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

Transcription

1 Ecological Entomology (24) 29, Phorid fly parasitoids of invasive fire ants indirectly improve the competitive ability of a native ant NATASHA J. MEHDIABADI, ELIZABETH A. KAWAZOE and LAWRENCE E. GILBERT Section of Integrative Biology and Brackenridge Field Laboratory, School of Biological Sciences, University of Texas at Austin, U.S.A. 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 7 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 5-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 5 days. These laboratory findings are interpreted with regard to the more complex interactions in the field. Key words. Biological control, Biological invasions, Forelius mccooki, indirect effects, interspecific competition, parasitism, Pseudacteon tricuspis, Solenopsis invicta. Introduction Biological invasions often wreak havoc on natural systems (Elton, 1958; Drake et al., 1986; Pimm, 1991; Vitousek et al., 1996; Human & Gordon, 1997; Simberloff et al., 1997; Mooney & Cleland, 21; Holway et al., 22a; Sanders et al., 23). Theirability to outcompete and displace native species is possibly theirmost devastating trait (Ward, 1987; Human & Gordon, 1996; Vitousek et al., 1996; Suarez et al., 1998, 2; Mack et al., 2; Mooney & Cleland, Correspondence: Natasha J. Mehdiabadi, Rice University, Ecology and Evolutionary Biology, MS 17, 61 Main Street, Houston, TX , U.S.A. njum@rice.edu 21; Wojcik et al., 21). Of the numerous invading organisms, social insects are among the most harmful (Vinson, 1986; Winston, 1991; Williams, 1994). The red imported fire ant, Solenopsis invicta, is a highly invasive species of southeastern U.S.A. Since its introduction from South America almost 7 years ago, S. invicta has caused extensive ecological (Porter & Savignano, 199; Vinson, 1997; Wojcik et al., 21) and economic damage (Thompson et al., 1995). This pest has broad impacts, affecting small mammals (Holtcamp et al., 1997), endangered cave invertebrates, and native ants just to name a few (Porter & Savignano, 199; Wojcik et al., 21). Furthermore, this invasive ant is capable of disrupting native ant communities not only at local, but also at biogeographic, scales (Gotelli & Arnett, 2). Since pesticides have failed to effectively # 24 The Royal Entomological Society 621

2 622 Natasha J. Mehdiabadi, Elizabeth A. Kawazoe and Lawrence E. Gilbert control the red imported fire ant, research efforts have focused on biological control. Phorid fly parasitoids from South America are currently being introduced into the U.S.A. as a potential biocontrol agent (Feener & Brown, 1992; Orr et al., 1995; Porter et al., 1995a; Morrison, 2a). These dipterans from the family Phoridae and genus Pseudacteon are specialised parasitoids of fire ants (Trager, 1991; Disney, 1994). These flies harass fire ant workers that are performing outside tasks, such as foraging and defence (Williams et al., 1973; Feener, 1987; Orr et al., 1995; Pesquero et al., 1996). Female flies attack numerous workers, ovipositing a single egg into the thorax of each ant host (Feener, 1987; Porter et al., 1995b; Morrison et al., 1997). After egg injection, the larva migrates to the head of the ant while consuming its haemolymph; at pupariation, decapitation of the host results and finally, an adult fly emerges from the head of the ant (Porter et al., 1995b). Although as few as 3% of ants from a colony are actually parasitised (Morrison et al., 1997), these parasitoid flies can dramatically affect their hosts through indirect effects on foraging and interspecific interactions (Feener, 1981; Feener & Brown, 1992; Orr et al., 1995; Porter et al., 1995a; Morrison, 1999; LeBrun & Feener, 22; Mehdiabadi & Gilbert, 22). The mere presence of phorids can elicit defensive postures in ants (Porter et al., 1995a; Orr et al., 1997; Brown & Morrison, 1999; Folgarait & Gilbert, 1999; Morrison et al., 1999) that can result in workers remaining motionless (Feener, 1987), and thus reducing their food harvesting capabilities substantially (Feener, 1981; Feener & Brown, 1992; Orr et al., 1995; Porter et al., 1995a; Morrison, 1999; Mehdiabadi & Gilbert, 22). Because the amount of food an ant colony collects is greatly influenced by competition with otherspecies (Ho lldobler& Wilson, 199), phorids can also