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.

Distinct colony boundaries and larval discrimination in polygyne red imported fire ants (Solenopsis invicta).

Evaluating the factors that promote invasive ant abundance is critical to assess their ecological impact and inform their management. Many invasive ant species show reduced nestmate recognition and an absence of boundaries between unrelated nests, which allow populations to achieve greater densities due to reduced intraspecific competition. We examined nestmate discrimination and colony boundaries in introduced populations of the red imported fire ant (Solenopsis invicta; hereafter, fire ant). Fire ants occur in two social forms: monogyne (colonies with a single egg-laying queen) and polygyne (colonies with multiple egg-laying queens). In contrast with monogyne nests, polygyne nests are thought to be interconnected due to the reduced antagonism between non-nestmate polygyne workers, perhaps because polygyne workers habituate the colony to an odour unique to Gp-9b -carrying adults. However, colony boundaries and nestmate discrimination are poorly documented, particularly for worker-brood interactions. To delimit boundaries between field colonies, we correlated the exchange of a 15 N-glycine tracer dissolved in a sucrose solution with social form. We also evaluated nestmate discrimination between polygyne workers and larvae in the laboratory. Counter to our expectations, polygyne colonies behaved identically to monogyne colonies, suggesting both social forms maintain strict colony boundaries. Polygyne workers also preferentially fed larval nestmates and may have selectively cannibalized non-nestmates. The levels of relatedness among workers in polygyne colonies was higher than those previously reported in North America (mean ± standard error: 0.269 ± 0.037). Our study highlights the importance of combining genetic analyses with direct quantification of resource exchange to better understand the factors influencing ant invasions.

Mutualism disruption by an invasive ant reduces carbon fixation for a foundational East African ant-plant.

Invasive ants shape assemblages and interactions of native species, but their effect on fundamental ecological processes is poorly understood. In East Africa, Pheidole megacephala ants have invaded monodominant stands of the ant-tree Acacia drepanolobium, extirpating native ant defenders and rendering trees vulnerable to canopy damage by vertebrate herbivores. We used experiments and observations to quantify direct and interactive effects of invasive ants and large herbivores on A. drepanolobium photosynthesis over a 2-year period. Trees that had been invaded for ≥ 5 years exhibited 69% lower whole-tree photosynthesis during key growing seasons, resulting from interaction between invasive ants and vertebrate herbivores that caused leaf- and canopy-level photosynthesis declines. We also surveyed trees shortly before and after invasion, finding that recent invasion induced only minor changes in leaf physiology. Our results from individual trees likely scale up, highlighting the potential of invasive species to alter ecosystem-level carbon fixation and other biogeochemical cycles.

Evolutionary history of the little fire ant Wasmannia auropunctata before global invasion: inferring dispersal patterns, niche requirements and past and present distribution within its native range.

The evolutionary history of invasive species within their native range may involve key processes that allow them to colonize new habitats. Therefore, phylogeographic studies of invasive species within their native ranges are useful to understand invasion biology in an evolutionary context. Here we integrated classical and Bayesian phylogeographic methods using mitochondrial and nuclear DNA markers with a palaeodistribution modelling approach, to infer the phylogeographic history of the invasive ant Wasmannia auropunctata across its native distribution in South America. We discuss our results in the context of the recent establishment of this mostly tropical species in the Mediterranean region. Our Bayesian phylogeographic analysis suggests that the common ancestor of the two main clades of W. auropunctata occurred in central Brazil during the Pliocene. Clade A would have differentiated northward and clade B southward, followed by a secondary contact beginning about 380,000 years ago in central South America. There were differences in the most suitable habitats among clades when considering three distinct climatic periods, suggesting that genetic differentiation was accompanied by changes in niche requirements, clade A being a tropical lineage and clade B a subtropical and temperate lineage. Only clade B reached more southern latitudes, with a colder climate than that of northern South America. This is concordant with the adaptation of this originally tropical ant species to temperate climates prior to its successful establishment in the Mediterranean region. This study highlights the usefulness of exploring the evolutionary history of invasive species within their native ranges to better understand biological invasions.

