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Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) Parasitism of Trichoplusia ni (Lepidoptera: Noctuidae) Eggs Under Different Temperatures

Author(s) :Thiago Da Silva Alto, Dirceu Pratissoli, Jos Romrio De Carvalho, Hugo Jos Gonalves Dos Santos Junior, Joo Paulo Pereira Paes, Regiane Cristina Oliveira De Freitas Bueno, and Adeney De Freitas Bueno Source: Annals of the Entomological Society of America, 105(1):82-89. 2012. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1603/AN11116 URL: http://www.bioone.org/doi/full/10.1603/AN11116

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ARTHROPOD BIOLOGY

Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) Parasitism of Trichoplusia ni (Lepidoptera: Noctuidae) Eggs Under Different Temperatures
THIAGO DA SILVA ALTOE,1 DIRCEU PRATISSOLI,1 JOSE ROMARIO DE CARVALHO,1 HUGO JOSE GONCALVES DOS SANTOS JUNIOR,1 JOAO PAULO PEREIRA PAES,1 REGIANE CRISTINA OLIVEIRA DE FREITAS BUENO,2 AND ADENEY DE FREITAS BUENO3,4

Ann. Entomol. Soc. Am. 105(1): 8289 (2012); DOI: http://dx.doi.org/10.1603/AN11116

ABSTRACT A study of the biological characteristics and thermal requirements of the parasitoid Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae) on eggs of Trichoplusia ni (Hubner, 1802) (Lepidoptera: Noctuidae) at several different temperatures was performed in this work. Eggs of T. ni were exposed to T. pretiosum strain Tspd parasitism for 5 hr and then transferred to environmentally controlled growth chambers set at the temperatures of 18, 21, 24, 27, 30, and 33 1 C. The duration of the T. pretiosum egg-to-adult period was affected by temperature, varying from 6 to 18 d over the range of the studied temperatures. The number of individuals emerged per egg and the sex ratio also were affected by temperature variations, but regression analysis did not nd correlation between the increase of temperature and the observed variation of these biological parameters. Similarly, parasitism viability (percentage) was inuenced by temperature variation, but always exceeded 80% at all tested temperatures. The thermal lower limit of development (Tbase) and the thermal constant (K) for T. pretiosum were 11.84 C and 128.37 DD, respectively. These results here reported indicate that T. pretiosum was impacted by the temperature, however, this parasitoid had a satisfactory performance on T. ni eggs at all studied temperature (from 18 to 33 C), showing potential to be used successfully as a biological control agent of this pest in different regions that t in this tested temperature range. Also, the rearing temperature of this parasitoid might be changed from 18 to 33 C, according to commercial demands for accelerating or retarding mass production for eld releases without damages to the parasitoid development. KEY WORDS Insecta, biological control, egg parasitoid, biological characteristic

The cabbage looper, Trichoplusia ni (Hubner, 1802) (Lepidoptera: Noctuidae), is an important pest worldwide attacking an large range of hosts including plants of the families Brassicaceae, Fabaceae, Solanaceae, and Cucurbitaceae, among others. Therefore, this pest has been found throughout South America, Canada, Mexico, the United States, and wherever those crops are cultivated on any other country or continent (Janmaat and Myers 2003, Milanez et al. 2009). Traditionally, insecticides have been the most common control measure employed against T. ni outbreaks on those different crops (Maxwell et al. 2006), which are often overused by growers. It triggers some negative effects (Song and Swinton 2009) such as pesticides rapid
1 Universidade Federal do Esprito Santo, Centro de Ciencias Agra rias, Departamento de Produca Vegetal, Nucleo de Desenvol o vimento Cientco e Tecnologico em Manejo Fitossanita rio, Setor de Entomologia, Alto Universita rio, s/ no Cx. Postal 16, Guararema 29500-000, Alegre, State of Esprito Santo, Brazil. 2 Universidade de Rio Verde, FESURV, Fazenda Fontes do Saber, Caixa Postal 104. Rio Verde, State of Goia 75901-970, Brazil. s, 3 Embrapa Soja, Caixa Postal 231, 86001-970, Londrina, State of Parana Brazil. , 4 Corresponding author, e-mail: adeney@cnpso.embrapa.br.

