BIOLOGICAL CONTROL

Inuence of Temperature on Development Time and Longevity of Tachinaephagus zealandicus (Hymenoptera: Encyrtidae), and Effects of Nutrition and Emergence Order on Longevity
MARIA A. FERREIRA DE ALMEIDA,1 ANGELO PIRES DO PRADO,1 CHRISTOPHER J. GEDEN2
AND

Environ. Entomol. 31(2): 375380 (2002)

ABSTRACT Tachinaephagus zealandicus Ashmead is a gregarious endoparasitoid that attacks third instars of muscoid ies in the Southern Hemisphere. The purpose of the current study was to evaluate the inuence of six constant temperatures (16, 18, 20, 22, 25, and 27 C) on development time, the inuence of emergence order on longevity, and the effects of temperature and food treatment on longevity. Emergence success was greatest at 22 C for both males and females; signicantly fewer (24.130.4%) parasitoids emerged at 16 and 25 C compared with 22 C. Development time ranged from 24.0 to 56.9 d for both sexes. No emergence was observed at 27 C. Early-emerging parasitoids had greater longevity than parasitoids that emerged later from the same cohorts. The longevity of females given honey and water decreased with increasing temperature, and those reared at 16 C lived about three times longer than those kept at 27 C. Females given honey and water had similar longevities at 16 20 C, and females that were given only water lived for only 4.8 7.6 d at all temperatures. Females lived signicantly longer overall than males at all temperatures except 16 C, but differences due to sex were small compared with the effects of temperature and nutrition. Further investigations will be necessary to determine the climatic zones in which T. zealandicus is most likely to be an effective biological control agent of muscoid ies. KEY WORDS Tachinaephagus zealandicus, muscoid ies, temperature, longevity, development rate

Tachinaephagus zealandicus ASHMEAD is a gregarious endoparasitoid of muscoid y third instars that appears to be indigenous to the Southern Hemisphere (Olton 1971). Legner et al. (1967) observed T. zealandicus parasitizing Musca domestica L. breeding in bovine manure in southern Uruguay. The importation of T. zealandicus from areas of Australia and New Zealand (Legner and Olton 1968) into climatically similar sections of southern California provided an opportunity for establishment of this species in a relatively empty niche (Olton 1971). Thus, colonies were established in southern California in 1967 (Legner and Olton 1968) and aspects of the biology of this species were studied by Olton (1971). Silveira et al. (1989) provided the rst report of T. zealandicus attacking Cochliomyia hominivorax (Coquerell) (Calliphoridae) in the State of Sao Paulo, Brazil, and attacking Synthesiomyia nudiseta (Wulp) (Muscidae) in the State of Minas Gerais, Brazil. Costa (1989) found T. zealandicus associated with pupae of M. domestica, Stomoxys calcitrans (L.), and Muscina stabulans (Fallen) (Muscidae) collected in a poultry
Departamento de Parasitologia, Instituto de Biologia, UNICAMP, CP 6109, CEP 13083970, Campinas, Sao Paulo, Brasil. 2 Medical and Veterinary Entomology Research Laboratory, U.S. Department of Agriculture, Agricultural Research Service, Gainesville, FL 32604 (e-mail: cgeden@nersp.nerdc.u.edu).
1

house located in the interior of State of Sao Paulo. Monteiro and Pires do Prado (2000) found T. zealandicus emerging from pupae of M. domestica, Chrysomya putoria (Wiedemann), and Muscina stabulans collected in poultry facilities in the interior of Sao Paulo. From monthly samples collected in a poultry facility in the interior of Sao Paulo, during 1997 and 1998, we collected T. zealandicus from pupae of M. domestica and C. putoria. Parasitism at this site was highest from August to December in both years (unpublished data). A colony of T. zealandicus was established from these samples, and laboratory studies of the biology of T. zealandicus were conducted. The objectives of the current study were to evaluate the inuence of different constant temperatures on development time and longevity of this species and to evaluate the effects of nutrition and emergence order on longevity. Materials and Methods Insect Colonies. Tachinaephagus zealandicus were from a colony originally established from samples collected from a poultry farm in Santa Cruz da Conceicao (21 59 S; 47 21 W and 597,0 m), Sao Paulo, Brazil, and had been maintained on C. putoria for 12 generations at the time of testing.
2002 Entomological Society of America

