Seasonal patterns of activity among species of black fire ant parasitoid flies ( Pseudacteon:...

Biological Control 28 (2003) 368–378

www.elsevier.com/locate/ybcon

Seasonal patterns of activity among species of black fireant parasitoid flies (Pseudacteon: Phoridae) in Argentina explained

by analysis of climatic variables

Patricia J. Folgarait,a,* Octavio A. Bruzzone,a and Lawrence E. Gilbertb

a Centro de Estudios e Investigaciones, Universidad Nacional de Quilmes, Roque Saenz Pe~nna 180, Bernal B1876BXD, Buenos Aires, Argentinab Section of Integrative Biology and Brackenridge Field Laboratory, University of Texas Austin, TX 78712, USA

Received 5 February 2002; accepted 9 April 2003

Abstract

We monitored weekly relative abundances of adult female Pseudacteon (Diptera: Phoridae) species between February 1998 and

May 2000 in Argentina. Fire ant-phorids were active around mounds of Solenopsis richteri Forel throughout the year. Phorid species

richness ranged from six species during the summer-fall, to a single, large species during the winter. Species were classified as winter,

summer, or fall-spring species, depending on times of peak mean abundance. We used descriptive multivariate techniques to analyze

phorid phenological data (correspondence analysis), climatic data (principal component analysis), and their relationships (canonical

correspondence analysis¼CCA) at three temporal scales. The long-term mean temperatures, the mean and minimum sampling-time

temperature, and the cumulative number of days without rain from the two months preceding each sampling day explained >90% of

the variance when the data for sampling dates were averaged across the same months over the two years. Pseudacteon borgmeieri

Schmitz, the winter dominant, was associated with lower temperatures and rainfall, whereas Pseudacteon curvatus Borgmeier, the

summer dominant, showed the opposite pattern. Among the fall-spring species, Pseudacteon comatus Borgmeier was associated with

months of higher maximum temperatures, longer photoperiods, and lower relative humidity. Pseudacteon nudicornis Borgmeier, in

contrast, showed the opposite pattern. Pseudacteon tricuspis Borgmeier, was associated with months, typically in fall, having greater

rainfall and fewer days with frosts. Implications of these patterns for the process of selecting particular species of S. richteri-at-

tacking Pseudacteon for use in biological control introductions against imported fire ants are discussed in relation to climates of

source and release areas.

� 2003 Elsevier Science (USA). All rights reserved.

Keywords: Biological control; Buenos Aires; Circannual; Fire ants; Pseudacteon; Solenopsis richteri

1. Introduction

All animals, including insects, have activity schedulesthat change through the day and throughout the year.

Such circadian and circannual phenological patterns are

intrinsically interesting because they provide important

information about the natural history of a species, such

as their physiological adaptations and potential inter-

specific relationships (Tauber et al., 1986). This paper

* Corresponding author. Fax: +54-11-4365-7100/7182/7101x225.

E-mail address: [email protected] (P.J. Folgarait).

1049-9644/$ - see front matter � 2003 Elsevier Science (USA). All rights res

doi:10.1016/S1049-9644(03)00093-8

analyzes the phenology of a parasitoid community of

Pseudacteon phorid flies in Argentina.

Little is known about the phenology of most of thedipteran family Phoridae (Disney, 1994). Exceptions

include those phorids that specialize in attacking

Solenopsis fire ants (Fowler et al., 1995; Morrison et al.,

1999, 2000; Wuellner and Saunders, 2003). Because

South American species of Pseudacteon parasitoids are

being considered as biological control agents of im-

ported fire ants (Solenopsis invicta Buren and Solenopsis

richteri Forel) in the US, it is important to know theactivity patterns of these flies in their native habitats.

Such data, in concert with analyses of the climatic cor-

relates of phorid activities in their native habitats, are

erved.

mail to: [email protected]

P.J. Folgarait et al. / Biological Control 28 (2003) 368–378 369

relevant to selecting the best species for classical bio-logical control efforts because they can help: (1) predict

whether a potential control agent may be expected to be

active year round or at certain months, (2) design suites

of phorid species with complementary activity patterns,

and (3) ensure meaningful matches between the native

habitats of the candidate species and the climate in

which fire ants are introduced pests.

