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

Home , Phoridae, Pseudacteon, Pseudacteon tricuspis

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

LLOYD W. MORRISON1

Section of Integrated Biology and Brackenridge Field Laboratory, University of Texas, Austin, TX 78712

Ann. Entomol. Soc. Am. 93(4): 841Ð849 (2000) ABSTRACT I conducted a series of laboratory experiments to quantify the effects and elucidate the mechanisms by which Pseudacteon tricuspis Borgmeier phorid ßies affect the exploitative and interference components of interspeciÞc 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 signiÞcantly less than in the tray without phorids. There were no signiÞcant 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 signiÞcantly 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 ßies had no effect on the outcome of interspeciÞc 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 Þghting was signiÞcantly different than the spatial distribution of parasitization attempts.

KEY WORDS Pseudacteon tricuspis, Solenopsis geminata, Solenopsis invicta, exploitative competition, interference competition, parasitism

INTERSPECIFIC COMPETITION HAS been demonstrated to phorid/ant species pairs (Feener 1988, Morrison be an important factor limiting many ant populations 1999). (reviewed in Ho¨lldobler and Wilson 1990). Predators, Both the exploitative and interference components pathogens, and parasites may also affect the popula- of interspeciÞc competition among ants may be af- tion dynamics of their ant prey or hosts (Ho¨lldobler fected by phorid ßies, and the exact mechanisms by 1970, Edwards et al. 1974, Waller and Moser 1990, which phorids indirectly affect competitive interac- Briano et al. 1995, Gotelli 1996), particularly when tions are potentially diverse. Phorids may inßuence such organisms also affect the competitive ability of worker behavior, caste size ratios, and number of ants (Feener 1981, MacKay 1982). The Phoridae is a worker ants recruiting to a food resource or enemy ant diverse group of minute ßies, many species of which species (Feener 1981, 1988; Feener and Moss 1990; are parasitoids of ants (Disney 1990). Phorid parasi- Feener and Brown 1992; Orr 1992; Orr et al. 1995; toids affect their host ants directly, by developing Porter et al. 1995b; Orr and Seike 1998; Folgarait and inside infected workers, killing them in the process Gilbert 1999, Morrison 1999). The end result of such (Disney 1994, Porter et al. 1995a). Phorid parasitoids behavioral modiÞcations is that the host ant species is may also indirectly affect their hosts, by altering the placed at a competitive disadvantage relative to other behavior of workers and changing the outcome of ants in the community. interspeciÞc competition (Þrst described by Feener Because of their potential to modify competitive [1981]). The magnitude of such indirect effects may interactions, phorid ßies of the genus Pseudacteon are be greater than the direct effect of mortality for many being evaluated as biocontrol agents of imported Þre ants (Solenopsis invicta Buren and S. richteri Forel) in 1 Current address: Center for Medical, Agricultural and Veterinary the United States. Field observations in South America Entomology, USDA-ARS, P.O. Box 14565, Gainesville, FL 32604. have revealed that the presence of Pseudacteon species

