Exploitation and interference competition between the invasive Argentine ant,Linepithema humile,and native ant species

Interactions between the invasive Argentine ant, Linepithema humile, and native ant species were studied in a 450-ha biological reserve in northern California. Along the edges of the invasion, the presence of Argentine ants significantly reduced the foraging success of native ant species, and vice versa. Argentine ants were consistently better than native ants at exploiting food sources: Argentine ants found and recruited to bait more consistently and in higher numbers than native ant species, and they foraged for longer periods throughout the day. Native ants and Argentine ants frequently fought when they recruited to the same bait, and native ant species were displaced from bait during 60% of these encounters. In introduction experiments, Argentine ants interfered with the foraging of native ant species, and prevented the establishment of new colonies of native ant species by preying upon winged native ant queens. The Argentine ants' range within the preserve expanded by 12 ha between May 1993 and May 1994, and 13 between September 1993 and September 1994, with a corresponding reduction of the range of native ant species. Although some native ants persist locally at the edges of the invasion of Argentine ants, most eventually disappear from invaded areas. Both interference and exploitation competition appear to be important in the displacement of native ant species from areas invaded by Argentine ants.     

Exploitative strategies of the invasive Argentine ant (Linepithema humile) and native ant species in a southern Spanish pine forest

The Argentine ant, Linepithema humile (Mayr, 1868), is displacing native ant species in Do?ana National Park (Spain). This paper discusses the results of experiments aimed at analyzing exploitation competition between the invading species and other ant species in a park community. The Argentine ant was found to implement several strategies favoring its success in exploitation competition: mass recruitment, use of various microhabitats (on the ground and in trees), and activity over a wide range of temperatures. Although these strategies were not exclusive to L. humile, their joint use, together with the large number of workers forming each "unicolony," conferred a clear advantage for resource exploitation. Some native species were more severely affected than others by the presence of L. humile in terms of both abundance and behavior. The worst affected species were those whose ecological characteristics were similar to those of the Argentine ant, e.g., Pheidole pallidula (Nylander, 1849); the species least affected was Cataglyphis floricola Tinaut, 1993, possibly because of its subordinate and thermophilous nature (little overlap of daily activity rhythms with the exotic species).     

Genetics and behavior of a colonizing species: the invasive Argentine ant

Baker and Stebbins's 1965 book The Genetics of Colonizing Species aimed to draw together scientists from a variety of disciplines to provide a conceptual framework for the study of species introductions. A goal of their volume was to examine how studies on biological invasions could be used to provide insight into basic research questions as well as to develop practical strategies for control. In this article, we attempt to follow the goals of Baker and Stebbins by reviewing work on the genetics and behavior of a widespread colonizing species, the Argentine ant (Linepithema humile). Specifically, we examine the evolutionary changes that have taken place as a result of this species being introduced into new environments and synthesize recent research on Argentine ants from the perspective of population genetics, recognition systems, and the mechanisms that may underlie their ecological success.     

A native ant armed to limit the spread of the Argentine ant

Argentine ants (Linepithema humile) usually actively displace native ants through a combination of rapid recruitment, high numerical dominance and intense aggressive fights. However, in some cases, native ants can offer a strong resistance. In Corsica, a French Mediterranean island, local resistance by the dominant Tapinoma nigerrimum has been proposed as a factor limiting Argentine ant invasion. With the aim of evaluating the abilities of T. nigerrimum in interference and exploitative competition, this study tested in the laboratory the aggressive interactions between this native dominant ant and the invasive Argentine ant. We used four different assays between L. humile and T. nigerrimum: (1) worker dyadic interactions, (2) symmetrical group interactions, (3) intruder introductions into an established resident colony, and (4) a competition for space and food. This study confirms the ability of Argentine ants to compete with native species, by initiating more fights, using cooperation and simultaneously deploying physical and chemical defenses. However, despite Argentine ant fighting capabilities, T. nigerrimum was more efficient in both interference and exploitative competition. Its superiority was obvious in the space and food competition assays, where T. nigerrimum dominated food in 100% of the replicates after 1 h and invaded Argentine ant nests while the reverse was never observed. The death feigning behavior exhibited by Argentine ant workers also suggests the native ant’s superiority. Our study thus demonstrates that T. nigerrimum can offer strong competition and so may be able to limit the spread of Argentine ants in Corsica. This confirms that interspecific competition from ecologically dominant native species can affect the invasion success of invaders, notably by decreasing the likelihood of incipient colony establishment and survival.     