Considering that various species of more than 16Pseudacteon parasitoids of fire ants have been or will be

imported to the US from their native Argentina and

Brazil, it is essential to have information on the phe-

nology of these flies in their native habitats. The phe-

nology of species in a South American Pseudacteon

community was studied throughout the year (Fowler

et al., 1995) and in another brazilian study diurnal

activity patterns of Pseudacteon were also reported(Pesquero et al., 1996). These brazilian studies, however,

did not fully address the climatic correlates of phorid

seasonal activity.

The climate of Buenos Aires, Argentina, corresponds

well with certain areas in North America, where red (S.

invicta ) or black (S. richteri) imported fire ants or their

hybrids have spread (Fig. 1). Although the phorid spe-

cies we studied are associated with S. richteri nearBuenos Aires, in another study we have established that

most species will attack and then develop on S. invicta

hosts (Folgarait et al., 2002a). Therefore, Pseudacteon

species and populations adapted to climates around

Buenos Aires, and which can use S. invicta as larval

Fig. 1. Comparative climatographs of source populations in Argentina and s

have been (Dallas) or may be introduced in the future. Vapor point deficit (V

dryness because it incorporates temperature and humidity. Both climatograp

have been found to date in South or North America. Data for US sites from

host, are of special interest in regions where climate maybe one constraint to successful introductions of tropical

phorids, such as the Brazilian Pseudacteon tricuspis (e.g.,

Gilbert and Patrock, 2002). The phenological informa-

tion presented herein will supplement information being

generated from the laboratory rearing of many Pseu-

dacteon species considered as control candidates (Fol-

garait et al., 2002a,b; Gilbert and Morrison, 1997;

Morrison et al., 1997, 1999; Porter and Briano, 2000;Porter et al., 1995a,b, 1997). In particular, our data, in

combination with the phenological information that is

being gathered for US native phorid flies and patterns of

activity of fire ants (Morrison et al., 1999, 2000;

Wuellner and Saunders, 2003), provide a basis for

judging the likely suitability of various species for in-

troductions into specific climatic regions of Texas. The

main goals of this study were to: (1) describe the phe-nology of a community of Pseudacteon species across

months and years, and (2) determine climatic and me-

teorological correlates that could best explain the phe-

nological patterns of the Pseudacteon community.

2. Materials and methods

We studied the phorid community from the Reserva

Ecol�oogica Costanera Sur (RECS) (35.5�N, 58.5�W) in

Buenos Aires, Argentina. The reserve represents a nat-

urally colonized 350 ha area of river terrace, which

parallels the La Plata River. The site is characterized by

ink areas in Texas where Pseudacteon curvatus and other Pseudacteon

Pd) is a meterological descriptor that can be viewed as a measure of air

h axes extend the ranges expected where Solenopsis host Pseudacteon

NOAA; data for Argentina sites from Schwerdtfeger (1976).

370 P.J. Folgarait et al. / Biological Control 28 (2003) 368–378

a mosaic of Cortadeira sp. and other grasses interdis-persed with wetlands.

From February 1998 to May 2000, the abundance of

phorids by species was recorded, twice per week during

the first 18 months and once per week thereafter.

Phorids were not found on some sampling days, but

because we have maintained our sampling effort

throughout weeks within months and across the two

years, our confidence has increased progressively thatthe absence of a particular species at a certain time re-

flects its true absence in the field.

All data were gathered at S. richteri mounds, which

were disturbed by digging a hole in them. To maintain a

high ant activity in order to attract parasitoids, the

surface of the mound was baited with tuna fish. At least

five mounds were monitored on each observation day at

each of two sites for three h per site per person; one ortwo people went to the RECS for gathering these data.

Sampling was done mostly between 1100 and 1500 h.

