BIOLOGICAL CONTROL Field Studies of the Parasitic Solenopsis daguerrei (: Formicidae) on Fire in Argentina

1 1 2 L. A. CALCATERRA, J. A. BRIANO, AND D. F. WILLIAMS

Environ. Entomol. 28(1): 88Ð95 (1999) ABSTRACT The workerless parasitic ant Solenopsis daguerrei (Santschi) has been considered a potential candidate for biological control of imported Þre ants in the since the 1970s. We estimated the detrimental effects of S. daguerrei in Þre ant colonies from Argentina by comparing the composition of parasitized and nonparasitized Þeld colonies of the black imported Þre ant S. richteri Forel. We recorded mound density and volume, incidence of , number of queens per colony, queen weight, and presence and abundance of brood and sexuals. Also, we studied aspects of the parasiteÕs biology such as parasitization rates, presence of sexuals, abundance and weight of queens, and sex ratio. S. daguerrei occurred in 1.2Ð23.7% of the colonies at 21 collecting sites. The mound density at parasitized sites was signiÞcantly lower than in parasite-free sites (161 versus 239 mounds per hectare). Parasitized colonies had signiÞcantly fewer host queens than nonparasitized ones (2.9 versus 5.5 queens per colony). The percentage of colonies with worker brood was signiÞcantly lower (in fall) in parasitized than in nonparasitized colonies. Also, worker brood was signiÞcantly less abundant (in fall and spring) in parasitized colonies. A short delay in the production of sexual brood by the host was observed in parasitized colonies. These detrimental effects look promising but should be evaluated in the long-term and conÞrmed in other areas. A better understanding of the host and parasite is required to introduce S. daguerrei into the United States to control imported Þre ants.

KEY WORDS Solenopsis richteri, Solenopsis daguerrei, Þre ants, parasitic ants, colony composition, biological control

THE IMPORTED FIRE ants Solenopsis invicta Buren and S. similar manner to their own mother queen, whereas richteri Forel are major pests in the southeastern the parasite brood are reared by the host workers United States (Lofgren 1986). According to Porter et simultaneously with the host brood (Bruch 1930). al. (1997), their higher densities in the United States The presence of the parasite was surveyed in South might be, at least partially, the result of biological America (Silveira-Guido et al. 1962Ð1969, Briano et al. release from natural enemies present in their native 1997) and it appears that S. daguerrei has no speciÞc , where Þre ant populations are 4Ð7 preferences. It can be found in dry and wet times less abundant than in North America. This sug- environments, in different soil types and topography, gests that the importation of successful biological con- and in different plant communities. However, the par- trol agents of Þre ants should reduce the pest to levels asite has been found only in nests of Solenopsis sae- similar to those found in South America. vissima F. Smith complex such as S. richteri, S. The workerless parasitic ant Solenopsis daguerrei invicta, S. saevissima, and S. macdonaghi Santschi (Sil- (Santschi) (formerly Labauchena daguerrei) has been veira-Guido et al. 1973, Briano et al. 1997). considered a potential candidate for biological control Observations on the biology and behavior of S. da- of imported Þre ants in the United States since the guerrei were reported by Bruch (1930), Silveira-Guido 1970s. Jouvenaz (1990) and Wojcik (1990) reported et al. (1962Ð1969, 1973) and Briano et al. (1997). Ac- that this parasitic ant could be one of the most prom- cording to Bruch (1930), under laboratory conditions ising candidates among the for introduc- the parasite can kill the host queens by decapitation. tion into the United States. S. daguerrei, like the par- Silveira-Guido et al. (1965, 1973), however, found no asitic ant Teleutomyrmex schneideri Kutter and other evidence of decapitation, but reported that the para- species, is a permanent parasite because it spends its site inhibits egg production, especially the production entire life cycle in the nest of the host species (Ho¨ll- of host sexuals. In extreme cases this causes the col- dobler and Wilson 1990). S. daguerrei queens attach to lapse of the host ant colony. Yet, little is known about the host queens and Þre ant workers tend them in a the actual impact of this and other natural enemies on native South American Þre ant populations (Porter et al. 1997). The objectives of this study were to estimate 1 USDAÐARS South American Biological Control Laboratory, Bo- livar 1559 (1686) Hurlingham, Buenos Aires Province, Argentina. detrimental effects of S. daguerrei in native Argentine 2 USDAÐARS Center for Medical, Agricultural, and Veterinary Þre ant colonies and to study some aspects of the Entomology, P.O. Box 14565, Gainesville, FL 32604. parasiteÕs biology. February 1999 CALCATERRA ET AL.: FIELD STUDIES OF S. daguerrei 89

