Intraspecific competition influences the symmetry and intensity of aggression in the Argentine ant

Cooperative social groups rely on the ability to distinguishmembers from nonmembers. Accordingly, social insects have evolveda variety of systems that allow discrimination of nest matesfrom non–nest mates. In this study, we show that experiencecan modify patterns of intraspecific aggression in Argentineants (Linepithema humile). In laboratory experiments, we foundthat aggression between colonies was often asymmetrical, butin all five cases, this asymmetry shifted to symmetrical aggressionafter contact with a hostile colony. Moreover, in the field,aggression between workers collected from colony borders wassymmetrical, whereas polarized aggression occurred between workerscollected 500 m away from colony borders. Coinciding with thisshift in aggression symmetry, we also observed an increase inboth the overall level of aggression and the frequency of aggressionin both the field and laboratory bioassays. We found littleevidence for colony-level competitive asymmetries stemming frompolarities in aggression at the worker level, either in thelaboratory or in the field. These results illustrate that recognitionsystems in Argentine ants are surprisingly dynamic and provideexperimental evidence for how recognition can be adjusted inresponse to specific circumstances—in this case the presenceof intraspecific competitors.     

The diminutive supercolony: the Argentine ants of the southeastern United States

Native to Argentina and Brazil, the Argentine ant (Linepithema humile) is an invasive species that has become established on six continents and many oceanic islands. In several parts of its introduced range, including the western United States, southern Europe and Chile, the Argentine ant is unicolonial, forming extensive supercolonies. We examined population genetic structure and intercolony aggression in two regions of the introduced range of this species in the United States: California and the southeastern United States. Our results show that the southeastern L. humile population has high genotypic variability and strong intercolony aggression relative to the California population. In the California population, intercolony aggression was absent and 23 alleles were found across seven polymorphic microsatellite loci. However, in the Southeast, aggression between colonies was high and 47 alleles were present across the same seven loci in an equal number of colonies. We suggest that distinctly different colonization patterns for California and the Southeast may be responsible for the striking disparity in the genetic diversity of introduced populations. Southeastern colonies may have descended from multiple, independent introductions from the native range, undergoing a bottleneck at each introduction. In contrast, the California supercolony may have originated from one or more colonies inhabiting the southeastern United States, thus experiencing a double bottleneck. The differences in present-day distribution patterns between California and the Southeast may be due to the combined effect of two factors: lower winter temperatures in the Southeast and/or competition with another successful and widely distributed ant invader, the fire ant Solenopsis invicta.     

A Disjunct Argentine Ant Metacolony in Macaronesia and Southwestern Europe

The Argentine ant, Linepithema humile, originally from South America, is now a major pest in many parts of the world with Mediterranean-like climates. Earlier research indicated that southwestern European L. humile populations are segregated into two distinct supercolonies, the ‘Main’ supercolony extending through Portugal, Spain, southern France, and Italy, and the ‘Catalonian’ supercolony in eastern Spain. Both supercolonies are unicolonial, with workers showing no aggression towards members of the same supercolony, but severe aggression towards members of the other supercolony. Here we evaluated the behavioral relationships among non-native L. humile populations on the Macaronesian islands of Madeira and the Azores and non-native populations in southwestern Europe. We conducted aggression assays among L. humile workers from Madeira, the Azores, and the two southwestern European supercolonies. We found no aggressive interactions among any combination of workers from Madeira, the Azores, and the Main supercolony. However, workers from Madeira and the Azores always fought aggressively with workers from the Catalonian supercolony. Thus, the populations of L. humile in Madeira and the Azores appear to be unicolonial and act as if they belong to the Main supercolony of southwestern Europe. This set of geographically separated but mutually compatible supercolonies, which we term a ‘metacolony,’ appears to descend from one supercolony. Historical evidence suggests that the first L. humile population in the greater Mediterranean region was established in Madeira and that propagules from the dominant supercolony in Madeira gave rise to the dominant supercolonies in to other parts of the region.     