However, other times of the day were sampled

throughout the year to gain confidence that the absence

of a species was not related to circadian rhythms. All

data on phorid abundance was standardized per unit

sampling effort (number of phorids collected, divided by

the person-hours for that effort). By using a 15� handlens, one can identify females of Pseudacteon species

based on the shape of their ovipositors. However, males

cannot be distinguished among species using field tech-

niques (Porter and Pesquero, 2001). In general, at the

end of each sampling period, we released the phorids

Table 1

Climatic and meteorological variables used in canonical correspondence phe

Historical monthly means or extremes Field site samp

Variables related to moisture (rainfall and relative humidity)

Rainfall at AMSa Accumulated ra

Relative humidity at AMSa Accumulated d

Relative humidity at SMa Mean rainfall a

Rainfall at SMa Mean rainfall a

Vapor pressure deficit at AMSa

Vapor pressure deficit at SMa

Variables related to temperature and photoperiod

Number of days with frosts at AMSa Maximum at sa

Number of days with frosts at SMa Mean maximum

Extreme maximum at AMSa Mean at sampl

Extreme maximum at SMa Mean minimum

Mean maximum at AMSa Minimum at sa

Mean maximum at SMa

Mean temperature at AMSa

Mean temperature at SMa

Extreme minimum at AMSa

Extreme minimum at SMa

Mean minimum at AMSa

Mean minimum at SMa

Mean photoperiod

Variable related to moisture, including rainfall and humidity; variables raMeteorological stations from Buenos Aires City (AMS, besides La Plata

and 20 km, respectively, from RECS).

after identification. If identifications were uncertain,then the specimens were transported to the laboratory

for examination. Thus, phenological data consisted of

phorid abundance based on collections of females

through time. With respect to climatic measurements,

we obtained long-term (historical) data (from 1980 to

1990), and daily measurements of standard climatolog-

ical variables (e.g., several related to temperature, pre-

cipitation, and relative humidity). Climatological datawere collected at the Aeroparque (AMS) Meteorological

Station, located approximately 2 km from our field site.

Frosts are rare along the La Plata River where AMS and

the RECS are located, but are quite frequent at other

localities where these phorids are present in Argentina,

as well as in many areas in the United States where bi-

ological control introductions might be made. Consid-

ering this variation, we also obtained the sameclimatological data from Villa Ortuzar (VO) and San

Miguel Meteorological Stations (10 and 20 km away

from the river, respectively) also within Buenos Aires.

We considered 28 meteorological and climatic vari-

ables (Table 1), from which we selected a subset for the

final analyses (Table 2). This subset retrieved the most

important variables according to their relative weights

on the first axes of various canonical correspondenceanalyses. This subset included historical (1981–1990)

variables such as mean monthly precipitation, relative

humidity, temperature, photoperiod, and days with

frosts. It also included those variables for which mea-

surements were taken only within the sampling period

nological analyses

ling

infall two months before the sampling time

ays without rainfall two month before the sampling time

t sampling time

t VOa at sampling time

mpling time

at sampling time

ing time

at sampling time

mpling time

elated to temperature and photoperiod.

River, less than 2 km from RECS, and VO and SM, inland, less than 10

Table 2

Variables chosen for the final analyses, and their correlation with the first three axes of the canonical correspondence analysis

Variable Correlation value

Axis 1 Axis 2 Axis 3

Historical mean rainfall at AMSa 0.696 0.404 0.055

Historical mean photoperiod 0.694 )0.196 )0.490Historical mean number of days with frosts at SMa )0.690 )0.254 0.026

Historical mean relative humidity at AMSa )0.615 0.039 0.512

Maximum temperature at sampling time 0.784 )0.104 )0.404Historical mean temperature at AMSa 0.915 )0.076 )0.250Mean temperature at sampling time 0.898 )0.057 )0.315Minimum temperature at sampling time 0.898 )0.140 )0.036Accumulated rainfall two months before sampling time 0.795 )0.065 0.338

Mean rainfall at sampling time 0.704 )0.185 0.311

Accumulated days without rainfall two months before the sampling time )0.797 0.118 )0.027aMeteorological stations from Buenos Aires City (AMS, besides La Plata River, less than 2 km from RECS, and SM, inland, less than 20 km

from RECS).


