Research Status and Scope for Biological Control of Sucking Pests in India: Case Study of Thrips

J Bio/. Control. 21(Speciai Issue): 1-19,2007

Research status and scope for biological control of sucking pests in India: Case study of thrips

S. SITHANANTHAM~ R. VARATHARAJANl, CHANDISH R. BALLAL2 and P. N. GANGA VISALAKSHY3 Sun Agro Biotech Research Centre, Parur, Chennai - 600116, Tamil Nadu, India E-mail: sithanantham@}yahoo.com

ABSTRACT: Thrips are an important group of sucking insects causing substantial yicld losses in several tropical crops, as direct pests and/or as virus ve(:tors. In Indi:l, thrips arc signil'icant pests on vegetables (e.g., chillies, onion), legumes (e.g., cowpeas, ground nuts), cereals (e.g., rice), spices (e.g., cardamom, turmeric), poly-house crops (e.g., rose) and 1>lantation crops (e.g., tea). The emerging inter est at national level in organic farming and export agriculture calls for development of appropriate and wide range of eco-friendly ~lnd biological products for thrips management. Entomopathogens (like Verticilli/ll/l iecmri) have shown promise for augmentative biologic:11 control (of Scirtofflrips dorsalis), ~lIld there is scope for identifying more adapted and virulent strains of the entomopathogens, besides devel oping improved formulations for extending their shell'- and field life. I)redators (like Orill,I') have also shown some potential, in natural conditions, but research has to be intensified on aspects like their mass production technology, field attack rate, predation potential, adaptation to physical and chemicul stresses, besides biodiversity, tri-trophic interactions and behavioural and chemical ecology. Parasitoids (like CerallislIs) are of limited potential as biological control agents and emphasis is needed on their ill situ conservation strategies, besides cost-effective mass rearing and release systems. Scope exists for strengthening multi-disciplinary approach and inter-institutional collaboration, possibly through work ing group and network strategies to establish a biological control based thrips management research experts' consortium so as to cater to scientific backstopping and complimentarity in relevant expertise. There is need to focus on research and development (R&O) with public-private partnerships, for widen ing the range and refining the technology options as well as the integration of different biological control agents with other pest control technologies, besides linking them to the crop munagement practices so as to evolve holistic Integrated Pest Management (lPJ\.1) strategies.

KEY WORDS: Biological control. natural enemies, thrips

INTRODUCTION caused by destruction of the native natural enemies of pests. In addition, there is emerging support at national In the recent decades in India, there is increasing level for promoting export oriented agriculture as well as interest in adopting more of eco-friendly control rnethods organic fanning as means of capturing niche markets as part of the Integrated Pest Management (1 PM) and thus enhance the incomes and livelihood of the rural approach. This is due to the build-up of awareness that and farming communities in India. These market-linked continued resort to the lise of synthetic pesticides is farming systems call for adoption of "green" practices ecologically unsustainable, because of the associated for maximising compliance to the regulations in export problems of pesticide resistance and resurgence of pests crops. As such, biological control is being more sought

I. Department of Life Sciences, Manipur University, Imphal - 795 003, Manipur, India 2, Project Directorate of Biological Control, Bellary Road, Bangalore - 560 024, Karnataka. India 3. Indian Institute of Horticultural Research, Hessaraghatta Farm P.O., Bangalorc. Karnataka. India SITIIA NA NTHA M ('/ 11/,

after as the major means of ecologically friendly sweet pepper (Kumar, 1995). In onion, SI-inivas et. al.. management of insect pests on our agricultural crop (2004) I·eported that Thrips tabaci could cause yield loss ecosystems, especially those of the high value crops. in the range of46-87 percent, while Mohite et at. (1992) estimated the loss to be around 50 per cent in that crop, In the recent decades, there has also been a In paddy, Hap/olorhrips ganglballer; has been known significant increase in the research and developmcnt to cause 1.6 - 8. 1% loss (Nair, 1986; Rao et al., 1997), (R&D) initiatives to promote the dcvelopment and whereas in green gram Thrips palmi caused about 40 per adoption of biological control tcchnologies in It~dia. cent loss (Sreekanth e/ ai., 2(02). Nevertheless, the target pests, which have received emphasis are more of chcwing pests, especially Nevertheless, there is need to develop baseline lepidoptcra, compared to sucking insect pests. It is data on crop losses caused by thrips in nationally gratifying that the present symposium is focussed on important target Cl·OpS across a network of benchmark the latter group. While hemipteran pests are the more sites, representing the agro-eco-zones of their common target pests among the slicking insects, thrips cultivation. This would lay the foundation for developing offer special challenges and opportunities for biological bio-control strategies appropriate over space and time control, due to their distinct feeding habit and often besides also providing convincing loss data fOI· policy concealed habitat. Of course, thrips are also a significant makers to j lIstify funding the research for their control. production constraint to several agriculturally important 1.2 EtTect of weather factors on thrips incidence including high value and export crops in the tropics. They are known to cause significant crop yield losses The importance of weather factors on thrips both as direct pests due to impaired crop growth and population has been studied only to a limited extent. A also as vectors of plant pathogens of crops positive correlation of S. dorsalis incidence has been (Allanthakrishnan, 1984). found with maximum temperature and negative association with rainfall, minimum ternperature, mean This paper deals with thrips as case study, relative humidity and mean vapoul· pressure in chilli reviewing the current research status and future priority ecosystem (Panickar and Patel, 2001; Varadarasan and research thrusts for improved use of the biological Veeravcl, 1995). In cotton, population control agents, towards their sustainable management, Thrips tahaci levels showed significant positive correlation with wind especially the key pest species of the high value crops in India. speed, while in pigeon pea, there was significant negative correlation between Megalurothrip population and mean 1. Occurrence and economic importance of temperature (Panickar and Patel 200 I ). There are studies thrips in agro-ecosystems in which season, as such has an overall influence on the effects of individual weather factors. For instance, the 1.1. Extent of losses caused in ta.-get crops incidence level of S. dorsalis on chill i has been reported to be grater during the dry season, when the temperaturc Ananthahishnan (1984) has provided a sOllnd is 30°C and above, with no rainfall (Lingeri et al., 199X: analysis of the thrips species diversity associated with Manjunath ef al., 200 I a). In onion, T. {abaci showed several crop ecosystems in India and elsewhere (Table higher incidence level (78%) in Rabi season crops in I). The author has drawn attention to the role of the nOI1- Maharashtra (Srinivas and Lawande, 2004). The target host plants in the population dynamics of thrips interaction of phenology with weather factors needs in the target crops. The available estimates of crop losses elucidation. For instance, in groundnut, S. dorsalis due to thrips include about 45 - 47 per cent loss in infestation was found to be greater where the drought cardamom due to Sciothrips cardal11ol11i (Varadarasan, stress for the crop was less. Thrips incidence was found 1995), while in tea, Scir{oti1rips bispillosis has been to subsequently reverse and with the ageing of crop, found to cause about I 1-17 per cent loss (Selvasundaram they became more abundant at the wettcr end of thc ef al.. 2004). Kandasamy e/ al. (1990) estimated that gradient. Incidence of S. dorsalis was highest during about 30 - 50 per cent loss in chillies was caused by March-April, with the emergcnce orncv\,' llush (Wheatly Scirtothrips dorsalis. Quantitative yield loss due to S. el a/.. 1989). It may be pointed out that while these few dorsa/is has also been fOLlnd to be more than 90 per cent studies have shown the potential role of climatic and on chilli pepper, compared to 11- 32 per cent in sweet host phenological factors, there is nced for more holistic I pepper, while quality loss of 88-92 Yc, was observed in study of the ecosystem interactions, so as to establ ish a

