Arthropod Natural Enemies of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in India

Biocontrol Science and Technology (1996) 6, 481± 508

R EVIEW

Arthropod Natural Enemies of Helicoverpa armigera (HuÈ bner) (Lepidoptera: Noctuidae) in India

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J. ROM EIS

AND

T. G. SHANOW ER

Crop Protection Division, International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Andhra Pradesh 502 324, India (Received for publication 16 November 1995; revised manuscript accepted 27 May 1996 )

H elicover pa arm igera (H uÈ bner ) (Lepidopt era: Noctuidae ) is one of the most seriou s insec t pests in the O ld World . In India, it causes substan tial losses to legu me, ® bre, cereal oilseed and vegetab le crops . This pape r reviews the literatur e on the biology , ecology , ef® cacy, rearin g and aug mentatio n of ende mic parasit oids and predato rs, as well as exotic parasit oids introduc ed and release d in India. It also provide s update d lists of H . arm igera natura l enem ies native to India. In addition , reports of aug m entativ e release s of Trichogra m m a spp., the m ost extensiv ely studie d natura l enemy of H. arm igera are sum marized . K eyw ord s: Helicover pa armigera, natura l enem ies, biologic al control , India

INTRO DU CTIO N H elicover pa arm igera (H uÈ bner) (Lepidopt era: N octuidae ) is one of the m ost seriou s insect pests in the O ld W orld . It is widely distribut ed from the C ape V erde Island s in the Atlantic Ocean, throug h Africa, A sia and Australi a to the South Paci® c island s and from souther n Europ e to New Zealan d (Reed & Pawar, 1982). In India, H. arm igera has been recorde d on at least 181 plan t specie s from 45 plan t families (M anjunat h et al., 1989), includin g m ajor crops such as cotton (Gossypium spp.), sorghu m (Sorghu m bicolo r Linnaeus) , tom ato (Lycopersi con esculent um M ill.), pigeonp ea (Cajanu s caja n (Linnaeus ) M illspaug h) and chickpe a (Cicer arietinu m Linnaeus) . Annua l losses due to H. arm igera in pigeonp ea and chickpe a have recentl y been estim ated to exceed US$600 m illion (Interna tiona l Crops R esearc h Institut e for the Sem i-arid Tropics (ICR ISAT), 1992). Losse s in othe r crop s add substant ially to the total dam age caused by H . arm igera . Life-tabl e studie s reveal that H. arm igera often show s a typica l type III survivor ship curv e (Fitt, 1989 ) and m ost m ortality , biotic and abiotic , occurs durin g the egg and early larva l stag e (e.g. Kyi et al., 1991). How ever, survivor ship m ay vary between differen t crops and season s (e.g. V an den Berg & Cock, 1993a) . K ing et al. (1982) , King and C oleman (1989 ) and Fitt (1989 ) review ed the potentia l for biologic al contro l of H eliothis /H elicover pa spp., focusin g m ainly on the N ew W orld specie s Helicover pa zea (Boddie ) and H eliothi s virescen s (Fabricius ). King et al. (1982) listed severa l examples from the U S where, in the absenc e of insectic ides, natura l enemies m aintain Heliothis spp. populat ions belo w econo m ic levels . 0958±3157/96/040481±28 $7.50

Ó 1996 Journals Oxford Ltd

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482

J . R OM EIS & T . G . SH ANO W ER

This pape r revie ws researc h on the natura l enemies of H . arm igera in India . Include d are update d lists of ende m ic parasitoi ds and predator s, replacin g earlie r lists from M anjunat h et al. (1989) and Nikam and G aikwald (1989) , as well as a list of exotic parasito ids introduc ed into India against H . armigera. The use of mass release s of Trichogr amm a spp. (native and exotic ) for the biologi cal contro l of H. arm igera in India is also revie wed. M uch of the work reviewed in this pape r is unpubli shed or appear s in books and journal s not widely availabl e outsid e India. The prim ary objectiv es of this paper are to m ake these results availabl e to biocontr ol w orkers outsid e India, and to provid e a basis for furthe r researc h on H . arm igera natura l enem ies within India. The term ` percenta ge parasitis m ’ is used through out this revie w. There are severa l proble m s associat ed with this term (see Van Driesch e (1983 ) for furthe r discussi on). In the studie s cited here, H . arm igera eggs and/or larva e w ere collecte d in the ® eld and held in the laboratory. The percent age parasitis m has been estimated by sim ply dividin g the num ber of hosts produci ng parasitoids by the total num ber of hosts collecte d. This does not accurat ely re¯ ect the im pact of speci® c parasitoi ds on H . arm igera populati ons, but is the only measure m ent given in thes e studies . In this review , parasitis m levels are only cited when both the host stag e and the num ber of hosts collected are reported . N ATIVE EGG A ND EG G±LA RVA L PA RA SITOID S Six egg parasitoids from tw o fam ilies are recorde d from India (Table 1), but only T. chilonis Ishii (Hymenopter a: Trichogra m matidae ) is found in signi® cant num bers in the eggs of H. arm igera (M anjunath et al., 1970 ; Sithanant ham et al., 1982a) . This specie s w as earlier kno wn as T. australi cum G irault or T. confusu m Viggiani , which were synono m ized w ith T. chilonis by N agarkatt i and N agaraj a (1979) . O f the seve n Trichogra m m atoide a nativ e to India (N agaraja , 1978), T. arm igera N agaraja, T. bactrae Nagaraj a and T. bactrae sp. fum ata Nagaraj a have been recorde d from H. arm igera eggs . O nly a single, uncon® rm ed report of egg parasitism of H . arm igera by a Telenom us sp. (H ym enopter a: Scelionid ae) exists (M anjunat h et al., 1970) . Four egg±larva l parasito ids, all specie s of C helonus (Hym enoptera : Braconid ae), have been recorde d parasiti zing H. arm igera eggs (Table 1). The levels of egg parasitism by endem ic Trichogr am ma spp. vary w idely on differen t host plants (Table 2). The reason s for low parasitis m rates on sun¯ ow er (Helianthu s annuu s Linnaeus) have not been investig ated ; on okra (Abelm oschu s esculent us (H.) M oench) , trichogr amm atid s are trappe d and killed by the stick y exudat e on the capsule s (G oretzkay a, 1940). C hickpe a secrete s an acid exudat e from all green tissues w hich is though t to interfer e with Trichogram ma spp. searchi ng behavio ur (Yadav et al., 1985 ; Paw ar et al., 1986b) . T he only record of egg parasitis m by nativ e trichogr am m atid s on chickpe a was by G angarad di (1987) , who foun d 4% of eggs parasiti zed by T. achaeae Nagaraj a and N agarkatt i aroun d D harw ad (K arnataka ). N o details of sam plin g procedu res or frequenc y w ere given, m akin g it dif® cult to assess . O n pigeonp ea, parasitoids are repelle d on or near the plan t surfac e and walking behavio ur has been foun d to be signi® cantly hindere d by trichom es and trichom al exudate s on pigeonp ea bud s and pod s (J. R om eis, unpubli shed). In tradition al pigeonp ea±sorghu m inter-cro pping syste m s in India , where pigeonp ea produce s ¯ owers at least 1 m onth afte r sorghu m anthesis , Trichogram ma spp. w ere foun d to parasiti ze only low levels of H. arm igera eggs on the pigeonp ea (Bhatnaga r & Davies, 1981). W hen shortduratio n pigeonp ea is inter-cr opped with hybrid sorghu m , ¯ ow erin g tim es and the availabi lity of H . arm igera eggs are m ore closely synchro nized . In this system , Duf® eld (1994 ) found that the m ovem ent of the parasito ids to pigeonp ea was facilitat ed and egg parasitis m levels of up to 69% on differen t pigeonp ea genotyp es were recorde d. Sim ilar studie s have not been able to duplicat e these results (J. R om eis, unpubli shed). M anjunat h (1972 ) reporte d an averag e parasitis m leve l of 4.5% (n 5 1175) for T. arm igera in H . arm igera eggs on tuberos e (Polianthu s tuberos a Linnaeus) . There are no report s of ® eld parasiti sm rate s for T. bactrae and T. bactrae sp. fum ata. Sim ilary , no levels of parasitis m are reporte d for Telenom us sp.

NA TUR AL ENEM IES O F H . A RMIGER A IN INDIA

TABLE 1.

Parasitoids of H. armigera reported from India

Order, family and species

a

DIPTER A Sarcophagidae Sarcophaga sp. Seniorwhitea reciproca (Walker) (as Sarcophaga orientaloides White)

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Tachinidae Carcelia sp. Carcelia S. L. ? illolacum c Carcelia kockiana Townsend {Carcelia peraequalis M esnil} c Carcelia raoi Compsilura concinnata Meigen Exorista bombycis (Louis) Exorista japonica (Townsend) Exorista xanthaspis (Wiedemann) Exorista xanthaspis (Wiedemann) (as E. fallax of authors) Goniophthalmus halli Mesnil Hystricovoria bakeri Townsend (as Afrovoria indica (M esnil) {Pales coeruleo-nigra (M esnil)} Palexorista sp. Palexorista (as Drino) sp. nr. unisetosa Palexorista laxa (Curran) (as Drino imberbis (Wiedemann)) d Palexorista (as Drino) munda (Wiedemann) Palexorista solennis (W alker) Peribaea spp. Peribaea orbata (Wiedemann) Peribaea orbata (Wiedemann) (as Strobliomyia aegyptia (Villeneuve)) Pseudogonia ru® frons (W iedemann) (as Isomera cinerascens (Rondani)) Senometopia (as Eucarcelia) illota (Curran) c Sisyropa apicata Sisyropa formosa M esnil Sturmiopsis inferens Townsend Suensonomyia n. sp. Thecocarcelia acutangulata (Macquart) (as T. incedens (Rondani)) Voria ruralis (Fallen) Voria ruralis (Fallen) (as V. edentata Baranov) Winthemia sp. nr? diversoides Baranov

Host stage b parasitized

Reference

L? Lp

Srinivas & Jayaraj, 1989 CIBC, 1974

L? L? L? L? L? L L L L L

Achan et al., 1968 Raodeo, 1971 (in Raodeo & Sarkade, 1979) Achan et al., 1968 Achan et al., 1968 Rao, 1968 CIBC, 1974 Swam y et al., 1993 Achan et al., 1968 Bhatnagar et al., 1982 Achan et al., 1968

Lp L

Achan et al., 1968 Raodeo et al., 1982

L L L L

CIBC, 1974 Mathur, 1970 Achan et al., 1968 Achan et al., 1968

L L L L L

Chauthani & Hamm, 1967 ICRISAT, 1976 Tripathi & Sharma, 1985 Chari et al., 1992 Achan et al., 1968

Lp

Achan et al., 1968

L or Lp L L L ? L

Achan et al., 1968 Achan et al., 1968 Raodeo et al., 1982 ICRISAT, 1976 Achan et al., 1968 Achan et al., 1968

L L

Achan et al., 1968 Achan et al., 1968

L

Achan et al., 1968

Chloropidae Mepachymerus ensifer (Thomson)

L

Verma et al., 1971

HYM ENOPTERA Bethylidae Goniozus sp. Goniozus (as Parasierola) sp. Odontepyris sp.

