Biol Invasions
DOI 10.1007/s10530-007-9103-3
ORIGINAL PAPER
The role of competitive dominance in the invasive ability
of the Argentine ant (Linepithema humile)
Soledad Carpintero Æ Joaquı́n Reyes-López
Received: 30 May 2006 / Accepted: 12 February 2007
Springer Science+Business Media B.V. 2007
Abstract To assess the importance of competition in the advance of invasive species, bait
stations have been used to determine the dominance hierarchy of a community of native ants in
Doñana National Park, southern Spain, and the
status of the introduced species Linepithema
humile (Argentine ant). Some native species,
e.g. Cataglyphis floricola or Camponotus pilicornis, seem to be subordinate, i.e. occupy a low
position in the competitive hierarchy; some are
dominant (e.g. Pheidole pallidula), and others
(e.g. Aphaenogaster senilis) occupy an intermediate position in the hierarchy. The Argentine ant is
a competitively dominant species, because of its
aggressive behavior and relative abundance. Irrespective of their position in the dominance
hierarchy, L. humile and some native species
adopt what games theory terms ‘‘the bourgeois
strategy’’ during agonistic encounters with other
species. Lone workers tend to be submissive in
encounters whereas workers in the presence of
S. Carpintero
Departamento de Ciencias Ambientales, Área de
Zoologı́a, Universidad Pablo de Olavide, Ctra. de
Utrera km 1, Sevilla 41013, Spain
J. Reyes-López (&)
Área de Ecologı́a, Campus de Rabanales,
Universidad de Córdoba, Cordoba 14071, Spain
e-mail: joaquin@uco.es
other colony members are aggressive. L. humile
was the only species which aggressively displaced
large numbers of ants of other species from the
bait. L. humile also expanded its range in the
course of the experiment, displacing native species from parts of the study area.
Keywords Linepithema humile Invasion Dominance hierarchy Bourgeois strategy
Introduction
Species invasions are a principal component of
global change, causing large losses in biodiversity,
and economic damage (Arim et al. 2006). Given
the importance of this problem, several studies
have attempted to understand and predict the
success of invasive species, their patterns of
spread, and the characteristics of vulnerable
invaded ecosystems and communities.
Many studies of ants have highlighted the
importance of both intraspecific and interspecific
competition in structuring communities (Cerdá
et al. 1998; Eldridge and Traniello 1981; Fox et al.
1985; Holway 1999; Human and Gordon 1999;
Passera et al. 1996; Perfecto 1994; Punttila et al.
1994; Savolainen 1990; Yamaguchi 1992). Competitive ability is important because the resource
requirements of many ant species overlap substantially (Pisarski and Vepsäläinen 1989), not
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Biol Invasions
just between closely-related species but also
between distantly-related species (Mabelis
1984). As a result, introduction of a new species,
for example the invasive Argentine ant (Linepithema humile, Mayr, 1868), may prompt major
convulsions in the native ant community (Holway
1999; Human and Gordon 1999; Suarez et al.
1998).
An important topic in the study of social
behavior is dominance. Dominance can be
described as an attribute of any individual or
species that usually wins agonistic encounters.
The winner is ‘‘dominant’’ and the loser is
‘‘subordinate’’ (De Vries 1998; Drews 1993).
Using this definition, several dominance hierarchies have been reported in ant communities
(Hölldobler and Wilson 1990; Vepsäläinen and
Pisarski 1982). For example, Vepsäläinen and
Pisarski (1982) classified species on a scale ranging from those that usually win contests to those
that usually lose contests, although this does not
necessarily mean that the lowest-ranked species
are unable to survive in communities with dominant species.
The lowest rank consists of species with very
little aggression which usually only fight to defend
their nests. Ants of this kind are the same as the
‘‘opportunist’’ species described by Wilson (1971)
on bait. The workers of these species are often
very efficient at finding new food resources and
are often the first to arrive, though they may later
be displaced by more aggressive species. Also
included in this group are species characterized
by small colony and worker sizes and elusive
workers that avoid confrontation with other
species (Hölldobler and Wilson 1990).
The intermediate region of the scale contains
species that maintain spatio-temporal territories,
defending food sources and their nests (Hölldobler and Lumsden 1980). This type of defense
occurs when food or other resources are unpredictable. These species usually come into greater
conflict with the dominant species than those in
the previous category (Vepsäläinen and Pisarski
1982; Hölldobler and Wilson 1990). Also included
in this category are ants that make fairly stable
food trails, for example the Old and New World
graminivorous ants, and leaf-cutter ants from the
tropics (Hölldobler and Lumsden 1980).
123
The highest-ranking species are usually very
aggressive, and actively defend a permanent
territory containing their nests and a relatively
large foraging area. Dominant species usually
patrol wide areas and can have an important
effect on local communities, not just of ants but
also of other arthropods and plants (Hölldobler
and Lumsden 1980; Punttila et al. 1994).