2 Research st

Table 1. Examples ofthrips and their host plants in India

Thrips species (Common name) Host Plant Anaphothrips sudanensis Trybol11 Cereal crop + Ayyaria chaetophora Kan1Y Pulses and Oilseeds ++ Caliothrips indiclls (Bagnall) Pulse crops ++ Frankliniella schliltzei (Trybom) Highly polyphagous pest of economically important plants and transmits tospo virus Megalurothrips distalis Karny Pulse crops ++ Canchaetothrips indicus (Bangnall) Turmeric and Banana + Retithrips syriacus (Mayet) Rose, CastOl', Cassava + Cotton, Grapevine, Groundnut Rhipiphorothrips cruentatus Hood (Grapevine thrips) Grapevine, Rose + Sciothripscardamomi Ramak(Cardamom thrips) Major pest of cardamom Scirtothrips bispinosus Bagnall Tea and Coffee ++ Scirtothrips dorsalis Hood (Chilli thrips) Polyphagous and important pest of crops Selenothrips rubrocinctus Giard Cashew, Cocoa + Stenchaetothrips biformis (Bagnall) (Paddy thrips) Paddy seedlings ++ Thrips hawaiiensis (Margan) Polyphagous flower thrips ++ Thrips tabaci Lindeman (Onion thrips) Important polyphagous pest of crops and vector of tospo virus

+ Indicates minor pest status; ++ Indicates seasonal pest status with appreciable density sound ecological basis for developing biological control parasitoids of thrips recorded in India (Ananthakrishnan, strategies for thrips, This is in"lportant since very often 1984) is fumished below. crop entomologists tend to focus on the target pest/ crop in isolation from the other associated attributes of 2.2.lrnpact and scope for conservation the target ecosystem, which can equally affect the There is very limited information on this aspect potential impact of biological control. also in India. CcranisLis maculatLls has been found to lay its eggs inside the body of larvae of 2. Parasiotids as biological control agents Rhipiphorothrips crllentatus. The females of this 2.1 Natural occurrence of parasitoid species eulophid are known to search for second and third instar larvae and pierce their abdomen with their ovipositor to The information on paras ito ids natural enem ies of lay their eggs inside, leading to subsequent death of the thrips available in India is rather limited. The list of host (Rahman and Bharadwaj, 1937). Parasitism of T.

Parasitoid species Thrips species Crop Ceranisus sp. Thrips tabaci Onion Ceranisus maculaflls Rhipiphorothrips crucnlatlls Grape Alegaphragma longiciliatul11 Frankliniella /ilivora Grape RhipipllOrotlirips erllel1lalllS, Thripastichus gel/filei (Del Guercio) Grape GYl1aiko!lirips llzeli Thripobius scm iluteus Pallc!Jaetothrips illdiells Turmeric