alter interspecific interactions (Feener, 1981; Feener & Brown, 1992; Orr et al., 1995; Porter et al., 1995a; Morrison, 1999, 2b). Past work has demonstrated for a variety of phorid and host species that these flies can cause a reduction in both host food retrieval (Feener & Brown, 1992; Morrison, 1999; Mehdiabadi & Gilbert, 22) and worker recruitment to food baits (Orr et al., 1995, 1997; Porter et al., 1995a; Folgarait & Gilbert, 1999; Mehdiabadi & Gilbert, 22). In addition to impacting such aspects of exploitative competition, phorids have also been shown to influence interference aspects of competition (i.e. fighting) (Porter et al., 1995a; Orr et al., 1995, 1997; Morrison, 2b). Most previous studies on phorid fly ant interactions have focused on the direct and indirect impacts of parasitoids on their ant host (Feener, 1981; Feener & Brown, 1992; Orr et al., 1995; Porter et al., 1995a; Morrison, 1999, 2b). For example, Mehdiabadi and Gilbert (22) recently investigated the colony-level effects of phorid fly parasitoids that are currently being introduced into the U.S.A. as possible biological control agents of their host, the red imported fire ant. Phorids decreased colony protein consumption and the numbers of large-sized workers (Mehdiabadi & Gilbert, 22). Here the complementary data from the same experiment are presented, yet a different approach from most studies is taken by examining the effects of these phorids on a competitor of the host. Such an investigation reveals whetherthe introduction of S. invicta-specific phorids as biocontrol agents will increase the competitive ability, and ultimately populations, of native ants. The aim of the study was to quantify the effects of the recently introduced phorid fly parasitoid, Pseudacteon tricuspis, on the foraging and competitive ability of a red imported fire ant competitor, Forelius mccooki. This native ant coexists with S. invicta (Camilo & Phillips, 199), possibly because of its tolerance of extremely high temperatures (Holway et al., 22b). The prediction is that F. mccooki should improve its competitive abilities against the red imported fire ant when S. invicta-specific phorids are present compared with when they are absent. The effects that P. tricuspis has on the following were examined: (1) the abundance and travelling rates of F. mccooki foragers, (2) the proportion of F. mccooki defenders (i.e. workers fighting aggressively against red imported fire ants), and (3) native ant colony growth after 5 days. Methods Collection and maintenance of Forelius mccooki and Solenopsis invicta colonies Thirteen multiple-queen colonies of F. mccooki and 12 multiple-queen colonies of S. invicta were collected in Austin, Texas between April and August 2. This experiment had 12 replicates. Each replicate consisted of a control (without phorid fly exposure) and an experimental (with phorid fly exposure) treatment. For each replicate, a field-collected colony of both F. mccooki and S. invicta was divided in half (however, in one case, an F. mccooki field colony was divided into three colony fragments and in three cases, a F. mccooki field colony remained as one colony). This blocking factorwas used because workers from different colonies may vary in task and brood-rearing capabilities (Porter & Tschinkel, 1985). Each F. mccooki colony fragment had at least one queen, approximately 5 workers, and brood. Solenopsis invicta colony fragments were of similar size to F. mccooki subcolonies (one mated queen, 5 workers: 425 minors, 4 small majors and 35 large majors, and 2.5 g of brood). Although F. mccooki is a small ant, colonies of the two species were equalised according to numbers, not biomass, for a realistic estimate of competition pressure. None of the F. mccooki colonies collected in the field had sufficient worker populations to equalise the two competing species according to biomass. Thus, it would have been unrealistic to give F. mccooki such a disproportionate numerical advantage over S. invicta. Individual sub-colonies were housed in plastic nest boxes (43.2 cm 27.9 cm 7.6 cm), which were connected by transparent tubing to foraging arenas (55.9 cm 43.2 cm 7.6 cm). Both species shared one foraging arena. All tubing and boxes were lined with Fluon # to prevent ants from escaping. Colonies were reared under a LD 12:12 h cycle at 3 C.

