Effect of temperature on the development and progeny production of Glyptapanteles muesebecki (Blanchard) (Hymenoptera: Braconidae) parasitizing larvae of Pseudaletia sequax Franclemont (Lepidoptera: Noctuidae)

Efeito da temperatura no desenvolvimento e reprodução de Glyptapanteles muesebecki (Blanchard) (Hymenoptera: Braconidae) parasitando lagartas de Pseudaletia sequax Franclemont (Lepidoptera: Noctuidae)

BIOLOGICAL CONTROL

Effect of temperature on the development and progeny production of Glyptapanteles muesebecki (Blanchard) (Hymenoptera: Braconidae) parasitizing larvae of Pseudaletia sequax Franclemont (Lepidoptera: Noctuidae)

Efeito da temperatura no desenvolvimento e reprodução de Glyptapanteles muesebecki (Blanchard) (Hymenoptera: Braconidae) parasitando lagartas de Pseudaletia sequax Franclemont (Lepidoptera: Noctuidae)

Luís A. Foerster; Marion do R.F. Avanci; Augusta K. Doetzer

Depto. de Zoologia, UFPR, Caixa postal 19.020, 81531-990, Curitiba, PR

ABSTRACT

The developmental time of Glyptapanteles muesebecki (Blanchard) parasitizing the armyworm Pseudaletia sequax Franclemont, and the number of pupae/host were determined at six constant temperatures ranging from 14° to 30°C. The egg + larval stages lasted from 17.8 days at 26° and 29°C to 56.4 days at 14°C, while the pupal stage ranged from 6.4 days at 29°C to 34.5 days at 14°C. G. muesebecki required 291.9 degree-days (DD) above the lower threshold of 8.9°C to complete the egg + larval development, while the pupae required 107.0 DD above 11.1°C. Development from egg to adult was completed after 397.4 DD above the lower threshold of 9.6°C. The number of pupae/host was not significantly different between 18°° and 26°C, and ranged from 86.9 at 22°C to 92.1 at 18°C. At the lower (14°°C) and upper (29°C) threshold temperatures, this number was significantly lower, averaging 27.6 and 19.8 pupae/host, respectively. Moreover, at 14° and 29°C the proportion of parasitized caterpillars was significantly lower than in the range between 18° and 26°C and at the lower temperature there was no synchronism in the pupation of parasitoids from the same host. At 30°C, the host larvae died before the emergence of the parasitoids. At 18, 22 or 26°C, the development and progeny production of G. muesebecki was not affected in the laboratory after five consecutive generations.

Key words: Insecta, endoparasitoid, biological control, parasitism, thermal requirements.

RESUMO

O tempo de desenvolvimento de Glyptapanteles muesebecki (Blanchard) e o número de pupas produzido por hospedeiro foram avaliados em seis temperaturas constantes entre 14° e 30°C, utilizando como hospedeiro lagartas de segundo ínstar de Pseudaletia sequax Franclemont. A duração dos estágios internos do parasitóide (ovo e larva) variou entre 17,8 dias (26° e 29°C), e 56,4 dias (14°C), enquanto que o estágio de pupa variou de 6,4 a 34,5 dias a 29° e 14°C, respectivamente. Os estágios internos requereram um total de 291,9 graus-dia (GD) acima da temperatura base (Tb) de 8,9°C, e o estágio de pupa necessitou de 107,0 GD acima da Tb de 11,1°C. O desenvolvimento de ovo a adulto foi completado em 397,4 GD acima da Tb de 9,6°C. Entre 18° e 26°C, o número de pupas de G. muesebecki por hospedeiro foi estatisticamente semelhante e variou de 86,9 (22°C) a 92,1 (18°C). Nas duas temperaturas extremas, este valor foi significativamente menor, resultando em 27,6 e 19,8 pupas por lagarta a 14° e 29°C, respectivamente. Nestas duas temperaturas, a proporção de lagartas parasitadas foi significativamente menor do que entre 18° e 26°C, e a 14°C não houve sincronismo na emergência dos adultos de uma mesma lagarta. A 30°C, as lagartas hospedeiras morreram antes da emergência dos parasitóides. O desenvolvimento e a produção de descendentes do parasitóide não foram alterados após a sua criação por cinco gerações consecutivas entre 18° e 26°C em laboratório.

