Mechanisms of Pseudacteon Parasitoid (Diptera: Phoridae) Effects on Exploitative and Interference Competition in Host Solenopsis Ants (Hymenoptera: Formicidae)

Abstract

I conducted a series of laboratory experiments to quantify the effects and elucidate the mechanisms by which Pseudacteon tricuspis Borgmeier phorid flies affect the exploitative and interference components of interspecific competition in host Solenopsis invicta Buren ants. In manipulative experiments, workers retrieved 50% less food in a foraging tray with phorids present, compared with an equidistant foraging tray with the same food resource but without phorids. The average number of workers actively foraging in the tray with phorids was significantly less than in the tray without phorids. There were no significant differences in either average worker size or average number of workers present at the food resource at the end of the trials in trays with phorids versus trays without phorids. In a control set of trials in which no phorids were added to either foraging tray, the size of foraging workers averaged over both foraging trays was significantly larger than in either the phorid or no-phorid tray of the manipulative experiments. This suggests that colonies can communicate the generalized presence of phorids in an area, which leads to a decrease in foraging by major workers. S. invicta workers retrieved an intermediate amount of food in the foraging trays of the control experiment compared with the phorid and no-phorid trays of the manipulative experiment. Moreover, the overall amount of food obtained in both foraging trays was similar for the manipulative and control experiments, suggesting that the S. invicta colonies were able to compensate for harassment by phorids by altering their foraging strategy, which resulted in no net loss of food retrieved. When S. invicta was paired with S. geminata (F.) in interference competition experiments, phorid flies had no effect on the outcome of interspecific interactions. Phorids did not appear to be attracted to host workers once they were engaged in combat with enemy workers, and the spatial distribution of fighting was significantly different than the spatial distribution of parasitization attempts.

Interspecific competition has been demonstrated to be an important factor limiting many ant populations (reviewed in Hölldobler and Wilson 1990). Predators, pathogens, and parasites may also affect the population dynamics of their ant prey or hosts (Hölldobler 1970, Edwards et al. 1974, Waller and Moser 1990, Briano et al. 1995, Gotelli 1996), particularly when such organisms also affect the competitive ability of ants (Feener 1981, MacKay 1982). The Phoridae is a diverse group of minute flies, many species of which are parasitoids of ants (Disney 1990). Phorid parasitoids affect their host ants directly, by developing inside infected workers, killing them in the process (Disney 1994, Porter et al. 1995a). Phorid parasitoids may also indirectly affect their hosts, by altering the behavior of workers and changing the outcome of interspecific competition (first described by Feener [1981]). The magnitude of such indirect effects may be greater than the direct effect of mortality for many phorid/ant species pairs (Feener 1988, Morrison 1999).

Both the exploitative and interference components of interspecific competition among ants may be affected by phorid flies, and the exact mechanisms by which phorids indirectly affect competitive interactions are potentially diverse. Phorids may influence worker behavior, caste size ratios, and number of worker ants recruiting to a food resource or enemy ant species (Feener 1981, 1988,; Feener and Moss 1990; Feener and Brown 1992; Orr 1992; Orr et al. 1995; Porter et al. 1995b; Orr and Seike 1998; Folgarait and Gilbert 1999, Morrison 1999). The end result of such behavioral modifications is that the host ant species is placed at a competitive disadvantage relative to other ants in the community.

Because of their potential to modify competitive interactions, phorid flies of the genus Pseudacteon are being evaluated as biocontrol agents of imported fire ants (Solenopsis invicta Buren and S. richteri Forel) in the United States. Field observations in South America have revealed that the presence of Pseudacteon species decreased foraging of Solenopsis saevissima complex workers and at times contributed to species turnover at baits (Orr et al. 1995, 1997,; Porter et al. 1995b; Folgarait and Gilbert 1999).

Although these field studies measured an overall effect of Pseudacteon phorids on S. saevissima complex species, a drawback of such studies is that it is not always possible to separate the two components of interspecific competition, and the mechanisms underlying the measured effects are not always apparent.

I conducted a series of laboratory experiments in which I could control variables such as state of hunger, colony size, colony caste ratio, and colony location of ants, as well as number, sex, age, and reproductive status of phorids. I quantified the effects of one Pseudacteon species, P. tricuspis Borgmeier, on the pure exploitative (i.e., competition for food in the absence of any other species) and pure interference (i.e., direct, aggressive interactions in the absence of food resources) components of interspecific competition in North American populations of S. invicta.