The role of cuticular hydrocarbons as chemical cues for nestmate recognition in the invasive Argentine ant (<Emphasis Type="Italic">Linepithema humile</Emphasis>)

Argentine ants (Linepithema humile) in their native South American range, like most other ant species, form spatially restricted colonies that display high levels of aggression toward other such colonies. In their introduced range, Argentine ants are unicolonial and form massive supercolonies composed of numerous nests among which territorial boundaries are absent. Here we examine the role of cuticular hydrocarbons (CHCs) in nestmate recognition of this highly damaging invasive ant using three supercolonies from its introduced range. We conducted behavioral assays to test the response of Argentine ants to workers treated with colonymate or non-colonymate CHCs. Additionally, we quantified the amount of hydrocarbons transferred to individual ants and performed gas chromatography-mass spectrometry (GC/MS) to qualitatively characterize our manipulation of CHC profiles. The GC/MS data revealed marked differences in the hydrocarbon profiles across supercolonies and indicated that our treatment effectively masked the original chemical profile of the treated ants with the profile belonging to the foreign individuals. We found that individual workers treated with foreign CHCs were aggressively rejected by their colonymates and this behavior appears to be concentration-dependent: larger quantities of foreign CHCs triggered higher levels of aggression. Moreover, this response was not simply due to an increase in the amount of CHCs applied to the cuticle since treatment with high concentrations of nestmate CHCs did not trigger aggression.The results of this study bolster the findings of previous studies on social insects that have implicated CHCs as nestmate recognition cues and provide insight into the mechanisms of nestmate recognition in the invasive Argentine ant. Received 6 February 2007; revised 31 May and 27 July 2007; accepted 16 August 2007.     

Effect of temperature on the oviposition rate of Argentine ant queens (Linepithema humile Mayr) under monogynous and polygynous experimental conditions

Data concerning the influence of temperature on a species' physiological parameters can be a useful tool for predicting its potential distribution range, but in the case of the Argentine ant, data based on its physiological needs are too scarce and incomplete to make accurate predictions of this type. In the present study, we offer new and complete data concerning the Argentine ant queen's oviposition rate under a wide range of temperatures in the laboratory. We analyzed the oviposition rate of the Argentine ant (Linepithema humile) at 12 experimental temperatures: 10, 12, 14, 16, 18, 21, 24, 26, 28, 30, 32 and 34 degrees C under monogynous conditions (one queen per nest) and three different polygynous conditions (two, four and eight queens per nest). We found that temperature affected their oviposition rate and that the effect was similar regardless of the number of queens in the nest. Egg laying was at its maximum at 28 degrees C, with variation in the upper and lower temperature limits at which oviposition took place depending on the degree of polygyny. Oviposition rates were negatively correlated with the number of queens in the nest. We also observed a marked variation in the oviposition rate of queens subjected to the same experimental conditions.     

Behavioral and Genetic Differentiation Between Native and Introduced Populations of the Argentine Ant

In this paper, we examine the hypothesis that reduced intraspecific aggression underlies the competitive prowess of Argentine ants in their introduced range. Specifically, we test three predictions of this hypothesis by comparing the genetic diversity, behavior, and ecology of Argentine ants in their native range to introduced populations. Differences between native and introduced populations of Argentine ants were consistent with our predictions. Introduced populations of the Argentine ant appear to have experienced a population bottleneck at the time of introduction, as evidenced by much reduced variation in polymorphic microsatellite DNA markers. Intraspecific aggression was rare in introduced populations but was common in native populations. Finally, in contrast to the Argentine ant's ecological dominance throughout its introduced range, it did not appear dominant in the native ant assemblages studied in Argentina. Together these results identify a possible mechanism for the widespread success of the Argentine ant in its introduced range.     

Genetic relationships among populations of the Argentine ant Linepithema humile introduced into Japan

Since some colonies of Argentine ant Linepithema humile were discovered in Japan in 1993, populations of this invasive alien ant species have been expanding their distribution. To resolve the number of invasions and the genetic structure in the early stages of introduction, we inferred the genetic structure and relationships among colonies from eight localities, from analyses of eight nuclear microsatellite DNA markers. F _ST analysis, principal component analysis and assignment test showed that at least three highly genetically differentiated groups of Argentine ants are present in Japan. Populations from Hiroshima Bay were grouped together (Hiroshima, Hatsukaichi, Otake, Iwakuni Central and Iwakuni Kuroiso), while those from Kobe and Yanai were both genetically distant from each other and from the Hiroshima Bay group. Hatsukaichi and Kobe are international seaports, suggesting that the by-ship invasion occurred at least twice. The invasion route of the Yanai population is unknown at this moment. The Aichi population was genetically distant from that of the Hiroshima Bay group by the difference in allele frequencies, and it was plausible that the Aichi population was introduced from the Hiroshima Bay group by human-mediated jump dispersal.     