Palavras-chave: Insecta, endoparasitóide, lagarta do trigo, exigências térmicas

Glyptapanteles muesebecki (Blanchard) is a gregarious endoparasitoid of the armyworm Pseudaletia sequax Franclemont, a pest of winter cereals and pastures in Southern Brazil. The life cycle of the parasitoid was studied under laboratory conditions by Oliveira & Foerster (1986); parasitism took place between the second and fourth instars of the host and parasitoids emerged from the host to pupate during the last instar of P. sequax, independently of the age of the host at the time of parasitism. Estimates of thermal requirements indicate the degree of synchrony in development between parasitoids and their hosts and provide accurate predictions of phenological events within the range of temperatures encountered in the field (Lysyk & Nealis, 1988). Foerster (1996) estimated the thermal requirements of P. sequax, establishing a lower threshold of 8.4ºC for the larval stage and 396.4 degree-days (DD) above such temperature for the completion of this stage. Threshold temperatures and thermal constants have been determined for a number of braconids parasitizing lepidopterous larvae (Butler Jr. et al.1983; Madar & Miller 1983; Al-Maliky et al. 1988). The present study reports the development and progeny production of G. muesebecki at six constant temperatures ranging from 14º to 30ºC and discusses the possibility of mass-rearing the parasitoid for field-release purposes.

Material and Methods

The experiment was conducted in temperature-controlled chambers adjusted to 14°, 18°, 22°, 26°, 29° and 30°C (± 0,5°C) and photoperiod of 12 hours, in a completely randomized design, using 20 replicates/treatment. Mated females of G. muesebecki obtained in the laboratory from field-collected armyworm larvae were transferred to the different chambers and allowed to parasitize second-instar P. sequax for 24 hours. Hosts were parasitized individually and reared on kikuyu grass (Pennisetum clandestinum Hochstetter) in 80 ml polythene tubes. Humidity was measured with a digital thermo-hygrometer inserted through the lid of a rearing tube, and was kept at 70 ± 10% by a moistened filter paper disk placed at the bottom of the tubes; fresh food was provided and faecal pellets were removed daily. The number of parasitoids emerging from each host and the duration of the internal (egg + larval) and pupal stages were recorded. At 18°, 22° and 26°C, the experiment was conducted for five consecutive generations, in order to investigate the effects of long-term rearing on the rate of development of the parasitoids and to evaluate the viability of large-scale production of G. muesebecki in the laboratory. The data for developmental time and number of pupae/host among generations were submitted to analysis of variance, and means were compared by Tukey's test (P<0.05). The lower temperature thresholds (T₀) and the thermal constants (K) were estimated for the immature stages and for the complete developmental cycle by means of the least square linear regression equation (Haddad & Parra 1984) within 95% confidence limits (software Statistica, Version 5), using the reciprocal of the developmental time.

Results and Discussion

Females of G. muesebecki were able to parasitize larvae of P. sequax at all temperatures, but the proportion of hosts that survived until the parasitoids completed the larval stage was severely reduced at 14°C and 29º and 30°C (Table 1). At 14ºC although ca. 60% of the hosts had been parasitized, only 17.4% of the parasitized caterpillars produced adult parasitoids (Table 1); moreover, the emergence of the parasitoids from the hosts was not synchronized as at the other temperatures. At 29º and 30ºC, although parasitism took place, adult emergence was low at 29°C, and at 30ºC all hosts died before the emergence of the parasitoids. Death of the hosts was due to parasitism, because unparasitized larvae of P. sequax are able to pupate at 30ºC although the adults fail to emerge (Foerster 1996). At 29ºC only 22.8% of the caterpillars exposed to parasitism produced adults of G. muesebecki (Table 1). The development of two hymenopterous parasitoids of the jack pine budworm Choristoneura pinus pinus Freeman (Lepidoptera: Tortricidae), Apanteles fumiferanae Viereck (Braconidae) and Glypta fumiferanae Viereck (Ichneumonidae) was also inhibited above 27ºC (Lysyk & Nealis 1988).

