Abstract

Tachinidae of Indian Helicoverpa Hardwick / Heliothis Ochsenheimer - A Review

S. V. Chaudhari

Asso. Prof.  and Head Dept. of Zoology, Arts, Science & Commerce College, Rahuri 413705, Dist. Ahmednagar, Maharashtra (India)

E-mail: su1dha@yahoo.co.in , Mob.No.9890756874.

Abstract- Present communication deals with the review of Tachinidae of Indian Helicoverpa Hubner/Heliothis Ochsenheimer. Three species of Helicoverpa viz., H.armigera (Hubner), H.assulata (Guenee) and H.peltigera (Schiffermuller) occur in India. Altogether 162 arthropod parasitoids have been recorded in India on Helicoverpa spp. Of the recorded number of parasitoids (114)- 30, 19 and 20 parasitoid species occur on H.armigera, H.assulata and H.peltigera, respectively. Parasitic Diptera are next to the parasitic Hymenoptera in natural control of Helicoverpa species, but host range of Diptera come from more animal groups. In India altogether 31 dipteran parasitoids have been recorded of which, 30 tachinid parasitoids are recorded on Helicoverpa species. Of these 28,6 and 4 species of Tachinidae belonging to subfamily Goniinae attack on H.armigera, H.assulata and H.peltigera, respectively. The tachinid parasitoids are mainly larval, and larvo-pupal which invade on old larvae, 3-6 instars and prevent the economic loss caused by the Helicoverpa spp. of the crop. The tachinid parasitoids are mainly useful on cotton, pigeonpea, tomato, sorghum and sunflower crops. Amongst these, Carcelia illota Curran, Goniopthalmus halli Mesnil, Palaxorista laxa Curran, Drino imberbis Wiedmann and Exorista xanthospis Wiedmann are common tachinid species recorded on H.armigera. C.illota and G.halli are common on three species of Helicoverpa. Palexorista and P.laxa are common on H.armigera and H.assulata. P.solennis Walker common on H.armigera and H.peltigera. The percent parasitism recorded on H.armigera for C.illota 4-52%, G.halli 18-20%, P.laxa12-18%, Drino imbrbis 25%, Exorista xanthospis and C.illota 24.54 %. In general dipteran tachinids can parasitise 22-25%. This paper also mentions the work done by different workers on indigenous and exotic species. The tachinid are more active during cooler months of November to January. There has been found confusion, labeling and identification of tachinids. There is need of universal cataloging by Zoological Survey.

          The genus Helicoverpa Hardwick / Heliothis Ochsenheimer consists of more than 75 species or subspecies (Todd, 1978). It belongs to the order Lepidoptera, family Noctuidae and subfamily Heliothinae. Three species of subfamily Heliothinae, namely Helicoverpa armigra (Hubner), Helicoverpa assulata (Guenee) and Helicoverpa peltigera (Denis and Schiffermuller) occur in India. H. armigera is a serious pest on several crops. It is widely distributed in Europe, Africa, Asia, Australia and New Zealand. H. armigera is highly polyphagaus pest. In India, it has been recorded on 181 cultivated and wild plant species (Manjunath et al., 1989). From the 1980s, serious outbreaks of this species have been occurred in the states of Andhra Pradesh, Karnataka, and Punjab on crops such as cotton, chickpea and pigeonpea. It is evident from the surveys conducted in farmer’s fields that average annual losses caused by H. armigera on chickpea and pigeonpea alone may exceed $300 million per year (Reed and Pawar, 1982). The loss may be due to sporadic outbreaks and resistance of Helicoverpa species to insecticides.