L L L

Sivagami et al., 1975 Divakar et al., 1983 Rao, 1968

Braconidae Agathis fabiae (Nixon) Aleiodes (Rogas) sp. e Aleiodes sp.? testaceus (Spinola) Apanteles sp.

L L L L

Srinivas & Jayaraj, 1989 Yadav, 1980 Pawar et al., 1986a Achan et al., 1968

483

484 TABLE 1.

J . R OM EIS & T . G . SH ANO W ER

Continued

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Order, family and species

a

Host stage b parasitized

Reference

Apanteles sp. nr. taprobanae Cameron Apanteles sp. (vitripennis group) Apanteles angaleti M uesebeck Bracon sp. Bracon cushmani M uesebeck Bracon gelechiae Ashm ead Bracon greeni (Ashm ead) Bracon lefroyi (Dudgeon & Gough)

L L L L L L L L

Chelonus sp. Chelonus curvimaculatus (Cameron) Chelonus formosanus Sonan Chelonus heliopae Gupta Chelonus narayani Subba Rao Cotesia (as Apanteles) sp. nr. glomeratus (Linnaeus) Cotesia (as Apanteles) sp. (glomeratus group) Cotesia (as Apanteles) ru® crus (Haliday) Cryptosalius sp. Glyptapanteles (as Apanteles) sp. nr. phytometrae (Wilkinson) Habrobracon (as Bracon) brevicornis (Wesmael) Habrobracon (as Bracon) hebetor (Say) Microplitis sp. Microplitis ¯ aviventris Ivanov Snellenius (as Microplitis) maculipennis (Szepligeti)

El El El El El L L L L? L

Yadav, 1980 Kushwaha, 1995 Patil et al., 1991 Achan et al., 1968 CIBC, 1974 Achan et al., 1968 Achan et al., 1968 Seshu Reddy, 1973 (in Jayaramaiah & Jagadeesh Babu, 1992) Bhatnagar et al., 1982 Bhatnagar et al., 1982 Yadav, 1980 Achan et al., 1968 Subba Rao, 1955 Achan et al., 1968 Achan et al., 1968 Achan et al., 1968 Srinivas & Jayaraj, 1989 Yadav, 1980

L L L L L

Achan et al., 1968 CIBC, 1974 Hussain & M athur, 1924 Yadav, 1980 Krishnamurti & Usman, 1954

P

Achan et al., 1968

Ð

Singh et al., 1990

L L L

Mathur, 1970 Singh & Balan, 1986 Yadav, 1980

P

Cherian & Subramaniam, 1940

Lp L L Lp L? L L L L L L L P L L L

Mathur, 1970 Hussain & M athur, 1924 Mathur, 1967 Mathur, 1967 Yadav, 1980 CIBC, 1974 ICRISAT, 1976 Dutt, 1923 Kakar & Dogra, 1989 Nanthagopal & Uthamasamy, 1989 Singh et al., 1990 Pawar et al., 1986b Raodeo et al., 1982 Achan et al., 1968 Pawar et al., 1986b ICRISAT, 1976

L L L

Gauld & M itchell, 1981 Gauld & M itchell, 1981 Bilapate, 1981a

Chalcididae Brachymeria albicrus (Klug) (as B. responsator (W alker)) Brachymeria marmonti (Girault) (as B. wittei (Schmitz)) f Eulophidae Euplectrus sp. Euplectrus euplexiae Rohwer Stenomesius japonicus (Ashm ead) (as S. impressus Masi) Tetrastichus howardi (Olliff) (as T. ayyari Rohwer) Ichneumonidae Agrypon nox Morley Attractodes sp. Banchopsis ru® cornis (Cameron) Barichneumon sp. Briborus sp. Campoletis sp. Campoletis chlorideae Uchida Campoletis multicinctus Gravenhorst Campoplex collinus (Morley) Charops aditya Gupta & Maheshwary Charops bicolor (Szepligeti) Disophrys sp. Ecthromorpha sp. Enicospilus sp. Enicospilus sp. nr. shinkanus Uchida Enicospilus sp. nr. insinuator (Sm ith) (as nr. zyzzus Chiu) Enicospilus capensis (Thunberg) Enicospilus heliothidis Viereck Enicospilus heliothidis Viereck (as E. biconatus Townes, Townes & Gupta)

NA TUR AL ENEM IES O F H . A RMIGER A IN INDIA

TABLE 1.

Continued

Order, family and species

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485

a

Enicospilus melanocarpus Cameron Enicospilus shinkanus (Uchida) Enicospilus signativentris (Tosquinet) Enicospilus signativentris (Tosquinet) (as E. pectiniclavae Rao & Nikam) Eriborus sp. Eriborus argenteopilosus (Cameron) Eriborus pilosellus (Cameron) Eriborus trochanteratus (M orley) Eutanyacra (as Am blyteles) albuannulatus Cameron Gelis sp. Ichneumon sp. Leptobatopsis indica (Cameron) Metopius rufus Cameron Netelia sp. Temelucha sp. Xanthopimpla sp. Xanthopimpla punctata (Fabricius) c Xanthopimpla scutellare (Fabricius) Xanthopimpla stemmator (Thunberg) Scelionidae Telenomus sp. Trichogrammatidae Trichogramma sp. Trichogramma achaeae Nagaraja & Nagarkatti Trichogramma chilonis Ishii g (as T. australicum Girault, T. confusum Viggiani ) Trichogrammatoidea sp. Trichogrammatoidea armigera Viggiani Trichogrammatoidea bactrae Nagaraja Trichogrammatoidea bactrae sp. fumata Nagaraja

Host stage b parasitized

Reference

L Lp L L

Gauld & M itchell, 1981 Bhatnagar et al., 1982 Nikam, 1980 Nikam, 1980

L L L L P L? L L? L? L L L? P P Lp

Achan et al., 1968 Achan et al., 1968 Achan et al., 1968 Bhatnagar et al., 1982 CIBC, 1974 Singh, 1994 ICRISAT, 1976 Srinivas & Jayaraj, 1989 ICRISAT, 1976 Mathur, 1970 Bhatnagar et al., 1982 Srinivas & Jayaraj, 1989 CIBC, 1974 CIBC, 1974 ICRISAT, 1976

E

Manjunath et al., 1970

E E E

Bhatnagar et al., 1982 Nagaraja & Nagarkatti, 1969 Manjunath et al., 1970

E E E E

Bhatnagar et al., 1982 Manjunath, 1972 Jai Rao et al., 1980 Bhatnagar et al., 1982

a

Species in {square brackets} are African (N. P Wyatt, personal communication, 1996). E 5 egg; El 5 egg±larval; L 5 larval; Lp 5 larval±pupal; P 5 pupal parasitoid; L? 5 larvae were attacked, host stage of emergence is unknown; ? 5 unknown. c These species names are probably not valid (N. P. W yatt, personal communication, 1996). d M isidenti® cation recognized by CIBC (1978). e The genus Rogas was transferred to Aleiodes (see Van den Berg et al., 1988). f Hyper-parasitoid of Braconidae and Ichneumonidae (BoucÏ ek, 1988). g Synonomized by Nagarkatti and Nagaraja (1979). b

Little is kno wn about the ecolog y of C helonus spp. egg±larva l parasito ids. Parasitis m levels caused by C . heliopae Gupta and C . narayan i Subba Rao were found to be ` negligi ble’ in R ajastha n (A chan et al., 1968). For C. curvimaculatu s (Cam eron), parasitis m levels (based on sam ples of ® rst to third insta r larvae ) w ere foun d to be belo w 2% on differen t crops, w ith 7.5% recorde d on pearl millet by Pawar et al. (1986a ) (Table 3). In addition , D uf® eld (1993 ) found that up to 5% of the ® rst and second insta r larva e collecte d (n 5 784 ) on differen t pigeonp ea varietie s w ere parasiti zed by this parasito id. Sim ilar low levels of parasitism were reporte d by Kushwaha (1995) from ® rst to sixth instar larvae collecte d on chickpe a (n 5 1495), pigeonp ea (n 5 965) ( , 1% ) and lucern e (M edicag o sativa Linnaeus ) (2% , n 5 280) . The levels of parasitis m caused by this group of parasito ids are likely to have been underes timated in m any studies ; the ® rst two larval instars , which are dif® cult to ® nd in the ® eld and are often overloo ked, are the optim al host stages from which to sample Chelonus spp. The m ass rearing of Trichogram ma spp. has been widely studied . In India, they are usually reared on eggs of the factitiou s host C orcyra cephalo nica Stainto n (Lepidopt era: Pyralidae )

486

J . R OM EIS & T . G . SH ANO W ER

TABLE 2.