The following questions were addressed: (1) What is the magnitude of the effect of P. tricuspis on resource retrieval (i.e., exploitative competition component) in S. invicta? (2) What is the magnitude of the effect of P. tricuspis on aggressive interactions (i.e., interference competition component) between S. invicta and its congener S. geminata (F.)? (3) What are the important mechanism(s) underlying these effects? (4) How much of an overall limiting factor are Pseudacteon phorids to Solenopsis ant populations?

Materials and Methods

Solenopsis invicta colonies were collected from Travis County and S. geminata colonies were collected from Hays County, TX. All colonies were of the polygyne, or multiple queen, form. P. tricuspis were reared at the University of Texas at Austin’s Brackenridge Field Laboratory (BFL) from stock originally collected in Sao Paulo State, Brazil. This is the northern form of P. tricuspis as described by Borgmeier and Prado (1975). Reference specimens of S. invicta,S. geminata, and P. tricuspis have been placed in the Natural History Museum of Los Angeles County, CA; the Museu de História Natural, UNICAMP, Sao Paulo, Brazil; and at BFL.

All experiments were conducted between January and May 1999 at BFL. I set up experimental ant colonies consisting of a measured quantity of workers, brood, and a single queen. An electronic balance was used to weigh all workers and brood. The experimental colonies were placed in open trays (25 by 18 by 7 cm), the sides of which were coated with Fluon (polytetrafluoroethylene; ICI Fluoropolymers, Exton, PA) to prevent escapes. A petri dish (90 mm diameter, 15 mm high) containing damp plaster to maintain humidity was provided as a nesting chamber.

The mother colonies from which the experimental colonies were derived were kept in the laboratory at ≈28°C for at least 2 wk before experimental colony formation, fed a standardized diet of water and sugar water ad libitum (in test-tubes plugged with cotton), and provided fresh frozen crickets every day. After initiation, the experimental colonies were maintained at ≈28°C, provided with water and sugar water ad libitum, and fed two fresh frozen crickets every other day for 1 wk before the beginning of the experiments. All trays described below except the colony trays contained a layer of plaster on the bottom, which was moistened before the experiments to maintain a relative humidity of ≈75%. All experiments were conducted at ≈28°C.

Resource Competition

I set up experimental S. invicta colonies containing 4 g of workers and 2 g of brood. S. invicta workers were sieved through a screen with 0.85-mm openings, and each experimental colony received 2 g of “major” workers >0.85 mm and 2 g of “minor” workers <0.85 mm. This procedure resulted in a worker caste size ratio typical of monogyne colonies (see Discussion). Each gram of majors consisted of ≈370 workers, and each gram of minors consisted of ≈1,600 workers.

Experimental colonies were starved for 48 h before the beginning of the trials to produce a uniform state of hunger. Each tray containing an experimental colony was connected via a 12-cm length of opaque Tygon tubing (1 cm i.d.) to two adjacent foraging trays of the same dimensions on opposite sides of the colony tray, providing a choice of foraging in two equidistant trays containing the same food resource (Fig. 1).The trays were connected for 1 h before introduction of the food resource during which time ants were allowed to explore both foraging trays. Two freeze-killed crickets were then placed in the center of each foraging tray, on white plastic cards (5 by 5 cm). The crickets were stripped of the legs and antennae, which could have been dismembered and carried away, and were pinned down to prevent ants from moving them. Glass tops were placed over both foraging trays.

Fig. 1.

Design of the exploitative (top) and interference (bottom) competition experiments

Resource retrieval rates were measured by quantifying precisely the amount of food retrieved in 60 min. Crickets were weighed with an electronic balance immediately before and after exposure to ants. In each trial, a control set of crickets was left out for 60 min to measure weight loss by desiccation. The average weight loss of the control group was then subtracted from the weight loss of the experimental group. I also measured three potential mechanisms underlying this effect: (1) worker activity, (2) number of workers recruited, and (3) worker size. To quantify worker activity, the number of workers crossing the edge (nearest to the colony tray) of the 5 by 5-cm card were counted for 2 min at 10-min intervals. To quantify number of workers recruited to the bait, all workers on the 5 by 5-cm cards at the end of the trials were collected and counted. To quantify worker size, I measured head widths in a random subsample of 25 workers taken from all workers collected from each card at the end of the trials.

