Geographical transition zone of Solenopsis fire ants (Hymenoptera: Formicidae) and Pseudacteon fly parasitoids (Diptera: Phoridae) in the state of São Paulo, Brazil

ECOLOGY, BEHAVIOR AND BIONOMICS

Geographical transition zone of Solenopsis fire ants (Hymenoptera: Formicidae) and Pseudacteon fly parasitoids (Diptera: Phoridae) in the state of São Paulo, Brazil

MA Pesquero^I; AMPM Dias^II

^IUniv Estadual de Goiás, UnU de Morrinhos, Morrinhos, GO, Brasil

^IIUniv Federal de São Carlos, Depto de Ecologia e Biologia Evolutiva, São Carlos, SP, Brasil

^{Correspondence}

ABSTRACT

Solenopsis saevissima (Smith) and Solenopsis invicta Buren are the most abundant and widely distributed fire ants in Brazil. The occurrence of the two fire ant species and of their parasitoids Pseudacteon spp. is described for a climatic and phytophysiognomic transition area in the state of São Paulo. Both fire ant species have a parapatric distribution, apparently determined by the climate: S. saevissima predominates in the north part of São Paulo (Aw climate), while S. invicta in the south (Cfa climate). A sympatric area is observed between the latitudes 21ºS and 23ºS. Two different communities of parasitic decapitating flies were associated with S. saevissima in the north and with S. invicta in the south, with a sympatric area in the municipality of São Carlos (21º58'S 47º53'W). The possible causes of this biogeographic pattern are discussed. Preference tests with Pseudacteon flies challenge the association of P. litoralis Borgmeier, P. curvatus Borgmeier, P. wasmanni Schmitz, P. pradei Borgmeier and P. obtusus Borgmeier with S. saevissima, and P. dentiger Borgmeier, P. disneyi Pesquero and P. lenkoi Borgmeier & Prado with S. invicta.

Keywords: Host selection, community, biological control

Introduction

Previous research has resulted in considerable knowledge about the taxonomy and geographic distribution of Pseudacteon decapitating flies in South America (Patrock et al 2009, Plowes et al 2009). Due to the high species richness of fire ants and the natural occurrence of parasitoids in South America, the host specificity is an important aspect to be considered when selecting natural enemies for fire ant biological control in the US (Vazquez et al 2004, Folgarait et al 2005b). Moreover, the ecological differentiation among parasitoid species such as daily activity (Pesquero et al 1996, Folgarait et al 2007a), attack place (Pesquero et al 1993, Orr et al 1997, Folgarait et al 2007b) and host size (Williams & Banks 1987, Campiolo et al 1994, Morrison et al 1997) has also been demonstrated to be important in species composition of local communities.

Solenopsis saevissima (Smith) and S. invicta Buren are the most common fire ants species in Brazil. Solenopsis saevissima occupies a large central area where the Brazilian savannah dominates, extending to the north, northeast and southeast regions of Brazil (Ross et al 2010). Solenopsis invicta also has a wide distribution, including Paraguay, a great extension in Bolivia, in northeastern Argentina, north of Uruguay and a north-south band of Brazil that goes from the state of Rondônia to the state of Rio Grande do Sul. Both S. invicta and S. saevissima are parapatric in Brazil, with known zones of contact in the states of Mato Grosso do Sul, São Paulo and Paraná (Porter et al 1992, MacKay et al 1994, Shoemaker et al 2006).

Of the 36 described Pseudacteon species that parasitize fire ants in the Neotropical region, 19 are associated with S. saevissima and S. invicta in South America, and 16 are listed as common to both species of fire ants (Patrock et al 2009). However, 11 of these species have ranges that are mostly limited to one species or another. Only five species of parasitoids (P. borgmeieri Schmitz, P. cultellatus Borgmeier, P. nudicornis Borgmeier, P. solenopsidis Schmitz and P. tricuspis Borgmeier) have ranges that broadly overlap with both fire ant species (Patrock et al 2009). Furthermore, the oviscape of P. nudicornis, P. cultellatus, and P. tricuspis shows intraspecific variation (Porter & Pesquero 2001), suggesting the occurrence of populations in process of reproductive isolation. Here we describe the occurrence of Pseudacteon parasitoid species and their fire ant hosts in a transition zone between two different described communities for Brazil (Pesquero 1997). We have also conducted tests to determine the preference of Pseudacteon species for S. saevissima and S. invicta in the field.

Material and Methods

Field work was carried out in six municipalities situated in the state of São Paulo: Anhembi (AN: 22º47'S, 48º7'W), Itirapina (IT: 22º24'S, 47º54'W), São Carlos (SC: 21º58'S, 7º53'W), Rincão (RI: 21º35'S, 47º57'W), Barrinha (BA: 21º12'S, 48º10'W) and Sales Oliveira (SO: 20º52'S, 47º53'W). The region has transition characteristics of the Brazilian savanna and the Atlantic Forest (Fig 1a), and is located between the two main climatic zones according to the Köppen's classification, "Aw" to the north and "Cfa" to the south of the state (Fig 1b). Two pasture areas (0.2 ha) 5-10 km apart, located near to a river, stream or lake were demarcated in each municipality to estimate the richness and abundance of species of Solenopsis and Pseudacteon. All colonies found in the areas were disturbed with the aid of a small shovel to encourage the exit of ants and to attract the parasitoids.