Mean parasitism levels of H. armigera eggs caused by naturally occurring populations of Trichogramma spp. on different crops and weeds

Host plant Chickpea

Parasitism level (% )

Reference a

4 084 1 022 865 650

0.0 0.0 0.0 0.0

158 86 40 150 245 150

60.1 51.0 50.0 38.0 29.8 3.0

Patel, 1980 Naganagoud & Thontadarya, 1984 Yadav et al., 1985 Sithanantham et al., 1982a Pawar et al., 1986a Dhandapani et al., 1992

887 1 048

37.0 35.8

Sithanantham et al., 1982a Pawar et al., 1986a

23

17.4

Pawar et al., 1986a

709 2 805

32.3 14.8

Sithanantham et al., 1982a Pawar et al., 1986a

122

29.5

Yadav et al., 1985

392 3 150

47.2 32.9

Sithanantham et al., 1982a Pawar et al., 1986a

150 124 680 676

8.0 5.0 0.1 0.1

255 3 281

15.3 12.5

Sithanantham et al., 1982a Pawar et al., 1986a

26 756 6 887

0.2 0.2

Pawar et al., 1986a Sithanantham et al., 1982a

Potato

407

56.0

Yadav et al., 1985

Saf¯ ower

612

17.5

Pawar et al., 1986a

9 466 35 408

40.6 33.6

Sithanantham et al., 1982a Pawar et al., 1986a

Sun¯ ower

287

0.3

Tomato

585 440 447

14.9 2.3 2.2

Yadav et al., 1985 Sithanantham et al., 1982a Pawar et al., 1986a

1 175

35.7

M anjunath, 1972

Acanthospermum hispidum

173

4.0

Pawar et al., 1986a

Cleome gynandra

160

0.0

Pawar et al., 1986a

Cocculus hirsutus

50

6.0

Pawar et al., 1986a

Commelina benghalensis

115

9.6

Pawar et al., 1986a

Corchorus trilocularis

108

1.0

Pawar et al., 1986a

2 688

0.4

Pawar et al., 1986a

50

6.0

Pawar et al., 1986a

Cotton

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No. of eggs collected

Cowpea Green gram Groundnut Lucerne Maize Okra

Pearl millet Pigeonpea

Sorghum

Tuberose

Datura metel Emilia sonchifolia

Pawar et al., 1986a Sithanantham et al., 1982a Yadav & Patel, 1981 Yadav et al., 1985

Thontadarya et al., 1978 Naganagoud & Thontadarya, 1984 Pawar et al., 1986a Sithanantham et al., 1982a

Pawar et al., 1986a

NA TUR AL ENEM IES O F H . A RMIGER A IN INDIA

TABLE 2.

487

Continued No. of eggs collected

Host plant Lagascea mollis

b

Parasitism level (% )

Reference

1 935 4 204

0.5 5.9

Pawar et al., 1986a Romeis, unpublished

Sesbania bispinosa

50

16.0

Pawar et al., 1986a

Sonchus oleraceus

295

9.1

Pawar et al., 1986a

a

Parts of the data in Pawar et al. (1986a) have been reported in Bhatnagar et al. (1982, 1983) and Pawar et al. (1986b, 1989a). b Earlier misidenti® ed as Gomphrena celosioides (N. J. Armes, personal communication, 1996).

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TABLE 3.

Parasitism levels of H. armigera larvae by common parasitoids on different crops and weeds in Andhra a Pradesh, M aharashtra and Karnataka (after Pawar et al., 1986a) No. of b larvae collected

Crop

L1±L3

L4±L6

Bean Chickpea Cotton Cowpea Green gram Groundnut Linseed M aize Onion Pearl millet Pigeonpea Saf¯ ower Sorghum Sun¯ ower Tomato

9 33 960 86 1 949 58 3 627 1 040 556 21 784 21 294 2 831 19 104 224 973

116 30 398 115 4 256 738 3 308 1 020 1 669 80 365 68 394 2 509 18 627 127 2 076

485

1 566

1 546 2 227 3 943 101

480 2 891 1 800 592

Acanthospermum hispidum Cleome gynandra Datura metel Lagascea mollis e Sesbania bispinosa

Parasitism level (%) caused by Chelonus c curvimaculatus

,

,

,

Senometopia d illota

Goniophtalmus d halli

0.0 0.1 0.0 0.1 0.0 0.2 12.1 0.5 0.0 1.3 5.6 6.5 1.4 0.0 0.1

0.9 7.0 0.0 0.8 3.1 1.5 8.1 0.3 3.8 6.3 8.2 7.5 3.4 0.0 0.3

1.7 0.4 0.0 3.3 0.4 1.9 15.2 0.2 1.2 0.5 7.4 1.6 0.4 4.7 0.3

3.7

0.2

0.0

0.1

7.1 0.0 3.0 0.0

0.8 0.0 0.4 13.9

0.0 0.9 0.5 4.6

0.0 0.2 1.0 20.1

0.0 0.1 0.0 0.2 1.7 0.1 0.5 0.0 0.0 7.5 0.1 1.0 1.3 0.0 0.0

Eriborus spp.

,

c

a Parts of the data in Pawar et al. (1986a) have been reported in Bhatnagar et al. (1983) and Pawar et al. (1985a, 1986b, 1989a). b L1±L3 5 ® rst to third instar larvae; L4±L6 5 fourth to sixth instar larvae. c Parasitism levels are based on collected ® rst to third instar larvae. d Parasitism levels are based on collected fourth to sixth instar larvae. e Earlier misidenti® ed as Gomphrena celosioides (N. J. Armes, personal communication, 1996).

(Singh et al., 1994a) . N avaraja n Paul et al. (1981 ) have show n this to be a suitabl e alternati ve to H. armigera . B efore exposur e to the parasito ids, C . cephalo nica eggs should be kille d becaus e the larvae are canniba listic. Eggs are usuall y killed by ultraviol et (UV ) irradiati on (M aninde r & V arm a, 1980; Singh et al., 1994a) . The reco mm ended exposur e tim e varies accordi ng to the intensit y of the UV source . Hugar et al. (1990 ) showed that eggs could be killed by chillin g at 2 5 °C for 48 h, but these eggs were signi® cantly less accepta ble to T. chilonis than were untreate d eggs. Parasitiz ed eggs can be store d at 10 °C for as long as 49 days without affectin g parasitoid surviva l (Jalali & Singh, 1992). Patil et al. (1978 ) reporte d that eggs parasiti zed by the

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488

J . R OM EIS & T . G . SH ANO W ER

exotic T. brasilie nsie Ashm ead could be store d at 8 °C for up to 1 week w ithou t affectin g parasitoid fecundit y. Several potentia lly seriou s constrai nts to mass rearin g T. chilonis have been reporte d. Laborator y-reare d fem ales have show n a signi® cantly highe r degree of sterilit y than w ild-typ e females (Nagarkatti & Nagaraja , 1978), and laborato ry-reare d populati ons w ere m ore sensitiv e to both high and low tem perature s than wild types (N agarkatt i, 1979). In searchin g for strains of T. chilonis bette r adapte d to certain ® eld conditio ns, M andal and Som choudhu ry (1991) , as well as Jalali and Singh (1993) , com pared parasitoid populati ons collecte d from differen t habitat s and localitie s. They foun d variatio ns in m orpho metric and biologi cal attribute s, such as the num ber of host eggs parasiti zed per fem ale and adult longevi ty. A braham and Pradha n (1976) atte mpted to selec t a T. chilonis strain adapte d to high tem perature s and low hum idity , but w ithou t success . M ass release s of severa l Trichogr amm a spp., predo minantly T. chilonis but also T. brasilie nsie, have been made on differen t crop s (Table 4). Unfortun ately , it is not often possibl e to determ ine w hether these release s have been success ful from the availabl e reports . In some cases, only the post-rel ease egg m ortalit y was measured . This has little value in determ inin g the econo mic bene® t of the release since pest densit y and the leve l of dam age m ust also be conside red. The biologic al contro l of H . arm igera on tom ato usin g Trichogr amm a spp. has been show n to be feasibl e with ® eld release s (Table 4). Singh et al. (1994a ) reco mm ended the releas e of T. chilonis or T. achaeae in cotto n at a rate of 150 000 fem ales ha 2 1 every week for 6 weeks startin g with the appeara nce of the pest. O ne of the constrai nts to the practica l and effectiv e use of Trichogram ma egg parasitoi ds is the low quality of ` Trichocar ds’ currentl y availabl e in India (J. R om eis, unpubli shed). Anothe r egg parasito id, T. bactrae , was successf ully reare d on C. cephalo nica eggs (Jai Rao et al., 1980). Neithe r specie s of Trichogra m matoida e has been m ass reared . The potential for m ass rearin g the egg±larva l parasito id C . heliopa e has been studie d by Patel et al. (1973) . O ne-day- old eggs of Spodop tera litur a Fabricius (Lepodop tera : Noctuidae ) were the most suitabl e factitiou s hosts . Super-par asitism was comm on in laborato ry culture s and was suspected to be the reaso n w hy larg e numbers of parasiti zed eggs faile d to hatch . Subba Rao (1955) successf ully reared C . narayan i on C. cephalo nica. Patel (1975 ) atte mpted weekly ® eld release s of C . heliopae in 0.4-h a plots of tom ato and chickpe a. In tomato, the highes t parasiti sm rate (6±7% ) was reache d after tw o release s of 150 000 parasitoids per hectar e per week or afte r ® ve release s of 100 000 parasito ids per hectar e per w eek. In chickpe a, the m aximum parasitis m rate w as higher (up to 21% ) after four release s of 100 000 parasitoids per hectar e per week. ` Y oung ’ post larvae were collecte d to evaluat e the parasitis m level. This parasitoid w as not success ful in regulati ng H. arm igera populati ons in eithe r crop. N ATIVE LAR VAL A ND LA RVA L±PUPAL PA RASITO ID S The larges t group of H . arm igera natura l enem ies reporte d from India are the larval and larval±pupal parasito ids w ith m ore than 60 identi® ed specie s (Table 1). The m ost im portan t and well-studi ed larva l parasitoi d, C am poletis chloride ae Uchid a (Hym enoptera : Ichneu m onidae) , is reporte d to be an importan t m ortalit y facto r for H. arm igera on severa l crop s and w eeds (Table 5). It preferen tially attack s secon d insta r larvae (Nikam & G aikwald, 1989) and is therefor e potentia lly effectiv e in suppres sing larval populat ions before signi® cant dam age is caused (N ikam & G aikwald, 1991 ; K ushw aha, 1995). Parasitoi d larva e em erge from third and fourth insta r host larvae to pupate and spin a cocoon , and thus sam pling the ® rst thre e instars of H . arm igera larva e w ould be necessar y to evaluat e accurate ly the impact of this parasitoi d. U nfortuna tely , very few author s have collecte d only the sm all (® rst to third instar) larvae . Therefor e, as a com parison , parasitis m levels m easure d on collecti ons of ® rst to sixth instar larvae are also listed in Table 5. As the table show s, collectin g all larval instars underes timates the actual parasito id im pact. Pimbert and Srivastav a (1989 ) foun d signi® cantly highe r levels of H. arm igera larvae parasiti zed by C. chloride ae on chickpe a inter-cr oppe d w ith coriand er (Coriandr um sativu m

7 10 7 7

5

10 8 6 c ?

Tomato

?

