Download Interference competition by Argentine ants displaces native ants

Biol Invasions (2007) 9:73–85
DOI 10.1007/s10530-006-9009-5
ORIGINAL PAPER
Interference competition by Argentine ants displaces native
ants: implications for biotic resistance to invasion
Alexei D. Rowles Æ Dennis J. O’Dowd
Received: 24 January 2006 / Accepted: 22 March 2006 / Published online: 8 June 2006
Springer Science+Business Media B.V. 2006
Abstract The Argentine ant Linepithema
humile (Dolichoderinae) is one of the most
widespread invasive ant species in the world.
Throughout its introduced range, it is associated with the loss or reduced abundance of
native ant species. The mechanisms by which
these native species are displaced have received limited attention, particularly in Australia. The role of interference competition in
the displacement of native ant species by L.
humile was examined in coastal vegetation in
central Victoria (southeastern Australia). Foragers from laboratory colonies placed in the
field consistently and rapidly displaced the
tyrant ant Iridomyrmex bicknelli, the bigheaded ant Pheidole sp. 2, and the pony ant
Rhytidoponera victoriae from baits. Numerical
and behavioural dominance enabled Argentine
ants to displace these ants in just 20 min; the
abundance of native species at baits declined
3.5–24 fold in direct relation to the rapid
A. D. Rowles Æ D. J. O’Dowd (&)
Australian Centre for Biodiversity, School of
Biological Sciences, Monash University, Clayton, Vic.
3800, Australia
e-mail: [email protected]
A. D. Rowles
Current address: Department of Entomology, North
Carolina State University, Campus Box 7613, Raleigh,
NC 27695-7613, USA
increase in L. humile. Most precipitous was the
decline of I. bicknelli, even though species in
this typically dominant genus have been
hypothesized to limit invasion of L. humile in
Australia. Interspecific aggression contributed
strongly to the competitive success of Argentine ants at baits. Fighting occurred in 50–75%
of all observed interactions between Argentine
and native ants. This study indicates that
Argentine ants recruit rapidly, numerically
dominate, and aggressively displace from baits
a range of Australian native ant species from
different subfamilies and functional groups.
Such direct displacement is likely to reduce
native biodiversity and indirectly alter food
web structure and ecosystem processes within
invaded areas. Biotic resistance to Argentine
ant invasion from native ants in this coastal
community in southeastern Australia is not
supported in this study.
Keywords Ant Æ Argentine Australia Æ Biotic
resistance Æ Interference competition Æ Invasion Æ
Iridomyrmex Æ Linepithema humile Æ nest raids
Introduction
Introduced ants are among the worst biological
invaders and sometimes cause large changes in the
structure and dynamics of recipient communities
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(Holway et al. 2002b; O’Dowd et al. 2003). Most
typically invasive ant species displace native ant
fauna (e.g. Haines and Haines 1978; Porter and
Savignano 1990; Hoffmann et al. 1999; Le Breton
et al. 2003). Argentine ants (Linepithema humile)
are no exception and cause large reductions in
abundances of native ants in California (e.g. Erickson 1971; Holway 1998a), Hawaii (Cole et al.
1992), South Africa (Bond and Slingsby 1984), and
Japan (Touyama et al. 2003). The mechanisms by
which Argentine ants displace native ant species
have been less widely explored, but have been
experimentally shown in California to rely on
superior ability in both exploitation and interference competition (Human and Gordon 1996;
Holway 1999).
One important factor in the competitive
asymmetry between Argentine ants and native
ants is the disparity in respective population
densities. Although unicoloniality may occur
within the native range of Argentine ants (Heller
2004), introduced populations are acutely unicolonial (Holway et al. 2002b) and combined with
genetically similar workers lacking intraspecific
aggression (Tsutsui et al. 2000; 2001), they can
form expansive supercolonies (Giraud et al. 2002;
Holway et al. 2002b). In the absence of intraspecific aggression, more resources may be allocated
to colony growth (Holway et al. 1998), providing
this invader with a numerical advantage and
allowing rapid recruitment of many workers.
These attributes help explain the proficiency of
L. humile in exploiting resources, but they are
only part of the requirements necessary for
effectively displacing or excluding native ant
species from a resource. Argentine ants also express pronounced physical aggression above levels normally occurring between competing ants
(Hölldobler and Wilson 1990; Human and Gordon 1999). Behavioural dominance via aggression
combined with extremely high abundance provide
the basis for ‘ecological dominance’ (Davidson
1998) which generates an interference ability that
transcends the small body size of L. humile relative to many native ant species (Ness et al. 2004).
Native ants are the most likely competitors of
Argentine ants and the large, diverse native ant
fauna in Australia (Shattuck 1999) may resist and
limit their invasion. Dominance by Iridomyrmex
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Rowles and O’Dowd
spp. in many Australian ant communities
(e.g. Greenslade 1976; Fox et al. 1985; Gibb and
Hochuli 2004), where they may dictate ant community composition (Andersen and Patel 1994),
has been proposed to limit Argentine ant invasion
on this continent (Majer 1994; Andersen 1997;
Walters and Mackay 2005). Nevertheless, evidence is scant; interference competition has been
examined with only two Iridomyrmex species
(Thomas and Holway 2005; Walters and Mackay
2005). Furthermore, Iridomyrmex does not dominate all regions and habitats (Greenslade and
Halliday 1982; Andersen 1986b) and biotic resistance by a broader array of Australian species has
not yet been explored.
This study tested interference competition between Argentine ants and three abundant native
ant species, including one species of Iridomyrmex,
in coastal vegetation in southeastern Australia. Its
outcomes help explain the mechanism of any
displacement or changes in abundance of these
species by Argentine ants, the behaviours used by
L. humile in interfering with the foraging of native ant species, and the likelihood that native
Australian ants can resist and limit invasion by
the Argentine ant.