  

Distribution and host plants

Helicoverpa species: Distribution and host plants

             Helicoverpa armigera is distributed all over in India and is seen through the year on seasonal crops, orchards and weeds. It has caused serious damage in citrus orchards in Abohar (Punjab) in 1994-96, damaging 8.8 to 55.4 percent fruits (Arora et al., 1996). It is recorded as prominent pest in India of Chicory in Himachal Pradesh (Singh et al., 2002); potato in Punjab and Himachal Pradesh (Singh and Chaudhuri, 1974); mustard in Satpura plateau of Madhya Pradesh (Sharma, 1993); black cumin (Kala zira) in Himachal Pradesh (Bhardwaj and Panwar, 1990; Sharma et al., 1997; Sharma, 1998) and Castor in Andhra Pradesh (Satyanarayana et al., 2000).  It has been observed feeding on a dozen annual flowers in India at Punjab  (Singh and Arora, 1989) and Himachal Pradesh (Singh, 1983) and on rose snapdragon, geranium, gladiolus, marigold, and several others in Karnataka. In India it has been recorded on about three dozen wild plants and weeds (Saini and Mahla, 1991; Rao et al., 1991). It has been also recorded from Asam, Bihar, Delhi, Gujarat, Harayana, Jammu and Kashmir, Karnataka, Kerala, Maharashtra, Meghalaya, Orisa, Rajsthan, Tamil Nadu, Uttar Pradesh and West Bengal on cotton, tomato, pigeonpea, chickpea and other crop plants. This pest damages seasonal crop in summer, monsoon and winter. In Motipur (Bihar), H. armigera infestation on maize was 21% while adjacent pigeonpea fields remained totally free from this pest (Anonymous, 1974). Kaushik et al., (1969) recorded 14-56% damage to cotton in Madhya Pradesh. 14% damage to same crop was recorded in Anand (Gujarat) Manjunath (1974). Bhatnagar et al., (1981, 1982) in Andhra Pradesh recorded 25-65% & 6% damage to pigeonpea & chickpea crops, respectively. 15-20% yield loss of sorghum was reported in Bangalore (Karnataka) (Anonymous, 1974). The tomato fruits were heavily damaged (40-50%) by this pest in Tamil Nadu (Srinivasan, 1959) and 80% in Karnataka, (Anonymous, 1974). In Andhra Pradesh, Bhatnagar & Davies (1978 b) recorded 32% H. armigera adults in safflower monocrop & 57% intercrops by light traps.

            Pigeon pea was most preferred among the key host plants recorded for oviposition,  & feeding followed by field bean, chickpea, tomato, cotton, mungabean & sorghum. Same host plants in the descending order of preference were observed for oviposition (Vijayakumar, 1980).  Among the acidic exudates, presence of oxalic acid (0.9 – 0.09%) attracted maximum number of eggs.  A higher population of H.armigera in sunflower plots adjacent to pigonpea plots was observed indicated the effect of neighbouring host plants on the population of H.arnigera.  Pigeonpea was more preferred in comparison to cotton (Singh et al., 2002).

 H.peltigera: It is pest of safflower.  It mainly feeds on weeds like Acanthospermum hispidium, Xanthium occidentale, Salvia glutinosa etc.  It is distributed in Andhra Pradesh, Gujarat, and Karnataka & Punjab.

H. assulata: It occurs in Andhra Pradesh, Assam, Bihar, Gujarat, Himachal Pradesh, Karnataka, Madhya Pradesh, Maharashtra, Meghalaya, Orissa, Tamil Nadu & Uttar Pradesh. This pest is very common on tobacco.  In India both H.peltigera & H. assulata are mostly restricted to weeds. 

Impact of parasitoids on Helicoverpa

Impact of parasitoids on Helicoverpa species:

             Three stages namely, eggs, larvae & pupae of Helicoverpa species are invaded by parasitoids, in addition to pathogens & predators.  In India, near about 162 arthropod parasitoids   have been recorded on H. armigera.  Among the three life stages of the pest H.armigera, larval stage is preferred by largest number of parasitoids (110) followed by egg (19), larval-pupal (13), pupal (12) & egg-larval (8) (Lingappa et al., 2001).  Of the recorded number of parasitoids (114) - Hymenoptera (82) & Diptera (30) nematoda (02) on H. armigera; 20 – Diptera (6), Hymenoptera (13), Nematoda (1) on H. Peltigera; and 19 – Diptera (04), Hymenoptera (14), Nematoda (01) on H.assulata were recorded. These natural enemies suppress the population of Helicoverpa species by destroying their immature forms.

