As SE Test statistic P value r 2 equivalent

Litter cover
Red clay −0.054 ± 0.015
−849 ± 156 1296 ± 142.0 (85.7) 214.1 LLR3,6 = 85.3 < 0.0001 0.70
White sand −0.095 ± 0.031
Carbon concentration
Red clay −5.37 ± 1.89 −0.14 ± 0.06 15.08 ± 1.19 1.66 F 7,9 = 17.98 0.0017 0.84
White sand −3.08 ± 1.07 −0.1 ± 0.06 6.90 ± 0.79 0.87 F 7,9 = 12.96 0.0044 0.79
Nitrogen concentration
Red clay −0.51 ± 0.19 −0.10 ± 0.05 1.34 ± 0.14 0.14 F 7,9 = 16.35 0.0023 0.82
White sand −0.23 ± 0.75 −0.10 ± 0.05 0.53 ± 0.06 0.05 F 7,9 = 17.40 0.0019 0.83
Cation exchange capacity
Red clay −4.08 ± 1.30 −0.11 ± 0.04 13.76 ± 0.93 0.99 F 7,9 = 21.32 0.0011 0.86
White sand −2.38 ± 0.95 −0.18 ± 0.09 69.57 ± 0.56 0.94 F 7,9 = 10.23 0.0084 0.75
Proton concentration
Red clay −2.37 ± 0.73 −0.15 ± 0.05 9.00 ± 0.43 0.67 F 7,9 = 25.32 0.0006 0.88
White sand −1.05 ± 0.63 −0.29 ± 0.16 5.83 ± 0.28 0.63 F 7,9 = 9.97 0.0090 0.74

For all variables, exponential models following the formula y = a × exp(b × TP) + c were fitted (TP, transect points). In case of ‘litter cover’, a
mixed-effects model with random effects for the different colonies and soil type as covariate was fitted (only b differed between soil types), while
for the other variables, individual exponential models were fitted for samples pooled within soil type as detailed in the text. Parameter estimates
together with their SE are given.

litter cover (Fig. 2, Table 1) and showed a similar pattern
with distance from the nests. To give an example, the N
concentration of red clay soils was considerably reduced, by
more than 2.5-fold, on nest centres (0.50 g kg−2 ), reaching
90% of undisturbed forest levels (1.34 g kg−2 ) at a distance
of c. 13.7 m from the nest edge.
Discussion
In contrast to the generally accepted view that leaf-cutting
ant activities increase nutrient availability to plants (Haines,
1978, 1983; Alvarado et al., 1981; Moutinho et al., 2003;
Pinto-Tomas et al., 2009, but see also Wirth et al., 2003;
Jiménez et al., 2008; Sousa-Souto et al., 2008), our data
suggest that A. cephalotes reduces nutrient availability in the
uppermost soil horizons at nest sites. We found decreased
concentrations of soil organic C and total N, higher H+
concentrations, reduced cation exchange capacity and reduced
leaf litter cover around nest sites across two distinct soil
types. Moreover, these changes in soil properties were not
restricted to the nests themselves, but persisted for several
tens of metres into the forest, with each colony influencing
an estimated forest area of up to 0.5 ha. To understand such
contrasting results, it is important to note that many of the
studies describing increased nutrient availability around ant
nests focused on Atta species with above-ground refuse dumps
(A. colombica). Other studies have investigated Atta species
with below-ground refuse storage but analysed deep nest soils
(up to 350 cm depth), which are documented as being nutrient-
rich (Alvarado et al., 1981; Moutinho et al., 2003; Verchot
et al., 2003; Sousa-Souto et al., 2008) and the nutrients may
be accessed by lateral roots from large trees (Sternberg et al.,
2007) or leached into the groundwater (Haines, 1983). By
contrast, although we examined nests characterised by below-
ground refuse chambers, we aimed to determine the influence
of A. cephalotes activities on soil properties relevant to plant
recruitment and seedling dynamics. Therefore, we concentrated
on changes in the topsoil, as the rooting depth of seedlings is
typically restricted to the top 20 cm of the soil (Markesteijn
& Poorter, 2009) and the establishment and early survival of
seedlings are critical for plant recruitment.