1998–2000. The latter subset included accumulated

mean rainfall and the number of days without rain in theprevious two months before the sampling day, the mean

rainfall, the mean temperature, and the extreme maxi-

mum and minimum temperature.

3. Statistical analysis

Decisions to include variables in the analyses fol-lowed evaluation of the overall data set, using corre-

spondence (CA) and principal component (PCA)

analyses (Digby and Kempton, 1987). We used CA to

determine if different phorid species grouped with each

other through time, so as to infer possible similarities in

physiological requirements. CA can be interpreted as

finding the best simultaneous representation that maxi-

mizes the variation of a data set such as ours, repre-sented by the rows (species) and columns (observation

times, i.e., days or months). Therefore, each axis of a

CA represents the simultaneous ordering of species and

times that produces the maximum possible correspon-

dence between them, subjected to the constraint that all

axes are orthogonal with each other (Lebart et al., 1984).

PCA was used to find the principal dimensions that

characterized the maximum variation in climatic vari-ables and then helped us to identify variables that best

correlated with these dimensions. The PCA was applied

on the correlation matrix of the climatic variables

gathered through time.

Once our final variable list was chosen, we addressed

our question as to the extent to which phorid phenology

could be successfully explained by climate using ca-

nonical correspondence analyses (CAC) (Ter Braak,1986). Supplementary variables such as phorid species

and month were used in the ordination diagrams to al-

low interpretation of subjacent operating factors (Le-

bart et al., 1984). All these analyses accounted for three

scales: day-by-day data (total of 114 observations

through time), month-by by-month data (means of daily

data for the same month), but keeping months separatefor different years (26 observations), and finally by using

mean monthly data (daily data were averaged across

years for each month, 12 observations).

Given the constraint of using a secondary matrix

(meteorological and climatic data) to explain the varia-

tion found in the primary matrix (phenological data), a

CCA analyses could never explain more variation in the

first matrix than the amount of variation explained bythe CA analyses by itself. Therefore, we used the ratio

between the accumulated variance explained in each of

the first three axes of the CCA and CA as a measure of

efficiency for each scale of analysis; the closer to 100%

the greater the explanatory power. Multivariate analyses

were carried out using the PC-ORD software system

(Mc Cune and Mefford, 1997).

4. Results

We collected six Pseudacteon species: Pseudacteon

borgmeieri Schmitz, Pseudacteon comatus Borgmeier,

Pseudacteon curvatus Borgmeier, Pseudacteon nudicornis

Borgmeier, Pseudacteon obtusus Borgmeier, and Pseu-

dacteon tricuspis Borgmeier. The only species collectedthroughout the year was P. borgmeieri. At the other

extreme, P. obtusus was only found six months of the

year. All other species were present from seven to nine

months of the year (Fig. 2). P. borgmeieri was also the

most abundant species (mean annual number phorids

per sampling effort¼ 2.83), followed by P. curvatus (1.7)

and P. nudicornis (1.5); the least abundant was P. ob-

tusus (0.06). The relative abundance of phorid species inthis community, as well as their specific months of peak

abundance, changed slightly across the years, although

not for the three most abundant and most frequent

species (Fig. 3). Annual peak of abundance for each of

the species differed (Fig. 3). We classified each species

Fig. 2. Relative (in percentage) mean abundance of phorids, per sampling effort, throughout the year for P. borgmeieri, P. comatus, P. curvatus, P.

nudicornis, P. obtusus, P. tricuspis, found at the Reserva Ecol�oogica Costanera Sur. Seasons are indicated in the x-axis below the months.


according to its time of greater mean abundance. P.

borgmeieri was the only species present during the winter

and had its greatest abundance during that time of year.

We therefore classified it as a winter dominant. P.

curvatus, on the other hand, was present most of the

year, but peaked in mean abundance during the sum-

mer, and as such was classified as a summer dominant.