Fatty Amines from Little Black Ants, Monomorium minimum, and Their Biological Activities Against Red Imported Fire Ants, Solenopsis invicta.

Red imported fire ants, Solenopsis invicta, are significant invasive pests. Certain native ant species can compete with S. invicta, such as the little black ant, Monomorium minimum. Defensive secretions may contribute to the competition capacity of native ants. The chemistry of ant defensive secretions in the genus Monomorium has been subjected to extensive research. The insecticidal alkaloids, 2,5-dialkyl-pyrrolidines and 2,5-dialkyl-pyrrolines have been reported to dominate the venom of M. minimum. In this study, analysis of defensive secretions of workers and queens of M. minimum revealed two primary amines, decylamine and dodecylamine. Neither amine has been reported previously from natural sources. Toxicity and digging suppression by these two amines against S. invicta were examined. Decylamine had higher toxicity to S. invicta workers than dodecylamine, a quicker knockdown effect, and suppressed the digging behavior of S. invicta workers at lower concentration. However, the amount of fatty amines in an individual ant was not enough to knockdown a fire ant or suppress its digging behavior. These amines most likely work in concert with other components in the chemical defense of M. minimum.

North American Invasion of the Tawny Crazy Ant (Nylanderia fulva) Is Enabled by Pheromonal Synergism from Two Separate Glands.

A new invader, the "tawny crazy ant", Nylanderia fulva (Hymenoptera: Formicidae; Formicinae), is displacing the red imported fire ant, Solenopsis invicta (Formicidae: Myrmicinae), in the southern U.S., likely through its superior chemical arsenal and communication. Alone, formic acid is unattractive, but this venom (= poison) acid powerfully synergizes attraction of tawny crazy ants to volatiles from the Dufour's gland secretion of N. fulva workers, including the two major components, undecane and 2-tridecanone. The unexpected pheromonal synergism between the Dufour's gland and the venom gland appears to be another key factor, in addition to previously known defensive and detoxification semiochemical features, for the successful invasion and domination of N. fulva in the southern U.S. This synergism is an efficient mechanism enabling N. fulva workers to outcompete Solenopsis and other ant species for food and territory. From a practical standpoint, judicious point-source release formulation of tawny crazy ant volatiles may be pivotal for enhanced attract-and-kill management of this pest.

Effects of Solenopsis invicta (Hymenoptera: Formicidae) and Its Interaction With Aphids on the Seed Productions of Mungbean and Rapeseed Plants.

Although many reports suggested the economic importance of the red imported fire ant, Solenopsis invicta Buren, few attempts to test the hypothesis that the red imported fire ant-aphid mutualism enhances the occurrence of red imported fire ant on crops, thereby interfering with their flowering and fruiting and affecting their output. To address this problem, we compare the effects of red imported fire ant on the flowering and fruiting of self-pollinating and cross-pollinating crops by field investigations and indoor experiments. In the field, our results revealed that regardless of the aphid interaction, red imported fire ant preferred flowering mungbean plants, and their activities decreased the yields of single plants, total pod number, kernel number, and kernel weight. The interaction of red imported fire ant and aphids generated unfavorable effects on rapeseed yields per plant, total pod number, grain number, grain weight, and thousand-kernel weight and stimulated an elevated proportion of malformed seeds. However, the differences were not significant if only red imported fire ant was present. In the laboratory, although red imported fire ant display no apparent preference toward the seedlings of mungbean or rapeseed, the ants clearly favor the flowering plants of mungbeans. Therefore, this study indicated that one of the main mechanisms whereby red imported fire ants affect the crop yield is by compromising the reproduction processes.

Predicting the potential distribution of the Pheidole megacephala in light of present and future climate variations.