The average number of actively foraging workers throughout the course of the trials was likely to be positively correlated with number of workers present at the baits at the end of the trials. This potentially strong correlation does not preclude testing for each effect individually, however, because Pseudacteon phorids may cause Solenopsis workers to remain immobile for many minutes at a time (Porter et al. 1995b, Orr et al. 1997, Morrison 1999). This effect on activity may be manifested independently of number of workers present.

In the first, or manipulative, set of experimental trials, five mated, 1-d-old P. tricuspis females were added to one of the foraging trays 10 min after the introduction of the food resource. Not all phorids actively attacked ants, and additional flies were added over time if necessary. I attempted to have at least two phorids actively attacking workers at all times. No phorids were added to the opposite foraging tray. The trials lasted for 60 min after introduction of flies. The same data were collected from the foraging tray with phorids and the foraging tray without phorids in each trial, and were compared with paired t-tests. Because multiple comparisons were made within the same experiment, the sequential Bonferroni method was used to control the group-wide type I error rate (Rice 1989).

In a second, or control, set of trials, the same procedure was followed, except that no phorids were added to either foraging tray. Paired t-tests revealed no significant differences (P > 0.05) between the two foraging trays for any of the four measured variables. Thus, the values for each variable were averaged between the two foraging trays of the control experiment, and compared with the values for the phorid and no-phorid treatments in the manipulative experiment, by a one-way analysis of variance (ANOVA). The Bonferroni method of multiple comparisons with a family confidence level of 90% was used to compare the average values of the control experiment to both the phorid and no-phorid treatments of the manipulative experiment.

Although I attempted to have a constant number of actively attacking phorids, there was an unavoidable amount of variation among the trials in the number of active flies. In foraging trays with phorids present (the manipulative experiment), the number of actively attacking phorids was counted for 1 min immediately before and 1 min immediately after counting recruiting ants, as described above. I averaged the number of actively attacking flies in each trial and, in simple linear regressions, regressed each of the four variables described above on average number of attacking flies, in four separate regressions, to see if more active flies resulted in a significantly greater effect.

Interference Competition

I tested the effect of phorids on short-term interference competition by measuring the spatial dimensions of interspecific combat between S. invicta and S. geminata. Experimental colonies of S. invicta were set up as described previously. Workers of S. geminata are on average larger than workers of S. invicta (Trager 1991), and previous work has revealed that S. invicta wins interspecific contests in the moderate to long-term when S. invicta and S. geminata colonies are equivalent by biomass, but this outcome is reversed when the colonies are equivalent by worker number (Morrison 2000). This difference was not significant in the short term, however, and the outcome of short-term interspecific interactions was more equal when colonies were equivalent by worker number (Morrison 2000). Thus, I set up S. geminata colonies that were equivalent in worker number to the S. invicta colonies. I sieved S. geminata workers through the 0.85-mm screen, and found that each gram of “majors” consisted of ≈190 workers, and each gram of “minors” consisted of ≈1,380 workers. I then set up colonies consisting of 3.9 g of S. geminata majors, and 2.3 g of S. geminata minors. This procedure resulted in ≈740 majors and ≈3,180 minors per colony tray, for both S. invicta and S. geminata.

A S. geminata colony and a S. invicta colony were each connected to opposite ends of a larger (37 by 24 by 7 cm) tray via 12-cm lengths of opaque Tygon tubing (1 cm i.d.). This tray contained eight opaque walls that turned the central tray into a maze (Fig. 1). The walls and sides of the tray were white, and coated with Fluon to prevent the ants from escaping or scaling the walls. The bottom of the tray was covered with white plaster. A grid containing 72 squares, in nine rows and eight columns, was marked off in the maze tray. A gate coated with Fluon was placed in the center of the tray. The S. geminata and S. invicta colonies were equidistant from the gate, with 36 squares between the gate and each colony tray.