The rest of the species were classified as fall species (P.

tricuspis and P. obtusus peaked in March), or fall-sum-mer species (P. nudicornis and P. comatus peaked in

April and sometime during the summer). Averaging all

sampling days across months and years, there were 7.28

females/per person-hour sampling effort. The six species

collected fell into two broad size classes: P. tricuspis, P.

obtusus, and P. borgmeieri were significantly larger than

P. curvatus, P. nudicornis, and P. comatus (thorax width,

Folgarait et al., 2002a).The CCA/CA ratio for the day-by by-day analysis

was 62.2, 53.7, and 44.6% for axes 1, 2, and 3, respec-

tively, whereas for the month-by-month analysis (keep-

ing years separately) was 87.0, 80.9, and 75.9%,

respectively. Interestingly, the average month-by-aver-

age month analysis explained 100% for each axis.

Therefore, we kept the latter scale of analysis and all the

results reported from here on will refer to it.Considering the three first axes, the CA analysis ex-

plained 93.9% of the variance found in the phenological

data (Fig. 4). The first axis separated P. borgmeieri,which was clearly associated with winter months, from

the rest of the species. The second axis discriminated

between P. curvatus, associated with summer, from P.

nudicornis, P. comatus, and P. tricuspis. The third axis

separated P. comatus, more associated with December,

from P. nudicornis, more associated with the fall (April

and May).

The PCA explained, among the first three axes,99.19% of the variation found in the climatic data. In

fact, most of the variance was explained by the first axis,

which could be interpreted as a precipitation axis

(Fig. 5). The variable with greatest weight ()7.5) was

rainfall accumulated during the preceeding two months,

followed by the historical rainfall ()3.1), and in the

opposite direction, photoperiod (3.5) and number of

days with frost (3.4). Because rainfall in this study waslower in winter, a time when frosts occurred and pho-

toperiod was shorter, the latter two variables were in-

versely correlated with precipitation measures.

Using the climatic data, the CCA explained 93.9% of

the variation in the phenological patterns (Fig. 6). The

first axis could be interpreted mainly as a temperature

axis given by the historical mean temperature, and the

mean and minimum sampling temperatures at one end.In the opposite direction, the main variable was the

number of days without rain in the last two months

Fig. 3. Mean abundance of phorids, per sampling effort, for each sampled month throughout the years for P. borgmeieri, P. comatus, P. curvatus, P.

nudicornis, P. obtusus, P. tricuspis, found at the Reserva Ecol�oogica Costanera Sur. Seasons are indicated below the months, from darkest (black) for

winter to clearest (white) for summer, with increasing intensities of grey for spring and fall.


before sampling, which in this study was greatest for

winter. The second axis, which explained less variance,

instead could be interpreted as a precipitation axis,with the historical mean precipitation and the number

of days with frosts in opposite directions (see Table 2

for correlation values of each variable with the CCA

axes.)

The ordination diagram showed an association be-

tween winter months with lower temperatures and

longer periods of time without rain, and P. borgmeieri

activity, whereas the opposite association was found forP. curvatus, associated with summer, and with P. nudi-

cornis, P. comatus, and P tricuspis. There was also an

association between P. nudicornis activity and Decem-

ber, and an association among P. comatus and P. tric-

uspis with April and May, both related to greatest

precipitation and fewest frosts. The third axis separated

P. comatus, more associated with December, from P.

nudicornis, more associated with the fall months (Apriland May). The other end of the axis was explained by

the historical expectations of relative humidity and was

associated with P. nudicornis and May (see Table 2 for

correlation values of each variable with the axes).