A sample of fire ant workers was removed from each colony for species identification (Trager 1991). Flies were collected during the first seven hours from sunrise, a period that includes the peak of activity of all the species found in the wider region (Pesquero 1997). Flies that approached the colonies and hovered over fire ant workers in attack mode (Porter 1998) were collected with an aspirator. A cooler (circa 12ºC) was used to store the flies prior to species identification (Porter & Pesquero 2001) with a hand lens (20x). Voucher specimens of Solenopsis and Pseudacteon were retained by the authors and deposited in the Museu de Zoologia, Universidade de São Paulo, state of São Paulo, Brazil.

One colony identified as S. invicta and another as S. saevissima, collected in Anhembi and Sales Oliveira, respectively, were separated from soil particles by flotation (Jouvenaz et al 1977), transferred to white plastic trays (35 x 40 x 10 cm) coated internally with Fluon (ACG Chemicals Americas Incorporation, Bayonne, NJ) and fed with insects, water and sugar water during the study. These trays of fire ants were used in the host selection assays. In each sampling place a test of host choice was established, where the parasitoid flies could choose between the nest of S. saevissima or S. invicta simultaneously.

Trays were 10 m apart one from another to reduce mutual interference in the attraction of parasitoids, and were transferred to another distant point 50 m from the previous one at 1h intervals. The flies captured were stored and identified as described previously and released before dusk. Rates of attack, parasitoid pupation and emergence were not observed. Data on the preference of species of Pseudacteon for the two species of Solenopsis was analyzed by Wilcoxon matched pairs test with the Systat program (Systat Incorporation 2010).

Results

A total of 84 colonies of fire ants with estimates of densities varying between 10 and 70 colonies/ha (38.2 ± 6.44, n = 12) was found at the sampling sites. Solenopsis saevissima was dominant in the sites to the north of SC (RI, BA, SO), with 92% of the 27 colonies, while S. invicta was dominant in the sites to the south of SC (IT, AN), with 70% of the 20 colonies. Only S. saevissima colonies were found below IT to the south, and only S. invicta colonies were found above RI to the north. In SC, 27% of the 37 colonies belonged to S. invicta and 38% to S. saevissima, with 19% having ambiguous characteristics between both species and six colonies seemed to belong to two other fire ants species.

A total of 186 unidentified males and 398 females of Pseudacteon were collected. Fifteen species of Pseudacteon were observed in the whole sampling sites. Two communities of parasitoids were recognized: a northern community with nine species (5.11 ± 0.32, n = 6) associated with S. saevissima, and a southern community with eight species (4.68 ± 0.84, n = 4) associated with S. invicta (Fig 2). A mixture of Pseudacteon species of the two communities (13 species, 9 ± 0, n = 2) was observed in SC. Pseudacteon tricuspis, P. nudicornis and P. solenopsidis occurred in territories of both species of fire ants, and P. borgmeieri occurred only in SC associated with a single unidentified fire ant species. The most abundant species in the southern community were P. wasmanni Schmitz, P. tricuspis, P. litoralis and P. pradei Borgmeier, and in the northern were P. cultellatus, P. affinis Borgmeier, P. disneyi Pesquero, P. fowleri Pesquero and P. dentiger Borgmeier (Table 1).

A total of 106 males and 195 females belonging to 14 species of Pseudacteon were observed on the two trays of fire ants (Table 2). The two communities of Pseudacteon flies recognized the dominant Solenopsis species at the sampling sites (z = 3.29, n = 14, P < 0.001). In an analysis restricted to the species of parasitoids that were simultaneously attracted to the colonies of S. invicta and S. saevissima (P. affinis, P. disney, P. dentiger, P. tricuspis, P. pradei and P. wasmanni), the preference for the local host ant remained significant (z = 2.20, n = 6, P < 0.03).

Discussion

The average density of fire ant colonies in the region (38.18 ± 6.44, n=12) was intermediate if compared with the values found for S. invicta (30 ± 37 and 55 ± 8 colonies/ha) in surveys carried out in South America by Porter et al (1992, 1997). Solenopsis saevissima and S. invicta had a narrow latitudinal sympatric band in the study region situated between 22º24' and 21º35'S. However, records of S. saevissima in the state of Paraná expand its distribution area by approximately 420 km to the south of the study region into the S. invicta territory (Shoemaker et al 2006). It is possible that the climatic conditions are a limiting factor to the distribution of these ants, although the two zones have similar average annual rainfall (circa 1500 mm³). In the north area of the state of São Paulo, characterizing the climate "Aw", the temperature, potential evaporation and hydric deficiency are higher than those of the south "Cfa" climate area (Rolim et al 2007). However, the occurrence of S. invicta in lower latitudes (Porto Velho 8°36'S, 63°54'W) (Lofgren et al 1975) and the high latitudinal overlap between the two fire ant species (circa 17º of difference between the most northern occurrence of S. invicta) (Lofgren et al 1975) and the most southern occurrence of S. saevissima (Shoemaker et al 2006) require more studies, including examination of competitive exclusion. The high recruitment response and dominance abilities of S. invicta reinforce this hypothesis (Cacaterra et al 2008).

