Foraging ecology and patterns of diversification in dipteran parasitoids of fire ants in south Brazil

1. At least sixteen species of parasitoid flies in the genus Pseudacteon (family Phoridae) attack fire ants in the Solenopsis saevissima subcomplex in South America. Little is known of behavioural or ecological differences among Pseudacteon parasitoids of fire ants, although their coexistence in multispecies communities would suggest that important differences exist. Seven Pseudacteon species in two separate communities were studied in south-east Brazil. The way in which hosts detect and respond to the presence of parasitoids, attack rates of the parasitoids, and host location behaviour of the parasitoids were examined.
2. Reductions in fire ant recruitment were more closely related to the number of ants attacked along a foraging trail than to the amount of time that a phorid was present.
3. Pseudacteon solenopsidis differed from other phorid species by flying backwards while pursuing ants, by attacking at lower rates than other phorids, and by spending longer around fire ant foraging trails than other phorids before departing. Fire ant recruitment to food often rebounded in the continued presence of P. solenopsidis.
4. In each of the two communities, certain Pseudacteon species appeared frequently at Solenopsis foraging trails, whereas others appeared predominantly at mound disturbances. Two distinct size classes of phorids were present in each community, and the community with the larger ant host species also had a third and larger phorid species. No phorid species from the same community had similar body sizes and similar host location behaviours, although numerous species from different communities shared both of these traits.
5. Heterogeneity in host size and in the ecological circumstances under which hosts are vulnerable to attack appears to have influenced the evolution and perhaps maintenance of diverse Pseudacteon communities.     

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.     

Phorid fly parasitoids of invasive fire ants indirectly improve the competitive ability of a native ant

Abstract.  1. The red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), is an invasive species of south-eastern U.S.A. Since its introduction from South America approximately 70 years ago, this pest has devastated natural biodiversity.
2. Due to such ecological costs, Pseudacteon phorid fly parasitoids (Diptera: Phoridae) from South America are being introduced into the U.S.A. as a potential biological control agent. Here, the indirect effects of these specialised parasitoids on an interspecific native ant competitor, Forelius mccooki (Hymenoptera: Formicidae), are evaluated.
3. Over the course of a 50-day laboratory experiment, the results show that the native ant improved aspects of exploitative, but not interference, competition when S. invicta -attacking flies were present compared with when they were absent.
4.  Forelius mccooki colonies from the phorid treatment had approximately twice as many foragers at food baits relative to controls; however, there was no significant difference in interference aspects of competition or native ant colony growth between the two treatments.
5. These results suggest that the S. invicta -specialised parasitoids help shift the competitive balance more in favour of F. mccooki than if these flies were not present; however, this competitive advantage does not translate into increased colony growth after 50 days. These laboratory findings are interpreted with regard to the more complex interactions in the field.     

Assembly rules for functional groups of North American shrews: effects of geographic range and habitat partitioning

Trophic cascades exist in numerous terrestrial systems, including many systems with ants as the top predator. Many studies show how behavioral modifications of herbivores are especially important in mediating species interactions and trophic cascades. Although most studies of trophic cascades focus on predator-herbivore-plant links, the trophic cascades concept could be applied to almost any level of trophic interactions. Especially considering the importance of parasites we consider here the interactions between the parasitic phorid fly, Pseudacteon sp. (Diptera: Phoridae), its ant host, Azteca instabilis (F. Smith) (Hymenoptera: Formicidae), and the herbivore, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae) in the coffee agroecosystem. We investigated the effects of phorid flies on ant behavior by monitoring ant recruitment to tuna baits over a 30-min period in the presence or absence of phorid flies. To study the indirect effects of phorids on larvae, we placed baits on coffee plants to elevate ant foraging levels to levels near to ant nests, placed larvae near baits, and recorded the effects of ants on larvae either in the presence or absence of phorid flies. We found that phorid fly presence significantly reduced ant ability to recruit to baits through behavioral modifications and also significantly lessened ant ability to attack, carry away, or force herbivores off plants. We conclude there is a behaviorally-modified species-level trophic cascade in the coffee agroecosystem, with potentially important effects in ant and herbivore communities as well as for coffee production.     