0013-8746/00/0841Ð0849$02.00/0 ᭧ 2000 Entomological Society of America 842 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 93, no. 4 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 Þeld 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 interspeciÞc 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 quantiÞed 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 interspeciÞc 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. in- Fig. 1. Design of the exploitative (top) and interference victa and its congener S. geminata (F.)? (3) What are (bottom) competition experiments. the important mechanism(s) underlying these effects? (4) How much of an overall limiting factor are Pseudacteon phorids to Solenopsis ant populations? water ad libitum (in test-tubes plugged with cotton), and provided fresh frozen crickets every day. After Materials and Methods initiation, the experimental colonies were maintained Ϸ Њ Solenopsis invicta colonies were collected from Tra- at 28 C, provided with water and sugar water ad vis County and S. geminata colonies were collected libitum, and fed two fresh frozen crickets every other from Hays County, TX. All colonies were of the po- day for 1 wk before the beginning of the experiments. lygyne, or multiple queen, form. P. tricuspis were All trays described below except the colony trays reared at the University of Texas at AustinÕs Bracken- contained a layer of plaster on the bottom, which was ridge Field Laboratory (BFL) from stock originally moistened before the experiments to maintain a rel- Ϸ collected in Sao Paulo State, Brazil. This is the north- ative humidity of 75%. All experiments were con- Ϸ Њ ern form of P. tricuspis as described by Borgmeier and ducted at 28 C. Prado (1975). Reference specimens of S. invicta, S. Resource Competition. I set up experimental S. in- geminata, and P. tricuspis have been placed in the victa colonies containing4gofworkers and2gof Natural History Museum of Los Angeles County, CA; brood. S. invicta workers were sieved through a screen the Museu de Histo´ria Natural, UNICAMP, Sao Paulo, with 0.85-mm openings, and each experimental colony Brazil; and at BFL. received2gof“major” workers Ͼ0.85 mm and2gof All experiments were conducted between January “minor” workers Ͻ0.85 mm. This procedure resulted and May 1999 at BFL. I set up experimental ant col- in a worker caste size ratio typical of monogyne colonies consisting of a measured quantity of workers, onies (see Discussion). Each gram of majors consisted brood, and a single queen. An electronic balance was of Ϸ370 workers, and each gram of minors consisted used to weigh all workers and brood. The experimen- of Ϸ1,600 workers. tal colonies were placed in open trays (25 by 18 by 7 Experimental colonies were starved for 48 h before cm), the sides of which were coated with Fluon (poly- the beginning of the trials to produce a uniform state tetraßuoroethylene; ICI Fluoropolymers, Exton, PA) of hunger. Each tray containing an experimental col- to prevent escapes. A petri dish (90 mm diameter, 15 ony was connected via a 12-cm length of opaque Ty- mm high) containing damp plaster to maintain hu- gon tubing (1 cm i.d.) to two adjacent foraging trays midity was provided as a nesting chamber. of the same dimensions on opposite sides of the colony The mother colonies from which the experimental tray, providing a choice of foraging in two equidistant colonies were derived were kept in the laboratory at trays containing the same food resource (Fig. 1). The Ϸ28ЊC for at least 2 wk before experimental colony trays were connected for 1 h before introduction of formation, fed a standardized diet of water and sugar the food resource during which time ants were al- July 2000 MORRISON:MECHANISMS OF PARASITOID EFFECTS 843 lowed to explore both foraging trays. Two freeze- and no-phorid treatments in the manipulative exper- killed crickets were then placed in the center of each iment, by a one-way analysis of variance (ANOVA). foraging tray, on white plastic cards (5 by 5 cm). The The Bonferroni method of multiple comparisons with crickets were stripped of the legs and antennae, which a family conÞdence level of 90% was used to compare could have been dismembered and carried away, and the average values of the control experiment to both were pinned down to prevent ants from moving them. the phorid and no-phorid treatments of the manipu- Glass tops were placed over both foraging trays. lative experiment. Resource retrieval rates were measured by quanti- Although I attempted to have a constant number of fying precisely the amount of food retrieved in 60 min. actively attacking phorids, there was an unavoidable Crickets were weighed with an electronic balance amount of variation among the trials in the number of immediately before and after exposure to ants. In each active ßies. In foraging trays with phorids present (the trial, a control set of crickets was left out for 60 min to manipulative experiment), the number of actively at- measure weight loss by desiccation. The average tacking phorids was counted for 1 min