The species of Pseudacteon observed here represent 75% of all known species of this group associated with fire ants of S. saevissima group in South America. The southern community corresponded to flies previously described for the region of Rio Claro (SP) (22°24'S, 47°33'W) on S. invicta, while the northern community corresponded to flies found in Goiânia (GO) (16°42'S, 49°15'W) on S. saevissima (Pesquero 1997). Populations of P. tricuspis and P. nudicornis found in the territories of S. saevissima and S. invicta have the biotypes previously described for the state of Goiás and São Paulo, respectively (Porter & Pesquero 2001). Pseudacteon affinis and P. cultellatus were identified as the biotypes found in the state of Goiás, and P. curvatus Borgmeier in the state of São Paulo (Porter & Pesquero 2001).

The territories of the two communities studied here were abruptly interrupted in São Carlos (SC), indicating strong environment changes. Three non-exclusive hypotheses may contribute to this geographic distribution pattern. The first hypothesis is that parasitoids can be species specific to the fire ants and, therefore, follow the distribution of their host. Although the development of Pseudacteon flies on non-host fire ants species is possible under laboratory conditions, the approach and attack rates are reduced compared with local fire ant species (Folgarait et al 2002, Folgarait et al 2005b). Ecological and behavioral factors are considered as so or more important as physiological and taxonomic limitations in the determination of the host range in other groups of parasitoids (Whitfield & Wagner 1988, Morehead & Feener Jr 2000, Stireman & Singer 2003).

Although the reduced number of fire ant species colonies (n = 1) can underestimate intercolonial variation, assays for host selection demonstrated the preference of the Pseudacteon fly communities for the local fire ants species. However, P. affinis, P. dentiger, P. disneyi, P. pradei, P. tricuspis and P. wasmanni were attracted by the two fire ants species (Table 2). Of these parasitoids, P. tricuspis and P. disneyi have regional biotypes and attack different Solenopsis species (Pesquero 1997, Calcaterra et al 2005); P. pradei and P. wasmanni occur in areas having an association with more than one fire ant host species (Patrock et al 2009), but P. affinis and P. dentiger seem to be limited to the distribution area of S. saevissima (Pesquero 1997, Patrock et al 2009).

In our second hypothesis, the climatic differences between the northern and the southern areas can enforce important physiological restrictions regarding to body temperature and water balance for these small insects (Porter & Gates 1969). Indeed, Folgarait et al (2005a) found a significant association between climatic variables (mainly temperature and precipitation) and groupings of Pseudacteon species in South America. However, the limiting factors for the regional climatic variations can be overcome by acclimatization of these species. Evaluating the period of daily activity of two communities of Pseudacteon in places with different climates in Brazil, Pesquero (1997) reported that the majority of species in the community located in tropical climate with dry winters had crepuscular activity, while those species situated in humid climate with hot summers were active during the warmest hours of the day.

In our last hypothesis, we assume that communities can be saturated, making difficult the introduction of a new species (Ricklefs 1987). This subject is little explored in communities of Pseudacteon, but the predominance (84%) of local assemblies with a lower richness (up to four species) as compared with the richness observed for regional assemblies in South America (Patrock et al 2009), and the convergence of structure between two regional communities in Brazil (Pesquero 1997) suggest the role of competition in the community structure of these insects.

This study represents the first register of geographic transition zone between populations of fire ants S. invicta and S. saevissima, and between communities of Pseudacteon parasitoid flies supported by these ants in Brazil. The distribution of parasitoid flies seems to be determined by host specificity, while fire ants distribution seems to result from climatic influence. However, data on change of niche of Pseudacteon (Pesquero 1997) and dominance of Solenopsis (Calcaterra et al 2008) indicate that interespecific competition must also be taken into consideration in the inquiry of this phenomenon.

Acknowledgments

Nivaldo D Oliveira assisted during field collections. Rafael F Juliano (UEG - UnU Morrinhos) and two anonymous reviewers of the manuscript provided a number of helpful suggestions. This study was supported by a research assistantship provided by FAPESP.

Received 07 February 2011 and accepted 12 July 2011

Edited by Fernando L Cônsoli - ESALQ/USP

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Publication Dates

• Publication in this collection
  06 Feb 2012
• Date of issue
  Dec 2011

History

• Accepted
  12 July 2011
• Received
  07 Feb 2011