Edward G. LeBrun

Trophic ecology of invasive Argentine ants in their native and introduced ranges

Although the ecological effects of invasions often become obvious soon after introduced species become established, more gradual effects may take years to manifest and can thus require long-term data for quantification. We analyzed an 8-year record of stable isotope data on Argentine ants (Linepithema humile) from southern California to infer how the trophic position of this widespread invasive species changes over time as native ant species are displaced. We couple this longitudinal analysis with a biregional comparison of stable isotope data (δ15N) on ants from Argentina (native range) and California (introduced range) to quantify (i) how the trophic position of L. humile differs between native and introduced populations, and (ii) how relative trophic position as estimated by δ15N values of Argentine ants compare with those of other ants at the same site. Both long-term and biregional comparisons indicate that the Argentine ants relative trophic position is reduced at sites with a longer history of occupation. Over the course of 8 years, the relative trophic position of L. humile remained high at the leading edge of an invasion front but declined, on average, behind the front as native ants disappeared. Relative to native populations, where L. humile is among the most carnivorous of ants, Argentine ants from California occupied lower trophic positions. These results support the hypothesis that Argentine ants shift their diet after establishment as a result of resource depletion and increasing reliance on plant-based resources, especially honeydew-producing Hemiptera. Our results demonstrate the value of long-term and biregional data in uncovering ecological effects of invasions.

Intercontinental differences in resource use reveal the importance of mutualisms in fire ant invasions

Mutualisms play key roles in the functioning of ecosystems. However, reciprocally beneficial interactions that involve introduced species also can enhance invasion success and in doing so compromise ecosystem integrity. For example, the growth and competitive ability of introduced plant species can increase when fungal or microbial associates provide limiting nutrients. Mutualisms also may aid animal invasions, but how such systems may promote invasion success has received relatively little attention. Here we examine how access to food-for-protection mutualisms involving the red imported fire ant (Solenopsis invicta) aids the success of this prominent invader. Intense interspecific competition in its native Argentina constrained the ability of S. invicta to benefit from honeydew-producing Hemiptera (and other accessible sources of carbohydrates), whereas S. invicta dominated these resources in its introduced range in the United States. Consistent with this strong pattern, nitrogen isotopic data revealed that fire ants from populations in the United States occupy a lower trophic position than fire ants from Argentina. Laboratory and field experiments demonstrated that honeydew elevated colony growth, a crucial determinant of competitive performance, even when insect prey were not limiting. Carbohydrates, obtained largely through mutualistic partnerships with other organisms, thus represent critical resources that may aid the success of this widespread invasive species. These results illustrate the potential for mutualistic interactions to play a fundamental role in the establishment and spread of animal invasions.

Imported crazy ant displaces imported fire ant, reduces and homogenizes grassland ant and arthropod assemblages

A recently introduced, ecologically dominant, exotic ant species, Nylanderia fulva, is invading the Southeastern United States and Texas. We evaluate how this invader impacts diversity and abundance of co-occurring ants and other arthropods in two grasslands. N. fulva rapidly attains densities up to 2 orders of magnitude greater than the combined abundance of all other ants. Overall ant biomass increases in invaded habitat, indicating that N. fulva exploits resources not fully utilized by the local ant assemblage. At high density, as N. fulva spreads, it eliminates the current ecologically dominant invasive ant, red imported fire ants (Solenopsis invicta). Compared to imported fire ant dominated habitat, N. fulva invasion zones have lower non-ant arthropod species richness and abundance with impacts differing by trophic category. Further, N. fulva reduces abundance and species richness of the remainder of the ant assemblage and does so in a non-random manner: impacting species with small sized workers much less than species with larger workers. In these and other ant assemblages with a large exotic component, the exotics tend to be small bodied species. As a result, N. fulva almost completely eliminates regionally distributed species, but leaves globally distributed species largely unaffected, thereby systematically favoring introduced over native diversity. S. invicta impacts wildlife and arthropod assemblage structure and is nearly ubiquitous in non-forested habitats of the Southeastern United States and Texas. Its displacement by N. fulva has critical implications for the natural systems of this region.