3 SITlIi\N/\NTllr\M ('/ al.

rabun" on onion by ('cranislts sp. ranged from 2 to 180/" Cara}'ol1ocori.... · indiells M uraleedharan, which usually during the season, but the incidence of the parasitoid lived" in the inflorescence of Cassia JIlarginata in South was low (Saxena, 1981). Ananthakrishnan and India and fed on Haplothrips ganglhaueri Schmutz and Swaminalhan (1977) reported the parasitisation ofsecond Frankliniella schultzei (Tryb.), besides M. Illoraguesi, instar larval stages of the gall forming thrips, which lives in the galls of20 species of Thy san optera on 5ic/wcdollirips oricntalis by 7£'lrastichus thripiphollllS as many host plants and feeds especially on and the parasitism kvcls were as high as 20 per cent. GYllaiko/hrips hellgalcnsis Ananthakrishnan; also X},/oeoris clanls (Dist.), which lives in leaf litter in 2.3 Further thrust on insect parasitoids and s~llthern India and preys on litter insects including nematode parnsitcs of thrips Dcxio{I! rips Illadrascns is (A n an th ak ris h n an) (Malaeolhrips l11adrasensis) and Apelallfloti1rips !\ Ithough parasitoids of thrips seem to have limited indieus (Ananthakrishnan) (M. indicus); and scope li.>r augmentative biological cOl1trol, the potential Scoloposcelis paralle/us (Motsch.) which was found tl)f cost effective mass rearing of the parasitoids and on decaying bark of Erythrina spp. in August-September planting of nectar-sources for adult feeding could be and preyed on fungus thrips (Ecacanthotlirips studied. sangllinells 8agn.). In India, anthocorids have been recorded as potential biological control agents of different 3. Predators as biological control agents species of thrips (Table 2). The majority of anthocorid 3.1. Natural occurrence of predators research is records on different thrips pests, while very limited work has been done on production or field There are several predators reported to provide evaluation of anthocorid predators in thrips biological natural control of thrips in crop ecosystems in India. For control in various crop ecosystems. Systematic studies instance, tea thrips arc reported to be predated by the are lacking on the seasonal occurrence of the different anthocorid - Orills sp., and predatory thrips like potential anthocorid predators in our country. ('o/c(}llirips intermedills and A4ymarothrips garuda Information is lacking on the extent of control of thrips (Murakedharan, 1(95). Singh (1993) reported feeding of exerted by the natural populations of anthocorid Cara,l'ollo('oris iudiclls and GrillS maxidelltex on predators in the different agro-ecosystems. This Afega/lIro(/lrips dis/aU,·, an anthophilolls pest of legume information is necessary to identify the potential crops. Mirid bugs, larvae of syrphids, lacewings, anthocorids which do a good job in nature and which coccinellids, predatory mites, spiders, sphecid wasps and need to be conserved. pseudoscorpion are reported among common predators of thrips on various crop plants (Ananthakrishnan, 3.2. Host range and seasonal incidence 1984; Varatharajan and James Keisa, 2000). The predatory inquiline, Andropthripsjlavipes Schmutz, was recorded Laboratory studies indicated that Grius max:identex in galls caused by Arrhenothrips ramakrishnae Hood Ghauri and Carayoflocoris indieus Muraleedharan had on leaves of Mimusops elengi and also in galls caused a greater preference for Scirtothrips dorsa/i.<; Hood over by Schedothrips orientalis (Ananthakrishnan), the other species offered, possibly because of their Gynaikothripsjlaviantennatus Moult and Brachythrips comparatively sma1ler size. The bugs appeared to dalllahasta Ramakrishna on various plants. The recognize their prey only by tOLlch (Kumar and predators feed on the eggs, first and second instar Ananthakrishnan, 1984). Fie1d studies on the seasonal nymphs and to a very limited extent on pupae. The occurrence of anthocorid predators were conducted by anthocorid, Alontandolliola moraguesi (Put.) was also Kumar and Ananthakrishnan (1984). C. indicus appeared found preying on G jlavianlennatus and S. orienta lis, on Cassia marginata and mango after these began to but cross prt:dation on A. jlavipes within their galls was flower and populations built lip as thrips populations observed (Ananthakrishnan and Varadarasan, 1977). increased. Peak numbers of the predator were recorded Natural populations of these predators have been on mango in March and on Cassia in july. Grill'<; successful in maintaining the pest populations at low maxidentex was present from January. Scymnus nubilus levels (Muraleedharan and Ananthakrishnan, 1978; Muls., Laius externenotatus Pic, Orius albidipennis Ananthakrishnan and Sureshkumar, 1985). The important (Reut.), Chrysopa sp. and Aeolothrips collad\' Priesner anthocorids liste' as potential predators of thrips by were found preying on Thrips {abaci Lind on onion. Muraleedharar nd Ananthakrishnan (1978) are The predators consumed 23-96 thrips larvae per day, but

4 Rt:s'::'lr<.:h status and scope for biollliCi~al '''l1tml "I' thnps in India

their incidence was very low in comparison with that of Techniques to muss rear Orills spp. were not theirprey (Saxena, 1981). Some control ofH. gang/halteri available in India till reecntly. At the Project Directorate on rice was achieved by D. maxidelllex which could feed of Biological Control, Bangalore, methods have now been on the larvae and adults (Ananthakrishnan and standardised to multiply Grills talltil/us on different host Thangavelu, 1976). Population fluctuations of three eggs. Earlier studies had indicatcd that the progcny species of anthophilous thrips such as Mega/lfrothrips production by Orius muxidel1tcx when reared on dis/a lis, Frallk/ iniel/a schu/tzei and Haplolilrips sorghum midge was 35.l per female and 23.6 per female ganglballeri were studied in the flowers of Cliricidia when reared on thrips. There arc problems associated sepiul1/ (= G macula/a) in relation to the numerical with continuolls multiplication of host insects like thrips response of their predator, Drills mil/lltlls L. It was found and midges. Hence other alternate laboratory host eggs that O. minutlls is an effective predator and that predation were tried. O. tail/iI/liS could be continuously mUltiplied is density-dependent (Viswanathan and for 12 generations on UV irradiated C cep/w/ol1icu eggs. Ananthakrishnan, 1974). However, the progeny production was very low, the mean value being 3.1 per female. The UV-irradiated eggs of 3.3. Impact and scope for conservation Silo/roga cerea/ella was also tried. It has now been fOllnd that O. talllil/us eould be reared more efficiently On sesame, Oriw,· maxidentcx red on Thrips palmi on .\'. cerea/ella eggs than on C. ccp/wlollic{[ eggs (Fig Karny on the young foliage, migmting later to prey 011 I ). From a sma \I number of licld- collected fcm

