Zombie fire ant workers: behavior controlled by decapitating fly parasitoids

Laboratory observations were conducted on four separate red imported fire ant, Solenopsis invicta, colonies that contained workers parasitized by the decapitating fly, Pseudacteon tricuspis. Parasitized S. invicta workers remained inside the nest during parasitoid larval development and left the nest approximately 8 – 10 hours before decapitation by the parasitoid. When parasitized ants left the nest, they were highly mobile, were responsive to tactile stimuli, and showed minimal defensive behavior. Ants ultimately entered into a grass thatch layer, where they were decapitated and the fly maggots pupariated. This study reveals that parasitized ants exhibit behaviors that are consistent with host manipulation to benefit survival of the parasitoid. Received 9 November 2006; revised 26 January 2007; accepted 7 February.     

Post-Release Host-Specificity Testing of Pseudacteon tricuspis, a Phorid Parasitoid of Solenopsis Invicta Fire Ants

Inherent in any biological control program is the risk of nontarget effects. Pseudacteon tricuspisBorgmeier, a parasitoid phorid fly, has been introduced to the United States from South America as a potential biocontrol agent of the red imported fire ant, Solenopsis invictaBuren. We conducted tests of host specificity on introduced populations of P. tricuspis, which are attracted to alarm pheromones released by their hosts during events such as mound disturbances and interspecific interactions. We monitored disturbed mounds of S. invicta and its close congener, S. geminata(F.), during the expansion of P. tricuspis across north Florida and after populations had been established for ~3 years. We also tested host acceptance in established populations of P. tricuspis by offering trays containing S. invicta, S. geminata, and 14 additional ant species representing 12 different non-Solenopsis genera. Although P. tricuspiswas commonly observed to hover over and attempt to oviposit on S. invicta, we never observed any parasitization attempts on any other ant species. As predicted by laboratory tests, released populations of P. tricuspis appear to be highly host specific and pose no obvious threat to nontarget species.     

Host preference in Pseudacteon phorid flies: response of P. tricuspis and P. curvatus to black, red and hybrid imported Solenopsis fire ants in multiple choice bioassays

Host preferences in both sexes of Pseudacteon tricuspis Borgmeier (Jaguariuna biotype) and Pseudacteon curvatus Borgmeier (Formosa biotype) and their relative attraction to the imported fire ants (IFA), Solenopsis invicta Buren (red IFA), Solenopsis richteri Forel (black IFA) and S. invicta × S. richteri hybrids (hybrid IFA) were investigated in two separate experiments utilizing multiple choice flight bioassays. The results of both experiments clearly showed that both sexes of the Jaguariuna biotype of P. tricuspis could distinguish among the three IFA species and demonstrated greater preference for hybrid IFA and red IFA. This conclusion is supported by a variety of data collected on the number of fly visits, attack rate, and hovering duration (Experiment 1), and on the number of trapped flies (Experiment 2), which showed that black IFA is the least preferred of the three species. Similar results were recorded for the Formosan biotype of P. curvatus, although the data were not as strongly conclusive. Females of this biotype spent a significantly greater amount of time in hovering mode over red IFA and hybrid IFA compared to black IFA, but the other data were not significant. The red IFA is the natural host of both phorid fly biotypes and our results suggest that both biotypes may have evolved a specialized relationship with red IFA including an ability to discriminate it from related fire ants. These results are discussed in relation to the possible role of fire ant chemicals in mediating host preferences in phorid flies, contributions of male phorid flies to fire ant biocontrol, and the practical implications of the key findings.     