immediately weight loss of the control group was then subtracted before and 1 min immediately after counting recruit- from the weight loss of the experimental group. I also ing ants, as described above. I averaged the number of measured three potential mechanisms underlying this actively attacking ßies in each trial and, in simple effect: (1) worker activity, (2) number of workers linear regressions, regressed each of the four variables recruited, and (3) worker size. To quantify worker described above on average number of attacking ßies, activity, the number of workers crossing the edge in four separate regressions, to see if more active ßies (nearest to the colony tray) of the 5 by 5-cm card were resulted in a signiÞcantly greater effect. counted for 2 min at 10-min intervals. To quantify Interference Competition. I tested the effect of number of workers recruited to the bait, all workers on phorids on short-term interference competition by the 5 by 5-cm cards at the end of the trials were measuring the spatial dimensions of interspeciÞc com- collected and counted. To quantify worker size, I bat between S. invicta and S. geminata. Experimental measured head widths in a random subsample of 25 colonies of S. invicta were set up as described previ- workers taken from all workers collected from each ously. Workers of S. geminata are on average larger card at the end of the trials. than workers of S. invicta (Trager 1991), and previous work has revealed that S. invicta wins interspeciÞc The average number of actively foraging workers contests in the moderate to long-term when S. invicta throughout the course of the trials was likely to be and S. geminata colonies are equivalent by biomass, positively correlated with number of workers present but this outcome is reversed when the colonies are at the baits at the end of the trials. This potentially equivalent by worker number (Morrison 2000). This strong correlation does not preclude testing for each difference was not signiÞcant in the short term, how- effect individually, however, because Pseudacteon ever, and the outcome of short-term interspeciÞc in- phorids may cause Solenopsis workers to remain im- teractions was more equal when colonies were equiv- mobile for many minutes at a time (Porter et al. 1995b, alent by worker number (Morrison 2000). Thus, I set Orr et al. 1997, Morrison 1999). This effect on activity up S. geminata colonies that were equivalent in worker may be manifested independently of number of work- number to the S. invicta colonies. I sieved S. geminata ers present. workers through the 0.85-mm screen, and found that In the Þrst, or manipulative, set of experimental each gram of “majors” consisted of Ϸ190 workers, and trials, Þve mated, 1-d-old P. tricuspis females were each gram of “minors” consisted of Ϸ1,380 workers. I added to one of the foraging trays 10 min after the then set up colonies consisting of 3.9 g of S. geminata introduction of the food resource. Not all phorids majors, and 2.3 g of S. geminata minors. This procedure actively attacked ants, and additional ßies were added resulted in Ϸ740 majors and Ϸ3,180 minors per colony over time if necessary. I attempted to have at least two tray, for both S. invicta and S. geminata. phorids actively attacking workers at all times. No A S. geminata colony and a S. invicta colony were phorids were added to the opposite foraging tray. The each connected to opposite ends of a larger (37 by 24 trials lasted for 60 min after introduction of ßies. The by 7 cm) tray via 12-cm lengths of opaque Tygon same data were collected from the foraging tray with tubing (1 cm i.d.). This tray contained eight opaque phorids and the foraging tray without phorids in each walls that turned the central tray into a maze (Fig. 1). trial, and were compared with paired t-tests. Because The walls and sides of the tray were white, and coated multiple comparisons were made within the same ex- with Fluon to prevent the ants from escaping or scal- periment, the sequential Bonferroni method was used ing the walls. The bottom of the tray was covered with to control the group-wide type I error rate (Rice 1989). white plaster. A grid containing 72 squares, in nine In a second, or control, set of trials, the same pro- rows and eight columns, was marked off in the maze cedure was followed, except that no phorids were tray. A gate coated with Fluon was placed in the center added to either foraging tray. Paired t-tests revealed of the tray. The S. geminata and S. invicta colonies were no signiÞcant differences (P Ͼ 0.05) between the two equidistant from the gate, with 36 squares between the foraging trays for any of the four measured variables. gate and each colony tray. Thus, the values for each variable were averaged be- Workers from each colony were allowed to explore tween the two foraging trays of the control experi- the maze tray for 15 min. In this time, workers of both ment, and compared with the values for the phorid species traveled throughout the maze to the central 844 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 93, no. 4