7

000 000 000 000

250 000

100 000

250 000

250 000

250 125 50 250

250 000

1 000 000

No. of females 2 released (ha

1

) b

chilonis chilonis brasiliense chilotraeae

T. chilonis

T. chilonis

T. chilotraeae

T. chilonis

T. T. T. T.

T. chilonis

T. chilonis

Species released

0.2

1.0

?

0.2

0.2 0.2 1.0 ?

0.2

1.0

Plot size (ha)

Parasitism level record is either maximum or range. b Released together with 50 000 Brinckochrysa scelestes/per release per hectare. c Unknown.

a

Chickpea

?

7

?

?

7

5

Sun¯ ower

Potato

7

3

Cotton

14

No. of releases

Interval between releases (days)

0

3

94

35±94

27±96 20±50 78 92

32±96

32

Test plot

0

0

?

13±84

15±52 0±11 12 ?

4±5

3

Control

Parasitism level (%)

a

Augmentative releases of Trichogramma spp. against H. armigera on different crops in India

Crop

TABLE 4.

No record

No record

No record

69% Reduction in H. armigera larvae

40% Reduction in H. armigera larvae 70% Reduction in fruit damage 65% Reduction in fruit damage No record 55% Reduction in fruit damage 50±75% Reduction in fruit damage

40% Reduction in H. armigera larvae

Evidence of success

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Yadav et al., 1985

Singh et al., 1994b

Yadav et al., 1985; Patel, 1980 Patel (in Stinner, 1977)

Yadav et al., 1985 Yadav et al., 1985 Singh et al., 1994b Patel (in Stinner, 1977)

Yadav et al., 1985

Dhandhapani et al., 1992

Reference

NA TUR AL ENEM IES O F H . A RMIGER A IN INDIA

489

490

J . R OM EIS & T . G . SH ANO W ER

TABLE 5.

Mean parasitism levels of H. armigera larvae caused by C. chlorideae on different crops and weeds No. of larvae a collected

Crop

L1±L3

L1±L6

33 960

78 14 950 64 358 666 30 222

Chickpea

18 111 Cotton

405 135 201 119

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86 Cowpea

Parasitism a level (%) L1±L3

L1±L6

29.2

35.9 18.5 15.4 12.2 8.8

Prasad & Chand, 1986 Kushwaha, 1995 b Pawar et al., 1986a Bilapate, 1981b Bilapate et al., 1988

10.4 9.6 3.5 2.5

Bilapate, 1981b Patel, 1980 Pawar et al., 1986a Kushwaha, 1995

14.7

8.1

Reference

1 949

6 205

6.9

2.2

Pawar et al., 1986a

58

796

13.8

1.0

Pawar et al., 1986a

Groundnut

3 627

6 935

6.8

3.6

Pawar et al., 1986a

Linseed

1 040

2 060

13.6

6.8

Pawar et al., 1986a

3.9

Kushwaha, 1995

4.4 3.8

Pawar et al., 1986a Kushwaha, 1995

Green gram

Lucerne

566

Maize

556

2 225 52

Pea

17.8

86

Pearl millet

784

1 149

Pigeonpea (1 256) 21 294 13 625 Saf¯ ower 2 831

Sorghum

19 104 (402)

Sun¯ ower

c

965 202 1 393 89 688 26 437 738 5 340 49 481 37 731

24.4

Kushwaha, 1995

49.0

33.4

Pawar et al., 1986a

(1.6) 3.6 1.4

10.2 1.5 1.4 0.9 0.7

Kushwaha, 1995 Bilapate, 1981b Duf® eld, 1993 Pawar et al., 1986a Bilapate et al., 1988

36.2 22.1 12.2 11.8

Pawar et al., 1985a Pawar et al., 1986a Bilapate, 1981b Kushwaha, 1995

49.2 (17.2)

24.9

Pawar et al., 1986a Duf® eld, 1993 c

41.6

224

351

6.3

4.0

Pawar et al., 1986a

3 311 3 049

5.3

4.2 1.7

Kushwaha, 1995

973 485

2 051

2.1

0.5

Pawar et al., 1986a

Cleome gynandra

1 546

2 026

6.6

5.0

Pawar et al., 1986a

Datura metel

2 227

5 118

7.6

3.2

Pawar et al., 1986a

3 943

5 743

21.4

14.7

Pawar et al., 1986a

101

693

23.8

3.5

Pawar et al., 1986a

65

230

24.6

7.0

Pawar et al., 1986a

Tomato Acanthospermum hispidum

Lagascea mollis

d

Sesbania bispinosa Aeschynomene indica

L1±L3 5 ® rst to third instar larvae; L1±L6 5 ® rst to sixth instar larvae. Parts of the data in Pawar et al. (1986a) have been reported in Bhatnagar et al. (1983) and Pawar et al. (1985a, 1986b, 1989a,b). c Data in parentheses are based on collected ® rst to fourth instar larvae. d Earlier misidenti® ed as Gomphrena celoisoides (N. J. Armes, personal communication, 1996). a b

NA TUR AL ENEM IES O F H . A RMIGER A IN INDIA

TABLE 6.

Crop

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Chickpea Cotton Pigeonpea Saf¯ ower Sorghum

491

Parasitism levels of ® rst to sixth instar H. armigera larvae by the tachinids Carcelia spp. (most probably including S. illota) in Maharashtra (after Bilapate, 1981b) No. of larvae (® rst to sixth instar) collected 666 405 202 49 25

Parasitism level (% ) caused by Carcelia spp.

G. halli

0.0 0.5 4.0 0.0 52.0

6.5 1.2 5.9 10.2 8.3

Linnaeus ) than on sole croppe d chickpe a plants . They suggest ed that nectar-ri ch coriande r plants w ere used as an adult food source and attracte d parasito ids to the chickpe a crop . There w as much confusi on abou t the taxono mic statu s of C. chlorid eae. It w as earlie r m isidenti ® ed as D iadegm a (Horogene s) fenestra le (H olm gren ) (Tikar & Thakare , 1961 ; see M athur & D harm adhikari , 1970 ) or as C . ¯ avicinct a (Ashm ead) (C. perdisti nctu s (V iereck)) (Gangrade , 1964 ; Achan et al., 1968; Vaisham paya n & V eda, 1980). The latter is know n as a parasitoid of Heliothis spp. from the Am erica s (K ogan et al., 1989 ) and does not occur in India. This m isidenti ® cation w as discuss ed by Gupta (1974) . How ever, Singh et al. (1991 ) still listed D . fenestra le as a parasito id of H . arm igera . One othe r genu s of hym enoptera n larval parasitoi ds, Eriborus spp. (H ym enopter a: Braconidae ), can cause signi® cant m ortalit y in the ® rst to third instar larvae on som e crop s and w eeds (T able 3). Kushwaha (1995 ) collecte d ® rst to sixth instar larva e on differen t crop s and reporte d 23% parasitis m from pigeonp ea (n 5 90) and less than 1% from chickpe a (n 5 14 950) and lucern e (n 5 112). Duf® eld (1993 ) collecte d over 400 ® rst to fourth instar larva e sorghu m and reporte d less than 1% parasitis m by Eriborus spp. They preferen tially parasitiz e second insta r larvae (Nikam et al., 1990). Tachinid s are the most importan t group of diptera n parasito ids. They parasitize olde r instars and em erge from sixth instar larva e or pupa e (Bilapate , 1981a,c ; Nikam & Gaikw ald, 1989). A chan et al. (1968) and Rao (1968 ) foun d 16±20% of H . arm igera larvae (base d on collecti ons of ® rst to sixth insta r larvae ) to be parasiti zed by each of three species : Palexoris ta laxa (Curran ) (earlie r m isidenti ® ed as D rino imberbis (W iede mann), as recogniz ed by the C om m onwealth Institut e of Biologica l Control (C IBC), 1978) and the larval±pupa l parasitoi ds Seno m etopia (as Eucarcel ia) illota (C urran ) and G oniopht halm us halli M esnil. S. illota, em erge s from host larva e (as a larva l parasito id) when early instars have been parasitiz ed (Patel et al., 1970). Collectin g fourth to six or ® rst to sixth instar host larvae , Paw ar et al. (1986a ) and Bilapate (1981b ) respecti vely observe d differen ces in the leve l of parasitis m cause d by tachinids am ong differen t crops and weeds (Table s 3 and 6). One dif® culty w ith the study by Bilapate (1981b ) is that all larval instars (® rst to sixth) were collecte d. As m entione d earlier , this w ill underest im ate the level of parasiti sm and may also bias the com pariso n betw een host plants . For exam ple, small larva e are easier to ® nd on chickpe a than on pigeonp ea (R eed et al., 1987 ; Reed & Lateef, 1990) , and the proporti on of larg e larvae collecte d will be relativel y highe r on pigeonp ea, resultin g in an overesti m ate of the level of parasiti sm caused by tachinid s. Patel et al. (1970 ) reporte d a mean parasiti sm level of 9.9% caused by S. illota on fourth to sixth insta r host larvae (n 5 3982) collecte d on differen t crops. D uf® eld (1993 ) sampled third to sixth instar larvae (n 5 747) on piegeon pea and reporte d a parasitis m level of 6.3% cause d by tachinid s. The host plan t on w hich H . arm igera is foun d has an im portan t effec t on the distribut ion and abunda nce of larval parasito ids. Some author s (e.g . Bhatnaga r et al., 1982 ; Sithanant ham , 1985 ) have generali zed that larvae of H . arm igera on pigeonp ea suffer greate r parasitis m by diptera n than by hym enoptera n parasito ids, while on chickpe a the latte r are m ore com m on. This m ay be true for som e techinid s (Tables 3 and 6; Sithana ntha m, 1981 ) and C. chloride ae (Table 5) but

