Tetrastichus howardi was identified as a hyperparasitoid of the tachinids Goniophthalmus halli and Senometopia illota, both parasitoids of Helicoverpa armigera pupae, in pigeon pea fields in southern India. Fifty-nine percent of G. halli and S. illota pupae were parasitized by T. howardi, resulting in a hyperparasitism rate of 1.9%. Unlike previous studies, T. howardi was not recorded as a primary parasitoid of H. armigera pupae. Rather than behaving as a pupal guild parasitoid, the data suggest that T. howardi oviposit in the larval stage of tachinid parasitoids while they are developing inside H. armigera pupae. The fact that T. howardi was not a primary parasitoid of H. armigera pupae suggests that this species is able to distinguish between parasitised and unparasitized H. armigera pupae

Armes, N J

Jadhav, D R

Tawar, K B

ICRISAT Open Access Repository

J Blo/. Control, 10'9-13, 1996 Tetrastichus howardi (Olliff) (Hymenoptera: Eulophidae), a hyperparasitoid of tachinid natural enemies of Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) in India K. B. TAWAR, D. R. JA DHAV and N. J. ARMES* International Crops Research Institute for the Semi-Arid Tropics Patancheru 502 324, Arldhra Pradesh, India ABSTRACT : Tet rastichus howardi (Olliff) was found to be a hyperparasitoid of the tachinids Goniophthalmus halli (Mesnil) and Senometopia (= Eucarcelia) illota (Curran) parasitising Helicoverpa armigera (Hubner) pupae in pigeonpea fields in south India. Fifty nine per \ cent of G. haW and S. illota pupae were parasitized by T howardi resulting in a hyperparasitism rate of 1.9 per cent. Unlike previous studies, T howardi was not recorded �s a primary parasitoid of H armigera pupae. Rather than behaving as a pupal guild parasitoid, the data suggest that T howardi wasps oviposit in the larval stage of the tachinid parasitoids while they are developing inside the H armigera pupa. The fact that T howardi was not found to be a primary parasitoid of H armigera pupae, suggests that this species is able to distinguish between parasitised and unparasitised H armigera pupae. KEY WORDS : Goniophthalmus halli, Helicoverpa armigera, hyperparasitoid, pupal parasitoids, Senometopia illota, Tetrastichus howardi The parasitoid Tetrastichus howardi (Olliff) (Hymenoptera: Eulophidae), is widely distributed across the Indian subcontinent, the Far Ea�t and parts of A us tralasia (Boucek, 1988). It  has previously been recorded under a number of synonyms (Kfir et ai., 1993). In India, it is a common pupal parasitoid of several species of lepidopteran borers (Ayyar, 1927; Cheri an and Subramanian, 1940), * Present address: Cyanamid (Singapore) Pvt. Ltd., 100 Cecil Street # 1201102, The Globe, Singapore 069532. TAWARetal and attempts have been made to utilise it as a biological control agent against sugarcane borers in India (Rudriah and Sastry, 1959), and the spotted stem borer, Chilo partellus (Swinhoe) in South Africa (Kfir et al., 1993). It has also been reported as ahyperparasitoid on the pupae of several natural enemies including tachinid flies (Boucek, 1988; Kfir et al., 1993). In India it has been suggested as a control agent for the uzi fly, Exorista bombycis (Louis), a serious pest of silkworm (Bombyx mori L.) larvae (Kishore et al., 1994). This paper focuses on the role of T howardi as a hyperparasitoid of tachinid parasitoids of Helicoverpa armigera (Hubner) pupae. The data presented here result from an intensive study on pupal diapause of H. armigera, the major lepidopteran pest of cotton, legumes and tomatoes in India (Reed and Pawar, 1982). MATERIALS AND METHODS Over 2300 H armigera pupae were collected by excavating the top 10 cm of soil in pigeonpea fields on the ICRISAT research farm, Patancheru, Andhra Pradesh, India, harbouring heavy infestations of H armigera larvae between mid October, 1995 and midJanuary, 1996. Only apparently healthy pupae were retained. Pupae were kept individually in 80 x 20 mm glass tubes with tight fitting cotton bungs and placed in one litre plastic boxes which were buried in the soil to a depth of 15 cm to keep the pupae in as near natural temperature conditions as possible. The