0046-225X/02/03750380$02.00/0

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Parasitoids were maintained in 2-liter clear plastic boxes covered by snap-on plastic lids with screened openings. Cages were stocked with 2,000 parasitoids per cage and held at 25 1 C, 60 10% RH, with a photoperiod of 12:12 (L:D) h. Honey and water were provided to the insects and C. putoria larvae were exposed to 2-d-old females at a host:parasitoid ratio of 20:1 for four consecutive days. Parasitized pupae were removed from the cages daily and held in a rearing chamber at 22 1 C. Chrysomya putoria were also from a colony originally established from the poultry farm in Santa Cruz da Conceicao. Larvae were reared using the diet described by Leal et al. (1982), and adults were held in cages under the environmental conditions described above for T. zealandicus. Flies were given water and sugar ad libitum and periodically given fresh beef liver for egg maturation and oviposition. Inuence of Constant Temperatures on Development Time. T. zealandicus females were exposed to 1,300 C. putoria larvae at a host:parasitoid ratio of 10:1 at 25 C. Twenty-four hours later, parasitized pupae were placed into individual gelatin capsules (size number 00) and placed in groups of 100 in 100-ml clear plastic cups with snap-on plastic lids with screened openings. The pupae were then transferred to rearing chambers set at 16, 18, 20, 22, 25, and 27 C (two replications of 100 pupae per temperature), 70% RH, and a photoperiod of 12:12 (L:D) h. In addition, 100 unparasitized pupae were placed in each chamber as controls. Parasitism under these test conditions was 98%. Pupae were monitored twice daily for parasitoid emergence and the development time at each temperature was determined. The relative emergence success of parasitoids reared at different temperatures was determined by comparing emergence at 22 C with emergence at other temperatures using G-tests of independence to obtain estimates of 2 (Sokal and Rohlf 1981). Development data were t to the thermodynamic model of Sharpe and De Michele (1977) to describe the effects of temperature on development rates for T. zealandicus. The four-parameter form of the model, with high-temperature inhibition, was selected: rK 1 25*K/ 298.15* 1/K }/ 1/K)]}, exp HA/ 298.15* 1/ 298.15 exp HH/1.987* 1/TH

the parameters (SAS Institute 1992). Minor changes were made in the algorithm to accommodate changes in SAS command language since it was published. Regression analysis (observed versus predicted rate data) was performed to evaluate goodness-of-t of the models to the constant temperature data. Inuence of Emergence Order on Longevity at Different Temperatures. Parasitoids that emerged from pupae in the above experiment were isolated daily and placed individually in 100-ml plastic cups with screen lids, given honey and water and kept in the same chambers (at the same temperatures) in which they had completed development. Parasitoid mortality was monitored daily until all parasitoids had died. In this way, we were able to determine whether parasitoid longevity was affected by the order in which parasitoids emerged within a cohort at each temperature. Longevity differences within each temperature as a function of the day of emergence were evaluated by analysis of variance (ANOVA) using the GLM Procedure of SAS (SAS Institute 1992). Sample sizes varied depending on the numbers of parasitoids that emerged on any given day, for an overall average of 32.1 parasitoids per day of emergence and temperature (range, 5 84). Inuence of Temperature and Food Treatment on Longevity. Five hundred parasitized pupae of C. putoria were isolated in gelatin capsules for emergence of T. zealandicus at 25 C. Individual female and male parasitoids were collected within one hour of emergence and placed in 100-ml clear plastic cups covered by snap-on plastic lids with screened openings. Forty parasitoids of each sex were placed in each of six rearing chambers set at 16, 18, 20, 22, 25, and 27 C, 60 10% RH, and a photoperiod of 12:12 (L:D) h. Half of the parasitoids were given water and honey as food, and the other half were given only water (20 male and female parasitoids for each food and temperature combination). Parasitoid mortality was recorded daily. Differences in parasitoid mortality at six temperatures were evaluated by ANOVA, and means separated using Tukeys method under the GLM procedure of SAS (P 0.05) (SAS Institute 1992).