The dominance hierarchy of these species
provides a framework for examining the role of
aggressive behavior and interspecific competition
in structuring communities. It should be possible
to predict the relative abundance of species
according to their position in the hierarchy. For
example, it is unlikely that two dominant species
could co-exist locally, because of their strongly
territorial behavior (Holway 1999; Pisarski and
Vepsäläinen 1989; Savolainen 1990). Nevertheless, previous studies of social insects have noted
a trade-off between interference and exploitative
ability in species of differing ranks, which may
promote co-existence (Cerdá et al. 1997). Invasive species seem to disrupt this trade-off (Holway 1999; Feener 2000).
The Argentine ant has spread beyond its
original range to many parts of the world,
especially in areas with a Mediterranean climate
(both northern and southern latitudes, usually
between 30 and 36). Besides being a threat to
native ant communities, introduced Argentine
ants have been found to cause economic and
public health problems (Williams 1994; Vander
Meer et al. 1990). Their greatest effect, however,
is on the abundance and distribution of native ant
species (Fluker and Beardsley 1970; Human and
Gordon 1999; Majer 1994; Sanders et al. 2001;
Suarez et al. 1998). Their effect on local ant
communities is so great because these large
colonies of generalists make high demands on a
wide range of resources, bringing them into
competition with a wide range of species, in a
process known as ‘‘diffuse competition’’ (Holway
1999; Suarez et al. 1998). It has even been
suggested they become predators of native ant
species (Zee and Holway 2006).
Several factors have contributed to the spread
and establishment of Argentine ant populations
(Passera 1994), including their marked aggressiveness toward other species and their capacity
Biol Invasions
for mass recruitment (Holway et al. 1998; Liang
and Silverman 2000; Suarez et al. 1999; Tsutsui
et al. 2001). Despite their reputation as an invasive species, surprisingly few field studies have
addressed the behavior of Argentine ants, especially in Europe (Fowler et al. 1994; but see Way
et al. 1997). To examine competitive interactions
between Argentine ants and native ants, and add
to existing knowledge of the role of competition
in structuring communities, a series of field
experiments was designed in Doñana National
Park, southern Spain, where the Argentine ant
has recently become established. The main objectives of the study were to determine its position in
the dominance hierarchy with respect to native
species, and to determine how this affects its
success as an invader.
Experimental
Study site
Doñana National Park is located on the southwest coast of the Iberian Peninsula (provinces of
Huelva and Seville, Spain) and covers an area of
approximately 56,544 ha, which includes a large
area of marsh at the mouths of the Guadalquivir
and Guadiamar rivers. The local climate is ‘‘subhumid’’ Mediterranean, because of the effect of
the Atlantic, and, according to Gaussen’s (1968)
classification, can be included in the Mediterranean climatic region.
The vegetation consists mostly of scrubland,
sparsely populated with large isolated cork oaks
(Quercus suber) and patches of introduced pines
(Pinus pinea). As a result of its rolling topography, a legacy of the sand dune origin of the
region, and a shallow water table, the higher areas
are characterized by xerophytic vegetation and
the lower, damper, areas are characterized by
hygrophytic vegetation. A full description of the
habitat of Doñana National Park can be found in
Carpintero et al. (2003).
This study was undertaken in a pinewood next
to the Doñana visitors’ center at ‘‘El Acebuche’’.
The vegetation in the study area consisted of
Mediterranean stone pine (Pinus pinea), and an
understorey of Mediterranean scrub mostly comprising Cistus libanotis, Cistus salvifolius, Lygos
monosperma, Rosmarinus officinalis, Halimium
halimifolium, Lavandula stoechas, Thymus vulgaris, Ulex minor, and Cistus albidus.
Methods
The Argentine ant completely monopolized the
immediate vicinity of the visitors’ center. At the
limit of its local range, some distance from
the visitors’ center, Argentine ants and native
species were both found (Fig. 1). In this area of
overlap, six samples of tuna bait in 10 cm · 12 cm
plastic trays were placed on a 2 · 3 grid at 4-m
intervals. Tuna is often used as bait in studies of
interactions between ground-living ants (Andersen and Patel 1994; Human and Gordon 1999;
Savolainen and Vepsäläinen 1988; Torres 1984)
and in a previous experiment performed in the
same area using a variety of bait, tuna bait was
shown to attract all species present.
Bait is commonly used in studies of agonistic
interactions in ants (Cerdá et al. 1998; Holway
1999; Savolainen and Vepsäläinen 1988). Normally, when individual workers of different species
meet they move away from each other immediately. Sometimes the more aggressive species may
attack but these attacks are usually unsuccessful
(Jones and Phillips 1987). When the number of
opponents increases, however, for example around
high quality food sources, for example bait, the
opportunity for escape or evasion decreases, and
both intra and interspecific fighting and aggression
are common (Cerdá et al. 1998; Holway 1999;
Levings and Traniello 1981; Phillips et al. 1986).
The work was conducted over three days each
in May, July, and September 1990. For each hour
of daylight continuous 10-min observations were
made of each of the six bait stations. In May and
September, observations began at 9:00 am and
finished at 8:00 pm. In July observations lasted
from 8:00 am to 9:00 pm.
During each observation a record was kept of
the identity and the number of each ant species
on the bait, and of the type of behavioral
interactions observed. Each observation was
allocated to one of four categories:
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Biol Invasions
Fig. 1 Study site. Pine
forest close to the Doñana
visitors’ center ‘‘El
Acebuche’’, showing the
area of overlap of
Argentine ants and native
species (at a distance of
25–80 m from the center)
A only one species seen on the bait;
B two or more species present but no aggressive
interactions observed;
C two or more species on the bait interacting
aggressively; and
D no ants observed on the bait during the 10min observation period.