5. Discussion

This is the first analysis of a South American Pseu-

dacteon community to relate seasonal activity patterns

to several weather and metereological variables in con-

cert. The phenology of Pseudacteon communities have

been described in South Brazil (Fowler et al., 1995) and

Central Texas, USA (Morrison et al., 1999, 2000;

Wuellner and Saunders, 2003). All of these studies have

shown that peaks of activity vary according to species

throughout the year, either showing bimodal or uni-modal peaks of abundance. In Central Texas, cold

conditions in fall seem to shut down phorid activity,

except on mild days when the temperature rises above

20 �C (Morrison et al., 1999; Wuellner and Saunders,

2003). By contrast, in Brazil, where seasonality is less

pronounced in terms of temperature shifts, phorids seem

to be active throughout the year.

At RECS in Argentina, Pseudacteon phorids werepresent in every month of the year, but only P. borg-

meieri persisted as active adults through the winter

(during which temperatures average around 11 �C, andminimum temperatures can fall to 1 �C). In a different

Fig. 4. First and second axes (top), and first and third axes (bottom), of a correspondence analysis of phorid species abundance throughout the year.

Diamond symbols represent each of the Pseudacteon species; triangles represent each of the months of the year.


study at the same site, Folgarait and Gilbert (1999) re-

corded temperatures in the field and found that flies were

not active when temperatures were lower than 14 �C,which is 6 �C below the threshold activity registered in

the field for native Pseudacteon in Texas, US (Morrison

et al., 1999; Wuellner and Saunders, 2003). We infer

then, that P. borgmeieri may have physiological adap-

tations that allow it to remain active and fly at temper-

atures that are restrictive for other Pseudacteon species,

including those currently being introduced into the US.

Fig. 5. First and second axes of a principal component analysis for climatological variables. Variable names: HaverRhaero—historical average

relative humidity of Aeroparque, HaverRFaero—historical mean rainfall of Aeroparque, STWoutRF2monthbef—number of days without rainfall

two months before the sampling time, STRF2monthsbef—accumulated rainfall two months before the sampling time, STaverRF—mean rainfall at

sampling time, Stmaxtemp—maximum temperature at sampling time, STavertemp—mean temperature at sampling time, STmintemp—minimum

temperature at sampling time, Havertempaero—historical mean temperature at Aeroparque, HaverFrostSM—historical mean number of days with

frosts at San Miguel, Hphotoperi—historical photoperiod.


Brown (1992) has also showed that some Phoridae

flies are active during winter. However, the most com-

mon pattern seems to be that adults disappear during

colder months. There are three possible mechanisms by

which phorid species disappear for periods of time that

exceed their generation span, but are found again onceconditions improve (as we found in this study across

years): (1) observed patches occupied by the species�metapopulation undergo extinction every winter and are

re- colonized every spring from source populations; (2)

phorids decrease their metabolic activity during the

winter; or (3) they enter a period of diapause or quies-

cence during harsh times.

The first explanation has little power for decipheringseasonal patterns in a cool temperate system because

regions exposed to unsuitable climatic conditions en-

compass entire metapopulations, and the duration of

unsuitable temperatures exceeds phorid developmental

life cycles.

Immature phorids have considerable variation in

their developmental time, which lends support to the

possibility of decreased metabolism as a strategy fordealing with cold weather. The longest egg-to-adult de-

velopmental period recorded so far in Pseudacteon is 66

days although approximately 40 days is common for

most species (Folgarait et al., 2002a). These studies have

not been done under simulated winter conditions so it is

likely that developmental periods could be longer, if

development within the host occurs away from the

thermo-regulated sections of the colony. It appears thatmost Pseudacteon species could be able to slow and thus

extend developmental growth by 1–2 months over typ-

ical growth rates. To accomplish this the parasitoid

would have to grow at a slow pace without killing its

host. If this is the tactic employed by Pseudacteon,

maintaining parasitoid-infected ants at winter tempera-

tures for 3–4 months and subsequently increasing tem-

perature should mimic the phenological patterns of

phorid adult emergence found in the field.

With regard to the third hypothesis that the parasitoids

enter into diapause an important consideration is the

state of the host. If healthy, Solenopsis worker ants can

live for months. Because phorid-infected ants would onlyremain viable, if the parasitoids were arrested in egg or

early larval instars, we assume that these represent po-

tential stages for diapause. Changes in absolute and rel-

ative photoperiods could be sensed by the parasitoid via

host physiological responses as has been shown in other

parasitoids (Leather et al., 1993; Tauber et al., 1986).