Results Inuence of Different Temperatures on Development Time. Emergence success was greatest at 22 C for both males and females, although there were no signicant differences in emergence success at 18, 20, and 22 C. Signicantly fewer (24.130.4%) parasitoids emerged at the temperature extremes of 16 and 25 C compared with 22 C (Table 1). No emergence was observed at 27 C. Development times for females and males varied from 24.0 to 56.9 d over the range of temperatures from which parasitoids emerged (Table 1). Males and females had nearly identical development times at all temperatures. Median values for development time are also shown in Table 1. The time to 50% emergence was 23.5 d at 25 C for both females and males.

where r(K) development rate at temperature K (in degrees Kelvin), and Rho25, HA, TH, and HH are constants associated with a hypothetical single ratecontrolling enzyme that is limited by high temperatures (Schooleld et al. 1981). Briey, Rho25 is the development rate at 25 C (298.15 K), HA is the enthalpy of activation of the hypothetical enzyme, TH is the temperature (in degrees Kelvin) at which the enzyme is half-inactivated by heat, and HH is the change in enthalpy associated with high-temperature inhibition. Estimates of Rho25, HA, TH, and HH were obtained using the algorithm of Wagner et al.(1984), which uses a sequence of SAS procedures to estimate

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Temp, C

(df

1)

Mean (SE)

Median Observed 56.3 41.7 33.3 26.1 23.5 56.2 41.6 33.0 25.9 23.5 Predictedb 55.7 42.6 32.9 26.2 26.2 55.7 42.4 32.6 25.9 23.5

16 18 20 22 25 27 16 18 20 22 25 27
a

120 317 340 395 140 0 156 501 515 647 182 0

Females 46.22** 1.88NS 0.88NS 36.29** 261.4** Males 71.45** 2.77NS 2.21NS 28.13** 337.6**

56.9 (0.17) 42.3 (0.08) 33.6 (0.05) 27.1 (0.05) 24.0 (0.01) 56.9 (0.15) 42.2 (0.07) 33.6 (0.04) 27.0 (0.04) 24.0 (0.01)

NS, P 0.05, **, P 0.01 (G-test of independence for parasitoid emergence at 22 C compared with emergence at other temperatures). Parasitoid emergence as a percentage of emergence at 22 C. Predicted values from the Sharpe and DeMichele model using parameters presented in Table 2.

Parameter estimates for Sharpe and De Michele thermodynamic model are presented in Table 2, with model predictions and observed data presented in Table 1. The models t the data well in both cases (R2 0.972). Inuence of Emergence Order on Longevity at Different Temperatures. Adults of T. zealandicus emerged on different days, although larvae were parasitized at the same time. The longevity of adults from the same cohort, but which emerged on different days, is presented in Table 3. There was a tendency for greater longevity among parasitoids that emerged earlier rather than later at 16 22 C, although this difference was statistically signicant only at 16, 18, and 22 C. At 16 20 C the latest-emerging parasitoids only lived 45 60% as long as earliest-emerged individuals. Inuence of Temperature and Food Treatment on Longevity. The longevity of females given honey and water decreased with increasing temperature (Table 4). Females reared at 16 C lived approximately three times longer (18.0 d) than those kept at 27 C (6.2 d). Females given honey and water had similar longevities at 16 20 C (14.8 18.0 d). In contrast, females that were given water but not honey only lived for 4.8 7.6 d at all temperatures, and there were no signicant differences in longevity as a function of temperature except at the two temperature extremes (7.6 and 4.8 d at 16 and 27 C, respectively).
Table 2. Parameter estimates ( SE) for models of temperature-dependent rates of development of female and male T. zealandicus, and regression coefcients for goodness of t of predicted versus observed development rates Sex Females Males Model parameter Rho25 0.0590 (0.0076) 0.0603 (0.0072) HA 22040.8 (2779.6) 22437.2 (2565.2) TH 299.5 (0.48) 299.5 (0.33) HH 122,889 (92,338) 118,934 (73,311) R2 0.972 0.999