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492

J . R OM EIS & T . G . SH ANO W ER

should not be extrapol ated to all diptera n and hym enopter an larval parasitoi ds. Sithana ntha m et al. (1982b , 1983 ) observe d that the choic e of cultiva r could affec t the ef® cacy of larval parasito ids. They reporte d lower parasiti zatio n rates on resistan t, com pare d with suscepti ble, cultivar s of chickpe a and pigeonp ea. The develop m ent of techniqu es used to rear larva l parasito ids has largely focuse d on C . chloride ae. The optim al develop m ental temperatur e for C. chlorid ae w as 31 °C (N ikam & B asarkar , 1978); at this temperatur e, egg-to- adult develop m ent was com pleted in 17 days , and adult longevi ty was 9 days when insects w ere provide d with 20% honey solution . Patel et al. (1988a ) observe d 100% emergenc e in C. chloride ae pupae stored at 8.2 °C for 10 days , but afte r 15 days em ergenc e decline d to 75% . The adult life span, however, was not adverse ly affected . A lthoug h this preliminary w ork has been carried out, a techniqu e for mass produci ng C . chloride ae is still not availabl e (M anjunat h, 1992). Two factors lim iting C . chloride ae rearing are the high m ortalit y among parasiti zed larvae and an unfavou rable sex ratio ( . 4 m ales:fe males ) in laborato ry-reare d parasito ids (Patel, 1975) . Basarka r and Nikam (1982 ) also reporte d a m ale-bias ed sex ratio in laborato ry cultures . Krishna moorthy and M ani (1989 ) reco m mende d using 4-day-o ld S. litura larvae as an alternati ve host for rearin g E. argente opilosu s (C am eron ) becaus e laborato ry culture s are less suscepti ble to vira l and bacteria l diseases . S. litura is readily accepte d by the parasito id. Rearin g m ethod s for thre e tachini d parasito ids, G . halli, S. illota and Palexoris ta (as Drino ) m unda (W iedem ann), have been reported . G. halli m ust be reare d on H. arm igera larvae. A ttem pts to rear this specie s on alternati ve lepidopt eran hosts were not successf ul (Patel & Singh , 1972). A t 27 °C egg-to-a dult develop ment was complete d in 23 days. O nly one parasitoi d emerged from each host, but as many as 87% of the laborato ry-reare d pupari a produce d adults (Patel & Singh , 1972). Patel et al. (1970 ) reared S. illota at 27 °C ; egg-to-a dult develop m ent was complete d in 25 days and fem ales produce d an averag e of 168 eggs. At 32 °C develop m ent was faste r (22 days), but the em ergin g adult ¯ ies were unable to expand their wings. Highe r parasiti sm levels were recorde d when host larvae w ere infeste d w ith tw o or three parasito id eggs (60 or 64% respecti vely ) instea d of one (48% ). H ow ever , the percent age of parasitoi d pupari a obtaine d w as highe r when only one egg w as placed in each host larv a (48, 35 and 30% for one, tw o and three eggs respectively), becaus e generall y only one parasito id maggo t em erge d from each host (Patel et al., 1970). Host larva e w ere anaesthe tized to reduce host defensiv e behavio ur. A rearing metho d for P. munda was develop ed in the US afte r im portatio n from India. Chauthan i and H am m (1967 ) reare d this parasito id at 26±28 °C and 70±90% relativ e hum idity on both H . virescen s and S. frugiper da (J. E. Smith) (Lepidopt era: N octuidae ). Severa l author s have observe d that tachini d parasito ids m ust be expose d to sunligh t to stim ulate mating (Achan et al., 1968; Patel et al., 1970 ; Patel & Singh , 1972). In contrast , Chauthan i and Hamm (1967 ) reporte d that P. munda m ated success fully unde r laboratory conditio ns withou t such exposur e. The potentia l for usin g larva l parasitoi ds in augm entativ e release s has been evaluate d in the US with promising results (King et al., 1982 ; King & Colem an, 1989), but no such effort has been made in India. M ass rearin g larva l parasito ids on H. arm igera is laboriou s and inef® cien t sinc e parasiti zed larvae m ust be reared in isolatio n to avoid cannibal ism (Nagarkatt i, 1982). A n effectiv e and econom ical m ass-rear ing m etho d m ust be develop ed before larva l parasito ids can be used in biologic al control . Possible solution s w ould be to use factitiou s hosts or an arti® cial diet; som e success ful exam ples of the latte r are listed by Grean y et al. (1984) . The larva e of H . peltiger a (D enis & Schiffer muÈ ller) (Lepidopt era: Noctuida e) could be used as an alternati ve host for som e parasito ids (N . J. A rmes, persona l com municatio n, 1995). Larvae of H. peltiger a are not cannibalisti c and are hosts of im portan t parasitoids such as C. chloride ae (M anjunath et al., 1976). N ATIV E PUPAL PAR ASITO IDS In contras t to the larg e number of larva l parasito ids, only ® ve pupa l parasito ids have been recorde d from H . arm igera in India : the chalci d Brachym eria albicru s (Klug) (as B. respons ator

NA TUR AL ENEM IES O F H . A RMIGER A IN INDIA

493

W alker) , the eulophid Tetrastichus howardi (Olliff) (as T. ayyari R hower) and three ichneu m onid s (Table 1). Only negligi ble parasitis m levels are reporte d for these pupa l parasito ids (Cheria n & Subram aniam , 1940 ; A chan et al., 1968; CIB C, 1974). However, in life-tabl e studies , pupa l mortalit y is underest im ated. As H . arm igera pupates under the soil surfac e (G hosh et al., 1986), pupa e are only rarely sam pled . Therefore , the pupal m ortalit y reporte d in H . arm igera life tables (e.g. Bilapate et al., 1979 ; Nanthago pal & U tham asam y, 1989 ; Tripathi & Singh, 1991 ) is cause d by larval±pupal parasito ids and does not includ e the impact of true pupal parasitoi ds. The effec t of pupal parasitoids m ay be importan t and should not be underest im ated. For exam ple, in A ustralia , M urray (1991 ) foun d that 8.2% of the pupae (n 5 124 ) collecte d in chickpe a were parasiti zed by Ichneu m on promissoriu s Erichson (Hymenopter a: Ichneu m onidae) .

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PR EDA TORS In India m ore than 60 specie s of arthropo ds are recorde d as predato rs of H. arm igera (Table 7). H owever, this relations hip has not been con® rm ed for about one-thir d of them under ® eld conditi ons. The biolog y of m ost of these predato rs is unkno w n, and their role in regulating H. arm igera populat ions, individu ally or as a group, has not been quanti ® ed. Few studie s have attem pted to estim ate the im pact of potentia l predato r specie s on H. arm igera populati ons. In com parison , Van den B erg and Cock (1993a, b) have show n that in East A frica , predator s, especial ly ants and anthoco rids, are the m ost im portan t group of natura l enem ies of H. arm igera on maize , sorghu m and sun¯ ow er. Chrysopi ds have been the m ost extensiv ely studie d grou p of H. arm igera predator s. Singh et al. (1994b ) studie d the feedin g potentia l of four nativ e chrysop id predator s in the laborato ry. M allada boninen sis (O kamoto) was the m ost effective , and consu med up to 463 H . arm igera eggs /® rst insta r chrysop id larva, follo wed by Apertochr ysa sp. (364 eggs /larva) , M . astur (Banks) (244 eggs/larva ) and C hrysope rla carne a Stephens (175 eggs/larva). Durin g its larval develop m ent, a single larv a of Brinckoch rysa (as Chrysopa ) scelestes (Banks ) (N europter a: Chrysopi dae) consum ed 665 eggs or 410 youn g larvae . Its larva l develop m ent was com pleted in 8.6 days when fed on eggs and 11.7 days when fed on larvae (Krishna moorthy & M ani, 1982). However, the feedin g potentia l of chrysop ids has not been teste d in the ® eld. Other predator s such as the mud wasps, Delta pyrifor m e (Fabricius) , D. companifor m e esuriens Fabriciu s and D. conoide us (Gm elin ) (H ymenopter a: Eum enidae) , which prey on larva e of H . arm igera , have only limited value in controll ing the pest becaus e of their long generati on tim e. Their activity m ight be increas ed by providi ng source s of w ater and nestin g sites protecte d from ants (Paw ar & Jadhav , 1983). This type of habita t m anipulat ion to augm ent natura l enemies has not been investig ated . The feedin g potentia l of the ant specie s recorde d as predator s on H . arm igera is still unkno w n. O bservati ons by King (1986) at ICRISA T indicate d a high larval m ortalit y by Cam ponotus sp. A n ongoin g stud y at ICRISA T indicate s that ants may be im portan t predator s of H. arm igera pupae (K. B. Tawar, persona l com municatio n, 1995). T he host plan t has an impact on the ef® cacy of ants and perhap s othe r predato rs. R om eis et al. (1996) observe d Paratrec hina longico rnis (Latreille ) removing H. arm igera eggs from potted pigeonp ea plants . Large numbers of eggs w ere removed from leaves , w hile eggs on ¯ ower-buds , ¯ ower-petal s or pods suffere d signi® cantly less predatio n. The differen ce seem s to be due to the type and distribu tion of trichom es on differen t pigeonp ea plant structur es. Very few studie s have investig ated the abundan ce and w ithin-pla nt distribut ion of differen t predato rs. D uf® eld (1993 , 1995 ) studie d predator s in pigeonp ea±sorghu m ® elds and foun d the follo wing predator y group s to be most abundan t: neuropte rans, m ainly chrysop ids; coccinel lids, m ainly Chilom enes (as M enochilu s) sexmaculatu s (Fabricius); anthoco rids, mainly Orius spp. and spiders . O nly the anthoco rids showed a seasona l abunda nce and within-plant distribu tion pattern m irrorin g that of H. arm igera eggs. A nthocori ds m ay use H . arm igera eggs as prey m ore

494 TABLE 7.

J . R OM EIS & T . G . SH ANO W ER

Arthropod predators of H. armigera reported from India

Order, family and species

Reference

COLEOPTERA Anthicidae Formicomus sp.

E

Sigsgaard, 1996

Carabidae b Calosoma indicum Hope

?

Singh et al., 1990

Coccinellidae Chilomenes (as M enochilus) sexmaculatus Fabricius Coccinella septempunctata (Linnaeus)

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Reported stage a attacked

Staphilinidae Unidenti® ed species

E, L

Bhatnagar et al., 1983

E, L

M ehto et al., 1986

L

Singh, 1994

L

Bhatnagar et al., 1983

L

Bhatnagar et al., 1983

Labiduridae Nala lividipes (Dufour)

L

Bhatnagar et al., 1983

OR THOPTE RA M antidae Humbertiella sp.

L

Bhatnagar et al., 1983

DE RMAPTERA Carcinophoridae Euborellia annulata (Fabricius) (as E. stalli (Dohrn)) Euborellia annulipes (Lucas)

HE MIPTERA Anthocoridae Orius albidipennis (Reuter) b Orius maxidentex (Ghauri) Orius tantillus (Motschulsky)

E, L E, L E, L

Salim et al., 1987 Bhatnagar et al., 1983 Sigsgaard & Esbjerg, 1994

Lygaeidae Paromius gracilis (Rambur)

L

Bhatnagar et al., 1983

M iridae Cyrtopeltis (as Nesidiocoris) tenuis (Reuter)b

?