Workers from each colony were allowed to explore the maze tray for 15 min. In this time, workers of both species traveled throughout the maze to the central gate. A glass cover was placed on top of the maze tray and five mated, 1-d-old, female P. tricuspis phorids were introduced. I recorded the precise locations of fighting between the Solenopsis species within the grid, as well as parasitization attempts by P. tricuspis, at 5-min intervals for 60 min. Usually after 60 min, fighting had spread throughout a large portion of the maze tray, and parasitization attempts by P. tricuspis had decreased (see Results).

In most of the trials, two or more phorids began attacking S. invicta immediately. Sometimes the phorids added at the beginning of the trial did not attack readily, and some phorids were eventually caught by ants in some of the trials. When fewer than two phorids were actively attacking within the 5-min observation interval, two additional phorids were added.

A total of 10 manipulative trials were conducted in this manner, using different S. invicta colonies, S. geminata colonies, and P. tricuspis females in each trial. A series of 10 control trials were also conducted, which were the same in every respect except that phorids were not added. A two-way ANOVA was used to test for an effect of Solenopsis species and phorid presence on the outcome of the interactions.

Results

Exploitative Competition

In all trials, S. invicta colonies foraged in both foraging trays. In the manipulative experiment only about half as much of the resource was retrieved in trays with phorids as in trays without phorids (Table 1).In the trays with phorids, fewer workers actively foraged, fewer workers were present at the bait at the end of the trials, and the average size of the workers present at the bait was smaller, compared with the foraging trays without phorids (Table 1). The effects on resource retrieval and average number of workers actively foraging were both significant at P < 0.05 (paired t-tests).

Table 1.

Effects of phorids on resource retrieval, and the underlying mechanisms, in S. invicta

In the control experiment, in which phorids were absent from both foraging trays, there were no differences between the two trays in any of the measured variables (all P > 0.05). Thus, the values for each variable were averaged between foraging trays, and compared with the values for the phorid and no-phorid treatments in the manipulative experiment. For the first three variables, the average values of the control trials were intermediate between the phorid and no-phorid treatments of the manipulative trials (Table 1). Average worker size at the end of the trials, however, was larger for the control than either treatment of the manipulative trials.

There were no significant differences between the controls and the phorid treatment, or the controls and the no-phorid treatment, for resource retrieval, worker activity, or number of foragers, by the Bonferroni method with a 90% confidence level. Average worker size in the control trials, however, was significantly larger than average worker size in both the phorid and no-phorid treatments of the manipulative trials, at the 90% confidence level.

On average, the colonies retrieved a total of 0.083 g of food in the manipulative experiment (summing the phorid and no-phorid treatments). In the control experiment, the colonies retrieved 0.086 g of food (doubling the average of the two control trays). Thus, it appears that the colonies were able to compensate for decreased food retrieval caused by phorid harassment by increasing food consumption when food was available elsewhere.

Simple linear regressions of number of active flies versus the four measured variables were all nonsignificant (P > 0.05). Thus, the magnitude of the effects observed were independent of the number of flies actively attacking worker ants. The average number of actively attacking flies was fairly low, however, and fell within a narrow range (0.25–2.75).

Interference Competition

In the interference competition trials, fierce interspecific fighting occurred immediately after the gates were opened and quickly spread through the maze toward each colony tray (Fig. 1). Fighting was consistently observed farther within the S. invicta than the S. geminata territory. The location of the interspecific combat over time was very similar for both the manipulative and control trials (Fig. 2).A two-way ANOVA revealed a significant effect of species (F = 9.50, df = 1, P = 0.0039), but the presence of phorids was not significant (F = 0.96, df = 1, P = 0.33). The interaction was also not significant (F = 0.05, df = 1, P = 0.83).

Fig. 2.

Number of squares fighting extended into the territories of each species in the interference competition trials

Phorids qualitatively seemed more excited at the beginning of the interference competition trials than in the exploitative competition trials, possibly because of alarm pheromones released in the context of interspecific aggression. Workers of the two ant species began grappling with each other quickly after the gate was opened, clamping on to each other with their mandibles. Most phorids did not seem interested in attacking host workers attached to enemy workers. In fact, most of the phorids spent most of their time attempting to parasitize host workers recruiting to the battle from the colony tray. Thus, although the majority of fighting occurred in the center of the maze, the distribution of parasitization attempts was skewed toward the S. invicta colony tray (Fig. 3).This variation in the distribution of attacks versus the distribution of fighting was highly significant (χ² = 26.16, df = 8, P = 0.001, chi-square test of homogeneity).