Materials and Methods males. Those colonies with no host queen were not included in the data for polygyny and number of Study Area. The study was conducted from May queens. The abundance of each caste or stage was 1996 (fall) to June 1997 (fall) at San Eladio, Buenos rated by using 3 categories: 0, none; 1, few; and 2, Aires Province (59Њ 10Ј W, 34Њ 45Ј S). This area was many. selected because it had the highest abundance (7.0%) Host queens were dissected and their spermatheca of S. daguerrei in South America (Briano et al. 1997). examined to conÞrm insemination. Colonies with only Њ The area has a mean annual temperature of 18.7 C 1 inseminated queen were considered as probable mo- Њ Ϫ Њ with extremes of 41 C (December) and 8 C (June), nogyne and colonies with Ͼ1 inseminated queen as an average of 57.5 d with frost per year (range, 30Ð81 polygyne. The live weight of 278 queens from 52 non- d), and an annual rainfall of 1,009 mm (10-yr records, parasitized and 138 queens from 34 parasitized colo- Ministerio de Asuntos Agrarios 1987Ð1996). Topo- nies was recorded. For comparison studies, the graphically, the area is ßat and the formation of tem- weights of queens in polygyne colonies were aver- porary puddles is common. The vegetation is composed aged. mainly of gramineae and is used for livestock grazing. Parasite Colony Composition. The presence and These natural pastures have not been cultivated for abundance of S. daguerrei multiple queens were re- the last few years. Annual crops have been introduced corded from 96 parasitized colonies excavated in the recently in the area. Þeld. Every queen (n ϭ 114) from 33 of these colonies Percentage of Parasitism and Mound Density. A was weighed. For comparison studies, the weights of total of 2,580 colonies of Þre ants (mainly S. richteri) parasite queens per host colony were also averaged. was examined by excavating and scattering them on We considered queens as those physogastric wingless the ground to detect the presence of adults or queens females or those found yoked to the host queens. The of the parasitic ant. The collecting sites were located presence of sexuals was monitored in the Þeld sea- in natural pastures on 5 ranches (San Mariano, sonally. Cheroga, Pylmaique´n, Santa Ca´ndida, and Santa Lu- In addition, 30 colonies of S. daguerrei collected cõ´a) where the parasite was found. The area of the from December 1995 to January 1997 in several local- 1⁄ pastures ranged from 3 to 30 ha. The density of Þre ant ities of Buenos Aires Province were sampled for sex colonies in each pasture was estimated in 3 transects ratio. In small colonies, all sexuals of the parasite were randomly located. Each transect was Ϸ300 m long by counted; and in large colonies, a sample of Ϸ150 sexu- 3 m wide (except in a couple of small pastures, where als was used. A total of 3,566 sexuals was counted. they were shortened to Ϸ100 m). All active mounds After examination in the laboratory, some of the found within the transects were counted. For the parasitized colonies were shipped to the quarantine purpose of this study, we considered each mound as a facilities of the USDAÐARS, Center for Medical, Ag- colony because mounds are fully functional units (Ma- ricultural, and Veterinary Entomology, Gainesville, com and Porter 1996). Mound density in the sites FL, for further research. Voucher specimens were where the parasite was present was compared with the kept at the USDAÐARS, South American Biological mound density of 53 parasite-free pastures surveyed in Control Laboratory and some were sent to the Museo 20 localities from November 1995 to April 1996 de La Plata, Paseo del Bosque, 1900 La Plata, Buenos (L.A.C., unpublished data). The localities were 40Ð Aires Province, Argentina. 150 km apart from San Eladio and were similar in Statistical Analysis. Statistical analysis to compare habitat, land use, and climate. In each pasture the the parasitized and nonparasitized colonies was done density of Þre ants was estimated in 3 transects ran- with Minitab Statistical Software (1991). A 2-sample domly located as above. t-test was used to compare mound density, volumes of Mound Volume. We measured the height, length, mounds, and weight of host and parasite queens. Chi- and width of the mounds of 62 parasitized and 84 square tests were used to analyze the proportion of nonparasitized colonies of S. richteri. All parasitized polygyny, plus presence of sexuals and brood. MannÐ colonies found within the pastures were measured. Whitney U tests were used to compare the number of Nonparasitized colonies were selected within the queens per colony and the abundance of sexuals and transects mentioned above using a random number brood. We used linear regression to relate the number table. Mound volume (V) was calculated using the of queens per colony with queen weight. The means Ϯ formula for half a spheroid, V ϭ 2⁄3 ␲abc, where a is the 1 SE are reported. length/2, b is the width/2, and c is the height (Porter 1992). Host Colony Composition. The S. richteri colony Results and Discussion composition was compared between 149 nonparasit- Percentage of Parasitism and Mound Density. Of ized and 140 parasitized colonies. After excavation, the the 2,580 colonies of S. richteri examined within the 21 colonies were put in 10-liter buckets dusted with talc collecting sites from the area of San Eladio, we found and brought to the laboratory. The colonies were S. daguerrei in 131 colonies (5.1%). The percentage of separated from the soil by ßotation (Banks et al. 1981), parasitism in the different pastures ranged from 1.2 to put in plastic rearing trays (40 by 30 by 15 cm), and 23.7% of the colonies (average 4.6%) (Table 1). Be- examined for polygyny, number of queens per colony, cause of the low parasitation rates in most of the worker brood, sexual brood, and winged females and pastures, a large number of host colonies were exam- 90 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 1