Table 1. Effects of phorids on resource retrieval, and the underlying mechanisms, in S. invicta

Manipulative experiment Control experiment Phorids present Phorids absent P Avg of 2 trays Effect: Resource retrieval (g) 0.028 Ϯ 0.016 0.055 Ϯ 0.029 0.0064* 0.043 Ϯ 0.018 Mechanism: Avg no. of active workers 142.0 Ϯ 73.2 189.8 Ϯ 43.2 0.0152* 180.2 Ϯ 60.7 No. of workers at bait 167.8 Ϯ 90.6 183.2 Ϯ 77.5 0.3898 176.5 Ϯ 56.0 Avg worker size (HW in mm) 0.699 Ϯ 0.084 0.728 Ϯ 0.090 0.1788 0.799 Ϯ 0.058

The manipulative experiment consisted of a choice between foraging in trays with or without phorids. The control experiment was set up the same, but no phorids were present in either tray. Numbers represent means Ϯ SD. P-values are from two-tailed, paired t-tests. * SigniÞcant at ␣ ϭ 0.05 by the sequential Bonferroni method. Four comparisons were made within the same experiment.

gate. A glass cover was placed on top of the maze tray control trials were intermediate between the phorid and Þve mated, 1-d-old, female P. tricuspis phorids and no-phorid treatments of the manipulative trials were introduced. I recorded the precise locations of (Table 1). Average worker size at the end of the trials, Þghting between the Solenopsis species within the however, was larger for the control than either treat- grid, as well as parasitization attempts by P. tricuspis, ment of the manipulative trials. at 5-min intervals for 60 min. Usually after 60 min, There were no signiÞcant differences between the Þghting had spread throughout a large portion of the controls and the phorid treatment, or the controls and maze tray, and parasitization attempts by P. tricuspis the no-phorid treatment, for resource retrieval, had decreased (see Results). worker activity, or number of foragers, by the Bon- In most of the trials, two or more phorids began ferroni method with a 90% conÞdence level. Average attacking S. invicta immediately. Sometimes the pho- worker size in the control trials, however, was signif- rids added at the beginning of the trial did not attack icantly larger than average worker size in both the readily, and some phorids were eventually caught by phorid and no-phorid treatments of the manipulative ants in some of the trials. When fewer than two pho- trials, at the 90% conÞdence level. rids were actively attacking within the 5-min obser- On average, the colonies retrieved a total of 0.083 g vation interval, two additional phorids were added. of food in the manipulative experiment (summing the A total of 10 manipulative trials were conducted in phorid and no-phorid treatments). In the control ex- this manner, using different S. invicta colonies, S. gemi- periment, the colonies retrieved 0.086 g of food (dou- nata colonies, and P. tricuspis females in each trial. A bling the average of the two control trays). Thus, it series of 10 control trials were also conducted, which appears that the colonies were able to compensate for were the same in every respect except that phorids decreased food retrieval caused by phorid harassment were not added. A two-way ANOVA was used to test by increasing food consumption when food was avail- for an effect of Solenopsis species and phorid presence able elsewhere. on the outcome of the interactions. Simple linear regressions of number of active ßies versus the four measured variables were all nonsig- niÞcant (P Ͼ 0.05). Thus, the magnitude of the effects Results observed were independent of the number of ßies Exploitative Competition. In all trials, S. invicta col- actively attacking worker ants. The average number of onies foraged in both foraging trays. In the manipu- actively attacking ßies was fairly low, however, and fell lative experiment only about half as much of the re- within a narrow range (0.25Ð2.75). source was retrieved in trays with phorids as in trays Interference Competition. In the interference com- without phorids (Table 1). In the trays with phorids, petition trials, Þerce interspeciÞc Þghting occurred fewer workers actively foraged, fewer workers were immediately after the gates were opened and quickly present at the bait at the end of the trials, and the spread through the maze toward each colony tray average size of the workers present at the bait was (Fig. 1). Fighting was consistently observed farther smaller, compared with the foraging trays without within the S. invicta than the S. geminata territory. The phorids (Table 1). The effects on resource retrieval location of the interspeciÞc combat over time was very and average number of workers actively foraging were similar for both the manipulative and control trials both signiÞcant at P Ͻ 0.05 (paired t-tests). (Fig. 2). A two-way ANOVA revealed a signiÞcant In the control experiment, in which phorids were effect of species (F ϭ 9.50, df ϭ 1, P ϭ 0.0039), but the absent from both foraging trays, there were no differ- presence of phorids was not signiÞcant (F ϭ 0.96, df ϭ ences between the two trays in any of the measured 1, P ϭ 0.33). The interaction was also not signiÞcant variables (all P Ͼ 0.05). Thus, the values for each (F ϭ 0.05, df ϭ 1, P ϭ 0.83). variable were averaged between foraging trays, and Phorids qualitatively seemed more excited at the compared with the values for the phorid and no- beginning of the interference competition trials than phorid treatments in the manipulative experiment. in the exploitative competition trials, possibly because For the Þrst three variables, the average values of the of alarm pheromones released in the context of inter- July 2000 MORRISON:MECHANISMS OF PARASITOID EFFECTS 845

battle from the colony tray. Thus, although the ma- jority of Þghting 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 Þghting was highly signiÞcant (␹2 ϭ 26.16, df ϭ 8, P ϭ 0.001, chi-square test of homogeneity). 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 Þghting was very low, and could have been a result of phorid presence, although this was not quantiÞed.