Fig. 3.

Distribution of fighting between S. geminata and S. invicta and distribution of parasitization attempts by P. tricuspis on S. invicta The S. geminata colony was nearest to row A, whereas the S. invicta colony was nearest to row I

Phorids often hovered around the entrance tube to the colony, attempting to parasitize workers entering the maze. In some experimental trials, S. invicta recruitment to the fighting was very low, and could have been a result of phorid presence, although this was not quantified.

Discussion

Overview of Phorid/Ant Interactions

A number of field studies have documented the effects of parasitic phorids on their host worker ants. Apocephalus phorids have been documented to affect both foraging and defense behavior of host Pheidole ants (Feener 1981, 1988,), as well as the frequency of hitchhiking minim workers in the leaf-cutting Atta columbica (Feener and Moss 1990). Neodohrniphora phorids have been shown to influence caste ratios and numbers of foraging Atta cephalotes (Orr 1992, Feener and Brown 1993). Pseudacteon phorids (P. pusillum and an undescribed species) have been documented to decrease foraging in the Argentine ant, L. humile (Orr and Seike 1998).

Many recent studies of ant/phorid interactions have focused on Solenopsis fire ants and their associated Pseudacteon parasitoids. In South America, the presence of Pseudacteon flies that parasitize S. saevissima complex ants has been shown to decrease worker foraging, and contribute to food resources being lost to competing ant species (Orr et al. 1995, 1997,; Porter et al. 1995b; Folgarait and Gilbert 1999). In Central and North America, Pseudacteon flies that parasitize S. geminata complex ants have also been documented to decrease food retrieval (Feener and Brown 1992, Morrison 1999). An effect of Pseudacteon phorids on interference competition involving S. geminata has not been found, however (Morrison 1999).

All of the above studies have been conducted in the field, with phorid and ant species native to the respective areas. Separating the exploitative and interference components of interspecific competition in the field is often difficult, however, as is precisely evaluating the magnitude of the effects. It may not be possible, for example, to manipulate the presence or abundance of phorids, or control for differences in the size and location of host ant colonies, or presence of enemy ants. Thus, the experiments described in this article represent the first detailed laboratory study of the effects of phorids on the pure exploitative and interference components of interspecific competition, and the underlying mechanisms.

Exploitative Competition

When S. invicta workers were given a choice to forage in trays with or without P. tricuspis flies, resource retrieval was 50% less in the tray with phorids. Significantly fewer workers actively foraged in the tray with phorids. Fewer, and smaller, workers were present at the end of the trials in the tray with phorids, but these differences were not significant. In control trials, when no phorids were present in either tray, the amount of resource retrieved was intermediate to that of the phorid versus no-phorid treatments, indicating that the colonies were obtaining more food from the no-phorid tray to compensate for decreased food retrieval in the phorid tray. This is the first evidence that host ants may be able to compensate for diminished food retrieval caused by phorid harassment.

In nature, this mechanism may be manifested by a spatial shift to increased underground foraging during the day when phorids are active, or a temporal shift to increased aboveground foraging at night, when phorids are not active. A study of the diet of S. invicta and S. geminata revealed that a large proportion of their diet may be obtained from subterranean sources (Tennant and Porter 1991), and both species commonly forage diurnally as well as nocturnally (Claborn and Phillips 1986, Morrison 1999).

Significantly larger workers foraged in the control trials than in either treatment of the experimental trials. Solenopsis workers appear to be able to communicate the presence of phorids to nestmates by alarm pheromones (C. G. Dall’Aglio-Holvorcem, unpublished data). Thus, the colonies may have been aware of the general presence of phorids in the area, and larger workers did not forage in the no-phorid trays because of the ultimate, rather than proximate, risk of parasitization.

In the foraging trays of the experimental set-up, there was no significant relationship between variation in the number of actively attacking phorids and variation in any of the measured variables. Although the presence of a single female is often sufficient to disrupt worker foraging at a localized food resource (Feener and Brown 1992, Orr et al. 1995), higher phorid densities have been associated with lower resource retrieval rates in the field (Morrison 1999). Variation in attack frequency among individual phorids may obscure this relationship, however. Orr et al. (1997) reported that the degree of response in workers was more closely related to number of attacks than amount of time that a phorid was present. Likewise, in the context of the laboratory experiments of this study, the degree of response of S. invicta may be more closely associated to the number of attacks than the number of phorids attacking. It is also possible that an effect of phorid number may emerge over a wider range of fly densities.