In India, very few workers studied the biology, breeding methods & the impact of dipterous parasitoids on Helicoverpa species in comparison with hymenopterous parasitoids.  The trichogrammatids (11), Scelionidae (02) are the main egg parasitoids (Manjunath et al., 1970, Manjunath, 1972; Mani & Krishnamoorthy, 1983; Lingappa, 2001;Singh et al., 2002). The tachinids 30, bethylids (02), braconids (31) & ichneumonids (33) are the larval parasitoids, of which some are active on all the crops (Achan et al., 1968; Rao, 1968; Anonymous, 1974; Pawar et al., 1986 a, b).  Chalcids (02) & some tachinids (07) are the larval-pupal parasitoids. Few are egg – larval parasitoids. International Crops Research Institute for the Semi Arid Tropics (ICRISAT) has identified 27 species of parasites from Andhra Pradesh, Maharashtra and Karnataka states (Bhatnagar et al., 1982). Ten of these species are relatively effective in controlling the Helicoverpa populations. Dipterous parasitoids invade mainly on old larvae 3-6 instars, while hymenopterans prefer younger larvae (1-3 instars). Host plants also play important role in selection of host by their parasitoids.  Acidic exudates on chickpea & pigeonpea plants affect the parasitism mainly for hymenopterous egg parasitoids.

Dipteran parasitoid complex

Dipteran parasitoid complex on Helicoverpa species:

A list of dipteran parasitoids invading Helicoverpa species can be summarized bellow (table1).

Table no.1: Dipteran Parasitoids on Helicoverpa species.

Order/family	H.armigera	H.assulata	H.peltigera	Total parasitoid species	Reference
Diptera Sarcophagidae	1	-	-	1	Achan et al., (1968)
Tachinidae	26	4	6	27	”     ”        ”
Chloropidae	1	-	-	1	”     ”        ”

Manjunath et al., 1985 cited 27 species of tachinidae on Helicoverpa spp. while referring the work of Achan et al., (1968) who made mention of 17 tachinid species. Lingappa et al., (2001) mentioned 30 species of tachinidae on bollworm.

Biosystematics of Tachinidae

 Biosystematics of Tachinidae:

Diptera are two winged, or “ true”, flies. Although the parasitic Diptera are not quite so biologically diverse as the parasitic Hymenoptera, they are parasites on hosts from more animal groups. Family Tachinidae (Tachinidae, from the Greek Taxivas, a here, from Taxivas, swift) referring to the active adults. German, Raupenfliegen Tachina (tachina) Flies; Tachinid Flies. They are ecologically important in balance of nature because larvae are parasites in other insects, spiders, woodlice and centipedes; employed in biological control of pests. It consists of about 300 genera and 5,000 species, distributed throughout the world. In North America there are some 190 genera and 1,500 species (Essig, 1982). In Southern Asia about 18genera and 30 species of tachinidae are recorded. In India 15 larval tachinid and 7 larvo-pupal parasitoids are recorded on H. armigera on cotton (Lingappa et al., 2001). Achan et al., (1968) recorded 17 species on different crops. On H. assulata 4 and on H. peltigera 6species of tachinidae are reported from Asia.

DeBach (1943), placed parasitoid according to egg laying habits as i.e. (i) oviposition apart from the host (ii) oviposition on the host and (iii) oviposition in the host e.g. in S.illota, oviposition is of second type. Eggs deposited allover the body. Van Emeden (1954) divided the Tachinidae into five sub-families as Phasiinae, Dexiinae, Macquartiinae, Tachininae, and Goniinae e.g. Gonia, Nmorilla, Carcelia, and Zenillia. All 30 species of tachinidae belong to subfamily Goniinae and play major role in control of H.armigera. Askew (1971) has given the modifications in Tachinidae, into six groups as (1) in some larvae or eggs are laid apart from the host on leaves or the surface of soil.  The eggs must be minute.  One female may lay upto 6000 eggs. (2) Larviparous or ovoviviparous place their progeny to the host's body. (3) Oviparous, eggs laid on foliage.  The eggs are very small (microtype), usually less than 0.2 mm long. (4) Oviparous, lay large eggs (macrotype) on the host.  The egg approaches one millimeter in length and may be soft shelled and attached to the host hair by stalk (Carcelia) (100 to 200 eggs). (5) Oviparous species that insert their thin-shelled eggs into the host by means of a piercing substitute ovipositor. (6) Larviparous or oviparous, introduce their progeny inside the body of host by a piercing apparatus. These modifications help for identification and classification of tachinidae.