3 Effects of parasitoids on a host s competitor 623 Observations One freeze-killed cricket and a sugarwatertest tube were placed in the foraging arena on alternate days, 2 days per week, for 5 days. Each of the 14 foraging periods lasted approximately 2 h. During foraging observations, the barrier between F. mccooki and S. invicta was removed for all subcolonies, and four female and two male phorids were introduced for half the sub-colonies (i.e. those in the phorid treatment). Male flies were added to the phorid treatment for the following two reasons: (1) to ensure that females were mated, and thus were able to inject eggs into their ant hosts, and (2) to mimic what occurs in nature because both male and female phorid flies are often found hovering above ants in the field (Feener, 1987; Feener & Brown, 1992; Porter et al., 1995a; Morrison et al., 1999). Experimental sub-colonies were always exposed to parasitoids when food was presented. Colonies received protein (crickets) only in the foraging arenas; however, sugar water was placed in the foraging arenas as well as in the nest boxes so that colonies would not starve. Nevertheless, sugar water tubes were removed from the nest boxes 24 h before foraging observations to promote foraging and competitive interactions. Both sugar water and crickets were placed in the foraging arenas because carbohydrates provide workers with energy to perform various tasks for colony maintenance and survival (Ho lldobler & Wilson, 199) whereas protein food sources are important for brood development (e.g. Sorenson et al., 1983). The following data were collected during the 5-day experiment: the abundance and travelling rates of foraging ants, the proportion of defenders [no. of F. mccooki defenders/(no. of F. mccooki defenders þ no. of S. invicta defenders)], and worker population size (numbers of surviving workers at the start and end of the experiment). At the end of each 2-h foraging observation, the numbers of workers on and around each food bait were counted in order to determine the abundance of F. mccooki foragers; food baits were placed on white index cards (8 mm 2 ) so that counting was consistent. Travelling rates were estimated by counting the numberof F. mccooki foragers crossing an arbitrary line on the index card en route from the food bait and the nest in a 3-s time interval, after 3 min and 64 min of each foraging period. Defenders were strictly identified as workers engaged in direct, aggressive behaviours toward interspecific competitors, and recorded at the end of each foraging observation. Finally, the effects of phorids on colony growth of F. mccooki were determined by measuring the change in colony biomass before and after the 5-day experiment. All colonies were weighed on a precision balance, and weights were then converted to numbers of workers making up a colony. Data analysis Data were analysed in StatView (Version 5, SAS Institute Inc., Cary, North Carolina) using ANOVA ora one-group t-test where applicable. For foraging and defence results, the following criteria were used for analysis: first, an ANOVA was performed in order to determine whether there was a significant colony (i.e. each of the field-collected colonies split in two) effect fora given dependent variable; the factors were colony and phorid (absence vs. presence of parasitoid flies). Because colony was significantly different for all dependent variables and explained a majority of the variance, colony phorid was used as the error term and a paired analysis was employed to test whether phorids significantly altered foraging and defence of F. mccooki. Data were averaged across the 14 foraging periods over the 5-day experiment. In addition, data from both the sugar water and protein food sources were combined in the analysis of the foraging results. The difference between sub-colonies with phorids present (i.e. experimental treatment) and subcolonies without phorids present (i.e. controls) within colony pairs was determined, that difference was divided by their sum to get the proportional change, and an arcsine transformation was performed. Then, a one-sample t-test (hypothesised mean ¼ ) was used, which is analogous to a paired t-test (pairs within colonies). It was decided not to use a pair ed t-test because it would not have been possible to analyse proportional differences. For colony growth results, a factorial ANOVA without interactions was used; the factors were colony and phorid and the dependent variable was the natural log of colony mortality rate (i.e. no. of ants at end of experiment/no. of ants at start of experiment). Colony phorid was the error term. Results The results show that phorids indirectly altered the foraging behaviours of F. mccooki. The average abundance of F. mccooki foragers at the end of the 14 foraging observations increased by 51% forexperimental colonies with S. invictaspecific phorids compared with controls without the flies (one sample t-test: mean ¼.516, t 11 ¼ 2.691, P ¼.21). Thus, F. mccooki colonies in the phorid treatment were capable of improving their abundance at food baits due to fire ants being harassed by the parasitoid flies (Fig. 1). No. of workers Control With phorids A B C D E F G H I J K L Colony pairs Fig. 1. Mean abundance of Forelius mccooki foragers for the 12 colony pairs (average number of foragers on and around protein and carbohydrate food sources at the end of 14 foraging observations; þse). Each colony pairconsisted of one sub-colony with phorid flies and another without phorids.