Evaluating biological control of fire ants using phorid flies: effects on competitive interactions

The effects of the parasitic phorid fly, Pseudacteon tricuspis Borgmeier, on the competitive interactions between the red imported fire ant, Solenopsis invicta Buren, and a native North American ant, Forelius pruinosus (Roger), were investigated in the laboratory. P. tricuspis is a highly host-specific endoparasitoid of S. invicta workers that is currently being reared and released as a biological control agent of S. invicta in the US. We tested the effect of P. tricuspis on the colony growth rate of S. invicta when S. invicta was forced to compete with F. pruinosus for a protein resource (freeze-killed crickets) in laboratory competition arenas. In addition to colony growth rate, we quantified the effect of the phorid flies on the foraging rate of S. invicta. Though S. invicta significantly reduced its foraging rate in the presence of the phorid flies, we did not detect an effect of the flies on colony growth rate. Possible explanations for these results include behavioral compensation by S. invicta for the presence of the flies. We present these laboratory results in light of a literature search indicating that laboratory tests of biological control agent efficacy are good predictors of field efficacy. We conclude that P. tricuspis alone is unlikely to suppress S. invicta populations in the field by reducing their competitive ability.     

Behavioral and Electroantennogram Responses of Phorid fly <Emphasis Type="Italic">Pseudacteon tricuspis</Emphasis> (Diptera: Phoridae) to Red Imported Fire Ant <Emphasis Type="Italic">Solenopsis invicta</Emphasis> Odor and Trail Pheromone

The phorid fly, Pseudacteon tricuspis is an introduced parasitoid of the red imported fire ant, Solenopsis invicta in the United States. Previous studies show that phorid flies are attracted to host ant workers at disturbed colonies, to colonies exhibiting aggressive interspecific interactions, and to fire ant mating flights. In a series of behavioral and electroantennogram (EAG) experiments, we confirm the possible use of fire ant odor as cues for host location by P. tricuspis. We tested the response of P. tricuspis of different sex and mating status to several host-related odor stimuli including live fire ant workers, extracts of worker whole body, head, thorax, and abdomen, and (E,E)-α-farnesene, a trail pheromone component of Solenopsis fire ants. Results from Y-tube olfactometer bioassays demonstrated the attraction of mated female P. tricuspis to live S. invicta workers. In addition, extracts of S. invicta worker whole body and thorax elicited strong olfactometer response in female flies (mated and unmated) and mated males, but not in unmated males. Pseudacteon tricuspis did not show significant attraction to extracts of S. invicta worker head and abdomen, or to (E,E)-α-farnesene, irrespective of sex and mating status. In EAG experiments, female and male P. tricuspis showed significant EAG response to extracts of worker whole body, head, and abdomen, and to a less extent, thorax extract, but not to (E,E)-α-farnesene. Females showed slightly greater EAG response than males, but EAG response was not affected by mating status. These results suggest that fire ant thorax is likely the source of kairomones used as host location cues by P. tricuspis, and support the hypothesis that fire ant worker trail pheromones are not likely used by P. tricuspis for host location.     

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.     

Phorid fly, Pseudacteon tricuspis, response to alkylpyrazine analogs of a fire ant, Solenopsis invicta, alarm pheromone

The phorid fly, Pseudacteon tricuspis Borgmeier, is a parasitoid of the red imported fire ant, Solenopsis invicta Buren. This fly has been reported to use fire ant chemicals, specifically venom alkaloids and possibly alarm pheromone to locate its host. A recent study identified 2-ethyl-3,6-dimethyl pyrazine as a component of the alarm pheromone of S. invicta. To determine the possible involvement of this fire ant alarm pheromone component in mediating fire ant-phorid fly interactions, we tested electroantennogram (EAG) and behavioral responses of P. tricuspis females to the commercially available mixture of 2-ethyl-3,6-dimethyl pyrazine and its 3,5-dimethyl isomer, as well as six structurally related alkylpyrazine analogs at varying doses. Pseudacteon tricuspis females showed significant EAG response to 2-ethyl-3,6(or 5)-dimethyl pyrazine (herein referred to as pheromone-isomer) at all doses, 0.001-10 μg. Among the tested alkylpyrazine analogs, 2,3-diethyl-5-methyl pyrazine showed significant EAG activity at 0.1 and 1 μg. 2,3-dimethyl pyrazine also showed significant EAG activity at 0.1 μg. Results of four-choice olfactometer bioassays demonstrated significant attraction of P. tricuspis females to the pheromone-isomer (2-ethyl-3,6(or 5)-dimethyl pyrazine) at all tested doses (0.01, 0.1, 1 and 10 μg). The analogs, 2,3-diethyl-5-methyl pyrazine and 2,3-dimethyl pyrazine were significantly better than the control at the higher doses (0.1, 1 and 10 μg). The pheromone-isomer was significantly better than both analogs at two doses, 0.1 and 1 μg. These results confirm that the reported fire ant alarm pheromone component plays a role in mediating attraction of phorid flies to host workers. Venom alkaloids were previously shown to attract P. tricuspis; therefore, we propose that fire ant alarm pheromones may act in tandem or synergistically with venom alkaloids to attract phorid fly parasitoids to fire ant workers.     