Behavior during agonistic encounters between
species was classified as follows:
Aggressive behavior
Physical attack: The attacker bites the body,
antennae or legs of its antagonist.
Chemical attack: The attacker bends its abdomen forward and directs a noxious secretion at
its enemy.
Threat: The individual faces its opponent with
open mandibles.
Submissive behavior
Escape: The individual moves rapidly away
after making contact with another individual.
Other behavior
Indifference: After making contact, the individual shows neither aggressive nor submissive
behavior.
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Results
During the experiment bait was visited by seven
ant species. Two of these (Camponotus lateralis
and Messor marocanus) were seen very infrequently (n = 3 individuals) and were not included
in analyses. All six bait stations were used by the
five most abundant species (n = 174 individuals:
Linepithema humile, Pheidole pallidula, Tapinoma nigerrima, Aphaenogaster senilis, Cataglyphis
floricola), apart from bait station 1 which was
never used by T. nigerrima. Colony and worker
size, foraging strategy and diet for each of these
five species are shown in Table 1.
A total of 684, 10-min observations were made
of the bait stations. The frequency of each class of
observation A–D (Methods section) is shown in
Fig. 2. Observations were not distributed evenly
across classes (v2 = 515.90, P < 0.001). The most
frequent class of observation was type A (only
one species seen on the bait) indicating that ants
rarely share bait stations. The least frequent class
was type B (two or more species present but no
aggressive interactions observed), indicating that
not only did ants rarely share baits, but also when
they did they usually interacted aggressively
(72.6% of observations with >1 species
and aggressive interactions). There was also a
Biol Invasions
Table 1 Worker and colony size, type of recruitment and diet of the most abundant species found at the bait stations
Species
Worker Size (mm)
Colony Size
Recruitment
Diet
L. humile (*)
P. pallidula (*)
T. nigerrima (**)
A. senilis (***)
C. floricola (****)
2.1–2.6
1.6–2.6
2.8–5.1
6.4–7.7
5.4–6.7
Thousands
Thousands
Thousands
Hundreds
Hundreds
Mass
Mass
Mass
Group
No recruitment
Omnivore (honeydew)
Omnivore (graminivore)
Omnivore (honeydew)
Omnivore
Petals + insects
Terms in parentheses indicate favored food types. Data from (*), Bernard 1968; (**), Cerdá et al. 1998; (***), Gómez and
Espadaler 1996; (****), Tinaut 1993 and Cerdá et al. 1996
Class D
(n=218)
Class A
(n=393)
Class C
(n=53)
Class B
(n=20)
type C, where different species interact aggressively on the bait stations, the mean number of
individuals of each species was greater than for
type B, suggesting that abundance is important in
prompting aggressive interactions. For species
with mass recruitment, the mean number of
individuals counted during class A observations
was significantly different from the mean number
counted during class B and class C observations
(Mann–Whitney U test, P < 0.005, in all cases).
Agonistic interactions between species
Fig. 2 Frequencies of observations of each class: A = only
one species seen on the bait; B = two or more species with
no aggressive interactions; C = two or more species with
aggressive interactions; D = no ants seen
relatively high frequency of observations of type
D (31.9%) when no ants were seen on the bait.
This phenomenon has been reported in several
studies, which have shown that the borders
between the territories of some dominant species
constitute a ‘‘no man’s land’’ low in ant abundance and species richness (Adams 1994; Mabelis
1984; Mercier et al. 1997).
For each species, the frequency of observations
in each class and the mean number of individuals
seen on the bait are shown in Table 2. When only
one species was observed on the bait (observation
class A), those species with mass recruitment
(L. humile, P. pallidula, T. nigerrima) were present in relatively large numbers (Table 2). In those
observations where two or more species shared
the bait but did not interact aggressively (class B)
there were few individuals present, even of massrecruiting species. Two or more species can only
coexist on a bait station without conflict if very
few individuals are present. In observations of
Species altered their behavior depending on the
number of colony-members present on the bait,
and on whether they were initiating or responding
to a confrontation (Table 3).
During encounters, species tended to initiate
attacks if there were more individuals of their
own species on the bait, and escape if there were
fewer, with the exception of C. floricola, for which
aggressive behavior was never observed. Indeed,
the numbers of individuals present on bait when
encounters resulted in initiation of attack and
escape differed significantly (Kruskal–Wallis test:
H = 1.82, P = 0.0001, n = 341). A similar abundance pattern was observed for responses to
encounters, although differences were not significant (Kruskal–Wallis test: H = 1.22, P = 0.27,
n = 422).