boxes were checked for emergence of 10 either the host or parasitoids 2-3 times every week. Parasitism and hyperparasitism were confirmed by observing emergence from the host pupa or parasitoid pupa, respectively. If parasitism was suspected to be the cause of death but no parasitoid emerged, the host was dissected to confirm the presence of a parasitoid and its identity ascertained. In the laboratory an experiment was conducted to determine whether T howardi could parasilise H armigera larvae and pupae. Twenty five sixth instar larvae and 25 pupae (1-3 days old) were placed individually in 80 x 20 mm glass tubes. Helicoverpa armigera larvae were provided with chickpea based semi­synthetic artificial diet (Armes et al., 1992). At least t�enty freshly emerged T howardi adults (approx. 1: 1 sex ratio) were placed in each tube fitted with a cotton bung, wetted each day with 10 per cent honey solution to provide food for the wasps. The wasps were left in the tubes until all had died which was between 48 and 96 h after the start of the experiment. In the tests with larvae, all wasps had died before host pupation. Parasitism of H armigera larvae and pupae was confirmed by observing the emergence of progeny from the host. Laboratory temperature was maintained at 25 ± 2°C, with natural photoperiod (approx. 12 h light: 12 h dark). RESULTS AND DISCUSSION From the field collections of H. armigera pupae, two tachinid larval - pupal HyperparasItIsm by T howardl parasitoids viz., Goniophthalmus halli (Mesnil) and Senometopia ( Eucarcelia) illota (Curran) were recorded. For both species, parasitism frequencies were low (0.6 - 0.7%) (Table 1). Tetrastichus howardi adults emerged from 1.9 per cent of collected H armigera pupae; all emerged from the pupae of G. halli and S. illota. There were no instances where T. howardi behaved as a primary parasitoid of H armigera pupae. Hyperparasitism rates were very high, with 59 per cent of a combination of G. halli and S. illota pupae being parasitised by T. howardi. field collections, and the pupae were immediately transferred to individual tubes with tight fitting plugs (thereby excluding entry of parasitoid wasps), it is evident that T howardi must have stung the tachinid parasitoids during their early larval stage while in the live H armigera host. T his  has very interesting implications with reference to the biology of this species and possibly other related species in the genus. From the literature it is generally assumed that Tetrastichus spp. are solely pupal guild parasitoids (Smith et al., 1993), stinging either the Table 1. Emergence and developmental periods of H armigera pupae and its pupal parasitoids and hyperparasitoid Species H armigera G halli S. illota T. howardi Number 2268 14 17 45 Range 9-29 10-29 12-26 13-32 Approximate numbers of T howardi emerging from G. halli and S. illota pupae ranged from 40:80 with a 1: 1 sex-ratio. Dmations from the time of host collection to either host or parasitoid emergence were similar for H armigera, G. halli and S. illota (t-test, P> 0.05); T. howardi dmations were significantly longer (Hest, P < 0.0 1) (Table 1). In view of the fact that only live H annigera pupae were retained from the 11 Time taken to emergence (days) Mean ±SD Population (%) 18.0 6.9 96.8 18.9 7.6 0.6 18.7 4.8 0.7 21.9 5.6 1.9 host pupa (as a primary parasitoid), or the pupal stage of its tachinid parasitoid upon emergence from the host (as a hyperparasitoid). Om results suggest that under certain circumstances T howardi can behave as a larval - pupal parasitoid, stinging the parasitoid larva and the resulting progeny emerging from the pupal stage of the parasitoid. Also from our results it appeared that T howardi could differentiate between parasitised and unparasitised H armigera pupae, as it was TAWARetal only recorded as a hyperparasitoid in this study. Under laboratory conditions we were unable to get T howardi to parasitise either 6th instar larvae or pupae of H armigera, contrary to the observations of Kfir et al. (1993) who routinely used one day old H. armigera pupae for laboratory rearing of T howardi. Further, Okeyo-Owuor et