Table 1. Abundance of S. daguerrei in San Eladio, Argentina density is signiÞcantly lower than the one observed in nonparasitized sites, 239 Ϯ 15 mounds per hectare No. of Colonies Collecting No. of (range, 78Ð600) (t ϭ 3.74, df ϭ 61, P Ͻ 0.001). How- colonies parasitized site no. mounds/ha examined ever, other potential sources of variation in the density No. % of Þre ants colonies such as topography, soil type, and 1 44 35 1 2.9 presence of other natural enemies were not included 2 70 58 1 1.7 in this study. 3 89 60 1 1.7 4 111 50 1 2.0 Briano et al. (1995) reported densities of 120Ð162 5 122 277 39 14.1 colonies per hectare at Saladillo, Buenos Aires Prov- 6 122 50 1 2.0 ince, where S. richteri colonies were highly infected 7 122 53 1 1.9 with the microsporidium, Thelohania solenopsae Knell, 8 122 38 9 23.7 9 144 109 3 2.7 Allen & Hazard, (Microsporida: Thelohaniidae). The 10 161 125 9 7.2 presence of S. daguerrei, however, was very low 11 161 75 2 2.7 (1.4%). 12 167 240 3 1.2 The mound densities recorded in Argentina are 13 167 140 3 1.8 14 170 107 3 2.8 much lower than the ones reported by Porter et al. 15 189 130 5 3.8 (1991, 1992) for polygyne populations of S. invicta in 16 200 105 2 1.9 the United States (544Ð680 mounds per hectare); and 17 200 205 12 5.8 higher than the densities reported by Porter et al. 18 222 275 22 8.0 19 233 102 5 4.9 (1992) for probable monogyne populations of S. in- 20 237 74 1 1.3 victa in (27 mounds per hectare). However, 21 333 272 9 3.3 comparisons of Þre ant densities are of relative value Total or range 44Ð333 2,580 131 5.1 because the studies were conduced under different Avg 161 122.9 6.2 4.6 (roadside versus pasture), land use, and sam- pling methods. ined to obtain the required number of parasitized The mean percentage of parasitism was 3.5% in sites colonies for comparison studies. with high mound density (above the mean), whereas The high variation observed in the parasitism rate in sites with low mound density (below the mean) it among the pastures surveyed (1.2Ð23.7%) might be the was 5.7%. This suggests an inverse relationship be- result of the population dynamics of the parasite, tween mound density and parasitization levels, but it which showed a contagious distribution. We speculate was not signiÞcant (r2 ϭ 0.04: F ϭ 0.08; df ϭ 1, 19; P ϭ that this might be explained by the fact that a single 0.777). The effect of S. daguerrei on the density of the polygyne colony occupies several interconnected host colonies should be evaluated over the long-term. nests, through which the parasite could disperse easily Even small reductions in the host population levels as brood or adult. Further Þeld work is needed to test could be biologically important. this assumption. Differences in land use (history of the Mound Volume. The volume of parasitized colonies pastures) could also increase variation in the density was 6.0 Ϯ 0.5 liters (range, 0.3Ð21.3), which is similar of the host and parasite. to the mound volume of nonparasitized colonies, 5.9 Ϯ The highest parasitization rate (23.7%) in San 0.5 liters (range, 0.5Ð34.6) (t ϭ 0.08, df ϭ 144, P ϭ Eladio is smaller than one reported by Silveira-Guido 0.94). In previous surveys in different areas of Argen- et al. (1973) in the area of Las Flores (38.4%) Buenos tina and Uruguay (L.A.C., unpublished data), we Aires Province, type locality of S. daguerrei. However, found similar volumes for parasitized colonies (5.2 Ϯ in a recent study, Briano et al. (1997) did not detect 0.9 liters; range, 0.9Ð18.8) (t ϭ 0.78, df ϭ 85, P ϭ 0.439). the presence of the parasite in that area. The reason These volumes are smaller than those reported by for this remains uncertain. Briano et al. (1995) for S. richteri in Saladillo and Las Although the low presence of S. daguerrei in San Flores (10.3 Ϯ 1.2 and 18.7 Ϯ 1.7 liters), but similar to Eladio is discouraging, it might not be a good indicator the volumes reported by Porter et al. (1997) for So- of its ecological impact on its host. Feener (1981) lenopsis spp. in South America (5.1 liters), and for S. found that the competitive ability of the ant Pheidole invicta in North America (7.4 liters). However, be- dentata Mayr dramatically decreased against its enemy cause the mound size varies greatly with different soil Solenopsis texana Emery because of the effect of pho- types, soil moisture, vegetation, and sampling habitat rid ßies, whose parasitism rate was Ͻ5%. If this is also (Lofgren et al. 1975), comparisons are also of relative the case for S. daguerrei remains unclear and should be value. conÞrmed. Once in a new habitat (e.g., the United The size distribution of mounds in nonparasitized States), the establishment and dispersal of S. daguerrei and parasitized colonies was similar. Around 30% of will be difÞcult to predict, as has been the case for most the mounds had a volume up to 3.5 liters, 40% of the natural enemies artiÞcially introduced for biological mounds were between 3.6 and 7.0 liters, and the re- control. Eventually, the prevalence of this parasite maining 30% were Ͼ7.0 liters (Fig. 1). could be increased as soon as its dispersal mechanism When all colonies (parasitized and nonparasitized) is understood. were considered, the mound volumes of monogyne The mound density at parasitized sites was 161 Ϯ 14 and polygyne colonies were similar (5.2 Ϯ 0.5 liters; mounds per hectare (range, 44Ð333; Table 1). This range, 0.3Ð16.5 versus 5.3 Ϯ 0.6 liters; range, 0.5Ð21.3, February 1999 CALCATERRA ET AL.: FIELD STUDIES OF S. daguerrei 91