昆明红火蚁种群发生特征

【目的】2013年10月云南省元谋县首次发现红火蚁。掌握红火蚁蚁巢各品级发生动态,能为当地红火蚁的防控提供技术支撑。【方法】2015年1—12月,在昆明宜良县对红火蚁蚁巢取样、分离,红火蚁取样、称重,统计红火蚁各品级的头数。【结果】地上蚁巢红火蚁蚁群数量发生高峰期在8—9月,其次是3—4月。蚁后数量比例高峰在3—4月;有翅雌蚁比例高峰在4月,其次是7月;有翅雄蚁比例高峰的在5月,其次是9月;生殖蚁幼虫和蛹比例高峰的3、4和12月。地上蚁巢工蚁、兵蚁、职能蚁幼虫和蛹数量发生的高峰期在8—9月,发生小高峰期在4月。【结论】昆明红火蚁蚁群数量动态有2个峰值,第一个峰值为8—9月,以职能蚁防治为主;第二个蜂值3—4月,以生殖蚁和职能蚁防治为主。该结果为昆明红火蚁防控技术提供了数据支撑。     

红火蚁迁巢时间动态及与生境类型和蚁群社会型的关系

红火蚁Solenopsis invicta是我国具有重大生态和经济影响的入侵物种,明确其蚁群迁移(迁巢)发生情况对理解其生态适应性及科学制定防控策略具有重要意义,迄今虽已有这方面的一些报道,但有关其迁巢发生程度、季节特点及不同生境中是否存在差异等缺乏认识。研究对浙江中部一草地中两种社会型红火蚁迁巢情况进行了观察,同时在浙江、江西、广东调查了31个红火蚁发生区块中(以绿化带和荒草地为主)的空巢比例。结果显示,在单蚁后型红火蚁活动季节,几乎各个时期均有蚁巢被废弃,以2-7月废弃比例较高(最高接近12%),8月下旬后则明显较低;废弃巢穴和新巢形成之间无明显数量关系。废弃蚁巢被重新利用的现象也在各月均有发生,且与废巢总数量存在显著正相关。多蚁后型弃巢比例总体要低于单蚁后型。在所调查的各地31个区块中,有27个(87.1%)见到空巢;空巢比例在不同社会型、生境和区块间存在一定差异。其中绿化带中80%所查区块的空巢比例为10%-35%,在荒草地中则接近70%的区块空巢比例不到10%,但这两类生境中均有个别区块空巢比例高于35%。表明红火蚁迁巢是一种普遍现象并存在明显的季节特征,迁巢后所形成的空巢比例因地而异,且与生境类型、蚁群社会型等存在一定关系。     

Parasitoid–host relationships when host size varies: the case of Pseudacteon flies and Solenopsis fire ants

Abstract. 1. Phorid flies in the genus Pseudacteon are parasitoids of ants. Variation in host size preferences of four South American and two North American Pseudacteon species on monogyne and polygyne forms of their host Solenopsis species [ S. invicta Buren and S. geminata (F.), respectively] was documented.
2. Monogyne Solenopsis workers were, on average, significantly larger than polygyne workers, and the average size monogyne worker attacked was significantly larger than the average size polygyne worker attacked in four of the six Pseudacteon species.
3. Three South American Pseudacteon species attacked larger than average size workers, whereas one attacked smaller than average size workers, in both monogyne and polygyne forms. Both North American Pseudacteon species attacked larger than average size polygyne workers and smaller than average size monogyne workers.
4. Three Pseudacteon species were reared from eggs to adults in infected ants in the laboratory. The size of the emergent phorid fly was related positively to the size of the host worker ant, with females emerging from larger hosts. Similar patterns were documented for both monogyne and polygyne forms.
5. The mean size of worker host from which phorids emerged did not differ significantly between the monogyne and polygyne forms in the subsample of phorids reared to adults.
6. The observed patterns elucidate factors that may cause variation in Pseudacteon sex ratios, and have implications for biological control efforts of pest Solenopsis species.     