selection of pest strains that are resistant to a given active ingredient (Diez-Rodriguez and Omoto 2001) or the reduction of natural biological control agents, especially when broad spectrum insecticides are used (Carmo et al. 2010). Because chemicals still are inevitable in todays agriculture, a way of addressing this problem aiming at maintaining the sustainability of agriculture, over medium and long terms, is the adoption of integrated pest management (IPM) principles, which aim toward the rational use of insecticides as well as the harmonious integration of different control strategies (Pratissoli et al. 2008, Zalucki et al. 2009). Among these strategies, a lot of attention has been given to the biological control, which has been emphasized by researchers as a promising alternative to insecticide application (Bueno et al. 2009a,b) helping to reduce the negative impacts of intensive agriculture on the environment (van Lenteren and Bueno 2003). Regarding the biological control strategy, a procedure that has shown efcient results in controlling pest outbreaks, mainly from the order Lepidoptera such as the T. ni, is the release of egg parasitoids from the genus Trichogramma (Hymenoptera: Trichogramma-

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tidae) (Parra et al. 1987). This genus belongs to the most studied and used groups of natural enemies applied worldwide for the biological control of caterpillars (Parra et al. 1987, Pratissoli et al. 2008, Bueno et al. 2009a). The Trichogramma genus contains 180 species, has a wide geographical distribution, and its members are used for efcient control of a large number of economically important insect pests, such as T. ni, among others (Bueno et al. 2009a). Some of the advantages in using Trichogramma spp. in biological control programs are that these egg parasitoids are reared easily on alternative hosts such as the Anagasta kuehniella Zeller (Lepidoptera: Pyralidae), considered the most appropriated factious host, and are highly aggressive in parasitizing eggs of different pest species as well (Smith 1996, Wajnberg and Hassan 1994). Studies on Trichogramma spp. have been carried out in 50 countries and commercial releases occur in 32 million ha every year (Smith 1996). However, it is important to point out that the success of Trichogramma spp. release basically depends on the knowledge of the biological characteristics of the selected parasitoid specie to be used, and on its interaction with the specic host, because these characteristics are determinant to the parasitoid efciency in controlling the targeted pest species in eld conditions (Bourchier and Smith 1996). Therefore, previous laboratory studies are crucial to properly evaluate the parasitoid biology, parasitism capacity and viability, and its biological cycle of the parasitoid, among other biological features that might differ among the different Trichogramma species and strains, and also may vary according to host and temperature (Hassan 1997, Scholler and Hassan 2001). Therefore, it is also important to determine its thermal requirements as to allow predicting the ideal temperature for parasitoid development. This is especially important in planning parasitoid mass rearing in laboratory, because through the knowledge of the thermal requirements it is possible to predict the day of the parasitoid eclosion, thus allowing the fulllment of eld needs (Haddad et al. 1999). The knowledge of these characteristics allows us to determine the optimal temperature for insect development, thus optimizing the rearing of the host and the parasitoid, as well as to determine the parasitoids potential as a biological control agent for a given pest and region (Pratissoli and Parra 2000). Moreover, it allows us to better understanding the parasitoid efcacy on eld conditions accordingly to the climatic challenges faced by the biological control agent after its release. Therefore, this research aimed at evaluating the biological characteristics and thermal requirements of T. pretiosum on eggs of T. ni, to provide information to support the use of this egg parasitoid in future biological control program of T. ni. T. pretiosum strain Tspd was chosen as the best egg parasitoid to be used in this research because Milanez et al. (2009) studying different species of Trichogramma including different strains of T. pretiosum showed that T. pretiosum strain Tspd, which is a strain collected in Piracicaba County, Sa Paulo o State Brazil, voucher specimen number Tspd deposit