Introducing Phorid Fly Parasitoids of Red Imported Fire Ant Workers from South America to Texas: Outcomes Vary by Region and by Pseudacteon Species Released

Abstract Since the first report on introductions to Texas of Pseudacteon decapitating flies, a variety of participants have released flies in a range of sites. The expansions of Pseudacteon populations have been systematically and widely monitored. Before 2002, the widely released initial species P. tricuspis Borgmeier did not become established. Severe drought in 1996–2001 and host-size-dependent sex ratio were proposed constraints in establishing this species. In recent years, however, these limitations have been lifted in some areas by favorable weather, irrigation of release sites, and/or by use of a smaller Pseudacteon species, P. curvatus Borgmeier, not reliant on larger fire ant workers to produce females. Beginning in 2002, the USDA-APHIS collaboration with USDA-ARS and Texas Cooperative Extension programs began to supplement release sites in Texas beyond those initiated by the University of Texas, Austin phorid fly project. In 2005, private citizens began to participate in the spread of Pseudacteon to new sites. By fall 2006, P. tricuspis, expanding from releases between 1999 and 2001, was found on more than 3 million hectares of Central and Coastal Texas, while P. curvatus, with its later start, is only now beginning to expand at some sites. Pseudacteon that established more easily in mesic and moderate climates has difficulty surviving unfavorable weather in South Texas. However, two sites where flies “failed” to become established were revealed to be false negatives after the record rains of summer 2007. Starting in late 2006, the first releases of P. obtusus Borgmeier in North America established, and three to five additional species are being released.

Chemical Warfare Among Invaders: A Detoxification Interaction Facilitates an Ant Invasion

Know Your Enemy Fire ants accidentally introduced to North America from their native range in Argentina have been hugely invasive and difficult to eradicate and caused both environmental and economic damage. Recently, another accidentally introduced Argentine ant, the tawny crazy ant, appears to be displacing the fire ants. How? LeBrun et al. (p. 1014, published online 13 February; see the Perspective by Kaspari and Weiser) show that tawny crazy ants have a chemical and behavioral response to the toxic bite of fire ants that vastly reduces their mortality during confrontations and that allows the tawny crazy ants to outcompete their rivals. After fire ants invade, they can be invaded in turn by tawny crazy ants. [Also see Perspective by Kaspari and Weiser] As tawny crazy ants (Nylanderia fulva) invade the southern United States, they often displace imported fire ants (Solenopsis invicta). After exposure to S. invicta venom, N. fulva applies abdominal exocrine gland secretions to its cuticle. Bioassays reveal that these secretions detoxify S. invicta venom. Further, formic acid from N. fulva venom is the detoxifying agent. N. fulva exhibits this detoxification behavior after conflict with a variety of ant species; however, it expresses it most intensely after interactions with S. invicta. This behavior may have evolved in their shared South American native range. The capacity to detoxify a major competitor’s venom probably contributes substantially to its ability to displace S. invicta populations, making this behavior a causative agent in the ecological transformation of regional arthropod assemblages.

Indirect competition facilitates widespread displacement of one naturalized parasitoid of imported fire ants by another.

Species abundances in natural systems are usually close to some equilibrium, making mechanisms that maintain or prevent species coexistence difficult to discern. Biological control projects provide an opportunity to observe systems transition between equilibriums as a result of the influence of the newly introduced species. In the southeastern United States and Texas, species of phorid fly parasitoids are being sequentially introduced as control agents for imported fire ants. The first two species introduced, Pseudacteon tricuspis and P. curvatus, partition the host niche based upon body size and co-exist broadly in their native range in Argentina, indicating they would form a co-existing and complementary suite of parasitoids in North America. This study examines the interaction between these parasitoids at multiple temporal and spatial scales. Surprisingly, data at all scales reveal that as P. curvatus establishes at a site it competitively displaces P. tricuspis. However, the speed of this reduction appears to differ between ecoregions, suggesting that the rate of displacement depends on environment. At the site where P. curvatus has been established the longest, this population interaction approaches complete displacement. Tests of potential mechanisms causing this displacement reveal that direct competition for host workers alters the operational sex ratio of the P. tricuspis population, but the strength of this effect is insufficient to explain the displacement. Experiments reveal the operation of a strong, indirect effect whereby locally common species preempt reproductive opportunities from rarer species by inducing host behavioral defenses. Finally, a re-examination of published data from their native range reveals that a previously overlooked negative relationship between the densities of these two species also exists there, suggesting that the same processes as those reported here also operate in South America.

Dynamic expansion in recently introduced populations of fire ant parasitoids (Diptera: Phoridae).

