Acessibilidade / Reportar erro

Emergence, longevity and fecundity of Trissolcus basalis and Telenomus podisi after cold storage in the pupal stage

Emergência, longevidade e fecundidade de Trissolcus basalis e Telenomus podisi após estocagem no estágio pupal

Abstracts

Pupae of Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead (Hymenoptera: Scelionidae) were stored at 12ºC and 15ºC for 120-210 days, after different periods of parasitism at 18ºC in order to evaluate adult emergence, longevity and ovipositional capacity. There was no emergence of adults at 12ºC. The rate of emergence of parasitoids transferred to 15ºC at the beginning of the pupal stage was 1.5% and 26.3%, for T. basalis and T. podisi respectively, whereas those parasitoids transferred one day before the expected date of emergence at 18ºC showed 86.4% of emergence for T. basalis and 59.9% for T. podisi. Mean adult longevity was also significantly lower when pupae were transferred to 15ºC at the beginning of the pupal stage. Females emerged after storage and maintained for 120 to 210 days at 15ºC parasitized host eggs after transference to 25ºC; however, fecundity of T. podisi was reduced in about 80% after cold storage.

Insecta; hibernation; egg parasitoids; biological control


Pupas de Trissolcus basalis (Wollaston) e Telenomus podisi Ashmead (Hymenoptera: Scelionidae) armazenadas a 12ºC e 15ºC por 120 a 210 dias, após diferentes períodos de parasitismo a 18ºC, foram avaliadas quanto à emergência, longevidade e capacidade de parasitismo dos adultos. Não houve emergência de adultos a 12ºC. Os índices de emergência de parasitóides transferidos a 15ºC no início do estágio pupal foram 1,5% e 26,3%, em T. basalis e T. podisi, respectivamente, enquanto os transferidos um dia antes da data prevista para a emergência dos adultos a 18ºC apresentaram índices de emergência de 86,4% em T. basalis e 59,9% em T. podisi. De forma semelhante, a longevidade média dos adultos foi significativamente menor quando a transferência para 15ºC foi realizada no início do estágio pupal. Fêmeas emergidas após estocagem das pupas e mantidas por 120 a 210 dias a 15ºC parasitaram ovos hospedeiros após transferência para 25ºC; no entanto, a fecundidade de T. podisi foi reduzida em cerca de 80% quando mantida em baixa temperatura.

Insecta; hibernação; parasitóides de ovos; controle biológico


ENTOMOLOGIA

Emergence, longevity and fecundity of Trissolcus basalis and Telenomus podisi after cold storage in the pupal stage

Emergência, longevidade e fecundidade de Trissolcus basalis e Telenomus podisi após estocagem no estágio pupal

Luís Amilton Foerster; Augusta Karkow Doetzer; Letícia Cunha Ferreira de Castro

Universidade Federal do Paraná, Dep. de Zoologia, Caixa Postal 19020, CEP 81531-990 Curitiba, PR. E-mail: foerster@ufpr.br

ABSTRACT

Pupae of Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead (Hymenoptera: Scelionidae) were stored at 12ºC and 15ºC for 120-210 days, after different periods of parasitism at 18ºC in order to evaluate adult emergence, longevity and ovipositional capacity. There was no emergence of adults at 12ºC. The rate of emergence of parasitoids transferred to 15ºC at the beginning of the pupal stage was 1.5% and 26.3%, for T. basalis and T. podisi respectively, whereas those parasitoids transferred one day before the expected date of emergence at 18ºC showed 86.4% of emergence for T. basalis and 59.9% for T. podisi. Mean adult longevity was also significantly lower when pupae were transferred to 15ºC at the beginning of the pupal stage. Females emerged after storage and maintained for 120 to 210 days at 15ºC parasitized host eggs after transference to 25ºC; however, fecundity of T. podisi was reduced in about 80% after cold storage.

Index terms: Insecta, hibernation, egg parasitoids, biological control.

RESUMO

Pupas de Trissolcus basalis (Wollaston) e Telenomus podisi Ashmead (Hymenoptera: Scelionidae) armazenadas a 12ºC e 15ºC por 120 a 210 dias, após diferentes períodos de parasitismo a 18ºC, foram avaliadas quanto à emergência, longevidade e capacidade de parasitismo dos adultos. Não houve emergência de adultos a 12ºC. Os índices de emergência de parasitóides transferidos a 15ºC no início do estágio pupal foram 1,5% e 26,3%, em T. basalis e T. podisi, respectivamente, enquanto os transferidos um dia antes da data prevista para a emergência dos adultos a 18ºC apresentaram índices de emergência de 86,4% em T. basalis e 59,9% em T. podisi. De forma semelhante, a longevidade média dos adultos foi significativamente menor quando a transferência para 15ºC foi realizada no início do estágio pupal. Fêmeas emergidas após estocagem das pupas e mantidas por 120 a 210 dias a 15ºC parasitaram ovos hospedeiros após transferência para 25ºC; no entanto, a fecundidade de T. podisi foi reduzida em cerca de 80% quando mantida em baixa temperatura.