Individual behavior also depended upon
whether the ant was initiating or responding to
behavior during an encounter. Species initiating
encounters tended to be more aggressive (M-L,
v2 = 12.5, df = 4, P = 0.0140) whereas those
on the receiving end usually, but not always,
behaved submissively (M-L, v2 = 16.84, df = 4,
P = 0.0021). This was reflected in the frequencies
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Biol Invasions
Table 2 Frequencies of observations of each class (N) and the associated mean (s.d.) number of individuals on the bait
Class A
Class B
Class C
L. humile
P. pallidula
T. nigerrima
A. senilis
C. floricola
N = 191
36.8 ± 51.1
N = 15
2.3 ± 2.2
N = 39
6.1 ± 13.1
N = 54
39.3 ± 44.8
N = 11
2.7 ± 1.6
N = 32
20.8 ± 33.3
N = 28
30.7 ± 31.6
N=4
1.0 ± 0.0
N=9
2.8 ± 1.9
N = 11
2.0 ± 2.0
N=8
1.5 ± 0.7
N = 26
5.4 ± 7.3
N = 108
1.9 ± 1.7
N=6
1.5 ± 0.5
N=7
2.6 ± 2.9
Class A = only one species seen on the bait; B = two or more species with no aggressive interactions; C = two or more
species with aggressive interactions
Table 3 Frequency of encounters (N) classified by behavior type (aggression: physical attack, chemical attack and
threat; submission: escape) of individuals initiating and
L. humile
P. pallidula
T. nigerrima
Aggression (action)
Aggression (response)
Submission (response)
Submission (action)
38.7 ± 43.8
N = 124
58.6 ± 37.6
N = 55
3.2 ± 3.1
N=8
8.3 ± 8.8
N=9
65 ± 49.5
N=2
1
N=1
3.5 ± 0.7
N=2
1±0
N=2
1±0
N=2
N=0
12.6 ± 8.6
N = 148
N=0
3.6 ± 1.5
N=8
8.6 ± 16.4
N = 69
14.6 ± 18.4
N = 146
1.4 ± 0.6
N = 69
2.6 ± 2.5
N = 17
2.5 ± 1.6
N = 93
C. floricola
A. senilis
of observations of initiation and response associated with aggression or escape. The frequency of
encounters involving aggressive behavior (physical attack, chemical attack, and threat) was
98.24% for individuals initiating encounters (actors) (n = 341) compared with only 4.83% for
individuals responding to encounters (receivers)
(n = 414). The frequency of encounters involving
submissive behavior (escapes) was 1.76% for
actors (n = 341) and 95.17% for receivers
(n = 414). Whether an individual acted as an
actor or receiver depended on the number of
conspecifics on the bait, because for all species the
mean number of conspecifics present for actors
was greater than for receivers (30.8 ± 40.3 (s.d.)
compared with 8.0 ± 4.5; Kruskal–Wallis test:
H = 221.9, P = 0, n = 902).
The most common form of aggressive behavior
observed for all species was physical attack, which
accounted for 90.98% of all aggressive encounters. The only species observed to carry out
chemical attacks was L. humile when confronted
by T. nigerrima, but this occurred much less
frequently than physical attacks (five occasions
123
responding to encounters, with the mean number of
conspecifics ± s.d. on the bait at the time of encounter
N=0
N=0
only). The only submissive behavior observed was
escape. Only ten fatal attacks were observed: on
four occasions A. senilis killed L. humile workers,
and on six occasions the same species killed
P. pallidula workers.
Displacements of ant species from bait
Bait stations were not always occupied by the
same species, and replacement of one species on a
bait station by another reflected daily or seasonal
activity patterns (unpublished data) and the
outcome of conflicts. For example, during the
cooler times of day, in the morning and late
afternoon, bait was occupied by L. humile,
P. pallidula, T. nigerrima, or A. senilis whereas
during the hottest period, around mid-day, it was
occupied by the thermophilous C. floricola
(Tinaut 1993). Such patterns of dual bait occupancy do not suggest aggressive displacement.
On other occasions, however, a species took
over a bait station initially occupied by another
species after an aggressive encounter. The only
species recorded to take over a bait station
Biol Invasions
already occupied by a large number of workers of
another species was the Argentine ant (on two
occasions they displaced P. pallidula and on
one occasion A. senilis). Although A. senilis,
T. nigerrima, and P. pallidula sometimes initiated
fights and attempted to take food from bait
stations already occupied by large numbers of
another species, they were never observed to
succeed in displacing their opponents.
In one of the two cases of aggressive displacement of P. pallidula by L. humile, which occurred
in July, the Argentine ant was observed to form a
broad trail from the bait to the nest of the
displaced P. pallidula within an hour of arrival.
In this instance P. pallidula did not put up much
aggressive resistance. Not only did the Argentine
ants succeed in occupying the bait station, they
also entered the nest of P. pallidula and, shortly
afterward, workers of the Argentine ant were seen
removing larvae of the native species, thus confirming brood predation (as suggested by Zee and
Holway 2006). The following day, P. pallidula had
completely disappeared from the area and only
workers of L. humile were seen entering and
leaving the nest. In the second instance of aggressive displacement of P. pallidula by L. humile, this
time in September, the same situation was
observed, with complete displacement of P. pallidula from the bait then occupation of its nest. In
contrast, on two occasions when skirmishes were
observed between relatively small numbers of
L. humile and P. pallidula workers at bait stations,
it was P. pallidula rather than the Argentine ant
that gained control of the bait station.