Similar results were obtained with males. Males that were given honey and water lived about three times longer at 16 C (14.5 d) than those held at 27 C (4.4 d) (Table 4). Males that were given water but not honey lived for 1.8 (27 C) to 7.1 d (16 C), but differences in longevity were small (and not statistically signicant) in the temperature range of 16 25 C. Females lived signicantly longer overall than males at all temperatures except 16 C, but differences due to sex were small compared with the effects of temperature and nutrition. The effect of sex on longevity was modulated by nutrition in some cases, as indicated by signicant sex food treatment interactions at 18 and 22 C. Differences in longevity between males and females were small among parasitoids that were given only water and were only statistically signicant at 27 C. In contrast, females that were given honey and water lived signicantly longer than males in the same food treatment groups at all temperatures except 16 and 20 C. Discussion One of the purposes of this study was to evaluate the response of T. zealandicus to selected constant temperatures. Understanding the response of parasitoids to temperature is critical to elucidation of the numerical relationships between a parasitoid and its host (Ables et al. 1976). T. zealandicus is commonly collected in poultry facilities located in the State of Sao Paulo (Brazil), where it is associated with M. domestica and other muscoid ies such as C. putoria (Silveira et al. 1989, Costa 1989, Monteiro and Pires do Prado 2000). In eld observations during 1998 we observed that T. zealandicus was most prevalent from August to December (M.F.A., unpublished data). Data provided by CATI (Coordenadoria de Assistencia Tecnica In tegral, from State of Sao Paulo) indicated that average temperatures for the nearby city of Santa Cruz da

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Table 3. Inuence of emergence order on mean ( SE) longevity (in days) of T. zealandicus adults (males and females combined) at ve constant temperatures Mean ( SE) longevity of parasitoids that emerged in the following order (in days since day of rst emergence): 1st 16 18 20 22 25 16.9 (0.7) 20.1 (0.6) 17.8 (1.3) 15.7 (0.9) 6.4 (0.8) 2nd 12.4 (0.6) 15.1 (0.9) 15.7 (0.6) 16.2 (0.9) 6.4 (1.1) 3rd 12.4 (0.5) 15.1 (0.9) 14.1 (0.9) 18.5 (0.9) 7.0 (0.5) 4th 10.5 (0.6) 17.9 (0.5) 15.2 (1.5) 10.7 (1.1) 7.2 (1.0) 5th 7.9 (0.8) 17.1 (0.6) 11.0 (4.6) 10.8 (3.6) 6th 8.2 (0.9) 11.2 (1.5) 15.9 (1.1) ANOVA F 15.14** 7.67** 1.63NS 5.18** 0.16NS Overall longevity 10.7 (0.2) 16.4 (0.3) 15.2 (0.4) 15.5 (0.2) 6.9 (0.3)

Temp, C

df 5,271 5,274 4,149 6,115 3,83

Results of one-way ANOVAs for effect of emergence order on longevity at each temperature. (**, P 0.01; *, P 0.05; NS, P 0.05). , No parasitoids emerged.

Conceicao varied from 17.0 to 24.6 C (minimum and maximum, respectively) in August; 18.4 to 25.8 C in September; 19.0 to 25.4 C in October; 19.9 to 28.0 C in November, and 21.7 to 28.9 C in December. In the nal sample that was collected (23 December. 1998) the rate of parasitism by T. zealandicus was 90% (unpublished data). Field records made by Bishop et al. (1996) showed that T. zealandicus isolations were made mostly (22/23 samples) from January through April in New Zealand. Twenty-one of the samples of parasitized larvae were from North Island localities, with Lucilia spp. and Calliphora stygia (F.) identied as hosts in all but four cases. T. zealandicus was also reared from Chrysomya rufacies (Macquart) collected from a sheep carcass in the Wairarapa. Legner et al. (1975) found no evidence of T. zealandicus establishment on California poultry farms after making a large release of T. zealandicus when the M. domestica population was at its peak during January. The reasons for this are not understood, because our data indicate that cooler weather should have favored establishment of this species. T. zealandicus was also recovered once from a dissected Fannia pupa, which suggests that this species can parasitize and kill Fannia spp. (Legner et al. 1975). The apparently greater activity of T. zealandicus during cooler weather in Brazil may be due to innate preferences of this parasitoid for lower temperatures or to increases in the developmental time of its hosts, thus making them available for a longer period of time (Olton and Legner 1974).
Table 4.