at Nucleo de Desenvolvimento Cientco e Tecnolo gico em Manejo Fitossanita rio de Pragas e Doencas, NUN EMAFI from Federal University of Espirito Santo State, Brazil, statistically was more efcient than other tested species or strains of Trichogramma on controlling T. ni. Materials and Methods The experiment was carried out under laboratory controlled conditions at the Nucleo de Desenvolvi mento Cientco e Tecnologico em Manejo Fitossani ta de Pragas e Doencas (NUDEMAFI) of the Enrio tomology Department of the Agrarian Sciences Center of the Federal University of Espirito Santo, Brazil (CCA-UFES). The experiment consisted of the following steps: Cultures of the Parasitoid and Hosts. The culture of T. pretiosum strain Tspd that had the best performance among different species and strains on T. ni were established as described by Bueno et al. (2009a). Eggs of the factitious host Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae) were glued with the aid of gum arabic (30% wt:vol) on cardboard (8.0 cm by 2.0 cm) and rendered nonviable by exposing them to UV light, thus preventing cannibalism of the parasitized eggs (Stein and Parra 1987). After that, the eggs were offered for parasitism for 24 h. Newly emerged parasitoids were used either for trials or for maintaining cultures. As a source of food for these parasitoids, small drops of honey were placed in the tubes. This parasitoid culture were kept in climate chambers set to environmental conditions of 25 2 C temperature, 70 10% RH, and a photoperiod of 14:10 (L:D) h. T. ni culture also was kept under the same controlled environmental conditions (25 2 C temperature, 70 10% RH, and a photoperiod of 14:10 [L:D] h) in the laboratory. The caterpillars originally were collected at Domingos Martins County, Espirito Santo State, Brazil, infesting cabbage plants and reared on the articial diet made with water (3,400 ml), agar (46 g), dry beans (250 g), wheat germ (200 g), soybean protein (100 g), casein (75 g), torula yeast (125 g), ascorbic acid (12 g), vitamin mixture (20 g), tetracycline (250 mg), formalin (40%), methyl P-hydroxybenzoate (10 g), and sorbic acid (6 g) as proposed by Greene et al. (1976). At pupae stage the insects were sexed and placed in plastic pots containing moistened lter paper in the bottom. After emergence, the adults were transferred to 60-cm by 50-cm by 50-cm woodenframe cages, each containing a cabbage leaf that was used as an oviposition site. A 10% honey solution, renewed every 48 h, was used to feed the adults. Effect of Temperature on T. pretiosum Development. Eggs of T. ni between 12 and 14 h old were collected from cabbage leaves with the aid of a brush, and transferred to 2.0-by 4.0-cm Bristol-board cards (MD Nicolaus, Brazil). On each card, 20 T. ni eggs were glued using 30% (wt:vol) gum Arabic. This card with eggs was transferred to a glass tube, which then was sealed with PVC lm. Immediately after, two T. pretiosum females up to 6 hr old were introduced into

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each tube, allowing parasitism for 5 hr (Pratissoli 1995). The tubes then were maintained in climate chambers set at 25 1 C, 70 10% RH, and a photoperiod of 14:10 (L:D) h. After that period, the parasitoids were removed, and the vials then were placed into environmental chambers set at different constant temperatures (mean SD) of: 18 1 C, 21 1 C, 24 1 C, 27 1 C, 30 1 C, and 33 1 C, 70 10% RH (RH); and a photoperiod of 14:10 (L:D) h. These temperatures were chosen for the study based on previous researches with different Trichogramma species and strains that evaluated the range from 15 to 34 C (e.g., Butler and Lopez 1980, Bueno et al. 2009a). The following biological parameters then were evaluated: developmental time (egg to adult), percent emergence (viability), number of parasitoids per host egg, longevity, and sex ratio (number of female/[number of female number of male]). Trials were carried out in a completely randomized design with seven treatments (temperatures) and 10 replications per treatment (each replication made of 20 T. ni eggs). Evaluations were performed on a daily basis to precisely determine T. pretiosum developmental time (egg to adult). The parasitoid emergence was evaluated by counting the hatched eggs with the aid of a stereomicroscope. Results data were computed for normality and then submitted to analysis of variance (ANOVA). If data had normal distribution, means were compared by Tukey test (P 0.05) (SAS Institute 2001). In addition, regression analyses were used to further understand the relationship between the temperature variation and the observed results. The choice of the equation that best t the data were based on the biological parameters, the coefcient of determination (R2), the signicance of the coefcients of regression ( i), and regression by F test, at 5% probability. Determination of T. pretiosum Thermal Requirements and Developmental Rate. Lower thermal threshold (Tbase) (expressed in degrees Celsius) and thermal constant (K) (expressed in degree-days) were estimated as reported previously by Bueno et al. (2009a) and Mascarini and Prado (2002). First, the total development time of T. pretiosum strain Tspd on eggs of T. ni was recorded at constant temperatures of 18, 21, 24, 27, 30, and 33 C (with 1 C of maximum variation) as detailed previously. The base development temperature (Tbase) was determined by the hyperbole method (Bean 1961) using the total development times from these six constant temperature groups. Thermal constant (K) was obtained from the equation K D(T-Tbase), where K thermal constant, D development time (hours), T temperature in which the insect grew, and Tbase base temperature of the insect (Krebs 1989). Results Egg-to-Adult Period (Days). T. pretiosum egg-toadult period reared on eggs of T. ni was affected signicantly by temperature, showing an inverse correlation with the increase in temperature, besides be-