Ecological interactions of Pseudacteon parasitoids and Solenopsis ant hosts: environmental correlates of activity and effects on competitive hierarchies

1. Solenopsis (Hymenoptera: Formicidae) fire ants are host to Pseudacteon (Diptera: Phoridae) parasitoids. The activity of S. geminata (F.) hosts and relative abundance of Pseudacteon phorids, along with five environmental variables, were measured at weekly intervals over an 8‐month period at two sites. 2. Pseudacteon relative abundances often varied greatly from week to week, and were only weakly positively correlated with S. geminata activity. 3. A quadratic function of soil temperature was the single best predictor of ant activity at both sites, explaining 32 and 73% of the variation in ant activity. A linear function of soil moisture was the single best predictor of phorid relative abundance at one site (r² = 0.23) whereas no measured variables were significant predictors of phorid relative abundance at the other site. 4. Interspecific interactions at 600 baits were monitored at a third site to document dominance hierarchies and determine whether the presence of Pseudacteon phorids mediated interspecific interactions in their host, S. geminata. 5. Solenopsis geminata was near the top of dominance hierarchies, which did not diverge greatly from a linear pattern. Three species (S. geminata, S. invicta Buren, and Crematogaster laeviuscula Mayr) won the majority of their interspecific interactions and appear to be co‐dominants at this microhabitat‐rich site. 6. Overall, the presence of phorids had no significant effect on the outcome of interspecific contests involving S. geminata and all other ant species grouped together. Phorids may have contributed to some of the S. geminata losses against other co‐dominant species.     

Conditions favoring queen execution in young social insect colonies

Summary. Previous attempts to explain worker aggression against extra queens in young social insect colonies have used kin selection arguments. These have been inconsistent with experimental evidence demonstrating aggression against extra queens without strong evidence of kin discrimination. Using a game theoretical model, I suggest a series of decision rules that are consistent with the current experimental evidence from study of young colonies of the fire ant Solenopsis invicta. These decision rules are: 1) When workers cannot directly determine which queen is their mother, they should behave in favor of a queen that maximizes the product of the chance that a queen is the workers mother multiplied by the chance that it will survive to colony maturity. In some cases, the survival potential of the different queens may be the only character that influences the workers decision. 2) Workers should delay aggression against extra queens until the workers can gain their greatest advantage through such aggression. 3) Queens may adopt strategies that allow them to dominate rivals, either by gaining an advantage in fights among the queens or by increasing their attractiveness to workers.Received 2 June 2004; revised 5 July 2004; accepted 14 July 2004.     

Defensiveness of the fire ant, Solenopsis invicta, is increased during colony rafting

Colonies of the fire ant, Solenopsis invicta, can survive flood conditions by forming a raft of ants that floats on the water’s surface until the flood recedes or higher ground is found. Having been forced from the protection of their subterranean nests, rafting colonies are totally exposed and are without retreat. I tested the hypothesis that rafting S. invicta colonies would compensate for their elevated vulnerability by increasing their defensiveness. I measured defensiveness using the amount of venom workers delivered per sting (venom dose), since the repellent effects (i.e., pain and tissue damage) of fire-ant venom are dose-dependent. In the laboratory I assayed colony defensiveness before and after flooding colonies from their nests with water. Colonies were consistently and significantly more defensive while rafting (i.e., each colony’s workers delivered higher venom doses when their colony was rafting than they did when it was assayed pre-flood). The larger venom doses of rafting colonies may reduce their chances of being damaged by encounters with other animals by reducing the duration of such encounters through increased repellency. Encounters with S. invicta during flood conditions have the potential to be unusually dangerous; large concentrations of workers are exposed and available for defense, and they deliver significantly larger venom doses when they sting. Received 29 March 2005; revised 20 June 2005; accepted 24 June 2005.     