Adults of all Pseudacteon species studied to date in

our laboratories never live longer than 10 days in therefrigerator (10–15 �C; Folgarait, unpublished; Gilbert

unpublished), therefore, they may not be able to hide

and wait for better climatic conditions. Pupae phorids

are also candidates to undergo diapause, but this pos-

sibility has not been supported in the laboratory thus far

after extensive study (Wuellner, personal communica-

tion). We discard adult quiescence as a possibility be-

cause during our monthly sampling across two years,there were abnormal days, in terms of temperature and

rainfall; yet we did not record the appearance of any

unexpected species. Most importantly, the day-by-day

multivariate analysis was less successful at explaining the

phenology of this community than the monthly analysis.

Our study is the first to account for a great part of the

variability exhibited in phorid communities by using a

multivariate approach to show the relative importanceof various climatic variables on phenological (circan-

nual) patterns of species within a dipteran parasitoid

community. We have shown that simple variables such

as mean temperature (long term monthly means versus

those recorded at a single point in time during an ex-

periment) as well as the lack of precipitation, largely

explained the variation in the phenology of adult

Fig. 6. First and second axes (top), and first and third axes (bottom), of a canonic correspondence analysis used to explain abundance of phorids

throughout the year based on climatological variables. See Fig. 3 for name of species and Fig. 5 for codes of climatic variables. Diamond symbols

represent each of the Pseudacteon species; triangles represent each of the months of the year.


activity within a community of fire ant parasitoids in

Argentina. Others have previously shown a small effect

of humidity and temperature for few species (Morrison

et al., 2000; Pesquero et al., 1996). Considering all

available information, we can say that species of Pseu-

dacteon phorids may respond differentially to levels of

temperature and moisture and that sympatric species

display great variety in how they tune their life cycles to


seasonally changing abiotic conditions. At RECS wefound that the six Pseudacteon species evaluated, seg-

regated from each other along axes that were related to

different variables. This species-specific response to en-

vironmental variables has never been formally addressed

before for this genus. In this study, we found that

P. borgmeieri predominated at lower temperatures, less

rain, and could be found on days when there were frosts,

whereas P. curvatus was found under warm, rainy con-ditions. These results from multivariate analyses are in

agreement with our a priori classification of species ac-

cording only to their relative abundance across months.

In this study we have shown that the broader the

temporal scale of analysis the better the ability to ex-

plain the data. This result was probably related to the

amount of variation present in daily data, which masked

patterns found when variables were averaged. However,a mixture of long term, as well as sampling time mea-

sures of climatic variables (see variables selected in

Table 2), was important to explain the phenology of the

phorids. Therefore, it seems that these Pseudacteon

species are primarily adapted to long-term (historical)

averages of temperature and precipitation, but popula-

tion density cycles are modulated according to current

meteorological conditions.

5.1. Implications

The information herein is useful for the selection of

biological control agents of imported fire ants. The

number of months in which a species is present and its

relative abundance through time gives an idea of the

efficiency of the candidate species in terms of the win-dow of time during which it will be able to affect the

ants. Therefore, candidate species could be chosen be-

cause of their complementary activity patterns. Pheno-

logical data collected for Argentina phorids is of

particular use to North American biocontrol efforts

because Argentina�s climate more closely parallels the

conditions in North America than does Brazil

(Schwerdtfeger, 1976). For instance, one of the reasonsP. tricuspis has been deemed a good candidate for bio-

control in the US is because it is active year round in

Brazil. However, populations of the same (or closely

related species) are only active seven months of the year

in Argentina, suggesting the presence of a diapause

pattern in this ecotype/species that could be more ap-

propriate for North America.