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.     

Chemical defense by the native winter ant (Prenolepis imparis) against the invasive Argentine ant (Linepithema humile)

The invasive Argentine ant (Linepithema humile) is established worldwide and displaces native ant species. In northern California, however, the native winter ant (Prenolepis imparis) persists in invaded areas. We found that in aggressive interactions between the two species, P. imparis employs a potent defensive secretion. Field observations were conducted at P. imparis nest sites both in the presence and absence of L. humile. These observations suggested and laboratory assays confirmed that P. imparis workers are more likely to secrete when outnumbered by L. humile. Workers of P. imparis were also more likely to secrete near their nest entrances than when foraging on trees. One-on-one laboratory trials showed that the P. imparis secretion is highly lethal to L. humile, causing 79% mortality. The nonpolar fraction of the secretion was chemically analyzed with gas chromatography/mass spectrometry, and found to be composed of long-chain and cyclic hydrocarbons. Chemical analysis of dissected P. imparis workers showed that the nonpolar fraction is derived from the Dufour's gland. Based on these conclusions, we hypothesize that this chemical defense may help P. imparis to resist displacement by L. humile.     

Long-term dynamics of the distribution of the invasive Argentine ant, Linepithema humile, and native ant taxa in northern California

Invasive species, where successful, can devastate native communities. We studied the dynamics of the invasive Argentine ant, Linepithema humile, for 7 years in Jasper Ridge, a biological preserve in northern California. We monitored the distributions at the hectare scale of native ant taxa and L. humile in the spring and fall from 1993 to 1999. We also studied the invasion dynamics at a finer resolution by searching for ants in 1-m² plots. Our results are similar at both scales. The distributions of several native species are not random with regard to L. humile; the distributions of several epigeic species with similar habitat affinities overlap much less frequently than expected with the distribution of L. humile. We found that season had a significant influence on the distributions of L. humile and several native taxa. Over the 7-year period, L. humile has increased its range size in Jasper Ridge largely at the expense of native taxa, but there is seasonal and yearly variation in this rate of increase. Studies of invasions in progress which sample across seasons and years may help to predict the spread and effects of invasive species.     

Temporal shifts in interactions between alien trees and the alien Argentine ant on native ants

Synergistic effects between various stressors on native biodiversity are poorly understood, especially adverse synergisms between different invasive organisms. While it is known that alien trees and the invasive Argentine ant Linepithema humile individually impact indigenous ant assemblages, little is known about how the impacts of these two types of aliens have a joint effect, and even less about the temporal dynamics of this interaction. We found that the Argentine ant benefited from invasion by alien trees through creation of less extreme environmental conditions at the hottest and coolest times of the year. We also found that the impacts of the two types of aliens were synergistic on the native ant assemblage. However, this synergistic impact also varied in intensity throughout the year, especially so in the more open natural sites. The alien tree canopy, when dense, created more constant environmental conditions throughout the year, leading to more constant Argentine ant levels and consequently more even impacts on the native ants. The various native ants varied considerably in their response to the impacts of both types of aliens, with many formicine ants being particularly sensitive. Our results show that the synergistic impacts, both negative and positive, of the two alien types are particular to each native ant species. Furthermore, the intensity of the adverse synergism is highly variable across the year.     