Methods and materials
All observations and experiments were conducted
at two sites separated by 2.5 km in coastal scrub
vegetation along the boundary of the Mornington
Peninsula National Park, situated ~90 km southeast of Melbourne, in central Victoria, Australia.
Historically, native vegetation along this boundary has been anthropogenically disturbed and
subject to weed invasion (Calder 1975). Argentine ants have invaded from urban areas into
native coastal vegetation, creating a mosaic of
invaded and uninvaded sites along the boundary
(Rowles 2005). Argentine ants were collected
near Sorrento, 2.5 km northeast of the nearest
field site, extracted in the laboratory using a soilfree technique (T. Craven, pers. comm.), and
dispensed into laboratory colonies until each of
22 colonies contained 1500–1700 workers and 6
queens. This colony size was selected to allow a
competent measure of competitive ability and
Interference competition by Argentine ants
allow more meaningful comparisons with studies
elsewhere (Holway and Case 2001). These tests
are likely to be conservative because these laboratory colonies are considerably smaller than
established populations of L. humile at invaded
sites. Furthermore, colonies of this size provide
insight into the interaction strength of smaller
L. humile colony fragments likely to invade new
areas (Walters and Mackay 2005).
Each colony was housed within a clear plastic
container (26 cm long · 18 cm wide · 9 cm high)
with walls lined with Fluon (Polytetrafluoroethylene, 60 wt.% dispersion in water) to prevent
ant escape. A 0.5 cm exit hole was cut into one
end of each container and remained plugged until
used in experiments. A smaller plastic nest box
(8 cm · 8 cm · 4 cm water reservoir with an
8 cm · 8 cm · 0.5 cm nesting area above) covered in black plastic film was placed in each colony container. Ants were provided with 20%
sucrose solution daily and fed weekly with a
standard laboratory diet (Hölldobler and Wilson
1990), supplemented with live beetles. The colonies were given at least one month in the laboratory to settle before being used in field
experiments. Provision of food ceased 1 week
prior to experimentation.
Laboratory colonies were taken into the field
and experiments staged against field colonies of
three native ant species: Iridomyrmex bicknelli
(Dolichoderinae), Pheidole sp. 2 (Myrmicinae)
and Rhytidoponera victoriae (Ponerinae). These
three species were among the most common
native species at the sites (Rowles 2005).
Each represents a different sub-family and
functional group (Dominant Dolichoderinae,
Generalised Myrmicinae and Opportunists,
respectively—Greenslade 1978; Andersen 1990;
1997). Nevertheless, these native ant species
share similarities with the Argentine ant in that
they are epigeic, frequently associated with disturbed habitats, and have flexible foraging times
and relatively unspecialised diets (Andersen
1986a, b; Shattuck 1999). Furthermore, Iridomyrmex bicknelli and L. humile, formerly congeners (Shattuck 1992a, b), share many
morphological, population, and behavioural traits
that could increase ecological overlap and interspecific competition. The sizes of these ant species
75
varied. Only Pheidole sp. 2 (minors 2.2 – 0.1 mm
(SE) in length; n = 6) was smaller than the
Argentine ant (2.7 – 0.1 mm; n = 6), but Iridomyrmex bicknelli (4.3 – 0.1 mm, n = 6) and
R. victoriae (4.3 – 0.3 mm; n = 6) were larger.
All observations and experiments were conducted in March–April 2004 (austral autumn)
when activity of Argentine ants was highest at the
sites. After transport to field sites, the laboratory
colonies were kept in the shade for 30 min.
Experiments were conducted when native ants
were actively foraging. For both R. victoriae and
Pheidole sp. 2, this was from mid-morning to early
afternoon during both sunny and overcast conditions. Pheidole sp. 2 was tested at 18–24C while
the temperature was consistently ~20C during
experiments with R. victoriae. All tests of
I. bicknelli occurred during mid-afternoon under
warm, sunny conditions (20–25C). Unlike the
other two native species, I. bicknelli nest entrances occurred in less sheltered areas, often on
exposed sandy surfaces.
Experiments were replicated using five different field colonies for each of the three native
ant species. No native ant nest was reused. Of
the 22 L. humile laboratory colonies, four were
reused, but only after a gap of at least 3 days. If
foragers from the nest of a particular native
species did not colonise the bait or if Argentine
ants did not recruit to the resource, experiments
were discontinued. Such experiments were repeated to attain the required number of replicates.
A Before–After Control-Impact (BACI) design was used in the experiments. Paired bait trays
were used in each test, one which had L. humile
introduced as the impact, while the other functioned as a control. This allowed comparison of
the abundance of these species in the presence or
absence of Argentine ants while simultaneously
controlling for other factors (e.g. native ant colony size, microhabitat, time of observation). The
‘‘impact’’ and ‘‘control’’ baits were placed 20–
30 cm from the nest entrance, but on opposite
sides such that they were separated by approximately 40–60 cm. The bait station trays were
constructed from 90 mm plastic petri dish bases
with three sections of the 12 mm sidewall removed to provide access and the base lightly
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sanded to improve traction. The attractive bait,
tuna in vegetable oil and honey (approximately
2.5 gm of each), represented a range in dietary
requirements for these ant species.
Native ant workers were first allowed to colonise and forage at both bait trays; counts at the
bait trays were made every 5 min for 20 min.
Thereafter, Argentine ants from a laboratory
colony were given access to the randomly selected
‘‘impact’’ bait tray from 20 cm distance (i.e. the
same distance to the bait as the native ant nest).
After initial discovery of the bait by an Argentine
ant, counts of their and native ant abundances at
both the ‘‘impact’’ and ‘‘control’’ baits were made
at 5-min intervals for another 20 min. This
counting method was not well suited to the solitary foraging behaviour of Rhytidoponera victoriae, typical of the genus (Ward 1981; Pamilo et al.