Termos para indexação: Insecta, hibernação, parasitóides de ovos, controle biológico.

Introduction

Several egg parasitoids of subtropical and temperate regions overwinter in a hibernation state (Boivin, 1994), which can determinate their population dynamics, geographic distribution and potential as biological control agents (Mansingh, 1971; Boivin, 1994). The developmental stage susceptible to hibernation differs between species; however, most egg parasitoids hibernate as larvae or pupae within the host egg (Boivin, 1994).

Low temperatures and short photoperiods can induce hibernation on egg parasitoids and this procedure is useful to optimize mass-production of these natural enemies and to improve synchronization between the pest and the parasitoid (Boivin, 1994).

Most research on cold storage of egg parasitoids has been conducted on Trichogramma species (Stinner et al., 1974; Curl & Burbutis, 1977; Jalali & Singh, 1992; Laing & Corrigan, 1995), Ooencyrtus ennomus Yoshimoto (Encyrtidae) (Anderson & Kaya, 1974, 1975) and Encarsia formosa Gahan (Aphelinidae) (Lacey et al., 1999).

The storage of Telenomus remus Nixon in the pupal stage at 10ºC for seven days did not influence parasitoid survival (Gautam, 1986). Storage of Trissolcus basalis (Wollaston) and Telenomus podisi Ashmead eggs and larvae was unsuitable for parasitoid emergence. However, adults of T. basalis and T. podisi that emerged at 15ºC when pupae were stored one day before the predicted date for emergence survived for about five months at the low temperature (Foerster & Nakama, 2002).

The objective of this work was to determine the effect of pupae storage at 12ºC and 15ºC after different periods of parasitism on adult emergence, longevity and fecundity of Trissolcus basalis and Telenomus podisi.

Material and Methods

Stink bugs Nezara viridula (L.) and Euschistus heros (Fabr.) (Heteroptera: Pentatomidae) were used as hosts for Trissolcus basalis and Telenomus podisi, respectively. Specimens used in this work were obtained from the Laboratory of Integrated Control of Insects at the Universidade Federal do Paraná, Brazil.

Egg masses with 40 eggs of N. viridula and E. heros were exposed respectively to five females of T. basalis and T. podisi, at 18±0,5ºC (12L: 12D), during 48 hours. After this period, the parasitoids were discarded and the parasitized eggs remained on moistened filter paper. At different dates after parasitism, these eggs were transferred from 18ºC to either 15±0,5ºC or 12±0,5ºC (10L:14D) to evaluate adult emergence. Storage at 12ºC was made 15, 20 and 25 days after parasitism; at 15ºC, both parasitoids were stored 15, 20, 25, 26, 28 and 30 days after parasitism and for T. podisi, the parasitoids were also stored 33 days after parasitism, because this species has lower developmental rate than T. basalis. Emergence rate, developmental time and progeny sex ratio were recorded in each treatment.

Adults were fed with honey and maintained in glass tubes (17x 2 cm) partially covered with black paper; previous results showed that this procedure increases their longevity (Doetzer, 2003). Mortality of T. basalis and T. podisi was daily recorded.

The effect of pupal storage at 15ºC on the fecundity of parasitoids emerged was evaluated. Females of T. basalis and T. podisi emerged after storage one day before the predicted date for emergence were maintained at 15ºC between 120 and 210 days and then transferred to 25ºC at 30 days intervals. Ten females of each species were individually exposed to 50 E. heros eggs for 24 hours one day after transference to 25ºC. Parasitoids were discarded after this period and the eggs were maintained on moistened filter paper. The number of parasitized eggs per female and progeny sex ratio was recorded. Results were analyzed in relation to a control treatment, conducted with females developed continuously at 25ºC and exposed to host eggs one day after emergence.

Data were submitted to analysis of variance and means compared by Tukey's test (p<0.05). Comparisons between species were done by t test (p<0.05). The relationships between storage age and emergence rate, developmental rate, progeny sex ratio and adult longevity were evaluated by linear regression analysis.

Results and Discussion

Adults failed to emerge when T. basalis and T. podisi pupae were transferred from 18ºC to 12ºC at any of the pupal ages evaluated, showing that storage at this temperature is lethal to the parasitoids in the pupal stage.

