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Brazilian Archives of Biology and Technology

versão impressa ISSN 1516-8913versão On-line ISSN 1678-4324

Braz. arch. biol. technol. v.46 n.1 Curitiba jan. 2003 

Temperature effects on Trichogramma pretiosum Riley and Trichogrammatoidea annulata De Santis



Arlei MacedaI; Celso L. HohmannII; Honório R. dos SantosIII

ISecretaria de Estado da Agricultura e Abastecimento; Av. Souza Naves, 2410; 86870-000; Ivaiporã - PR - Brazil
IIÁrea de Proteção de Plantas; Instituto Agronômico do Paraná - IAPAR; C. P. 481; 86001-970; Londrina - PR - Brazil
Dept. de Ciências Exatas e Biológicas; UFMS; 79804-970; Dourados - MS - Brazil





The influence of temperature on lifetime attributes of Trichogramma pretiosum Riley and Trichogrammatoidea annulata De Santis (Hymenoptera: Trichogrammatidae) was evaluated at four constant temperatures (15, 20, 25, and 30º C), RH 70 ± 10%, photophase 14 h. Anagasta kuehniella (Lepidoptera: Pyralidae) eggs were used as hosts. Developmental times of both parasitoid species were similar when exposed to 20, 25, or 30º C. T. annulata, however, developed slightly faster than T. pretiosum at 15º C. Emergence rates of both species were above 89%. The temperature threshold for T. pretiosum and T. annulata was 11º C and the number of degree-days required for their development was 126.9 and 122.3, respectively. Parasitization was maximal at 25º C. T. annulata, however, parasitized significantly more hosts than T. pretiosum in the entire temperature range. Temperature had no effect in brood size.T. annulata progeny consisted predominantly of males, except at 15º C, whereas in T.pretiosumitconsisted predominantly of females, except at 30º C. Parental females lived longer than males.

Key words: Insecta, biological control, avocado fruit borer, temperature


A influência da temperatura sobre parâmetros biológicos de Trichogramma pretiosum Riley e Trichogrammatoidea annulata De Santis (Hymenoptera: Trichogrammatidae) foi avaliada à 15, 20, 25 e 30° C. Foi usado como hospedeiro ovos de Anagasta kuehniella (Lepidoptera: Pyralidae). A progênie de ambos parasitóidesapresentou um desenvolvimento similar quando submetidas a 20, 25 ou 30º C. T. annulata, contudo, apresentou um desenvolvimento ligeiramente mais rápido que T. pretiosum à 15° C. A porcentagem de emergência foi elevada para ambas espécies em todas as temperaturas, não havendo influência destas sobre o número de parasitóides emergindo por hospedeiro. O número de graus dia para desenvolvimento de T. pretiosum e T. annulata foi 126,9 e 122,3, respectivamente, e a temperatura base de desenvolvimento 11° C. A taxa de parasitismo aumentou com o aumento da temperatura, sendo máxima a 25° C. Fêmeas de T. annulata,entretanto, parasitaram um número significativamente maior de hospedeiros que T. pretiosum nas quatro temperaturas. A progênie de T. annulata foi constuída principalmente por machos, exceto a 15° C, enquanto que a de T. pretiosum por fêmeas, exceto a 30° C. A longevidade de ambas espécies de parasitóides diminuiu com o aumento da temperatura sendo que as fêmeas viveram por um periodo significativamente maior que os machos.