1985). Instead, R. victoriae activity was determined by counting the total number of times that
workers entered each bait tray over each 20 min
period before and after L. humile introduction.
Behavioural interactions between Argentine
ants and each native species were assessed by
using the same categories as in assays for intraspecific aggression between Argentine ants from
different colonies (Suarez et al. 1999; Roulston
et al. 2003). Most interactions were one-on-one;
however, those involving more than one L. humile with a native worker were scored in the same
way. Category ‘‘ignore’’ (=0) included contacts
where no interest or aggression was displayed
whereas, if interest was shown via antennation, it
was considered a ‘‘touch’’ (=1). Contact where
both ants retreated from each other quickly was
scored as ‘‘avoid’’ (=2). Where contact included
lunging, biting or leg pulling it was regarded as
‘‘aggression’’ (=3); however, prolonged incidences of aggression, individuals locked together
and active flexing of gasters in the use of stings or
chemical defences, was instead scored as ‘‘fighting’’ (=4).
All tests conducted were analogous to typical
Before–After Control-Impact (BACI) designs.
The effects of Impact and Time (fixed factors) on
the abundance of each native ant species were
tested using a factorial Randomised Complete
Block design (RCB) (Quinn and Keough 2002).
‘‘Impact’’ (Argentine ant invaded and control)
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Rowles and O’Dowd
was compared between nests, but ‘‘Time’’ (before
and after Argentine ant invasion) was compared
within each nest (block). Logistics of the experiments required that both the impact and control
bait trays were supplied with native ant workers
from the same nest. While this removed independence from the design, despite the baits being
well separated physically, it did eliminate confounding issues. Separate hypothesis tests were
performed where Impact was tested against Impact · Nest (block) and Time was tested against
Time · Nest. The interaction of most interest in
this model was Impact · Time since it indicates
whether a difference occurred in native ant
abundance after the introduction of Argentine
ants. This interaction was tested against Impact · Nest · Time. As random factors cannot be
tested (Quinn and Keough 2002), no results could
be derived from Nest and its interactions. Prior to
analysis using SYSTAT (Wilkinson 2000), the
assumptions for ANOVA were checked using box
plots (normality) and by plotting the residuals of
the group means (homogeneity of variance).
Distribution and dispersion of count data for each
native ant species were greatly improved by
square-root transformation.
Native ant abundance at both bait trays was
counted before and after Argentine ant introduction. Because the time L. humile took to
locate baits varied (26.3 – 8.8 min (SE)), native
ant abundance just prior to L. humile discovery
of the bait was used as the ‘‘before’’ value for
I. bicknelli and Pheidole sp. 2 in these analyses.
For R. victoriae, the index of activity at the bait
trays was used for the 20 min immediately before bait discovery by L. humile. The ‘‘after’’
count for all three native species was taken
20 min after L. humile discovery of the ‘‘impact’’
tray.
Analysis of interspecific interactions after
L. humile invasion used the mean relative
frequencies of the five score categories across
n = 5 tests for each native ant species. Oneway ANOVAs followed by Tukey’s tests were
conducted separately for each of the three
native species (square-root transformed) to
determine any differences between the relative
frequencies of each interspecific interaction
category.
Interference competition by Argentine ants
77
Results
P = 0.270; Pheidole, F1,4 = 1.786, P = 0.252;
R. victoriae, F1,4 = 6.558, P = 0.063; Fig. 1).
Argentine ants significantly decreased the abundance of each of the native ant species at the
impact baits after 20 min, as indicated by the
significant Impact · Time interactions (Table 1,
Fig. 1). Compared to control baits, numbers of I.
bicknelli and Pheidole sp. 2 were reduced 24 and
9-fold, respectively, and the activity of R. victoriae
declined three-fold (Fig. 1). In contrast, abundances or activity of native species did not change
significantly at control baits in the absence of
All three native ant species tested (Iridomyrmex
bicknelli, Pheidole sp. 2 and Rhytidoponera victoriae) were almost completely displaced from
bait trays within 20 min of invasion (in 15 out of
15 experiments), aside from a few residual
workers of Pheidole sp. 2 and R. victoriae (Fig. 1).
The initial rate of recruitment by I. bicknelli and
Pheidole sp. 2 did not differ significantly between
impact and control bait trays, nor did the activity
of R. victoriae (I. bicknelli, F1,4 = 1.634,
No. of Worker Ants
80
Iridomyrmex bicknelli
(a)
Control
Impact
40
0
0
No. of Worker Ants
80
5
(b)
10
15
20
0
5
10
15
20
0
5
10 15
After (min)
20
Pheidole sp. 2
40
0
200
Activity Index
Fig. 1 Mean abundances
(–SE, n = 5) of three
native ant species (a,
Iridomyrmex bicknelli; b,
Pheidole sp 2; c,
Rhytidoponera victoriae)
at bait trays either
invaded (Impact) and
uninvaded (Control) by
Argentine ants
(Linepithema humile) at
times before and after
invasion. Both I. bicknelli
and Pheidole sp 2
abundance counts
indicate numbers
attending the bait trays at
5 min intervals over
20 min Time ‘‘0’’ before
and time ‘‘0’’ after
represent the initial point
of native ant bait
discovery and Argentine
ant discovery of the
impact bait, respectively.