The rate of parasitism and progeny production did not differ statistically in the range between 18º and 26ºC; the percentage of parasitism was higher than 80% at these temperatures, and the mean number of pupae/host ranged from 86.9 at 22ºC to 92.1 at 18ºC (Table 1). At 14º and 29ºC, besides the reduced proportion of parasitoids reaching the adult stage, the number of progeny/host was significantly lower than at the other temperatures (Table 1). A similar reduction in progeny production was reported by Al-Maliky & Al-Izzi (1990) in Apanteles sp. group ultor, in which significantly more progeny was produced at 26ºC than at either 15ºC or 30ºC.

Developmental time of the immature stages of G. muesebecki was inversely related to temperature; the egg+larval stages ranged from 17.8 days at 26º and 29ºC to 56.4 days at 14ºC, and the pupal stage lasted between 6.4 and 34.5 days at 29ºC and 14ºC, respectively (Table 2).

Developmental rate, i.e. the reciprocal of developmental time, was linearly correlated with temperature between 18º and 26ºC (Fig. 1); the pupal stage was relatively less responsive to low temperatures, with no development at 11.1ºC (Fig. 1b). This value for the egg+larval stages was 8.9ºC, indicating that the stages within the host are more tolerant to the cold (Fig. 1a), and close to the lower limit of the larval stage of its host, P. sequax (8.4ºC) (Foerster 1996). The parasitoid required a total of 291.9 DD above the lower threshold temperature to complete the egg+larval stages and 107 DD for the pupal stage. The entire development of G. muesebecki was completed in 397.4 DD (Fig. 1c). This value is close to the amount of heat required by P. sequax to complete its larval stage (396 DD) (Foerster 1996), showing that the generation time of G. muesebecki is shorter than that of P. sequax. The development cycle of P. sequax is completed in 573.9 DD (Foerster 1996).

There was no difference in the development time of males and females; all adults from a single host emerged within one hour, in the range between 18° and 26°C, indicating that males and females of G. muesebecki emerge simultaneously. Nealis & Fraser (1988), on the other hand, found that males of the solitary braconid A. fumiferanae required approximately 15% less time to complete larval development than did females.

We conclude that the optimal temperature range for both the parasitoid and its host lies between 18º and 26ºC; outside these limits the proportion of parasitoids reaching the pupal stage and the progeny production of G. muesebecki were severely affected; at 30ºC parasitism led to the death of the hosts and the parasitoid was unable to complete its larval stage.

Continuous rearing of G. muesebecki. The parasitoid was reared continuously in the laboratory for five generations at 18°, 22° and 26°C using larvae of P. sequax as hosts. Although the developmental time from oviposition to adult emergence and the mean number of pupae/host were not significantly affected (Table 3), a progressive decline in the production of female progeny led to the termination of the colony, which was then resumed with the collection of field parasitized larvae of P. sequax. The probable reason for the male-biased progeny of G. muesebecki was the small size of the hosts at the time of parasitism (one day-old second instars), since smaller hosts tend to produce a male-biased sex-ratio (Fisher 1971, Vinson & Iwantsch 1980, Singh 1982). After the re-establishment of the colony, larger hosts were used (two to three day-old second instars) and the sex-ratio of G. muesebecki has remained constant. Nealis & Fraser (1988) reported quantitative and qualitative changes in the development and progeny production of another braconid, A. fumiferanae, in the laboratory after five generations. Neither the developmental time, nor the quality and number of emerging adults were affected by the continuous rearing of G. muesebecki in the laboratory. The use of an artificial diet to rear P. sequax may contribute to the mass-rearing of G. muesebecki by reducing the time spent in feeding parasitized larvae with natural food.