3.4.1 Rearing of anthocorids It has 110\V been realised that anthocorids are effective predators and playa useful role in the natural In India, very few attempts have been made to rem' control of many insect pests in the differcnt pat'ts ot! the the anthocorid predators. M ukheljee et al. (1971) tried a world (Table 3). Techniques have been evolved in other synthetic diet for rearingXjlavipes (Reut.). Mass rearing countries to mass rcar anthocorid pl'edators and release methods have been standardised for four potential them in the field or glass hOllses for management of anthocorid predators, Cardiastethus exigllus Poppius several pests, especially tlll'ips. (Ballal ef at., 2003a), Blaptostelhlls pallescen.)· Poppius (Balla! el ul., 2003b) and Xv/ocorisjlavipcs (Reuter) and The following are projected as future thrust areas DrillS taHtil/us Motschulsky (Chandish R.Ballal, for utilising antrocorid ~)I"cdators in biological control of unpublished). thrips:

5 C/l Table 2. Known and potential predators ofthrips in India =i ::I: > Predators Host plant Z Target thrips Source > Z Orills sp. Groundnut -l Thrips Singheta/.(I991) ::I: > ills aibidipellllis (Reut.) Onion ~ Thrips tabaci Saxena(I977)and(1981) ~ Orills b(filarills Ghauri Polyphagous Thrips/lal'lIS and Veer (1984) Thrips hawaiiel1sis

Orills maxidelltex Ghauri Sesame, Thrips palmi Kumar and Ananthakrishnan (1984) Croton sparsifloms Morong, Frank/iniella scllllltzei Ananthakrishnan and ThangaveIu ( 1976) PaniClll11maxil1ll1111 .Iaeg. Thrips palmi Anaphothrips slldanellsis Caliothrips gramillicola Scirtothrips dorsalis

Prosopis spicigera L., rice Hap/othrips ganglballeri I

Orills maxidelltex Ghauri and Onion and garlic Thrips tabaci Muraleedharan and Ananthakrishnan (1978) 0. tamil/lis Motsch. Chilli. tea and other plants, rice Scirtothrips dorsalis. Baliofhrips biformis 0" Groundnut, sesbania and bajra Ca!iothrips illdiclls Chrysanthemum, dahlia and Microcepha/othrips abdomina/is maJ"ygoldVarioLls plants Hap/othrips gang/balleri 0. inSidioslts. o.mC/xidellfcx. Onion Thrips tabaci Ae%{hrips ('ol/aris. SCylllllllS III/hi/liS. Laius cxlemCllofatllS. Chl1wpa sp. and C. oreste~

OrillS millllllls (L.) G/iricidia sepilllll (Jacq.) Megalllrofhrips distalis Viswanathan and Ananthakrislman (1974) (= G maclI/ata) Frallklilliella scllllltzei Haplofhrips gal/g/baueri Caramllocoris illdiclIs Cassia lIIargillata Roxb. and mango Hap/othrips gang/balleri Muraleedharan and Ananthakrishnan (1978) Muraleedharan Fral1klil/iel/a sclllllt:::ei and KLImaI' and Ananthakrishnan ( 1984)

,\Jomal/doniv/a moragllesi (Put.) DifTerent plants Gall makers, G) '/Ia ikorh rips Ananthakrishnan and Varadarasan (1977) j7al'iantel/l1atus Moult, Schedothl'ljJs oriel1falis (Ananthakrishnan) G.maikorf7rips benga/ellsis Ananthakrishnan MuraIeedharan and Ananthakrishnan (1978)

- ;N ~ !>:"" ri ;;;r '" MOlltalldonio/a moraguesi (Put.) Blac k pepper Leptothrips karnyi ~ Muraleedharan and Ananthakrishnan (1978) iii

'":l Xylocoris clarus Not mentioned Thrips on litter material Muraleedharan and Ananthakrishnan (1978) C. V> (l o Scoloposcelis para lIe Ius Not mentioned Thrips infesting dead and Muraleedharan and Ananthakrishnan (1978) "0 decaying plant pal1S (1) ~' Grills spp. Egg plant Thrips palmi Nagai (1991) Cl'o 0" (J:; Grills indicLis Cajanus cajan (Flowers) Mega!urothrips lligricol71is Rajasekhara and Chattelji (1970) (i' (nymphs and adults) ~ (l o :::; Holothrips anacardU Hood Rose Rhipiphorothrips cruentalus Dhaliwal (1975) ... Hood (Nymphs) £...... ,o I ,.. ~ 'Sl :::;

e:p -..J

Table 3. Field releases of anthocorid predators for thrips biological control in other countries

Anthocorid Host plant/ material Host insect Place Source MOlltandoniola l1Ioragliesi (Put.) Ficus ret usa GYl1aikothrips jico/'UI7l (Marchal) BCl111Uda Groves (1974)

Drills sp. Cucumber Franklil1iella occidentalis Pergande Gem1any Buhl and Bassler (1992)

Orills il1sidioslls Say Chrysanthemum Frankliniel/a occidentalis Netherlands Fransen and Tolsma (1992) Ornamentals Frankliniella occidcnfalis Sweden Sorensson and Nedstam(l993)

Orills lael'igatlls (Fieber) Strawberry Frallkliniella occidentalis France Villevieille and Millot( 1991)

sweet pepper Frankliniella accidenlalis UK Chambers et al. (1993)

Trottin Caudal et al. (1991) I Drills majl/sell/lls (Reuter) Cucumber Franklilliella occidentalis France Chrysanthemum Franklinie//a occide/1ta/is UK Buxton and Finlay (1993) SITIlANANTIIAM ('/ at.