Fig. 1. Mound size distribution of parasitized and nonparasitized colonies of S. richteri (n ϭ 146) in San Eladio, Argentina. respectively; t ϭϪ0.1, df ϭ 115, P ϭ 0.92). Briano et lack of aggression toward polygyne conspeciÞcs. Be- al. (1995) reported similar volumes in Saladillo, 6.2 and cause polygyne colonies are less territorial, they use 5.8 liters, in monogyne and polygyne colonies respec- available resources better, resulting in larger Þre ant tively. populations. This lower aggressiveness of polygyne Host Colony Composition. Polygyny Approximately populations permits the integration of fertilized young half of the S. richteri colonies examined in San Eladio queens into colonies of their own species and would was polygyne. The presence of multiple queens in also allow the parasite to establish more easily than in nonparasitized colonies was 57.6%, which was not sig- monogyne populations (Buschinger 1986). niÞcantly different from the 43.7% found in parasitized Porter et al. (1992) suggested that the occurrence of colonies (␹2 ϭ 3.610, df ϭ 1, P Ͼ 0.05, n ϭ 188). These polygyny might be linked to the absence of biological percentages are consistent with the high incidence of control agents. Moreover, Keller (1995) mentioned polygyny reported by Briano et al. (1995) in Þre ant that 1 potential advantage of polygyny is an increased populations in Argentina. They found polygyny in genetic variability and lower susceptibility to para- 25.7Ð41.5% of the S. richteri colonies in Saladillo and sites. Our data contrast with PorterÕs and KellerÕs hy- in 46% of the colonies in Las Flores. According to potheses because we found a high incidence of po- Porter (1992) and Porter et al. (1991, 1992), polygyny lygyny (56.7%) in parasitized populations. Why is also common in the southern United States (15Ð54% polygyny is so common in San Eladio and other areas of the sampled sites for S. invicta). Porter et al. (1992) of Argentina is unknown. However, according to Ho¨ll- reported 67% of the colonies of S. invicta at polygyne dobler and Wilson (1977), ant populations may sites were conÞrmed as polygyne. S. invicta has not change from the monogyne to the polygyne form (and been reported in the polygyne form in Brazil (Jouve- vice versa) depending on environmental conditions. naz et al. 1989; Porter et al. 1992, 1997). Moreover, according to Buschinger (1986) and Ho¨ll- Monogyne and polygyne colonies of S. richteri co- dobler and Wilson (1990), host polygyny is a sufÞ- existed in the sites surveyed in San Eladio. We did not ciently frequent phenomenon in ants to represent a Þnd any exclusively monogyne sites, which contrast condition from which a permanent parasite such as S. with Jouvenaz et al. (1989) who reported that 25 of 33 daguerrei may have evolved. sites (76%) had only monogyne colonies of S. richteri Number of Queens per Colony. The mean number of in Argentina. Þre ant queens per colony was signiÞcantly lower in According to Macom and Porter (1996), an impor- parasitized colonies (2.9 Ϯ 0.5; range, 1Ð40) than in tant reason for the high incidence of polygyny is the nonparasitized colonies (5.5 Ϯ 2.0; range, 1Ð180) (U ϭ 92 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 1

Table 2. Percentage of parasitized and nonparasitized S. richteri colonies with brood and sexuals from 1 May 1996 to 28 May 1997 in the area of San Eladio, Argentina