Although only females were used in the experimental trials, P. tricuspis males may have similar effects on worker behavior. P. tricuspis males are attracted to worker ants, apparently to find mates, and appear to feign attacks on workers (unpublished data), possibly to increase worker excitement and release of pheromones which may attract P. tricuspis females. The presence of both male and female Pseudacteon phorids has been documented to disrupt foraging of Solenopsis workers in the field (Feener and Brown 1992, Porter et al. 1995b).

Interference Competition

The presence of P. tricuspis had no effect on the outcome of short-term interspecific competition, based on the spatial location of fighting. Interspecific interactions between S. invicta and S. geminata usually involved workers of each species clasping each other with their mandibles and grappling for extended periods (several minutes to the end of the trials). At times, three or more workers were attached to each other. (Detailed descriptions of the interspecific interactions of S. geminata and S. invicta are given in Bhatkar [1988] and Morrison [2000].) The phorids did not appear interested in these clusters of workers. Pseudacteon phorids exhibit size-specific preferences for host ants (Morrison et al. 1997, Morrison and Gilbert 1998), and two or more workers grappling together probably do not fit their search image for hosts.

There was a significant difference between the spatial distribution of fighting and the spatial distribution of parasitization attempts. Most parasitism attempts occurred between the active fighting and the tube leading to the S. invicta colony tray, where individual S. invicta workers could be found. Thus, the effect of Pseudacteon phorids on the interference component of interspecific competition in the field is likely to depend upon the spatial location of interspecific interactions relative to the host Solenopsis colony. S. geminata and S. invicta use extensive underground tunnel systems (Markin et al. 1975), however, and are able to reach areas distant from the colony with little above-ground exposure. Thus, the effect of phorids on interference competition is likely to be relatively small in most cases. In a field study of interference competition between S. geminata and S. invicta at rich food resources, S. geminata workers were observed to travel only short distances above ground from underground tunnel entrances to the contested resources (Morrison 1999).

The identity of competing ant species may also be important in determining the effect of phorids on interference competition. If interspecific interactions with other ant species involve less grappling of workers attached to each other, the effect of phorids may be greater. For example, Monomorium is a genus found in sympatry with S. invicta that relies heavily on chemical defense, rather than physical grappling (Baroni-Urbani and Kannowski 1974). Such an interaction may result in more parasitization pressure on S. invicta, although the dispersal of airborne venom could negatively affect Pseudacteon parasitization.

The effects of phorids on interference interactions were evaluated over a relatively short period in this laboratory study. A previous study indicated that the ultimate winner (based on reduction of colony size) of interference interactions could usually, but not always, be predicted based on the short-term distribution of fighting (Morrison 1999). In the previous study, S. geminata and S. invicta workers were observed to fight for several days before such territorial disputes were resolved, and it was not practical to run the experiments of the current study for such a long period. It is possible that phorids may have a greater effect over a longer period in nature, but any potential effects will be limited by the spatio-temporal dimensions of the interference interactions. In nature many interactions may not be accessible to phorids at all, such as fighting occurring underground or at night.

Implications for Biocontrol

In the first test of the effects of South American Pseudacteon phorids on resource retrieval by North American S. invicta populations, a single P. tricuspis female decreased food retrieval by 15% in laboratory trials, although the mechanisms underlying the decrease in food retrieval were not identified (Morrison 1999). It was qualitatively observed that few majors entered the foraging trays, however, and minors foraged largely unmolested. Random samples of polygyne S. invicta were used, in which the average worker size was only 0.62 mm. P. tricuspis, however, prefers workers with a head width of ≈0.93 mm (Morrison et al. 1997, Morrison and Gilbert 1998). The experiment in Morrison (1999) was designed differently than the current study, and did not allow a simultaneous choice of phorid or no-phorid food sources. Each colony was instead tested sequentially with phorid and no-phorid treatments.