Coping with invasive alien species: the Argentine ant and the insectivorous bird assemblage of Mediterranean oak forests

Cork oak forests invaded by the Argentine ant Linepithema humile have a lower abundance and biomass of arthropod prey for birds than uninvaded forests. We studied whether the biomass of breeding insectivorous birds was also lower in invaded areas. We explored this and other possible effects of the ant invasion on the bird community by censusing birds in transects located in four invaded and four uninvaded forest sites in Catalonia (NE Spain) for 3 years. Redundancy analysis showed only slight differences in the community composition between forests. Two insectivorous species, Luscinia megarhynchos and Fringilla coelebs, tended to be less abundant in invaded areas although two others, Phylloscopus bonelli and Sylvia melanocephala, showed the opposite trend. Overall, the differences in prey biomass between invaded and uninvaded areas did not entail a biomass shift in the guild of insectivorous birds, regardless of whether they were shrub or canopy foragers. The main role of the habitat structure in determining bird densities and food resources being non-limiting in the studied forests are two possible non-exclusive explanations for this inconsistency. At today’s levels, the Argentine ant invasion does not appear to have greatly determined the insectivorous bird assemblage of the forests evaluated.     

Spatiotemporal patterns of intraspecific aggression in the invasive Argentine ant

The Argentine ant, Linepithema humile, is a widespread invasive species characterized by reduced intraspecific aggression within introduced populations. To illuminate the mechanisms underlying nestmate recognition in Argentine ants, we studied the spatial and temporal fidelity of intraspecific aggression in an introduced population of Argentine ants within which intraspecific aggression does occur. We quantified variation in the presence or absence of intraspecific aggression among nests over time both in the field and under controlled laboratory conditions to gain insight into the role of environmental factors as determinants of nestmate discriminatory ability. In addition, we compared levels of intraspecific aggression between nest pairs to the similarity of their cuticular hydrocarbons to determine the potential role of these compounds as labels for nestmate discrimination. In both field and laboratory comparisons, nest pairs behaved in a consistent manner throughout the course of the experiment: pairs that fought did so for an entire year, and pairs that did not fight remained nonaggressive. Moreover, we found a negative relationship between cuticular hydrocarbon similarity and the degree of aggression between nests, suggesting that these hydrocarbons play a role in nestmate discriminatory ability. In contrast to the prevailing pattern, ants from one site showed a marked change in behaviour during the course of this study. A concomitant change was also seen in the cuticular hydrocarbon profiles of ants from this site. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Unadapted behaviour of native,dominant ant species during the colonization of an aggressive,invasive ant

Among the factors driving the invasive success of non-indigenous species, the “escape opportunity” or “enemy release” hypothesis argues that an invader’s success may result partly from less resistance from the new competitors found in its introduced range. In this study, we examined competitive interactions between the little fire ant Wasmannia auropunctata (Roger) and ant species of the genus Pheidole in places where both are native (French Guiana) and in places where only species of Pheidole are native (New Caledonia). The experimental introduction of W. auropunctata at food resources monopolized by the Pheidole species induced the recruitment of major workers only for the Guianian Pheidole species, which were very effective at killing Wasmannia competitors. In contrast, an overall decrease in the number of Pheidole workers and no recruitment of major workers were observed for the New Caledonian species, although the latter were the only ones able to kill the Wasmannia workers. These results emphasize the inappropriate response of native dominant New Caledonian species to W. auropunctata and, thus, the importance of enemy recognition and specification in the organization of ant communities. This factor could explain how invasive animal species, particularly ants, may be able to successfully invade species-rich communities.     

The spread of the Argentine ant: environmental determinants and impacts on native ant communities

The increasing numbers of invasive species have stimulated the study of the underlying causes promoting the establishment and spread of exotic species. We tracked the spread of the highly invasive Argentine ant (Linepithema humile) along an environmental and habitat gradient on the northeastern Iberian Peninsula to determine the role of climatic, habitat and biotic variables on the rate of spread, and examine impact on native ant communities. We found the species well-established within natural environments. The mean annual rate of spread of the invasion (7.94 ± 2.99 m/year) was relatively low compared to other studies, suggesting that resistance posed by native ants in natural environments with no or low human disturbance might delay (although not prevent) the spread of the invasion irrespectively of the land-use type. Factors related to the distance to urban areas and characteristics of native and introduced populations explained the rate of spread of the invasion, while habitat-related variables determined the distribution of native ants and the impact of the Argentine ant on them. Native ant communities became more homogeneous following the invasion due to the decline of species richness and abundance. Only few species (Plagiolepis pygmaea and Temnothorax spp.) were able to cope with the spread of the invasion, and were possibly favored by the local extinction of other ant species. Taken together, our results indicate that land uses per se do not directly affect the spread of L. humile, but influence its invasive success by molding the configuration of native ant communities and the abiotic suitability of the site.     