• Methods should be standardised for mass of the first and second instar larvae of Chrysoperla production of thrips, which is an essential step carnea at 3 per plant, resulted in significant reduction of for conducting evaluation studies using the pest (Wadaskar et al., 2004). anthocorid predators 4. Entomopathogens as biological control • Search for potential anthocorids for releases agents for thrips against thrips 4.1 Natural occurrence of pathogens and their • Taxonomy of anthocorids to be strengthened incidence level • Studies on the interaction between thrips and anthocorids in different crop ecosystems during The pathogens reported as occurring on thrips or different seasons promising for their control are as below: • Mass rearing technologies to be standardised for i. Protozoa unthocorid predators and available technologies to be disseminated to commercial insectaries A microsporidian parasite - Mrazekia sp. has been found infecting the larval forms of Scirtothrips • Compatibility studies between anthocorid oligochaetus (Raizada, 1976). predators and other potential bio-agents (insect pathogens and parasitoids). ii. Entomopathogenic fungi • Availabe anthocorid predators in culture to be Certain species of Cephalosporium and evaluated against thrips Aspergillus, Cladm:poriuln clac/osporioides and 3.6 Other predators for thrips biological control Entomophthora thripidillll1 are also reported to be effective against thrips species (Ananthakrishnan, 1984). An experiment carried out on the effectiveness of A list of the mycopathogens recorded in India is controlling thrips in C. annum indicated that releasing furnished in Table 4.

500

400

300

200

100

o Q 0 Q :.:> Q ....l ....l ....l ....l S :3 ....l > > x >< X > >= o Orills on Corcyra • Orills on Sitotro!:a

Fig. 1. Ori~/s tall til/us r~ared for .12 generations on Corcyra cephalollica and Sitotrogtl ceretl/ella (L(' Jab generation; Fe: Field collected anthocorids; Chandish R. Ballal, unpublished)

8 Research status and scope for biological contt-ol of thrips in India

Table4. List of my co-pathogens known as natural enemies of thrips in India

M yco-pat ho gens Thrips Cladosporium cladosporioides Scirtothrips dorsal is Trichothecium roseum Thrips tabaci Entomophthora thripidiul11 Thrips tabaci Cephalosporium sp_ Thrips tabaci Aspergillus sp. Thrips tabaci, Frankliniella iI/tonia, Anaplio/hrips obscurus, Paecilomycesfianosoroseus Thrips tabaci Hirsutella thompsonii Thrips in general Verticillium sp. Frankliniella occidelltalis iii. Nematode parasite different oils and stickers have been tested (Tables 5 and 6) Flower inhabiting thrips such as Frankliniella schultzei and Microcephalothrips abdominali.,,· 5. Progress and success in thrips biological occurring on sunflower were found infected by the control elsewhere nematode, Anguillulina aptini (Varatharajan, 1985). 5.1 Promising research results on biological 4.2 Extent of natural control/impact control of thrips

The natural incidence of entomopathogenic fungi In countries like France, UK, Netherlands and at different phases in the life cycle of T inconsequences Germany, anthocorid predators have been multiplied and was determined in sugar maple stands in Vennont The released in the green houses and fields for the most commonly isolated species were Beauveria ntanagement of thrips. Amongst the different bassiana, Paecilomysis farinosus, A1etarhizium anthocorids, Orius spp. appears to be the most promising. anisopliae, V. lecanii, V. fusisporum and Hirsutella sp. O. sauteri is known to be an important predator of thrips, The incidence of the entomopathogen V. lecal/ii on T spider mites, aphids and eggs of lepidopterous insects inconsequens was found to vary with the microhabitat in fields and orchards in Japan, China, Korea and Russian of the host. The highest incidence of (I 1.9 %) was Far East and has been shown to be effective in recorded from larvae followed by adults (5.9 %), while suppressing. Thrips palmi in egg plants (Yano and Van only I .9 % was recorded for thri ps collected from under Lenteren, 1996). In Switzerland, Orius majuscillus could storey as well as from upper canopy (Brownbridge et al., reduce populations of thrips on sweet pepper and 1999). cucumber (Fischer et at., i 992)_ Application of the entomopathogenic fungus V. Artificial diets have been developed and evaluated lecal/ii caused significant reduction of the population for some anthocorids. 0_ sautcri cou ld be reared on an of western flower thrips, Frankliniella occidcntalis and arti ficial diet (Zhou and Wang, 1989). Castane and Zalom a visible reduction in leaf damage on bush beans, ( 1994) found that an arti ficial ovipositional medium made Phaseo/us vulgaris cv. marona (Meyer et al., 2002) and of carrageenan salt of potassium chloride and covered thrips on cucumber (Gillespi, 1986). with paratTin wax was suitable tor rearing 0. insidioslts. 4.3 Recent research advances at I1HR The anthocorid species, which have been lIHR has isolated an efficient strain of V fecal/ii C0111mon Iy used for fie ld re leases. are A IIfhocoris from T palmi with higher infection potential on S. IIcl1loralis, and Orill.~ spp. Anthocol-ids are now being dorsalis. Et1icacy of the isolate and its compatibility with commercially produced in several countries. In Ontario, SfTIIANANTHAM ef al.

Table S. Efficacy of Verticillillllliecallii against different instars of Scirtothrips dorsalis*

Treatments Percent cumulative mortality (hours after inoculation) Nymphs Adult 24 hours 48 hours 72 hours 24 hours 48 hours 72 hours

3x I 04 (conidia /ml) 4.0(9.9) 8.0(IS.9) 10.0(18.9) 5.0(10.0) 8.0( IS.9) 12.0(21.00) 3x I 0' (conidia/ml) 8.0( IS.9) 10.0(18.9) 12.5{23.6) 10.0(IS.9) 12.0(20.5) 14.0(23.0) 3x 10('(conidia/ml) 8.0(IS.9) 14.0(22.1 ) 20.0(29.3) 18.0(22.1) 20.0(26.6) 32.0(35.0) 3x I 0 7 (conidia/ml) 14.0(22.1) 24.0(29.6) 40.0(43.3) 30.0(29.5) 32.0(34.6) 48.0(44.1)

3x I Os (conidia Iml) 16.0(23.7) 26.0(30.9) S7.S{S2.24) 30.0(28.9) 349(35.9) 52.0(46.5)

3x 1O'I(conidia/ml) 24.0(28.3) 46.0(43.0) 72.S(62.12) 4S.0(37.3) 52.0(41.8) 82.0(65.7)

Control 09(4.05) 0.0(4.05) 2.5(5.06) 0.0(4.05) 0.0(4.05) 2.5(7.0) CV% 29.4 14.5 20.1 23.2 18.3 18.7

CDatO.05 6.S 4.5 7.0 6.3 6.1 8.3 * Source: Ganga Visalakshi (unpublished), IIHR study.