Indigenous dipteran parasitoids

 Indigenous dipteran parasitoids:

In India total 30 species of tachinidae are distributed as mentioned in table no.2.Among all total tachinid dipteran parasitoid in India three Drino (Posturmia) imberbis Wiedmann, Curran, Carcelia illota Curran, Goniopthalmus halli Mesnil, are well known for   control of H. armigera. These attack old age larvae and control 12-18%, 4-16%, and 18-20% of H. armigera population. C.illota, G.halli, Exorista xanthaspis Wiedemann, Peribaea orbata Wiedemann and P.laxa are most common in Andhra Pradesh, Gujarat, Karnataka, Madhya Pradesh, Maharashra, Orissa, Rajsthan and Tamil Nadu, Uttar Pradesh (Achan et al., 1968;Pawar et al., 1986). These are recorded on host plants, chickpea, cotton, pigeonpea, tomato, sorghum sunflower and other crops.Among indigenous Indian dipterans, P.laxa, C.illota, G.halli, and Peribaea orbata were amenable to mass production and merit field evaluation. The tachinid successfully developed on H.zea (Manjunath, 1972).

Table no.2. -The name of dipteran parasitoid, host stage invasion on Helicoverpa species.

Family/genus/species	Host stage parasitoized	Helicoverpa species
		HA	HAS	HP
SARCOPHAGIDAE Sarcophaga orientoides S.W.3 TACHINIDAE Carcelia sp. 1 Carcelia (Senometopia) illota Curran1, 7** Carcelia (Senometopia) kolkiana Towensend1 Carcelia raoi Mesnil8 Carcelia peraequalis Mesnil1 Compsilura concinnata Meigen3 Drino (Prosturmia) imberbis Wiedemann1 Drino sp. nr. unisotosa Barranov1 Eucelatoria bryani Sabrosky*2 Exorista fallaxMeign1 Exorista japonica Towensend1 Exorista xanthaspis Wiedemann8*** Goniopthalmus halli Mesnil1, 8 Pales coeruleonigra Mesnil3 Palexorista sp. 4 Palexorista imberbis Wiedemann10 Palexorista  laxa Curran5 , 6 Palexorista solennis Walker6 Peribaea orbata Wiedemann10** Pseudogonia rufifrons Wiedemann10**(=Isomera cinerascens Rondani1) Sisyropa apicata Baranov1 Spallanzania sp. 1 Strobliomyia aegyptia Vill. 1 Sturmiopsis inferens Towensend6 Suensonomyia n. sp. 1 Thecocarcelia incedens Rondani1 Voria edentata Baranov1 Voria ruralis Fallen1 Winthemia sp.nr. diversoides Baranov1 CHLOROPIDAE Mepachymerus ensifer Thompson9	l lp lp lp lp lp l l l l l l l lp l l l l l lp l l l l l l l l l l l	+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + +	+ + + + + +	+ + + +

References - 1.Achan et al., 1968; 2.CIBC, 1968; 3.CIBC, 1974; 4.ICRISAT, 1974-85; 5.Manjunath et al., 1976; 6.Patel & Patitundu, 1981; 7.Pawar et al., 1985; 8.Rao, 1968; 9.Verma et al., 1971; 10. Lingappa et al., 2001, recently reported the tachinid species on cotton (typed in bold letters). *Imported parasitoid; field recovery reported. ** Recorded from noctuidae in Africa (Berg et al., 1988). ***Recorded from several families of Lepidoptera in Africa (Berg et al., 1988). L= larval; lp= larvo-pupal; HA=Helicoverpa armigera; HAS= Helicoverpa assulata; HP=Helicoverpa peltigera