A newly-discovered mode of colony founding among fire ants

Summary Queen ants start new colonies either unassisted by workers (independent founding), assisted by workers from their natal nest (dependent founding), or assisted by the workers of other species (dependent, socially parasitic). The monogyne form of the fire ant,Solenopsis invicta, founds independently in summer, but in the fall it also produces a few sexuals some of which overwinter, then fly and mate in early spring. These overwintered queens lack the nutritional reserves and behaviors for independent colony founding. Rather, they seek out unrelated, mature, orphaned colonies, enter them and exploit the worker force to found their own colony through intraspecific social parasitism. Success in entering orphaned colonies is higher when these lack overwintered female alates of their own. When such alates are present, orphaning causes some to dealate and become uninseminated replacement queens, usually preventing entry of unrelated, inseminated replacement queens. Such colonies produce large, all-male broods. Successful entry of a parasitic queen robs the host colony of this last chance at reproductive success. Only overwintered sexuals take part in this mode of founding.     

基于气候变化情景下红火蚁在贵州的适生区预测

【目的】预测分析红火蚁的贵州适生区,以便制定有效的管控措施,防止红火蚁在贵州进一步蔓延。【方法】基于环境变量数据和红火蚁在贵州的发生分布数据,运用MaxEnt生态位模型与ArcGIS分析相结合预测方法,模拟预测红火蚁在当前和未来气候条件下在贵州的适生区域。并通过ROC (receiver operatin characteristic)曲线下面积(area under the curve, AUC)评估预测模型的精度。【结果】红火蚁MaxEnt模型预测结果训练数据和测试数据的AUC值分别为0.935和0.932,预测结果精度高。红火蚁在贵州的潜在适生区面积约占全省面积的72.56%,高、中、低适生区各占全省面积的8.92%、31.99%、31.65%。高、中适生区主要集中于贵州南部。其中,高适生区主要集中在贵州省黔西南州以及黔东南等少量地区;中适生区是高适生区的外围扩展,主要分布在安顺市、黔南州和黔东南州。未来不同气候情景下,红火蚁在贵州的适生区面积总体呈增加势态,其质心逐渐向北迁移。环境变量重要性分析结果表明,影响红火蚁在贵州分布的关键环境因子为温度和降水。【结论】红火蚁在贵州省潜在适生范围广,需强化监测预警体系建设,采取有效控制措施,阻止红火蚁传播,减少经济损失。     

Expressed sequence tags from the red imported fire ant, Solenopsis invicta: annotation and utilization for discovery of viruses

An expression library was created and 2304 clones sequenced from a monogyne colony of Solenopsis invicta. The primary intention of the project was to utilize homologous gene identification to facilitate discovery of viruses infecting this ant pest that could potentially be used in pest management. Additional genes were identified from the ant host and associated pathogens that serve as an important resource for studying these organisms. After assembly and removal of mitochondrial and poor quality sequences, 1054 unique sequences were yielded and deposited into the GenBank database under Accession Nos. EH412746 through EH413799. At least nine expressed sequence tags (ESTs) were identified as possessing microsatellite motifs and 15 ESTs exhibited significant homology with microsporidian genes. These sequences most likely originated from Thelohania solenopsae, a well-characterized microsporidian that infects S. invicta. Six ESTs exhibited significant homology with single-stranded RNA viruses (3B4, 3F6, 11F1, 12G12, 14D5, and 24C10). Subsequent analysis of these putative viral ESTs revealed that 3B4 was most likely a ribosomal gene of S. invicta, 11F1 was a single-stranded RNA (ssRNA) virus contaminant introduced into the colony from the cricket food source, 12G12 appeared to be a plant-infecting tenuivirus also introduced into the colony as a field contaminant, and 3F6, 14D5, and 24C10 were all from a unique ssRNA virus found to infect S. invicta. The sequencing project illustrates the utility of this method for discovery of viruses and pathogens that may otherwise go undiscovered.     