Discussion Overview of Phorid/Ant Interactions. A number of Þeld 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 inßuence caste ratios and numbers of foraging Atta cephalotes (Orr 1992, Feener and Brown 1993). Pseudacteon phorids (P. pusillum and an unde- scribed species) have been documented to decrease Fig. 2. Number of squares Þghting extended into the foraging in the Argentine ant, L. humile (Orr and Seike territories of each species in the interference competition 1998). trials. Many recent studies of ant/phorid interactions have focused on Solenopsis Þre ants and their associated Pseudacteon parasitoids. In South America, the pres- speciÞc aggression. Workers of the two ant species ence of Pseudacteon ßies that parasitize S. saevissima began grappling with each other quickly after the gate complex ants has been shown to decrease worker was opened, clamping on to each other with their foraging, and contribute to food resources being lost mandibles. Most phorids did not seem interested in to competing ant species (Orr et al. 1995, 1997; Porter attacking host workers attached to enemy workers. In et al. 1995b; Folgarait and Gilbert 1999). In Central fact, most of the phorids spent most of their time and North America, Pseudacteon ßies that parasitize S. attempting to parasitize host workers recruiting to the geminata complex ants have also been documented to decrease food retrieval (Feener and Brown 1992, Mor- rison 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 Þeld, with phorid and ant species native to the re- spective areas. Separating the exploitative and interference components of interspeciÞc competition in the Þeld is often difÞcult, 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 Þrst detailed laboratory study of the effects of phorids on the pure exploitative and interference components of interspeciÞc competition, and the underlying mechanisms. Fig. 3. Distribution of Þghting between S. geminata and Exploitative Competition. When S. invicta workers S. invicta and distribution of parasitization attempts by P. were given a choice to forage in trays with or without tricuspis on S. invicta The S. geminata colony was nearest to P. tricuspis ßies, resource retrieval was 50% less in the row A, whereas the S. invicta colony was nearest to row I. tray with phorids. SigniÞcantly fewer workers actively 846 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 93, no. 4 foraged in the tray with phorids. Fewer, and smaller, workers in the Þeld (Feener and Brown 1992, Porter workers were present at the end of the trials in the tray et al. 1995b). with phorids, but these differences were not signiÞ- Interference Competition. The presence of P. tri- cant. In control trials, when no phorids were present cuspis had no effect on the outcome of short-term in either tray, the amount of resource retrieved was interspeciÞc competition, based on the spatial location intermediate to that of the phorid versus no-phorid of Þghting. InterspeciÞc interactions between S. in- treatments, indicating that the colonies were obtain- victa and S. geminata usually involved workers of each ing more food from the no-phorid tray to compensate species clasping each other with their mandibles and for decreased food retrieval in the phorid tray. This is grappling for extended periods (several minutes to the the Þrst evidence that host ants may be able to com- end of the trials). At times, three or more workers pensate for diminished food retrieval caused by phorid were attached to each other. (Detailed descriptions of harassment. the interspeciÞc interactions of S. geminata and S. In nature, this mechanism may be manifested by a invicta are given in Bhatkar [1988] and Morrison spatial shift to increased underground foraging during [2000].) The phorids did not appear interested in the day when phorids are active, or a temporal shift to these clusters of workers. Pseudacteon phorids exhibit increased aboveground foraging at night, when pho- size-speciÞc preferences for host ants (Morrison et al. rids are not active. A study of the diet of S. invicta and 1997, Morrison and Gilbert 1998), and two or more S. geminata revealed that a large proportion of their workers grappling together probably do not Þt their diet may be obtained from subterranean sources search image for hosts. (Tennant and Porter 1991), and both species com- There was a signiÞcant difference between the spa- monly forage diurnally as well as nocturnally (Claborn tial distribution of Þghting and the spatial distribution and Phillips 1986, Morrison 1999). of parasitization attempts. Most parasitism attempts SigniÞcantly larger workers foraged in the control occurred between the active Þghting and the tube trials than in either treatment of the experimental leading to the S. invicta colony tray, where individual trials. Solenopsis workers appear to be able to com- S. invicta workers could be found. Thus, the effect of municate the presence of phorids to nestmates by Pseudacteon phorids on the interference component alarm pheromones (C. G. DallÕAglio-Holvorcem, un- of interspeciÞc competition in the Þeld is likely to depend upon the spatial location of interspeciÞc in- published data). Thus, the colonies may have