On the occasion of aggressive displacement of
A. senilis by L. humile six individual workers of
A. senilis showing very aggressive behavior were
seen on the bait, suggesting recruitment to the
bait station. Despite this, Argentine ants moved
on to the bait and, although A. senilis killed some
workers of the introduced species, they eventually
had to surrender the bait station. On two other
occasions, however, A. senilis was seen to successfully defend bait stations against mass-recruiting species—once they held the bait station
against approximately forty P. pallidula workers
trying to take food; on another occasion they
actively defended the bait against a similar
number of L. humile workers.
Seasonal patterns in the activity of different
species (unpublished data) might also have
affected the occupancy of bait stations; such
patterns could explain, for example, why
T. nigerrima was seen only in May. But longterm species displacement patterns were observed
that cannot be accounted for by seasonal activity.
For example, during the last month of sampling,
L. humile was the only species found at some bait
stations, suggesting the introduced species had
expanded its range (Fig. 3).
Discussion
Ant species present in the study area rarely
shared bait stations. When two or more species
were present on the same bait encounters
between workers were generally antagonistic
(Fig. 2); it was thus possible to develop a
dominance hierarchy for the species present.
C. floricola never behaved aggressively and
always fled from bait stations in the presence of
other species (Table 3) and so was placed at the
bottom of the hierarchy. The level of aggression
shown by a species is often related to its diet and
social structure; species living in small colonies,
for example, tend to be less aggressive than those
forming very large colonies. Interference competition is most likely to be observed for species
exploiting large and/or predictably-located food
resources (Holway 1999; Levings and Traniello
100
80
60
40
20
0
MAY
JULY
C. floricola
A. senilis
P. pallidula
L. humile
SEPTEMBER
T. nigerrima
Fig. 3 Percentage of monthly bait-station observations
associated with the occupancy of each species (n = 684)
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Biol Invasions
1981; Phillips et al. 1986). The diet of C. floricola
consists largely of small dead insects randomly
distributed in the environment, typically harvested by solitary foragers. Unusually for its
genus, C. floricola gathers large numbers of
Halimium halimifolium petals which also provide
a limited, seasonal food resource, thus further
promoting a non-aggressive ‘‘scramble’’ harvesting strategy (Cerdá et al. 1996). The colonies of
this species are small, so it would be risky and
expensive to be aggressive towards neighbors and
defend a territory (Levings and Traniello 1981).
The other native species occupy the next level
in the hierarchy and actively defend food sources
and their nests, leading to territories that change
in size and shape over time (Hölldobler and
Lumsden 1980; Hölldobler and Wilson 1990). All
these species recruit conspecifics to exploit and
defend food resources. P. pallidula and T. nigerrima recruit many workers (>100 ants) to food
sources (mass recruitment), leading to the formation of food trails (Detrain et al. 1991), whereas
A. senilis recruits workers in smaller numbers
(<100 ants, group recruitment) (Cerdá et al. 1988;
Gómez and Espadaler 1996). The first species to
occupy a bait station in large numbers maintains
its ownership of the bait station. There were no
instances of a bait station held by large numbers
of workers of one native species being taken over
by another. For these species many factors
contribute to obtaining and defending resources,
including efficiency and speed in locating new
food resources, distance to the nest, colony size,
and recruitment efficiency (Eldridge and Traniello 1981). The observation that the first group or
individual to occupy a resource will hold it against
competitors has been reported for other animal
species, including other ant species (Maynard
Smith and Parker 1976; Torres 1984). Describing
this finding, Hölldobler and Wilson (1990) quoted
a remark made by General Nathan Bedford
Forrest during the American Civil War: ‘‘The
winners arrive on the battlefield first with the
greatest numbers.’’ When these species become
owners of a bait station their levels of aggression
increase. These species are relatively submissive
when they do not have ownership of the bait,
however (Table 3), although individuals will try
to steal bait from occupied stations.
123
The Argentine ant maintains larger fixed territories, not just to monopolize particular food
sources but also to control the entire foraging
area by excluding all other ant species (Fluker
and Beardsley 1970; Human and Gordon 1999;
Sanders et al. 2001; Wilson 1971). The territoriality of the Argentine ant is similar to that of
other dominant species (Adams 1994; Gordon
1995; Hölldobler and Wilson 1990; Traniello and
Levins 1986)—several nests are scattered
throughout the territory rather than concentrated
in the center. Groups of workers with queens and/
or young can be found in all areas of the territory.
This nest arrangement enables a large proportion
of the area encompassed within these large
territories to be efficiently patrolled and exploited
while simultaneously avoiding the high cost of
with transporting food from distant locations to a
single central nest. The Argentine ant has even
been observed to move its young after finding a
new food source (Holway and Case 2000). This
system has important implications for optimum
territory size—if the cost of territory defense is
proportional to perimeter length, and benefits are
proportional to territory area, then territories
should be as large as possible (i.e. maximizing the
perimeter-to-area ratio). Indeed, in polygynous
and polycalic species, for example L. humile,
territory sizes are limited only by the availability
of suitable habitat (Hölldobler and Lumsden
1980; Holway and Case 2000).