Measures of total or soil extractable nutrients, as performed
in this study, do not necessarily reflect nutrient availability to
plants (Sayer et al., 2012), yet the amount of total N in the soil
close to the nests was less than half the amount in the topsoil in
undisturbed forest. Soil organic C and cation exchange capacity
followed a very similar pattern, with two- to three-fold higher
values in the undisturbed forest soil than in the soil around
the nests (Fig. 2). These differences are so large that impacts
on seedling growth can be readily expected. In addition,
Atta colonies showed a marked reduction in leaf litter cover.
Whereas our modelled estimate of litter cover (1.3 kg m−2 ) in
the undisturbed forest lies well in the published range of leaf
litterfall for the Atlantic Forest (1.26 ± 0.47 kg m−1 in forest
interior and 1.47 ± 0.28 at the forest edges; Schessl et al.,
2008), litter cover was drastically reduced in the proximity of
the nests (Fig. 2). These marked reductions in litter cover are
important because, in tropical forests on nutrient-poor soils,
a large proportion of the available nutrients are stored in
the living biomass and productivity is maintained by rapid
recycling and uptake of nutrients from decomposing litter
(e.g. Richards, 1996). Indeed, direct uptake of nutrients from
decomposing litter by roots and mycorrhizae in tropical forests
is thought to be common (Herrera et al., 1978; Stark & Jordan,
1978) and to substantially increase seedling growth and affect
regeneration success (Brearley et al., 2003). Previous work on
the role of litterfall in tropical forest nutrient cycling has shown

© 2013 The Royal Entomological Society, Ecological Entomology, 38, 497–504


that the removal of litter decreased nutrient concentrations in
the uppermost layers of the mineral soil within a year, such that
nutrient concentrations in fresh litterfall were affected (Wood
et al., 2009; Sayer & Tanner, 2010). Further, litter inputs were
shown to be crucial for maintaining N availability to plants in
the longer term (Sayer et al., 2012) and may be the principal
source of phosphorus to plants when availability in the mineral
soil is very low (Attiwill & Adams, 1993), as was the case at
© 2013 The Royal Entomological Society, Ecological Entomology, 38, 497–504
Low-nutrient soils at leaf-cutting ant nests 501
Fig. 2. Measures of soil properties along gradi-
ents from Atta cephalotes nests into the surround-
ing Brazilian Atlantic Forest (left panels) and cor-
relations between soil properties and leaf litter
cover at measuring points (right panels). A clay-
rich soil (‘red clay’, closed circles and solid lines;
five colonies pooled) and a soil with a higher
sand content (‘white sand’, open circles and dashed
lines; three colonies pooled) were present in the
study area. Black lines represent best-fit exponen-
tial models (left panels; for statistics see Table 1)
or linear correlations with litter cover (right pan-
els; given with respective r- and P -values from
Pearson product-moment correlations); grey lines
represent 95% confidence bands for the estimated
models in the left panels, as described in the text.
For the gradients, ‘0’ marks the edge of nests
and ‘−4.6’ the average distance to the centre of
colonies.
both of our sites. The lower cation exchange capacity in soils
around the nests can also be attributed to the disruption of litter
inputs by ant activities, and is likely to further reduce nutrient
availability in the topsoil (Sayer et al., 2006). Collectively,
these findings support the premise that A. cephalotes acts as
an ecosystem engineer (sensu Jones et al., 1994, 2006) in
the Atlantic Forest by creating low-nutrient sites unfavourable
for seedling growth, i.e. affecting the availability or resources
502 Sebastian T. Meyer et al.
for other organisms (the definition of an ecosystem engineer).