4 624 Natasha J. Mehdiabadi, Elizabeth A. Kawazoe and Lawrence E. Gilbert Phorid presence had no effect on mean travelling rates of F. mccooki foragers when data were combined for both protein and carbohydrate food sources after 3 min (one sample t-test: mean ¼.25, t 11 ¼ 1.763, P ¼.156) and after64 min since food presentation to colonies (one sample t-test: mean ¼.382, t 11 ¼ 2.189, P ¼.51). However, when the data were analysed separately according to food type, travelling rates were 32% and 43% higherat the sugarwater after3 min (one sample t-test: mean ¼.321, t 11 ¼ 2.86, P ¼.155) and 64 min (one sample t-test: mean ¼.432, t 11 ¼ 2.684, P ¼.213) respectively (Fig. 2). Nevertheless, the numbers of F. mccooki foragers travelling to and from the protein food source and the nest in a 3-s observation were unaffected at either time interval (one sample t-test; 3 min: mean ¼.129, t 11 ¼ 1.41, P ¼.324; 64 min: mean ¼.317, t 11 ¼ 1.65, P ¼.1272). These results suggest that native ant workers either preferred to forage on carbohydrate food sources, possibly to improve their energy for foraging and/or defence or that they were, for some reason, bettercompetitors against S. invicta at the sugarwatervs. the protein food item. Despite disrupting exploitative aspects of competition, phorid flies did not significantly alter the outcome of interference competition in this study (Fig. 3). In other words, the proportion of F. mccooki defenders [no. of F. mccooki defenders/(no. of F. mccooki defenders þ no. of S. invicta defenders)] was no different in phorid treatments compared with controls (one sample t-test: mean ¼.158, t 11 ¼ 2.19, P ¼.686). Most, if not all, interference contests occurred away from the food source, allowing defenders to be easily distinguishable from foragers, who were near the food source. Overall, the above results show that phorids are capable of impacting aspects of exploitative, but not necessarily interference, competition of F. mccooki. However, such improvements did not translate into a significant increase in native ant colony growth after 5 days of this experiment (F 1,11 ¼.92, P ¼.3626; Fig. 4). The developmental time from egg to adult is believed to be unknown for a F. mccooki worker; developmental time is 23 days at 35 C fora Proportion of defenders S. invicta minor worker (Porter, 1988) and F. mccooki is a smallerant, so it is expected that at least one complete generation is to be included in the study. Discussion Treatment Control With phorids Fig. 3. Mean proportion of Forelius mccooki defenders [no. of F. mccooki defenders/(no. of F. mccooki defenders þ no. of S. invicta defenders); þse] in the phorid treatment and controls at the end of the 14 foraging observations. The results provide an estimate of the potential effects of a recently introduced phorid fly parasitoid (P. tricuspis) on the competitive ability and survivorship of a native ant competitor of the red imported fire ant. This experiment reveals two fundamental points. First, phorid fly parasitoids are capable of indirectly altering aspects of foraging (Figs 1 and 2). Second, these perceived improvements to the interspecific competitor, however, might not translate into enhanced colony growth or fitness at least as measured after 5 days (Fig. 4). Both the abundance and travelling rates (at the carbohydrate source) of F. mccooki foragers were higher in treatments with phorids in comparison to controls (Figs 1 and 2). The presence of parasitoids in the experimental treatment caused S. invicta to assume defensive postures Proportional change C p C wo /total min 64 min A B C D E F G H I J K L Difference in mortality (C p C wo ) A B C D E F G H I J K L 1.2 Colony pair 3 Colony pair Fig. 2. Proportional change [(sub-colony with phorids (C p ) control sub-colony (C wo ))/(sub-colony with phorids þ control sub-colony); SE] in travelling rates of Forelius mccooki foragers at the carbohydrate food source after 3 min and after 64 min averaged across the 14 foraging time periods for each colony pair. Fig. 4. Difference in mortality [sub-colony with phorids (C p ) control sub-colony (C wo )] foreach of the 12 Forelius mccooki colony pairs at the end of the 5-day experiment. Values below the line denote that there was lower mortality for sub-colonies in the phorid treatment relative to the controls, and vice versa.