An index of R. victoriae
activity at the bait trays
over 20 min before and
after invasion is given due
to the different counting
measure required for this
species. Note: differences
in scale on the y axes. See
text for detailed
description
5
10 15
Before (min)
0
(c)
20
Rhytidoponera victoriae
Control
Impact
100
0
Before
After
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78
Table 1 Three-factor
unreplicated ANOVAs
showing the effect of the
Argentine ant (Linepithema
humile) on the abundance
of (a) Iridomyrmex
bicknelli, (b) Pheidole sp 2,
and (c) Rhytidoponera
victoriae at baits. Blocked
within single nests of each
species (Nest effect), native
ant abundance was
compared before and after
Argentine ant invasion
(Time treatment) and
between paired bait trays;
one control bait free of
Argentine ants and another
bait where they were
introduced (Impact
treatment) (df = degrees of
freedom, MS = mean
squares, F = F-ratio,
P = probability). F-ratios
for Nest and Impact · Nest
could not be calculated. See
text for details
Rowles and O’Dowd
Source
(a) Iridomyrmex bicknelli
Between Nests
Impact
Nest
Impact · Nest
Within Nests
Time
Impact · Time
Nest · Time
Impact · Nest · Time
(b) Pheidole sp. 2
Between Nests
Impact
Nest
Impact · Nest
Within Nests
Time
Impact · Time
Nest · Time
Impact · Nest · Time
(c) Rhytidoponera victoriae
Between Nests
Impact
Nest
Impact · Nest
Within Nests
Time
Impact · Time
Nest · Time
Impact · Nest · Time
Argentine ants (for I. bicknelli, F1,4 = 2.142,
P = 0.217; Pheidole sp. 2, F1,4 = 0.054, P = 0.828;
R. victoriae, F1,4 = 4.052, P = 0.114).
Rapid recruitment and numerical dominance
at the bait assisted L. humile in displacing each of
the native species. Decline in the abundance of
the three native ant species at the impact baits
was directly related to the rapid recruitment by L.
humile during the 20 min after discovery (Fig. 2).
Workers of I. bicknelli, Pheidole sp. 2 and R.
victoriae at the impact baits were almost completely replaced by 3, 2 and 11 times more L.
humile (91.4 – 9.4, 135.6 – 32.2, and 150.0 – 41.6
workers, respectively) after 20 min (Fig. 2). This
strong inverse relationship highlights the ability
of L. humile to usurp control of an already
occupied resource. The overall decline of I.
bicknelli workers in the presence of Argentine
ants was far more rapid in comparison to either
Pheidole sp. 2 or R. victoriae (Fig. 2).
123
df
MS
F
P
1
4
4
6.467
0.308
2.869
2.254
–
–
0.208
–
–
1
1
4
4
45.754
20.348
4.207
1.185
10.867
17.173
–
–
0.030
0.014
–
–
1
4
4
17.815
10.711
3.639
4.895
–
–
0.091
–
–
1
1
4
4
38.175
43.416
3.598
1.570
10.610
27.656
–
–
0.031
0.006
–
–
1
4
4
1.343
21.008
5.815
0.231
–
–
0.656
–
–
1
1
4
4
6.996
65.695
4.768
3.679
1.467
17.856
–
–
0.292
0.013
–
–
Aggressive behaviour by the Argentine ant
also contributed to the displacement of native ant
workers from baits (Fig. 3). Both interaction frequency and strength of L. humile varied with
native species. In each case the relative frequency
of interaction categories was significantly skewed
towards fighting (I. bicknelli: F4,20 = 10.549,
P = 0.000; Pheidole sp. 2: F4,20 = 43.772,
P = 0.000; R. victoriae: F4,20 = 24.746, P = 0.000)
(Fig. 3). The low frequency of benign interactions
(e.g. ‘‘ignore’’, ‘‘touch’’ and ‘‘avoid’’) indicated
low tolerance between the Argentine ant and
these native species. Interaction strength was
greatest with Pheidole sp. 2, whose abundance at
baits (60 – 11.6 workers/bait) was more than
double that of other native species (I. bicknelli:
28.4 – 8.3; R. victoriae: 12.6 – 4.6) at the time
Argentine ants first discovered the bait (Fig. 2).
Furthermore, the relative frequency of fighting
was greatest with this species (Fig. 3b) but a few
Interference competition by Argentine ants
(a)
79
b
Fig. 2 Negative relationship between mean worker abundance (–SE, n = 5) for three native ant species and the
Argentine ant (Linepithema humile) at 0, 5, 10, 15 and
20 min after Argentine ant discovery of baits (a, Iridomyrmex bicknelli, R2 = 0.936, y = 60.931 x)0.9643; b, Pheidole sp
2, R2 = 0.910, y = )0.3455x + 54.809; c, Rhytidoponera
victoriae, R2 = 0.941, y = )0.0825 x + 13.648). Note: differences in scale on both the x and y axes
Iridomyrmex bicknelli
40
0
5
30
20
10
10
15
0
20
0
80
(b)
20
40
60
100
80
Pheidole sp. 2
0
Native ant abundance / bait tray
60
5
10
40
15
20
20
0
0
50
25
(c)
100
150
200
Rhytidoponera victoriae
20
5
15
0
10
10
15
5
20
0
0
50
100
150
200
Argentine ant abundance / bait tray
Pheidole sp. 2 remained at baits 20 min after
Argentine ant discovery (Fig. 2b). In contrast,
I. bicknelli workers were easily disturbed and
when alarmed by Argentine ants, scurried erratically over the bait trays. Consequently, they
showed a higher frequency of transient aggressive
exchanges with Argentine ants that did not lead
to prolonged fighting as well as a lower frequency
of fighting (Fig. 3a).
Over 75% of the 509 observed interactions
involved one-to-one fights between an Argentine
ant and a native ant. The remainder involved
‘‘group’’ attack (2–6 workers) by Argentine ants
on single native ants. Attacks by more than four
Argentine ants on a single native ant arose only
with Pheidole majors. There was no incidence of
multiple native opponents fighting lone Argentine
ants. Ants engaging in ‘‘fights’’ often became involved in prolonged grappling with frequent biting and flexing gasters in the direction of
opponents. Although the ultimate outcome of
each interaction was not determined, mortality
was observed in all species and occurred frequently in L. humile when the first round of
workers discovered the occupied bait.