ing different among all tested temperatures (Fig. 1A, Table 1). This parameter was 18.0 d at 18 C and 6.0 d at 33 C, i.e., an increase in temperature from 18 to 33 C shortened the eggadult period by 12 d (Table 1). Number of Parasitoids per Egg. The number of parasitoids per host egg varied among the different tested temperatures from 1.3 adult per egg (at 24 C) to 2.0 adult per egg (at 33 C) (Table 1). Even thought this difference was signicant according to Tukeys test (F 6.29, P 0.001), regression analysis showed that this difference was not directly correlated to the temperature variation, with a mean emergence of 1.6783 parasitoids per T. ni egg found at all temperatures studied (Fig. 1B). Sex Ratio. Similar to results recorded for the number of parasitoids per egg, the number of females divided by the number of total emerged parasitoids was from 0.57 to 0.72. It is important to emphasize that the recorded sex ratio was always superior to 0.5 (Table 1). Regression analysis did not nd a correlation between sex ratio and the temperature variation, with a mean sex ratio of 0.6436 (Fig. 1C). Parasitism Viability. T. pretiosum parasitism viability (percent emergence) when reared on T. ni eggs was affected by temperature over the range between 18 and 33 C (Fig. 1D). Despite some variation, however, viability always exceeded 80% (Table 1). Determination of T. pretiosum Thermal Requirements and Developmental Rate. The developmental rate in the eggadult period was obtained as a function of the parasitoid development at the temperatures of 18, 21, 24, 27, 30, and 33 C (Fig. 2). The data resulted in estimates of the lower thermal limit (Tbase) and thermal constant (K) of 11.84 C and 128.37 DD, respectively. Discussion The biological characteristics of T. pretiosum strain Tspd reared on T. ni eggs in laboratory conditions were inuenced by temperature, indicating that this parameter might affect the success of a biological control program using this biological control agent in the eld. Egg-to-Adult Period (Days). The development time needed for the parasitoid development decreased as the temperature increased, with statistically signicant differences among all studied temperatures. This shortening of the development time in response to temperature increase occurs as a consequence of the increase in the metabolic activity of the parasitoids (Bueno et al. 2009a). The longest time (18 0.08 d) required for T. pretiosum to complete its development on eggs of T. ni was at 18 C. This result was lower from the recorded time required for a different T. pretiosum strain to complete its development on the same egg host, which was around 24 and 17.6 d at 17 and 20 C, respectively (Butler and Lopez 1980). These authors, however, found similar results to the ones here reported regarding higher temperatures, with differences returning and set to occur when the temperature was 32 C. At 33 C, Butler and Lopez (1980) reported an increase in the required time to complete

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Fig. 1. Egg-to-adult developmental period (days) (A), number of individuals emerged per host egg (B), sex ratio (C), and percent emergence (viability) (D) of T. pretiosum reared on eggs of T. ni under different temperatures, constant 70 10% RH, and a photoperiod of 14:10 (L:D) h.

T. pretiosum development, whereas our results kept the same tendency of decreasing the needed time. These small differences might be because of the Trichogramma strain adaptation to the specic host and temperature because T. pretiosum strain Tspd was collected in Brazil, a tropical country where T. ni has been of widespread occurrence for many years, offering time for the co-evolution between this pest species and the T. pretiosum strain Tspd, which might have allowed an adaptation of the parasitoid to the

eggs of this specic host and temperature to span higher than the other T. pretiosum strains. It raties the crucial importance of this knowledge of strain differences in regard to developmental rate for widespread application of augmentative releases of Trichogramma spp. (Butler and Lopez 1980). Similar data were obtained by Bueno et al. (2009a) in studies of T. pretiosum strain RV on eggs of Pseudoplusia includens Walker and Anticarsia gemmatalis Hubner (Lepidoptera: Noctuidae). The parasitoid

Table 1. Trichogramma pretiosum biological characteristics when the parasitoid was reared on eggs of Trichoplusia ni at different constant temperatures, 70 10% RH, and a photoperiod of 14:10 (L:D) h Temperature C 18 21 24 27 30 33 F P df Mean Egg-to-adult period (days) (Mean SE) 18.0 0.08a 14.0 0.08b 13.0 0.08c 8.0 0.08d 7.0 0.09 6.0 0.08f 3353.29 0.001 59 No. parasitoids per egg (Mean SE) 1.9 1.9 1.3 1.7 1.5 2.0 0.08ab 0.04ab 0.03c 0.16abc 0.14bc 0.12a 6.29 0.001 59 Sex ratio (Mean SE) 0.68 0.72 0.57 0.66 0.66 0.57 0.04ab 0.02a 0.01c 0.03bc 0.03bc 0.04c 8.27 0.001 59 Parasitism viability (%) (Mean SE) 100.0 100.0 100.0 95.7 88.1 83.8 0.00a 0.00a 0.00a 2.39ab 5.16ab 3.41b 3.15 0.014 59

SE followed by the same letter within column are not statistically different according to the Tukey test, at 5% probability.