Presence of Late fall 1996a Winter 1996b Spring 1996c Summer 1996Ð1997d Early fall 1997e Parasitized colonies (n ϭ 140) Worker brood 5.7% 11.1% 93.9% 100.0% 68.0% Sexual brood 0% 0% 36.4% 15.0% 0% Winged females 7.5% 22.2% 6.1% 20.0% 24.0% Winged males 1.9% 11.1% 3.0% 10.0% 20.0% No. of colonies examined 53 9 33 20 25 Nonparasitized colonies (n ϭ 149) Worker brood 25.0% 17.4% 100.0% 100.0% 72.7% Sexual brood 0% 0% 21.7% 10.0% 0% Winged females 8.3% 4.3% 8.7% 20.0% 18.2% Winged males 6.2% 4.3% 8.7% 10.0% 13.6% No. of colonies examined 48 46 23 10 22

a Late fall, 1 MayÐ20 June. b Winter, 21 JuneÐ20 September. c Spring, 21 SeptemberÐ20 December. d Summer, 21 DecemberÐ20 March. e Early fall, 21 MarchÐ28 May.

8,272.5; n1 ϭ 96, n2 ϭ 92; P Ͻ 0.05). This reduction of inhibits the growth of its host by maximizing the pro- queen number (47%) in parasitized colonies could be duction of parasite queens and males. an important detrimental effect of S. daguerrei on Þre Sexual Brood. The presence of S. daguerrei did not ant populations. The magnitude of this effect could be signiÞcantly affect Þre ant sexual brood production. of enormous value in biological control of the Þre ant. The percentage of colonies with sexual brood was Additional laboratory tests are needed to conÞrm 36.4% (spring) and 15.0% (summer) for parasitized BruchÕs hypothesis (1930) of decapitation. We spec- colonies, which is similar to the 21.7% (spring) and ulate that the parasite might increase the number of 10.0% (summer) for nonparasitized colonies (Table monogyne colonies in S. richteri populations because 2). We found no differences in sexual brood abun- of the detrimental effect on the number of host dance. queens. This might be associated with the lower den- We did not Þnd sexual brood in the fall and winter, sities at parasitized sites and must be investigated. presumably because of the low temperatures. We ob- Worker Brood. The percentage of colonies with served a short delay in the production of sexual brood worker brood during the study ranged between 5.7% in parasitized colonies (October to mid February) (late fall 1996) and 100% (summer) for parasitized compared with nonparasitized colonies (September colonies and 17.4% (winter) and 100% (spring and to mid February). summer) for nonparasitized colonies (Table 2). We The unexpected larger percentage of parasitized observed seasonal differences in the worker brood colonies with sexual brood, although not signiÞcant, production between parasitized and nonparasitized may be explained by the fact that more queens were colonies only in late fall and spring of 1996. In late fall found in nonparasitized colonies, which, according to of 1996, the percentage of colonies with worker brood Vargo and Fletcher (1987), could inhibit the produc- was 5.7% for parasitized colonies and 25.0% for non- 2 tion of sexuals. parasitized colonies (␹ ϭ 7.45, df ϭ 1, P Ͻ 0.01). Worker brood were less abundant in parasitized than Winged Females and Males. Winged forms were ob- served throughout the study period in parasitized and in nonparasitized colonies (U ϭ 2,452.5; n1 ϭ 53, n2 ϭ 48; P Ͻ 0.01). In spring, the percentage of parasitized nonparasitized S. richteri nests in similar frequencies and nonparasitized colonies with worker brood were and abundances. The presence of winged females similar, 93.9 versus 100%, respectively (␹2 ϭ 1.45, df ϭ ranged between 6.1% (spring) and 24.0% (early fall 1, P Ͼ 0.1); however, worker brood were less abundant 1997) for parasitized colonies, and between 4.3% in parasitized than in nonparasitized colonies (U ϭ (winter) and 20.0% (summer) for nonparasitized col- onies (Table 2). 795.0; n1 ϭ 33, n2 ϭ 23; P Ͻ 0.005). In parasitized colonies, we found worker brood in In parasitized colonies, we found females in May, May, August, October, November, and December of June, July, and October of 1996, and in January, Feb- 1996, and in January, February, March, April, and May ruary, April, and May of 1997 (in September of 1996, of 1997. In nonparasitized colonies, we found worker we did not Þnd parasitized colonies). In nonparasit- brood in every month from May 1996 to May 1997. The ized colonies, we found females from May 1996 to lower production of worker brood in parasitized col- January 1997, and from April to May 1997. onies in late fall and spring of 1996 suggests a detri- Adult males were less common than females in both mental effect of the parasite on the seasonal growth of parasitized and nonparasitized colonies. The percent- the host colonies. This would be consistent with Wil- age of colonies with adult males ranged between 1.9% son (1971), who reported that an inquiline species (late fall 1996) and 20.0% (early fall 1997) for para- February 1999 CALCATERRA ET AL.: FIELD STUDIES OF S. daguerrei 93