Acknowledgements

The authors are grateful to Dr. P. M. Marsh, retired research entomologist from the Systematic Entomology Laboratory, USDA for the identification of G. muesebecki, and to Dr. A.C. Pont from the Dept. of Entomology, Oxford University for the revision of the manuscript. Voucher specimens of G. muesebecki are deposited in the entomological collection of the Department of Zoology, UFPR. This research was supported by CNPq.

Literature Cited

Received 27/V/98. Accepted 15/III/99.

• Al-Maliky, S. K. & M.A.J. Al-Izzi.1990. The progeny production of a hymenopterous parasitoid, Apanteles sp. group ultor, as affected by temperature. Entomophaga 35: 217-222.
• Al-Maliky, S.K., M.A.J. Al-Izzi & N.F. Jabbo.1988 Effects of temperature and photoperiod on the development and oviposition of Apanteles sp. group ultor (Hym., Braconidae), a larval parasite of the carob moth Ectomyelois ceratoniae (Lep., Pyralidae). Entomophaga 33: 193-200.
• Butler Jr., G.D., A.G. Hamilton & J.D. Lopez Jr.1983.Cardiochiles nigriceps (Hymenoptera: Braconidae): development time and fecundity in relation to temperature. Ann. Entomol. Soc. Am. 76: 536-538.
• Fisher, R.C 1971. Aspects of the physiology of endoparasitic Hymenoptera. Biol. Rev. 46: 243-278.
• Foerster, L.A.1996 Efeito da temperatura no desenvolvimento das fases imaturas de Pseudaletia sequax Franclemont, 1951(Lepidoptera: Noctuidae). An. Soc. Entomol. Brasil 25: 27-32.
• Haddad, M. L. & J.R.P. Parra. 1984. Métodos para estimar os limites térmicos e a faixa ótima de desenvolvimento das diferentes fases do ciclo de desenvolvimento de insetos. Piracicaba, Fundação de Estudos Agrários "Luiz de Queiroz", 12p. (Série Agricultura e Desenvolvimento).
• Lysyk, T.J. & V.G. Nealis. 1988. Temperature requirements for development of the jack pine budworm (Lepidoptera: Tortricidae) and two of its parasitoids (Hymenoptera). J. Econ. Entomol. 81: 1045-1051.
• Madar, J.R. & J.C. Miller. 1983. Developmental biology of Apanteles yakutatensis (Hymenoptera: Braconidae), a primary parasite of Autographa californica (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 76: 683-687.
• Nealis, V.G. & S. Fraser. 1988. Rate of development, reproduction and mass-rearing of Apanteles fumiferanae Vier. (Hymenoptera: Braconidae) under controlled conditions. Can. Entomol. 12: 197-204.
• Oliveira, J. & L.A. Foerster. 1986. Ciclo evolutivo e preferência para oviposição de Apanteles muesebecki Blanchard, 1947 (Hymenoptera: Braconidae), parasitóide de Pseudaletia sequax Franclemont, 1951 (Lepidoptera: Noctuidae). An. Soc. Entomol. Brasil 15: 371-378.
• Singh, P. 1982. The rearing of beneficial insects. N. Zeal. Entomol. 7: 304-310.
• Vinson, S.B. & G.F. Iwantsch.1980. Host suitability for insect parasitoids. Annu. Rev. Entomol. 25: 397-419.

Publication Dates

• Publication in this collection
  29 May 2006
• Date of issue
  June 1999

History

• Accepted
  15 Mar 1999
• Received
  27 May 1998