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Fig. 2. Development time (days) and development rate (1/d) of T. pretiosum strain Tspd reared on eggs of T. ni under different temperatures, constant 70 10% RH, and a photoperiod of 14:10 (L:D) h. Tbase base temperature (degree Celsius), K thermal constant (degree-days).

took longer to develop on eggs of P. includens, mainly at 18 C, when the difference was 3.35 d. At the remaining temperatures, the differences among the developmental times on the two hosts were negligible. Salt (1940) reported that for T. evanescencens the developmental rate is not only affected by temperature, but also by the host by which the parasitoid is reared. This also was observed for other Trichogramma species and strains for which different data were recorded regarding to egg-to-adult period (Pratissoli 1995, Zago et al. 2006). Thus, this biological parameter depends not only on temperature variation, but also on the adaptation of the Trichogramma strain to the studied host and temperature (Pratissoli and Parra 2000). Because in the literature it has not been reported that there were large differences in the biology of Trichogramma spp. when the parasitoid was laboratoryreared under constant or uctuating temperatures (Consoli and Parra 1995a,b; Butler and Lopez 1980), it indicates that this biological control agent will perform similarly on T. ni in the eld conditions. Number of Parasitoids per Egg. The emergence of different numbers of parasitoids per host egg is directly related to the size and the nutrition quality of the egg as a host to support Trichogramma spp. development of one or more individuals(Bueno et al. 2009a). When a single parasitoid emerges per host eggs, it is probably a consequence of the mortality that occurs when more than one Trichogramma egg is laid inside the same host egg. It occurs mainly because of the competition for nutrients. This phenomenon has already been reported for Telenomus remus Nixon 1937 (Hymenoptera: Scelionidae) and other strains of T. pretiosum (Dass and Parshad 1983). For most of the hosts, however, the emergence of more than one parasitoid per host egg is quite common, mainly at laboratory conditions where the insect is conned inside tubes with a restrict number of host eggs. It is impor-

tant to point out that even in these conditions; the emergence of more than one adult of the parasitoid per egg might vary in different host species. Differences in host eggs had been pointed out previously as an important feature of Trichogramma spp survival and development by Consoli et al. (1999). These differ ences found for different host eggs already have been reported in the literature. Bueno et al. (2009a) reported the emergence of a single T. pretiosum per egg of Pseudoplusia includens, whereas a higher number of adults emerged when the host was Anticarsia gemmatalis. These differences might be because of the bigger size of the A. gemmatalis eggs as compared with the eggs of P. includens. Consequently, the higher amount of nutrients available was directly responsible for the number of adults supported per egg host (Parra 1997). Furthermore, the number of offspring of T. pretiosum on eggs of T. ni reported here are higher than previous studies of Trichogramma atopovirilia Oatman and Platner, 1983 (Hymenoptera: Trichogrammatidae) on Diaphania hyalinata Lineau, 1758 (Lepidoptera: Pyralidade) (Melo et al. 2007) demonstrating that T. ni offer good nutritional quality for T. pretiosum development. Sex Ratio. Temperature often has been reported as a highly important factor in determining the sex ratio in species of Trichogramma (Parra and Sales 1995, Pratissoli and Parra 2000, Pratissoli et al. 2009). However, the inuence of temperature on the sex ratio in Trichogramma varies according to the species, strain, or both (Bueno et al. 2009a). Temperature changes altered the sex ratio of T. pretiosum and Trichogrammatoidea annulata De Santis, 1972 (Hymenoptera: Trichogrammatidae) (Maceda et al. 2003), which did not occur with T. galloi; T. pretiosum; T. atopovirilia; T. distinctum Zucchi, 1988; and T. exiguum Pinto & Platner, 1978 (Hymenoptera: Trichogrammatidae) on different hosts (Calvin et al. 1984, Melo et al. 2007).