While many Argentine ant workers remained
at the baits during the displacement of the native
ants, others frequently fought their way up their
foraging trails to the nest entrance. This occurred
in 4 of 5 experiments with each native ant species
(80% of all experiments). Ultimately, the invading Argentine ants attempted to breach the native
species nest entrances and they were frequently
successful in gaining entry. On average, fewer
L. humile workers were recorded entering the
nests of R. victoriae (9.8 – 3.8 L. humile workers)
compared to both I. bicknelli (15.3 – 9.2) and
Pheidole sp. 2 (14.5 – 7.4).
123
80
Rowles and O’Dowd
0.8
b
Fig. 3 Mean relative frequencies (–SE) of five categories
of behavioural interactions (0 = ignore, 1 = touch,
2 = avoid, 3 = aggression, 4 = fighting) between invading
Argentine ants (Linepithema humile) and native ant
species (a, Iridomyrmex bicknelli; b, Pheidole sp 2; and c,
Rhytidoponera victoriae) determined from a total of 133,
230 and 146 interactions observed across n = 5 tests for
each species, respectively. Bars with different letters differ
significantly (P < 0.05, Tukey’s test)
(a) Iridomyrmex bicknelli
c
0.6
bc
0.4
Discussion
ab
0.2
a
a
0.0
0
2
1
3
4
(b ) Pheidole sp. 2
c
Relative Frequency
0.8
0.6
0.4
b
0.2
ab
a
0.0
a
1
0
2
3
4
(c) Rhytidoponera victoriae
0.8
c
0.6
0.4
b
0.2
a
a
a
0.0
0
1
2
3
Behavioural Interaction
123
4
Interference competition is one mechanism by
which Argentine ants displace native ant species.
When L. humile discovered resources already
colonised by native ant species, they actively
displaced them through a combination of rapid
recruitment, high sustained numerical abundance,
and intense interspecific aggression. Furthermore,
they exhibited strong territoriality, usually fighting their way up foraging trails and raiding the
nests of each native species. These findings provide a mechanism that helps explain marked
compositional differences in ant communities
between sites invaded or uninvaded by Argentine
ants in coastal southeastern Australia (Rowles
2005). Given an appropriate match with abiotic
conditions (Human et al. 1998; Holway et al.
2002a) and disturbance regimes (Holway 2005),
and sufficient propagule pressure (Hee et al.
2000), this package of traits can lead to effective
invasion and displacement of native Australian
ants by Argentine ants.
Recruitment rates influence numerical abundance at baits and the outcome of interspecific
competition (Fellers 1987). Argentine ant workers rapidly achieved high numbers at the baits
relative to all three native species in our study,
consistent with findings in California (Human and
Gordon 1996; Holway 1998b). Outcomes are also
affected by the recruitment ability of native species in the recipient community. For example, the
low recruitment response by Rhytidoponera victoriae, whose numbers at baits were limited by
innately poor recruitment behaviour (Ward 1981;
Pamilo et al. 1985), would have contributed to its
displacement by L. humile. Although better able
Interference competition by Argentine ants
to recruit, both I. bicknelli and Pheidole sp. 2
were also unable to reach the numbers achieved
by these laboratory colonies of L. humile and this
reduced their competitiveness.
Colony size influences recruitment rates and
numerical abundance at baits. In our study, a
single colony size—1500 to 1700 workers and six
queens—was used to test interference competition, so the effect of colony size on the outcome is
unknown. Disparities between the size of the
Argentine ant laboratory colonies and those of
the three native species might have affected
competitive outcomes based on the abundance of
workers available to recruit. Nevertheless,
L. humile worker densities recruiting to baits in
these experiments (~125 workers per bait) were
lower than those recruiting to baits at nearby invaded sites (~175 workers per bait) with established populations of Argentine ants (Rowles
2005), meaning that these experimental tests are
likely to be conservative. While sizes of the native
ant colonies were unknown, not one was sufficient
to resist Argentine ants at the baits.
Numerical dominance and superior recruitment ability contributed to interference and displacement of competitors from baits by L. humile,
but strong, frequent, and consistent interspecific
aggression—fighting-was also key. Although we
recorded only the category of interspecific
aggression in each encounter, Argentine ants
initiated most interactions in other studies (Lieberburg et al. 1975; Human and Gordon 1999;
Holway and Case 2001). Nevertheless, L. humile
workers were not necessarily superior in one-onone interactions and they frequently perished in
individual bouts with native ants. In contrast,
whole colonies of L. humile were invariably successful in displacing native ants in our study.
Holway (1999) showed mixed success in one-onone interactions between Argentine ants and a
range of native ant species in California. However, at the colony-level, Argentine ants still displaced most native ants from baits. Similarly,
Morrison (2000) demonstrated that a larger
number of smaller workers were essential to the
competitive success of the red imported fire ant
S. invicta against a native ecological equivalent,
S. geminata. The greater success of colony-level
interactions over those between individual
81
workers illustrates that the capacity of Argentine
ants to interfere depends upon high local abundances. Consequently, the competitive advantage
of L. humile at baits seen in our study requires the
integration of strong recruitment, numerical
dominance, and interspecific aggression.
The strong interference ability of L. humile is
not limited to competition at food baits, as was
evident in their frequent nest raids in our study.
Breaching the nests of native ants by Argentine
ants has been witnessed before but probably does
not involve competition for nest space. Argentine
ants form shallow, often impermanent nests
(Newell and Barber 1913) distinct from those of
the three native ants examined here, and no evidence exists that they occupy the nests from which
they displace native ants (Holway 1999). This may
simply reflect the territorial behaviour of L. humile
and its intolerance of co-occurring epigeic ants
(e.g. Fluker and Beardsley 1970; De Kock 1990).