Variation in the level of aggression, chemical and genetic distance among three supercolonies of the Argentine ant in Europe

In their invasive ranges, Argentine ant populations often form one geographically vast supercolony, genetically and chemically uniform within which there is no intraspecific aggression. Here we present regional patterns of intraspecific aggression, cuticular hydrocarbons (CHCs) and population genetics of 18 nesting sites across Corsica and the French mainland. Aggression tests confirm the presence of a third European supercolony, the Corsican supercolony, which exhibits moderate to high levels of aggression, depending on nesting sites, with the Main supercolony, and invariably high levels of aggression with the Catalonian supercolony. The chemical analyses corroborated the behavioural data, with workers of the Corsican supercolony showing moderate differences in CHCs compared to workers of the European Main supercolony and strong differences compared to workers of the Catalonian supercolony. Interestingly, there were also clear genetic differences between workers of the Catalonian supercolony and the two other supercolonies at both nuclear and mitochondrial markers, but only very weak genetic differentiation between nesting sites of the Corsican and Main supercolonies (F(ST) = 0.06). A detailed comparison of the genetic composition of supercolonies also revealed that, if one of the last two supercolonies derived from the other, it is the Main supercolony that derived from the Corsican supercolony rather than the reverse. Overall, these findings highlight the importance of conducting more qualitative and quantitative analyses of the level of aggression between supercolonies, which has to be correlated with genetic and chemical data.     

Argentine ant foraging activity and interspecific competition in complete vs. queenless and broodless colonies

Introduction experiments may prove useful in understanding the mechanisms underlying the successful establishment of invasive ant species into new areas. These manipulative introductions could be particularly helpful in exploring the interactions between invasive species and the local fauna and flora. However, the inherent risk of accidental establishment in such experiments poses unacceptable ethical concerns. Some of the worst invasive species are tramp ant species, which can adversely affect biodiversity and community structure after establishment. We conducted laboratory and field experiments investigating a safe methodology for carrying out introduction experiments using the sterile workers of the invasive Argentine ant, Linepithema humile, as a model. We found no difference in foraging rate between worker-only colonies of L. humile and complete colonies, containing queens, workers and brood. Worker-only L. humile colonies showed the same exploitative and interference ability as complete colonies in bait dominance trials with the odorous house ant, Tapinoma sessile, in both laboratory and field trials. We suggest that for those invasive ant species with sterile workers, worker-only colonies may be substituted for complete colonies in short-term field experiments in new areas. Received 18 January 2007; revised 19 June 2007; accepted 22 June 2007.     

Linking nutrition and behavioural dominance: carbohydrate scarcity limits aggression and activity in Argentine ants

Predicting the outcome of competitive interactions is a fundamental goal in ecology. Ecological stoichiometry, which relates nutrient balance to ecological processes, provides a framework for identifying mechanistic links among macronutrient availability, nutritional physiology and competitive performance. Because carbohydrates serve as a principal metabolic fuel, carbohydrate scarcity may impinge upon behaviours affecting competitive dominance (e.g. aggression, activity) to a greater extent than deficiencies of protein or other nutrients used preferentially for growth. Here, we tested this prediction with a diet manipulation study involving laboratory colonies of Argentine ants (Linepithema humile), a widespread and aggressive invasive species. The availability of both sucrose and insect prey influenced brood production and worker survival after three months. However, colonies became less aggressive and less active only when deprived of sucrose (but not prey). Scarcity of sucrose (but not prey) was also associated with reduced fat mass in individual workers. These data provide the first experimental support that carbohydrate scarcity compromises aggression and activity in ants, and illustrate, in principle, how access to carbohydrate-rich resources (e.g. plant exudates, hemipteran honeydew) might influence behavioural investments that contribute to competitive performance. Such investments might be especially important for invasive ants, given their aggressiveness and tendency to interact with honeydew-producing Hemiptera.     