No parasitoids emerged in this study when they were held at a constant temperature of 27 C. Olton (1971) also observed no development when parasitoids were held at 29 and 32 C. This does not necessarily mean that short exposures to these higher temperatures are lethal when they occur in a uctuating temperature regime. Liu et al. (1995) reported that conclusions drawn from studies using constant temperatures should be viewed with caution and that the effect of variable temperatures on development rates merits more extensive analysis. Differences in development times between constant and varying temperatures can usually (but not always) be accounted for by the effects of simple rate summation used on the curvilinear relationship between temperature and rate of development. For example, in a related study Geden (1997) observed that constant exposure to 35 C was lethal for Muscidifurax raptor Girault & Sanders and three Spalangia spp., but that uctuating temperature regimes that included 6 h/day of exposure to this temperature resulted in very low mortality. High temperatures can also have indirect effects on the host:parasitoid relationship. Olton (1971) observed that a variable number of parasitoid eggs and early instars were completely encapsulated when their development was retarded by high temperature. Upon eclosion, the rst instar of T. zealandicus retains the chorion for 8 12 h. In many cases the chorion is melanized when it is displaced into the hemolymph of the host. This melanization of cast chorions accounts for the black bodies present in hosts containing para-

Mean ( SE) longevity of females and males of T. zealandicus at six constant temperatures under two feeding treatments Mean ( SE) longevity (in days) of parasitoids at temp ANOVA F Sex 3.19NS 28.61** 8.41** 6.50* 9.29** 46.64** Feeding trt 65.19** 65.24** 114.93** 43.62** 5.94** 30.94** Sex Feeding trt 1.90NS 15.67** 0.07NS 5.24* 2.02NS 2.62NS

Temp, C Honey 16 18 20 22 25 27

Females given: water Water only 7.6 (1.15)Ba 6.4 (0.34)BCab 7.1 (0.16)Ba 6.8 (0.33)Cab 6.7 (0.14)Bab 4.8 (0.94)Bb Honey 18.0 (1.27)Aa 17.6 (1.20)Aa 14.8 (1.02)Aab 13.6 (0.79)Ab 8.6 (0.80)Ac 6.2 (0.58)Ac

Males given: water Water only 7.1 (0.94)Ba 5.1 (0.47)Cab 4.7 (0.34)Bb 6.6 (0.45)Cab 5.9 (0.25)Bab 1.8 (0.13)Cc 14.5 (1.03)Aa 8.9 (1.31)Bbc 12.9 (1.01)Aab 9.9 (1.18)Bbc 6.3 (0.51)Bcd 4.4 (0.37)Bd

Means within columns followed by the same lowercase letter and means within rows followed by the same uppercase letter are not signicantly different at P 0.05 using Tukeys method. Results of two-way ANOVAs run separately for each temperature. df 1, 76 for all model effects (**, P 0.01; *, P 0.05; NS, P 0.05). trt, treatment.

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sitoid early instars (M.A.F.A., unpublished data). Apparently, incomplete melanization in this species is a normal oxidative phenomenon and a host defense reaction. The process of cellular encapsulation results when the hosts hemocytes surround and adhere to the surface of the invading object, forming a multicellular capsule-like envelope. Factors that can affect the frequency of parasitoid encapsulation include host and parasitoid species, the hosts physiological age and physiological condition, the host origin (or strain), superparasitism, and the rearing and/or ambient temperature (Blumberg 1997). Our development times were similar to those observed by Olton (1971). Although T. zealandicus is active in the eld during months when ambient temperatures are near levels that appear to be lethal, it is possible that parasitoid and host behaviors limit their exposure to high-temperature extremes. Because T. zealandicus is a parasitoid of dipteran third instars, the temperature conditions that the parasitoids experience as immatures are determined by the habitat and microclimate selections of the hosts after they have been parasitized. Little is known about the depth at which host larvae pupate in the eld, but they are commonly found several cm below the surface of the soil in open-sided poultry houses. Temperature conditions in the soil are less volatile than ambient air temperatures. For example, we observed in the eld that if the air temperature was 28 C, the temperature of the soil ( 5 cm of depth) was 2324 C (unpublished data). The high humidity ( 70%) and relatively low temperatures experienced by parasitized pupae under these conditions would favor parasitoid survival even when ambient air temperatures routinely exceed the upper developmental limit of 25 C. Presumably, parasitoid survival would be even higher at greater depths. Olton (1971) found that the lower threshold for development of T. zealandicus is near 15 C. The lower temperature that we used was 16 C. It is possible that host encapsulation is promoted by low temperatures as well as at the higher temperatures. It would be interesting to investigate development rates and host encapsulation using other species of ies as hosts such as M. domestica and Sarcophaga bullata. Muscoid ies in poultry houses often are attacked by other parasitoids, mostly in the pteromalid genera Muscidifurax and Spalangia. The rates of development of M. raptor and S. endius observed by Ables et al. (1976) showed that M. raptor undergoes limited development at 12.8 C and after 7 mo, when transferred to 26.7 C produced adult parasitoids within 10 d. The upper threshold for this species appears to be between 32.2 and 35 C (Ables et al. 1976, Geden, 1997, Mann et al. 1990). These authors reported that S. endius cannot survive prolonged exposure to low temperatures. Development rates at 22 C for M. raptor and S. endius were 28 and 39 d, respectively, compared with our results of 27 d at this temperature for T. zealandicus (Table 1). These three parasitoid genera occur sympatrically in our region (Ferreira de Almeida and Pires do Prado 1999, Monteiro and Pires do Prado 2000; M.A.F.A., unpublished data).