5 Effects of parasitoids on a host s competitor 625 (N. J. Mehdiabadi, pers. obs.; Feener, 1987; reviewed in Morrison, 2a) or return to the nest, allowing the interspecific competitor F. mccooki to improve its competitive ability at shared food items (Figs 1 and 2). Phorid fly parasitoids are well known for inhibiting foraging of their ant hosts (Feener, 1981, 1988; Feener & Brown, 1992; Orr et al., 1995; Porter et al., 1995a; Morrison, 1999; Mehdiabadi & Gilbert, 22). This decrease in foraging is manifested as a reduction in both the number of foragers (Feener & Brown, 1992; Porter et al., 1995a; Orr et al., 1995, 1997; Folgarait & Gilbert, 1999) and the quantity of food intake (Morrison, 1999; Mehdiabadi & Gilbert, 22). Such investigations seem just as valuable forcompetitors of the ant host. Despite affecting exploitative aspects of competition, the presence of the S. invicta-specific flies did not significantly alter outcomes of interference competition in the experiment. There was no significant difference in the proportion of F. mccooki defenders when comparing sub-colonies from the experimental treatment and controls (Fig. 3). Previous work has shown that in their native South America, fire ants sometimes lost to interspecific competitors at food baits when phorids were present (Orr et al., 1995), but not always (Porter et al., 1995a; Orr et al., 1997); the outcome seemed to be dependent on the level of ant recruitment at food resources when phorid flies first appeared. In a laboratory study, Morrison (2b) examined interference competition (without a food resource) between the native fire ant, S. geminata, and S. invicta in the presence and absence of P. tricuspis, and documented that phorids had no significant effect on altering the outcomes of these contests. Future studies need to examine in the field whether P. tricuspis can modify such aggressive behaviours at various levels of ant recruitment, and for a range of native ant species that co-occurwith S. invicta. Despite the efficacy of phorids in enhancing the competitive ability of F. mccooki, these improvements had no significant influence on colony growth (Fig. 4). Fifty days might not have been sufficient time to observe a substantial increase in colony growth due to the increased foraging. Experiments over longer periods of time are needed in order to determine whether phorids can in fact indirectly increase native ant populations by providing a host s interspecific competitorwith a competitive advantage at shared food resources. Although the laboratory study allowed for a relatively accurate estimate of the effects of phorids on an interspecific competitorby controlling forpotential confounding factors, the relevance of these results must be discussed in terms of the more complex fire ant phorid fly interactions in the field. During the 5-day experiment, colonies were either always (i.e. phorid treatment) or never (i.e. control) exposed to phorid fly parasitoids so that an attempt could be made to quantify precisely the impacts of phorids on F. mccooki; thus, the only intended difference between the two treatments was the absence or presence of phorids. In the field, S. invicta colonies can be attacked by phorids at some food sources, but not at others; thus, varying levels of phorid pressure are expected. Nevertheless, abundance of parasitoids in this study was on average one attacking fly per2 S. invicta foragers (Mehdiabadi & Gilbert, 22), which is similarto those experienced by colonies in their native range (see Orr et al., 1995; Folgarait & Gilbert, 1999). Also, in their native South America, fire ants are exposed to a variety of phorid species that attack different worker castes, implying that exposure to multiple phorid species can have stronger impacts on fire ants than just a single species (Morrison et al., 1997). In addition to phorid attack rates, the level of competition in the experiment was practical. Even though F. mccooki and S. invicta were forced to compete at food baits, the intensity of competition was realistic, as colonies were equalised according to number and not biomass. As mentioned before, F. mccooki, a monomorphic species, is a relatively small ant compared with S. invicta; a red imported fire ant minor is roughly twice the size of a F. mccooki worker. In areas where the two species coexist, F. mccooki can outcompete otherants, including S. invicta, because of its impressive recruitment capabilities and because of its tolerance of high temperatures (Holway et al., 22b). The very premise for the use of phorids as biocontrol agents rests upon the capabilities of these flies to reduce imported fire ant populations via indirect effects (reduction in foraging), which in theory should allow native ants to enhance theircompetitive ability, and hopefully theirpopulations, against this highly invasive species (Feener& Brown, 1992; Orr et al., 1995; Porter et al., 1995a,b; Gilbert & Morrison, 1997; Porter & Alonso, 1999). This study shows that phorids promote F. mccooki foraging, but the foraging advantage did not translate into enhanced colony growth. Nevertheless, the improvements to F. mccooki foraging demonstrate that phorids can alter ant competitive interactions, which may translate into significant effects in the field. Obviously, field studies are crucially needed in order to determine the efficacy of these recently introduced parasitoids as biological control agents. Acknowledgements Resident Manager J. Crutchfield facilitated our work at Brackenridge Field Laboratory. We thank fire ant/phorid lab personnel J. Bradner, S. Bramblett, D. Broglie, A. Cottingham, J. Dunn, P. Field, F. Kozuh, L. Morrison, C. Papp, R. Patrock, and C. Smith for logistical support, advice, and various other kinds of help. Professor U. Mueller (UT), provided a special degree of inspiration and advice for N.J.M. during the project, and W. Rogers (Rice) and E. Siemann (Rice) provided crucial statistical assistance. Two anonymous reviewers provided much appreciated comments on earlier versions of this manuscript and at Rice, K. Foster, W. Holtcamp, T. Platt, and J. Strassmann provided useful critiques of later versions. This work was funded by the Texas Imported Fire Ant Research and Management Project to L.E.G., and a Carl Gottfried Hartman Graduate Research Fellowship, a Dorothea Bennett Memorial Graduate Research Fellowship, and an

6 626 Natasha J. Mehdiabadi, Elizabeth A. Kawazoe and Lawrence E. Gilbert Ari Yehiel Blattstein Endowed Presidential Scholarship from the University of Texas at Austin to N.J.M. References Brown, B.V. & Morrison, L.W. (1999) New Pseudacteon (Diptera: Phoridae) from North America that parasitises the native fire ant Solenopsis geminata (Hymenoptera: Formicidae). Annals of the Entomological Society of America, 92, Camilo, G.R. & Phillips, S.A. Jr(199) Evolution of ant communities in response to invasion by the fire ant Solenopsis invicta. Applied Myrmecology: A World Perspective (ed. by R. K. VanderMeer, K. Jaffe and A. Cedeno), pp Westview Press, Boulder, Colorado. Disney, R.H. (1994) Scuttle Flies: the Phoridae. Chapman & Hall Press, London. Drake, J.A., Mooney, H.A., di Castri, F., Groves, R.H., Kruge, F.J., Rejmanek, M. et al., eds(1986) Biological Invasions: a Global Perspective. Wiley, Chichester, U.K. Elton, C.S. (1958) The Ecology of Invasions by Animals and Plants. Wiley, New York. Feener, D.H. Jr (1981) Competition between ant species outcome controlled by parasitic flies. Science, 214, Feener, D.H. Jr (1987) Size-selective oviposition in Pseudacteoncrawfordi (Diptera, Phoridae), a parasite of fire ants. Annals of the Entomological