In combination with interference competition
reported here, Argentine ants also excel at
exploiting resources that would otherwise be used
by native ant species (Human and Gordon 1996;
Holway 1999). This exploitative ability also depends on numerical abundance where Argentine
ants find and recruit to baits more quickly, in
higher numbers, and for longer periods than native ants (Human and Gordon 1996; Holway
1998b; 1999). A trade-off is usually involved between interference and exploitative capacities
where dominant ants are better at interference
and subordinates at exploitation (Fellers 1987;
Andersen and Patel 1994). Argentine ants appear
able to break this trade off between the two forms
of competition (Holway 1999) due to their
behavioural and numerical dominance in invaded
areas (Davidson 1998). By escaping from the
competitive hierarchy thought to structure most
native ant communities, Argentine ants attain
ecological dominance and consequently a competitive advantage over these and many other
native ant species. Disruption of former structure
has meant that the remaining ant community is
now controlled by the competitive dominance of
this single invasive species (Sanders et al. 2003).
Tyrant ants (Iridomyrmex) dominate many
Australian ant communities and may confine the
spread of Argentine ants in natural areas (Majer
123
82
1994; Andersen 1997; Walters and Mackay 2005).
Not only is this genus taxonomically diverse
(Shattuck 1999), but shared attributes, including
large colony sizes (Greenslade and Halliday 1983),
high rates of activity and recruitment (Andersen
and Patel 1994), and extreme aggressiveness
(Andersen 1992; Andersen and Patel 1994) may
allow Iridomyrmex to structure ant communities
(Greenslade 1976; Fox et al. 1985; Andersen and
Patel 1994; Gibb and Hochuli 2004).
Tests of this biotic resistance are few, involving
either I. bicknelli or I. rufoniger, but the rapid and
consistent displacement of I. bicknelli by L. humile
in our field study indicated that it provides little
resistance to invasion at these sites. Interestingly,
I. bicknelli only occurred in the interior of invaded
sites where densities of Argentine ants were very
low (Rowles 2005). The only other results for
I. bicknelli are equivocal (Thomas and Holway
2005). Field tests of interspecific competition along
boundaries between L. humile and I. bicknelli in
and near Perth, Western Australia showed that
L. humile controlled two-thirds of baits, but
monopolised more under warm (25C) than hot
(33C) conditions. Furthermore, I. bicknelli prefers open, dry habitats (Andersen 1986b) where
they may be less likely to coincide with invading
Argentine ants. Thus, the strength of biotic resistance of Iridomyrmex to invading L. humile may
depend upon the mosaic of microclimate and
species-specific environmental tolerances.
In contrast, laboratory tests and field introductions in urban Adelaide, South Australia,
showed that Argentine ants could not displace
I. rufoniger from baits, except at the very largest
colony sizes tested (2500–5000 workers, i.e.
~1.5–3 times the colony size of L. humile used in
our study) (Walters and Mackay 2005). Yet, in
Western Australia, L. humile monopolized twothirds of baits in interactions with I. rufoniger
suchieri (Thomas and Holway 2005). Thus, there
is no consistent evidence that any tyrant ant
consistently resists invasion by L. humile. In fact,
in the only comparisons of sites either invaded or
uninvaded by Argentine ants in southern
Australia, abundances of Iridomyrmex were
strongly reduced at invaded sites (native vegetation—Rowles 2005; urban lawns—Walters in
press). Clearly, more tests with a variety of
123
Rowles and O’Dowd
Iridomyrmex species are needed under a range of
colony sizes, abiotic conditions, habitats, and
disturbance regimes.
Although the coastal ant community in our
study was dominated by Rhytidoponera and
Pheidole and to a lesser extent by Iridomyrmex,
Argentine ants completely displaced I. bicknelli
in these experiments and the abundances of the
other two Iridomyrmex in the community, I. vicina and I. foetans, were reduced at invaded sites
(Rowles 2005). If anything, Pheidole showed the
greatest capacity to resist invasion by L. humile.
More Pheidole workers recruited to baits than for
the other two native species, its incidence of
fighting with Argentine ants was greater, and the
rate of displacement from baits was slower than
I. bicknelli. Multiple workers of L. humile were
often needed to cooperatively attack the larger
Pheidole majors. In Bermuda, Pheidole megacephala slowed the rate of expansion of an
Argentine ant incursion to the extent that it regained its lost territory (Crowell 1968; Lieberburg
et al. 1975). What first appeared to be slow
replacement by L. humile, ultimately led to a
shifting equilibrium between the two species
forming a mosaic-like distribution (Haskins and
Haskins 1988). Nevertheless, the abundances of
Pheidole sp. 2 and Pheidole sp. 1 (ampla group)
were 3.6 and 3.7 times lower, respectively, in
coastal vegetation invaded by Argentine ants
than at uninvaded sites in Victoria (Rowles 2005).
There is no evidence that native ants in this
coastal ant community offered a greater degree of
biotic resistance to invasion by the Argentine ant
than that seen on other continents. Indeed, displacement of native ants was as strong and more
consistent as that reported in California. There,
Human and Gordon (1996) found that L. humile
consistently outcompeted Pheidole californica,
but Messor andrei was displaced from baits only
half the time. Conversely, Camponotus semitestaceus both excluded and displaced L. humile.
Similarly, Holway (1999) observed that Argentine
ant colonies reduced the number of workers at
baits for 6 of 7 native species, the exception being
Monomorium ergatogyna.
Interference competition is an important
mechanism by which Argentine ants displace
native ant species when invading new habitats.