Combating invasive species requires a detailed, mechanistic understanding of the manner and speed with which organisms expand their ranges. Biological control efforts provide an opportunity to study the process of species invasions and range expansions under known initial conditions. This study examines the rate, pattern and mechanisms of spread for two populations of the biological control agent Pseudacteon tricuspis, phorid-fly parasitoids of imported fire ants. We employ a trap-based survey method that detects phorid flies in low-density populations, and provides data on abundance. This technique allows us to differentiate between continuous population spread and effective long-distance dispersal and to examine density gradients of phorid flies across the expanding population front. We find that occupied sites in front of the leading edge of continuous populations were common; forming small populations we refer to as satellite populations. Satellite populations are tens of kilometers from the nearest possible source. Wind governs the dynamics of spread in these two central Texas populations. Population edges expanding with the wind exhibited a higher frequency of effective long-distance dispersal than did populations expanding into the wind. This enhanced effective long-distance dispersal rate translated into a five times faster rate of spread for population edges traveling with the wind. This planned invasion shares many characteristics in common with unplanned species invasions including: protracted establishment phase during which densities were below detection thresholds, and slow initial spread immediately after establishment followed by rapid, accelerating spread rates as population sizes grew.

A Review of Pseudacteon (Diptera: Phoridae) That Parasitize Ants of the Solenopsis geminata Complex (Hymenoptera: Formicidae)

ABSTRACT Some phorid flies of the genus Pseudacteon Coquillett parasitize workers of Solenopsis geminata (F.) complex fire ants. The group is found to comprise at least 21 species of flies, of which 11 are new to science and described here: P. amuletum, P. andinus, P. annulus, P. catarinae, P. deltoides, P. hippeus, P. kungae, P. laticarinatus, P. palomita, P. quinni, and P. robustus. An identification key to the females is included. This expansion of known Pseudacteon species parasitizing the S. geminata complex makes it an interesting system for comparison with Pseudacteon flies that parasitize fire ants of the S. saevissima (Smith) complex.

Molecular diversity of the microsporidium Kneallhazia solenopsae reveals an expanded host range among fire ants in North America.

Kneallhazia solenopsae is a pathogenic microsporidium that infects the fire ants Solenopsis invicta and Solenopsis richteri in South America and the USA. In this study, we analyzed the prevalence and molecular diversity of K. solenopsae in fire ants from North and South America. We report the first empirical evidence of K. solenopsae infections in the tropical fire ant, Solenopsis geminata, and S. geminata×Solenopsis xyloni hybrids, revealing an expanded host range for this microsporidium. We also analyzed the molecular diversity at the 16S ribosomal RNA gene in K. solenopsae from the ant hosts S.invicta, S. richteri, S. geminata and S. geminata×S. xyloni hybrids from North America, Argentina and Brazil. We found 22 16S haplotypes. One of these haplotypes (WD_1) appears to be widely distributed, and is found in S. invicta from the USA and S. geminata from southern Mexico. Phylogenetic analyses of 16S sequences revealed that K. solenopsae haplotypes fall into one of two major clades that are differentiated by 2-3%. In some cases, multiple K. solenopsae haplotypes per colony were found, suggesting either an incomplete homogenization among gene copies within the 16S gene cluster or multiple K. solenopsae variants simultaneously infecting host colonies.

By their own devices: invasive Argentine ants have shifted diet without clear aid from symbiotic microbes

The functions and compositions of symbiotic bacterial communities often correlate with host ecology. Yet cause–effect relationships and the order of symbiont vs. host change remain unclear in the face of ancient symbioses and conserved host ecology. Several groups of ants exemplify this challenge, as their low‐nitrogen diets and specialized symbioses appear conserved and ancient. To address whether nitrogen‐provisioning symbionts might be important in the early stages of ant trophic shifts, we studied bacteria from the Argentine ant, Linepithema humile – an invasive species that has transitioned towards greater consumption of sugar‐rich, nitrogen‐poor foods in parts of its introduced range. Bacteria were present at low densities in most L. humile workers, and among those yielding quality 16S rRNA amplicon sequencing data, we found just three symbionts to be common and dominant. Two, a Lactobacillus and an Acetobacteraceae species, were shared between native and introduced populations. The other, a Rickettsia, was found only in two introduced supercolonies. Across an eight‐year period of trophic reduction in one introduced population, we found no change in symbionts, arguing against a relationship between natural dietary change and microbiome composition. Overall, our findings thus argue against major changes in symbiotic bacteria in association with the invasion and trophic shift of L. humile. In addition, genome content from close relatives of the identified symbionts suggests that just one can synthesize most essential amino acids; this bacterium was only modestly abundant in introduced populations, providing little support for a major role of nitrogen‐provisioning symbioses in Argentine ants dietary shift.