C.illota, Eucelatoria bryani, Goniopthalmus halli, Vora ruralis are common in India and America (Kogan et al., 1989). C.illota, Exorista sorbillans, Exorista xanthospis, G.halli, Plexorista imberbis, P.laxa, are common in India and Africa on cotton (Greathead and Girling, 1989). C.illota is common in India and Australia (Michael, 1989).

Exotic tachinid parasitoid, Work on Tacinidae

Exotic tachinid parasitoid-Importation and establishment trials in India:

The tachinid Eucelatoria bryani was released and evaluated for control of Heliothis. Other research on this parasite includes assessing the toxicity of selected insecticides (Kushwaha, 1989).

Table no.3. -Tachinid parasitoids of H.armigera introduced in to India (Nagarkatti and Singh, 1989)

Species	Origin	Year of introduction	Establishment
Eucelatoria bryani Sabrosky Lespesia archippivora Riley	Arizona, USA Arizona, USA	1969,1978 1969,1970	Established at low level Not established

Sithanantham and Reed (1980) reported that in field cage   studies at ICRISAT, Hyderabad release of E. bryani in pigeonpea and chickpea resulted in 14.2% and 4% parasitism, respectively. These higher rates of parasitism could have been due to the flies being confined in field cages. In a subsequent report, ICRISAT entomologists reported that even after 40 generations of E.bryani in laboratory, it appeared to be biologically unchanged (Anonymus1982). Field release trials with this exotic fly around Bangalore (Karnataka) and Anand (Gujarat) revealed 0-8% control of H.armigera after recoveries of about 14 months release. This indicating that parasite can be temporarily established. Mani and Nagarkatti (in Nagarkatti and Singh, 1989) reported that certain insecticides such as quinolphos and the pyrethroid permethrin are highly lethal to E.bryani. So, indiscriminate use of these in or near release sites may delay or even prevent establishment of tachinid. This might be true with other indigenous tachinid and hymenopteran parasitoids; therefore we are not getting the expected results with natural enemies against H.armigera. Exotic tachinid, E.bryani was released during 1982-83 in Karnataka on tomato, lablab and gram, between December and April and the rate of parasitism ranged from 5 to 20 %; highest parasitism was recorded with this fly on tomato followed by red gram and lablab (Sivaprakasam et al., 1986a).

 Table no.4. - Export of tachinid parasitoids from INDIA into USA for control of Heliothis spp.

Species	Year	Destination States
Palexorista laxa Curran Exorista xanthaspis Wiedemann Carcelia spp. Goniopthalmus halli Mesnil	1963-65, 1968 1964-65 1964-65,1967-68 1966	AZ, GA GA AZ, GA NJ

AZ=Arizona, GA= Georgia, NJ=New Jersey

The parasitoids exported from India into USA for suppression of Pectinophora gossypiella (Saunders) the pink bollworms were also tried on Heliothis spp. larvae. These were not recovered after release (Powell, 1989), indicating their problem in establishment in new place. It might be because of some environmental factors and extensive use of pesticides.  

The tachinid P.laxa from Kenya has been studied to a great extent in the laboratory. This species often oviposit many times on a host larva as the number of eggs increases, the mean weight per puparium decreases. This results in size differential of adult flies. The relative number of progeny per medium and large female is significantly greater than that per small parent, thus rearing programme would be aimed at producing a greater proportion of medium sized flies (Powell, 1989). 