Table 6. Compatibility of different vegetable oils and stickers on the growth ofVerticilliulIl lecallii

Treatment Colony diameter in 'cm' Per cent growth ofmyce\ia Rate of growth in (cumulative) 15 1h day over control (cumulative) 'cm'/perday(10-15Ih day)

Sun flower oil 2.43" - 6.S4 0.061

Groundnut oil 1.2(}1 - 53.85 0.020 Coconut oil 3.63h 39.61 0.101

Gingilioil 1.27d - 51.15 0.022

Castor oil 3.47~ 33.46 0.096

Neemoil 4.47u 71.92 0.129

Pongamia oil 2.43" -6.54 0.061

Laboline 2.27" - 12.69 0.056

Triton XIOO 2.23~ - 14.23 0.054

Control 2.60" 0.067 CD=O.OI 0042

* Source: Ganga Visalakshi et al. (unpublished), IIHR study. the cost of production of 0. insidiosus was 0.03 dollar individuals of 0. laevigalus per plant could control per bug and up to 100,000 bugs could be reared per week Frankliniella occidentalis Pergande on pepper and 200 to 600 bugs could be reared in one zip - lock (Chambers et al., 1993). In Germany, good results were plastic bag (Sc1~ . idt, 1994). I n UK, releases of 1 or 2 achieved with 2 releases of Orius at fortnight intervals

10 Research status and scope for biological control of thrips in India

Table 7. Differential pathogenicity of entomopathogenic fungi strains on Megalllrotllrips sj()stetiti-ICI PE, Kenya*

Fungal species Strain (Yo germination Beauveria bassiana IClPE53 94.50 IClPE59 100.00 ICIPE78 90.30 ICIPE82 100.00 IClPE83 97.00 TP-GHA 68.30

Metarhizium anisopliae ICIPE 18 100.00 ICIPE20 72.50 ICIPE30 99.50 ICIPE60 94.30 ICIPE62 100.00

* Source: Ekesi et al. ( \998)

2 (0.5-1 insectlm ) against F. occidentalis in cucumbers bioassays and pot culture studies. Native strains of (Buhl and Bassler, 1992). In France, the efficiency of Orius Metarhizium with better growth and sporulation majusculus for the control of F occidentalis on attributes were tested for their'adaptation to a regime of cucumbers was studied in greenhouses and the predator temperatures and crop varieties and the better performing was shown to have great potential (Trottin Caudal et. ones were selected fOl- further testing (Table 7). al., 1991). The research at IC1PE focussed on choice of highly Drius majusculus was introduced for the control adapted native strains and also further choice among of F. occidentalis on chrysanthemums in a greenhouse them for strains that are equally effective for biological in the UK and appeared to reduce thrips numbers for at control of the cowpea flower thrips Mega/urothrips least the first two plantings. In Netherlands, Orius sjostedti, the western flower thrips, Frankliniella insidiosus was released on chrysanthemums for the recidentallis, as well as the onion thrips, Thrips tabaci control of F. occidentalis in greenhouses and pest (Ekesi et al., 1998 and 1999; Maniania et ai., 2001 and numbers were reduced to a great extent (Fransen et at., 2003). 1993). In Sweden, the predators Amblyseius cucumeris (= Neoseiulus cucumeris) and Orius insidiosus were very The field evaluation of Metarhizium for the control effective when they were released together on ornamental of thrips was invariably compared with synthetic plants (Saintpaulia impatiens, Gerbera spp. and insecticides, and competitiveness and cost effectiveness Brachyscome multifida) infested with F occidentalis in of the Metarhiziwn product could be clearly established. greenhouses (Sorensson and Nedstam, 1993). Orills Biweekly sprays of M. allisopliae were found to provide laevigatus was also observed to be a potential predator significant reduction in thrips infestation and in damage for the control of F. occidentalis on strawberries in ratings of onion thrips on par with biweekly sprays of greenhouses in France (Villeviel1e and M ilIot, 1991). demethoate in three field trials (Table 8, 9 and 10). Of course, significant increase in yield over control treatment 5.2 Deploying Metarhizium for biological could be observed with weekly sprays oflVl. anisopliae control of thrips in cowpea and onion in in one of the trials. Kenya 6. Complementary control methods for The collection, characterisation and selective possible integration with thrips biological deployment of promising native strains of Metarhizilll11 control anisopliae was one of the thrust areas in research on biological control of thrips on cowpeas and onion. The There are scvera I promising control mcthods for choice was facilitated by appropriate laboratory thrips that can be complimentary to biological control

I 1 SITIIANANTHAM el al.