The avocado fruit borer, Stenoma catenifer (Wals.) (Lepidoptera: Elachistidae) hasbecome a key pest on avocado, Persea americana (L.) in Brazil in the last decades. When infestations are high, the yield are low, which in pesticide free groves may reach 100% (Hohmann and Meneguim, 1993). As control measures have relied mainly on highly toxic insecticides, studies were initiated to evaluate other methods to reduce pest damage on avocados (Hohmann et al.,2000; Hohmann et al.,2001). The studies also included the identification of parasitoids in the family Trichogrammatidae. This family comprises the most studied and used egg parasitoids of lepidopterans worldwide (Hassan, 1988; Li, 1994). Two species were reared from S. catenifer eggs: Trichogramma pretiosum Riley and Trichogrammatoidea annulata De Santis (Hymenoptera: Trichogrammatidae) (Hohmann and Meneguim, 1993; Hohmann et al., 2001). Their broad distribution and parasitization rates in some areas suggested that these species could be considered as a tool to reduce S. catenifer damage on avocados. However, before any attempt is made to mass rear and release these egg parasitoids, the factors that may affect their distribution and abundance must be understood. In this regard one important factor to be considered is temperature (Andrewartha and Birch, 1954). The knowledge of the thermal requirements and the effects of temperature are among many attributes that influences the outcome of biological control projects (Butler and Lopez, 1980, Chihrane et al.,1993; Bernal, 1995). Therefore, the aim of this study was to estimate the developmental times and the thermal requirements, and evaluate temperature effects on prasitism capacity, sex ratio, and longevity of T. pretiosum and T. annulata.



Parasitoid's Culture Origin and Maintenance

T. pretiosum and T. annulata cultures were initiated with parasitized S. catenifer eggs collected on avocado by C. L. Hohmann, in Arapongas (Lat. 23º 25' 00' S, Longit. 51º 26" 00' W - GR) PR, Brazil, in 1990. At emergence, each parasitoid species was exposed to cards (9 X 10 cm) containing a large supply of sterilized (UV light) A. kuehniella eggs inside of polyethylene containers (10 X 13 cm). The host has been mass-reared in the Laboratory of Entomology of the Instituto Agronômico do Paraná – IAPAR, in Londrina, PR, Brazil for more than five years. Parasitoid cultures were initiated at different days to provide wasps whenever they were needed to start the experiments. The host as well as the parasitoid cultures were maintained at 25 ± 2º C, RH 70 ± 20%, and photophase of 14 h.

Experimental Conditions

The development times and the effect of temperature on parasitism capacity and longevity were measured at 15, 20, 25, and 30º C inside temperature cabinets (Fanem, Model 347). Relative humidity and photoperiod were 70 ± 10% and 14L: 10D, respectively. To determine developmental times and thermal constants, fifteen females of each species (< 12 h old) were individually placed in rearing units (Hohmann et al., 1988) containing 100 ± 10 A. kuehniella eggs (< 24 h old) during 24 h. The females were then removed and the vials placed inside of the respective environment chamber, and held for parasitoid development. The number and sex of the wasps were recorded daily during their period of emergence.

To determine the effect of temperature on parasitism capacity and longevity the same protocol described above was followed, except that the host eggs were replaced daily until all females died. Honey was provided as food source. The number of parasitized eggs, emergence, brood size and parental female's longevity were recorded.

Statistical Analysis

The variables developmental times, parasitoid’s emergence, parasitization rates, longevity, and sex ratio between treatment groups were compared using a one-way analysis of variance (ANOVA) (SAS Institute Inc. 1994) followed by Duncan's Multiple Range Test at 0.05 level. Data on emergence, and sex ratio were transformed (log x). Sex ratio was expressed as % of females [(no. of females/ no. of males + no. of females) x 100].

The development thresholds (t) and thermal constants (K) were estimated using the hyperbole method (Haddad and Parra, 1984).



The developmental times of T. pretiosum and T. annulata were similar at 20, 25, and 30º C (Table 1). At 15º C, however, T. annulata developed slightly faster than T. pretiosum (P<0.05). The developmental times increased from 6.6 days at 30º C to 29.7 days at 15º C in T. pretiosum, and from6.4 days at 30º C to 29.0 days at 15º C in T. annulata. This relationship has been consistent for various species of Trichogramma (Russo and Voegelé, 1982; Harrison et al., 1985; Bleicher and Parra, 1989; Cônsoli and Parra, 1995; Hohmann and Luck, 2000).



Emergence rates were high (> 89%) for both parasitoid species in the entire temperature range. Similar results have been reported for other species of Trichogramma (Harrison et al.,1985;Cônsoli and Parra, 1995).