Society of America, 8, Feener, D.H. Jr (1988) Effects of parasites on foraging and defense behaviourof a termitophagous ant, Pheidole titanis Wheeler (Hymenoptera: Formicidae). Behavioural Ecology and Sociobiology, 22, Feener, D.H. Jr & Brown, B.V. (1992) Reduced foraging of Solenopsis geminata (Hymenoptera: Formicidae) in the presence of parasitic Pseudacteon spp. (Diptera: Phoridae). Annals of the Entomological Society of America, 85, Folgarait, P.J. & Gilbert, L.E. (1999) Phorid parasitoids affect foraging activity of Solenopsis richteri underdifferent availability of food in Argentina. Ecological Entomology, 24, Gilbert, L.E. & Morrison, L.W. (1997) Patterns of host specificity in Pseudacteon parasitoid flies (Diptera, Phoridae) that attack Solenopsis fire ants (Hymenoptera, Formicidae). Environmental Entomology, 26, Gotelli, N.J. & Arnett, A.E. (2) Biogeographic effects of red fire ant invasion. Ecology Letters, 3, Hölldobler, B. & Wilson, E.O. (199) The Ants. Belknap, Cambridge. Holtcamp, W., Grant, W.N. & Vinson, S.B. (1997) Patch use under predation hazard: effect of the red imported fire ant on deer mouse foraging behaviour. Ecology, 78, Holway, D.A., Lach, L., Suarez, A.V., Tsutsui, N.D. & Case, T.J. (22a) The causes and consequences of ant invasions. Annual Review of Ecology and Systematics, 33, Holway, D.A., Suarez, A.V. & Case, T.J. (22b) Role of abiotic factors in governing susceptibility to invasion: a test with Argentine ants. Ecology, 83, Human, K.G. & Gordon, D.M. (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia, 15, Human, K.G. & Gordon, D.M. (1997) Effects of Argentine ants on invertebrate biodiversity in northern California. Conservation Biology, 11, LeBrun, E.G. & Feener, D.H. Jr (22) Linked indirect effects in ant phorid interactions: impacts on ant assemblage structure. Oecologia, 133, Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M. & Bazzaz, F.A. (2) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications, 1, Mehdiabadi, N.J. & Gilbert, L.E. (22) Colony-level impacts of parasitoid flies on fire ants. Proceedings of the Royal Society of London, Series B, 269, Mooney, H.A. & Cleland, E.E. (21) The evolutionary impact of invasive species. Proceedings of the National Academy of Sciences of the United States of America, 98, Morrison, L.W. (1999) Indirect effects of phorid fly parasitoids on the mechanisms of interspecific competition among ants. Oecologia, 121, Morrison, L.W. (2a) Biology of Pseudacteon (Diptera: Phoridae) ant parasitoids and their potential to control imported Solenopsis fire ants (Hymenoptera: Formicidae). Recent Research Developments in Entomology, 3, Morrison, L.W. (2b) Mechanisms of Pseudacteon parasitoid (Diptera: Phoridae) effects on exploitative and interference competition in host Solenopsis ants (Hymenoptera: Formicidae). Annals of the Entomological Society of America, 93, Morrison, L.W., Dall Aglio-Holvorcem, C.G. & Gilbert, L.E. (1997) Oviposition behaviourand development of Pseudacteon flies (Diptera: Phoridae), parasitoids of Solenopsis fire ants (Hymenoptera: Formicidae). Environmental Entomology, 26, Morrison, L.W., Kawazoe, E.A., Guerra, R. & Gilbert, L.E. (1999) Phenology and dispersal in Pseudacteon flies (Diptera: Phoridae), parasitoids of Solenopsis fire ants (Hymenoptera: Formicidae). Annals of the Entomological Society of America, 92, Orr, M.R., Seike, S.H., Benson, W.W. & Gilbert, L.E. (1995) Flies suppress fire ants. Nature, 373, Orr, M.R., Seike, S.H. & Gilbert, L.E. (1997) Foraging ecology and patterns of diversification in dipteran parasitoids of fire ants in south Brazil. Ecological Entomology, 22, Pesquero, M.A., Campiolo, S., Fowler, H.G. & Porter, S.D. (1996) Diurnal patterns of ovipositional activity in two Pseudacteon fly parasitoids (Diptera: Phoridae) of Solenopsis fire ants (Hymenoptera: Formicidae). Florida Entomologist, 79, Pimm, S.L. (1991) The Balance of Nature? Ecological Issues in the Conservation of Species and Communities. University of Chicago Press, Chicago, Illinois. Porter, S.D. (1988) Impact of temperature on colony growth and developmental rates of the ant, Solenopsis invicta. Journal of Insect Physiology, 34, Porter, S.D. & Alonso, L.E. (1999) Host specificity of fire ant decapitating flies (Diptera: Phoridae) in laboratory oviposition tests. Journal of Economic Entomology, 92, Porter, S.D., Pesquero, M.A., Campiolo, S. & Fowler, H.G. (1995b) Growth and development of Pseudacteon phorid fly maggots (Diptera, Phoridae) in the heads of Solenopsis fire ant workers (Hymenoptera, Formicidae). Environmental Entomology, 24, Porter, S.D. & Savignano, D.A. (199) Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology, 71, Porter, S.D. & Tschinkel, W.R. (1985) Fire ant polymorphism: the ergonomics of brood production. Behavioural Ecology and Sociobiology, 16, Porter, S.D., Vander Meer, R.K., Pesquero, M.A., Campiolo, S. & Fowler, H.G. (1995a) Solenopsis (Hymenoptera: Formicidae) fire ant reactions to attacks of Pseudacteon flies (Diptera: Phoridae) in southeastern Brazil. Annals of the Entomological Society of America, 88,

7 Effects of parasitoids on a host s competitor 627 Sanders, N.J., Gotelli, N.J., Heller, N.E. & Gordon, D.M. (23) Community disassembly by an invasive ant species. Proceedings of the National Academy of Sciences of the United States of America, 1, Simberloff, D., Schmitz, D.C. & Brown, T.C., eds (1997) Strangers in Paradise: Impact and Management of Nonindigenous Species in Florida. Island, Washington, DC. Sorenson, A.A., Busch, T.M. & Vinson, S.B. (1983) Behaviour of worker subcastes in the fire ant, Solenopsis invicta, in response to proteinaceous food. Physiological Entomology, 8, Suarez, A.V., Bolger, D.T. & Case, T.J. (1998) Effects of fragmentation and invasion on native ant communities in coastal southern California. Ecology, 79, Suarez, A.V., Richmond, J.Q. & Case, T.J. (2) Prey selection in horned lizards following the invasion of Argentine ants in southern California. Ecological Applications, 1, Thompson, L.C., Jones, D.B., Semevski, F.N. & Semenov, S.M. (1995) Fire ant economic impact: extending Arkansas survey results over the South. Proceedings of the Fifth International Pest Ant Symposia and the 1995 Annual Imported Fire Ant Conference, San Antonio, Texas (ed. by S. B. Vinson and B. M. Drees), pp Texas A & M University, College Station, Texas. Trager, J.C. (1991) A revision of the fire ants, Solenopsis geminata group (Hymenoptera: Formicidae: Myrmicinae). Journal of the New York Entomological Society, 99, Vinson, S.B. (1986) Economic Impact and Control of Social Insects. Praeger, New York. Vinson, S.B. (1997) Invasion of the red imported fire ant (Hymenoptera: Formicidae): spread, biology, and impact. American Entomology, 43, Vitousek, P.M., D Antonio, C.M., Loope, L.L. & Westbrooks, R. (1996) Biological invasions as global environmental change. American Scientist, 84, Ward, P.S. (1987) Distribution of the introduced Argentine ant (Iridomyrmex humilis) in natural habitats of the lower Sacramento Valley and its effects on the indigenous ant fauna. Hilgardia, 55, Williams, D.F. (1994) Exotic Ants: Biology, Impact, and Control of Introduced Species. Westview, Boulder, Colorado. Williams, R.N., Panaia, J.R., Gallo, D. & Whitcomb, W.H. (1973) Fire ants attacked by phorid flies. Florida Entomologist, 56, Winston, M.L. (1991) Killer Bees: the African Honey Bee in the Americas. Harvard University Press, Cambridge, Massachusetts. Wojcik, D.P., Allen, C.R., Brenner, R.J., Forys, E.A., Jouvenaz, D.P. & Lutz, R.S. (21) Red imported fire ants: impact on biodiversity. American Entomology, 47, Accepted 9 March 24