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In our study, more females than males of T. pretiosum emerged from eggs of T. ni, independently of temperature. According to Vinson (1997), the quality of the host is the main factor affecting the sex ratio of Trichogramma species. This sex ratio may occur as a consequence of the capacity of Trichogramma females to differentiate between host species, generating males or females according to the host quality. The inuence on the sex ratio also may be related to the different survival capacity of Trichogramma males and females within the host egg. Also, it is important to consider the presence of bacteria, from the genus Wolbachia, inside the female reproductive system of some Trichogramma species. These bacteria might be responsible for reproductive incompatibility, parthenogenesis, and feminization (Werren 1997), and their role on Trichogramma spp. sex ratio still is unknown (Stouthamer and Luck 1993, Tagami et al. 2001). Because the temperature did not have a huge impact of T. pretiosum strain Tspd sex ratio, we might suppose that this strain is not infected by this bacterium. Parasitism Viability. The values of percent emergence (viability), even with the difference observed at 33 C, were always above 80%, higher than the results for T. exiguum and T. pretiosum reared on eggs of Plutella xylostella (L., 1758) (Lepidoptera: Plutellidae) (Pereira et al. 2004) and Trichogramma pratissolii Querino & Zucchi, 2003 (Hymenoptera: Trichogrammatidae) on eggs of A. kuheniella and Corcyra cephalonica (Stainton, 1865) (Lepidoptera: Pyralidae) (Zago et al. 2006). These observations indicate that the parasitism viability of Trichogramma might be more inuenced by the host, and that the eggs of T. ni provide favorable conditions for the development of T. pretiosum within the temperature range of 18 to 33 C. Determination of T. pretiosum Thermal Requirements and Developmental Rate. The thermal requirements of insects can be appraised by K and, Tbase is the lowest temperature where metabolic processes result in a net substance gain in biomass (Sitte et al. 1999). They are essential parameters for the determination of the beginning and the end of the insect growing. Therefore, they have inuence on the modeling of annual insect population increase. These parameters have been used for many years in forecasting the insect occurrence and distribution in different areas (Mascarini and Prado 2002) and therefore, their knowledge is essential to understanding T. pretiosum strain Tspd potential to parasitize T. ni eggs in different regions. In this context, the embryonic development of T. pretiosum on eggs of T. ni is initiated when the temperature remains above 11.84 C (Tbase) and the accumulation of heat for its complete development is 128.37 DD (K). On one hand, Melo et al. (2007) reported similar results for T. atopovirilia on eggs of D. hyalinata. Those authors obtained Tbase and K estimates of 11.99 C and 130.42 DD, respectively. However, higher values were found by Foerster and Foerster (2009), who studied the biological aspects of the parasitoids T. pretiosum; T. atopovirilia; Trichogramma acacioi Brun, Moraes & Soares, 1984; Trichogramma lasallei Pinto 1999; and Trichogramma rojasi Nagaraja

& Nagarkatti 1973 (Hymenoptera: Trichogrammatidae) on eggs of A. gemmatalis at temperatures of 14, 18, 21, 26, and 30 C, and observed base temperature values of 9.60, 10.20, 8.10, 10.10, and 9.20 C, respectively. Moreover, Pratissoli et al. (2006) reported gures oscillating between 8.70 and 13.45 C, and 96.09 and 157.32 DD for the base temperature and thermal constant, respectively. This is probably because of the difference adaptation of the strain to the specic target host and temperature. Thus, the determination of the biological characteristics and thermal requirements of T. pretiosum, strain Tspd, on eggs of T. ni provided important information for the implantation and maintenance of a biological control program with this species, because the results obtained here demonstrate that this strain is able to develop from wide range of temperature (from 18 to 33 C). It is worth emphasizing that, although temperature is considered extremely important, it is not the only factor responsible for changes in the development and survival of Trichogramma spp. Other abiotic factors, such as photoperiod and relative humidity, and biotic factors, such as interspecic and intraspecic competition, may interfere with these biological characteristics (Parra 1997, Pratissoli and Parra 2001). Another point to be considered is the specic ability of T. pretiosum Tspd to introduce the ovipositor into the corium of the T. ni eggs once the egg gradually loses its turgidity after an increase in temperature (Bueno et al. 2009), an issue that certainly can be further studied in future researches aiming at the control of T. ni using egg parasitoids. Acknowledgments
We thank the Coordenaca de Aperfeicoamento de Pes o soal de Nvel Superior (CAPES) and the Conselho Nacional de Desenvolvimento Cientco e Tecnologico (CNPq) for the supported provided. Thanks also are extended to Janet W. Reid, Ph.D., JWR Associates, for the English revision of the manuscript.

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