Potential Global Range Expansion of the Invasive Fire Ant, Solenopsis invicta

The red imported fire ant, Solenopsis invicta Buren, is an invasive pest that has become widespread in the southern United States and Caribbean after introduction from South America in the 1930s. This species, which has diverse detrimental impacts on recipient communities, was recently discovered in Australia and New Zealand and has the potential to colonize numerous other regions. We used a dynamic, ecophysiological model of colony growth to predict the potential global range expansion of this invasive species. Based on minimum and maximum daily temperatures, the model estimates colony alate production and predicts future geographic range limits. Because S. invicta populations are limited by arid conditions as well as cold temperatures, we superimposed precipitation data upon temperature-based predictions, to identify regions that do not receive enough rainfall to support this species across the landscape. Many areas around the globe, including large portions of Europe, Asia, Africa, Australia, and numerous island nations, are at risk for S. invicta infestation. Quarantine officials should be vigilant for any accidental introductions of this pest in susceptible regions. Costs of eradication increase dramatically as the area of infestation grows, and large infestations may be impossible to eradicate. Other South American Solenopsis fire ants (e.g., S. richteri Forel) may become invasive if the opportunity arises, and our predictions for S. invicta may approximate the potential range limits for these species as well.     

Rodents balancing a variety of risks: invasive fire ants and indirect and direct indicators of predation risk

We used foraging trays to compare how oldfield mice, Peromyscus polionotus, altered foraging in response to the presence of fire ants, Solenopsis invicta, and in the presence of direct (predator urine) and indirect (sheltered or exposed microhabitat, moonlight, and precipitation) indicators of predation risk. Foraging reductions elicited by S. invicta were greater than reductions in response to well-documented indicators of risk (i.e., moonlit nights) and the presence of predator urine. The presence of S. invicta always led to reduced foraging, but the overall impact of S. invicta was dependent upon microhabitat and precipitation. When S. invicta was not present, foraging was greater in sheltered microhabitats compared to exposed microhabitats. S. invicta made sheltered microhabitats equivalent to more risky exposed microhabitats, and this effect was especially pronounced on nights without precipitation. The effect of S. invicta suggests that interactions with S. invicta may entail a potentially heavy cost or that presence of S. invicta may represent a more reliable indicator of imminent competition or predation compared to indirect cues of risk and predator urine. The presence of S. invicta led to reduced foraging under situations when foraging activity would otherwise be greatest (i.e., under vegetative cover), potentially reducing habitat quality for P. polionotus and the distribution of seeds consumed by rodents.     

Prevalence of Thelohania solenopsae infected Solenopsis invicta newly mated queens within areas of differing social form distributions

Newly mated queens (NMQs) originating from monogyne red imported fire ant (Solenopsis invicta) colonies and following a mating flight, initiate new colonies by sealing themselves in a nuptial chamber and relying solely on their own fat and crop reserves, as well as no longer needed wing muscles to rear their first workers (claustral colony foundation). This method of colony-founding is rarely successful for polygyne-derived NMQs, whose low weight critically limits the number of first workers they are able to produce. However, this observation may be confounded by the parasitic microsporidium, Thelohania solenopsae, thus far found to persist only in association with polygyne colonies. Infections of this microsporidium reduce the weight of female alates and may explain why polygyne NMQs are unlikely to successfully found colonies claustrally. NMQs collected following mating flights in Gainesville and Ocala, Florida were sorted by weight, checked for insemination and T. solenopsae infection. Insemination levels were greater than 90% for all weight classes at both collection sites and were not related to infection. Infection levels were lower in Gainesville than Ocala, averaging 1.67% and 14.14%, respectively. Polygyne-derived NMQs collected in Ocala, defined here as weighing 12mg (social form correctly assigned in 85% of samples examined by PCR), had the highest infection levels, 25.37% (17/67) in 2003 and 21.43% (6/28) in 2004. We conclude that infection by T. solenopsae cannot be completely responsible for the inability of polygyne NMQs to claustrally establish colonies.