The present documented changes in soil properties add to
the previously established ecosystem engineering effects of A.
cephalotes in terms of microclimate at nest sites, characterised
by a higher light interception, higher soil temperatures and
slightly lower water availability (Corrêa et al., 2010; Meyer
et al., 2011b), with some changes persisting even after 15 years
of colony death or nest abandonment (Bieber et al., 2011).
It is striking that all measurements of soil properties were
strongly correlated with litter cover. It is thus reasonable to
assume that by decreasing the litter standing crop around the
nests, A. cephalotes activities decrease soil nutrient levels.
In a similar way, subterranean termites affect soil nutrient
levels by reducing leaf litter cover, on which they directly
feed (Veeresh & Belavadi, 1986; Lobry de Bruyn & Conacher,
1994). Decreased accumulation of new litter is the most
parsimonious explanation for the sparse litter cover around ant
nests. Although increased decomposition rates could reduce
the litter standing crop, this is unlikely at nest sites, as
these are drier than the surrounding forest (Meyer et al.,
2011b). Unlike termites and the majority of lower Attine
ant species, Atta species seldom forage directly on leaf litter
as substrate for fungus cultivation. While their nest-clearing
behaviour (Garrettson et al., 1998; Meyer et al., 2011a),
which also involves litter removal or burrowing, may well
explain the occurrence of bare soil on central nest mounds, it
cannot account for the reduction in litter standing crop around
nests. Instead, it is probable that the litter production in the
vicinity of the nests is altered by ant activities. Three different
mechanisms can contribute to this effect. First, herbivory can
directly affect the rate of litter production, because colonies
remove large quantities of foliage from their foraging areas
(Wirth et al., 1997; Herz et al., 2007) and thereby effectively
reduce leaf biomass. Higher rates of herbivory close to nests
resulting from a higher relative proportion of exploited trees
per unit area would account for the observed gradient).
Secondly, gaps associated with A. cephalotes nests promote
environmental modifications for tens of metres around nests,
including lower sapling densities and a higher canopy openness
(Corrêa et al., 2010), which will also result in lower litter
inputs. In addition, changes in species composition in foraging
areas (Corrêa et al., 2010; Silva et al., 2012) can affect litter
quality and rates of decomposition as these vary widely among
tree species. Thirdly, and to a lesser extent, foraging on
litter material can directly contribute to lower litter standing
crop close to nests. While use of non-green plant material
(e.g. flowers, fruit parts, stipules) constitutes only 10–15%
of the harvest by A. cephalotes (P. Falcão, unpublished),
litter foraging by other Atta species has a greater potential
to affect litter standing crop (A. sexdens, Vasconcelos, 1990;
A. colombica, Wirth et al., 2003).
Although we did not assess natural plant regeneration at our
focal nests, we propose that ant activities affect vegetation
dynamics by decreasing the supply of nutrients available
to seedlings as well as altering microclimatic conditions at
the soil surface (Meyer et al., 2011b). This hypothesis is
supported by recent findings. First, experimentally planted
seedlings showed altered biomass allocation patterns towards
© 2013 The Royal Entomological Society, Ecological Entomology, 38, 497–504
higher root:shoot ratios in the vicinity of nests (Meyer et al.,
2011a), which suggests a greater investment of resources below
ground for nutrient acquisition. Secondly, abandoned nests of
A. cephalotes at our study sites supported largely impoverished
and sparse regenerating plant assemblages and were identified
as a persistent unsuitable habitat for plant recruitment (Bieber
et al., 2011). The strong gradient in litter depth close to
active nests can also directly alter competitive outcomes among
species of seedlings and thus influence patterns of plant
regeneration and forest dynamics because litter cover plays
a crucial role in seed germination, seedling establishment and
seedling survival (Molofsky & Augspurger, 1992). Additional
indirect effects of altered litter cover can be expected, as the
decrease in soil organic C indicates less incorporation of fresh
organic matter into the soil, which will in turn affect water
retention, soil porosity and pH (Sayer et al., 2006), parameters
that were shown to be altered at nest sites in this and previous
studies (Bieber et al., 2011; Meyer et al., 2011b).