been teractions relative to the host Solenopsis colony. S. aware of the general presence of phorids in the area, geminata and S. invicta use extensive underground and larger workers did not forage in the no-phorid tunnel systems (Markin et al. 1975), however, and are trays because of the ultimate, rather than proximate, able to reach areas distant from the colony with little risk of parasitization. above-ground exposure. Thus, the effect of phorids on In the foraging trays of the experimental set-up, interference competition is likely to be relatively small there was no signiÞcant relationship between varia- in most cases. In a Þeld study of interference compe- tion in the number of actively attacking phorids and tition between S. geminata and S. invicta at rich food variation in any of the measured variables. Although resources, S. geminata workers were observed to travel the presence of a single female is often sufÞcient to only short distances above ground from underground disrupt worker foraging at a localized food resource tunnel entrances to the contested resources (Morri- (Feener and Brown 1992, Orr et al. 1995), higher son 1999). phorid densities have been associated with lower re- The identity of competing ant species may also be source retrieval rates in the Þeld (Morrison 1999). important in determining the effect of phorids on Variation in attack frequency among individual pho- interference competition. If interspeciÞc interactions rids may obscure this relationship, however. Orr et al. with other ant species involve less grappling of work- (1997) reported that the degree of response in workers attached to each other, the effect of phorids may ers was more closely related to number of attacks than be greater. For example, Monomorium is a genus found amount of time that a phorid was present. Likewise, in in sympatry with S. invicta that relies heavily on chem- the context of the laboratory experiments of this study, ical defense, rather than physical grappling (Baroni- the degree of response of S. invicta may be more Urbani and Kannowski 1974). Such an interaction may closely associated to the number of attacks than the result in more parasitization pressure on S. invicta, number of phorids attacking. It is also possible that an although the dispersal of airborne venom could neg- effect of phorid number may emerge over a wider atively affect Pseudacteon parasitization. range of ßy densities. The effects of phorids on interference interactions Although only females were used in the experimen- were evaluated over a relatively short period in this tal trials, P. tricuspis males may have similar effects on laboratory study. A previous study indicated that the worker behavior. P. tricuspis males are attracted to ultimate winner (based on reduction of colony size) worker ants, apparently to Þnd mates, and appear to of interference interactions could usually, but not al- feign attacks on workers (unpublished data), possibly ways, be predicted based on the short-term distribu- to increase worker excitement and release of phero- tion of Þghting (Morrison 1999). In the previous study, mones which may attract P. tricuspis females. The S. geminata and S. invicta workers were observed to presence of both male and female Pseudacteon phorids Þght for several days before such territorial disputes has been documented to disrupt foraging of Solenopsis were resolved, and it was not practical to run the July 2000 MORRISON:MECHANISMS OF PARASITOID EFFECTS 847 experiments of the current study for such a long pe- (S. D. Porter, 2000), apparently would be more effec- riod. It is possible that phorids may have a greater tive in controlling polygyne S. invicta populations, all effect over a longer period in nature, but any potential else being equal. effects will be limited by the spatio-temporal dimen- The results of the laboratory experiments elucidate sions of the interference interactions. In nature many the mechanisms by which P. tricuspis decreases short- interactions may not be accessible to phorids at all, term resource retrieval in S. invicta. Whether this will such as Þghting occurring underground or at night. translate into long-term food limitation for the colony Implications for Biocontrol. In the Þrst test of the is difÞcult to predict. S. invicta workers never aban- effects of South American Pseudacteon phorids on doned any baits in the laboratory trials, and revealed resource retrieval by North American S. invicta pop- an ability to compensate for phorid harassment by ulations, a single P. tricuspis female decreased food foraging on alternate resources. The Þrst report of the retrieval by 15% in laboratory trials, although the effect of Pseudacteon phorids on Solenopsis Þre ant mechanisms underlying the decrease in food retrieval foraging in South America found evidence that phorid were not identiÞed (Morrison 1999). It was qualita- presence resulted in S. invicta abandoning baits to tively observed that few majors entered the foraging competing ant species (Orr et al. 1995). Such a strong trays, however, and minors foraged largely unmo- suppressive effect may occur primarily during initial lested. Random samples of polygyne S. invicta were recruitment to food