Pathogen-mediated natural and manipulated population collapse in an invasive social insect.

SignificanceInvasive social insects are among the most damaging of invasive organisms and have proved universally intractable to biological control. Despite this, populations of some invasive social insects collapse from unknown causes. We report long-term studies demonstrating that infection by a microsporidian pathogen causes populations of a globally significant invasive ant to collapse to local extinction, providing a mechanistic understanding of a pervasive phenomenon in biological invasions: the collapse of established populations from endogenous factors. We apply this knowledge and successfully eliminate two large, introduced populations of these ants. More broadly, microsporidian pathogens should be evaluated for control of other supercolonial invasive social insects. Diagnosing the cause of unanticipated population collapse in invasive organisms can lead to applied solutions.

Ritualized aggressive behavior reveals distinct social structures in native and introduced range tawny crazy ants.

How workers within an ant colony perceive and enforce colony boundaries is a defining biological feature of an ant species. Ants fall along a spectrum of social organizations ranging from single-queen, single nest societies to species with multi-queen societies in which workers exhibit colony-specific, altruistic behaviors towards non-nestmate workers from distant locations. Defining where an ant species falls along this spectrum is critical for understanding its basic ecology. Herein we quantify queen numbers, describe intraspecific aggression, and characterize the distribution of colony sizes for tawny crazy ant (Nylanderia fulva) populations in native range areas in South America as well as in their introduced range in the Southeastern United States. In both ranges, multi-queen nests are common. In the introduced range, aggressive behaviors are absent at all spatial scales tested, indicating that within the population in the Southeastern United States N. fulva is unicolonial. However, this contrasts strongly with intraspecific aggression in its South American native range. In the native range, intraspecific aggression between ants from different nests is common and ritualized. Aggression is typically one-sided and follows a stereotyped sequence of escalating behaviors that stops before actual fighting occurs. Spatial patterns of non-aggressive nest aggregation and the transitivity of non-aggressive interactions demonstrate that results of neutral arena assays usefully delineate colony boundaries. In the native range, both the spatial extent of colonies and the average number of queens encountered per nest differ between sites. This intercontinental comparison presents the first description of intraspecific aggressive behavior for this invasive ant and characterizes the variation in colony organization in the native-range, a pre-requisite to a full understanding of the origins of unicoloniality in its introduced range.

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 ant's dietary shift.

Evidence of niche shift and global invasion potential of the Tawny Crazy ant, Nylanderia fulva.

Analysis of an invasive species' niche shift between native and introduced ranges, along with potential distribution maps, can provide valuable information about its invasive potential. The tawny crazy ant, Nylanderia fulva, is a rapidly emerging and economically important invasive species in the southern United States. It is originally from east-central South America and has also invaded Colombia and the Caribbean Islands. Our objectives were to generate a global potential distribution map for N. fulva, identify important climatic drivers associated with its current distribution, and test whether N. fulva's realized climatic niche has shifted across its invasive range. We used MaxEnt niche model to map the potential distribution of N. fulva using its native and invaded range occurrences and climatic variables. We used principal component analysis methods for investigating potential shifts in the realized climatic niche of N. fulva during invasion. We found strong evidence for a shift in the realized climatic niche of N. fulva across its invasive range. Our models predicted potentially suitable habitat for N. fulva in the United States and other parts of the world. Our analyses suggest that the majority of observed occurrences of N. fulva in the United States represent stabilizing populations. Mean diurnal range in temperature, degree days at ≥10°C, and precipitation of driest quarter were the most important variables associated with N. fulva distribution. The climatic niche expansion demonstrated in our study may suggest significant plasticity in the ability of N. fulva to survive in areas with diverse temperature ranges shown by its tolerance for environmental conditions in the southern United States, Caribbean Islands, and Colombia. The risk maps produced in this study can be useful in preventing N. fulva's future spread, and in managing and monitoring currently infested areas.

Widespread Chemical Detoxification of Alkaloid Venom by Formicine Ants.