Implications of altered edaphic conditions around the nest
sites are likely to be context-dependent in human-disturbed
forests (Leal et al., 2011). Leaf-cutting ants occur in very
low densities in undisturbed forest (Wirth et al., 2007 and
references within). Thus, habitats created by their various acts
of ecosystem engineering are also rare and promote habitat
patchiness and heterogeneity (Wirth et al., 2003). This is
assumed to be the typical scenario regarding the effects of
ecosystem engineers at the landscape scale (Wright et al.,
2004). However, in human modified landscapes, leaf-cutting
ants are hyper-abundant near forest edges (Wirth et al., 2007;
Meyer et al., 2009; Dohm et al., 2011). Indeed, at high
colony densities of almost three colonies ha –1 of A. cephalotes
(Wirth et al., 2007), foraging areas (1 ha per colony; Urbas
et al., 2007), and therefore areas of reduced litter cover
(0.6 ha per colony; this study), would affect the entire edge
habitat, contributing to a homogenisation of the environmental
conditions (Meyer, 2008). It is also noteworthy that the
disruption of litter inputs and the resulting decrease in nutrient
availability in the topsoil will also apply to Atta species with
above-ground refuse dumps (e.g. A. colombica). In this case,
the nest site itself is nutrient-rich because of the accessibility
of refuse material, but the translocation of these nutrients from
the surrounding foraging area will ultimately reduce nutrient
levels in a large area around the nests. To our knowledge, this
possibility has not been investigated to date.
In conclusion, here we provide evidence that topsoil layers
of A. cephalotes nests, and the surrounding forest floor,
represent low-nutrient and edaphically disrupted sites, probably
largely due to the dramatic reduction in litter cover. Low-
nutrient soils and decreased litter cover have a high potential
to impact upon plant regeneration and, consequently, the
alteration of soil properties around nest sites can be regarded
as a further act of ecosystem engineering by Atta. Indeed,
there is increasing evidence that ecosystem engineering, in
addition to herbivory, by leaf-cutting ants represents one of
the forces driving forest dynamics across edge-affected habitats
(Meyer, 2008; Wirth et al., 2008; Bieber et al., 2011; Meyer
et al., 2011a,b). Future studies on the extent to which leaf-
cutting ants favour plant diversity by creating environmental

heterogeneity (the classical view) or reduce diversity by
imposing ecological filters for particular plant species should
consider this hypothesis in detail.
Acknowledgements
The study was supported by a Brazilian-German research
programme of CAPES and DAAD (PROBRAL, projects
257/07 and D/06/33907), grants to R.W. by the ‘Deutsche
Forschungsgemeinschaft’ (DFG, process WI 1959/1-1, 1-2)
and the AFW Schimper- Foundation, and to I.R.L. and M.T.
by the ‘Conselho Nacional de Desenvolvimento Científico e
Tecnológico’ (CNPq, processes 471904/2004-0, 473529/2007-
6). We are grateful to Burkhard Büdel (University of
Kaiserslautern) for the PhD position for S. Meyer, to the
DAAD for a grant to M.N. (formally M. Passlack), and to the
‘Usina Serra Grande’, the ‘Centro de Pesquisas Ambientais
do Nordeste’ (CEPAN) and ‘Conservação Internacional do
Brasil’ (CI-Brasil) for logistical support. We thank Hugh
Loxdale for his helpful comments, which helped to improve
earlier versions of the manuscript.
Supporting Information
Additional Supporting Information may be found in the online
version of this article under the DOI reference:
10.1111/een.12043
Appendix S1. Proportion of different soil size fractions in
the “white sand” and “red clay” soil types occuring in the study
area.
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Accepted 24 April 2013
First published online 11 June 2013