In pilot trials of the experimental set-up of the current study, P. tricuspis females rarely attacked S. invicta workers in foraging trays when offered a random subsample of polygyne S. invicta workers. The most likely reason was that the foraging workers were too small. Only ≈12% of the workers in the typical polygyne S. invicta colony in Travis County, TX, have head widths ≥0.93 mm (unpublished data). By sieving workers and adding a relatively larger proportion of majors, I obtained worker size distributions more typical of the monogyne form. In a previous study, the average head width of monogyne S. invicta workers was 0.86 mm (Morrison and Gilbert 1998). The screen used to separate S. invicta majors from minors had 0.85-mm openings. Natural monogyne colonies were not used because they are rare in central Texas.

Pseudacteon phorids are already being released in the southeastern United States as potential biocontrol agents of S. invicta (Porter et al. 1999). The overall effect of these introductions will depend to an extent on the Pseudacteon species introduced and S. invicta social form in question. There are at least 18 Pseudacteon species that attack S. saevissima complex fire ants in South America (Porter 1998). Multiple Pseudacteon species often coexist on the same Pseudacteon host species (Orr et al. 1997). One way these species appear to coexist is by partitioning their polymorphic hosts by size, with larger phorid species parasitizing larger worker ants (Morrison et al. 1997, Morrison and Gilbert 1998). Moreover, host worker size appears to determine the sex of the phorid offspring (Morrison et al. 1999).

The mechanisms documented in this laboratory study indicate that P. tricuspis is likely to have a larger effect on monogyne, rather than polygyne, S. invicta colonies. A smaller species of Pseudacteon, such as P. obtusus (Morrison and Gilbert 1999) or P. curvatus (S. D. Porter, 2000), apparently would be more effective in controlling polygyne S. invicta populations, all else being equal.

The results of the laboratory experiments elucidate the mechanisms by which P. tricuspis decreases short-term resource retrieval in S. invicta. Whether this will translate into long-term food limitation for the colony is difficult to predict. S. invicta workers never abandoned any baits in the laboratory trials, and revealed an ability to compensate for phorid harassment by foraging on alternate resources. The first report of the effect of Pseudacteon phorids on Solenopsis fire ant foraging in South America found evidence that phorid presence resulted in S. invicta abandoning baits to competing ant species (Orr et al. 1995). Such a strong suppressive effect may occur primarily during initial recruitment to food resources, however, and subsequent studies have found that after recruitment is established, enough workers usually remain at the resource in the presence of phorids to successfully defend the resource from competing ants (Porter et al. 1995b, Orr et al. 1997).

In field experiments conducted in central Texas with S. geminata and associated Pseudacteon phorids, S. geminata workers were observed never (Morrison 1999) or only very rarely (Morrison et al. 2000) abandoning a food resource to competing ants, even under harassment by multiple Pseudacteon females. Some workers (primarily minors) remained at the food resource, guarding it and covering it with soil and bits of debris, while other workers tunneled under the food resource, decreasing exposure to phorids.

It is difficult to make a generalized prediction regarding the overall effect of Pseudacteon phorids on Solenopsis ants. All studies to date have focused on short-term, behavioral effects lasting at most several hours (Feener and Brown 1992; Orr et al. 1995, 1997,; Porter et al. 1995b; Folgarait and Gilbert 1999; Morrison 1999). Solenopsis workers exhibit a number of characteristics or frequently observed behaviors that appear to decrease the impact of Pseudacteon phorids, however, and may be to some degree adaptations to Pseudacteon parasitism pressure. These include underground foraging tunnels or covered walkways, covering food with dirt or debris, and defensive posturing (reviewed in Morrison 1999). Altering foraging strategies to avoid phorid flies, as revealed in this study, may also be frequently employed. Yet the presence of Pseudacteon-specific defensive behaviors is evidence that these parasitoids are capable of having population-level impacts on their Solenopsis hosts, or such behaviors would not have evolved. Long-term field studies are needed to assess the magnitude of the population-level effects of Pseudacteon phorids on Solenopsis fire ants.

Acknowledgments

R. Guerra and E. A. Kawazoe assisted with the laboratory experiments. T. Alexander, D. Broglie, A. Cottingham, P. Field, F. Kozuh, R. Guerra, C. Papp, and J. Warr reared the phorid cultures that made this project possible. L. E. Gilbert was instrumental in motivating this study and providing the necessary resources. This research was funded by the State of Texas Fire Ant Research and Management Committee.