In the area bordering the range of the introduced ant, both L. humile and native species
(except C. floricola) altered their behavior
depending upon the number of conspecific workers present on the bait. This suggests that
L. humile, P. pallidula, T. nigerrima, and A. senilis
adopt the ‘‘bourgeois strategy’’ (Maynard Smith
and Parker 1976; Rasmusen 1989), behaving both
as ‘‘hawks’’ (aggressive behavior) and as ‘‘doves’’
(submissive behavior) depending on ownership of
the bait. This pattern of increased aggression
triggered by the presence of large numbers of
conspecifics associated with ownership of a food
resource or proximity to a nest has also been
observed in other ant species (Cammaerts and
Cammaerts 1996; Le Moli et al. 1984; Mabelis
1984; Mayades et al. 1993; Mercier et al. 1997;
Wenseleers et al. 2002). The mechanisms
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responsible for changing aggressive behavior
were not examined here, but other studies, for
example that of Cammaerts and Cammaerts
(1996) on P. pallidula, found that workers use
pheromones to identify shifting territories.
Another study has described A. senilis as a
subordinate species with little aggression (Cerdá
et al. 1998). Here, by contrast, when a sufficient
number of workers were present this species
fiercely defended bait stations and was the only
species that actually killed workers of other
species while defending bait. When few conspecific workers were present and the bait was held
by another species, however, they never behaved
aggressively and always fled after encounters with
other species. Individual workers of A. senilis
were observed to snatch pieces of bait and then
retreat rapidly. This behavior has been observed
in other species of Aphaenogaster (A. rudis) and
has been called the ‘‘jackal strategy’’ (Lynch et al.
1980).
The Argentine ant was the only species capable
of aggressively taking control of bait stations
already wholly occupied by another species. The
occupancy of bait stations by the Argentine ant
also increased over time (Fig. 3). This observation
is not consistent with any seasonal activity patterns, but rather suggests displacement of native
ants from the study area by this exotic species.
The idea of competitive displacement is supported
by two cases in which Argentine ants were seen to
expel P. pallidula colonies from their nests after
forcing them from baits. It is not known whether
these colonies were destroyed or just displaced, as
reported in other studies of this and other Pheidole species (Detrain and Pasteels 1992; Fluker
and Beardsley 1970). In any case, the Argentine
ant has a substantial negative effect on the fitness
of competitors, by forcing antagonists to waste
time and energy escaping and rebuilding nests and
by forcing displaced colonies to risk competing
with other colonies of the same or other species
(Gordon 1995). Although the competitive ‘‘bourgeois’’ strategy of individual Argentine ants on
bait stations is used by several species, the ability
of the Argentine ant to form large multi-nest
colonies (Hee et al. 2000; Holway 1999; Human
and Gordon 1999; Tsutsui et al. 2001) seems to
give them the edge when competing for resources
(bait) and territories. According to several
authors, aggressive behavior is an important
component of dominance, because it often results
in the establishment of a status enabling privileged access to resources such as food or space.
Levels of ant aggression are determined by their
position in the hierarchy and by worker density. In
general, the more aggressive and the greater the
dynamic density (individuals dm–2 min–1) of a
colony, the higher the position of the colony
in the dominance hierarchy (Savolainen and
Vepsäläinen 1988). As noted in other studies of
invasive species (Hook and Porter 1990, Dame
and Petren 2006), this emphasizes the importance
of considering behavioral mechanisms when trying to understand the success of aliens in native
ecosystems.
Despite the negative effects of this species on
ecosystems, few studies have addressed the effect
and distribution of the Argentine ant in Spanish
protected natural spaces (Carpintero et al. 2003;
Carpintero et al. 2005). There is currently no
concrete program for the future monitoring and
management of this invasive species in Doñana
National Park.
Acknowledgments The authors would to thank Antonio
Priego and Rafa ‘‘el francés’’ for their assistance in the
field. David Williams and Ricardo Reques provided many
of the bibliographical references, and Alberto Tinaut
cleared up all uncertainties about species identification.
Our thanks to Carmen Ortega, Alfonso Carpintero, Sylvia
Williams, and all the staff and colleagues at Doñana for
their help and kindness. We would like also to thank the
anonymous referees for valuable comments and
suggestions. This work was supported by a grant from
the Comunidad Autónoma de Andalucı́a to S. Carpintero.
The experiments comply with current legislation in Spain,
where they were performed.
References
Adams ES (1994) Territory defense by the ant Azteca
trigona: maintenance of an arboreal ant mosaic.
Oecologia 97:202–208
Andersen AN, Patel AD (1994) Meat ants as dominant
members of Australian ant communities: an experimental test of their influence on the foraging success
and forager abundance of other species. Oecologia
98:15–24
Arim M, Abades SR, Neill PE, Lima M, Marquet PA
(2006) Spread dynamics of invasive species. Proc Nat
Acad Sci USA 103(2):374–378
123
Biol Invasions
Bernard F (1968) Les fourmis (Hymenoptera Formicidae)
d’Europe occidentale et septentrionale. Faune de
l’Europe et du Bassin Méditerranéen. Ed. Masson.