Chari et al., 1992

Nabidae Nabis spp. Nabis (as Tropiconabis) capsiformis Germar

L L

Yadav, 1990 Bhatnagar et al., 1983

L L

Rajendra & Patel, 1971 Bhatnagar & Davies, 1978

L

Bhatnagar et al., 1983

L L L L L L L L L L

Sahayaraj & Ambrose, 1994 Sahayaraj, 1991 (in Am brose, 1995) Bhatnagar et al., 1983 Yadav, 1980 CIBC , 1974 Am brose, 1985 (in Am brose, 1995) Vennison, 1988 (in Ambrose, 1995) Bhatnagar et al., 1983 Am brose, 1985 (in Am brose, 1995) Lakkundi, 1989 (in Ambrose, 1995)

Pentatomidae b Andrallus spinidens (Fabricius) Cantheconidea (Eocanthecona) (as Canthecona) sp. Cantheconidea (Eocanthecona) furcellata (Wolff) Reduviidae b Acanthaspis pedestris StaÊl Acanthaspis quinquespinosa (Fabricius) b Catamiarus brevipennis (Serville) Coranus sp. Coranus spiniscutis Reuter b Ectomocoris tibialis Distant Ectomocoris xavierei Vennison & Am brose b, c Ectrychotes dispar Reuter b Edocla slateri Distant Endochus inornatus StaÊlb

NA TUR AL ENEM IES O F H . A RMIGER A IN INDIA

TABLE 7.

Continued Reported stage a attacked

Order, family and species b

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495

Endochus parvispinus Distant b Endochus umbrinus Distant b Euagoras plagiatus (Burmeister) b Isyndus heros Fabricius b Lestomerus (as Pirates) af® nis (Serville) Oncocephalus annulipes StaÊl Rhynocoris (as Harpactor) costalis (StaÊl) b

L L L L L L L

Rhynocoris Rhynocoris Rhynocoris Rhynocoris Rhynocoris

L L L L L

Reference

Sycanus indagator StaÊl b Sycanus reclinatus Dohrn

L L

b

L

Lakkundi, 1989 (in Ambrose, 1995) Sahayaraj, 1991 (in Am brose, 1995) Vennison, 1988 (in Ambrose, 1995) Lakkundi, 1989 (in Ambrose, 1995) Am brose, 1985 (in Am brose, 1995) CIBC , 1974 Krishnananda & Satyanarayana, 1984 (in Chari et al., 1992) CIBC , 1974 Am brose, 1985 (in Am brose, 1995) Joseph, 1959 Bhatnagar et al., 1983 Krishnananda & Satyanarayana, 1984 (in Chari et al., 1992) CIBC , 1974 Vennison & Am brose, 1992 (in Am brose, 1995) Kumaraswami & Am brose, 1992

HYM ENOPTERA Eumenidae Delta companiforme esuriens Fabricius Delta conoideus (Gm elin) Delta pyriformis (Fabricius)

L L L

Pawar & Jadhav, 1983 Pawar & Jadhav, 1983 Pawar & Jadhav, 1983

Formicidae Camponotus sp. Camponotus sericeus (Fabricius) d Cataglyphis bicolor (Fabricius) Dorylus labiatus Shuckard Paratrechina longicornis (Latreille) Pheidole sp. Solenopsis geminata (Fabricius) Tapinoma melanocephalum (Fabricius)

L L L L E E L E, L

fuscipes (Fabricius) kumarii Am brose & Livingstone b, c b lapidicola Samuel & Joseph marginatus (Fabricius) b,c scualis

Sycanus versicolor Dohrn

Sphecidae Sphex argentatus Fabricius Vespidae Polistes olivaceus (DeGeer) b Polistes olivaceus (DeGeer) (as P. hebraeus Fabricius) Ropalidia marginata (Lepeletier) Vespa orientalis (Linnaeus) b, c Vespa sincta Vespa tropica haemotodes Bequaert NE UROPTE RA Chrysopidae Apertochrysa sp.b Brinckochrysa (as Chrysopa) scelestes (Banks) Chrysopa sp. Chrysoperla sp. Chrysoperla carnea (Stephens) d b Mallada astur (Banks) Mallada boninensis (Okamoto) b

King, 1986 M anjunath et al., 1976 Khan & Sharma, 1972 M ehto et al., 1986 Romeis et al., 1995 Romeis et al., 1995 Dhandapani et al., 1994 M usthak Ali, personal communication, 1995

L

Bhatnagar et al., 1983

L L

Bhatnagar et al., 1983 Singh et al., 1990

L L L L

Bhatnagar et al., 1983 Bhatnagar et al., 1983 Bhat & Virupakshappa, 1992 Bhatnagar et al., 1983

E E, L E, L E, L E, L E E

Singh et al., 1994b Krishnamoorthy & M ani, 1982 Bhatnagar et al., 1983 Srinivas & Jayraj, 1989 M anjunath et al., 1976 Singh et al., 1994b Singh et al., 1994b

496 TABLE 7.

J . R OM EIS & T . G . SH ANO W ER

Continued

Order, family and species AR AC HNIDA : ARANEA E Araneidae Leucauge tessellata (Thorell) Neoscona theisi (W alckenaer)

Reference

L L

Bhatnagar et al., 1983 Bhatnagar et al., 1983

E, L L

Sigsgaard, 1996 Bhatnagar et al., 1983

Oxyopidae Oxyopes sp. Oxyopes ratnae Tikader

L L

Singh, 1994 Dhulia & Yadav, 1991

Thomisidae Ozyptila reenae Basu Thomisus sp.

L L

Bhatnagar et al., 1983 Bhatnagar et al., 1983

Clubionidae Cheiracanthium inornatum O. P. Cambridge Clubiona sp.

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Reported stage a attacked

E 5 egg; L 5 larvae; ? 5 unknown. These species were either observed preying on H. armigera in the laboratory or the location of the observation (® eld or laboratory) is unknown. c These species names are probably not valid (G. R. Stonedahl and A. Polaszek, personal communication, 1996). d First reported to attack H. peltigera but now recognized as also attacking H. armigera. a b

readily than othe r generali st predator s. The abundan ce of all predator s was m uch lower on pigeonp ea than on sorghu m, althoug h pigeonp ea supporte d higher densitie s of H. arm igera . For exam ple, anthoco rids were found at a peak ` per plant’ densit y of 3.6 on sorghu m and only 0.5 on pigeonp ea. Sim ilar crop-spe ci® c differen ces w ere reporte d for adult coccinel lids (1.6 versu s 0.6), neuropt eran eggs (3.0 versus 0.2) and spider s (1.2 versus 0.7) (Duf® eld, 1995). Sigsgaar d and Esbjerg (1994 ) also found O. tantillu s (M otschuls ky) to be a more effectiv e predato r on sorghu m than on pigeonp ea. The predato r was m ore activ e on reprodu ctiv e than vegetati ve structur es of both plants , and fed on eggs and ® rst instar larva e of H . arm igera . On blac k gram (Vigna mungo (Linnaeus ) Hepper) , Dhuri et al. (1986 ) foun d a signi® cantly highe r density of the coccinel lid C. septe mpunctat a (Linnaeus ) when it w as inter-cro pped w ith sorghu m and a large r number of the predator y w asp P oliste s olivaceu s (DeGeer) (as P. hebraeu s Fabricius ) (H ym enopter a: V espidae ) on plants inter-cr oppe d w ith green gram (V. radiata Linnaeus ) in com pariso n w ith sole crops . M ehto et al. (1986) recorde d a m axim um of 0.3 spider s and 0.7 C. septe mpunctat a per chickpe a plant. Other studie s have noted the abundan ce of predator y spiders , but withou t recordi ng their ef® cacy (Singh & Singh , 1977; Dhulia & Y adav, 1991). Laborato ry studie s of the feedin g potentia l of Clubiona sp. (A carina : Clubionidae) showed that thes e spider s can consu m e a larg e num ber of H. arm igera eggs (59/day) and young larvae (three/day) (ICRISAT, 1982). The usefulne ss of ants, anthoco rids and chrysop ids as egg predator s m ust be w eighte d agains t the possibl e disadva ntag e of them feedin g on parasitiz ed eggs . Egg predatio n m ay be an im portan t mortalit y factor for egg parasito ids becaus e parasitiz ed eggs remain in the ® eld up to thre e tim es longe r than unparasi tize d eggs, and are therefor e expose d to predato rs for a longer period . Krishna moorth y and M ani (1985) observe d the feedin g behavio ur of larvae of B. sceleste s on H. arm igera eggs parasitiz ed by T. chilonis . There was no differen ce in consum ptio n between fresh unparas itize d eggs and 1-day-ol d parasiti zed eggs, but the predato r consu m ed signi® cantly m ore parasitiz ed eggs w hen the eggs were greate r than 3 days old. H owever, it is unclea r if this has an im pact on the com bine d use of these natura l enem ies in the ® eld. There are other examples of m utua l interfer ence among H . arm igera natura l enemies. Ants have been reporte d to rem ove chrysopi d larva e from the plants (Singh et al., 1994b ) and