Fig. 2. Seasonal presence of males, females, and queens of S. daguerrei in Þre ant colonies of San Eladio, Argentina. sitized colonies, and between 4.3% (winter) and 13.6% queens per colony was 3.8 Ϯ 0.7 (range, 1Ð64). How- (early fall 1997) for nonparasitized colonies (Table 2). ever, the mean number of parasite queens was higher In parasitized colonies, we found males in June, in polygyne Þre ant colonies than in monogyne ones July, and October of 1996, and in January and April of (6.2 Ϯ 1.7; range, 1Ð64 versus 2.1 Ϯ 0.2; range, 1Ð10,

1997; whereas in nonparasitized colonies, we found respectively; U ϭ 1,744.5; n1 ϭ 49, n2 ϭ 39; P Ͻ 0.001). them in May, June, July, and October of 1996, and in In parasitized colonies maintained in the laboratory January, April, and May of 1997. under standard rearing procedures (Banks et al. 1981), The presence of sexuals of the host in parasitized we observed the emergence of new parasite queens colonies is in contrast with the Þndings of Silveira- (L.A.C., unpublished data). This agrees with Silveira- Guido et al. (1973), who did not observe them in Guido et al. (1973), who reported that sexuals of S. parasitized colonies. They assumed that the presence daguerrei mate inside the mound, at the exit-holes, or of the parasite inhibited the production of Þre ant on top of mounds, and with Wilson (1971), who stated sexuals, but this was not conÞrmed in our study. that in rare ant species such as S. daguerrei, there is no Weight of Host Queens. queen weights were evidence of with members of other colonies similar in parasitized and nonparasitized colonies, (exogamy). According to Wilson (1971) endogamy both in polygyne (14.9 versus 14.8 mg; t ϭ 0.1, df ϭ 44, (or inbreeding) in rare and isolated species would P ϭ 0.88) and monogyne colonies (18.5 versus 19.0 mg; ensure that many queens will be inseminated in each t ϭ 0.4, df ϭ 44, P ϭ 0.70). Queens from parasitized colony and that the loss of virgin reproductive females monogyne colonies were heavier than queens from will be reduced. We believe that, probably because of parasitized polygyne colonies (18.5 versus 14.9 mg; t ϭ their small size, S. daguerrei sexuals are not good ßyers. 3.4, df ϭ 32, P Ͻ 0.005). As expected, queens from We have never observed them ßying out of their host nonparasitized monogyne colonies were heavier than colony in the Þeld. However, in parasitized colonies queens from nonparasitized polygyne colonies (19.0 maintained in the laboratory, we have observed very versus 14.8 mg; t ϭ 4.1, df ϭ 49, P Ͻ 0.001). short and erratic ßights of female parasites, never The weights of nonparasitized polygyne queens of males. The dispersal mechanisms of this parasite are S. richteri were similar to those reported by Porter currently under study. (1992) for S. invicta (14.4 mg). However, the average Presence of Sexuals. The presence of males and fe- weight of nonparasitized monogyne queens was Ϸ5 males of S. daguerrei was seasonal during the study mg lower. We found physogastric queens (Ͼ17 mg) period (Fig. 2). We found males in MayÐJune of 1996 from August to early December (late winterÐspring). (fall) and from December 1996 to March 1997 (sum- Although we did not Þnd evidence to show that S. mer); females from May to August 1996 (fallÐwinter) daguerrei reduces the weight of individual host and from December 1996 to May 1997 (summerÐfall). queens, any detrimental effect could be masked by the Females were observed in the colonies for 2 mo more fact that fewer queens (and consequently heavier than males during both 1996 and 1997, but females and queens) are associated with the presence of the par- males disappeared 3 mo earlier in 1997 than in 1996. asite. As expected according to Vargo and Fletcher This was probably due to a severe drought during the (1989) for S. invicta, queen weight was inversely re- warm season of 1996Ð1997. We did not Þnd sexuals of lated to the number of queens per colony both in S. daguerrei from September to November 1996 nonparasitized (r ϭϪ0.53; F ϭ 8.77; df ϭ 1, 23; P Ͻ (spring) and in June of 1997 (fall) we found only 0.01) and parasitized colonies (r ϭϪ0.67; F ϭ 13.91; queens. df ϭ 1, 17; P Ͻ 0.005). According to Silveira-Guido et al. (1973), S. daguer- Parasite Colony Composition. Polygyny and Num- rei has 2 well-deÞned oviposition periods in this lati- ber of Queens. Based on our study, polygyny seems to tude, the 1st from July to October (winterÐspring) and be the most common form of S. daguerrei in San the 2nd from December to March (summer). Our Eladio. We found multiple queens in 64.9% of the observations contrast with this, and indicate that S. colonies examined. This agrees with Buschinger daguerrei starts an oviposition cycle only at the be- (1986), who stated that most interspeciÞc inquilines, ginning of the warm season (probably in October) and their hosts, are polygyne. The mean number of around 2 mo before the appearance of the 1st sexuals 94 ENVIRONMENTAL ENTOMOLOGY Vol. 28, no. 1