Our observed development times are similar to those of two other gregarious encyrtid parasitoids of squash bug eggs: Ooencyrtus anasae (Ashmead) and a closely related species Ooencyrtus sp. near anasae (Tracy and Nechols 1987). These species complete development in 18 d at 26.6 C to 32 d at 20.8 C. In our study, longevity of T. zealandicus was examined from two standpoints. First, we evaluated the longevity of individuals as a function of emergence order after having been reared at different temperatures. Emergence at all temperatures was distributed over several days, an observation that agrees with those of Olton (1971). Our results indicate that the parasitoids that emerge early have greater tness, at least regarding longevity, than those that emerge later (Table 3). This response was strongest at the lower temperatures of 16 20 C. Legner (1969) tested several solitary endo- and ectoparasitic species of muscoid Diptera and found that the size and density of hosts inuenced the distribution of emergence times. He alluded to various hypotheses proposed to explain this variation and found that differential larval and pupal development and delayed adult emergence were the causes for differences in emergence patterns among closely related species. The other aspect of longevity that we examined was the inuence of food treatment on longevity at different temperatures. Parasitoids that were given honey and water lived two to three times longer than those that were only given water. Madar and Miller (1983) found that adult longevity of Apanteles yakutatensis (Hymenoptera: Braconidae), a primary and gregarious larval endoparasitoid of Autographa californica (Speyer) (Lepidoptera: Noctuidae) was signicantly increased when the parasitoids were provided with a sugar-water food source. Nothing is known about the feeding behavior and nutritional ecology of T. zealandicus in the eld, so it is not known whether this species forages for nectar sources in nature. They do not host-feed and do not require a protein meal to develop their ovaries. If host larvae are present, the mortality of females increases rapidly after they have oviposited, and longevity is actually reduced substantially in the presence of hosts (M.A.F.A., unpublished data). This is why we did not include host larvae as a food treatment in the tests. Our results may thus be seen as representing the longevity of parasitoids that are searching for but have not yet located host larvae to attack. Fly larvae under eld conditions vary widely in abundance and are patchily distributed, so the parasitoids must be able to survive until they nd them. Field studies are needed to evaluate possible and actual carbohydrate sources for T. zealandicus under natural conditions. Further investigations also will be necessary to compare host attack rates and progeny production of T. zealandicus at different temperatures. Data on temperature-dependent host attacks are available for other parasitoids that occupy the same niche as T. zealandicus, and there are substantial differences among these species in their temperature optima for host attacks. For example, S. gemina is most effective

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at 25 C, S. cameroni is similar in the 20 30 C range but less effective of 15 and 35 C, and M. raptor is equally effective at killing y pupae at all temperatures tested except at the high extreme of 35 C (Geden 1996). Similar data are needed for T. zealandicus to determine the climatic zones in which it is most likely to be an effective biological control agent of muscoid ies. Acknowledgments
We thank J. C. Piva for allowing us to collect insect samples from his poultry farm, and O. Ferreira de Almeida for helping with the samples. This project was supported by FAPESP (Fundaca de Amparo a Pesquisa do Estado de Sao Paulo) o ` Process # 96/1570 8.

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