The ability to detoxify defensive compounds of competitors provides key ecological advantages that can influence community-level processes. Although common in plants and bacteria, this type of detoxification interaction is extremely rare in animals. Here, using laboratory behavioral assays and analyses of videotaped interactions in South America, we report widespread venom detoxification among ants in the subfamily Formicinae. Across both data sets, nine formicine species, representing all major clades, used a stereotyped grooming behavior to self-apply formic acid (acidopore grooming) in response to fire ant (Solenopsis invicta and S. saevissima) venom exposure. In laboratory assays, this behavior increased the survivorship of species following exposure to S. invicta venom. Species expressed the behavior when exposed to additional alkaloid venoms, including both compositionally similar piperidine venom of an additional fire ant species and the pyrrolidine/pyrroline alkaloid venom of a Monomorium species. In addition, species expressed the behavior following exposure to the uncharacterized venom of a Crematogaster species. However, species did not express acidopore grooming when confronted with protein-based ant venoms or when exposed to monoterpenoid-based venom. This pattern, combined with the specific chemistry of the reaction of formic acid with venom alkaloids, indicates that alkaloid venoms are targets of detoxification grooming. Solenopsis thief ants, and Monomorium species stand out as brood-predators of formicine ants that produce piperidine, pyrrolidine, and pyrroline venom, providing an important ecological context for the use of detoxification behavior. Detoxification behavior also represents a mechanism that can influence the order of assemblage dominance hierarchies surrounding food competition. Thus, this behavior likely influences ant-assemblages through a variety of ecological pathways.

Myrmecomorba nylanderiae gen. et sp. nov., a microsporidian parasite of the tawny crazy ant Nylanderia fulva.

A new microsporidian genus and species, Myrmecomorba nylanderiae, is described from North American populations of the tawny crazy ant, Nylanderia fulva. This new species was found to be heterosporous producing several types of binucleate spores in both larval and adult stages and an abortive octosporoblastic sporogony in adult ants. While microsporidia are widespread arthropod parasites, this description represents only the fifth species described from an ant host. Molecular analysis indicated that this new taxon is phylogenetically closely allied to the microsporidian family Caudosporidae, a group known to parasitize aquatic black fly larvae. We report the presence of 3 spore types (Type 1 DK, Type 2 DK, and octospores) with infections found in all stages of host development and reproductive castes. This report documents the first pathogen infecting N. fulva, an invasive ant of considerable economic and ecological consequence.

Chemical warfare among invaders: a detoxification interaction facilitates an ant invasion.

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.

Imported fire ants near the edge of their range: disturbance and moisture determine prevalence and impact of an invasive social insect.

1. Habitat disturbance and species invasions interact in natural systems, making it difficult to isolate the primary cause of ecosystem degradation. A general understanding requires case studies of how disturbance and invasion interact across a variety of ecosystem - invasive species combinations. 2. Dramatic losses in ant diversity followed the invasion of central Texas by red imported fire ants (Solenopsis invicta). However, recent manipulative studies in Florida revealed no effect on ant diversity following the removal of S. invicta from a disturbed pasture habitat, but moderate loss of diversity associated with their introduction into undisturbed habitat and no invasion occurred without disturbance. Thus, the importance of S. invicta in driving diversity loss and its ability to invade undisturbed systems is unresolved. 3. We examine the distribution and abundance of a large monogyne S. invicta population and its association with the co-occurring ant assemblage at a site in south Texas close to the aridity tolerance limit of S. invicta. 4. We document that moisture modulates S. invicta densities. Further, soil disturbing habitat manipulations greatly increase S. invicta population densities. However, S. invicta penetrates all habitats regardless of soil disturbance history. In contrast, controlled burns depress S. invicta densities. 5. In habitats where S. invicta is prevalent, it completely replaces native fire ants. However, S. invicta impacts native ants as a whole less strongly. Intriguingly, native ants responded distinctly to S. invicta in different environments. In wet, undisturbed environments, high S. invicta abundance disrupts the spatial structure of the ant assemblage by increasing clumping and is associated with reduced species density, while in dry-disturbed habitats, sites with high S. invicta abundance possess high numbers of native species. Analyses of co-occurrence indicate that reduced species density in wet-undisturbed sites arises from negative species interactions between native ants and S. invicta. However, these same data suggest that the high native species density of abundant S. invicta sites in dry-disturbed environments does not result from facilitation. 6. Monogyne S. invicta populations play different roles in different environments, driving ant diversity loss in some, but being largely symptomatic of habitat disturbance in others.