The estimated temperature threshold of both species was ca. 11° C and the number of degree-days for T. pretiosum and T. annulata was 126.9 and 122.3, respectively (Table 2). The lower temperature thresholds were very similar to that reported for T. pretiosum reared on Sitotroga cerealella Olivier (Lepidoptera: Gelechiidae) eggs (Goodenough et al.,1983), and for Trichoplusia ni Hübner (Lepidoptera: Noctuidae) eggs (Butler and Lopez, 1980).



Trichograma pretiosum parasitized fewer eggsthan T. annulata in all temperatures tested (Table 3) (P<0.05). Parasitization was maximal at 25º C, but no difference was detected between the number of eggs parasitized by T. pretiosum at 25 and 30º C. The number of eggs parasitized by T. annulata at 25º C differed significantly from that at 15, 20, and 30º C. These results are in accordance with studies carried out with other species of Trichogramma (Lund, 1938; Russo and Voegelé, 1982; Pak and Oatman, 1982; Harrison et al.,1985; Pak and van Heiningen, 1985).



Offspring sex ratio varied with parasitoid species and temperature (Table 4). In T. pretiosum the offspring was female-biased throughout the entire temperature range, being less abundant at 15º C (73%) and 30º C (52%) (P<0.05). Harrison et al.(1985) studying the temperature effects on T. pretiosum sex ratio reported that females were slightly less abundant at lower and upper thresholds fordevelopment. T. annulata offspring was mostly male-biased, except at the lowest temperature (15º C) (P<0.05). Similar results were revealed by Hutchison et al.(1990) in Trichogrammatoidea bactrea Nagaraja. According to the authors, the % of daughters ranged from 51.6% at 30º C to 77.1% at 15º C.



As temperature increased, longevity decreased accordingly (Table 5). T. pretiosum parental females lived significantly longer than T. annulata within the 20-30º C range, but no difference occurred at 15º C. Females lived significantly longer than their conspecific males at comparable temperatures, regardless of species, the differences being greater at the lower temperature range (Table 5).



Temperature effect on longevity was independent of the parasitoid species, indicating that the higher parasitism capacity of T. annulata was not a longevity artifact as it could be speculated, but rather, it resulted from its higher fecundity.

Longevity of T. pretiosum and T. annulata males and females changed with temperature. As temperature increased longevity decreased accordingly (Table 5). This result is in agreement with studies conducted with other Trichogramma species (Lund, 1938; Pak and Oatman, 1982; Harrison et al., 1985; Bleicher and Parra, 1989).

The present study revealed significant differences between T. pretiosum and T. annulata with respect to temperature requirements, and temperature effects on development and survival. T. annulata developed faster at 15º C and required less heat units to complete development than T. pretiosum. Theyalso confirmed their higher parasitism rate compared to T. pretiosum when exposed to A. kuehniella eggs in all temperatures tested (Hohmann et al.,2001).

T. pretiosum lived longer than T. annulata in the 20 to 30º C temperature ranges. This result, however, might not have a practical relevance unless Trichogramma females are able to find food after emergence. In the absence of a carbohydrate source they would not be able to survive more than two days (Hohmann et al.,1988).

Despite the statistical significance of the differences found, it is not certain whether these differences would be biologically important to give either species an advantage or not. Therefore, the results above need to be confirmed with more detailed laboratory and field studies, using the natural host S. catenifer.

The outcome of these and other studies (Maceda et al., 1994; Hohmann et al.,2001), when added up to information on parasitoids' spatial and seasonal distribution and abundance, may provide the tools to understand the major factors that are affecting T. pretiosum and T. annulata reproductive success. Moreover, all this information will be crucial to determine their potential role as biological control agents of the S. catenifer on avocados.



We thank Drs. Vitor O. Becker for identifying S. catenifer, John D. Pinto for identifying the parasitoids, and Sueli S. Martinez, Celso Jamil Marur and Ana M. Meneguim for their critical review of an earlier draft of the manuscript. We also thank Adauto Crispim for his help during the course of this study.



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Correspondence to
Celso L. Hohmann
Área de Proteção de Plantas; Instituto Agronômico do Paraná - IAPAR
C. P. 481
86001-970, Londrina - PR - Brazil

Received: May 23, 2001
Revised: August 13, 2001
Accepted: February 27, 2002

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