In general, if different Pseudacteon populations rep-resent ecotypes with their own set of local adaptations,

rearing tropical populations of these species and re-

leasing them in temperate US localities (as is currently in

progress) may be less appropriate than rearing popula-

tions with matching climates between the source of or-

igin and sink of release. Another consideration is the

degree of difference between climates occupied by im-

ported fire ant species in their native versus introducedranges. While North American climate types where S.

richteri or its hybrid with S. invicta is found are similar

to the climate of Buenos Aires habitats where S. richteri

and its specialist Pseudacteon species are native (Fig. 1),

the situation is very different in the case of the more

important pest, S. invicta. Although S. invicta�s naturalrange is primarily tropical and sub-tropical, most of its

North American distribution includes climatic zonesmore similar to Buenos Aires than to South Brazil

(Schwerdtfeger, 1976) where the P. tricuspis, currently

being release against S. invicta, originates. However, S.

invicta has been reported in western Argentina (Trager,

1991) in areas with drier and cooler conditions than

northeastern Argentina or Brazil. Therefore, if pro-

spective Pseudacteon are not found in these areas, it will

be important to study the suitability of S. invicta as ahost for South American temperate Pseudacteon which

use other Solenopsis species as hosts, such as the eco-

types or species documented in this study (e.g., P.

curvatus: Porter and Briano, 2000; P. cultellatus: Fol-

garait et al., 2002b, and other S. richteri-attacking

Pseudacteon: Folgarait et al., 2002a).

We assume that the climatic conditions under which

Pseudacteon flies flourish in their native habitats willprovide some indication as to how they will do in spe-

cific areas of North America (Folgarait et al., 2000). For

example, P. curvatus, an abundant species in Argentina,

which is being mass-reared in the US, and which is being

released in some states like Alabama, probably would

not do well during winter and/or drought, or at least will

not be active under such conditions. By contrast, P.

borgmeieri seems to be extremely well adapted to copingwith low temperatures and low rainfall and thus might

be more effective than Brazilian P. tricuspis at main-

taining harassment of fire ants through the cool months

in the northern hemisphere, when P. tricuspis cannot

maintain adult activity, but where red imported fire ants

are still active in places like Central Texas (Wuellner and

Saunders, 2003). Although P. borgmeieri has been

reared successfully in the laboratory (Folgarait et al.,2002a) and has been shown to have a considerable be-

havioral effect on its host species (Wuellner et al., 2002),

it is not host specific: this species will attack Solenopsis

geminata, an ant native to the US (Morrison and Gil-

bert, 1998, but see Folgarait et al., 2002a). Clearly, any

candidate species should be evaluated in terms of its

natural history, host specificity, as well as its physio-

logical suitability for a given climatic zone.Because of the wide breadth of climatic zones now

occupied by exotic S. invicta, it is impossible to match a

given phorid with both its native host and its favored

climate in most areas of North America where it might

be applied to biological control of imported fire ants. By

selecting phorids possessing appropriate climatic adap-

tations from among those known to switch successfully


from S. richteri to S. invicta under laboratory condi-tions, it may be possible to successfully introduce

Pseudacteon species into regions where attempts to in-

troduce species like Brazilian P. tricuspis have proven to

be problematic at best (Gilbert and Patrock, 2002).

Acknowledgments

We thank R. Patrock and C. Wuellner for their

careful and thoughtful comments on the manuscript. In

particular, R. Patrock has been extremely helpful for thefinal edition of the manuscript and the development of

the first figure. G. Zaccardi and N. Gorosito helped

gather data in the field at different stages. A. Albarrcin,

G. Freire, and the Atmospheric Science Library from

the University of Buenos Aires kindly provided in dif-

ferent formats parts of the climatological data. Climatic

data for USA and Brazil were gathered from Worldcli-

mate.com. We are indebted to the staff of the RECS, inparticular to Sergio Recio, who provided permits and

logistic support to perform this research. This research

was funded by the Helen C. Kleberg and Robert J.

Kleberg Foundation, and the Texas Imported Fire Ant

Research and Management Project and the Fondren

Foundation. P.J.F. thanks the Universidad Nacional de

Quilmes and CONICET for their support.

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