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chrysop id eggs are parasiti zed by Trichogr am ma sp. (Pawar et al., 1985b ; Kapadia & Puri, 1991). Chrysopi ds are the only H. arm igera predator s to be m ass produce d in India. Life tables have been construc ted unde r laborat ory conditio ns for C. carnea , M . boninen sis, M . astu r and Apertoch rysa sp. (Bakthava tsalam et al., 1994). The highes t net reprodu ctiv e rate was for C. carnea (R 0 5 559). Chrysopid larvae are easy to rear on C . cephalo nica eggs, but they are canniba listic and m ust be separate d (K rishna m oorth y & Nagarkatti, 1981 ; Patel et al., 1988b; Singh et al., 1994c) . Adults are maintaine d on an arti® cial diet. For C . carnea, Singh et al. (1994b ) reporte d the highes t fecundit y (abou t 900 eggs /fem ale) w ith a diet containi ng black gram ¯ our, honey , yeast and suga r in equal proport ions by volu me. A ccordin g to Singh et al. (1994b), eggs of C . carnea can be stored at 10 °C for 15 days w ithou t a reductio n in the proporti on hatchin g; storag e beyon d 30 days signi® cantly reduce d hatching . The age of the eggs (up to 60 h) at the tim e of storag e had no im pact on their ability to hatch . Singh et al. (1994c ) reco m mende d releasin g C. carnea or M . boninen sis at 50 000 ha 2 1 in cotton , tw ice during a season , at an interva l of 15 days. No data on the succes s of such ® eld release s in cotton have been reported . In a 2-yea r study , Venkates an et al. (1994 ) made thre e release s of ® rst instar larvae of B . sceleste s (one head 2 1) on sun¯ ower at 10-day intervals . They reporte d com plete suppres sion of the H. arm igera larval populati on in both years . However, the stud y was carrie d out using sm all plots and the results should be con® rm ed in larger ® eld studies . Dhandapa ni et al. (1992) release d B. sceleste s (50 000 ha 2 1) togethe r w ith T. chilonis (100 000 ha 2 1 ) in cotto n and reporte d a 40% reduction in H . arm igera larva e (T able 4). U nfortuna tely, the impact of the two biocontr ol agents was not separat ed. EX OT IC PARA SITOID S The ® rst introduc tion to India of an exotic natura l enem y to contro l H . arm igera was the egg parasito id T. pretiosu m Riley (H ymenopter a: Trichogra m m atidae ) in 196 4 (Sankaran , 1974). A total of 16 hymenopter an and two diptera n parasitoids of H . arm igera has been introduc ed from the A mericas, A fric a and Europe (T able 8). From the lim ited record s availabl e, it appear s that only one larval parasito id, the tachini d E ucelator ia bryani Sabrosk y (introdu ced as Eucelator ia sp. near arm igera (Coquillett )), is establis hed on H. armigera . The effectiv eness of exotic Trichogr amm a spp. is still in doubt. A m ong the specie s introduc ed into India, T. brasilie nse is the m ost frequent ly released . T his specie s has been success fully used in an inundati ve release progra m me on tom ato (Singh et al., 1994b ; Table 4). Singh et al. (1994a ) reco m mende d weekly release s of T. brasilie nse at 50 000 fem ales ha 2 1 in this crop. T. brasilie nse was not effectiv e in cotton . Between 197 4 and 1976 , Raode o et al. (1978 ) made w eekly release s at a rate of 50 000 parasitoi ds ha 2 1 in cotto n ® elds at differen t location s in M aharash tra. Alm ost six m illion parasito ids were release d in total. T. brasilie nse was recovere d on C . cephalo nica egg card s durin g the cotto n growing season , but no recover y was made in subsequ ent years . Singh and Jalali (1992 ) release d T. brasilie nse on potted cotton plants arti® cially infeste d with H. arm igera eggs . The experi ment was conduct ed outdoor s but it is not clea r if it was in a cotto n ® eld. Even at the highes t release rate of 250 000 parasito ids ha 2 1, few er than 8% of the eggs w ere parasitiz ed by T. brasilie nse, com pare d with at least 70% parasitis m cause d by the indigen ous T. chilonis and T. achaeae . D ivakar and Pawar (1987 ) were not able to recover T. brasilie nse afte r inundati ve release s of betw een 300 000 and 6 m illio n parasitoids/ year betw een 1977 and 198 3 aroun d B angalor e (K arnataka ) in differen t crops . U nfortuna tely, the author s only gave the tota l area covere d by the releas e but did not report the actual num ber of parasitoids released /unit area. Kaker et al. (1990 ) reporte d that no adult parasito ids em erged from H. arm igera eggs parasiti zed in the laborato ry by T. brasilie nse, T. perkinsi G irault and T. m inutum Riley. N o parasitoi ds emerged from parasitiz ed eggs (black egg stage) collecte d in tom ato ® elds afte r releasin g the three species . Balasubra m ania n et al. (1989 ) recorde d up to 62% parasiti sm by T. pretiosu m in chickpe a after m ass releases . This is the only record of high levels of parasitiz ed H . arm igera eggs collecte d

b

a

E 5 egg; El 5 egg±larval; L 5 larval parasitoid. Genus was partially revised by Sabrosky (1981).

USA

L

West Indies Europe

USA

L L

Ichneumonidae Campoletis ¯ avicincta Ashmead Hyposoter didymator (Thunberg)

USA West Indies East Africa USA Europe USA

South America ? South America USA USA & M exico USA West Indies South Africa

Origin

L

El El L L L L

Braconidae Chelonus blackburni Cameron Chelonus insularis Cresson Bracon kirkpatricki (Wilkinson) Cotesia (as Apanteles) marginiventris (Cresson) Cotesia (as Apanteles) kazak (Telenga) Glabromicroplitis (as Microplitis) croceipes (Cresson)

DIPTERA Tachinidae Eucelatoria bryani Sabrosky (introduced as (Eucelatoria sp. near armigera (Coquillett)) b Lespesia archippivora Riley

E E E E E E E E

HYM ENOPTERA Trichogrammatidae Trichogramma brasiliense Ashmead Trichogramma dendrolimi M atsumura Trichogramma perkinsi Girault Trichogramma pretiosum Riley Trichogramma semifumatum (Perkins) Trichogramma minutum Riley Trichogramma exiguum Pinto & Platner Trichogrammatoidea eldanae Viggiani

Host stage parasitized a

Exotic parasitoids introduced into India for control of H. armigera

Order, family and species

TABLE 8.

1969

1969

1981 1986

1976 1982 before 1977 1969 1985 1970

1968 ? 1966 1964 1973 1966 1978 1987?

First year of introduction

Sankaran, 1974

Sankaran & Nagaraja, 1979

Nagarkatti & Singh, 1989 Singh, 1994

Nagarkatti & Singh, 1989 Nagarkatti & Singh, 1989 Divakar & Pawar, 1987 Sankaran, 1974 Jalali et al., 1988b Sankaran, 1974

Sankaran, 1974 Singh & Jalali, 1992 Nagarkatti & Singh, 1989 Sankaran, 1974 Sankaran, 1974 H. Nagaraja, personal communication CIBC, 1979 Anonymous, 1992

Reference

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from chickpe a and was obtaine d with a single release of a relativel y sm all num ber of parasito ids (50 000 ha 2 1 ). This result is questio nable , but if con® rm ed in addition al trials it would be a very signi® cant ® nding . There is no report of perm anen t establis hm ent from any of the exotic Trichogr amm a spp. release d in India . Nagarkatt i and Singh (1989 ) gave thre e possibl e reason s for this: characteristic s inheren t in the exotic species , inter-sp eci® c com petitio n with the indigen ous specie s and unfavou rable m icrocli m atic conditio ns. The reason s for failure have neve r been investig ated . Release s of exotic egg±larval and larval parasito ids have been m ade, but w ith even less succes s than w ith trichogr am m atids. Chelonu s blackbu rni C am eron and Braco n kirkpatr icki (W ilkinson ) (Hym enoptera : B raconida e) were release d in unkno w n numbers in cotton , but no parasiti zed larva e of H. arm igera w ere recovere d from a sm all sample collecte d (Sarkate & R aodeo , 1980). A sim ilar lack of succes s w as recorde d on differen t crops by D ivakar and Paw ar (1987) afte r releasin g both parasitoids from 197 7 to 1983 ; between 700 and 14 200 C. blackbu rni and 1700 ±620 0 B. kirkpatr icki were release d each year. A s m entione d above, the releas e rate in this stud y w as not given . Prasad et al. (1982 ) w ere able to recove r C. blackbu rni from C . cephalo nica egg card s afte r weekly release s over 12 w eeks of a total of 30 000 parasitoi ds in chickpe a ® elds, but no evidenc e of contro l of the H. arm igera populat ion w as given. In cotton , C . blackbu rni has been recover ed at a low leve l durin g mass release usin g C . cephalo nica egg cards (Pawar et al., 1983) and from ® eld-coll ected H. arm igera larvae (Sarkate et al., 1978). No permanen t establis hm ent on H. arm igera is reporte d from any region . C. blackbu rni was consider ed to be a suitable candidat e for the biocontr ol of H . arm igera, prim arily becaus e it is easy to culture on C. cephalo nica (Jai R ao et al., 1979 ; Swam iappa n & B alasubra m anian , 1980 ; K umar & B allal, 1990). Rearin g m ethod s that m inim ize super-pa rasitis m were suggeste d becaus e of the high m ortalit y of parasiti zed eggs and its detrimental effect on progen y longevit y (Varma & M angat, 1984) . B. kirkpatr icki was successf ully reare d on ® nal insta r larvae of the alternati ve host C. cephalo nica (Sarkate & R aodeo , 1980). Cotesia (as A panteles ) marginive ntris (Cresson ) (H ymenopter a: Braconida e) was release d in tom ato ® elds near B angalore , but no subsequ ent recoveri es were reporte d (Rao et al., 1971). Early instar larva e of H . arm igera are the preferre d hosts of C. (as Apanteles ) kazak (Telenga) (Hymenopter a: B raconida e), and C. cephalonica larvae w ere not accepte d (Jalali et al., 1988a). In no-choi ce and choic e tests, Jalali et al. (1988b ) recorde d signi® cantly highe r parasitis m rate s by C . kazak on second instar H. arm igera larvae placed on cotton , tomato and okra than on pigeonp ea and chickpe a. In addition , more progen y w ere produce d by the parasitoi ds on thes e preferre d host plants , thoug h no differen ces in parasito id develop m ent or sex ratio were detected . N o release s have been reported . Hyposote r didy mator (Thunberg ) (Hym enoptera : Ichneu m onidae ) has been reared on larva e of S. litura (Kum ar et al., 1988). Parasitoid s w ere multiplie d and release d in pigeonp ea, but no subsequ ent recoveri es have been reporte d (Yadav , 1990). Sankara n and N agaraj a (1979 ) successf ully reared the tachini d E. bryani on H . armigera. R earing at 25 °C and 75% relativ e hum idity is optimal becaus e of a relativel y short prepupa l and pupal perio d (4.4 and 7.8 days respecti vely ) and a high number of parasitoi d puparia /host larv a (approx . eight) (Shekhara ppa et al., 1992). Super-pa rasitis m has a detrimenta l effec t on the develop ing and adult parasitoi d and should be avoide d in rearin g progra mm es (Shekhara ppa et al., 1988a) . Parasitoid pupari a have been store d at 5 °C for up to 18 days w ithou t affectin g adult em ergenc e (Shekhara ppa et al., 1988b) . Unfortun ately , there w as no evidenc e of perm anen t establis hm ent after release s for ® ve season s at IC RISA T (Andhra Pradesh ) (Sithanantha m, 1987). The reaso n seem ed to be high sum mer tem perature s; in laborato ry studies , the parasitoi d did not surviv e tem perature s abov e 35 °C (Bhatnaga r et al., 1983; Shekhara ppa et al., 1992). Establish ment has been reporte d from Karnatak a (Pawar et al., 1981 ; M ani & Krishna moorthy , 1983; Divakar & Paw ar, 1987), Tam il N adu (Sivaprak asam et al., 1986) and Uttar Pradesh (M ishra et al., 1982 , in N agarkatt i & Singh , 1989). Lespesi a archippi vora Riley (D iptera: Tachinid ae) w as release d near Bangalor e and in Tamil N adu, but no recoveri es have been reporte d (Nagarkatt i & Singh , 1989). O ther exotic larval

500

J . R OM EIS & T . G . SH ANO W ER

parasitoids have either not been m aintaine d in culture after their initia l introduc tion or have not been released .