Scavenging in Mediterranean ecosystems: effect of the invasive Argentine ant

Above-ground invertebrates may represent a high proportion of animal biomass, but few data are available on their fate after death. In Mediterranean ant communities, they are frequently scavenged by ants. Here, we assessed the consequences of Argentine ant invasion on the removal of arthropod corpses in Doñana National Park (SW Spain). In three natural habitats that differed in their degree of vegetation cover (i.e. protection for ants against high temperatures), we experimentally provided dead Drosophila, and observed their disappearance over a 60-min period at different times of day and year. The habitats used were isolated cork oak trees, pine tree forest and dry scrubland; we compared invaded with uninvaded plots in each. Oak trees were the most invaded habitat, while scrubland was the least and the only one where the Argentine ant coexisted with native ant species. In accordance with this degree of invasion, the Argentine ant removed the highest percentage of dead flies in oak trees and the lowest in scrubland. Its performance as scavenger was higher than uninvaded ant communities, but it was reduced at high temperatures, when native species were highly efficient. The saturated distribution of the Argentine ant colony seems to be the key to its efficiency. We discuss how the occurrence and scavenger efficiency of the Argentine ant could affect the nutrient cycling and the progression of its invasion.     

Colony-structure variation and interspecific competitive ability in the invasive Argentine ant

The success of some invasive species may depend on phenotypic changes that occur following introduction. In Argentine ants ( Linepithema humile) introduced populations typically lack intraspecific aggression, but native populations display such behavior commonly. We employ three approaches to examine how this behavioral shift might influence interspecific competitive ability. In a laboratory experiment, we reared colonies of Forelius mccooki with pairs of Argentine ant colonies that either did or did not exhibit intraspecific aggression. F. mccooki reared with intraspecifically non-aggressive pairs of Argentine ants produced fewer eggs, foraged less actively, and supported fewer living workers than those reared with intraspecifically aggressive pairs. At natural contact zones between competing colonies of L. humile and F. mccooki, the introduction of experimental Argentine ant colonies that fought with conspecific field colonies caused L. humile to abandon baits in the presence of F. mccooki, whereas the introduction of colonies that did not fight with field colonies of Argentine ants resulted in L. humile retaining possession of baits. Additional evidence for the potential importance of colony- structure variation comes from the Argentine ants native range. At a site along the Rio de la Plata in Argentina, we found an inverse relationship between ant richness and density of L. humile (apparently a function of local differences in colony structure) in two different years of sampling.     

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.     

Loss of Wolbachia infection during colonisation in the invasive Argentine ant Linepithema humile

WOLBACHIA are maternally inherited bacteria, which are very common in arthropods and nematodes. Wolbachia infection may affect host reproduction through feminisation, parthenogenesis, male-killing, cytoplasmic incompatibility and increased fecundity. Previous studies showing discrepancies between the phylogenies of Wolbachia and its arthropod hosts indicate that infection is frequently lost, but the causes of symbiont extinction have so far remained elusive. Here, we report data showing that colonisation of new habitats is a possible mechanism leading to the loss of infection. The presence and prevalence of Wolbachia were studied in three native and eight introduced populations of the Argentine ant Linepithema humile. The screening shows that the symbiont is common in the three native L. humile populations analysed. In contrast, Wolbachia was detected in only one of the introduced populations. The loss of infection associated with colonisation of new habitats may result from drift (founder effect) or altered selection pressures in the new habitat. Furthermore, a molecular phylogeny based on sequences of the Wolbachia wsp gene indicates that L. humile has been infected by a single strain. Horizontal transmission of the symbiont may be important in ants as suggested by the sequence similarity of strains in the three genera Linepithema, Acromyrmex, and Solenopsis native from South and Central America.     