Intraspecific aggression and the colony structure of the invasive ant Myrmica rubra

1. Patterns of aggression between ants from different nests influence colony and population structure. Several species of invasive ants lack colony boundaries over large expanses, forming ‘supercolonies’ with many nests among which workers can move without encountering aggression. 2. Bioassays of aggression were used to determine the colony structure of the invasive ant Myrmica rubra (L.) at eight sites in Massachusetts, the state where the species was first discovered in North America. To improve the ability to distinguish systematic patterns from background variability in aggressiveness, a repeated‐measures design was used and replicate assays for each pair of nests were conducted. 3. Aggressive responses showed that populations at all sites consisted of multiple distinct colonies. Patterns of aggression were repeatable and transitive, with few exceptions. Colonies were identified as clusters of nests whose workers showed little to no aggression towards one another but were aggressive towards conspecifics from more distant nests. 4. The degree of aggression varied considerably among different colony pairs but did not depend in any consistent way on the distance of separation or on whether colonies were neighbours. 5. Territories of neighbouring colonies abutted, indicating that they were restricted by intraspecific competition. Mapped territories ranged in size from 0.03 to 1.2 ha, but colonies at the study sites have not undergone the enormous expansions seen in introduced populations of some other species of invasive ants, and neighbouring colonies compete locally.     

Genetics, behaviour and chemical recognition of the invading ant Pheidole megacephala

Introduced species often become ecologically dominant, displacing native species and posing a serious threat to ecosystem function and global biodiversity. Ants are among the most widespread and damaging alien species; introductions are often accompanied by population-level behavioural and genetic changes contributing to their success. We investigated the genetic structure, chemical profile and nestmate recognition in introduced populations of the invasive big-headed ant, Pheidole megacephala, in Australia. Behavioural analyses show that workers are not aggressive towards conspecifics from different nests, even at large geographical scales (up to 3000 km) and between populations encompassing a wide range of environmental conditions. By contrast, interactions with workers of other species invariably result in agonistic behaviours. Genetic analyses reveal that populations have low genetic diversity. No genetic differentiation occurs among nests of the same population; differentiation between populations, though significant, remains weak. Chemical analyses indicate that cuticular lipids are similar between colonies of a population, and that differentiation between populations is low. Altogether, these results indicate that the big-headed ant P. megacephala forms a large unicolonial population across northern/eastern Australia.     

Characterization of microsatellite loci for the Argentine ant,Linepithema humile,and their potential for analysis of colony structure in invading Hawaiian populations

We developed primers for five polymorphic microsatellite loci to analyse the genetic structure of colonies in an invading Argentine ant population located in Haleakala National Park on the island of Maui, Hawaii. Microsatellite loci were isolated using both a polymerase chain reaction‐based and a cloning‐based method. With a range of 3–18 alleles and expected levels of heterozygosity of 0.46–0.77, these loci provide useful markers for the detection of colony and population structure in new or expanding populations of this species.     

Aggressive interactions between the introduced Argentine ant, Linepithema humile and the native odorous house ant, Tapinoma sessile

The Argentine ant (Linepithema humile) is an invasive species that disrupts the balance of natural ecosystems by displacing indigenous ant species throughout its introduced range. The mechanisms by which Argentine ants effectively compete against native ant species have been previously addressed in field studies that centered on interference and exploitation competition at baits and mainly examined the colony-level performance of Argentine ants. Detailed behavioral observations explaining the basis for the strong competitive ability of L. humile are comparatively rare. To gain a better understanding of the mechanisms by which Argentine ants displace native ants we examined the aggressive interactions between the Argentine ants and the odorous house ant, Tapinoma sessile in four different aggression assays: (1) worker dyad interactions, (2) symmetrical group interactions, (3) intruder introductions into an established resident colony, and (4) a resource competition assay which focused on competition for food and nesting space. Our results demonstrate a clear disparity between worker-level and colony-level fighting ability of Argentine ants and provide behavioral evidence to explain the superior interference ability of Argentine ants in group assays. Argentine ants experienced mixed success in fighting against odorous house ants in dyad interactions, but gradually gained a numerical advantage in symmetrical group interactions by active cooperation among nestmates. Results of the resource competition assay indicate that Argentine ants recruit rapidly, numerically dominate food and nesting sites, and aggressively displace T. sessile from baits. Taken together, the results of these assays allow us to pinpoint the behavioral mechanisms responsible for the remarkable competitive ability of Argentine ants.     