Interference competition by Argentine ants
In this study, Argentine ants were able to usurp
food resources by displacing native ants. Within
invaded areas, where Argentine ant densities
exceed those presented by laboratory colonies,
there is a high potential for I. bicknelli, Pheidole
sp. 2, R. victoriae and other native ant species to
be lost or reduced in abundance through interference competition. These three are among the
most abundant native ant species in this coastal
community (Rowles 2005) and their loss or reduced abundance could trigger a variety of
indirect impacts. Aside from the broad, direct
impacts of omnivorous Argentine ants, displacement of native ant species may alter food
web structure, e.g. when native ant species constitute specific prey required by other fauna
(Suarez et al. 2000). Similarly, reduced abundance of Pheidole and Rhytidoponera, both of
which are important dispersal agents and predators of seeds (Hughes and Westoby 1992;
Rogerson 1998), could affect plant recruitment
and community composition.
Acknowledgements We thank J. Majer, J. Silverman and
K. Abbott for comments on an earlier draft and B. Rowles-van Rijswijk for manuscript review and field assistance.
T. Craven and P. Davis provided advice on extraction of
ants from soil. D. Mackay, M. Burd and M. Thomas advised on the design of laboratory ant colonies. Parks Victoria provided access to sites in the Mornington Peninsula
National Park under permit no. 10002268. This is contribution no. 102 from the Australian Centre for Biodiversity: Analysis, Policy and Management at Monash
University.
References
Andersen AN (1986a) Diversity, seasonality and community organisation of ants at adjacent heath and
woodland sites in south-eastern Australia. Aust J
Zool 34:53–64
Andersen AN (1986b) Patterns of ant community organisation in mesic south-eastern Australia. Aust J Ecol
11:87–98
Andersen AN (1990) The use of ant communities to
evaluate change in Australian terrestrial ecosystems: a
review and a recipe. Proc Ecol Soc Aust 16:347–357
Andersen AN (1992) Regulation of ‘‘momentary’’ diversity by dominant species in exceptionally rich ant
communities of the Australian seasonal tropics. Am
Natural 140:401–420
Andersen AN (1997) Functional groups and patterns of
organization in North American ant communities: a
comparison with Australia. J Biogeogr 24:433–460
83
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
Bond W, Slingsby P (1984) Collapse of an ant-plant
mutualism the Argentine ant Iridomyrmex humilis
and myrmecochorous Proteaceae. Ecology 65:1031–
1037
Calder WB (1975) Peninsula perspectives. WB Calder,
Melbourne, Australia
Cole FR, Medeiros AC, Loope LL, Zuehlke WW (1992)
Effects of the Argentine ant on arthropod fauna of
Hawaiian high-elevation shrubland. Ecology 73:1313–
1322
Crowell KL (1968) Rates of competitive exclusion by the
Argentine ant in Bermuda. Ecology 49:551–555
Davidson DW (1998) Resource discovery versus resource
domination in ants: a functional mechanism for
breaking the trade-off. Ecol Entomol 23:484–490
De Kock AE (1990) Interactions between the introduced
Argentine ant, Iridomyrmex humilis Mayr, and two
indigenous fynbos ant species. J Entomol Soc South
Africa 53:107–108
Erickson JM (1971) The displacement of native ant species
by the introduced Argentine ant Iridomyrmex humilis
Mayr. Psyche 78:257–266
Fellers JH (1987) Interference and exploitation in a guild
of woodland ants. Ecology 69:1466–1478
Fox BJ, Fox MD, Archer E (1985) Experimental confirmation of competition between two dominant species
of Iridomyrmex (Hymenoptera:Formicidae). Aust J
Ecol 10:105–110
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
Gibb H, Hochuli DF (2004) Removal experiment reveals
limited effects of a behaviorally dominant species on
ant assemblages. Ecology 85:648–657
Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of Southern Europe.
Proc Natl Acad Sci USA 99:6075–6079
Greenslade PJM (1976) The meat ant Iridomyrmex purpureus (Hymenoptera:Formicidae) as a dominant
member of ant communities. J Aust Entomol Soc
15:237–240
Greenslade PJM (1978) Ants. In: Low A (ed) The physical
and biological features of Kunnoth in Central Australia. CSIRO Division of Land Resources Management Technical Paper No. 4
Greenslade PJM, Halliday RB (1982) Distribution and
speciation in meat ants, Iridomyrmex purpureus and
related species (Hymenoptera:Formicidae). In: Barker WR, Greenslade PJM (eds) Evolution of the
Flora and Fauna of Arid Australia. Peacock Publications, Adelaide, pp 249–255
Greenslade PJM, Halliday RB (1983) Colony dispersion
and relationships of meat ants Iridomyrmex purpureus
and allies in an arid locality in South Australia. Insect
Sociaux 30:82–99
123
84
Haines IH, Haines JB (1978) Pest status of the crazy ant,
Anoplolepis longipes (Jerdon) (Hymenoptera:Formicidae), in the Seychelles. Bull Entomol Res 68:
627–638
Haskins CP, Haskins EF (1988) Final observations on
Pheidole megacephala and Iridomyrmex humilis in
Bermuda. Psyche 95:177–183
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 14:559–563
Heller NE (2004) Colony structure in introduced and native populations of the invasive Argentine ant, Linepithema humile. Insect Sociaux 51:378–386
Hoffmann BD, Andersen AN, Hill GJE (1999) Impact of
an introduced ant on native rain forest invertebrates:
Pheidole megacephala in monsoonal Australia. Oecologia 120:595–604
Hölldobler B, Wilson EO (1990) The Ants. Belknap Press,
Cambridge
Holway DA (1998a) Effect of Argentine ant invasions on
ground-dwelling arthropods in northern California
riparian woodlands. Oecologia 116:252–258
Holway DA (1998b) Factors governing rate of invasion: a
natural experiment using Argentine ants. Oecologia
115:206–212
Holway DA (1999) Competitive mechanisms underlying
the displacement of native ants by the invasive
Argentine ant. Ecology 80:238–251
Holway DA (2005) Edge effects of an invasive species
across a natural ecological boundary. Biol Conserv
121:561–567
Holway DA, Case TJ (2001) Effects of colony-level variation on competitive ability in the invasive Argentine
ant. Anim Behav 61:1181–1192
Holway DA, Suarez AV, Case TJ (1998) Loss of intraspecific aggression in the success of a widespread
invasive social insect. Science 283:949–952
Holway DA, Suarez AV, Case TJ (2002a) Role of abiotic
factors in governing susceptibility to invasion: a test
with Argentine ants. Ecology 83:1610–1619
Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ
(2002b) The causes and consequences of ant invasions. Ann Rev Ecol System 33:181–233
Hughes L, Westoby M (1992) Fate of seeds adapted for
dispersal by ants in Australian sclerophyll vegetation.