(December). The end of the oviposition cycle remains Acknowledgments uncertain but it is probably at the end of the warm We thank Anne-Marie Callcott (USDAÐAPHIS, Gulfport, season (May). The period in which the sexuals stay in MS), Dan Wojcik, Weste Osbrink (USDAÐARS, Center for the colony after emergence has not been determined. Medical, Agricultural, and Veterinary Entomology, Gaines- We observed that sexuals of the host and the par- ville, FL), and Willie Cabrera (USDAÐARS, South American asite emerged simultaneously within the colony. This Biological Control Laboratory, Hurlingham, Argentina) for is in contrast with Bourke (1991) who speculated that reviewing the manuscript. We are grateful to Milena Braun female larvae of parasitic species mask their sexuality for her invaluable Þeld assistance. We thank also the ranch- ers, especially Luis Arau´ , for permitting us to work on their by being small and by acting as worker larvae. They properties. The surveys and Þeld studies were partially sup- would emerge with the workers and before the host ported by funds provided by a subcontract of USDAÐAPHIS sexuals to avoid gyne suppression. Clearly, further grant 95-8100-0229 to the University of Arkansas-Monticello. research on this and other parasitic ant species is required to determine if a reproductive isolation mechanism, such as temporal or spatial separation of References Cited mating episodes, gave origin to inquiline species such Banks, W. A., C. S. Lofgren, D. P. Jouvenaz, C. E. Stringer, as S. daguerrei. P. M. Bishop, D. F. Williams, D. P. Wojcik, and B. M. Weight of Queens. The parasite queens were 10 Glancey. 1981. Techniques for collecting, rearing and times lighter than the average host queen. The mean handling imported Þre ants. U.S. Dep. Agric. Sci. Educ. weight of queens of S. daguerrei was 1.9 Ϯ 0.1 mg Admin. Adv. Agric. Tech. AAT-S-21. (range, 0.6Ð3.2) and no differences were observed Bourke, A.F.G. 1991. Alternative adaptations, sympatric Ϯ speciation, and the evolution of parasitic, inquiline ants. between monogyne and polygyne host colonies (2.2 Biol. J. Linn. Soc. 43: 157Ð178. 0.1 versus 1.9 Ϯ 0.1 mg, respectively; t ϭ 1.66, df ϭ 31, Briano, J. A., R. S. Patterson, and H. A. Cordo. 1995. Rela- P ϭ 0.11). We found, as in the host, physogastric tionship between colony size of Solenopsis richteri (Hy- parasite queens (Ͼ1.7 mg) from September to early menoptera: Formicidae) and infection with Thelohania December (spring). solenopsae (Microsporida: Thelohaniidae) in Argentina. Sex Ratio. In the majority of colonies sampled, fe- J. Econ. Entomol. 88: 1233Ð1237. Briano, J. A., L. A. Calcaterra, D. P. Wojcik, D. F. Williams, males were more numerous than males. The ratio of W. A. Banks, and R. S. Patterson. 1997. Abundance of males to females was Ϸ1:3 (23.2Ð76.8%), however, the parasitic ant Solenopsis daguerrei (Hymenoptera: For- high variation was observed among the colonies. Per- micidae) in South America, a potential candidate for the centages of males within a colony ranged from 0 to biological control of the red imported Þre ant in the 95.3%, and percentages of females ranged from 4.6 to United States. Environ. Entomol. 26: 1143Ð1148. 100%. The sex ratio reported here agrees with Silveira- Bruch, C. 1930. Notas preliminares acerca de Labauchena daguerrei Santschi. Rev. Soc. Entomol. Argent. 3: 73Ð82 Guido et al. (1963Ð1964), who stated that the males (plates 1 and 2). constitute 25% of the population of S. daguerrei. Buschinger, A. 1986. Evolution of social parasitism in ants. We conclude that the reduction in the host queen Trends Ecol. Evol. 1: 155Ð160. number observed in parasitized colonies is a major Feener, D. H., Jr. 1981. Competition between ant species: factor in favor of S. daguerrei as a potential biological outcome controlled by parasitic ßies. Science (Wash. control organism for Þre ants. The biological impact of D.C.) 214: 815Ð817. Ho¨lldobler, B., and E. O. Wilson. 1977. The number of this detrimental effect should be evaluated over a queens: an important trait in ant evolution. Naturwissen- longer period in large Þre ant populations. The Þnding schaften 64: 8Ð15. of lower densities of Þre ants in parasitized pastures Ho¨lldobler, B., and E. O. Wilson. 1990. The ants. Belknap, compared with nonparasitized ones looks very Cambridge, MA. promising but needs to be studied in other areas to Jouvenaz, D. P. 1990. Approaches to biological control of conÞrm if the sole presence of the parasite was Þre ants in the Unites States, pp. 620Ð627. In R. K. Vander Meer, K. Jaffe, and A. Ceden˜ o [eds.], Applied myrme- responsible for this reduction. In addition, the lower cology: a world perspective. Westview, Boulder, CO. production of S. richteri worker brood found in fall Jouvenaz, D. P., D. P. Wojcik, and R. K. Vander Meer. 1989. and spring and the delay in the presence of sexual First observation of polygyny in Þre ants, Solenopsis spp., brood in parasitized colonies might provide addi- in South America. Psyche 96: 161Ð165. tional evidence of detrimental effects of S. daguerrei Keller, L. 1995. Parasites, worker , and queen against Þre ants; the magnitude of these effects number in social . Am. Nat. 145: 842Ð847. Lofgren, C. S. 1986. History of imported Þre ants in the needs to be determined. United States, pp. 36Ð47. In. C. S. Lofgren and R. K. The search for other sites in South America with Vander Meer [eds.], Fire ants and leaf-cutting ants: bi- high densities of this parasite should be intensiÞed to ology and management. Westview, Boulder, CO. replicate Þndings, to conduct additional Þeld studies, Lofgren, C. S., W. A. Banks, and B. M. Glancey. 1975. Bi- and to monitor the host-parasite relationship over a ology and control of imported Þre ants. Annu. Rev. En- long period. A better understanding of the population tomol. 20: 1Ð30. Macom, T. E., and S. D. Porter. 1996. Comparison of poly- dynamics of the host and parasite is required to in- gyne and monogyne red imported Þre ant (Hymenop- troduce S. daguerrei into the United States to control tera: Formicidae) population densities. Ann. Entomol. imported Þre ants. Soc. Am. 89: 535Ð543. February 1999 CALCATERRA ET AL.: FIELD STUDIES OF S. daguerrei 95