Phorid flies, Pseudacteon spp. (Diptera: Phoridae), affect forager size ratios of red imported fire ants Solenopsis invicta (Hymenoptera: Formicidae) in Texas

Multiple species of Pseudacteon phorid flies (Diptera: Phoridae) are currently being released throughout the southern United States to aid biological control of red imported fire ants, Solenopsis invicta Buren (Hymenoptera: Formicidae). It is anticipated that these flies will interfere with S. invicta foraging, allowing native ant assemblages to outcompete S. invicta for available resources. Numerous studies have shown a decrease in S. invicta foraging intensity when exposed to phorids. This study documents a behavioral change in phorid-exposed S. invicta colonies at a phorid release site in central Texas. Significant differences in forager size ratios were detected between phorid-exposed and phorid-absent colonies. A similar phenomenon was recently documented in the native range of these insects in South America as well. Experimental manipulation of ratios of S. invicta worker sizes has been shown to have important effects on colony success. This newly documented phorid-mediated S. invicta colony-level effect represents a significant shift in S. invicta foraging dynamics and may provide an additional mechanism by which phorids can influence S. invicta populations in their United States range.     

Indirect effects of phorid fly parasitoids on the mechanisms of interspecific competition among ants

Indirect effects, which occur when the impact of one species upon another requires the existence of an intermediary species, are apparently very common and may be of greater magnitude than direct effects. Behaviorally mediated indirect effects occur when one species affects the behavior of a second, which in turn affects how that species interacts with a third. I studied behaviorally mediated indirect effects on the mechanisms of competition in two congeneric fire ant species in the presence and absence of parasitoid phorid flies, which parasitized only one ant species. In observational and experimental field studies, the presence of native Texas phorid flies in the genus Pseudacteon decreased food retrieval by their host, Solenopsis geminata (F.), by as much as 50%. In the presence of phorid flies, many S. geminata workers assumed a stationary, curled defensive posture and did not forage. Although the phorid parasitoids had a relatively large effect on exploitative competition, there was no measurable effect on interference competition. Fierce interspecific aggression was observed between S. geminata and S. invicta Buren, and the presence of phorids had no effect on the outcome of these contests. The indirect effects of Pseudacteon parasitoids on Solenopsis fire ant resource retrieval appear to be larger than the direct effect of mortality. Some aspects of the foraging behavior of these Solenopsis species may be, in part, evolutionary adaptations to phorid parasitoid pressure. Because of the relatively large indirect effects, South American Pseudacteon phorids may be promising biocontrol agents of imported fire ants, S. invicta, in the USA. In a laboratory study, a single South American Pseudacteon female was able to significantly decrease food retrieval rates of a North American population of the imported fire ant, S. invicta. Received: 11 May 1998 / Accepted: 18 April 1999     

Developmental rates and host specificity for Pseudacteon parasitoids (Diptera: Phoridae) of fire ants (Hymenoptera: Formicidae) in Argentina

This study extends our comparative knowledge of Pseudacteon interactions with Solenopsis fire ant workers. Reported in this work are development times for seven Argentinean parasitoid species reared on two hosts, Solenopsis richteri Forel and Solenopsis invicta Buren, under laboratory temperature regimes comparable with those of the climatic zones occupied by these host species. Developmental times spanned 31-66 d across phorid species, and in general did not differ between genders or host species, but were longer at lower temperatures. The size distribution of flies reared was bimodal, with a group of large (Pseudacteon borgmeieri, Pseudacteon nocens, Pseudacteon obtusus and Pseudacteon tricuspis) and small (Pseudacteon cultellatus, Pseudacteon curvatus, and Pseudacteon nudicornis) species. P. borgmeieri was exceptional with respect to length of developmental time. Also reported are results of initial oviposition and developmental studies of some of these phorid species on other Argentinean Solenopsis ant species; P. curvatus was the only species able to complete its development on nonhost fire ants. These results support the concept of incorporating several complementary species of Pseudacteon in the biological control of pest fire ants.     