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C ON CLUSIONS H . arm igera is a devastat ing pest on severa l crop s in India, despite the som etim es high levels of parasiti sm reporte d for som e parasitoi ds. Thoug h the parasito id and predato r lists given in this pape r appea r to be extensiv e, new specie s continu e to be discove red. The taxono m ic statu s of m any specie s m ust be clari® ed as there have been m any misidenti ® cations , as dem onstrate d for the m ost im portan t larval parasito id, C. chloride ae. Record s of specie s belongi ng to the Sarcopha gida e as parasitoi ds of H. arm igera m ay not be correct. This grou p deposi t larva e in w ounds, dam aged tissues , and dead animals and plants (see V an den B erg et al., 1988). N onethele ss, specie s of Sarcopha gida e are listed as parasito ids of Heliothis spp. from the A mericas (K ogan et al., 1989) and H. arm igera from A fric a (Van den Berg et al., 1988). Of greate r im portanc e is the paucit y of inform atio n concern ing the im pact of know n natura l enem ies of H. arm igera populations in the ® eld. The identi® catio n of key natura l enemies and kno w ledge of their effectiv enes s is essentia l for the develop m ent and implem entatio n of m anage m ent strategie s (Bellow s et al., 1992; Room et al., 1990). Life-tabl e studie s of H . arm igera conduct ed by Bilapate and others (B ilapate et al., 1979 , 1988 ; B ilapate , 1981a,c ) repor t generation surviva l rate s of 37±94% . The m ortalit y of the differen t life stage s is highly underes timated becaus e of the desig n of thes e studies (see Fitt, 198 9 for discussi on). In comparison , life-tabl e studie s of H. arm igera conduct ed in East Afric a reveale d generati on surviva l rates of only 7±18% (Van den B erg & C ock, 1993a) . Two H. arm igera life-tabl e studie s from India report generati on surviva l rate s similar to Van den Berg and Cock (1993a) . Tripath i and Singh (1991 ) recorde d generati on surviva l betw een 13 and 28% in larva e expose d to ® eld conditi ons. Only parasiti sm was recorde d in this study ; no impact of predator s (or unkno wn causes ) was given . Nanthago pal and Utham asam y (1989) reporte d generati on surviva l of 2±5% for H . arm igera on cotton . The impact of parasito ids was generally low and m ortalit y from ª m igratio n and unkno wnº causes was high. T his may be indirec t evidenc e for the existenc e of chew ing predator s. Indirec t evidenc e suggest s that natura l enem ies and/or abiotic factors have the greates t im pact on H. arm igera populat ions on sorghu m; reporte d egg densitie s are high , but larval populati ons are often low (Paw ar et al., 1989a) . The populati on-regu latin g m echanis m s that keep H. arm igera at sub-econ omic levels in sorghu m are unkno w n. Understan ding thes e m echanis m s in sorghu m could provid e an insigh t into the reason s why they fail to regulat e H . arm igera populati ons in other crops. To underst and H . arm igera populati on dyna mics, accurat e and complete life-tabl e studie s are needed . T his w ould includ e experi m ents to evaluat e the impact of natura l enemies using exclusi on techniq ues, observat ions of egg and larval cohort s and feedin g trac e m ethods (Kiritan i & Dem pster, 1973 ; Luck et al., 1988 ; Bellow s et al., 1992) . C urrently , in the absenc e of thes e studies , the full im pact of natura l enemies on H. arm igera populati on dyna m ics in India is unknow n. Attempts to suppres s Heliothis spp. populati ons by augmentin g natura l enem y populati ons have been inconsis tent, and econo mic feasibili ty has rarely been dem onstrate d (K ing et al., 1982; K ing & Coleman, 1989). A highly fecund , polypha gous and m obile insec t such as H. arm igera can increas e in number rapidly and dispers e to new host plants . L arge quantiti es of natura l enem ies are neede d at ® eld releas e site s soon afte r eggs or early insta r larva e are observe d. For these reasons , Trichogram ma spp. and, to som e extent , chrysop ids have been the preferre d candida tes for augm entative- release progra m mes. In India, the only successf ul examples of the practica l use of natura l enemies to contro l H . arm igera have utilize d Trichogr amm a spp. In the m ost w ell-docu m ented exam ple, inundati ve release s of T. chilonis on cotton , com bine d with the release of the predato r B. sceleste s, w ere as successf ul in suppres sing H . arm igera as insectic ides, and had a sim ilar cost±bene® t ratio (D handapa ni et al., 1992). Thoug h successf ul, widesprea d

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adoptio n of these strategi es has not occurre d. U ntil an analysi s of the reason s for lack of adoptio n is m ade, the constrai nts to using this pest contro l strateg y will remain unkno wn. The introduc tion of exotic natura l enem ies into India may still be useful , especial ly the strateg y of ® ndin g new host±parasit e associat ions (Pim entel, 1963). It is dif® cult to recom m end a speci® c parasitoid guild , as suggeste d by G reathea d and G irling (1982) , as a candida te specie s for an H . arm igera biologic al contro l progra m me in India , for two reasons . Firstly , as previous ly discuss ed, the im pact of indigen ous parasito ids is unkno wn, so it is not clea r which guild is ineffect ive. Secondly , the parasitoi d faun a for H . arm igera differs betw een crop s and therefor e ` gaps’ in the parasito id guild may be crop-spe ci® c. O ne possibil ity could be the introduc tion of Telenom us egg parasito ids from A frica or Australia . In A frica the w idesprea d, host-spe ci® c T. ullyetti Nixon is abunda nt, w ith a secon d species , T. laevicep s (FoÈ rster), occurrin g in N orth A fric a and Europe . In A ustralia , an addition al (undescr ibed ) specie s of Telenom us is com mon on H . arm igera (A. Polaszek , persona l com municatio n, 1996). Future classica l biologic al contro l progra m m es must be carrie d out carefull y and reporte d in far greate r detail than has previous ly been the case , includi ng an analysi s of reason s in the case of failur e (Stiling, 1993). This is essentia l if these progra mm es are to advanc e beyon d the ` try-it-an d-see ’ stage (Cock, 1986).

A CK NO W LEDG EM EN TS The author s than k the taxono mists at the Natura l History M useum (London ) who checke d the specie s nam es in this review : P. D . H illyard (spiders ), N. P. W yatt (Diptera) , G. R. Stonedahl (Heteropte ra) and A. Polasze k (Interna tional Institut e of Entomology, London ) who checke d all rem aining names w ith the aid of the CA BI A rthropo d Name Index (AN I). The author s would also like to thank H. Nagaraj a for providi ng helpfu l com m ents and H . V an den Berg, J. A. W ightm an, N . J. Arm es, M . A . H oy, A . B. S. King and an anony mous review er for suggestions on earlie r drafts of the m anuscri pt. This pape r was approve d as journa l article no. JA 184 7 by ICRISA T. R EFEREN CES A BRAHAM , C.C. & P RADHAN , S. (1976) Studies on developing races of Trichogramma australicum Girault suitable for high temperature, low humidity conditions. M adras Agricultural Journal 63, 550±556. A CHAN , P.D., M ATHUR , K.C., D HARMAD HIKAR I, P.R. & M ANJUNA TH , T.M. (1968) Parasites of Heliothis spp. in India. Commonwealth Institute of Biological Control, Technical Bulletin 10, 129±149. A M BROSE , D.P. (1995) Reduviids as predators: their role in biological control, in Biological Control of Social Forest and Plantation Crops Insects (A NANT HAKRISHNA N , T.N., Ed.) Oxford & IBH, New Delhi, pp. 153±170. A NONYMO US (1992) Annual Report, All Indian Coordinated Research Project on Biological Control of Crop Pests and Weeds. Biological Control Centre, National Centre for Integrated Pest M anagement, technical document no. 39, Bangalore, India (limited distribution). B AKT HAVATSALAM , N., S INGH , S.P., P USHPAL ATHA , N.A. & B HUMMAN NAVA R , B.S. (1994) Life tables of four species of chrysopids (Neuroptera: Chrysopidae). Journal of Entomological Research 18, 357±360. B ALASUBRAMANIAN , S., A RORA , R.S. & P AW AR , A.D . (1989) Biological control of Heliothis armigera (Hubn.) using Trichogramma pretiosum Riley and nuclear polyhedrosis virus in Sriganganagar district of Rajasthan. Plant Protection Bulletin, India 41, 1±3. B ASARKA R , C.D. & N IKAM , P.K . (1982) Longevity, fecundity and sex-ratio of Campoletis chlorideae Uchida (Hymenoptera: Ichneumonidae). Indian Journal of Parasitology 6, 125±126. B ELLOWS , T.S., V AN D RIESCHE , R.G. & E L KINTON , J.S. (1992) Life-table construction and analysis in the evaluation of natural enemies. Annual Review of Entomology 37, 587±614. B HAT , N.S. & V IRUPAK SHAPPA , K. (1992) Present status of Heliothis on sun¯ ower and strategies for its management in India, in Helicoverpa M anagement: Current Status and Future Strategies. Proceedings of the First National Workshop, 30±31 August 1990 (S ACHAN , J.N . Ed.) Directorate of Pulses Research, Kanpur, pp. 115±120. B HAT NAGAR , V.S. & D AVIES , J.C. (1978) Factors affecting populations of gram pod borer, Heliothis armigera (HuÈ bner) (Lepidoptera: Noctuidae) in the period 1974±77 at Patancheru (Andhra Pradesh). Bulletin of Entomology 19, 52±64. B HAT NAGAR , V.S. & D AVIE S, J.C. (1981) Pest management in intercrop subsistence farming, in International Workshop on Intercropping, International Crops Research Institute for the Semi-arid Tropics, Patancheru, Andhra Pradesh, pp. 249±257.

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