Parasitoids stored at 15ºC in the pupal stage continued to develop and emerged at this temperature. Emergence of T. basalis occurred in all treatments at 15ºC, whereas no adults of T. podisi emerged when their pupae were stored 15 days after parasitism (Table 1). Pupal age at storage significantly influenced adult emergence (T. basalis: y = -84.06 + 5.89x, R2 = 0.80, p<0.05; T. podisi: y = -38.23 + 3.05x, R2 = 0.59, p<0.05) and developmental rate of the parasitoids (T. basalis: y = 89.04 - 1.92x, R2 = 0.77, p<0.05; T. podisi: y = 85.29 - 1.47x, R2 = 0.60, p<0.05) (Figure 1).


Cold storage of pupae did not affect the sex ratio of the parasitoids, as also found for T. remus (Gautam, 1986). Progeny sex ratio of T. basalis ranged from 0.67 to 0.95 and for T. podisi, ranged from 0.71 to 0.80 (Table 1). Relationships between the age of the stored pupae and progeny sex ratio were not detected (T. basalis: y = 96.23 - 0.59x, R2 = 0.04, p>0.05; T. podisi: y = 75.98 + 0.01x, R2 = 0.01, p>0.05) (Figure 1).

Adult parasitoids that emerged after pupal storage at 15ºC hibernated with a drastic reduction in mobility and feeding (Mansingh, 1971). Pupal age at storage affected adult longevity for both species (p<0.05) (T. basalis, males: y = 5.38 + 6.34x, R2 = 0.11 and females, y = -263.56+18.23x; R2 = 0.42; T. podisi, males: y = -78.09 + 6.34x, R2 = 0.32 and females, y = -93.61 + 10.29x, R2 = 0.25) (Figure 2). Highest longevity was verified when parasitoids were stored at 15ºC one day before the predicted date of emergence (nine and eight months, for T. basalis and T. podisi, respectively) and decreased when the pupae were stored at the beginning of the stage. Females survived longer than males and T. basalis longevity was higher than T. podisi (Table 2).


Parasitoids stored at earlier stages of pupal development spent more energy to complete their development and, therefore, their longevity was shorter. Similarly, the longevity of females of T. oenone that emerged at 15ºC was lower than of those that emerged at 17.5ºC (James & Warren, 1991). Adults of T. basalis emerging at 15ºC were small, inactive and survived less than one day (Orr et al., 1985).

Foerster & Nakama (2002) found that the mean longevity of T. basalis and T. podisi transferred from 25ºC to 15ºC one day before the predicted date for emergence was of about five months; this value is lower than the results obtained in this work. Longevity of T. basalis and T. podisi at 15ºC was also higher than that of other Scelionidae species such as Ceratobaeus masneri Austin (Austin, 1984) and Trissolcus oenone (Dodd) (James & Warren, 1991).

Females of T. basalis and T. podisi emerging after pupal storage one day before the predicted date for emergence and maintained at 15ºC for 120 to 210 days, parasitized host eggs (Figure 3). Fecundity of T. basalis decreased as storage period increased from 120 to 180 days; however, after storage for 210 days, fecundity values increased as those recorded for females reared at 25ºC (Figure 3). This increased fecundity after storage for seven months could not be explained, which shows the need for additional research in order to fully understand the reproductive dynamics of this species. Females of T. podisi were more affected by adult maintenance at 15ºC, than T. basalis. The fecundity of T. podisi after storage at 15ºC was lower than that of females reared at 25ºC and the mean number of parasitized eggs decreased as the storage period increased, ranging from 0.0 to 6.4 parasitized eggs (Figure 3). Progeny sex ratio ranged from 0.87 to 0.92 for T. basalis, and from 0.34 to 0.69 for T. podisi and was not influenced by adult maintenance at 15ºC. Several studies have shown the impact of cold storage on the fecundity of egg parasitoids; Flanders (1938) states that this impact is due to the fact that the reproductive organs are the ones most likely to be affected by the low temperature. Foerster & Nakama (2002) found that T. basalis and T. podisi kept for 20 days at 15ºC had their fecundity reduced by more than 80% and 95%, respectively, and as reported for T. remus, parasitoids maintained at 5ºC for three days had a significant reduction in fecundity (Gautam, 1986).


Conclusions

1. Pupae of T. basalis and T. podisi do not survive at 12ºC, independently of their developmental stage at the time of storage.

2. Adult longevity at 15ºC is higher when the pupae are transferred to 15ºC at the end of the pupal stage.

3. Females of Trissolcus basalis parasitize eggs of Euschistus heros at 25ºC after remaining in hibernation at 15ºC for 120-210 days; females of Telenomus podisi do not parasitize eggs after 180 days at 15ºC.