resources, however, and subse- used, in which the average worker size was only 0.62 quent studies have found that after recruitment is mm. P. tricuspis, however, prefers workers with a head established, enough workers usually remain at the width of Ϸ0.93 mm (Morrison et al. 1997, Morrison and resource in the presence of phorids to successfully Gilbert 1998). The experiment in Morrison (1999) was defend the resource from competing ants (Porter et al. designed differently than the current study, and did 1995b, Orr et al. 1997). not allow a simultaneous choice of phorid or no-pho- In Þeld experiments conducted in central Texas rid food sources. Each colony was instead tested se- with S. geminata and associated Pseudacteon phorids, S. quentially with phorid and no-phorid treatments. geminata workers were observed never (Morrison In pilot trials of the experimental set-up of the 1999) or only very rarely (Morrison et al. 2000) aban- current study, P. tricuspis females rarely attacked S. doning a food resource to competing ants, even under invicta workers in foraging trays when offered a ran- harassment by multiple Pseudacteon females. Some dom subsample of polygyne S. invicta workers. The workers (primarily minors) remained at the food re- most likely reason was that the foraging workers were source, guarding it and covering it with soil and bits of too small. Only Ϸ12% of the workers in the typical debris, while other workers tunneled under the food polygyne S. invicta colony in Travis County, TX, have resource, decreasing exposure to phorids. head widths Ն0.93 mm (unpublished data). By sieving It is difÞcult to make a generalized prediction re- workers and adding a relatively larger proportion of garding the overall effect of Pseudacteon phorids on majors, I obtained worker size distributions more typ- Solenopsis ants. All studies to date have focused on ical of the monogyne form. In a previous study, the short-term, behavioral effects lasting at most several average head width of monogyne S. invicta workers hours (Feener and Brown 1992; Orr et al. 1995, 1997; was 0.86 mm (Morrison and Gilbert 1998). The screen Porter et al. 1995b; Folgarait and Gilbert 1999; Mor- used to separate S. invicta majors from minors had rison 1999). Solenopsis workers exhibit a number of 0.85-mm openings. Natural monogyne colonies were characteristics or frequently observed behaviors that not used because they are rare in central Texas. appear to decrease the impact of Pseudacteon phorids, Pseudacteon phorids are already being released in however, and may be to some degree adaptations to the southeastern United States as potential biocontrol Pseudacteon parasitism pressure. These include under- agents of S. invicta (Porter et al. 1999). The overall ground foraging tunnels or covered walkways, cover- effect of these introductions will depend to an extent ing food with dirt or debris, and defensive posturing on the Pseudacteon species introduced and S. invicta (reviewed in Morrison 1999). Altering foraging strat- social form in question. There are at least 18 Pseudac- egies to avoid phorid ßies, as revealed in this study, teon species that attack S. saevissima complex Þre ants may also be frequently employed. Yet the presence of in South America (Porter 1998). Multiple Pseudacteon Pseudacteon-speciÞc defensive behaviors is evidence species often coexist on the same Pseudacteon host that these parasitoids are capable of having popula- species (Orr et al. 1997). One way these species appear tion-level impacts on their Solenopsis hosts, or such to coexist is by partitioning their polymorphic hosts by behaviors would not have evolved. Long-term Þeld size, with larger phorid species parasitizing larger studies are needed to assess the magnitude of the worker ants (Morrison et al. 1997, Morrison and Gil- population-level effects of Pseudacteon phorids on So- bert 1998). Moreover, host worker size appears to lenopsis Þre ants. determine the sex of the phorid offspring (Morrison et al. 1999). The mechanisms documented in this laboratory Acknowledgments study indicate that P. tricuspis is likely to have a larger R. Guerra and E. A. Kawazoe assisted with the laboratory effect on monogyne, rather than polygyne, S. invicta experiments. T. Alexander, D. Broglie, A. Cottingham, P. colonies. A smaller species of Pseudacteon, such as P. Field, F. Kozuh, R. Guerra, C. Papp, and J. Warr reared the obtusus (Morrison and Gilbert 1999) or P. curvatus phorid cultures that made this project possible. L. E. Gilbert 848 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 93, no. 4 was instrumental in motivating this study and providing the Markin, G. P., J. O’Neal, and J. Dillier. 1975. Foraging tun- necessary resources. This research was funded by the State nels of the red imported Þre ant, Solenopsis invicta (Hy- of Texas Fire Ant Research and Management Committee. menoptera: Formicidae). J. Kans. Entomol. Soc. 48: 83Ð 89. Morrison, L. W. 1999. Indirect effects of phorid ßy parasitoids on the mechanisms of interspeciÞc competition References Cited among ants. Oecologia 121: 113Ð122. Baroni Urbani, C., and P. B. Kannowski. 1974. Patterns in Morrison, L. W. 2000. 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