Interactions between ant species increase arrival rates of an ant parasitoid

Behaviours or traits associated with aggression and communication may increase an animal's conspicuousness to predators or parasitoids. Most examples of this come from instances of aggression or communication within a species. We tested whether interspecific encounters between ants enhance the host location success of a parasitoid (Diptera: Phoridae) that attacks ants in the genus Linepithema. At food resources recruited to by Linepithema, parasitoid discovery rates were lower when Linepithema was alone than when other ant species were present. In experimentally controlled encounters, parasitoid discovery rates were elevated when Linepithema confronted an ant species that elicited use of chemicals, but not when it confronted an ant species that primarily elicited physical aggression. These results indicate that phorid parasitoids of Linepithema use the ant's chemicals as host location cues. Because Linepithema is known to abandon food resources in the presence of its phorid parasitoids, its use of chemicals during interspecific encounters may diminish its competitive success when phorids are nearby. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Habitat complexity modifies ant–parasitoid interactions: implications for community dynamics and the role of disturbance

Species must balance effective competition with avoidance of mortality imposed by predators or parasites to coexist within a local ecological community. Attributes of the habitat in which species interact, such as structural complexity, have the potential to affect how species balance competition and mortality by providing refuge from predators or parasites. Disturbance events such as fire can drastically alter habitat complexity and may be important modifiers of species interactions in communities. This study investigates whether the presence of habitat complexity in the form of leaf litter can alter interactions between the behaviorally dominant host ants Pheidole diversipilosa and Pheidole bicarinata, their respective specialist dipteran parasitoids (Phoridae: Apocephalus sp. 8 and Apocephalus sp. 25) and a single species of ant competitor (Dorymyrmex insanus). We used a factorial design to manipulate competition (presence/absence of competitors), mortality risk (presence/absence of parasitoids) and habitat complexity (presence/absence of leaf litter). Parasitoid presence reduced soldier caste foraging, but refuge from habitat complexity allowed increased soldier foraging in comparison to treatments in which no refuge was available. Variation in soldier foraging behavior correlated strongly with foraging success, a proxy for colony fitness. Habitat complexity allowed both host species to balance competitive success with mortality avoidance. The effect of fire on habitat complexity was also studied, and demonstrated that the immediate negative impact of fire on habitat complexity can persist for multiple years. Our findings indicate that habitat complexity can increase dominant host competitive success even in the presence of parasitoids, which may have consequences for coexistence of subordinate competitors and community diversity in general.     

Cascading trait‐mediated interactions induced by ant pheromones

Trait‐mediated indirect interactions (TMII) can be as important as density‐mediated indirect interactions. Here, we provide evidence for a novel trait‐mediated cascade (where one TMII affects another TMII) and demonstrate that the mechanism consists of a predator eavesdropping on chemical signaling. Ants protect scale insects from predation by adult coccinellid beetles – the first TMII. However, parasitic phorid flies reduce ant foraging activity by 50% – the second TMII, providing a window of opportunity for female beetles to oviposit in high‐quality microsites. Beetle larvae are protected from ant predation and benefit from living in patches with high scale densities. We demonstrate that female beetles can detect pheromones released by the ant when attacked by phorids, and that only females, and especially gravid females, are attracted to the ant pheromone. As ants reduce their movement when under attack by phorids, we conclude that phorids facilitate beetle oviposition, thus producing the TMII cascade.     

Cascading indirect effects in a coffee agroecosystem: effects of parasitic phorid flies on ants and the coffee berry borer in a high-shade and low-shade habitat

Nonconsumptive effects (NCE) of parasites on hosts vary with habitat complexity thereby modifying trait-mediated effects on lower trophic levels. In coffee agroecosystems, Pseudacteon sp. phorid fly parasites negatively affect Azteca instabilis F. Smith ants via NCE thereby indirectly benefiting prey. It is unknown how differences in habitat complexity influence Azteca-phorid interactions or how phorids affect the coffee berry borer (Hypothenemus hampei Ferrari), an important pest of coffee (Coffea arabica L). We tested the following hypotheses in field and lab experiments to find the impact of NCE of phorids on A. instabilis and trait-mediated indirect effects of phorids on the coffee berry borer: (1) Phorid effects on A. instabilis differ between complex and simple shade habitats and (2) Phorids, by modifying A. instabilis behavior, indirectly affect coffee berry borer abilities to invade coffee berries. Phorids had greater impacts on A. instabilis activity in low-shade farms, but differences in phorid impacts were not mediated by phorid density or light availability. In the lab, phorids had strong cascading effects on abilities of A. instabilis to deter coffee berry borers. Without phorids, A. instabilis limited coffee berry borer attacks, whereas when the coffee berry borer was alone or with A. instabilis and phorids, more coffee fruits were attacked by coffee berry borer. These results indicate that A. instabilis has stronger biological control potential in high-shade farms, but the exact mechanism deserves further attention.     