Food availability and brood number do not influence intraspecific aggression in Argentine ants

Summary. Nestmate recognition cues can derive from both environmental and genetic factors, but can also be modulated in response to context-specific cues. Synchronous changes in nestmate recognition systems occur seasonally in some species of ants, however the mechanisms underlying these seasonal changes are often unknown. We studied two mechanisms, relative brood number and food availability, to determine if they generate temporal variation in intraspecific aggression in an introduced population of the Argentine ant, Linepithema humile. Using data from previous studies we found that seasonal increases in aggression levels correlate with seasonal increases in brood-to-worker ratios in the field. However, when we manipulated brood-to-worker ratios in paired experimental colonies, we found no direct evidence that relative brood numbers influenced aggression levels. To determine if food availability influenced aggression we conducted a second experiment in which we randomly assigned pairs of experimental colonies to starved or fed treatments and then measured aggression levels weekly for five weeks. We observed no difference in the level of aggression between these two treatment groups indicating that food availability also has no affect on aggression levels between hostile conspecific colonies.Received 24 August 2004; revised 15 September 2004; accepted 23 September 2004.     

Global-scale analyses of chemical ecology and population genetics in the invasive Argentine ant

Ants are some of the most abundant and ecologically successful terrestrial organisms, and invasive ants rank among the most damaging invasive species. The Argentine ant is a particularly well-studied invader, in part because of the extreme social structure of introduced populations, known as unicoloniality. Unicolonial ants form geographically vast supercolonies, within which territorial behaviour and intraspecific aggression are absent. Because the extreme social structure of introduced populations arises from the widespread acceptance of conspecifics, understanding how this colonymate recognition occurs is key to explaining their success as invaders. Here, we present analyses of Argentine ant recognition cues (cuticular hydrocarbons) and population genetic characteristics from 25 sites across four continents and the Hawaiian Islands. By examining both hydrocarbon profiles and microsatellite genotypes in the same individual ants, we show that native and introduced populations differ in several respects. Both individual workers and groups of nestmates in the introduced range possess less diverse chemical profiles than ants in the native range. As previous studies have reported, we also find that introduced populations possess much lower levels of genetic diversity than populations in the native range. Interestingly, the largest supercolonies on several continents are strikingly similar to each other, suggesting that they arose from a shared introduction pathway. This high similarity suggests that these geographically far-flung ants may still recognize and accept each other as colonymates, thus representing distant nodes of a single, widely distributed supercolony. These findings shed light on the behaviour and sociality of these unicolonial invaders, and pose new questions about the history and origins of introduced populations.     

Hydrocarbon-released nestmate aggression in the Argentine ant, Linepithema humile, following encounters with insect prey

Argentine ants, Linepithema humile, were attacked by their nestmates following contact with a particular prey item, the brown-banded cockroach, Supella longipalpa. Contact with prey, as brief as 2 min, provoked nestmate aggression. Argentine ants contaminated with hydrocarbons extracted from S. longipalpa also released nestmate aggression behavior similar to that released by the whole prey item, confirming the involvement of hydrocarbons. In contrast to S. longipalpa, little or no nestmate aggression was induced by other ant prey from diverse taxa. A comparison of prey hydrocarbon profiles revealed that all hydrocarbons of S. longipalpa were very long chain components with 33 or more carbons, while other prey had either less, or none, of the very long chain hydrocarbons of 33 carbons or greater. We identified the hydrocarbons of S. longipalpa and some new groups of long chain hydrocarbons of L. humile. The majority of S. longipalpa hydrocarbons were 35 and 37 carbons in length with one to three methyl branches, and closely resembled two previously unidentified groups of compounds from L. humile of similar chain length. The hydrocarbons of S. longipalpa and L. humile were compared and their role in the Argentine ant nestmate recognition is discussed.