Table 8. Interaction of Melarhizjum strains with temperature and crop cultivars -ICIPE study, Kenya*

Insect directly exposed Floral tissues sprayed

Factor F DF P F OF P

Temperature 79.33 3,96 0.0001 61.45 3,96 0.0003

Variety 13.90 2,96 0.0001 10.81 2,96 0.0001

M. anisopliae 126.51 3,96 0.0001 104.51 3,96 0.0001

Tempemture + Variety 0.86 6,96 0.5306 0.92 6,96 0.7412

Temperature + M llnisopliae 11.05 9,96 0.0011 8.74 9,96 0.0001

Variety + M. (lllisop/iae 2.15 6,96 0.0041 3.41 6,96 0.0052

Temperature + Variety + M. anisop/iae 0.24 18,96 0.6300 0.31 )g,96 0.5407

of< Source: Ekesi et al. (1998); "Means were angularly tmnsfomled before analysis; analysis of variance for mortality of /\1egaluroti1rips sjostedti interaction between temperature, variety and Metarhizium anisopliae Table 9. Effect of M. Ullisopliaecompared to synthetic insecticide (dimethoate) application on onion thrips damage ratings- ICIPE, Kenya*

Treatment Damage rating (X ± SE) a

First trial Second trial Third trial

Control 3.4 ± 0.4,,10 1.5 ± 0.2ah 3.2 ± 0.6"h

M. anisopliae weekly 2.4 ± O.lh 1.1 ± O.Ob 1.5 ± 0.2°

M. anisopliae bi - weekly 2.1 ± 0.110 1.3 ± 0.11> 1.7 ± 0.21>

Dimethoate bi - weekly 2.3±0.lb 1.5 ± O.Oh 1.5 ± 0.11>

* Source: Maniania et al. (2000); U Damage rating: 1 - No apparent damage, 2 - Light damage: upto 25 % of the leaf area, 3 - Moderate damage: 26-50 % of the leaf area, 4 - Heavy damage: 51-7 5 % of the leaf area,S - Very heavy damage: above 75 % of the leaf area; bMeans within a column followed by the same letter are not significantly different by SNK (P =0.05) test; 'Applied at lOll conidia ha· 1 •

Table to. Effect ofMetarhizjum on onion yield, ICIPE, Kenya-study (Onion yield (Mean ± SE) following application of M. anisopliae and dimethoate to control onion thrips)*

Treatment Damage rating (X ± SE) a

First trial Second trial Third trial

Control 22326.3 ± 1884.0 aU 10994.0 ± 190J.9ab 16142.5 ± 1820.7b"

M. al/isopliae weekly C 23888.5 ± 2124.5a 15344.0 ± 3081.0ab 24172.3 ± 1828.8a

M. al1i"~"",Je bi - weekly" 26985.8 ± 4750.la 12988.3 ± 1298.0ab 19039.3 ± 2657.6ab Dimethoate bi - weekly 25748.0 ± 3327.7a 17191.8 ± 696.3a 18460.5 ± 2335.0ab

* Source: Maniania e: af. (2000); a ~~ans within a column followed by the same letter are not signif1cantly different by SNK (P =0.05) test; b A)lied at 1011 cOnIdia ha· 1

12 AJ "tfl :;" ro ::r tfl ~ C tfl to Table 11. Experiments on cultural/trap practices for thrips control in India ~ tfl () o '0 Type of test Practicel Parameters studied Nature of results Reference () product tested for safety 0' "\ cr Pot experiment in chillies Oil cake based vem1icompost l.Thrips population Lowest thrips population Subasmita et al. (2005). (5 0- cr. against Scirtothrips dorsalis 2.Fruit yield (14.0-16.513 leaves) fruit yield - ;:; 240 to 260 glplantlpot to ro Field trial - intercrops Mung bean intercropped with Thrips population Peanut Peanut, sorghum and maize inter Sreekanth et af. (2004). ~ pigeon pea, sorghum, maize, Bud necrosis virus incidence crops recorded reduction in thrips ~ o...., pearl millet, castor and cotton population on 71, 62 and 57% ~ (Rabi season); 69, 62 and 60 % -i3' tfl

reduction (Kharif season). ~.

Captured population of White coloured traps captured Sarath Bahu et al. (2004). 0- Field trap colour experiment 4 colour traps were tested: r:.;' White, yellow, blue and green thrips significantly greater number. In (,...J (Thrips palmi) all colour traps occurred in significant number in all the season.

Field trial on chillies Necm products and their Mean thrips population Least popUlation observed Rao et al. (1999). (Scirtothrips dorsalis) combination (Neem oil 15 leaves (3.88 thrips) in the combination (spray, seedling root dip) of seedling root dip with 1% Neem cake (soil application) neem oil + neem cake soil application (500kglJ1a) + neem oil spray I % at weekly interval. compared to control (22.73). Gupta and Singh (2002). Crop trial - neem Neem oil Not mentioned Effective on thrips larvae and pupae which occur in soil

* Source: IIHR study by Ganga Visalakshi et. al (unpublished) SITHANANTHAM et III.

and could be targeted for integration. These include the pathway, which may also be involved in recruiting following: natural enemies of herbivores. For instance, in tomato plants, jasmonate induced resistance (J I R) i) Field sallitation: Removal ofweed hosts from the resulted in reduced abundance of the herbivores cropping areas, as weeds are often the reservoirs in three feeding guilds such as leaf chewers, for thrips (Ananthakrishnan, 1984). This is phloem feeders and cell content feeders (Thaler, applicable in general for vegetable crops, cotton, 1999). Field application ofjasmonic acid in a cotton tea, cardamom, etc. Removal of dried leaf sheath, field was found to significantly reduce the density old panicles, dried flowers, as in the case of of thrips, Franklinielfa occidentalis. besides the cardamom, can help expose the eggs which are laid aphid, Aphis gos,\ypii. Similarly, the activity of the within the leaf sheath for easier access to control predatory thrips, Scolo/hrips takahw;hii was found interventions (Varadarasan, 1995; 2003). to be enhanced by the herbivore-induced plant volatiles (Shimoda et al.. 1997; Takahashi et al., ii) Cropping practices: Studies on thrips in 2001). groundnut indicated that intercropping with pearl millet significantly reduced the incidence of thrips 7. Major thrust areas for future research besides also leaf miners and leafhoppers, compared and development with groundnut monocultures. Adjusting the planting period of chillies also reduced thrips 7.1. Field identification and biosystematics of infestation (Bagle, 1993). The available information thrips species on cultural practices is summarised in Table 11. ©> Improve capacity for field identification among iii) Use of traps : Diraviam and Uthamasamy ( 1992) bio-control scientists/staff found that yellow sticky traps are effective not only to monitor thrips density, but also to trap the thrips ©> Network among taxonomists for expert as a means of population reduction. Infestations identification to assist bio-control scientists of Scirtothrips dorsalis on Capsicum annuum i§> Establish molecular characterisation protocols have been found significantly reduced due to and training to bio-control scientists yellow pan water trap (James Keisa et al., 1996). 7.2. Biodiversity characterisation and iv) Botanicals: A number of botanicals have been repository support for bio-control agents evaluated against rice thrips in the nursery / seedling stage (Samiayyan and Chandrasekaran, ©> Assemble native biodiversity with GIS-linked 1995). Neem pesticides were also reported to be ecologically based-surveys effective against chilli thrips (James Keisa and Varatharajan, 1995) and onion thrips (Sattar Shah = Ensure biological/potency evaluation under et al., 2005). standard methodology vii) Host plant resistance: Thrips palmi is a common = Provide electronic database on the accessions pest in Latin America, infesting legumes, cucurbits, and avail free access to them solanaceous and ornamental plants; after repeated 7.3. Develop cost effective product for screening trials, five genotypes of Phaseolus vulgaris were identified as resistant to T. palmi commercialisation