The big-headed ant, Pheidole megacephala (Fabricius), has a widespread distribution across numerous regions globally. The International Union for Conservation of Nature (IUCN) has identified it as one of the 100 worst invasive alien species worldwide, given the severe ecological and economic harm it causes in invaded areas. In this study, we predicted the present and future global distribution of P. megacephala, taking into account known distribution points and bioclimatic factors. Our results indicated that temperature is the primary factor affecting the distribution of P. megacephala, with potential suitable areas currently found mainly in South America, Southern North America, Western Europe, Coastal areas of the Mediterranean and Red Seas, Southern Africa, Southern Asia, Islands in Southeast Asia, and coastal regions of Australia. The total suitable area spans 3,352.48 × 104 km2. In China, the potential suitable area for P. megacephala is 109.02 × 104 km2, representing 11.36% of China's land area. In the future, based on different climatic conditions, the suitable area of P. megacephala generally showed a declining trend, but some newly added suitable areas showed that it had a tendency to expand to higher latitudes. Relevant agencies should implement effective measures to control P. megacephala populations to mitigate damage in invaded areas and slow down or prevent the spread of big-headed ants into noninvaded regions.

2-Methoxybenzaldehyde effectively repels ants.

Ants can particularly make for harmful pests, infesting human homes and reducing crop yields. The damage caused by ants and the efforts to mitigate the damage are hugely costly. Broad-spectrum insecticides are used most commonly; however, due to their negative side effects, there is increasing interest in nontoxic alternatives. One promising commercially available alternative is 2-hydroxybenzaldehyde, which is naturally produced by various arthropods as a means of chemical defense and effectively repels ants. Here we conduct a structure-activity relationship investigation, testing how different chemical modifications alter the repellence of 2-hydroxybenzaldehyde. We find that 2-methoxybenzaldehyde is considerably more effective than 2-hydroxybenzaldehyde at repelling the common black garden ant, Lasius niger. We next compare the most effective repellent chemicals against 4 particularly harmful ant species to confirm that the results obtained with L. niger are general to ants and that our results are relevant to mitigate the costs of ant damage.

Complete chromosome-level genome assembly data from the tawny crazy ant, Nylanderia fulva (Mayr) (Hymenoptera: Formicidae).

The tawny crazy ant, Nylanderia fulva (Mayr) (Hymenoptera: Formicidae) has a native range that extends from northern Argentina to southern Brazil. In the U.S.A. this species has often been misidentified as Nylanderia (Paratrechina) pubens or N. cf. pubens and has likely been present in Florida and Texas for several decades [1]. In the early 2000's explosive population growth in Texas and neighboring states drew renewed taxonomic focus. Genetic analyses [2,3] aided in identifying the pest species as N. fulva. This species poses an invasive threat to native flora and fauna and human structures. In its invasive range it has been reported to displace another invasive species, the red imported fire ant. The specimens used for genome sequencing were obtained from the coastal region of Mississippi. DNA was extracted from pupae. The genome data set was deposited to the National Center for Biotechnology Information as submission ID: SUB10775679, Project ID: PRJNA796544, Accession IDs: SAMN24895442 and JAKFQQ000000000. The organism taxid is 613905, locus tag prefixes are L1K79. The assembly, USDA_Nfulva_1.0, was generated in collaboration with Dovetail Genomics (now Cantata Bio) to yield a chromosome-level assembly of 375 Mb with a 15.67 Mb N50 and 78X coverage and revealing 16 putative chromosomes. This high-quality chromosome-level genome assembly was released prior to publication as a public service to the research community.

Effect of Irrigation on the Control of Red Imported Fire Ants (Hymenoptera: Formicidae) by Water-Resistant and Standard Fire Ant Baits.

The red imported fire ant, Solenopsis invicta (Buren), is an invasive pest of agricultural, urban, and natural areas. It is also considered a public health pest due to its painful stings. While it can be efficiently controlled by commercially available fire ant baits formulated with a corn-grit carrier, rain or irrigation is thought to degrade the carrier, compromising bait effectiveness. This study assessed the effect of irrigation on the efficacy of water-resistant and standard fire ant bait formulations, by comparing worker number, brood volume, and queen survivorship after access to water-soaked baits and to irrigated, bait-treated sod. In initial testing, wetted water-resistant and standard baits reduced fire ant colonies less than dry baits, both when baits were given to colonies directly and when colonies were given access to baits broadcasted (i.e., scattered) atop sod. Comparisons of the efficacy of piled versus broadcast applications of water-resistant and standard baits revealed reductions of >88% in adults and brood and no surviving queens for all bait treatments. This result was unexpected because piled baits were hypothesized to be better protected from irrigation than broadcast bait applications. In a field study, irrigated water-resistant and standard baits caused similar and significantly higher reductions in fire ant foraging activity relative to an untreated control. These results indicated that both the water-resistant and standard fire ant bait provided significant fire ant reductions even after irrigation.