Behavioural and olfactory variations in the leek moth, Acrolepiopsis assectella, after several generations of rearing under diverse conditions

Females of the parasitic phorid Neodohrniphora sp. were collected in the field and released singly inside an observation chamber placed between a laboratory colony of Atta sexdens (L.) and its foraging arena. The number and speed of loaded and unloaded ants returning to the nest, the weight of foragers and their loads, the number of leaf fragments abandoned by ants, and the number of small workers 'hitchhiking' on leaf fragments were measured before phorids were released, while they were in the observation chamber, and after they were removed. Relatively few ants were attacked by Neodohrniphora sp., but the presence of flies prompted outbound ants to return to the nest and caused a significant reduction on the number and mass of foragers. Additionally, the weight of leaf fragments transported by ants was reduced and the number of abandoned fragments increased in response to Neodohrniphora sp. Presence of the parasitoid caused no significant changes in the number of hitchhiking ants. The regular ants' traffic was resumed after phorids were removed, but foraging activity remained below normal for up to three hours. In the field A. sexdens forages mostly at night, but colonies undergo periods of diurnal foraging during which ants are subject to parasitism from several species of phorid flies. Considering that daytime foraging may be necessary for nutritional or metabolical needs, phorids may have a significant impact on their hosts by altering their foraging behavior regardless of the numerical values of parasitism.     

Parasite Lost: Chemical and Visual Cues Used by <Emphasis Type="BoldItalic">Pseudacteon</Emphasis> in Search of <Emphasis Type="BoldItalic">Azteca instabilis</Emphasis>

An undescribed species of phorid fly (genus: Pseudacteon) parasitizes the ant Azteca instabilis F Smith, by first locating these ants through the use of both chemical and visual cues. Experiments were performed in Chiapas, Mexico to examine a) the anatomical source of phorid attractants, b) the specific chemicals produced that attract phorids, and c) the nature of the visual cues used by phorids to locate the ants. We determined that phorid-attracting chemicals were present within the dorsal section of the abdomen, the location of the pygidial gland. Further experiments indicate that a pygidial gland compound, 1-acetyl-2-methylcyclopentane, is at least partially responsible for attracting phorid flies to their host. Finally, although visual cues such as movement were important for host location, size and color of objects did not influence the frequency with which phorids attacked moving targets.     

Spatial and temporal variation in host–parasitoid interactions: leafcutter ant hosts and their phorid parasitoids

1. Parasitoid–host interactions are important components of ecological communities. Although parasitoid–host interactions are strongly shaped by evolutionary history, the abundance of both the parasitoid and the host may have a role in determining the nature of the interaction once phylogenetic relationships are considered. 2. Leafcutter ants are hosts of phorid parasitoids and represent a well‐defined and specialised module within a larger network of ant–symbiont interactions. A low specificity host taxa and a positive association between host abundance and parasitoid interaction frequency were expected due to the close phylogenetic relatedness of the hosts. 3. The interactions among all species of leafcutter ants and their parasitoids were quantified in two localities with different species richness. This study also characterised the spatial‐temporal variability of these interactions, determined the patterns of parasitoid specificity and host selection, and tested for an association between host abundance and parasitoid interaction frequency. 4. Contrary to expectation, most parasitoid species were highly specialised and interaction frequency for parasitoid species was not related to host abundance. All host ant species were attacked by more than one phorid species. Some phorid species used more than one host species and showed preference for the same species over space and time, suggesting that there are physiological and/or behavioural restrictions on host use. 5. These results show that there is a tendency for specialisation even when hosts are highly similar in their ecology. From a biological control perspective, these parasitoids may be effective candidates, due to the high specificity of some species and little host‐use variation through time.     

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 hosts 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.     