Ecology 73:1285–1299
Human KG, Gordon DM (1996) Exploitation and interference competition between the invasive Argentine
ant, Linepithema humile, and native ant species.
Oecologia 105:405–412
Human KG, Gordon DM (1999) Behavioral interactions
of the invasive Argentine ant with native ant species.
Insect Sociaux 46:159–163
Human KG, Weiss S, Weiss A, Sandler B, Gordon DM
(1998) Effects of abiotic factors on the distribution
and activity of the invasive Argentine ant (Hymenoptera:Formicidae). Environ Entomol 27:822–833
Le Breton J, Chazeau J, Jourdan H (2003) Immediate impacts of invasion by Wasmannia auropunctata (Hymenoptera:Formicidae) on native litter ant fauna in a New
Caledonian rainforest. Austral Ecol 28:204–209
123
Rowles and O’Dowd
Lieberburg I, Kranz PM, Seip A (1975) Bermudian ants
revisited: the status and interaction of Pheidole
megacephala and Iridomyrmex humilis. Ecology
56:473–478
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, Boulder, CO, pp163–173 and 332
Morrison LW (2000) Mechanisms of interspecific competition among an invasive and two native fire ants.
Oikos 90:238–252
Ness JH, Bronstein JL, Andersen AN, Holland JN (2004)
Ant body size predicts dispersal distance of antadapted seeds: implications of small-ant invasions.
Ecology 85:1244–1250
Newell W, Barber TC (1913) The Argentine ant. Bureau
Entomol Bull 122:1–98
Pamilo P, Crozier RH, Fraser J (1985) Inter-nest interactions, nest autonomy, and reproductive specialization
in an Australian arid-zone ant, Rhytidoponera sp 12.
Psyche 92:217–236
Porter SD, Savignano DA (1990) Invasion of polygyne fire
ants decimates native ants and disrupts arthropod
community. Ecology 71:2095–2106
O’Dowd DJ, Green PT, Lake PS (2003) Invasional
‘meltdown’ on an oceanic island. Ecol Lett 6:
812–817
Quinn GP, Keough MJ (2002) Experimental design and
data analysis for biologists. Cambridge University
Press, Cambridge, UK
Rodgerson L, (1998) Mechanical defense in seeds adapted
for ant dispersal. Ecology 79:1669–1677
Roulston TH, Buczkowski G, Silverman J (2003) Nestmate
discrimination in ants: effect of bioassay on aggressive
behavior. Insect Sociaux 50:151–159
Rowles AD (2005) Invasion by Argentine ants (Linepithema humile) in southeastern Australia: direct and
indirect effects and mechanisms for impacts. PhD
thesis, Monash University, Australia, p 231
Sanders NJ, Gotelli NJ, Heller NE, Gordon DM (2003)
Community disassembly by an invasive species. Proc
Natl Acad Sci USA 100:2474–2477
Shattuck SO (1992a) Generic revision of the ant subfamily
Dolichoderinae (Hymenoptera:Formicidae). Sociobiology 21:1–181
Shattuck SO (1992b) Review of the Dolichoderine ant
genus Iridomyrmex Mayr with descriptions of three
new genera (Hymenoptera:Formicidae). J Aust
Entomol Soc 31:13–18
Shattuck SO (1999) Australian ants their biology and
identification. CSIRO, Collingwood, Victoria, Australia
Suarez AV, Richmond JQ, Case TJ (2000) Prey selection in horned lizards following the invasion of
Argentine ants in southern California. Ecol Appl
10:711–725
Suarez AV, Tsutsui ND, Holway DA, Case TJ (1999)
Behavioral and genetic differentiation between native
and introduced populations of the Argentine ant. Biol
Invas 1:43–53
Interference competition by Argentine ants
Thomas ML, Holway DA (2005) Condition-specific competition between invasive Argentine ants and Australian Iridomyrmex. J Anim Ecol 74:532–542
Touyama Y, Ogata K, Sugiyama T (2003) The Argentine
ant, Linepithema humile, in Japan: assessement of
impact on species diversity of ant communities in
urban environments. Entomol Sci 6:57–62
Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000)
Reduced genetic variation and the success of an
invasive species. Proc Natl Acad Sci USA 97:5948–
5953
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
85
Walters AC, Mackay DA (2005) Importance of large
colony size for successful invasion by Argentine ants
(Hymenoptera:Formicidae): evidence for biotic resistance by native ants. Austral Ecol 30:395–406
Walters AC (in press) The invasion of Argentine ants
(Hymenoptera:Formicidae) in South Australia: impacts on community composition and abundance of
invertebrates in urban parklands. Austral Ecol 31
Ward PS (1981) Ecology and life history of the Rhytidoponera impressa group (Hymenoptera:Formicidae)
I Habitats, nest sites, and foraging behavior. Psyche
88:89–108
Wilkinson L (2000) SYSTAT 10. SPSS Inc, Chicago,
Illinois
123