Acknowledgements

To CNPq, for financial support.

Received on December 30, 2003 and accepted on May 4, 2004

  • ANDERSON, J.F.; KAYA, H.K. Diapause induction by photoperiod and temperature in the elm spanworm egg parasitoid, Ooencyrtus sp. Annals of the Entomological Society of the America, v.67, p.845-849, 1974.
  • ANDERSON, J.F.; KAYA, H.K. Influence of temperature on diapause termination in Ooencyrtus ennomus, an elm spanworm egg parasitoid. Annals of the Entomological Society of America, v.68, p.671-672, 1975.
  • AUSTIN, A.D. The fecundity, development and host relationships of Ceratobaeus spp. (Hymenoptera: Scelionidae), parasites of spider eggs. Ecological Entomology, v.9, p.125-138, 1984.
  • BOIVIN, G. Overwintering strategies of egg parasitoids. In: WAJNBERG, E.; HASSAN, S.A. (Ed.). Biological control with egg parasitoids Oxon: CAB International, 1994. p.219-244.
  • CURL, G.D.; BURBUTIS, P.P. The mode of overwintering of Trichogramma nubilale Ertle and Davis. Environmental Entomology, v.6, p.629-632, 1977.
  • DOETZER, A.K. Sobrevivência dos parasitóides de ovos de Trissolcus basalis (Wollaston) e Telenomus podisi Ashmead (Hymenoptera: Scelionidae) durante a entressafra da soja e sua eficiência após estocagem em baixas temperaturas 2003. 146p. Tese (Doutorado) - Universidade Federal do Paraná, Curitiba.
  • FLANDERS, S.E. The effect of cold storage on reproduction of parasitic Hymenoptera. Journal of Economic Entomology, v.31, p.633-634, 1938.
  • FOERSTER, L.A.; NAKAMA, P.A. Efeito da estocagem em baixa temperatura na capacidade reprodutiva e longevidade de Trissolcus basalis (Wollaston) e Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Neotropical Entomology, v.31, p.115-120, 2002.
  • GAUTAM, R.D. Effect of cold storage on the adult parasitoid Telenomus remus Nixon (Scelionidae: Hymenoptera) and the parasitized eggs of Spodoptera litura (Fabr.) (Noctuidae: Lepidoptera). Journal of Entomological Research, v.10, p.125-131, 1986.
  • JALALI, S.K.; SINGH, S.P. Differential response of four Trichogramma species to low temperatures for short-term storage. Entomophaga, v.37, p.159-165, 1992.
  • JAMES, D.G.; WARREN, G.N. Effect of temperature on development, survival, longevity and fecundity of Trissolcus oenone Dodd (Hymenoptera: Scelionidae). Journal of the Australian Entomological Society, v.30, p.303-306, 1991.
  • LACEY, L.A.; MILLAR, L.; KIRK, A.A.; PERRING, T.M. Effect of storage temperatures and duration on survival of eggs and nymphs of Bemisia argentifolii (Homoptera: Aleyrodidae) and pupae of the whitefly parasitoid Encarsia formosa (Hymenopera: Aphelinidae). Arthropod Biology, v.92, p.430-434, 1999.
  • LAING, J.E.; CORRIGAN, J.E. Diapause induction and post-diapause emergence in Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae): the role of host species, temperature, and photoperiod. Canadian Entomologist, v.127, p.103-110, 1995.
  • MANSINGH, A. Physiological classification of dormancies in insects. Canadian Entomologist, v.103, p.983-1009, 1971.
  • ORR, D.B.; BOETHEL; D.J.; JONES, W.A. Development and emergence of Telenomus chloropus and Trissolcus basalis (Hymenoptera: Scelionidae) at various temperatures and relative humidities. Annals of the Entomological Society of America, v.78, p.615-619, 1985.
  • STINNER, R.E.; RIDGWAY, R.L.; KINZER, R.E. Storage, manipulation of emergence, and estimation of numbers of Trichogramma pretiosum Environmental Entomology, v.3, p.505-507, 1974.

Publication Dates

  • Publication in this collection
    03 Nov 2004
  • Date of issue
    Sept 2004

History

  • Accepted
    04 May 2004
  • Received
    30 Dec 2003
Embrapa Secretaria de Pesquisa e Desenvolvimento; Pesquisa Agropecuária Brasileira Caixa Postal 040315, 70770-901 Brasília DF Brazil, Tel. +55 61 3448-1813, Fax +55 61 3340-5483 - Brasília - DF - Brazil
E-mail: pab@embrapa.br