Work on Tachinidae:

            Bess, (1936) studied the biology of Leschenaultia exul Townsend, a tachnid parasite of Malacosoma americana Fabricius and Malacosoma distria Hubner. Jones, (1939) studied the biology of   Paradrino halli Curran. The biology of Tachinidae is reviewed by Clausen (1940) and Herting (1960). Reed (1965) regularly recorded C. evolans (illota) as a parasite of H. armigera at Ukiriguru (Tanzania).  Chauthani and Hamm (1967) worked on exotic parasite Drino munda Wied, on H.zea (Boddie). Achan et al., (1968) described the breeding technique for C. illota and other three tachinid spp. viz. Palexorista laxa, Exorista fallax, and Goniophthalmus halli. Jackson et al., (1969) reared Eucelatoria armigera in the laboratory at several constant temperatures. Patel and Singh (1970) studied the bionomics of C. illota; Sriharan et al., (1971) worked on Uzi fly, Tricholyga bombycis, a parasite of Bombyx mori (L). Patel and Singh (1972) studied the biology of G. halli Mesnil; the duration of developmental stages of Drino halli Curran has been studied by Robertson (1973). Hughes (1975) studied the biology, mating, longevity larvipostion, fecundity, and mortality of larviparprous tachinid Archytas marmoratus (Townsend) under controlled conditions. Nettles and Burks (1975) searched a chemical substance from Helicoverpa larvae stimulating larvipostion by females of A. marmoratus (Townsend). Jackson et al., (1976) described the biology of Palexorista laxa Curran parasitizing Helicoverpa zea Boddie. Ziser et al., (1977) determined the effects of the number of maggots per host (H. Virescens) on length of development of larvae and pupae, puparial weight and adult emergence of Eucelatoria spp. Datta and Mukherjee (1978), worked on life history of Uzi fly, Tricholyga bombycis. Sankaran and Nagraja, (1979) studied the development and multiplication of Eucelatoria sp.near armigera (Coq.) in India, a exotic species from USA The biology of Pseudopodia ruffifrons Wiedemann under its synonym Gonia cinerascens has been extensively studied by Campadelli and Barionio (1979). Yadav (1980) reared Eucarcelia illota Curran; Drino imberbis Wied; Exorista xanthospis Wied; Palexorista laxa Curran; Goniophalmus halli Mesnil and an unidentified species form H. armigera.  Bilapate (1981) recorded the percent parasitization on larvae of H. armigera by Carcelia spp. on sunflower, jowar and pigeonpea during August to November 1978. Bhatnagar et al., (1982) observed C.illota as larval pupal parasite of H. armigera in South- Central India. It was reported as one of the dominant parasitoid recovered from the H. armigera. The level of parasitism was too low. The effect of pod borer resistant and susceptible cultivars of pigeonpea on the natural larval parasitism of H. armigera at International Crops Research Institute for the Semi- Arid Tropics, Patancheru (A.P.) (ICRISAT) center were compared (Sithananthan et. al., 1981-82). The influence of cultivars was more distinct during October - November when C. illota was the dominant parasite. Percent larval parasitism in 4-6 instars by C. illota has been studied on crops like sorghum, pearl millet, groundnut, pigeonpea and chickpea (Pawar et al., 1986).

KasturiBai et al., (1986) control of Uzi fly, Tricholyga bombycis, by semiochemicals. Recently Pawar et al., (1986) recovered C. illota. E. xanthaspis, G. halli, P laxa, Curran, P.solennis Walker; Palexorista spp. Sturmiopsis inferns Townsend form H. armigera, H. peltigera and H. assulta in Andhra Pradesh, Maharashtra and Karnataka (1977 - 1985). These tachinid species were tried as biological control agents for Helicoverpa spp. Berg et.al.,  (1988) reviewed the natural enemies of H. armigera in Africa. Pandit (1992) studied the host plant extract preference by C. illota on H. armigera on extracts of leaves of cotton, brinjal and tomato. Chaudhari, (1996,2000,2001,2002,2003) studied the biology, biometry, effect of temperature, breeding method, mating and oviposion behaviour, reproductive biology, host age selection, seasonal incidence, host plant preference, nutrition and longevity and effect of insecticides with Carcelia=Senometopia illota. Chaudhari and Nikam (1999) first studied the life tables and intrinsic rate of increase in C. illota.