First Report of the Tramp ant Technomyrmex vitiensis Mann, 1921 (Formicidae: Dolichoderinae) in Brazil with Cytogenetic and Sperm Structure Data and an Updated Key to Brazilian Dolichoderinae Genera.

Invasive ants are usually harmful taxa and are considered a potential problem to biodiversity due to their negative ecological impacts, as they can outcompete native ant species. Ten such species are reported in Brazil. In this study, we report for the first time the Asian tramp ant Technomyrmex vitiensis Mann, 1921 at the municipality of Oiapoque, in the Brazilian Amazon. The colony studied contained workers, intercastes, males and larvae, which provided sperm structure and cytogenetic data. Considering the unprecedented report of the genus Technomyrmex as well as the recent finding of the primarily Australian genus Leptomyrmex in Brazil, we present a revised key for the workers of Brazilian Dolichoderinae genera. Technomyrmex vitiensis presented 2n = 16 chromosomes; all metacentrics and comparative cytogenetics on the genus is provided. A single rDNA 18S site located in intrachromosomal region was observed in this species, which is a common trait in ants. The spermatozoa of T. vitiensis had a filiform shape, with 78.13 (± 1.96) µm of total length and 11.43 (± 0.51) µm of nucleus length. Total and nucleus sperm size length fit with the known variation observed in other ant species. The occurrence of T. vitiensis in Brazil is probably a result of traffic between French Guiana and the Amapá state. Cytogenetics and sperm structures of T. vitiensis enhance the biological knowledge of this tramp species. We highlight the scarce knowledge of ant diversity in the state of Amapá and the consequences that the presence of this species may have in this region.

Chemical identification of an active component and putative neural mechanism for repellent effect of a native ant's odor on invasive species.

The invasive Argentine ants (Linepithema humile) and the red imported fire ants (Solenopsis invicta) constitute a worldwide threat, causing severe disruption to ecological systems and harming human welfare. In view of the limited success of current pest control measures, we propose here to employ repellents as means to mitigate the effect of these species. We demonstrate that cuticular hydrocarbons (CHCs) used as nestmate-recognition pheromone in the Japanese carpenter ant (Camponotus japonicus), and particularly its (Z)-9-tricosene component, induced vigorous olfactory response and intense aversion in these invasive species. (Z)-9-Tricosene, when given to their antennae, caused indiscriminate glomerular activation of antennal lobe (AL) regions, creating neural disarray and leading to aversive behavior. Considering the putative massive central neural effect, we suggest that the appropriate use of certain CHCs of native ants can facilitate aversive withdrawal of invasive ants.

Population genetic structure of the globally introduced big-headed ant in Taiwan.

Global commerce and transportation facilitate the spread of invasive species. The African big-headed ant, Pheidole megacephala (Fabricius), has achieved worldwide distribution through globalization. Since the late 19th century, Taiwan has served as a major seaport because of its strategic location. The population genetic structure of P. megacephala in Taiwan is likely to be shaped by international trade and migration between neighboring islands. In this study, we investigated the population genetics of P. megacephala colonies sampled from four geographical regions in Taiwan and elucidated the population genetic structures of P. megacephala sampled from Taiwan, Okinawa, and Hawaii. We observed a low genetic diversity of P. megacephala across regions in Taiwan. Moreover, we noted low regional genetic differentiation and did not observe isolation by distance, implying that long-distance jump dispersal might have played a crucial role in the spread of P. megacephala. We sequenced the partial cytochrome oxidase I gene and observed three mitochondrial haplotypes (TW1-TW3). TW1 and TW3 most likely originated from populations within the species' known invasive range, suggesting that secondary introduction is the predominant mode of introduction for this invasive ant. TW2 represents a novel haplotype that was previously unreported in other regions. P. megacephala populations from Taiwan, Okinawa, and Hawaii exhibited remarkable genetic similarity, which may reflect their relative geographic proximity and the historical connectedness of the Asia-Pacific region.