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.

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.

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 (delta(15)N) 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 delta(15)N values of Argentine ants compare with those of other ants at the same site. Both long-term and biregional comparisons indicate that the Argentine ant's 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.

When trade-offs interact: balance of terror enforces dominance discovery trade-off in a local ant assemblage.

1. Trade-offs underpin local species coexistence. Trade-offs between interference and exploitative competitive ability provie a mechanism for explaining species coexistence within guilds that exploit overlapping resources. 2. Omnivorous, leaf litter ants exploit a shared food base and occur in species-rich assemblages. In these assemblages, species that excel at usurping food items from other species are poor at finding food items first. In assemblages where some members are attacked by phorid fly parasitoids, host species face an additional trade-off between defending themselves against parasitic attack and maximizing their competitive abilities. Host species thus face two trade-offs that interact via the trait-mediated indirect interaction generated by phorid defence behaviour. 3. In this study we test for the existence of these trade-offs and evaluate the predictions of a model for how they interact in an assemblage of woodland ants in which two behaviourally dominant members are attacked by phorid fly parasitoids as they attempt to harvest food resources. 4. The major findings are that unparasitized species in the assemblage follow a dominance-discovery trade-off curve. When not subject to attack by phorid flies, host species violate that trade-off by finding resources too quickly for their level of behavioural dominance. In contrast, when attacked by their phorid parasitoids, the host species dominance drops such that they fall into the assemblage trade-off. 5. These results match the predictions of the balance of terror model, which derives the optimal host response to parasitism, indicating that the host species balance the competing fitness costs of reduced competitive dominance and loss of workers to parasitism. This result supports the view that understanding the structure of ecological communities requires incorporating the indirect effects created by trait plasticity.

Who is the top dog in ant communities? Resources, parasitoids, and multiple competitive hierarchies.

A wide variety of animal communities are organized into interspecific dominance hierarchies associated with the control and harvest of food resources. Interspecific dominance relationships are commonly found to be linear. However, dominance relations within communities can form a continuum ranging from intransitive networks to transitive, linear dominance hierarchies. How interference competition affects community structure depends on the configuration of the dominance interactions among the species. This study explores how resource size and the trait-mediated indirect effect (TMIE) specialist phorid fly parasitoids exert on interference competition, affect the transitive nature of competitive interactions in an assemblage of woodland ants. I quantify the linearity of networks of interactions associated with large and small food resources in the presence and absence of phorid parasitoids. Two distinct, significantly linear dominance hierarchies exist within the ant assemblage depending on the size of the disputed resource. However, the presence of phorid fly parasitoids eliminates the linearity of both dominance hierarchies. The host's phorid defense behaviors reduce the competitive asymmetries between the host and its subdominant competitors, increasing the indeterminacy in the outcome of competitive interactions. Thus, both resource size variation and phorid-induced TMIEs appear to facilitate coexistence in assemblages of scavenging ants.

Linked indirect effects in ant-phorid interactions: impacts on ant assemblage structure.

Interaction modifications arise when the presence of one species alters the behavior of a second thereby altering that species' interactions with a third. Species-specific phorid parasitoids that attack ants at food resources can modify the competitive interactions between their host and competing ant species. This study examines whether interaction modifications created during interactions between the phorid fly parasitoid, Apocephalus sp. 8, its host, Pheidole diversipilosa, and ant species with which P. diversipilosa competes determine P. diversipilosa's foraging success. We also explore how varying resource size affects the ability of P. diversipilosa to capture resources and if this factor changes the nature or magnitude of the interaction modifications. We find that conflict between the host ant and competitor species at resources greatly improves the ability of the parasitoid to locate its host. In addition, the presence of a parasitoid at a food resource strongly reduces the ability of the host ant to capture that food resource when competing with other ant species. A wide variety of competitor species benefit from these linked interaction modifications and do so in accordance with their abundance in the assemblage. Finally, the size of the food resource in dispute affects the ability of the host ant to capture the resource, but parasitism and resource size affect resource turnover independently. These results are relevant to understanding the importance of interaction modifications in determining structure of ant assemblages.