Introduction of the fire ant decapitating fly <Emphasis Type="Italic">Pseudacteon obtusus</Emphasis> in the United States: factors influencing establishment in Texas

The introduction and establishment of Pseudacteon obtusus Borgmeier (Diptera: Phoridae) into the United States is an important milestone in the effort to introduce a suite of parasitoids and pathogens as prospective biocontrol agents of the red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae). P. obtusus is the fourth species of phorid fly to be established in the US and is now present in at least 11 sites in Texas. This species has a greater propensity for attacking foraging worker ants, and to a lesser degree it will attend mound disturbance events. The effectiveness of alternate field release strategies was evaluated across 28 sites in Texas, with establishment success 35 times more likely when no other phorid species were present at the outset of the releases. This result implies that competition between phorid species may interfere with establishment. Therefore release strategies should be directed to locations lacking other naturalized species or to times when abundances of other species are low.     

Host Location Behavior in a Parasitoid of Imported Fire Ants

Female parasitoids use a hierarchy of cues to locate suitable hosts. We conducted a series of field observations and experiments to examine host location behavior in Pseudacteon tricuspis Borgmeier, a phorid parasitoid of Solenopsis invicta Buren worker ants. The parasitoids were frequently attracted to host workers at disturbed colonies, but were almost never attracted to host workers foraging at baits. When conspecific nonnestmate workers were introduced to baits, resulting in aggressive interactions, parasitoids appeared at the majority of baits. Moreover, larger numbers of parasitoids appeared at baits to which greater numbers of nonnestmate workers had been added. Addition of nonnestmate workers to disturbed colonies resulted in increased numbers of parasitoids attracted. Pseudacteon tricuspis did not display a pattern of uniform distribution at disturbed colonies but often was very abundant at some colony locations while absent or rare at nearby colony locations. Solenopsis invicta workers release alarm pheromones in aggressive interactions with nonnestmates, and this substance is likely an important chemical cue that attracts P. tricuspis flies to host workers from a distance.     

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.     

Colony-level impacts of parasitoid flies on fire ants

The red imported fire ant is becoming a global ecological problem, having invaded the United States, Puerto Rico, New Zealand and, most recently, Australia. In its established areas, this pest is devastating natural biodiversity. Early attempts to halt fire ant expansion with pesticides actually enhanced its spread. Phorid fly parasitoids from South America have now been introduced into the United States as potential biological control agents of the red imported fire ant, but the impact of these flies on fire ant populations is currently unknown. In the laboratory, we show that an average phorid density of as little as one attacking fly per 200 foraging ants decreased colony protein consumption nearly twofold and significantly reduced numbers of large-sized workers 50 days later. The high impact of a single phorid occurred mainly because ants decreased foraging rates in the presence of the flies. Our experiments, the first (to our knowledge) to link indirect and direct effects of phorids on fire ants, demonstrate that colonies can be stressed with surprisingly low parasitoid densities. We interpret our findings with regard to the more complex fire ant-phorid interactions in the field.     

No evidence of strong host resource segregation by phorid parasitoids of leaf-cutting ants

Resource segregation by species is a cornerstone ecological concept that may result from several processes such as interspecific competition, and can help structuring communities, in particular parasitoid communities. Phorid parasitoid flies that use ants as hosts usually employ one host per individual parasitoid, and thus the pressure for segregating the host resource should be high. At a particular community, these parasitoids might segregate resources by temporal differences in activity patterns, using different host species or nests from those available. Even if parasitoid species coexist on the same nest, they can take advantage of worker polymorphism and task division, searching for ants performing different tasks at different microsites of the same nest. Here we evaluated the segregation of parasitoid species in these hypothesized axes using leaf-cutting ant phorid parasitoids as a model system. We analyzed temporal data collected at two localities with contrasting host species richness; and compared parasitoid co-occurrence at the different niche axis. For most of the hypothesized niche axes tested we found either no departures from random expectations or significantly more niche overlap than expected by chance, ruling out the existence of biologically relevant host resource segregation in this system. However, there was evidence of segregation for some species, since one parasitoid species was only found in winter and another species showed a negative correlation of its abundance over nests with other two species. Furthermore, we found that several species were flexible in host use; Atta phorids varied in average host sizes preferred, whereas Acromyrmex phorids that were generalists were able to use different host species or microsites for host location. From an applied perspective, these results are encouraging when selecting species for the control of leaf-cutting ants because parasitoids coexistence seems to be unaffected by their overlap in niche dimensions.