First Polycipivirus and Unmapped RNA Virus Diversity in the Yellow Crazy Ant, Anoplolepis gracilipes.

The yellow crazy ant, Anoplolepis gracilipes is a widespread invasive ant that poses significant threats to local biodiversity. Yet, compared to other global invasive ant species such as the red imported fire ant (Solenopsis invicta) or the Argentine ant (Linepithema humile), little is known about the diversity of RNA viruses in the yellow crazy ant. In the current study, we generated a transcriptomic database for A. gracilipes using a high throughput sequencing approach to identify new RNA viruses and characterize their genomes. Four virus species assigned to Dicistroviridae, two to Iflaviridae, one to Polycipiviridae, and two unclassified Riboviria viruses were identified. Detailed genomic characterization was carried out on the polycipivirus and revealed that this virus comprises 11,644 nucleotides with six open reading frames. Phylogenetic analysis and pairwise amino acid identity comparison classified this virus into the genus Sopolycivirus under Polycipiviridae, which is tentatively named "Anoplolepis gracilipes virus 3 (AgrV-3)". Evolutionary analysis showed that AgrV-3 possesses a high level of genetic diversity and elevated mutation rate, combined with the common presence of multiple viral strains within single worker individuals, suggesting AgrV-3 likely evolves following the quasispecies model. A subsequent field survey placed the viral pathogen "hotspot" of A. gracilipes in the Southeast Asian region, a pattern consistent with the region being recognized as part of the ant's native range. Lastly, infection of multiple virus species seems prevalent across field colonies and may have been linked to the ant's social organization.

The complete mitochondrial genome of yellow crazy ant, Anoplolepis gracilipes (Hymenoptera: Formicidae).

The yellow crazy ant Anoplolepis gracilipes is an invasive species that threatens biodiversity in introduced ecosystems. We sequenced the A. gracilipes mitogenome using next-generation sequencing methods. The circular mitogenome of A. gracilipes was 16,943 bp included 13 protein-coding genes, two ribosomal RNA genes, 22 transfer RNAs, and a single large non-coding region of 893 bp. The base composition was AT-biased (72%). Three genomic rearrangements compared to ancestral insects were found. Phylogenetic analysis based on the concatenated nucleotide sequences of the 13 protein-coding genes supports A. gracilipes belonging to the Formicinae subfamily. We announce the A. gracilipes mitogenome as a DNA reference for further population genetic, phylogenetic, and evolutionary analyses.

A Review of the Tawny Crazy Ant, Nylanderia fulva, an Emergent Ant Invader in the Southern United States: Is Biological Control a Feasible Management Option?

The tawny crazy ant, Nylanderia fulva (Mayr) (Hymenoptera: Formicidae), has invaded states of the U.S. including Texas, Louisiana, Mississippi, Alabama, Florida, and Georgia. Native to South America, N. fulva is considered a pest in the U.S. capable of annoying homeowners and farmers, as well as displacing native ant species. As it continues to expand its range, there is a growing need to develop novel management techniques to control the pest and prevent further spread. Current management efforts rely heavily on chemical control, but these methods have not been successful. A review of the biology, taxonomy, ecology, and distribution of N. fulva, including discussion of ecological and economic consequences of this invasive species, is presented. Options for future management are suggested focusing on biological control, including parasitoid flies in the genus Pseudacteon, the microsporidian parasite Myrmecomorba nylanderiae, and a novel polynucleotide virus as potential biological control agents. We suggest further investigation of natural enemies present in the adventive range, as well as foreign exploration undertaken in the native range including Paraguay, Brazil, and Argentina. We conclude that N. fulva may be a suitable candidate for biological control.