al. (1991) reported that related Tet rast ichus species readily parasitised pupae of other noctuids. Our laboratory results do, however, confmn the field data where no instances of T howardi acting as a primary parasitoid of H armigera was found, while high levels of hyperparasitism of the two tachinid fly species were observed. On the basis of laboratory tests, Kfir et al. ( 1993) considered T howardi to be a facultative hyperparasitoid, preferring to parasitise noctuid and pyralid pupae over parasitoid puparia. Cherian and Subramanian (1940) reported T howardi (= T ayyari) as a pupal parasitoid of H armigera in south India. From our data it appears that T howardi is predominantly a hyperparasitoid of tachinid parasitoids, rather than a primary parasitoid of H armigera. This is consistent 'with Kishore et al. ( 1994) who considered T howardi only to be hyperparasitoid of E. bombycis and did not report it acting as a primary parasitoid of B. mori. It has been suggested that host preference in T howardi is dependent on previous oviposition experience and on the host species on 12 which the adults had been reared (Kfir et al., 1993). This may explain the inability of T howardi to behave as a primary parasitoid in the laboratory. Further experimentation is needed to ascertain the biology of T howardi and its status as a primary and/or hyperparasitoid lmder field conditions. ACKNOWLEDGEMENTS Parasitoids were identified through the insect identification service of the Natural History Museum, UK. Financial support was provided by the Natural Resources Institute, UK, through an Adaptive Research Initiative of the UK Government's Overseas Development Administration. REFERENCES Armes, N. J., Bond, G. S. and Cooter, R. J. 1992. The laboratory culture and development of Helicoverpa armigera. Natural Resources Institute Bulletin 57, Chatham,United Kingdom: Natural Resources Institute. Ayyar, T. V. R. 1927. The parasitic Hymenoptera of economic importance noted from South India. Bulletin of Entomological Research, 18:73-78. Boucek, Z. 1988. Australian Chalcidoidea (Hymenoptera). A bioystematic revision of genera of foUlieen families, with a reclassification of species. CAB . International, Wallingford, UK. HyperparasItism by T. howardl Cherian, M. C. and Subramanian, C. K. 1940. Tetrastichus ayyari Rohw. - a pupal parasite of some moth-borers in South India. Indian Journal of Entomology, 2:75-77. Kfir, R., Gouws, J. and Moore, S. D. 1993. B i o l ogy of Tetrastichus h owardi ( Olliff) (Hymenoptera : Eulophidae):a facultative hyperparasitoid of stem borers. Bi ocontrol Science and Technology, 3: 149- 159. Kishore, R., Kumar, P., Manjunath, D. and Datta, R. K.1994. Effect of temperature on the developmental period, progeny production and longevity of Tetrastichus howardi ( Olliff) (Hymenoptera: Eulophidae). Journal of Bi ological Contr ol, 8:10-13. Okeyo-Owuor, J. B., 0100, G. W. and A gwaro , P. O. 199 1. Bionomics of 13 Tetrastichus sesamiae (Hymenoptera: Eulophidae), a pupal endo - parasitoid of Maruca testulalis (Lepidoptera : pyralidae). Entomophaga, 36:417-423. Reed, W. and Pawar, C. S. 1982. Heliothis : a global problem. In Proceedings of the International Workshop on Heliothis Management, International Crops Research Institute for the Semi - Arid Tropics, Patancheru, AP-502 324, hldia, pp. 9 - 14. Rudriah, M. P. and Sastry, K. S. S. 1959. Studies on the biology of Tetrastichus ayyar i Rohwer, with attempts to utilise it in the control of sugarcane borers. Indian Journal of Entol1'lO!ogy, 20: 189- 198. Smith, J. W., Wiedenmann, R. N. and Overholt, W. A. 1993. Parasites of Lepidopteran stemborers of tropical graminaceous plants. ICIPE Science Press, Nairobi, Kenya. 

Tetrastichus howardi  (Olliff)  (Hymenoptera: Eulophidae), a hyperparasitoid of tachinid natural enemies of elicoverpa armigera (Hubner)  (Lepidoptera: Noctuidae)  in  India

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Tetrastichus howardi (Olliff) (Hymenoptera: Eulophidae), a hyperparasitoid of tachinid natural enemies of elicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) in India

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