(Cardona et al., 2002). e3> Verify the effectiveness of the product in thrips control viii) Host plant constituents promoting natural

control: Volatile organic compounds (VOCs) like ©> Simplify the mass production system for cost jasmonate-inducible plant defences can cause effecti veness increased parasitism of the herbivores. In many plants, the defence systems against insect = Ensure that product cost IS competitive to herbivores are induced through the octadecanoid alternative control options

14 Research status and scope I()r biological control of thrips in India

7.4. Improve the product formulation and dissemination and awarencss bui kling among end lIscrs. application technologies The solid ecological foundations laid by the pioncering and multi-faceted research of Prof. T. N. Ananthakrishnan ©> Identify IDevelop strains tolerant to climatic and his team could provide a firm base for these stresses initiatives. It is hoped that multi-disciplinary approach and inter-institutional collaboration will be nurtured in Include suitable additives for enhancing = moving forward towards a holistic Rand 0 programme, product shelflife with pathogens, predators and parasitoids in that order ©> Evolve suitable strategies for extending the of relative importance for evolving sllccessful biological field-life control technologies for key thrips pests in india. 7.5. Demonstrate economic and ecological REFERENCES benefits Alallzet, C., Dargagnon, D. and Ilatte, M. 1992. Production of = Assess the cost-returns for bio-agent versus the heteropteran predator, DrillS 1/J(~j1/SCIi/IIS chemical control (I-Icteroptera: Anthocoridae). Enlolllophaga, 37: 249-252. = Evaluate the impact on beneficial in the crop Ananthakrishnan, T N. 1994. Biocc%gy or Thrips. Indira ecosystem Publishing I louse, Michigan, USA, 233 p.

= Involve farmers as partners in ecosystem-based Ananthakrishnan, T N. 1993. Bionomics of thrips. AI1/1l/a/ assessment RCI'iew ofEn IOI/l u/ugy , 38: 71-92.

7.6. Integration and popularisation of bio Ananthakrishnan, T.N. and Sureshkumar, N. 1995. agents Anthocorids (Anthocoridae: I-Ieteropera) as efficient biologica I control agenl<; of thrips (Thysanoptera: Insecta). = Select compatible components for crop Current Science, 54: 9g7-990. protection and production Ananthakrishnan, T N. and Swami nathan, S. 1977. lIost = Ensure maximising the synergy with timing parasite and host-predator interactions in the gall thrips, adjustments Schedothrips orienta/is Anan. (Insecta: Thysanoptera). Elltol1lUI1, 2: 247-251. = Secure support from organic famling and export horticulture initiatives Ananthakrishnan, T N. and Thangavelu, K. 1976. The cereal = Provide market linkages for price incentives for thrips, Haplothrips gang/baueri Schmutz, with particular the crop produce reference to the trends of infestation on Oryza sativa and the weed, Echillochloa crllsgalli. Proceedings vIrile Indiall There is a great scope for improved conservation Academy ofSciences - B. 83: 196-20 I. and lor augmentation of natural enemies of thrips in many Ananthakrishnan, T N. and Varadarasan, S. 1977. Androthrips tropical agro-ecosystems. \Vhile research done so far in jlavipes Schmutz (Insecta: Thysanoptera), a predatory India has been focussed more on exploring and testing inquiline in thrips galls. Entolllon, 2: 105-107. of different manipulations towards enhancing the impact potential of augmentative biological control, there is need Bagle, B.G 1993. Studies on crop stage and number of to focus future research on thrips species identification, applications ofmonocrotophos in relation to thrips damage natural enemy biodiversity characterization up to strain in chilli. Indian Journal ofEII/oJJ1ologl', 55: 241-244. level, establishing a live repository of promising strains, improvements in product formulation and application of Ballal, C. R. Singh, S. P., Poorani, J. and Gupta, T. 2003a. Feasibility of mass multiplication and utilization of biological control agents and development of cost Cardiasteti1l1s exiglllls Poppius, a potential anthocorid effective production system and protocols for in-house predator of Opisill(l arellosella Walker (Lepidoptera: quality control. There is need to also support the Oecophoridae), pp. 29-33. In: Tandon, P. L, Ballal, C. R. validation of economic and ecological benefits of and Jalali, S. K. (Eds.), Biological C()lIfrol ofLepidojJlerall promising biological control agents and popularisation Pests, 354 p. programmes through training of trainers and training material preparation for a cascading effect in Ballal, C. R., Singh, S. P., Poorani, J. and liupta, T 2003b.

15 SITIIANANTHAM III (fl.

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16 Research status and scope for biological control or thrips in India

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