Ministerio de Asuntos Agrarios. 1996. Informe Agrometeo- enemies of ants. First, second, and Þnal reports. Entomol. rolo´gico. Estac. Exp. Mercedes II- XI: 1Ð6. Sect., Centro de Investigaciones en Fruticultura, Horti- Minitab Statistical Software. 1991. Reference manual, re- cultura y Vitivinicultura, Ministerio de Ganaderõ´a y Ag- lease 8. Minitab, State College, PA. ricultura, Montevideo, Uruguay. Porter, S. D. 1992. Frequency and distribution of polygyne Silveira-Guido, A., J. Carbonell, and C. Crisci. 1973. Ani- Þre ants (Hymenoptera: Formicidae) in Florida. Fla. En- mals associated with the Solenopsis (Fire ants) complex, tomol. 75: 248Ð257. with special reference to Labauchena daguerrei. Proc. Tall Porter, S. D., A. Bhatkar, R. Mulder, S. B. Vinson, and D. J. Timbers Conf. Ecol. Anim. Control Habitat. Manage. 4: Clair. 1991. Distribution and density of polygyne Þre 41Ð52. ants (Hymenoptera: Formicidae) in Texas. J. Econ. En- Vargo, E. L., and D.J.C. Fletcher. 1987. Effect of queen tomol. 84: 866Ð874. number on the production of sexuals in natural popula- Porter, S. D., H. G. Fowler, and W. P. Mackay. 1992. Fire ant mound densities in the United States and Brazil (Hy- tions of the Þre ant, Solenopsis invicta. Physiol. Entomol. menoptera: Formicidae). J. Econ. Entomol. 85: 1154Ð 12: 109Ð116. 1161. Vargo, E. L., and D.J.C. Fletcher. 1989. On the relationship Porter, S. D., D. F. Williams, R. S. Patterson, and H. G. between queen number and fecundity in polygyne col- Fowler. 1997. Intercontinental differences in the abun- onies of the Þre ant S. invicta. Physiol. Entomol. 14: 223Ð dance of Solenopsis Þre ants (Hymenoptera: Formicidae): 232. escape from natural enemies? Environ. Entomol 26: 373Ð Wilson, E. O. 1971. The societies. Belknap, Cam- 384. bridge, MA. Silveira-Guido, A., P. San Martı´n, C. Crisci-Pisano, and J. Car- Wojcik, D. P. 1990. Behavioral interactions of Þre ants and bonell-Bruhn. 1962–1965. Investigations on the biology their parasites, predators and inquilines, pp. 329Ð344. In and biological control of the Þre ant Solenopsis saevissima R. K. Vander Meer, K. Jaffe, and A. Ceden˜ o [eds.], Ap- richteri Forel, in Uruguay. First, second, third, and Þnal plied myrmecology: a world perspective. Westview, Boul- reports. Departamento de Sanidad Vegetal, Facultad de der, CO. Agronomõ´a, Universidad de la Repu´ blica, Montevideo, Uruguay. Silveira-Guido, A., J. Carbonell-Bruhn, C. Crisci-Pisano, and Received for publication 19 February 1998; accepted 27 Briozzo-Beltrame. 1967–1969. Investigations on natural August 1998.