Paris
Cammaerts MC, Cammaerts R (1996) Area marking in the
ant Pheidole pallidula. Behav Processes 37:21–30
Carpintero S, Reyes-López J, Arias de Reyna L (2003)
Impact of human dwellings on the distribution of the
exotic ant Argentine ant: a case study in the Doñana
National Park, Spain. Biol Conserv 115:279–289
Carpintero S, Reyes-López J, Arias de Reyna L (2005)
Impact of Argentine ants Linepithema humile) on an
arboreal ant community in Doñana National Park,
Spain. Biodivers Conserv 14:151–163
Cerdá X, Retana J, Carpintero S, Cros S (1996) An unusual ant diet: Cataglyphis floricola feeding on petals.
Insectes Soc 43:101–104
Cerdá X, Retana J, Cros S (1997) Thermal disruption of
transitive hierarchies in Mediterranean ant communities. J Animal Ecol 66:363–374
Cerdá X, Retana J, Cros S (1998) Critical thermal limits in
Mediterranean ant species: trade-off between mortality risk and foraging performance. Funct Ecol
12:45–55
Dame A, Petren K (2006) Behavioural mechanisms of
invasion and displacement in Pacific island geckos
(Hemidactylus). Animal Behav (71):1165–1173
Detrain C, Deneubourg JL, Goss S, Quinet Y (1991)
Dynamics of collective exploration in the ant Pheidole
pallidula. Psyche 98(1):21–31
Detrain C, Pasteels JM (1992) Caste polyethism and collective defense in the ant Pheidole pallidula: the outcome of quantitative differences in recruitment.
Behav Ecol Sociobiol 29:405–412
DeVries H (1998) Finding a dominance order most consistent with a linear hierarchy: a new procedure and
review. Animal Behav 55:827–843
Drews C (1993) The concept and definition of dominance
in animal behaviour. Behaviour 125(3–4):283–290
Eldridge SA, Traniello FA (1981) Chemical interference
competition by Monomorium minimum (Hymenoptera: Formicidae). Oecologia 51:265–270
Feener DH (2000) Is the assembly of ant communities
mediated by parasitoids? Oikos 90:79–88
Fluker SS, Beardsley JW (1970) Sympatric associations of
three ants: Iridomyrmex humilis, Pheidole megacephala and Anoplolepis longipes in Hawaii. Ann Entomol Soc Am 63:1290–1296
Fowler HG, Schlindwein MN, Medeiros MA (1994) Exotic
ants and community simplification in Brazil: a review
of the impact of exotic ants on native ant assemblages.
In: Williams DF (ed) Exotic ants. Biology, Impact,
and control of introduced species. Westview Press,
Boulder, CO, pp 151–162
Fox BJ, Fox MD, Archer E (1985) Experimental confirmation of competition between two dominant species
of Iridomyrmex (Hym.: Formicidae). Aust J Ecol
10:105–110
Gaussen H (1968) Les indices sérothermique et hygrotermique en Péninsule Hispanique et en Africa du Nord
partie N.W. Collectanea Botán 7:499–504
123
Gómez C, Espadaler X (1996) Distancias de forrajeo,
áreas de forrajeo y distribución espacial de Aphaenogaster senilis Mayr (Hym. Formicidae). Miscellánia
Zool 19(2):19–25
Gordon DH (1995) The development of an ant colonýs
foraging range. Animal Behav 49:649–659
Hee JJ, Holway DA, Suarez AV, Case TJ (2000) Role of
propagule size in the success of incipient colonies of
the invasive Argentine ant. Conserv Biol 14(2):559–
563
Hölldobler B, Lumsden CJ (1980) Territorial strategies in
ants. Science 210:732–739
Hölldobler B, Wilson EO (1990) The ants. Springer-Verlag, Berlin
Holway DA (1999) Competitive mechanisms underlying
the displacement of native ants by the invasive
argentine ant. Ecology 80(1):238–251
Holway DA, Case TJ (2000) Mechanisms of dispersed
central-place foraging in polydomous colonies of the
Argentine ant. Animal Behav 59:433–441
Holway DA, Suarez AV, Case TJ (1998) Loss of intraspecific aggression in the success of a widespread
invasive social insect. Science 282:949–952
Hook AW, Porter SD (1990) Destruction of harvester ant
colonies by invading fire ants in south-central Texas
(Hym.: Formicidae). Southwest Nat 35:477–478
Human KG, Gordon DM (1999) Behavioral interactions
of the invasive Argentine ant with native ant species.
Insectes Soc 46:159–163
Jones SR, Phillips SA (1987) Aggressive and defensive
propensities of Solenopsis invicta (Hym.: Formicidae)
and three indigenous ant species in Texas. Tex J Sci
39(2):107–115
Le Moli F, Mori A, Parmigiani S (1984). Studies on
interspecific aggression among red wood ant species.
Formica rufa L. vs Formica lugubris Zett. (Hym.:
Formicidae). Monitore Zool Ital (N.S.) 18:41–51
Levings SC, Traniello JFA (1981) Territoriality, nest dispersion, and community structure in ants. Psyche
88:265–319
Liang D, Silverman J (2000) ‘‘You are what you eat’’: Diet
modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile.