Changes in the photosynthetic characteristics of cotton leaves infested by invasive mealybugs tended by native ant species

Herbivore injury has a direct effect on the growth and performance of host plants through photosynthetic suppression. However, changes in plant photosynthesis affected by ant tending of hemipteran sap feeders remain poorly understood. We investigated the effects of an invasive mealybug (Phenacoccus solenopsis) tended by native ants (Paratrechina longicornis) on the chlorophyll content and chlorophyll fluorescence characteristics of cotton (Gossypium hirsutum) leaves under greenhouse conditions. The results showed that the relative chlorophyll content of the infested cotton leaves significantly decreased after 10 days, and the chlorophyll contents were reduced by 26.4 and 34.9 % after 20 days in the without and with ant treatments compared to the control, respectively. In addition, the light utilization efficiency and maximum relative electron transport rate were reduced by 53.0 and 51.3 % compared to the control, respectively. However, no significant differences in these factors were found between the without and with ant treatments. The light saturation coefficient, describing the capacity of a sample to resist glare, exhibited no significant difference among treatments. The number of tending P. longicornis ants increased with P. solenopsis numbers, and the P. solenopsis numbers decreased after 20 days compared to the without ant treatment. We suggest that the tending ants may enhance the feeding ability of individual mealybugs in spite of the decreased number of mealybugs in this situation. Additionally, P. longicornis decrease the relative chlorophyll content of infested cotton leaves and may accelerate the damage caused by P. solenopsis to plants over time.     

Ecological interactions between invasive and native fouling species in the reservoir of a hydroelectric plant

In this study, we investigate the main ecological interactions between fouling aquatic organisms (both invasive and native) present in the reservoir of the Governador José Richa hydroelectric plant, located in southern Brazil, and to identify the most suitable period for the interruption of machinery operation for cleaning and maintenance of the hydraulic systems of this plant. A total of 32 experimental plates were fixed to a metallic structure positioned close to the plant's water intake. Three species of invasive fouling were identified in our samples (Limnoperna fortunei [Mollusca], Cordylophora sp., and Hydra sp. [Cnidaria]) and six native taxa belonging to the phyla Protozoa, Ciliophora, Amoebozoa, and Arthropoda. Spring and summer were the seasons with the highest fouling rates, as well as densities of fouling organisms. The highest levels of diversity were recorded during the colder seasons. Several interactions between the organisms were identified, such as mutualism, commensalism, competition, epibiosis, cannibalism, and predation. The data obtained suggest that, from the biological point of view, the most suitable period for machine shutdown destined for the removal of biological fouling in the hydraulic systems of the studied plant is between the end of spring and the beginning of summer.

     

Contrasting effects of an invasive ant on a native and an invasive plant

When invasive species establish in new environments, they may disrupt existing or create new interactions with resident species. Understanding of the functioning of invaded ecosystems will benefit from careful investigation of resulting species-level interactions. We manipulated ant visitation to compare how invasive ant mutualisms affect two common plants, one native and one invasive, on a sub-tropical Indian Ocean island. Technomyrmex albipes, an introduced species, was the most common and abundant ant visitor to the plants. T. albipes were attracted to extrafloral nectaries on the invasive tree (Leucaena leucocephala) and deterred the plant’s primary herbivore, the Leucaena psyllid (Heteropsylla cubana). Ant exclusion from L. leucocephala resulted in decreased plant growth and seed production by 22% and 35%, respectively. In contrast, on the native shrub (Scaevola taccada), T. albipes frequently tended sap-sucking hemipterans, and ant exclusion resulted in 30% and 23% increases in growth and fruit production, respectively. Stable isotope analysis confirmed the more predacious and herbivorous diets of T. albipes on the invasive and native plants, respectively. Thus the ants’ interactions protect the invasive plant from its main herbivore while also exacerbating the effects of herbivores on the native plant. Ultimately, the negative effects on the native plant and positive effects on the invasive plant may work in concert to facilitate invasion by the invasive plant. Our findings underscore the importance of investigating facilitative interactions in a community context and the multiple and diverse interactions shaping novel ecosystems.