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 (Ho¨lldobler 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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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
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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 (Ho¨lldobler 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
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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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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.
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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,
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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
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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
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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).
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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
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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
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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).
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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)
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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
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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
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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
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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
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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.
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