Naturwissenschaften 87:412–416
Lynch JF, Balinsky EC, Vail SG (1980) Foraging patterns
in three sympatric forest ant species, Prenolepis imparis, Paratrechina melanderi and Aphaenogaster
rudis (Hymenoptera: Formicidae). Ecol Entomol
5:353–371
Mabelis AA (1984) Interference between Wood ants and
other ant species (Hymenoptera, Formicidae). Neth J
Zool 34(1):1–20
Majer JD (1994) Spread of Argentine ants (Linepithema
humile), with special reference to western Australia.
In: Williams DF (ed) Exotic ants. Biology, impact,
and control of introduced species. Westview Press,
Oxford, pp 161–173
Mayade S, Cammaerts M-C, Suzzoni JP (1993) Homerange marking and territorial marking in Cataglyphis
cursor (Hymenoptera, Formicidae). Behav Processes
30(2):131–142
Biol Invasions
Maynard Smith J, Parker GA (1976) The logic of asymmetric contests. Animal Behav 24:159–175
Mercier JL, Lenoir A, Dejean A (1997) Ritualised versus
aggressive behaviours displayed by Polyrhachis laboriosa (F. Smith) during intraspecific competition. Behav Processes 41:39–50
Passera L (1994) Characteristics of tramp species. In:
Williams DF (ed) Exotic ants. Biology, impact, and
control of introduced species. Westview Press, Oxford, pp 23–43
Passera L, Roncim E, Kaufmann B, Keller L (1996) Increased soldier production in ant colonies exposed to
intraspecific competition. Nature 379:630–631
Perfecto I (1994) Foraging behavior as a determinant of
asymmetric competitive interaction between two ant
species in a tropical agroecosystem. Oecologia
98:184–192
Phillips SA, Jones SR, Claborn DM (1986) Temporal
foraging patterns of Solenopsis invicta and native ants
of Central Texas. In: Lofgren CS, Vander Meer RK
(eds) Fire ants and leafcutting ants: biology and
management. Westview Press, Boulder, CO
Pisarski B, Vepsäläinen K (1989) Competition hierarchies
in ant communities (Hym., Formicidae). Ann Zool
Warszawa 42(13):321–328
Punttila P, Haila Y, Niemelä J, Pajunen T (1994) Ant
communities in fragments of old-growth taiga and
managed surroundings. Ann Zool Fennici 31:131–144
Rasmusen E (1989) Games and information. An introduction to Game Theory. Blackwell ed., Oxford
Sanders NJ, Barton KE, Gordon DM (2001) Long-term
dynamics of the distribution of the invasive Argentine
ant, Linepithema humile, and native ant taxa in
northern California. Oecologia 127:123–130
Savolainen R (1990) Colony success of the submissive ant
Formica fusca within territories of the dominant
Formica polyctena. Ecological Entomology 15:79–85
Savolainen R, Vepsäläinen K (1988) A competition
hierarchy among boreal ants: impact on resource
partitioning and community structure. Oikos 51:135–
155
Suarez AV, Bolger DT, Case TJ (1998) Effects of fragmentation and invasion on native ant communities
in coastal Southern California. Ecology 79(6):2041–
2056
Suarez AV, Tsutsui ND, Holway DA, Case TJ (1999)
Behavioral and genetic differentiation between native
and introduced populations of the Argentine ant. Biol
Invas 1:1–11
Tinaut A (1993) Cataglyphis floricola nov. sp. new species
for the genus Cataglyphis Förster, 1850 (Hymenoptera, Formicidae) in the Iberian Peninsula. Bull Soc
Entomol Suisse 66:123–134
Torres JA (1984) Niches and coexistence of ant communities in Puerto Rico: repeated patterns. Biotropica
16(4):284–295
Traniello JFA, Levings SC (1986) Intra- and intercolony
patterns of nest dispersion in the ant Lasius neoniger:
correlations with territoriality and foraging ecology.
Oecologia 69:413–419
Tsutsui ND, Suarez AV, Holway DA, Case TJ (2001)
Relationships among native and introduced populations of the Argentine ant (Linepithema humile) and
the source of introduced populations. Mol Ecol
10:2151–2161
Vander Meer RK, Jaffe K, Cedeno A (eds) (1990) Applied
myrmecology. A world perspective. Westview Studies
in Insect Biology, Boulder, San Francisco and Oxford
Vepsäläinen K, Pisarski B (1982) Assembly of island ant
communities. Ann Zool Fennici 19:327–335
Way MJ, Cammell ME, Paiva MR, Collingwood CA
(1997) Distribution and dynamics of the Argentine
ant Linepithema (Iridomyrmex) humile (Mayr) in
relation to vegetation, soil conditions, topography and
native competitor ants in Portugal. Insec Soc
44(4):415–433
Wenseleers T, Billen J, Hefetz A (2002) Territorial
marking in the desert ant Cataglyphis niger: does it
pay to play Bourgeois? J Ins Behav 15(1):85–93
Williams DF (ed) (1994) Exotic ants. Biology, impact, and
control of introduced species. Westview Press, Oxford
Wilson EO (1971) The insect societies. Harvard University
Press. Cambridge
Yamaguchi T (1992) Interspecific interference for nest
sites between Leptothorax congruus and Monomorium intrudens. Ins Soc 39:117–127
Zee J, Holway D (2006) Nest raiding by the invasive
Argentine ant on colonies of the harvester ant, Pogonomyrmex subnitidus. Insec Soc 53:161–167
123